Abstract
The Echinodermata are an ancient phylum of benthic marine invertebrates with a dispersal-stage planktonic larva. These animals have innate immune systems characterized initially by clearance of foreign particles, including microbes, from the body cavity of both larvae and adults, and allograft tissue rejection in adults. Immune responsiveness is mediated by a variety of adult coelomocytes and larval mesenchyme cells. Echinoderm diseases from a range of pathogens can lead to mass die-offs and impact aquaculture, but some individuals can recover. Genome sequences of several echinoderms have identified genes with immune function, including expanded families of Toll-like receptors, NOD-like receptors, and scavenger receptors with cysteine-rich domains, plus signaling pathways and cytokines. The set of transcription factors that regulate proliferation and differentiation of the cellular immune system are conserved and indicate the ancestral origins of hematopoiesis. Both larval and adult echinoderms are in constant contact with potential pathogens in seawater, and they respond to infection by phagocytosis and encapsulation, and employ proteins that function in immune detection and response. Antipathogen responses include activation of the SpTransformer genes, a complement system, and the production of many types of antimicrobial peptides. Echinoderms have homologues of the recombinase activating genes plus all associated genes that function in vertebrates for immunoglobulin gene family rearrangement, although their gene targets are unknown. The echinoderm immune system has been characterized as unexpectedly complex, robust, and flexible. Many echinoderms have very long life-spans that correlate with an excellent capacity for cell damage repair. In many marine ecosystems, echinoderms are keystone predators and herbivores, and therefore are species that can serve as optimal sentinels of environmental health. Coelomocytes can be employed in sensor systems to test for the presence of marine pollutants. When Elie Metchnikoff inserted a rose prickle into a larval sea star and observed chemotaxis, phagocytosis, and encapsulation by the mesenchyme cells, he initiated not only the field of immunology but also that of comparative immunology, of which the echinoderms have been an important part.
The original version of this chapter was revised. A correction to this chapter can be found at https://doi.org/10.1007/978-3-319-76768-0_32
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Change history
25 September 2018
Correction to: Chapter 13 in: E. L. Cooper (ed.), Advances in Comparative Immunology, https://doi.org/10.1007/978-3-319-76768-0_13
References
Al-Sharif WZ, Sunyer JO, Lambris JD, Smith LC (1998) Sea urchin coelomocytes specifically express a homologue of the complement component C3. J Immunol 160:2983–2997
Anderluh G, Kisovec M, Kraševec N, Gilbert RJC (2014) Distribution of MACPF/CDC proteins. Subcell Biochem 80:7–30
Andersen JH, Murray C, Larsen MM, Green N, Høgåsen T, Dahlgren E, Garnaga-Budrė G, Gustavson K, Haarich M, Kallenbach EM, Mannio J, Strand J, Korpinen S (2016) Development and testing of a prototype tool for integrated assessment of chemical status in marine environments. Environ Monit Assess 188(2):115
Ariki S, Takahara S, Shibata T, Fukuoka T, Ozaki A, Endo Y, Fujita T, Koshiba T, Kawabata S-I (2008) Factor C acts as a lipopolysaccharide-responsive C3 convertase in horseshoe crab complement activation. J Immunol 181:7994–8001
Arizza V, Giaramita FT, Parrinello D, Cammarata M, Parrinello N (2007) Cell cooperation in coelomocyte cytotoxic activity of Paracentrotus lividus coelomocytes. Comp Biochem Physiol A Mol Integr Physiol 147:389–394
Arnone MI, Byrne M, Martinez P (2015) Echinodermata. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates 6: deuterostomia. Springer-Verlag, Wein
Bak R, Carpay M, de Ruyter van Steveninck E (1984) Densities of the sea urchin Diadema antillarum before and after mass mortalities on the coral reefs of Curaqao. Mar Ecol 1:105–108
Bates A, Hilton B, Harley C (2009) Effects of temperature, season and locality on wasting disease in the keystone predatory sea star Pisaster ochraceus. Dis Aquat Org 86:245–251
Bauer JC, Agerter CJ (1987) Isolation of bacteria pathogenic for the sea urchin Diadema antillarum (Echinodermata: Echinoidea). Bull Mar Sci 40:161–165
Bauer JC, Agerter CJ (1994) Isolation of potentially pathogenic bacterial flora from tropical sea urchins in selected West Atlantic and East Pacific sites. Bull Mar Sci 55:142–150
Beauregard KA, Truong NT, Zhang H, Lin W, Beck G (2001) The detection and isolation of a novel antimicrobial peptide from the echinoderm, Cucumaria frondosa. Adv Exp Med Biol 484:55–62
Becker PT, Gillan DC, Eeckhaut I (2007) Microbiological study of the body wall lesions of the echinoid Tripneustes gratilla. Dis Aquat Org 77(1):73–82
Becker PT, Egea E, Eeckhaut I (2008) Characterization of the bacterial communities associated with the bald sea urchin disease of the echinoid Paracentrotus lividus. J Invertebr Pathol 98(2):136–147
Beddingfield SD, McClintock JB (2000) Demographic characteristics of Lytechinus variegatus (Echinoidea: Echinodermata) from three habitats in North Florida Bay, Gulf of Mexico. Mar Ecol 21:17–40
Bertheussen K (1981a) Endocytosis by echinoid phagocytes in vitro. II. Mechanisms of endocytosis. Dev Comp Immunol 5:557–564
Bertheussen K (1981b) Endocytosis by echinoid phagocytosis in vitro. I. Recognition of foreign matter. Dev Comp Immunol 5:241–250
Bertheussen K (1982) Receptors for complement on echinoid phagocytes. II. Purified human complement mediates echinoid phagocytosis. Dev Comp Immunol 6:635–642
Bertheussen K (1983) Complement-like activity in sea urchin coelomic fluid. Dev Comp Immunol 7:21–31
Bertheussen K, Seljelid R (1978) Echinoid phagocytes in vitro. Exp Cell Res 111:401–412
Bertheussen K, Seljelid R (1982) Receptors for complement on echinoid phagocytes. I. The opsonic effect of vertebrae sera on echinoid phagocytosis. Dev Comp Immunol 6:423–431
Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22(11):2275–2284
Blanchette C, Richards D, Engle J, Broitman B, Gaines S (2005) Regime shifts, community change and population booms of keystone predators at the Channel Islands. In: Proceedings of the California Islands Symposium
Blois J, Zarnetske P, Fitzpatrick M, Finnegan S (2013) Climate change and the past, present, and future of biotic interactions. Science 341:499–504
Bodnar AG, Coffman JA (2016) Maintenance of somatic regenerative capacity with age in short- and long-lived species of sea urchins. Aging Cell 15(4):778–787
Boman HG, Agerberth B, Boman A (1993) Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun 61(7):2978–2984
Boolootian RA, Giese AC (1958) Coelomic corpuscles of echinoderms. Biol Bull 115:53–63
Boolootian RA, Giese AC (1959) Clotting of echinoderm coelomic fluid. J Exp Zool 140:207–229
Boraschi D, Costantino L, Italiani P (2012) Interaction of nanoparticles with immunocompetent cells: nanosafety considerations. Nanomedicine 7:121–131
Böttger SA, McClintock JB (2009) The effects of chronic inorganic and organic phosphate exposure on bactericidal activity of the coelomic fluid of the sea urchin sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Comp Biochem Physiol Part C 150:39–44
Brockton V, Henson JH, Raftos DA, Majeske AJ, Kim Y-O, Smith LC (2008) Localization and diversity of 185/333 proteins from the purple sea urchin—unexpected protein-size range and protein expression in a new coelomocyte type. J Cell Sci 121(3):339–348
Brogden NK, Brogden KA (2011) Will new generations of modified antimicrobial peptides improve their potential as pharmaceuticals? Int J Antimicrob Agents 38(3):217–225
Brotz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG (1998) The antibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 42(1):154–160
Buckley KM, Rast JP (2011) Characterizing immune receptors from new genome sequences. Methods Mol Biol 748:273–298
Buckley KM, Rast JP (2012) Dynamic evolution of Toll-like receptor multigene families in echinoderms. Front Immunol 3:136
Buckley KM, Rast JP (2015) Diversity of animal immune receptors and the origins of recognition complexity in the deuterostomes. Dev Comp Immunol 49(1):179–189
Buckley KM, Smith LC (2007) Extraordinary diversity among members of the large gene family, 185/333, from the purple sea urchin, Strongylocentrotus purpuratus. BMC Mol Biol 8:68
Buckley KM, Munshaw S, Kepler T, Smith LC (2008a) The 185/333 gene family is a rapidly diversifying host-defense gene cluster in the purple sea urchin Strongylocentrotus purpuratus. J Mol Biol 379(4):912–928
Buckley KM, Terwilliger DP, Smith LC (2008b) Sequence variations in 185/333 messages from the purple sea urchin suggest post-transcriptional modifications to increase immune diversity. J Immunol 181:8585–8594
Buckley KM, Ho ECH, Hibino T, Schrankel CS, Schuh NW, Wang G, Rast JP (2017) IL17 factors are early regulators in the gut epithelium during inflammatory response to Vibrio in the sea urchin larva. elife 6:e23481
Burge C, Eakin C, Friedman C, Froelich B, Hershberger P, Hofmann E, Petes L, Prager K, Weil E, Willis B, Ford S, Harvell C (2014) Climate change influences on marine infectious diseases: implications for management and society. Annu Rev Mar Sci 6:249–277
Calestani C, Rogers DJ (2010) Cis-regulatory analysis of the sea urchin pigment cell gene polyketide synthase. Dev Biol 340(2):249–255
Calestani C, Rast JP, Davidson EH (2003) Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development 130(19):4587–4596
Cameron RA, Samanta M, Yuan A, He D, Davidson E (2009) SpBase: the sea urchin genome database and web site. Nucleic Acids Res 37(suppl 1):D750–D754
Canicatti C, D’Ancona G (1989) Cellular aspects of Holothuria polii immune response. J Invertebr Pathol 53:152–158
Carmona LM, Fugmann SD, Schatz DG (2016) Collaboration of RAG2 with RAG1-like proteins during the evolution of V(D)J recombination. Genes Dev 30:909–917
Carpenter RC (1988) Mass mortality of a Caribbean sea urchin: immediate effects on community metabolism and other herbivores. PNAS 85(2):511–514
Carpenter RC (1990) Mass mortality of Diadema antillarum. 1. Long-term effects on sea urchin population-dynamics and coral reef algal communities. Mar Biol 104(1):67–77
Castillo MG, Goodson MS, McFall-Ngai M (2009) Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev Comp Immunol 33(1):69–76
Chia F, Xing J (1996) Echinoderm coelomocytes. Zool Stud 35:231–254
Choe J, Kelker MS, Wilson IA (2005) Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain. Science 309(5734):581–585
Clow LA, Gross PS, Shih CS, Smith LC (2000) Expression of SpC3, the sea urchin complement component, in response to lipopolysaccharide. Immunogenetics 51(12):1021–1033
Clow LA, Raftos DA, Gross PS, Smith LC (2004) The sea urchin complement homologue, SpC3, functions as an opsonin. J Exp Biol 207:2147–2155
Coffaro KA, Hinegardner RT (1977) Immune response in the sea urchin Lytechinus pictus. Science 197(4311):1389–1390
Coleman J, Inukai M, Inouye M (1985) Dual functions of the signal peptide in protein transfer across the membrane. Cell 43(1):351–360
Connon RE, Geist J, Werne I (2012) Effect-based tools for monitoring and predicting the ecotoxicological effects of chemicals in the aquatic environment. Biosensors 12(9):12741–12771
Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745
Coteur G, DeBecker G, Warnau M, Jangoux M, Dubois P (2002a) Differentiation of immune cells challenged by bacteria in the common European starfish, Asterias rubens (Echinodermata). Eur J Cell Biol 81(7):413–418
Coteur G, Warnau M, Jangoux M, Dubois P (2002b) Reactive oxygen species (ROS) production by amoebocytes of Asterias rubens (Echinodermata). Fish Shellfish Immunol 12(3):187–200
Coteur G, Gosselin P, Wantier P, Chambost-Manciet Y, Danis B, Pernet P, Warnau M, Dubois P (2003a) Echinoderms as bioindicators, bioassays, and impact assessment tools of sediment-associated metals and PCBs in the North Sea. Arch Environ Contam Toxicol 45(2):190–202
Coteur G, Gillan D, Joly G, Pernet P, Dubois P (2003b) Field contamination of the starfish Asterias rubens by metals. Part 2: effects on cellular immunity. Environ Toxicol Chem 22(9):2145–2151
Danis B, Goriely S, Dubois P, Fowler SW, Flamand V, Warnau M (2004a) Contrasting effects of coplanar versus noncoplanar PCB congeners on immunomodulation and CYP1A levels (determined using an adapted ELISA method) in the common sea star Asterias rubens L. Aquat Toxicol 69(4):371–383
Danis B, Cotret O, Teyssié JL, Fowler SW, Warnau M (2004b) Coplanar PCB 77 uptake kinetics in the sea star Asterias rubens and subsequent effects on reactive oxygen species (ROS) production and levels of cytochrome P450 immunopositive proteins (CYP1A-IPP). Mar Ecol Prog Ser 279:117–128
Danis B, Wantier P, Flammang R, Pernet P, Chambost-Manciet Y, Coteur G, Warnau M, Dubois P (2006) Bioaccumulation and effects of PCBs and heavy metals in sea stars (Asterias rubens, L.) from the North Sea: a small scale perspective. Sci Total Environ 356(1–3):275–289
Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Schilstra MJ, Clarke PJ, Rust AG, Pan Z, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002) A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev Biol 246(1):162–190
Davidson AJ, Zon LI (2004) The ‘definitive’ (and ‘primitive’) guide to zebrafish hematopoiesis. Oncogene 23(43):7233–7246
Davidson CR, Best NM, Francis JW, Cooper EL, Wood TC (2008) Toll-like receptor genes (TLRs) from Capitella capitata and Helobdella robusta (Annelida). Dev Comp Immunol 32(6):608–612
de la Fuente-Nunez C, Reffuveille F, Fernandez L, Hancock REW (2013) Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 16(5):580–589
de Latour RA, Amer LS, Papanstasiou EA, Bishop BM, van Hoek ML (2010) Antimicrobial activity of the Naja atra cathelicidin and related small peptides. Biochem Biophys Res Commun 396:825–830
De Pooter R (2010) E proteins and the regulation of early lymphocyte development. Immunol Rev 238:93–109
Dempsey CE, Ueno S, Avison MB (2003) Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue. Biochemistry 42(2):402–409
Deng H, He C, Zhou Z, Liu C, Tan K, Wang N, Jiang B, Gao X, Liu W (2009) Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture 287(1–2):18–27
Dev S, Robinson JJ (2014) Comparative biochemical analysis of the major yolk protein in the sea urchin egg and coelomic fluid. Dev Growth Differ 56(6):480–490
Dewan PC, Anantharaman A, Chauhan VS, Sahal D (2009) Antimicrobial action of prototypic amphipathic cationic decapeptides and their branched dimers. Biochemistry 48(24):5642–5657
Dheilly NM, Nair SV, Smith LC, Raftos DA (2009) Highly variable immune response proteins (185/333) from the sea urchin, Strongylocentrotus purpuratus: proteomic analysis identifies diversity within and between individuals. J Immunol 182:2203–2212
Dheilly NM, Birch D, Nair SV, Raftos DA (2011a) Ultrastructural localization of highly variable 185/333 immune response proteins in the coelomocytes of the sea urchin, Heliocidaris erythrogramma. Immunol Cell Biol 89:861–869
Dheilly NM, Haynes PA, Bove U, Nair SV, Raftos DA (2011b) Comparative proteomic analysis of a sea urchin (Heliocidaris erythrogramma) antibacterial response revealed the involvement of apextrin and calreticulin. J Invertebr Pathol 106(2):223–229
Dheilly NM, Haynes PA, Raftos DA, Nair SV (2012) Time course proteomic profiling of cellular responses to immunological challenge in the sea urchin, Heliocidaris erythrogramma. Dev Comp Immunol 37(2):243–256
Dheilly NM, Raftos DA, Haynes PA, Smith LC, Nair SV (2013) Shotgun proteomics of coelomic fluid from the purple sea urchin, Strongylocentrotus purpuratus. Dev Comp Immunol 40(1):35–50
Dheilly NM, Coen A, Raftos DA, Benjamin G, Christoph G, Louis DP (2014) No more non-model species: the promise of next generation sequencing for comparative immunology. Dev Comp Immunol 45(1):56–66
Dishaw LJ, Smith SL, Bigger CH (2005) Characterization of a C3-like cDNA in a coral: phylogenetic implications. Immunogenetics 57(7):535–548
Du C, Anderson A, Lortie M, Parsons R, Bodnar A (2013) Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med 63:254–263
Duboc V, Lapraz F, Saudemont A, Bessodes N, Mekpoh F, Haillot E, Quirin M, Lepage T (2010) Nodal and BMP2/4 pattern the mesoderm and endoderm during development of the sea urchin embryo. Development 137(2):223–235
Dungan ML, Miller TE, Thomson DA (1982) Catastrophic decline of a top carnivore in the gulf of California rocky intertidal zone. Science 216(4549):989–991
Ebert TA (2007) Growth and survival of post-settlement sea urchins. In: Lawrence JM (ed) Edible sea urchins: biology and ecology, 2nd edn. Elsevier, Amsterdam, pp 95–134
Ebert TA (2008) Longevity and lack of senescence in the red sea urchin Strongylocentrotus franciscanus. Exp Gerontol 43:734–738
Ebert TA (2010) Demographic patterns of the purple sea urchin Strongylocentrotus purpuratus along a latitudinal gradient, 1985–1987. Mar Ecol Prog Ser 406:105–120
Ebert TA, Southon JR (2003) Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fish Bull 101(4):915–922
Ebert TA, Russell MP, Gamba G, Bodnar A (2008) Growth, survival, and longevity estimates for the rock-boring sea urchin Echinometra lucunter lucunter (Echinodermata, Echinoidea) in Bermuda. Bull Mar Sci 82(3):381–403
Eckert GJ, Engle J, Kushner D (1999) Sea star disease and population declines at the Channel Islands. In: Proceedings of the fifth California Island symposium, US Minerals Management Service, pp 390–394
Edds KT (1977) Dynamic aspects of filopodial formation by reorganization of microfilaments. J Cell Pathol 73:479–491
Edds KT (1993) Cell biology of echinoid coelomocytes. Diversity and characterization of cell types. J Invertebr Biol 61:173–178
Edmunds P, Carpenter R (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci U S A 98(9):5067–5071
El-Bibany AH, Bodnar AG, Reinardy HC (2014) Comparative DNA damage and repair in echinoderm coelomocytes exposed to genotoxicants. PLoS One 9(9):e107815
Eliseikina MG, Magarlamov TY (2002) Coelomocyte morphology in the holothurians Apostichopus japonicus (Aspidochirota: Stichopodidae) and Cucumaria japonica (Dendrochirota: Cucumariidae). Russ J Mar Biol 28:197–202
Ellis RP, Parry H, Spicer JI, Hutchinson TH, Pipe RK, Widdicombe S (2011) Immunological function in marine invertebrates: responses to environmental perturbation. Fish Shellfish Immunol 30(6):1209–1222
Endean R (1966) The coelomocytes and coelomic fluids. In: Boolootian RA (ed) Physiology of echinodermata. Intersciences, New York, pp 301–328
Engle J, Halvorson W, Maender G (1994) Perspectives on the structure and dynamics of nearshore marine assemblages of the California Channel Islands. In: The fourth California channel islands symposium: update on the status of resources, Santa Barbara
Falugi C, Aluigi MG, Chiantore MC, Privitera D, Ramoino P, Gatti MA, Fabrizi A, Pinsino A, Matranga V (2012) Toxicity of metal oxide nanoparticles in immune cells of the sea urchin. Mar Environ Res 76:114–121
Fey PD (2010) Modality of bacterial growth presents unique targets: how do we treat biofilm-mediated infections? Curr Opin Microbiol 13(5):610–615
Finch CE (1990) Longevity, senescence, and the genome. University of Chicago Press, Chicago, pp 206–226
Finch CE, Austad SN (2001) History and prospects: symposium on organisms with slow aging. Exp Gerontol 36:593–597
Fontaine AR, Lambert P (1977) The fine structure of the leucocytes of the holothurian, Cucumaria miniata. Can J Zool 55:1530–1544
Franchi N, Ballarin L (2014) Preliminary characterization of complement in a colonial tunicate: C3, Bf and inhibition of C3 opsonic activity by compstatin. Dev Comp Immunol 46:430–438
Franchi N, Ballarin L (2017) Morula cells as key hemocytes of the lectin pathway of complement activation in the colonial tunicate Botryllus schlosseri. Fish Shellfish Immunol 63:157–164
Franco CF, Santos R, Coelho AV (2011) Proteome characterization of sea star coelomocytes—the innate immune effector cells of echinoderms. Proteomics 11(17):3587–3592
Fuess LE, Eisenlord ME, Closek CJ, Tracy AM, Mauntz R, Gignoux-Wolfsohn S, Moritsch MM, Yoshioka R, Burge CA, Harvell CD, Friedman CS, Hewson I, Hershberger PK, Roberts SB (2015) Up in arms: immune and nervous system response to sea star wasting disease. PLoS One 10:e0133053
Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP (2006) An ancient evolutionary origin of the Rag1/2 gene locus. Proc Natl Acad Sci U S A 103:3728–3733
Fujito NT, Sugimoto S, Nonaka M (2010) Evolution of thioester-containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev Comp Immunol 34:775–784
Fulton KM, Twine SM (2013) Immunoproteomics: current technology and applications. In: Fulton MK, Twine MS (eds) Immunoproteomics: methods and protocols. Humana Press, Totowa, pp 21–57
Furukawa R, Takahashi Y, Nakajima Y, Dan-Sohkawa M, Kaneko H (2009) Defense system by mesenchyme cells in bipinnaria larvae of the starfish, Asterina pectinifera. Dev Comp Immunol 33(2):205–215
Furukawa R, Funabashi H, Matsumoto M, Kaneko H (2012a) Starfish ApDOCK protein essentially functions in larval defense system operated by mesenchyme cells. Immunol Cell Biol 90:955–965
Furukawa R, Matsumoto M, Kaneko H (2012b) Characterization of a scavenger receptor cysteine-rich-domain-containing protein of the starfish, Asterina pectinifera: ApSRCR1 acts as an opsonin in the larval and adult innate immune systems. Dev Comp Immunol 36(1):51–61
Furukawa R, Tamaki K, Kaneko H (2016) Two macrophage migration inhibitory factors regulate starfish larval immune cell chemotaxis. Immunol Cell Biol 94:315–321
Gallo A, Tosti E (2013) Adverse effect of antifouling compounds on the reproductive mechanisms of the ascidian Ciona intestinalis. Mar Drugs 11(9):3554–3568
Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3(9):710–720
Gao Z, Li M, Ma J, Zhang S (2014) An amphioxus gC1q protein binds human IgG and initiates the classical pathway: implications for a C1q-mediated complement system in the basal chordate. Eur J Immunol 44:3680–3695
Gao Z, Ma Z, Qu B, Jiao D, Zhang S (2017) Identification and characterization of properdin in amphioxus: implications for a functional alternative complement pathway in the basal chordate. Fish Shellfish Immunol 65:1–8
Garcia-Olmedo F, Molina A, Alamillo JM, Rodriguez-Palenzuela P (1998) Plant defense peptides. Biopolymers 47(6):479–491
Gelebart P, Opas M, Michalak M (2005) Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. Int J Biochem Cell Biol 37(2):260–266
Gellert M (2002) V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71:101–132
Gerdol M, Venier P (2015) An updated molecular basis for mussel immunity. Fish Shellfish Immunol 46:17–38
Ghosh J, Buckley KM, Nair SV, Raftos DA, Miller C, Majeske AJ, Hibino T, Rast JP, Roth M, Smith LC (2010) Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev Comp Immunol 34:235–245
Gibson AW, Burke RD (1985) The origin of pigment cells in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Biol 107(2):414–419
Gibson AW, Burke RD (1987) Migratory and invasive behavior of pigment cells in normal and animalized sea urchin embryos. Exp Cell Res 173(2):546–557
Giga Y, Ikai A (1985a) Purification and physical chemical characterization of 23S glycoprotein from sea urchin (Anthocidaris crassispina) eggs. J Biochem 98(1):237–243
Giga Y, Ikai A (1985b) Purification of the most abundant protein in the coelomic fluid of a sea urchin which immunologically cross reacts with 23S glycoprotein in the sea urchin eggs. J Biochem 98(1):19–26
Gilles K, Pearse J (1986) Disease in sea urchins Strongylocentrotus purpuratus: experimental infection and bacterial virulence. Dis Aquat Org 1:105–114
Glinel K, Thebault P, Humblot V, Pradier C-M, Jouenne T (2012) Antibacterial surfaces developed from bio-inspired approaches. Acta Biomater 8(5):1670–1684
Gowda NM, Goswani U, Khan MI (2008) T-antigen binding lectin with antibacterial activity from marine invertebrate sea cucumber (Holothuria scabra): possible involvement in differential recognition of bacteria. J Invertebr Pathol 99:141–145
Gross PS, Al-Sharif WZ, Clow LA, Smith LC (1999) Echinoderm immunity and the evolution of the complement system. Dev Comp Immunol 23:429–442
Gross PS, Clow LA, Smith LC (2000) SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 51:1034–1044
Gudenkauf BM, Eaglesham J, Aragundi W, Hewson I (2014) Discovery of urchin-associated densoviruses (family Parvoviridae) in coastal waters of the Big Island, Hawaii. J Gen Virol 95:652–658
Haag ES, Sly BJ, Andrews ME, Raff RA (1999) Apextrin, a novel extracellular protein associated with larval ectoderm evolution in Heliocidaris erythrogramma. Dev Biol 211(1):77–87
Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108
Hancock REW, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24(12):1551–1557
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus AD, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases--climate links and anthropogenic factors. Science 285(5433):1505–1510
Hatakeyama T, Suenaga T, Eto S, Niidome T, Aoyagi H (2004) Antibacterial activity of peptides derived from the C-terminal region of a hemolytic lectin, CEL-III, from the marine invertebrate Cucumaria echinata. J Biochem 135(1):65–70
Haug T, Kjuul AK, Styrvold OB, Sandsdalen E, Olsen OM, Stensvag K (2002) Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea). J Invertebr Pathol 81(2):94–102
He Y, Tankg B, Zhang S, Liu Z, Zhao B, Chen L (2008) Molecular and immunochemical demonstration of a novel member of Bf/C2 homolog in amphioxus Branchiostoma belcheri: implication for involvement of hepatic cecum in acute phase response. Fish Shellfish Immunol 24:768–778
Heller WT, Waring AJ, Lehrer RI, Harroun TA, Weiss TM, Yang L, Huang HW (2000) Membrane thinning effect of the β-sheet antimicrobial protegrin. Biochemistry 39(1):139–145
Henson JH, Schatten G (1983) Calcium regulation of the actin-mediated cytoskeletal transformation of sea urchin coelomocytes. Cell Motil Cytoskeleton 3:525–534
Henson JH, Nesbitt D, Wright BD, Scholey JM (1992) Immunolocalization of kinesin in sea urchin coelomocytes. Association of kinesin with intracellular organelles. J Cell Sci 103:309–320
Henson JH, Svitkina TM, Burns AR, Hughes HE, MacPartland KJ, Nazarian R, Borisy GG (1999) Two components of actin-based retrograde flow in sea urchin coelomocytes. Mol Biol Cell 10(12):4075–4090
Hetzel HR (1963) Studies on holothurian coelomocytes. I. A survey of coelomocyte types. Biol Bull 125:289–301
Hewson I, Button JB, Gudenkauf BM, Miner B, Newton AL, Gaydos JK, Wynne J, Groves CL, Hendler G, Murray M, Fradkin S, Breitbart M, Fahsbender E, Lafferty KD, Kilpatrick AM, Miner CM, Raimondi P, Lahner L, Friedman CS, Daniels S, Haulena M, Marliave J, Burge CA, Eisenlord ME, Harvell CD (2014) Densovirus associated with sea-star wasting disease and mass mortality. Proc Natl Acad Sci U S A 111(48):17278–17283
Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365
Hildemann WH, Dix TG (1972) Transplantation reactions of tropical Australian echinoderms. Transplantation 14(5):624–633
Hill SK, Aragona JB, Lawrence JM (2004) Growth bands in test plates of the sea urchins Arbacia punctulata and Lytechinus variegatus (Echinodermata) on the central Florida Gulf Coast shelf. Gulf Mexico Sci 22(1):96–100
Hisamatsu K, Tsuda N, Goda S, Hatakeyama T (2008) Characterization of the α-helix region in domain 3 of the haemolytic lectin CEL-III: implications for self-oligomerization and haemolytic processes. J Biochem 143(1):79–86
Ho ECH, Buckley KM, Schrankel CS, Schuh NW, Hibino T, Solek CM, Bae K, Wang G, Rast JP (2016) Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 94:861–874
Hogan MC, Griffin MD, Rossetti S, Torres VE, Ward CJ, Harris PC (2003) PKHDL1, a homolog of the autosomal recessive polycystic kidney disease gene, encodes a receptor with inducible T lymphocyte expression. Hum Mol Genet 12(6):685–698
Horswill AR, Stoodley P, Stewart PS, Parsek MR (2007) The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387(2):371–380
Howard-Ashby M, Materna SC, Brown CT, Tu Q, Oliveri P, Cameron RA, Davidson EH (2006) High regulatory gene use in sea urchin embryogenesis: implications for bilaterian development and evolution. Dev Biol 300(1):27–34
Huang HW (2000) Action of antimicrobial peptides: two-state model. Biochemistry 39(29):8347–8352
Huang G, Liu H, Han Y, Fan L, Zhang Q, Liu J, Yu X, Zhang L, Chen S, Dong M, Wang L, Xu A (2007) Profile of acute immune response in Chinese amphioxus upon Staphylococcus aureus and Vibrio parahaemolyticus infection. Dev Comp Immunol 31(10):1013–1023
Huang YB, Huang JF, Chen YX (2010) Alpha-helical cationic antimicrobial peptides: relationships of structure and function. Protein Cell 1(2):143–152
Huang H, Huang S, Yu Y, Yuan S, Li R, Wang X, Zhao H, Yu Y, Li J, Yang M, Xu L, Chen S, Xu A (2011) Functional characterization of a ficolin-mediated complement pathway in amphioxus. J Biol Chem 286:36739–36748
Huang G, Huang S, Yan X, Yang P, Li J, Xu W, Zhang L, Wang R, Yu Y, Yuan S, Chen S, Luo G, Xu A (2014) Two apextrin-like proteins mediate extracellular and intracellular bacterial recognition in amphioxus. Proc Natl Acad Sci 111(37):13469–13474
Huang S, Tao X, Yuan S, Zhang Y, Li P, Beilinson HA, Zhang Y, Yu W, Pontarotti P, Escriva H, Le Petillon Y, Liu X, Chen S, Schatz DG, Xu A (2016) Discovery of an active RAG transposon illuminates the origins of V(D)J recombination. Cell 166:102–114
Huff T, Muller CS, Otto AM, Netzker R, Hannappel E (2001) Beta-thymosins, small acidic peptides with multiple functions. Int J Biochem Cell Biol 33(3):205–220
Hughes TP, Keller BD, Jackson JBC, Boyle MJ (1985) Mass mortality of the echinoid Diadema antillarum Philippi in Jamaica. Bull Mar Sci 36:377–384
Hugli TE (1990) Structure and function of C3a anaphylatoxin. Curr Top Microbiol Immunol 153:181–208
Hyman L (1955) The invertebrates: echinodermata the coelomate bilateria, vol IV. McGraw-Hill, New York
Islam MS, Tanaka M (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Mar Pollut Bull 48(7–8):624–649
Ito T, Matsutani T, Mori K, Nomure T (1992) Phagocytosis and hydrogen peroxide production by phagocytes of the sea urchin Strongylocentrotus nudus. Dev Comp Immunol 16:287–294
Jangoux M (1987) Diseases of Echinodermata. 4. Structural abnormalities and general considerations on biotic diseases. Dis Aquat Org 3:221–229
Jangoux M (1990) Chapter 5: Diseases of echinodermata. In: Kinne O (ed) Diseases of marine animals, vol III. Wiley/Biologische Anstalt Helgoland, Hamburg
Jangoux M, Vanden Bossche J-P (1975) Morphology and dynamics of the coelomocytes of Asterias rubens L. (Echinodermata, Asteroidea). Forma Funct 8:191–208
Janies DA, Voight JR, Daly M (2011) Echinoderm phylogeny including Xyloplax, a progenetic asteroid. Syst Biol 60(4):420–438
Jellett FJ, Wardlaw AC, Scheibling RE (1988) Experimental infection of the echinoid Strongylocentrotus droebachiensis with Paramoeba invadens: quantitative changes in the coelomic fluid. Dis Aquat Org 4:149–157
Jiang J, Zhou Z, Dong Y, Jiang B, Chen Z, Yang A, Wang B, Guan X, Gao S, Sun H (2016) The in vitro effects of divalent metal ions on the activities of immune-related enzymes in from the sea cucumber Apostichopus japonicas. Aquac Res 47:1269–1276
Johnson P (1970) Studies on diseased urchins from Point Loma. Kelp habitat improvement project.California Institute of Technology, Pasadena, pp 82–90
Jones GM (1985) Paramoeba invadens n. sp. (Amoebida, Paramoebidae), a pathogenic amoeba from the sea urchin, Strongylocentrotus droebachiensis, in eastern Canada. J Eukaryot Microbiol 32(4):564–569
Jones G, Scheibling R (1985) Paramoeba sp. (Amoebida, Paramoebidae) as the possible causative agent of sea urchin mass mortality in Nova Scotia. J Parasitol 71:559–565
Jones G, Hebda A, Scheibling R, Miller R (1985) Histopathology of the disease causing mass mortality of sea urchins (Strongylocentrotus droebachiensis) in Nova Scotia. J Invertebr Pathol 45:260–271
Jurgens LJ, Rogers-Bennett L, Raimondi PT, Schiebelhut LM, Dawson MN, Grosberg RK, Gaylord B (2015) Patterns of mass mortality among rocky shore invertebrates across 100 km of northeastern Pacific coastline. PLoS One 10(6):e0126280
Kanungo K (1982) In vitro studies on the effects of the cell-free coelomic fluid, calcium, ad/or magnesium on clumping of the coelomocytes of the sea star Asterias forbesi (Echinodermata: Asteroidea). Biol Bull 163:438–452
Kapitonov VV, Koonin EV (2015) Evolution of the RAG1-RAG2 locus: both proteins came from the same transposon. Biol Direct 10:20
Kaplan G, Bertheussen K (1977) The morphology of echinoid phagocytes and mouse peritoneal macrophages during phagocytosis in vitro. Scand J Immunol 6:1289–1296
Karp RD, Hildemann WH (1976) Specific allograft reactivity in the sea star Dermasterias imbricata. Transplantation 22(5):434–439
Katow H (2004) The 5-HT receptor cell is a new member of secondary mesenchyme cell descendants and forms a major blastocoelar network in sea urchin larvae. Mech Dev 121(4):325–337
Kee BL (2009) E and ID proteins branch out. Nat Rev Immunol 9(3):175–184
Kiani N, Heidari B, Rassa M, Kadkhodazadeh M, Heidari B (2014) Antibacterial activity of the body wall extracts of sea cucumber (Invertebrata; Echinodermata) on infectious oral streptococci. J Basic Clin Physiol Pharmacol 25:367–373
Kim AD, Melick CH, Clements WK, Stachura DL, Distel M, Panakova D, MacRae C, Mork LA, Crump JG, Traver D (2014) Discrete Notch signaling requirements in the specification of hematopoietic stem cells. EMBO J 33(20):2363–2373
Kimura A, Sakaguchi E, Nonaka M (2009) Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 214:165–178
Kindred JE (1924) The cellular elements in the perivisceral fluid of echinoderms. Biol Bull 46:228–251
Kirkwood TBL (2005) Understanding the odd science of aging. Cell 120:437–447
Kober KM, Bernardi G (2013) Phylogenomics of strongylocentrotid sea urchins. BMC Evol Biol 13:88
Kominami T (2000) Establishment of pigment cell lineage in embryos of the sea urchin, Hemicentrotus pulcherrimus. Dev Growth Differ 42(1):41–51
Kominami T, Takata H (2003) Specification of secondary mesenchyme-derived cells in relation to the dorso-ventral axis in sea urchin blastulae. Dev Growth Differ 45(2):129–142
Kominami T, Takata H, Takaichi M (2001) Behavior of pigment cells in gastrula-stage embryos of Hemicentrotus pulcherrimus and Scaphechinus mirabilis. Dev Growth Differ 43(6):699–707
Kostakioti M, Hadjifrangiskou M, Hultgren SJ (2013) Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med 3(4):a010306
Krupke OA, Zysk I, Mellott DO, Burke RD (2016) Eph and Ephrin function in dispersal and epithelial insertion of pigmented immunocytes in sea urchin embryos. elife 5:e16000
Kuznetsova TA, Anisimov MM, Popov AM, Baranova SI, Afiyatullov SS, Kapustina II, Antonov AS, Elyakov GB (1982) A comparative study in vitro of physiological activity of triterpene glycosides of marine invertebrates of echinoderm type. Comp Biochem Physiol C 73(1):41–43
Laegdsgaard P, Byrne M, Anderson DT (1991) Reproduction of sympatric populations of Heliocidaris erythrogramma and H. tuberculata (Echinoidea) in New South Wales. Mar Biol 110(3):359–374
Lapraz F, Haillot E, Lepage T (2015) A deuterostome origin of the Spemann organizer suggested by Nodal and ADMPs functions in echinoderms. Nat Commun 6:8927
Lawrence J (1996) Mass mortalities of echinoderms from abiotic factors. Echinoderm Stud. M. Jangoux and G. J Lawrence. Rotterdam: Balkema 5:103–137
Le CF, Gudimella R, Razali R, Manikam R, Sekaran SD (2016) Transcriptome analysis of Streptococcus pneumoniae treated with the designed antimicrobial peptides, DM3. Sci Rep 6:26828
Leclerc M, Kresdorn N, Rotter B (2013) Evidence of complement genes in the sea-star Asterias rubens. Comparisons with the sea urchin. Immunol Lett 151:68–70
Lee PY, Davidson EH (2004) Expression of SpGatae, the Strongylocentrotus purpuratus ortholog of vertebrate GATA4/5/6 factors. Gene Expr Patterns 5(2):161–165
Lee MT, Chen FY, Huang HW (2004) Energetics of pore formation induced by membrane active peptides. Biochemistry 43(12):3590–3599
Lee JY, Yang ST, Lee SK, Jung HH, Shin SY, Hahm KS, Kim JI (2008) Salt-resistant homodimeric bactenecin, a cathelicidin-derived antimicrobial peptide. FEBS J 275(15):3911–3920
Leippe M (1999) Antimicrobial and cytolytic polypeptides of amoeboid protozoa—effector molecules of primitive phagocytes. Dev Comp Immunol 23(4–5):267–279
Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu Rev Ecol Syst 19:371–393
Lessios HA, Robertson D, Cubit J (1984) Spread of Diadema mass mortality through the Caribbean. Science 226(4672):335–337
Li J, Post M, Volk R, Gao Y, Li M, Metais C, Sato K, Tsai J, Aird W, Rosenberg RD, Hampton TG, Sellke F, Carmeliet P, Simons M (2000) PR39, a peptide regulator of angiogenesis. Nat Med 6(1):49–55
Li C, Haug T, Styrvold OB, Jorgensen TO, Stensvag K (2008) Strongylocins, novel antimicrobial peptides from the green sea urchin, Strongylocentrotus droebachiensis. Dev Comp Immunol 32(12):1430–1440
Li C, Blencke HM, Smith LC, Karp MT, Stensvag K (2010a) Two recombinant peptides, SpStrongylocins 1 and 2, from Strongylocentrotus purpuratus, show antimicrobial activity against Gram-positive and Gram-negative bacteria. Dev Comp Immunol 34(3):286–292
Li C, Haug T, Moe MK, Styrvold OB, Stensvag K (2010b) Centrocins: isolation and characterization of novel dimeric antimicrobial peptides from the green sea urchin, Strongylocentrotus droebachiensis. Dev Comp Immunol 34(9):959–968
Li C, Blencke HM, Haug T, Jorgensen O, Stensvag K (2014a) Expression of antimicrobial peptides in coelomocytes and embryos of the green sea urchin (Strongylocentrotus droebachiensis). Dev Comp Immunol 43(1):106–113
Li Z, Maa Z, van der Kuijpa TJ, Yuana Z, Huanga L (2014b) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468–469:843–853
Li C, Blencke HM, Haug T, Stensvag K (2015) Antimicrobial peptides in echinoderm host defense. Dev Comp Immunol 49(1):190–197
Liddell WD, Ohlhorst SL (1986) Changes in benthic community composition following the mass mortality of Diadema at Jamaica. J Exp Mar Biol Ecol 95:1–8
Liu H, Zheng F, Sun X, Hong X, Dong S, Wang B, Tang X, Wang Y (2010a) Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol 105:236–242
Liu SP, Zhou L, Lakshminarayanan R, Beuerman RW (2010b) Multivalent antimicrobial peptides as therapeutics: design principles and structural diversities. Int J Pept Res Ther 16(3):199–213
Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW (2005) DNA repair, genome stability, and aging. Cell 120(4):497–512
Long KA, Nossa CW, Sewell MA, Putnam NH, Ryan JF (2016) Low coverage sequencing of three echinoderm genomes: the brittle star Ophionereis fasciata, the sea star Patiriella regularis, and the sea cucumber Australostichopus mollis. GigaScience 5(1):1–4
Loram J, Raudonis R, Chapman J, Lortie M, Bodnar A (2012) Sea urchin coelomocytes are resistant to a variety of DNA damaging agents. Aquat Toxicol 124–125:133–138
Lun CM, Schrankel CS, Chou H-Y, Sacchi S, Smith LC (2016) A recombinant Sp185/333 protein from the purple sea urchin has multitasking binding activities towards certain microbes and PAMPs. Immunobiology 221(8):889–903
Lun CM, Bishop BM, Smith LC (2017a) Multitasking immune Sp185/333 protein, rSpTransformer-E1, and its recombinant fragments undergo secondary structural transformation upon binding targets. J Immunol 198(7):2957–2966
Lun CM, Samuel R, Gillmor SD, Boyd A, Smith LC (2017b) SpTransformer, a recombinant Sp185/333 protein, binds to phosphatidic acid and deforms membranes. Front Immunol 8:481
Luna-Acosta L, Bustamante P, Godefroy J, Fruitier-Arnaudin I, Thomas-Guyon H (2010) Seasonal variation of pollution biomarkers to assess the impact on the health status of juvenile Pacific oysters Crassostrea gigas exposed in situ. Environ Sci Pollut Res 17:999–1008
Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, Vethaak AD (2010) Using biological effects tools to define good environmental status under the European Union Marine Strategy Framework Directive. Mar Pollut Bull 60:1647–1651
Maes P, Jangoux M (1984) The bald-sea-urchin disease: a biopathological approach. Helgolander Meeresun 37:217–224
Majeske AJ, Oleksyk T, Smith LC (2013a) The Sp185/333 immune response genes and proteins are expressed in cells dispersed within all major organs of the adult purple sea urchin. Innate Immun 19(6):569–587
Majeske AJ, Bayne CJ, Smith LC (2013b) Aggregation of sea urchin phagocytes is augmented in vitro by lipopolysaccharide. PLoS One 8(4):e61419
Majeske AJ, Oren M, Sacchi S, Smith LC (2014) Single sea urchin phagocytes express messages of a single sequence from the diverse Sp185/333 gene family in response to bacterial challenge. J Immunol 193:5678–5688
Maltseva AL, Aleshina GM, Kokryakov VN, Krasnodembskii EG (2007) Diversity of antimicrobial peptides in acidic extracts from coelomocytes of starfish Asterias rubens L. Vestn S-Peterb Univ 3:85–94
Marino R, Kimura Y, De Santis R, Lambris JD, Pinto MR (2002) Complement in urochordates: cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53(12):1055–1064
Maroti G, Kereszt A, Kondorosi E, Mergaert P (2011) Natural roles of antimicrobial peptides in microbes, plants and animals. Res Microbiol 162(4):363–374
Martin I, Grotewiel MS (2006) Oxidative damage and age-related functional declines. Mech Ageing Dev 127:411–423
Materna SC, Davidson EH (2012) A comprehensive analysis of Delta signaling in pre-gastrular sea urchin embryos. Dev Biol 364(1):77–87
Materna SC, Nam J, Davidson EH (2010) High accuracy, high-resolution prevalence measurement for the majority of locally expressed regulatory genes in early sea urchin development. Gene Expr Patterns 10(4–5):177–184
Materna SC, Ransick A, Li E, Davidson EH (2013) Diversification of oral and aboral mesodermal regulatory states in pregastrular sea urchin embryos. Dev Biol 375:92–104
Matranga V, Toia G, Bonaventura R, Müller WEG (2000) Cellular and biochemical responses to environmental and experimentally induced stress in sea urchin coelomocytes. Cell Stress Chaperones 5(2):113–120
Matranga V, Bonaventura R, Di Bella G (2002) Hsp70 as a stress marker of sea urchin coelomocytes in short term cultures. Cell Mol Biol 48(4):345–349
Matranga V, Pinsino A, Celi M, Natoli A, Bonaventura R, Schröder HC, Müller WEG (2005) Monitoring chemical and physical stress using sea urchin immune cells. Progress in molecular and subcellular biology. Subseries marine molecular biotechnology. In: Matranga V (ed) Echinodermata. Springer, Berlin/Heidelberg
Matranga V, Pinsino A, Celi M, Di Bella G, Natoli A (2006) Impacts of UV-B radiation on short-term cultures of sea urchin coelomocytes. Mar Biol 149:25–34
Matsuzaki K, Murase O, Fujii N, Miyajima K (1996) An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry 35(35):11361–11368
McCauley BS, Weideman EP, Hinman VF (2010) A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev Biol 340(2):200–208
Melo MN, Ferre R, Castanho MARB (2009) Opinion: antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7(3):245–250
Messier-Solek C, Buckley KM, Rast JP (2010) Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol 22(1):39–47
Metchnikoff E (1893) Lectures on the comparative pathology of inflammation, delivered at the Pasteur Institute in 1891. Kegan Paul, Trench, Rtubner & Co., Ltd., London, pp xii–218
Miller RJ, Colodey AG (1983) Widespread mass mortalities of the green sea urchin in Nova Scotia, Canada. Mar Biol 73:263–267
Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TC (2007) The innate immune repertoire in Cnidaria—ancestral complexity and stochastic gene loss. Genome Biol 8(4):1–13
Miller CA, Buckley KM, Easley RL, Smith LC (2010) An Sp185/333 gene cluster from the purple sea urchin and putative microsatellite-mediated gene diversification. BMC Genomics 11(1):575
Mogilenko DA, Kudriavtsev IV, Orlov SV, Kharazova AD, Polevshchikov AV (2010) Expression of the starfish complement component C3 gene homologue under the influence of bacterial lipopolysaccharide. Mol Biol (Mosk) 44:74–84
Mohammadizadeh F, Ehsanpor M, Afkhami M, Mokhlesi A, Khazaali A, Montazeri S (2013) Evaluation of antibacterial, antifungal and cytotoxic effects of Holothuria scabra from the north coast of the Persian Gulf. J Mycol Med 23(4):225–229
Moore HB, Jutare T, Bauer JC, Jones JA (1963) The biology of Lytechinus variegatus. Bull Mar Sci Gulf Caribb 13:23–53
Moritz C, Agudo R (2013) The future of species under climate change: resilience or decline? Science 341:504–508
Moses C, Bonem R (2001) Recent population dynamics of Diadema antillarum and Tripneustes ventricosus along the north coast of Jamaica, WI. Bull Mar Sci 68:327–336
Mosser DD, Caron AW, Bourget L, Meriin AB, Sherman MY, Morimoto RI, Massie B (2000) The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20:7146–7159
Multerer KA, Smith LC (2004) Two cDNAs from the purple sea urchin, Strongylocentrotus purpuratus, encoding mosaic proteins with domains found in factor H, factor I, and complement components C6 and C7. Immunogenetics 56:89–106
Nair SV, Del Valle H, Gross PS, Terwilliger DP, Smith LC (2005) Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol Genomics 22(1):33–47
Narula J, Smith AM, Gottgens B, Igoshin OA (2010) Modeling reveals bistability and low-pass filtering in the network module determining blood stem cell fate. PLoS Comput Biol 6(5):e1000771
Narula J, Williams CJ, Tiwari A, Marks-Bluth J, Pimanda JE, Igoshin OA (2013) Mathematical model of a gene regulatory network reconciles effects of genetic perturbations on hematopoietic stem cell emergence. Dev Biol 379(2):258–269
Noll H, Matranga V, Cervello M, Humphreys T, Kuwasaki B, Adelson D (1985) Characterization of toposomes from sea urchin blastula cells: a cell organelle mediating cell adhesion and expressing positional information. Proc Natl Acad Sci U S A 82(23):8062–8066
Noll H, Alcedo J, Daube M, Frei E, Schiltz E, Hunt J, Humphries T, Matranga V, Hochstrasser M, Aebersold R, Lee H, Noll M (2007) The toposome, essential for sea urchin cell adhesion and development, is a modified iron-less calcium-binding transferrin. Dev Biol 310(1):54–70
Nonaka M, Azumi K (1999) Opsonic complement system of the solitary ascidian, Halocynthia roretzi. Dev Comp Immunol 23:421–427
Norris RD, Turner SK, Hull PM, Ridgwell A (2013) Marine ecosystem responses to Cenozoic global change. Science 341(6145):492–498
Nydam ML, De Tomaso AW (2011) Creation and maintenance of variation in allorecognition loci: molecular analysis in various model systems. Front Immunol 2:79
O’Laughlin PM, Waters JM (2004) A molecular and morphological revision of genera of Asterinidae (Echinodermata: Asteroidea). Mem Mus Victoria 61(1):1–40
Ogden JC, Abbott DP, Abbott, IA (eds) (1973) Studies on the activity pattern and food of the echinoid Diadema antillarum Philippi on a West Indian patch reef. Special publication no. 2, West Indies Laboratory of Fairleigh Dickinson Univ., St. Croix, Virgin Islands, p 96
Ohguro Y, Takata H, Kominami T (2011) Involvement of Delta and Nodal signals in the specification process of five types of secondary mesenchyme cells in embryo of the sea urchin, Hemicentrotus pulcherrimus. Dev Growth Differ 53(1):110–123
Oren T, Torregroza I, Evans T (2005) An Oct-1 binding site mediates activation of the gata2 promoter by BMP signaling. Nucleic Acids Res 33(13):4357–4367
Oren M, Barela Hudgell MA, D’Allura B, Agronin J, Gross A, Podini D, Smith LC (2016a) Short tandem repeats, segmental duplications, gene deletion, and genomic instability in a rapidly diversified immune gene family. BMC Genomics 17:900
Oren M, Barela Hudgell MA, Golconda P, Lun CM, Smith LC (2016b) Genomic instability and shared mechanisms for gene diversification in two distant immune gene families: the echinoid 185/333 and the plant NBS-LRR. In: Malagoli D (ed) The evolution of the immune system, conservation and diversification. Elsevier Inc/Academic Press, London, pp 295–310
Oweson C, Sköld H, Pinsino A, Matranga V, Hernroth B (2008) Manganese effects on haematopoietic cells and circulating coelomocytes of Asterias rubens (Linnaeus). Aquat Toxicol 89:75–81
Oweson C, Li C, Söderhäll I, Hernroth B (2010) Effects of manganese and hypoxia on coelomocyte renewal in the echinoderm Asterias rubens (L.). Aquat Toxicol 100:84–90
Pag U, Sahl HG (2002) Lanthionine-containing bacterial peptides. In: Dutton CJ, Haxell MA, McArthur HAI, Wax RG (eds) Peptide antibiotics: discovery, mode of actions, and applications. Dekker M, New York, pp 47–80
Pagliara P, Stabili L (2012) Zinc effect on the sea urchin Paracentrotus lividus immunological competence. Chemosphere 89(5):563–568
Palumbi SR, Lessios HA (2005) Evolutionary animation: how do molecular phylogenies compare to Mayr’s reconstruction of speciation patterns in the sea? Proc Natl Acad Sci U S A 102:6566–6572
Pancer Z (2000) Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci U S A 97:13156–13161
Pancer Z (2001) Individual-specific repertoires of immune cells SRCR receptors in the purple sea urchin (S. purpuratus). Adv Exp Med Biol 484:31–40
Pancer Z, Rast JP, Davidson EH (1999) Origins of immunity: transcription factors and homologues of effector genes of the vertebrate immune system expressed in sea urchin coelomocytes. Immunogenetics 49(9):773–786
Park CB, Kim HS, Kim SC (1998) Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem Biophys Res Commun 244(1):253–257
Pearse J, Costa D, Yellin M, Agegian C (1977) Localized mass mortality of red sea urchin, Strongylocentrotus franciscanus, near Santa Cruz, California. Fish Bull US 75:645–648
Pearson CE, Edamura KN, Cleary JD (2005) Repeat instability: mechanisms of dynamic mutations. Nat Rev Genet 6(10):729–742
Pena MH, Oxenford HA, Parker C, Johnson A (2010) Biology and fishery management of the white sea urchin, Tripneustes ventricosus, in the eastern Caribbean. FAO Fisheries and Aquaculture Circular No. 1056. FAO, Rome
Peng M, Niu D, Chen Z, Lan T, Dong Z, Tran TN, Li J (2017) Expression of a novel complement C3 gene in the razor clam Sinonovacula constricta and its role in innate immune response and hemolysis. Dev Comp Immunol 73:184–192
Perez-Portela R, Turon X, Riesgo A (2016) Characterization of the transcriptome and gene expression of four different tissues in the ecologically relevant sea urchin Arbacia lixula using RNA-seq. Mol Ecol Resour 16(3):794–808
Perry G, Epel D (1981) Ca2+-stimulated production of H2O2 from naphthoquinone oxidation in Arbacia eggs. Exp Cell Res 134(1):65–72
Pimanda JE, Ottersbach K, Knezevic K, Kinston S, Chan WYI, Wilson NK, Landry JR, Wood AD, Kolb-Kokocinski A, Green AR, Tannahill D, Lacaud G, Kouskoff V, Göttgens B (2007) Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci U S A 104(45):17692–17697
Pini A, Giuliani A, Falciani C, Runci Y, Ricci C, Lelli B, Malossi M, Neri P, Rossolini GM, Bracci L (2005) Antimicrobial activity of novel dendrimeric peptides obtained by phage display selection and rational modification. Antimicrob Agents Chemother 49(7):2665–2672
Pinsino A, Matranga V (2015) Sea urchin immune cells as sentinels of environmental stress. Dev Comp Immunol 49:198–205
Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post-traumatic response in the common sea star Asterias rubens. Cell Stress Chaperones Winter 12(4):331–341
Pinsino A, Della Torre C, Sammarini V, Bonaventura R, Amato E, Matranga V (2008) Sea urchin coelomocytes as a novel cellular biosensor of environmental stress: a field study in the Tremiti Island Marine Protected Area, Southern Adriatic Sea, Italy. Cell Biol Toxicol 24(6):541–552
Pinsino A, Russo R, Bonaventura R, Brunelli A, Marcomini A, Matranga V (2015) Titanium dioxide nanoparticles stimulate sea urchin immune cell phagocytic activity involving TLR/p38 MAPK-mediated signaling pathway. Sci Rep 5:14492
Pisani D, Feuda R, Peterson JK, Smith AB (2012) Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships. Mol Phylogenet Evol 62(1):27–34
Plytycz B, Seljelid R (1993) Bacterial clearance by the sea urchin, Strongylocentrotus droebachiensis. Dev Comp Immunol 17(3):283–289
Prado-Alvarez M, Rotllant J, Gestal C, Novoa B, Figueras A (2009) Characterization of a C3 and a factor B-like in the carpet-shell clam, Ruditapes decussatus. Fish Shellfish Immunol 26:305–315
Ramírez-Gómez F, García-Arrarás JE (2010) Echinoderm immunity. Invertebr Surviv J 7:211–220
Ramírez-Gómez F, Ortiz-Pineda PA, Rojas-Cartagena C, Suarez-Castillo EC, Garcia-Ararras JE (2008) Immune-related genes associated with intestinal tissue in the sea cucumber Holothuria glaberrima. Immunogenetics 60:57–71
Ransick A, Davidson EH (2006) Cis-regulatory processing of Notch signaling input to the sea urchin glial cells missing gene during mesoderm specification. Dev Biol 297(2):587–602
Ransick A, Davidson EH (2012) Cis-regulatory logic driving glial cells missing: self-sustaining circuitry in later embryogenesis. Dev Biol 364(2):259–267
Rast JP, Messier-Solek C (2008) Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol Bull 214(3):274–283
Rast JP, Oliveri P, Davidson EH (2000) Conserved linkage among sea urchin homologs of genes encoded in the vertebrate MHC region. In: Kasahara M (ed) The major histocompatibility complex: evolution, structure and function. Springer, Tokyo, pp 66–74
Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314:952–956
Ray S, Mukherjee S, Bhunia NS, Bhunia AS, Ray M (2015) Immunotoxicological threats of pollutants in aquatic invertebrates. In: Larramendy ML (ed) Emerging pollutants in the environment—current and further implications. InTech, Croatia, pp 147–165
Reddy KV, Yedery RD, Aranha C (2004) Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 24(6):536–547
Reich A, Dunn C, Akasaka K, Wessel G (2015) Phylogenomic analyses of Echinodermata support the sister groups of Asterozoa and Echinozoa. PLoS One 10(3):e0119627
Reinardy HC, Bodnar AG (2015) Profiling DNA damage and repair capacity in sea urchin larvae and coelomocytes. Mutagenesis 30:829–839
Reinardy HC, Chapman J, Bodnar AG (2016) Induction of innate immune gene expression following methyl methanesulfonate-induced DNA damage in sea urchins. Biol Lett 12:20151057
Reinisch CL, Bang FB (1971) Cell recognition: reactions of the sea star (Asterias vulgaras) to the injection of amebocytes of sea urchin (Arbacia punctulata). Cell Immunol 2(5):496–503
Ridzwan BH, Kaswandi MA, Azman Y, Fuad M (1995) Screening for antibacterial agents in three species of sea cucumbers from coastal areas of Sabah. Gen Pharmacol 26(7):1539–1543
Riemann D, Kehlen A, Langner J (1999) CD13—not just a marker in leukemia typing. Immunol Today 20(2):83–88
Rizzo F, Fernandez-Serra M, Squarzoni P, Archimandritis A, Arnone MI (2006) Identification and developmental expression of the ets gene family in the sea urchin (Strongylocentrotus purpuratus). Dev Biol 300(1):35–48
Robert J (2010) Comparative study of tumorigenesis and tumor immunity in invertebrates and nonmammalian vertebrates. Dev Comp Immunol 34:915–925
Robertson DR (1991) Increase in surgeonfish populations after mass mortality of the sea urchin Diadema antillarum in Panama indicate food limitation. Mar Biol 111(3):437–444
Rosado CJ, Kondos S, Bull TE, Kuiper MJ, Law RHP, Buckle AM, Voskoboinik I, Bird PI, Trapani JA, Whisstock JC, Dunstone MA (2008) The MACPF/CDC family of pore-forming toxins. Cell Microbiol 10(9):1765–1774
Rosenfeld Y, Papo N, Shai Y (2006) Endotoxin (lipopolysaccharide) neutralization by innate immunity host-defense peptides—peptide properties and plausible modes of action. J Biol Chem 281(3):1636–1643
Rosengarten RD, Nicotra ML (2011) Model systems of invertebrate allorecognition. Curr Biol 21(2):R82–R92
Roth RO, Wildins AG, Cooke GM, Raftos DA, Nair SV (2014) Characterization of the highly variable immune response gene family, He185/333, in the sea urchin, Heliocidaris erythrogramma. PLoS One 9(10):e62079
Ruffins SW, Ettensohn CA (1996) A fate map of the vegetal plate of the sea urchin (Lytechinus variegatus) mesenchyme blastula. Development 122(1):253–263
Russell MP, Ebert TA, Garcia V, Bodnar A (2012) Field and laboratory growth estimates of the sea urchin Lytechinus variegatus in Bermuda. In: Johnson C (ed) Echinoderms in a changing world. CRC Press, Boca Raton, FL, pp 133–139
Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39(12):1461–1468
Sammarco PW (1980) Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. J Exp Mar Biol Ecol 45:245–272
Sarrias MR, Gronlund J, Padilla O, Madsen J, Holmskov U, Lozano F (2004) The Scavenger Receptor Cysteine-Rich (SRCR) domain: an ancient and highly conserved protein module of the innate immune system. Crit Rev Immunol 24:1–37
Schatz DG (2004) Antigen receptor genes and the evolution of a recombinase. Semin Immunol 16:245–256
Scheibling R, Hennigar A (1997) Recurrent outbreaks of disease in sea urchins Strongylocentrotus droebachiensis in Nova Scotia: evidence for a link with large-scale meteorologic and oceanographic events. Mar Ecol Prog Ser 152:155–165
Scheibling R, Feehan C, Lauzon-Guay J (2010) Disease outbreaks associated with recent hurricanes cause mass mortality of sea urchins in Nova Scotia. Mar Ecol Prog Ser 408:109–116
Schillaci D, Arizza V, Parrinello N, Di Stefano V, Fanara S, Muccilli V, Cunsolo V, Haagensen JJA, Molin S (2010) Antimicrobial and antistaphylococcal biofilm activity from the sea urchin Paracentrotus lividus. J Appl Microbiol 108(1):17–24
Schillaci D, Cusimano MG, Cunsolo V, Saletti R, Russo D, Vazzana M, Vitale M, Arizza V (2013) Immune mediators of sea-cucumbers Holothuria tubulosa (Echinodermata) as a source of novel antimicrobial and anti-staphylococcal biofilm agents. AMB Express 3(1):35
Schillaci D, Cusimano MG, Spinello A, Barone G, Russo D, Vitale M, Parrinello D, Arizza V (2014) Paracentrin 1, a synthetic antimicrobial peptide from the sea-urchin Paracentrotus lividus, interferes with staphylococcal and Pseudomonas aeruginosa biofilm formation. AMB Express 4:78
Schillaci D, Spinello A, Cusimano MG, Cascioferro S, Barone G, Vitale M, Arizza V (2016) A peptide from human beta thymosin as a platform for the development of new anti-biofilm agents for Staphylococcus spp. and Pseudomonas aeruginosa. World J Microbiol Biotechnol 32(8):124
Schrankel CS, Solek CM, Buckley KM, Anderson MK, Rast JP (2016) A conserved alternative form of the purple sea urchin HEB/E2-2/E2A transcription factor mediates a switch in E-protein regulatory state in differentiating immune cells. Dev Biol 416(1):149–161
Schultz J (2016) Mass mortality events of echinoderms: global patterns and local consequences. MS Thesis, Simon Fraser University
Schultz J, Clouthier RN, Côté IM (2016) Evidence for trophic cascade on rocky reefs following sea star mass mortality in British Columbia. PeerJ 4:e1980
Schurr MJ, Martin DW, Mudd MH, Deretic V (1994) Gene cluster controlling conversion to alginate-overproducing phenotype in Pseudomonas aeruginosa: functional analysis in a heterologous host and role in the instability of mucoidy. J Bacteriol 176(11):3375–3382
Scott MG, Gold MR, Hancock REW (1999) Interaction of cationic peptides with lipoteichoic acid and Gram-positive bacteria. Infect Immun 67(12):6445–6453
Sekiguchi R, Fujito NT, Nonaka M (2012) Evolution of the thioester-containing proteins (TEPs) of the arthropoda, revealed by molecular cloning of TEP genes from a spider, Hasarius adansoni. Dev Comp Immunol 36:483–489
Service M, Wardlaw AC (1984) Echinochrome-A as a bactericidal substance in the coelomic fluid of Echinus esculentus (L.). Comp Biochem Physiol B Comp Biochem 79(2):161–165
Shah M, Brown KM, Smith LC (2003) The gene encoding the sea urchin complement protein, SpC3, is expressed in embryos and can be upregulated by bacteria. Dev Comp Immunol 27:529–538
Sherman LS, Schrankel CS, Brown KJ, Smith LC (2015) Extraordinary diversity of immune response proteins among sea urchins: nickel-isolated Sp185/333 proteins show broad variations in size and charge. PLoS One 10(9):e0138892
Sherwood DR, McClay DR (1999) LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126(8):1703–1713
Shi JS, Ross CR, Leto TL, Blecha F (1996) PR-39, a proline-rich antibacterial peptide that inhibits phagocyte NADPH oxidase activity by binding to Src homology 3 domains of p47(phox). Proc Natl Acad Sci USA 93(12):6014–6018
Shimizu M (1994) Histopathological investigation of the spotted gonad disease in the sea urchin, Strongylocentrotus intermedius. J Invertebr Pathol 63:182–187
Shin YP, Park HJ, Shin SH, Lee YS, Park S, Jo S, Lee YH, Lee IH (2010) Antimicrobial activity of a halocidin-derived peptide resistant to attacks by proteases. Antimicrob Agents Chemother 54(7):2855–2866
Shipp LE, Hill RZ, Moy GW, Gökırmak T, Hamdoun A (2015) ABCC5 is required for cAMP-mediated hindgut invagination in sea urchin embryos. Development 142(20):3537–3548
Shoguchi E, Tokuoka M, Kominami T (2002) In situ screening for genes expressed preferentially in secondary mesenchyme cells of sea urchin embryos. Dev Genes Evol 212(9):407–418
Shukla A, Fleming KE, Chuang HF, Chau TM, Loose CR, Stephanopoulos GN, Hammond PT (2010) Controlling the release of peptide antimicrobial agents from surfaces. Biomaterials 31(8):2348–2357
Silva JR (2000) The onset of phagocytosis and identity in the embryo of Lytechinus variegatus. Dev Comp Immunol 24(8):733–739
Sim RB, Sim E (1981) Autolytic fragmentation of complement components C3 and C4 under denaturing conditions, a property shared with alpha 2-macroglobulin. Biochem J 193(1):129–141
Skerjanc IS, Truong J, Filion P, McBurney MW (1996) A splice variant of the ITF-2 transcript encodes a transcription factor that inhibits MyoD activity. J Biol Chem 271(7):3555–3561
Skjoedt MO, Palarasah Y, Rasmussen K, Vitved L, Salomonsen J, Kliem A, Hansen S, Koch C, Skjodt K (2010) Two mannose-binding lectin homologues and an MBL-associated serine protease are expressed in the gut epithelia of the urochordate species Ciona intestinalis. Dev Comp Immunol 34:59–68
Smith VJ (1981) The echinoderms. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Academic Press, New York, pp 513–562
Smith LC (2002) Thioester function is conserved in SpC3, the sea urchin homologue of the complement component C3. Dev Comp Immunol 26:603–614
Smith LC (2012) Innate immune complexity in the purple sea urchin: diversity of the Sp185/33 system. Front Immunol 3:70
Smith LC, Coscia MR (2016) Tuning the host–pathogen relationship through evolution with a special focus on the echinoid Sp185/333 system. Invertebr Surviv J 13:355–373
Smith LC, Davidson EH (1992) The echinoid immune system and the phylogenetic occurrence of immune mechanisms in deuterostomes. Immunol Today 13(9):356–362
Smith LC, Davidson EH (1994) The echinoid immune system. Characters shared with vertebrate immune systems and characters arising in deuterostome phylogeny. Ann N Y Acad Sci 712:213–236
Smith LC, Lun CM (2016) Research highlight: multitasking rSp0032 has anti-pathogen binding activities predicting flexible and effective immune responses in sea urchins mediated by the Sp185/333 system. Pathog Infect Dis 2:e1394
Smith LC, Lun CM (2017) The SpTransformer gene family (formerly Sp185/333) in the purple sea urchin and the functional diversity of the antipathogen rSpTransformer-E1 protein. Front Immunol 8:725
Smith LC, Britten RJ, Davidson EH (1992) SpCoel1, a sea urchin profilin gene expressed specifically in coelomocytes in response to injury. Mol Biol Cell 3:403–414
Smith LC, Chang L, Britten RJ, Davidson EH (1996) Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags—complement homologues and other putative immune response genes suggest immune system homology within the deuterostomes. J Immunol 156:593–602
Smith LC, Shih CS, Dachenhausen SG (1998) Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J Immunol 161:6784–6793
Smith LC, Azumi K, Nonaka M (1999) Complement systems in invertebrates. The ancient alternative and lectin pathways. Immunopharmacology 42(1–3):107–120
Smith LC, Clow LA, Terwilliger DP (2001) The ancestral complement system in sea urchins. Immunol Rev 180:16–34
Smith LC, Ghosh J, Buckley KM, Clow LA, Dheilly NM, Haug T, Henson JH, Li C, Lun CM, Majeske AJ, Matranga V, Nair SV, Rast JP, Raftos DA, Roth M, Sacchi S, Schrankel, CS, Stensvåg K (2010) Echinoderm immunity. In: Soderhall K (ed) Invertebrate immunity. Madame Curie Bioscience Database, Landes Biosciences, Austin TX. Adv Exp Med Biol 708:260–301
Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, Elphick MR, Ettensohn CA, Foltz KR, Hamdoun A, Hynes RO, Klein WH, Marzluff W, McClay DR, Morris RL, Mushegian A, Rast JP, Smith LC, Thorndyke MC, Vacquier VD, Wessel GM, Wray G, Zhang L, Elsik CG, Ermolaeva O, Hlavina W, Hofmann G, Kitts P, Landrum MJ, Mackey AJ, Maglott D, Panopoulou G, Poustka AJ, Pruitt K, Sapojnikov V, Song X, Souvorov A, Solovyev V, Wei Z, Whittaker CA, Worley K, Durbin KJ, Shen Y, Fedrigo O, Garfield D, Haygood R, Primus A, Satija R, Severson T, Gonzalez-Garay ML, Jackson AR, Milosavljevic A, Tong M, Killian CE, Livingston BT, Wilt FH, Adams N, Bellé R, Carbonneau S, Cheung R, Cormier P, Cosson B, Croce J, Fernandez-Guerra A, Genevière A-M, Goel M, Kelkar H, Morales J, Mulner-Lorillon O, Robertson AJ, Goldstone JV, Cole B, Epel D, Gold B, Hahn ME, Howard-Ashby M, Scally M, Stegeman JJ, Allgood EL, Cool J, Judkins KM, McCafferty SS, Musante AM, Obar RA, Rawson AP, Rossetti BJ, Gibbons IR, Hoffman MP, Leone A, Istrail S, Materna SC, Samanta MP, Stolc V, Tongprasit W, Tu Q, Bergeron K-F, Brandhorst BP, Whittle J, Berney K, Bottjer DJ, Calestani C, Peterson K, Chow E, Yuan QA, Elhaik E, Graur D, Reese JT, Bosdet I, Heesun S, Marra MA, Schein J, Anderson MK, Brockton V, Buckley KM, Cohen AH, Fugmann SD, Hibino T, Loza-Coll M, Majeske AJ, Messier C, Nair SV, Pancer Z, Terwilliger DP, Agca C, Arboleda E, Chen N, Churcher AM, Hallböök F, Humphrey GW, Idris MM, Kiyama T, Liang S, Mellott D, Mu X, Murray G, Olinski RP, Raible F, Rowe M, Taylor JS, Tessmar-Raible K, Wang D, Wilson KH, Yaguchi S, Gaasterland T, Galindo BE, Gunaratne HJ, Juliano C, Kinukawa M, Moy GW, Neill AT, Nomura M, Raisch M, Reade A, Roux MM, Song JL, Su Y-H, Townley IK, Voronina E, Wong JL, Amore G, Branno M, Brown ER, Cavalieri V, Duboc V, Duloquin L, Flytzanis C, Gache C, Lapraz F, Lepage T, Locascio A, Martinez P, Matassi G, Matranga V, Range R, Rizzo F, Röttinger E, Beane W, Bradham C, Byrum C, Glenn T, Hussain S, Manning G, Miranda E, Thomason R, Walton K, Wikramanayke A, Wu S-Y, Xu R, Brown CT, Chen L, Gray RF, Lee PY, Nam J, Oliveri P, Smith J, Muzny D, Bell S, Chacko J, Cree A, Curry S, Davis C, Dinh H, Dugan-Rocha S, Fowler J, Gill R, Hamilton C, Hernandez J, Hines S, Hume J, Jackson L, Jolivet A, Kovar C, Lee S, Lewis L, Miner G, Morgan M, Nazareth LV, Okwuonu G, Parker D, Pu L-L, Thorn R, Wright R (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314(5801):941–952
Solek CM, Oliveri P, Loza-Coll M, Schrankel CS, Ho ECH, Wang G, Rast JP (2013) An ancient role for Gata-1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol 382(1):280–292
Solstad RG, Li C, Isaksson J, Johansen J, Svenson J, Stensvag K, Haug T (2016) Novel antimicrobial peptides EeCentrocins 1, 2 and EeStrongylocin 2 from the edible sea urchin Echinus esculentus have 6-Br-Trp post-translational modifications. PLoS One 11(3):e0151820
Spizek J, Novotna J, Rezanka T, Demain AL (2010) Do we need new antibiotics? The search for new targets and new compounds. J Ind Microbiol Biotechnol 37(12):1241–1248
Spoering AL, Gilmore MS (2006) Quorum sensing and DNA release in bacterial biofilms. Curr Opin Microbiol 9(2):133–137
Stabili L, Pagliara P (2009) Effect of zinc on lysozyme-like activity of the seastar Marthasterias glacialis (Echinodermata, Asteroidea) mucus. J Invertebr Pathol 100:189–192
Stabili L, Pagliara P (2015) The sea urchin Paracentrotus lividus immunological response to chemical pollution: the case of the pesticide lindane. Chemosphere 134:60–66
Stein A, Halvorsen O (1998) Experimental transmission of the Nematode Echinomermella matsi to the sea urchin Strongylocentrotus drobachiensis in the laboratory. J Parasitol 84:658–666
Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) (2013) IPCC, 2013: summary for policymakers. In: Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK/New York
Stokstad E (2014) Death of the stars. Science 344:464–467
Subbalakshmi C, Sitaram N (1998) Mechanism of antimicrobial action of indolicidin. FEMS Microbiol Lett 160(1):91–96
Suzuki MM, Satoh N, Nonaka M (2002) C6-like and C3-like molecules from the cephalochordate, amphioxus, suggest a cytolytic complement system in invertebrates. J Mol Evol 54:671–679
Sweet HC, Gehring M, Ettensohn CA (2002) LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 129(8):1945–1955
Szabo DT, Loccisano AE (2012) POPs and human health risk assessment. In: Schecter A (ed) Dioxins and health including other persistent organic pollutants and endocrine disruptors, 3rd edn. Wiley, Hoboken
Taguchi M, Tsutsui S, Nakamura O (2016) Differential count and time-course analysis of the cellular composition of coelomocyte aggregate of the Japanese sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 58:203–209
Taketa DA, DeTomaso AW (2015) Botryllus schlosseri allorecognition: tackling the enigma. DCI 48(1):254–265
Tamboline CR, Burke RD (1992) Secondary mesenchyme of the sea urchin embryo: ontogeny of blastocoelar cells. J Exp Zool 262(1):51–60
Terwilliger DP, Clow LA, Gross PS, Smith LC (2004) Constitutive expression and alternative splicing of the exons encoding SCRs in Sp152, the sea urchin homologue of complement factor B. Implications on the evolution of the Bf/C2 gene family. Immunogenetics 56:531–543
Terwilliger DP, Buckley KM, Mehta D, Moorjani PG, Smith LC (2006) Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpuratus. Physiol Genomics 26:134–144
Terwilliger DP, Buckley KM, Brockton V, Ritter NJ, Smith LC (2007) Distinctive expression patterns of 185/333 genes in the purple sea urchin, Strongylocentrotus purpuratus: an unexpectedly diverse family of transcripts in response to LPS, beta-1,3-glucan, and dsRNA. BMC Mol Biol 8:16
Thys RG, Lehman CE, Pierce LC, Wang Y-H (2014) The role of DNA secondary structures at human chromosomal fragile sites. Mol Biol 3(116):2
Tincu JA, Taylor SW (2004) Antimicrobial peptides from marine invertebrates. Antimicrob Agents Chemother 48(10):3645–3654
Tokuoka M, Setoguchi C, Kominami T (2002) Specification and differentiation processes of secondary mesenchyme-derived cells in embryos of the sea urchin Hemicentrotus pulcherrimus. Dev Growth Differ 44(3):239–250
Tomlinson S (1993) Complement defense mechanisms. Curr Opin Immunol 5(1):83–89
Turton G, Wardlaw A (1987) Pathogenicity of the marine yeasts Metschnikowia zobelli and Rhodotorula rubra for the sea urchin Echinus esculentus. Aquaculture 67:199–202
Ullrich-Lüter EM, Dupont S, Arboleda E, Hausen H, Arnone MI (2011) Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci U S A 108(20):8367–8372
Unuma T, Ikeda K, Yamano K, Moriyama A, Ohta H (2007) Zinc-binding property of the major yolk protein in the sea urchin—implications of its role as a zinc transporter for gametogenesis. FEBS J 274(19):4985–4998
Uversky VN (2010) Targeting intrinsically disordered proteins in neurodegenerative and protein dysfunction diseases: another illustration of the D2 concept. Expert Rev Proteomics 7:543–564
Vasilenko AA, Kovalchuk SN, Bulgakov AA, Petrova IY, Rasskazov VA (2012) Obtaining and refolding of a recombinant mannan-binding lectin from the holothurian Apostichopus japonicus. Biologiya Morya-Mar Biol 38:72–78
Veldhuizen EJ, Schneider VA, Agustiandari H, van Dijk A, Tjeerdsma-van Bokhoven JL, Bikker FJ, Haagsman HP (2014) Antimicrobial and immunomodulatory activities of PR-39 derived peptides. PLoS One 9(4):e95939
Vethamany VG, Fung M (1972) The fine structure of coelomocytes of the sea urchin, Strongylocentrotus droebachiensis (Muller, O. F.). Can J Zool 50:77–81
Vieira-Pires RS, Morais-Cabral JH (2010) 3(10) helices in channels and other membrane proteins. J Gen Physiol 136:585–592
Vijgen J, Abhilash PC, Li YF, Lal R, Forter M, Torres J, Singh N, Yunus M, Tian C, Schäffer A, Weber R (2011) Hexachlorocyclohexane (HCH) as new Stockholm convention POPs—a global perspective on the management of Lindane and its waste isomers. Environ Sci Pollut Res 18(2):152–162
Volanakis JE (1998) Overview of the complement system. In: Volanakis JE, Frank MM (eds) The human complement system in health and disease. Marcel Dekker, New York, pp 9–32
von Heijne G (1990) The signal peptide. J Membr Biol 115(3):195–201
Walmsley M, Ciau-Uitz A, Patient R (2002) Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus. Development 129(24):5683–5695
Wang Y, Xu G, Zhang C, Sun S (2005) Main diseases of cultured Apostichopus japonicus: prevention and treatment. Mar Sci 29:1–7
Wang D, Claus CL, Vaccarelli G, Braunstein M, Schmitt TM, Zuñiga-Pflücker J-C, Rothenberg EV, Anderson MK (2006) The basic helix–loop–helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J Immunol 177(1):109–119
Wang JJ, Chou SL, Xu L, Zhu X, Dong N, Shan AS, Chen ZH (2015) High specific selectivity and membrane-active mechanism of the synthetic centrosymmetric alpha-helical peptides with Gly-Gly pairs. Sci Rep 5:15963
Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32:W668–W673
Whitmore L, Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392–400
Wilson DR, Norton DD, Fugmann SD (2008) The PHD domain of the sea urchin RAG2 homolog, SpRAG2L, recognizes dimethylated lysine 4 in histone H3 tails. Dev Comp Immunol 32:1221
Wilson NK, Foster SD, Wang X, Knezevic K, Schütte J, Kaimakis P, Chilarska PM, Kinston S, Ouwehand WH, Dzierzak E, Pimanda JE, de Bruijn MF, Göttgens B (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Stem Cell 7(4):532–544
Xing K, Yang HS, Chen MY (2008) Morphological and ultrastructural characterization of the coelomocytes in Apostichopus japonicas. Aquat Biol 2(1):85–92
Xue Z, Li H, Wang X, Li X, Liu Y, Sun J, Liu C (2015) A review of the immune molecules in the sea cucumber. Fish Shellfish Immunol 44(1):1–11
Yang L, Harroun TA, Weiss TM, Ding L, Huang HW (2001) Barrel-stave model or toroidal model? A case study on melittin pores. Biophys J 81(3):1475–1485
Yeaman MR, Yount NY (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55(1):27–55
Yonezawa A, Sugiura Y (1992) Tachyplesin I as a model peptide for antiparallel beta-sheet DNA binding motif. Nucleic Acids Symp Ser 27:161–162
Yui M, Bayne C (1983) Echinoderm immunity: bacterial clearance by the sea urchin Strongylocentrotus purpuratus. Biol Bull 165:473–485
Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415(6870):389–395
Zhang C, Wang Y, Rong X (2006) Isolation and identification of causative pathogen for skin ulcerative syndrome in Apostichopus japonicus. J Fish China 30:118–123
Zhang P, Li C, Li Y, Zhang P, Shao Y, Jin C, Li T (2014) Proteomic identification of differentially expressed proteins in sea cucumber Apostichopus japonicus coelomocytes after Vibrio splendidus infection. Dev Comp Immunol 44(2):370–377
Zhang L, Li L, Guo X, Litman GW, Dishaw LJ, Zhang G (2015) Massive expansion and functional divergence of innate immune genes in a protostome. Sci Rep 5:8693
Zhao H, Mattila JP, Holopainen JM, Kinnunen PK (2001) Comparison of the membrane association of two antimicrobial peptides, magainin 2 and indolicidin. Biophys J 81(5):2979–2991
Zhong L, Zhang F, Chang Y (2012) Gene cloning and function analysis of complement B factor-2 of Apostichopus japonicus. Fish Shellfish Immunol 33:504–513
Zhou Z, Sun D, Yang A, Dong Y, Chen Z, Wang X, Guan X, Jiang B, Wang B (2011) Molecular characterization and expression analysis of a complement component 3 in the sea cucumber (Apostichopus japonicus). Fish Shellfish Immunol 31:540–547
Zilberman M, Elsner JJ (2008) Antibiotic-eluting medical devices for various applications. J Control Release 130(3):202–215
Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nature Reviews. Mol Cel Biol 7:9–19
Zipfel PF, Skerka C (2009) Complement regulators and inhibitory proteins. Nat Rev Immunol 9:729–740
Dedication
This work is dedicated to Valeria Matranga who passed away too young in April 2016 after a long and courageous battle against cancer. Valeria contributed immensely to our understanding of cellular and molecular immune processes in the sea urchin, Paracentrotus lividus. Her dedicated research on echinoderms led to an understanding of how they interact with their environment and how coelomocytes can be employed to evaluate environmental toxins and pollutants. She and her insight for creative approaches in eco-immuno-toxicology will be missed because her approach to thinking about how to answer difficult scientific questions would have been more and more valuable in the future.
AcknowledgementsResearch by the authors that was the basis of some of the information integrated into this chapter was supported by funding from the US National Science Foundation to LCS, DAR, MO, and JHH; the National Institute on Aging, a Bermuda charitable trust, and The Christian Humann Foundation to AGB; the European Molecular Biology Organization to NF; the Keio Gijuku Academic Development Funds to RF; the Chang Gung Medical Research Program and the Ministry of Science and Technology to SDF; HORIZON 2020 – The EU Framework Programme for Research and Innovation under the Marie Skłodowska-Curie Actions to AP; the Australian Research Council to DAR; the Canadian Institutes for Health Research and the Natural Sciences and Engineering Research Council of Canada to JPR; and the Tromsø Forskninsgstiftelse and the UiT The Arctic University of Norway to KS.
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Smith, L.C. et al. (2018). Echinodermata: The Complex Immune System in Echinoderms. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_13
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