Annelid Coelomic Fluid Proteins

  • Sven SchenkEmail author
  • Ulrich Hoeger
Part of the Subcellular Biochemistry book series (SCBI, volume 94)


The coelomic cavity is part of the main body plan of annelids. This fluid filled space takes up a considerable volume of the body and serves as an important site of exchange of both metabolites and proteins. In addition to low molecular substances such as amino acids and glucose and lactate, the coelomic fluid contains different proteins that can arise through release from adjacent tissues (intestine) or from secretion by coelomic cells. In this chapter, we will review the current knowledge about the proteins in the annelid coelomic fluid. Given the number of more than 20,000 extant annelid species, existing studies are confined to a relatively few species. Most studies on the oligochaetes are confined to the earthworms—clearly because of their important role in soil biology. In the polychaetes (which might represent a paraphyletic group) on the other hand, studies have focused on a few species of the Nereidid family. The proteins present in the coelomic fluid serve different functions and these have been studied in different taxonomic groups. In oligochaetes, proteins involved antibacterial defense such as lysenin and fetidin have received much attention in past and ongoing studies. In polychaetes, in contrast, proteins involved in vitellogenesis and reproduction, and the vitellogenic function of coelomic cells have been investigated in more detail. The metal binding metallothioneins as well as antimicrobial peptides, have been investigated in both oligochaetes and polychaetes. In the light of the literature available, this review will focus on lipoproteins, especially vitellogenin, and proteins involved in defense reactions. Other annelid groups such as the Pogonophora, Echiura, and Sipuncula (now considered polychaetes), have not received much attention and therefore, this overview is far from being complete.


Annelids Polychaetes Coelomic cells Lipoproteins Vitellogenin Reproduction Defense reactions Defensive proteins Metalloproteins Antimicrobial peptides 


  1. Altincicek B, Vilcinskas A (2007) Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii. Front Zool 4:18. Scholar
  2. Andrä J, Jakovkin I, Grötzinger J, Hecht O, Krasnosdembskaya AD, Goldmann T, Gutsmann T, Leippe M (2008) Structure and mode of action of the antimicrobial peptide arenicin. Biochem J 410(1):113–122Google Scholar
  3. Arosio P, Levi S, Gabri E, Stefanini S, Finazziagro A, Chiancone E (1984) Properties of ferritin from the earthworm Octolasium complanatum. Biochim Biophys Acta 787(3):264–269.
  4. Baert JL (1985) Multiple forms of vitellin in young oocytes of Perinereis cultrifera (Polychaete Annelid): occurrence and relation to vitellin maturation in the oocyte. Comp Biochem Physiol 81B:851–856. Scholar
  5. Baert JL (1986) Evidence for vitellin maturation within the oocytes of Perinereis cultrifera (Polychaete Annelid). Comp Biochem Physiol 83B:847–853. Scholar
  6. Baert JL, Slomianny MC (1987) Heterosynthetic origin of the major yolk protein, vitellin, in a nereid, Perinereis cultrifera (Polychaete annelid). Comp Biochem Physiol 88B:1191–1199. Scholar
  7. Baert JL, Slomianny MC (1992) Vitellin accumulation and vitellogenin synthesis in relation to oogenesis in Perinereis cultrifera (Polychaeta, Annelida). Invertebr Reprod Dev 21:121–128. Scholar
  8. Baert JL, Britel M, Slomianny MC, Delbart C, Fournet B, Sautiere P, Malecha J (1991) Yolk protein in leech. Identification, purification and characterization of vitellin and vitellogenin. Eur J Biochem 201 (1):191–198.
  9. Baert JL, Britel M, Sautiere P, Malecha J (1992) Ovohemerythrin, a major 14-kDa yolk protein distinct from vitellogenin in leech. Eur J Biochem 209(2):563–569. Scholar
  10. Beschin A, Bilej M, Hanssens F, Raymakers J, Van Dyck E, Revets H, Brys L, Gomez J, De Baetselier P, Timmermans M (1998) Identification and cloning of a glucan- and lipopolysaccharide-binding protein from Eisenia foetida earthworm involved in the activation of prophenoloxidase cascade. J Biol Chem 273(38):24948–24954. Scholar
  11. Bilej M, Brys L, Beschin A, Lucas R, Vercauteren E, Hanušová R, De Baetselier P (1995) Identification of a cytolytic protein in the coelomic fluid of Eisenia foetida earthworms. Immunol Let 45:123–128CrossRefGoogle Scholar
  12. Bodo K, Boros A, Rumpler E, Molnar L, Borocz K, Nemeth P, Engelmann P (2019) Identification of novel lumbricin homologues in Eisenia andrei earthworms. Dev Comp Immunol 90:41–46. Scholar
  13. Bokori-Brown M, Martin TG, Naylor CE, Basak AK, Titball RW, Savva CG (2016) Cryo-EM structure of lysenin pore elucidates membrane insertion by an aerolysin family protein. Nat Commun 7:11293. Scholar
  14. Bonnier P, Baert J-L (1992) Vitellogenesis in the sand worm, Nereis diversicolor. Comp Biochem Physiol B 102(5):785–790. Scholar
  15. Bruhn H, Winkelmann J, Andersen C, Andra J, Leippe M (2006) Dissection of the mechanisms of cytolytic and antibacterial activity of lysenin, a defence protein of the annelid Eisenia fetida. Dev Comp Immunol 30(7):597–606. Scholar
  16. Bruno R, Maresca M, Canaan S, Cavalier JF, Mabrouk K, Boidin-Wichlacz C, Olleik H, Zeppilli D, Brodin P, Massol F, Jollivet D, Jung S, Tasiemski A (2019) Worms' antimicrobial peptides. Mar Drugs 17(9).
  17. Calisi A, Lionetto MG, De Lorenzis E, Leomanni A, Schettino T (2014) Metallothionein induction in the coelomic fluid of the earthworm Lumbricus terrestris following heavy metal exposure: a short report. Biomed Res Int 2014:109386. Scholar
  18. Chino H, Downer RG, Takahashi K (1977) The role of diacylglycerol-carrying lipoprotein I in lipid transport during insect vitellogenesis. Biochim Biophys Acta 487(3):508–516. Scholar
  19. Cho JH, Park CB, Yoon YG, Kim SC (1998) Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA cloning and molecular characterization. Biochim Biophys Acta 1408(1):67–76. Scholar
  20. Claus H, Decker H (2006) Bacterial tyrosinases. Syst Appl Microbiol 29:3–14. Scholar
  21. Coates CJ, Decker H (2017) Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin. Cell Mol Life Sci 74(2):293–317. Scholar
  22. Cooper EL (2002) Invertebrate immune responses. In: Advances in comparative and environmental physiology, vol 23. Springer, Berlin.
  23. Cooper EL, Stein EA (1981) Oligochaetes. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New York, pp 76–140Google Scholar
  24. Cooper EL, Kauschke E, Cossarizza A (2001) Annelid humoral immunity: cell lysis in earthworms. In: Beck G, Sugumaran M, Cooper EL (eds) Phylogenetic perspectives on the vertebrate immune system. Adv. Exp. Med. Biol. Springer, Berlin,Google Scholar
  25. Costa-Paiva EM, Schrago CG, Halanych KM (2017) Broad phylogenetic occurrence of the oxygen-binding hemerythrins in bilaterians. Genome Biol Evol 9(10):2580–2591.
  26. Costa-Paiva EM, Schrago CG, Coates CJ, Halanych KM (2018) Discovery of novel hemocyanin-like genes in metazoans. Biol Bull 235:134–151. Scholar
  27. Çotuk A, Dales RP (1984) Lysozyme activity in the coelomic fluid and coelomocytes of the earthworm Eisenia foetida Sav. in relation to bacterial infection. Comp Biochem Physiol A 78:469–474. Scholar
  28. Dales RP, Dixon LJR (1980) Responses of polychaete annelids to bacterial infection. Comp Biochem Physiol A 67:391–396. Scholar
  29. Dales RP, Dixon RJ (1981) Polychaetes. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New York, pp 35–74Google Scholar
  30. de Eguileor M, Grimaldi A, Tettamanti G, Valvassori R, Cooper EL, Lanzavecchia G (2000) Lipopolysaccharide-dependent induction of leech leukocytes that cross-react with vertebrate cellular differentiation markers. Tissue Cell 32(5):437–445CrossRefGoogle Scholar
  31. Decker H, Rimke T (1998) Tarantula hemocyanin shows phenoloxidase activity. J Biol Chem 273(40):25889–25892. Scholar
  32. Deloffre L, Salzet B, Vieau D, Andries JC, Salzet M (2003) Antibacterial properties of hemerythrin of the sand worm Nereis diversicolor. Neuro Endocrinol Lett 24(1–2):39–45PubMedGoogle Scholar
  33. Demuynck S, Sautiere P, van Beeumen J, Dhainaut-Courtois N (1991) Homologies between hemerythrins of sipunculids and cadmium-binding metalloprotein (MP II) from a polychaete annelid, Nereis diversicolor. C R Acad Sci III 312(7):317–322PubMedGoogle Scholar
  34. Demuynck S, Li KW, Van der Schors R, Dhainaut-Courtois N (1993) Amino acid sequence of the small cadmium-binding protein (MP II) from Nereis diversicolor (annelida, polychaeta). Evidence for a myohemerythrin structure. Eur J Biochem 217 (1):151–156.
  35. Dhainaut A, Porchet-Henneré E (1988) Haemocytes and coelomocytes. In: Westheide W, Hermans CO (eds) Microfauna marina, vol 4. Gustav Fischer Verlag, Stuttgart, pp 216–230Google Scholar
  36. Dhainaut A, Raveillon B, Mberi M, Porchet-Henneré E, Demuynck S (1989) Purification of an antibacterial protein in the coelomic fluid of Nereis diversicolor (Annelida, Polychaeta)—similitude with a cadmium-binding protein. Comp Biochem Phys C 94(2):555–560. Scholar
  37. Eckelbarger KJ (2005) Oogenesis and oocytes. Hydrobiologia 535:179–198. Scholar
  38. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. Scholar
  39. Engelmann P, Palinkas L, Cooper EL, Nemeth P (2005) Monoclonal antibodies identify four distinct annelid leukocyte markers. Dev Comp Immunol 29(7):599–614. Scholar
  40. Fiołka MJ, Zagaja MP, Hułas-Stasiak M, Wielbo J (2012) Activity and immunodetection of lysozyme in earthworm Dendrobaena veneta (Annelida). J Invertebr Pathol 109:83–90. Scholar
  41. Fiołka MJ, Czaplewska P, Macur K, Buchwald T, Kutkowska J, Paduch R, Kaczynski Z, Wydrych J, Urbanik-Sypniewska T (2019a) Anti-Candida albicans effect of the protein-carbohydrate fraction obtained from the coelomic fluid of earthworm Dendrobaena veneta. PLoS ONE 14(3):e0212869. Scholar
  42. Fiołka MJ, Rzymowska J, Bilska S, Lewtak K, Dmoszynska-Graniczka M, Grzywnowicz K, Kazmierski W, Urbanik-Sypniewska T (2019b) Antitumor activity and apoptotic action of coelomic fluid from the earthworm Dendrobaena veneta against A549 human lung cancer cells. APMIS 127(6):435–448. Scholar
  43. Fischer A (1979) A vitellin-like antigen in the coelomic fluid of maturing Nereis virens females. Naturwissenschaften 66:316CrossRefGoogle Scholar
  44. Fischer A, Rabien H, Heacox AE (1991) Specific, concentration-dependent uptake of vitellin by the oocytes of Nereis virens (Annelida: Polychaeta) in vitro. J Exp Zool 260:106–115. Scholar
  45. Fischer A, Dorresteijn AWC, Hoeger U (1996) Metabolism of oocyte construction and the origin of histospecificity in the cleaving egg. Lessons from nereid annelids. Int J Develop 40:421–430Google Scholar
  46. Fontaine F, Gevaert MH, Porchet M (1984a) Acylglycerol metabolism in the coelomic constituents during vitellogenesis of Perinereis cultrifera (Annelida Polychaeta). Comp Biochem Physiol B 78:581–584. Scholar
  47. Fontaine F, Gevaert MH, Porchet M (1984b) Distribution of neutral lipids in coelomic constituents during oogenesis of Perinereis cultrifera (Annelida Polychaeta). Comp Biochem Physiol A 77:45–50. Scholar
  48. Fowler BA, Hildebrand CE, Kojima Y, Webb M (1987) Nomenclature of metallothionein. Experientia Suppl 52:19–22. Scholar
  49. García-Alonso J, Rebscher N (2005) Estradiol signalling in Nereis virens reproduction. Invert Repr Develop 48(1–3):95–100. Scholar
  50. García-Alonso J, Hoeger U, Rebscher N (2006) Regulation of vitellogenesis in Nereis virens (Annelida: Polychaeta): Effect of estradiol-17b on eleocytes. Comp Biochem Physiol A 143(1):55–61. Scholar
  51. Giangrande A, Licciano M, Pagliara P, Gambi MC (2000) Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea. Mar Biol 136(5):847–861. Scholar
  52. Gruber C, Stürzenbaum SR, Gehring P, Sack R, Hunziker P, Berger B, Dallinger R (2000) Isolation and characterization of a self-sufficient one-domain protein (Cd)-Metallothionein from Eisenia foetida. Eur J Biochem 267:573–582. Scholar
  53. Hafer J, Fischer A, Ferenz HJ (1992) Identification of the yolk receptor protein in oocytes of Nereis virens (Annelida, Polychaeta) and comparison with the locust vitellogenin receptor. J Comp Physiol B 162:148–152. Scholar
  54. Harris JR, Hoeger U, Adrian M (2001) Transmission electron microscopical studies on some haemolymph proteins from the marine polychaete Nereis virens. Micron 32(6):599–613.
  55. Hauenschild C (1956) Hormonale Hemmung der Geschlechtsreife und Metamorphose bei dem Polychaeten Platynereis dumerilii. Zt Naturforsch B 11:125–132CrossRefGoogle Scholar
  56. Hayashi Y, Miclaus T, Engelmann P, Autrup H, Sutherland DS, Scott-Fordsmand JJ (2016) Nanosilver pathophysiology in earthworms: Transcriptional profiling of secretory proteins and the implication for the protein corona. Nanotoxicology 10:303–311. Scholar
  57. Hirigoyenberry F, Lassalle F, Lassegues M (1990) Antibacterial activity of Eisenia fetida andrei coelomic fluid: Transcription and translation of lysozyme and proteins evidenced after bacterial infestation. Comp Biochem Physiol B 95:71–75. Scholar
  58. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol Biol Evol 35(2):518–522. Scholar
  59. Hoeger U, Abe H (2004) ß-Alanine and other free amino acids during salinity adaption of the polychaete Nereis japonica. Comp Biochem Physiol A 137(1):161–171. Scholar
  60. Hoeger U, Kunz I (1993) Metabolic enzymes in coelomic cells (eleocytes) of the polychaete Nereis virens: sex specific changes during sexual maturation. Mar Biol 115:653–660. Scholar
  61. Hoeger U, Märker C (1997) Nucleotide pool changes in coelomic cells (eleocytes) of the polychaete Nereis virens during sexual maturation. Exp Biol Online 2–12 (12)Google Scholar
  62. Hoeger U, Märker C, Geier G (1996) Adenylate storage, metabolism and utilization of the polychaete Nereis virens (Annelida, Polychaeta). Experientia 52:481–486CrossRefGoogle Scholar
  63. Hoeger U, Rebscher N, Geier G (1999) Metabolite supply in growing oocytes of Nereis virens: role of nucleosides. Hydrobiologia 402:163–174. Scholar
  64. Homa J, Ortmann W, Kolaczkowska E (2016) Conservative mechanisms of extracellular trap formation by annelida Eisenia andrei: serine protease activity requirement. PLoS ONE 11:e0159031. Scholar
  65. Hussain MM, Shi J, Dreizen P (2003) Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J Lipid Res 44(1):22–32. Scholar
  66. Ishitsuka R, Kobayashi T (2007) Cholesterol and lipid/protein ratio control the oligomerization of a sphingomyelin-specific toxin, lysenin. Biochemistry 46(6):1495–1502. Scholar
  67. Ito Y, Ayako Y, Hotani T, Fukuda S, Sugimura K, Imoto T (1999) Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur J Biochem 259:456–461. Scholar
  68. Jamieson BGM (2006) Reproductive biology and phylogeny of annelida. In: Reproductive biology and phylogeny, vol 4, 1st edn. CRC Press, Boca Raton.
  69. Jeong BR, Chung SM, Baek NJ, Koo KB, Baik HS, Joo HS, Chang CS, Choi JW (2006) Characterization, cloning and expression of the ferritin gene from the Korean polychaete, Periserrula leucophryna. J Microbiol 44(1):54–63PubMedGoogle Scholar
  70. Josková R, Šilerová M, Procházková P, Bilej M (2009) Identification and cloning of an invertebrate-type lysozyme from Eisenia andrei. Dev Comp Immunol 33:932–938. Scholar
  71. Journet AM, Saffaripour S, Wagner DD (1993) Requirement for both D domains of the propolypeptide in von Willebrand factor multimerization and storage. Thromb Haemost 70(6):1053–1057CrossRefGoogle Scholar
  72. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. Scholar
  73. Kauschke E, Mohrig W (1987) Cytotoxic activity in the coelomic fluid of the annelid Eisenia foetida Sav. J Comp Physiol B 157:77–83. Scholar
  74. Kauschke E, Pagliara P, Stabili L, Cooper EL (1997) Characterization of proteolytic activity in coelomic fluid of Lumbricus terrestris L (Annelida, Lumbricidae). Comp Biochem Physiol B 116(2):235–242. Scholar
  75. Kauschke E, Mohrig W, Cooper EL (2007) Coelomic fluid proteins as basic components of innate immunity in earthworms. Eur J Soil Biol 43:S110–S115. Scholar
  76. Kiyokawa E, Makino A, Ishii K, Otsuka N, Yamaji-Hasegawa A, Kobayashi T (2004) Recognition of sphigomyelin by lysenin and lysenin-related protein. Biochemistry 43:9766–9773. Scholar
  77. Klotz IM, Kurtz DM (1984) Binuclear oxygen carriers: hemerythrin. Accounts Chem Res 17(1):16–22.
  78. Kulakosky PC, Telfer WH (1990) Lipophorin as a yolk precursor in Hyalophora cecropia: Uptake kinetics and competition with vitellogenin. Arch Biochem Biophys 14:269–285. Scholar
  79. Lange S, Nussler F, Kauschke E, Lutsch G, Cooper EL, Herrmann A (1997) Interaction of earthworm hemolysin with lipid membranes requires sphingolipids. J Biol Chem 272(33):20884–20892. Scholar
  80. Lange S, Kauschke E, Mohrig W, Cooper EL (1999) Biochemical characteristics of Eiseniapore, a pore-forming protein in the coelomic fluid of earthworms. Eur J Biochem 262(2):547–556. Scholar
  81. Lassalle F, Lassegues M, Roch P (1988) Protein analysis of earthworm coelomic fluid - IV. Evidence, activity induction and purification of Eisenia fetida andrei lysozyme (Annelidae). Comp Biochem Physiol B 91:187–192. Scholar
  82. Lassegues M, Milochau A, Doignon F, Du Pasquier L, Valembois P (1997) Sequence and expression of an Eisenia fetida-derived cDNA clone that encodes the 40-kDa fetidin antibacterial protein. Eur J Biochem 246:756–762.
  83. Lee YR, Kim YN (1993) Selective transport of coelomic fluid protein into oocytes of a tubicolous polychaete, Pseudopotamilla occelata. Invert Reprod Develop 24(2):119–126. Scholar
  84. Lee BK, Nam HJ, Lee YR (1997) Receptor-mediated transport of vitellin during oogenesis of a polychaete, Pseudopotamilla ocelata. Kor J Biol Sci 1:341–344CrossRefGoogle Scholar
  85. Li W, Li S, Zhong J, Zhu Z, Liu J, Wang W (2011) A novel antimicrobial peptide from skin secretions of the earthworm Pheretima guillelmi (Michaelsen). Peptides 32:1146–1150. Scholar
  86. Li C, Chen M, Li X, Yang M, Wang Y, Yang X (2017) Purification and function of two analgesic and anti-inflammatory peptides from coelomic fluid of the earthworm, Eisenia foetida. Peptides 89:71–81. Scholar
  87. MacMahon BR, Wikens JL, Smith PJS (1997) Invertebrate circulatory systems. In: Dantzler WH (ed) Comparative Physiology. Oxford Univ. Press, New York, pp 931–1008Google Scholar
  88. Maltseva, AL, Kotenko, ON, Kokryakov, VN, Starunov, VV, Krasnodembskaya, AD (2014) Expression pattern of arenicins—the antimicrobial peptides of polychaete Arenicola marina. Front Physiol 5.
  89. Mangum CP, Woodin BR, Bonaventura C, Sullivan B, Bonaventura J (1975) Role of coelomic and vascular hemoglobin in annelid family terebellidae. Comp Biochem Phys A 51(2):281–294.
  90. Marcano L, Nusetti O, Rodriguez-Grau J, Briceño J, Vilas J (1997) Coelomic fluid lysozyme activity induction in the polychaete Eurythoe complanata as a biomarker of heavy metal toxicity. Bull Environ Contam Toxicol 59:22–28. Scholar
  91. Margoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79(17):4813–4814.
  92. Marusek CM, Trobaugh NM, Flurkey WH, Inlow JK (2006) Comparative analysis of polyphenol oxidase from plant and fungal species. J Inorg Biochem 100:108–123. Scholar
  93. Mazur AI, Klimek M, Morgan AJ, Plytycz B (2011) Riboflavin storage in earthworm chloragocytes and chloragocyte-derived eleocytes and its putative role as chemoattractant for immunocompetent cells. Pedobiologia 54:S37–S42. Scholar
  94. M'Beri M, Debray H, Dhainaut A (1988) Separation of two different populations of granulocytes of Nereis diversicolor (Annelida) by selective agglutination with lectins. Dev Comp Immunol 12(2):279–285. Scholar
  95. McKenzie HA, White FH Jr (1991) Lysozyme and α-lactalbumin: structure, function and interrelationships. Adv Prot Chem 41:173–315.
  96. McLaughlin J (1971) Biochemical studies on Eisenia foetida (Savigny, 1826), the brandling worm - I. Tissue lipids and sterols. Comp Biochem Physiol B 38:147–163. Scholar
  97. Milochau A, Lassègues M, Valembois P (1997) Purification, characterization and activities of two hemolytic and antibacterial proteins from coelomic fluid of the annelid Eisenia fetida andrei. Biochim Biophys Acta 1137:123–132. Scholar
  98. Minh B, Nguyen M, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195. Scholar
  99. Nagai T, Kawabata S (2000) A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J Biol Chem 275(38):29264–29267. Scholar
  100. Nejmeddine A, Dhainautcourtois N, Baert JL, Sautiere P, Fournet B, Boulenguer P (1988) Purification and characterization of a cadmium-binding protein from Nereis diversicolor (Annelida, Polychaeta). Comp Biochem Phys C 89(2):321–326.
  101. Nejmeddine A, Sautiere P, Dhainaut-Courtois N, Baert JL (1992) Isolation and characterization of a Cd-binding protein from Allolobophora caliginosa (Annelida, Oligochaeta): distinction from metallothioneins. Comp Biochem Physiol C 101(3):601–605. Scholar
  102. Nejmeddine A, Wouters-Tyrou D, Baert JL, Sautiere P (1997) Primary structure of a myohemerythrin-like cadmium-binding protein, isolated from a terrestrial annelid oligochaete. C R Acad Sci III 320(6):459–468CrossRefGoogle Scholar
  103. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. Scholar
  104. Nichol H, Law JH, Winzerling JJ (2002) Iron metabolism in insects. Annu Rev Entomol 47:535–559. Scholar
  105. Ohta N, Shioda S, Sekizawa Y, Nakai Y, Kobayashi H (2000) Sites of expression of mRNA for lysenin, a protein isolated from the coelomic fluid of the earthworm Eisenia foetida. Cell Tissue Res 302(2):263–270. Scholar
  106. Olivares Fontt E, Beschin A, van Dijck E, Vercruysse V, Bilej M, Lucas R, de Baetselier P, Vray B (2002) Trypanosoma cruzi is lysed by coelomic cytolytic factor-1, an invertebrate analogue of tumor necrosis factor, and induces phenoloxidase activity in the coelomic fluid of Eisenia foetida foetida. Dev Comp Immunol 26:27–34. Scholar
  107. Olsen I, Jantzen E (2001) Sphingolipids in bacteria and fungi. Anaerobe 7:103–112. Scholar
  108. Opper B, Bognar A, Heidt D, Nemeth P, Engelmann P (2013) Revising lysenin expression of earthworm coelomocytes. Dev Comp Immunol 39(3):214–218. Scholar
  109. Ovchinnikova, TV, Shenkarev, ZO, Nadezhdin, KD, Balandin, SV, Zhmak, MN, Kudelina, IA, Finkina, EI, Kokryakov, VN, Arseniev, AS (2007) Recombinant expression, synthesis, purification, and solution structure of arenicin. Biochem Biophys Res Com 360(1):156–162.
  110. Paiva-Silva GO, Cruz-Oliveira C, Nakayasu ES, Maya-Monteiro CM, Dunkov BC, Masuda H, Almeida IC, Oliveira PL (2006) A heme-degradation pathway in a blood-sucking insect. Proc Natl Acad Sci U S A 103(21):8030–8035. Scholar
  111. Pan, W, Liu, X, Ge, F, Han, J, Zheng, T (2004) Perinerin, a novel antimicrobial peptide purified from the clamworm Perinereis aibuhitensis Grube and its partial characterization. J Biochem 135(3):297–304.
  112. Pereira LOR, Oliveira PL, Almeida IC, Paiva-Silva GO (2007) Biglutaminyl-biliverdin IX alpha as a heme degradation product in the dengue fever insect-vector Aedes aegypti. Biochemistry 46(23):6822–6829.
  113. Périn J-P, Jollès P (1972) The lysozyme from Nephthys hombergi (Annelid). Biochim Biophys Acta 263:683–689. Scholar
  114. Plytycz B, Morgan AJ (2011) Riboflavin storage in earthworm chloragocytes/eleocytes in an eco-immunology perspective. Isj-Invert Surviv J 8(2):199–209Google Scholar
  115. Podobnik M, Savory P, Rojko N, Kisovec M, Wood N, Hambley R, Pugh J, Wallace EJ, McNeill L, Bruce M, Liko I, Allison TM, Mehmood S, Yilmaz N, Kobayashi T, Gilbert RJ, Robinson CV, Jayasinghe L, Anderluh G (2016) Crystal structure of an invertebrate cytolysin pore reveals unique properties and mechanism of assembly. Nat Commun 7:11598. Scholar
  116. Porchet-Henneré E (1990) Cooperation between different coelomocyte populations during encapsulation response of Nereis diversicolor demonstrated by using monoclonal antibodies. J Invert Pathol 56:353–361.
  117. Porchet-Henneré E, Nejmeddine A, Baert JL, Dhainaut-Courtois N (1987) Selective immunostaining of type-1 granulocytes of the polychaete annelid Nereis diversicolor by a monoclonal-antibody against acadmium-binding protein (Mp-II). Biol Cell 60(3):259–261Google Scholar
  118. Porchet-Hennere E, Vernet G (1992) Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes. Cell Tissue Res 269(1):167–174.
  119. Porchet-Hennere E, Dugimont T, Fischer A (1992) Natural killer cells in a lower invertebrate, Nereis diversicolor. Eur J Cell Biol 58(1):99–107PubMedGoogle Scholar
  120. Prochazkova P, Dvorak J, Silerova M, Roubalova R, Skanta F, Halada P, Bilej M (2011) Molecular characterization of the iron binding protein ferritin in Eisenia andrei earthworms. Gene 485(2):73–80. Scholar
  121. Racovitza E (1895) Sur le role des amibocytes chez les annélides polychètes. C R Acad Sci, Paris 120:464–467Google Scholar
  122. Ratcliffe NA, Rowley AF (1981a) Arthropods to urochordates. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 2. Academic Press, New YorkGoogle Scholar
  123. Ratcliffe NA, Rowley AF (1981b) General aspects. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New YorkGoogle Scholar
  124. Roch P, Ville P, Cooper EL (1998) Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coelomic fluid. Dev Comp Immunol 22(1):1–12. Scholar
  125. Roesijadi G, Fowler BA (1991) Purification of invertebrate metallothioneins. Meth Enzymol 205:263–273. Scholar
  126. Romieu M (1921) Sur les éléocytes de Perinereis cultrifera (Grube). C R Acad Sci Paris 173:246–249Google Scholar
  127. Ryan RO (1990) Dynamics of insect lipophorin metabolism. J Lipid Res 31:1725–1739PubMedGoogle Scholar
  128. Salzet-Raveillon B, Rentier-Delrue F, Dhainaut A (1993) Detection of mRNA encoding an antibacterial-metalloprotein (MPII) by in situ hybridization with a cDNA probe generated by polymerase chain reaction in the worm Nereis diversicolor. Cell Mol Biol (Noisy-le-grand) 39 (1):105–114Google Scholar
  129. Sánchez-Ferrer Á, Rodríguez-López JN, García-Cánovas F, García-Carmona F (1995) Tyrosinase: a comprehensive review of its mechanism. Biochim Biophys Acta 1247:1–11. Scholar
  130. Schenk S, Hoeger U (2009) Lipoprotein mediated lipid uptake in oocytes of polychaetes (Annelida). Cell Tiss Res 337(2):341–348. Scholar
  131. Schenk S, Hoeger U (2010) Lipid accumulation and metabolism in polychaete spermatogenesis: Role of the large discoidal lipoprotein. Mol Reprod Dev 77:710–719. Scholar
  132. Schenk S, Hoeger U (2011) Glutathionyl-biliverdin IXa, a new heme catabolite in a marine annelid: sex and cell specific accumulation. Biochimie 93(2):302–316CrossRefGoogle Scholar
  133. Schenk S, Harris JR, Hoeger U (2006) A discoidal lipoprotein from the coelomic fluid of the polychaete Nereis virens. Comp Biochem Physiol B 143(2):236–243. Scholar
  134. Schenk S, Krauditsch C, Fruhauf P, Gerner C, Raible F (2016) Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction. Elife 5.
  135. Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno ER, Salzet M, Tasiemski A (2008) Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol 181 (1083–1095).
  136. Schmidt O, Soderhall K, Theopold U, Faye I (2010) Role of adhesion in arthropod immune recognition. Ann Rev Entomol 55:485–504.
  137. Schüßler P, Potters E, Winnen R, Bottke W, Kunz W (1995) An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni. Mol Reprod Dev 41(3):325–330. Scholar
  138. Scott DM (1976) Circadian rhythm of anaerobiosis in a polychaete annelid. Nature 262:811–813. Scholar
  139. Sekizawa Y, Kubo T, Kobayashi H, Nakajima T, Natori S (1997) Molecular cloning of cDNA for lysenin, a novel protein in the earthworm Eisenia foetida that causes contraction of rat vascular smooth muscle. Gene 191(1):97–102. Scholar
  140. Seo J-K, Nam B-H, Go H-J, Jeong M, Lee K-Y, Cho S-M, Lee I-A, Park NG (2016) Hemerythrin-related antimicrobial peptide, msHemerycin, purified from the body of the lugworm, Marphysa sanguinea. Fish Shellfish Immunol 57:49–59.
  141. Shakor AB, Czurylo EA, Sobota A (2003) Lysenin, a unique sphingomyelin-binding protein. FEBS Lett 542(1–3):1–6. Scholar
  142. Silerova M, Prochazkova P, Joskova R, Josens G, Beschin A, De Baetselier P, Bilej M (2006) Comparative study of the CCF-like pattern recognition protein in different Lumbricid species. Dev Comp Immunol 30(9):765–771. Scholar
  143. Smith VJ, Söderhäll K (1991) A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev Comp Immunol 15:251–261. Scholar
  144. Smolenaars MMW, De Morreé A, Kerver J, Van der Horst DJ, Rodenburg KW (2007a) Insect lipoprotein biogenesis depends on an amphipatic ß cluster in apolipophorin II/I and is stimulated by microsomal triglyceride transfer protein. J Lipid Res 48:1955–1965. Scholar
  145. Smolenaars MMW, Madsen O, Rodenburg KW, Van der Horst DJ (2007b) Molecular diversity of the large lipid transfer protein superfamily. J Lipid Res 48:489–502. Scholar
  146. Soderhall K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10(1):23–28. Scholar
  147. Spaziani E, Havel RJ, Hamilton RL, Hardman DA, Stoudemire JB, Watson RD (1986) Properties of serum high-density lipoproteins in the crab, Cancer antennarius Stimpson. Comp Biochem Physiol B 85(2):307–314. Scholar
  148. Stürzenbaum SR, Kille P, Morgan AJ (1998) The identification, cloning and characterization of earthworm metallothionein. FEBS Lett 431(3):437–442. Scholar
  149. Stürzenbaum SR, Winters C, Galay M, Morgan AJ, Kille P (2001) Metal ion trafficking in earthworms. Identification of a cadmium-specific metallothionein. J Biol Chem 276 (36):34013–34018. 10.1074/jbc.M103605200Google Scholar
  150. Sturzenbaum SR, Georgiev O, Morgan AJ, Kille P (2004) Cadmium detoxification in earthworms: from genes to cells. Environ Sci Technol 38(23):6283–6289. Scholar
  151. Swiderska B, Kedracka-Krok S, Panz T, Morgan AJ, Falniowski A, Grzmil P, Plytycz B (2017) Lysenin family proteins in earthworm coelomocytes - Comparative approach. Dev Comp Immunol 67:404–412. Scholar
  152. Taki H, Baert JL, Dhainaut A (1989) Synthesis and release of vitellogenin-associated phospholipids by the coelomocytes of Perinereis cultifera (Annelida, Polychaeta). Comp Biochem Physiol B 92(1):167–173. Scholar
  153. Tasiemski A, Vandenbulcke F, Mitta G, Lemoine J, Lefebvre C, Sautiere PE, Salzet M (2004) Molecular characterization of two novel antibacterial peptides inducible upon bacterial challenge in an annelid, the leech Theromyzon tessulatum. J Biol Chem 279(30):30973–30982.
  154. Telfer WH, Pan M-L, Law JH (1991) Lipophorin in developing adults of Hyalophora cecropia: support of yolk formation and preparation for flight. Insect Biochem Mol Biol 21(-):653–663Google Scholar
  155. Tučková L, Rejnek J, Šíma P, Ondřejová R (1986) Lytic activities in coelomic fluid of Eisenia foetida and Lumbricus terrestris. Dev Comp Immunol 10(2):181–189.
  156. Vaillier J, Cadoret MA, Roch P, Valembois P (1985) Protein analysis of earthworm coelomic fluid. III. Isolation and characterization of several bacteriostatic molecules from Eisenia fetida andrei. Dev Comp Immunol 9(1):11–20.–305x(85)90055–2
  157. Valembois P, Roch P, Lassegues M, Davant N (1982) Bacteriostatic activity of a chloragogen cell secretion. Pedobiologia 24(4):191–195Google Scholar
  158. Valembois P, Seymour J, Roch P (1991) Evidence and cellular localization of an oxidase activity in the coelomic fluid of the earthworm Eisenia fetida andrei. J Invertebr Pathol 57:177–183CrossRefGoogle Scholar
  159. Vetvicka V, Sima P (2009) Origins and functions of annelide immune cells: the concise survey. Isj-Invert Surviv J 6(2):138–143Google Scholar
  160. Wang X, Wang X, Zhang Y, Qu X, Yang S (2003) An antimicrobial peptide of the earthworm Pheretima tschiliensis: cDNA cloning, expression and immunolocalization. Biotechnol Lett 25:1317–1323CrossRefGoogle Scholar
  161. Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81(2):569–628.
  162. Weers PM, Van Marrewijk WJ, Beenakkers AM, Van der Horst DJ (1993) Biosynthesis of locust lipophorin. Apolipophorins I and II originate from a common precursor. J Biol Chem 268 (6):4300–4303Google Scholar
  163. Westheide W (2013) Spezielle Zoologie, vol 1. Einzeller und wirbellose Tiere, 3rd edn. Springer-Spektrum, BerlinGoogle Scholar
  164. Won EJ, Rhee JS, Ra K, Kim KT, Au DW, Shin KH, Lee JS (2011) Molecular cloning and expression of novel metallothionein (MT) gene in the polychaete Perinereis nuntia exposed to metals. Environ Sci Pollut Res Int 19(7):2606–2618.
  165. Yamaji A, Sekizawa Y, Emoto K, Sakuraba H, Inoue K, Kobayashi H, Umeda M (1998) Lysenin, a novel sphingomyelin-specific binding protein. J Biol Chem 273(9):5300–5306. Scholar
  166. Zhang Y, Cui J, Zhang R, Wang Y, Hong M (2007) A novel fibrinolytic serine protease from the polychaete Nereis (Neanthes) virens (Sars): purification and characterization. Biochimie 89(1):93–103. Scholar
  167. Zhang L, Cui W, Chen Q, Ren Q, Zhu Y, Zhang Y (2020) Thymosin-beta12 characteristics and function in Urechis unicinctus. Comp Biochem Physiol B 239:110366.

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Authors and Affiliations

  1. 1.Max F. Perutz LaboratoriesVienna Biocenter (VBC)ViennaAustria
  2. 2.Institut für Molekulare PhysiologieJohannes Gutenberg-UniversitätMainzGermany

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