Cephalochordata: Branchiostoma

  • Zhan Gao
  • Shicui ZhangEmail author


The cephalochordate amphioxus, a basal chordate discovered by Pallas in 1774, is the best available stand-in for the proximate invertebrate ancestor of vertebrates. It has a vertebrate-like body plan, including a notochord, a hollow dorsal neural tube, a post-anal tail, segmented muscle blocks, gill slits, and posterior direction of blood flow in the dorsal vessels and anterior direction of blood flow in the ventral vessels (Kowalevsky 1867; Rähr 1979). However, this animal is much less complex than vertebrates as it has a genome (17% that of the human genome) uncomplicated by extensive genomic duplication (Gibson-Brown et al. 2003; Putnam et al. 2008) and lacks lymphoid organs and free circulating blood cells (Gans et al. 1996; Metchnikoff 1891; Möller and Philpott 1973a, b; Silva et al. 1995). Thus, amphioxus is an ideal model for gaining insights into the origin and evolution of the immune system in vertebrates. Over the past decade, great progress has been made in the study of amphioxus immunity. In this chapter we focus on the recent progress of immunity study in amphioxus.



During the writing of this chapter, the authors were supported by grants (U1401211; 31601862) from the Natural Science Foundation of China, and by the Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, China.


  1. Abe Y, Tokuda M, Ishimoto R, Azumi K, Yokosawa H (1999) A unique primary structure, cDNA cloning and function of a galactose-specific lectin from ascidian plasma. Eur J Biochem/FEBS 261(1):33–39CrossRefGoogle Scholar
  2. Abi-Rached L, Gilles A, Shiina T, Pontarotti P, Inoko H (2002) Evidence of en bloc duplication in vertebrate genomes. Nat Genet 31(1):100–105. CrossRefPubMedGoogle Scholar
  3. An Y, Fan N, Zhang S (2009) Creatine kinase is a bacteriostatic factor with a lectin-like activity. Mol Immunol 46(13):2666–2670. CrossRefPubMedGoogle Scholar
  4. Arakane Y, Muthukrishnan S (2010) Insect chitinase and chitinase-like proteins. Cell Mol Life Sci 67(2):201–216. CrossRefPubMedGoogle Scholar
  5. Bajoghli B, Aghaallaei N, Hess I, Rode I, Netuschil N, Tay BH, Venkatesh B, Yu JK, Kaltenbach SL, Holland ND, Diekhoff D, Happe C, Schorpp M, Boehm T (2009) Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 138(1):186–197. CrossRefPubMedGoogle Scholar
  6. Bertrand S, Campo-Paysaa F, Camasses A, Garcia-Fernandez J, Escriva H (2009) Actors of the tyrosine kinase receptor downstream signaling pathways in amphioxus. Evol Dev 11(1):13–26. CrossRefPubMedGoogle Scholar
  7. Beutler B, Eidenschenk C, Crozat K, Imler JL, Takeuchi O, Hoffmann JA, Akira S (2007) Genetic analysis of resistance to viral infection. Nat Rev Immunol 7(10):753–766. CrossRefPubMedGoogle Scholar
  8. Bidon N, Brichory F, Bourguet P, Le Pennec JP, Dazord L (2001) Galectin-8: a complex sub-family of galectins (review). Int J Mol Med 8(3):245–250PubMedGoogle Scholar
  9. Bloom BR, Bennett B (1966) Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153(3731):80–82CrossRefGoogle Scholar
  10. Boehm T, Hess I, Swann JB (2012) Evolution of lymphoid tissues. Trends Immunol 33(6):315–321. CrossRefPubMedGoogle Scholar
  11. Cai L, Zhu J, Yin D, Chen L, Jin P, Ma F (2014) Identification and characterization of complement factor H in Branchiostoma belcheri. Gene 553(1):42–48. CrossRefPubMedGoogle Scholar
  12. Callewaert L, Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci 35(1):127–160CrossRefGoogle Scholar
  13. Cannon JP, Haire RN, Litman GW (2002) Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol 3(12):1200–1207. CrossRefPubMedGoogle Scholar
  14. Cannon JP, Haire RN, Schnitker N, Mueller MG, Litman GW (2004) Individual protochordates have unique immune-type receptor repertoires. Curr Biol CB 14(12):R465–R466. CrossRefPubMedGoogle Scholar
  15. Cao DD, Liao X, Cheng W, Jiang YL, Wang WJ, Li Q, Chen JY, Chen Y, Zhou CZ (2016) Structure of a variable lymphocyte receptor-like protein from the amphioxus Branchiostoma floridae. Sci Rep 6:19951. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Clow LA, Raftos DA, Gross PS, Smith LC (2004) The sea urchin complement homologue, SpC3, functions as an opsonin. J Exp Biol 207(Pt 12):2147–2155CrossRefGoogle Scholar
  17. Collette Y, Gilles A, Pontarotti P, Olive D (2003) A co-evolution perspective of the TNFSF and TNFRSF families in the immune system. Trends Immunol 24(7):387–394CrossRefGoogle Scholar
  18. Cummings RD, Liu FT (2009) Galectins. In: Varki A, Cummings RD, Esko JD et al (eds) Essentials of glycobiology, 2nd edn, Cold Spring Harbor, New YorkGoogle Scholar
  19. Datta R, deSchoolmeester ML, Hedeler C, Paton NW, Brass AM, Else KJ (2005) Identification of novel genes in intestinal tissue that are regulated after infection with an intestinal nematode parasite. Infect Immun 73(7):4025–4033. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dheilly NM, Haynes PA, Bove U, Nair SV, Raftos DA (2011) 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. CrossRefPubMedGoogle Scholar
  21. Dishaw LJ, Giacomelli S, Melillo D, Zucchetti I, Haire RN, Natale L, Russo NA, De Santis R, Litman GW, Pinto MR (2011) A role for variable region-containing chitin-binding proteins (VCBPs) in host gut-bacteria interactions. Proc Natl Acad Sci U S A 108(40):16747–16752. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dishaw LJ, Leigh B, Cannon JP, Liberti A, Mueller MG, Skapura DP, Karrer CR, Pinto MR, De Santis R, Litman GW (2016) Gut immunity in a protochordate involves a secreted immunoglobulin-type mediator binding host chitin and bacteria. Nat Commun 7:10617. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dodd RB, Drickamer K (2001) Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11(5):71R–79RCrossRefGoogle Scholar
  24. Du J, Xie X, Chen H, Yang W, Dong M, Su J, Wang Y, Yu C, Zhang S, Xu A (2004) Macrophage migration inhibitory factor (MIF) in Chinese amphioxus as a molecular marker of immune evolution during the transition of invertebrate/vertebrate. Dev Comp Immunol 28(10):961–971. CrossRefPubMedGoogle Scholar
  25. Du J, Yu Y, Tu H, Chen H, Xie X, Mou C, Feng K, Zhang S, Xu A (2006) New insights on macrophage migration inhibitory factor: based on molecular and functional analysis of its homologue of Chinese amphioxus. Mol Immunol 43(13):2083–2088. CrossRefPubMedGoogle Scholar
  26. Dziarski R, Gupta D (2006) The peptidoglycan recognition proteins (PGRPs). Genome Biol 7(8):232. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Dziarski R, Gupta D (2010) Review: mammalian peptidoglycan recognition proteins (PGRPs) in innate immunity. Innate Immun 16(3):168–174. CrossRefPubMedGoogle Scholar
  28. Elkin SK, Matthews AG, Oettinger MA (2003) The C-terminal portion of RAG2 protects against transposition in vitro. EMBO J 22(8):1931–1938. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Elsbach P (1998) The bactericidal/permeability-increasing protein (BPI) in antibacterial host defense. J Leukoc Biol 64(1):14–18CrossRefGoogle Scholar
  30. Endo Y, Nonaka M, Saiga H, Kakinuma Y, Matsushita A, Takahashi M, Matsushita M, Fujita T (2003) Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, amphioxus. J Immunol 170(9):4701–4707CrossRefGoogle Scholar
  31. Forman HJ, Torres M (2002) Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med 166(12 Pt 2):S4–S8. CrossRefPubMedGoogle Scholar
  32. French AT, Knight PA, Smith WD, Brown JK, Craig NM, Pate JA, Miller HR, Pemberton AD (2008) Up-regulation of intelectin in sheep after infection with Teladorsagia circumcincta. Int J Parasitol 38(3–4):467–475. CrossRefPubMedGoogle Scholar
  33. Gans C, Kemp N, Poss S (1996) The lancelets: a new look at some old beasts. Weizmann, Isr J Zool 42:1–446Google Scholar
  34. Gao B, Jeong WI, Tian Z (2008) Liver: an organ with predominant innate immunity. Hepatology 47(2):729–736. CrossRefPubMedGoogle Scholar
  35. Gao Z, Li M, Wu J, Zhang S (2013) Interplay between invertebrate C3a with vertebrate macrophages: functional characterization of immune activities of amphioxus C3a. Fish Shellfish Immunol 35(4):1249–1259. CrossRefPubMedGoogle Scholar
  36. 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(12):3680–3695. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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. CrossRefPubMedGoogle Scholar
  38. Gibson-Brown JJ, Osoegawa K, McPherson JD, Waterston RH, De Jong PJ, Rokhsar DS, Holland LZ (2003) A proposal to sequence the amphioxus genome submitted to the joint genome institute of the US Department of energy. J Exp Zool B Mol Dev Evol 300(1):5–22CrossRefGoogle Scholar
  39. Grech A, Quinn R, Srinivasan D, Badoux X, Brink R (2000) Complete structural characterisation of the mammalian and Drosophila TRAF genes: implications for TRAF evolution and the role of RING finger splice variants. Mol Immunol 37(12–13):721–734CrossRefGoogle Scholar
  40. Guo P, Hirano M, Herrin BR, Li J, Yu C, Sadlonova A, Cooper MD (2009) Dual nature of the adaptive immune system in lampreys. Nature 459(7248):796–801. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Guo X, Xin J, Wang P, Du X, Ji G, Gao Z, Zhang S (2017) Functional characterization of avidins in amphioxus Branchiostoma japonicum: evidence for a dual role in biotin-binding and immune response. Dev Comp Immunol 70:106–118. CrossRefPubMedGoogle Scholar
  42. Han L, Zhang SC, Wang YJ, Sun XT (2006) Immunohistochemical localization of vitellogenin in the hepatic diverticulum of the amphioxus Branchiostoma belcheri tsingtauense, with implications for the origin of the liver. Invertebr Biol 125(2):172–176. CrossRefGoogle Scholar
  43. Han Y, Huang G, Zhang Q, Yuan S, Liu J, Zheng T, Fan L, Chen S, Xu A (2010) The primitive immune system of amphioxus provides insights into the ancestral structure of the vertebrate immune system. Dev Comp Immunol 34(8):791–796. CrossRefPubMedGoogle Scholar
  44. Hancock RE, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24(12):1551–1557. CrossRefPubMedGoogle Scholar
  45. Hansen SW, Ohtani K, Roy N, Wakamiya N (2016) The collectins CL-L1, CL-K1 and CL-P1, and their roles in complement and innate immunity. Immunobiology 221(10):1058–1067. CrossRefPubMedGoogle Scholar
  46. He Y, Tang 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: implications for involvement of hepatic cecum in acute phase response. Fish Shellfish Immunol 24(6):768–778. CrossRefPubMedGoogle Scholar
  47. Hehlgans T, Pfeffer K (2005) The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 115(1):1–20. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Helbig KJ, Beard MR (2014) The role of viperin in the innate antiviral response. J Mol Biol 426(6):1210–1219. CrossRefPubMedGoogle Scholar
  49. Hernandez Prada JA, Haire RN, Cannon JP, Litman GW, Ostrov DA (2004) Crystallization and preliminary X-ray analysis of VCBP3 from Branchiostoma floridae. Acta Crystallogr D Biol Crystallogr 60(Pt 11):2022–2024. CrossRefPubMedGoogle Scholar
  50. Hernandez Prada JA, Haire RN, Allaire M, Jakoncic J, Stojanoff V, Cannon JP, Litman GW, Ostrov DA (2006) Ancient evolutionary origin of diversified variable regions demonstrated by crystal structures of an immune-type receptor in amphioxus. Nat Immunol 7(8):875–882. CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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(1):349–365. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Houzelstein D, Goncalves IR, Fadden AJ, Sidhu SS, Cooper DN, Drickamer K, Leffler H, Poirier F (2004) Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol 21(7):1177–1187. CrossRefPubMedGoogle Scholar
  53. Huang G, Xie X, Han Y, Fan L, Chen J, Mou C, Guo L, Liu H, Zhang Q, Chen S, Dong M, Liu J, Xu A (2007) The identification of lymphocyte-like cells and lymphoid-related genes in amphioxus indicates the twilight for the emergence of adaptive immune system. PLoS One 2(2):e206. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Huang S, Yuan S, Guo L, Yu Y, Li J, Wu T, Liu T, Yang M, Wu K, Liu H, Ge J, Huang H, Dong M, Yu C, Chen S, Xu A (2008) Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Res 18(7):1112–1126. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Huang H, Huang S, Yu Y, Yuan S, Li R, Wang X, Zhao H, Li J, Yang M, Xu L, Chen S, Xu A (2011a) Functional characterization of a ficolin-mediated complement pathway in amphioxus. J Biol Chem 286(42):36739–36748. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Huang S, Wang X, Yan Q, Guo L, Yuan S, Huang G, Huang H, Li J, Dong M, Chen S, Xu A (2011b) The evolution and regulation of the mucosal immune complexity in the basal chordate amphioxus. J Immunol 186(4):2042–2055. CrossRefPubMedGoogle Scholar
  57. 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 U S A 111(37):13469–13474. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Huang S, Tao X, Yuan S, Zhang Y, Li P, Beilinson HA, 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(1):102–114. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Jin P, Zhou L, Song X, Qian J, Chen L, Ma F (2012) Particularity and universality of a putative gram-negative bacteria-binding protein (GNBP) gene from amphioxus (Branchiostoma belcheri): insights into the function and evolution of GNBP. Fish Shellfish Immunol 33(4):835–845. CrossRefPubMedGoogle Scholar
  60. Jing X, Zhang S (2011) An ancient molecule with novel function: alanine aminotransferase as a lipopolysaccharide binding protein with bacteriocidal activity. Dev Comp Immunol 35(1):94–104. CrossRefPubMedGoogle Scholar
  61. Juretic D, Vukicevic D, Petrov D, Novkovic M, Bojovic V, Lucic B, Ilic N, Tossi A (2011) Knowledge-based computational methods for identifying or designing novel, non-homologous antimicrobial peptides. Eur Biophys J EBJ 40(4):371–385. CrossRefPubMedGoogle Scholar
  62. Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3(6):e181. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Kasahara M, Nakaya J, Satta Y, Takahata N (1997) Chromosomal duplication and the emergence of the adaptive immune system. Trends Genet 13(3):90–92CrossRefGoogle Scholar
  64. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6(10):981–988. CrossRefPubMedGoogle Scholar
  65. Kemper C, Atkinson JP, Hourcade DE (2010) Properdin: emerging roles of a pattern-recognition molecule. Annu Rev Immunol 28:131–155. CrossRefPubMedGoogle Scholar
  66. Kirschning CJ, Au-Young J, Lamping N, Reuter D, Pfeil D, Seilhamer JJ, Schumann RR (1997) Similar organization of the lipopolysaccharide-binding protein (LBP) and phospholipid transfer protein (PLTP) genes suggests a common gene family of lipid-binding proteins. Genomics 46(3):416–425. CrossRefPubMedGoogle Scholar
  67. Klebanoff SJ (2005) Myeloperoxidase: friend and foe. J Leukoc Biol 77(5):598–625. CrossRefPubMedGoogle Scholar
  68. Kopp EB, Medzhitov R (1999) The toll-receptor family and control of innate immunity. Curr Opin Immunol 11(1):13–18CrossRefGoogle Scholar
  69. Kowalevsky AO (1867) Entwickelungsgeschichte des Amphioxus lanceolatus. Me’m Acad Imp Sci St Petersb 11:1–17Google Scholar
  70. Lee CG (2009) Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med J 50(1):22–30. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lei M, Liu H, Liu S, Zhang Y, Zhang S (2015) Identification and functional characterization of viperin of amphioxus Branchiostoma japonicum: implications for ancient origin of viperin-mediated antiviral response. Dev Comp Immunol 53(2):293–302. CrossRefPubMedGoogle Scholar
  72. Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743. CrossRefPubMedGoogle Scholar
  73. Leto TL, Geiszt M (2006) Role of Nox family NADPH oxidases in host defense. Antioxid Redox Signal 8(9–10):1549–1561. CrossRefPubMedGoogle Scholar
  74. Li HY, Zhang SC (2010) Hepatic caecum of amphioxus and origin of vertebrate liver. Yi Chuan Hereditas/Zhongguo yi chuan xue hui bian ji 32(5):437–442CrossRefGoogle Scholar
  75. Li Z, Zhang S, Wang C, Pang Q (2008) Complement-mediated killing of Vibrio species by the humoral fluids of amphioxus Branchiostoma belcheri: implications for a dual role of O-antigens in the resistance to bactericidal activity. Fish Shellfish Immunol 24(2):215–222. CrossRefPubMedGoogle Scholar
  76. Li J, Yuan S, Qi L, Huang S, Huang G, Yang M, Xu L, Li Y, Zhang R, Yu Y, Chen S, Xu A (2011) Functional conservation and innovation of amphioxus RIP1-mediated signaling in cell fate determination. J Immunol 187(8):3962–3971. CrossRefPubMedGoogle Scholar
  77. Liang Y, Zhang S, Wang Z (2009) Alternative complement activity in the egg cytosol of amphioxus Branchiostoma belcheri: evidence for the defense role of maternal complement components. PLoS One 4(1):e4234. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Lin B, Cao Z, Su P, Zhang H, Li M, Lin Y, Zhao D, Shen Y, Jing C, Chen S, Xu A (2009) Characterization and comparative analyses of zebrafish intelectins: highly conserved sequences, diversified structures and functions. Fish Shellfish Immunol 26(3):396–405. CrossRefPubMedGoogle Scholar
  79. Litman GW, Dishaw LJ, Cannon JP, Haire RN, Rast JP (2007) Alternative mechanisms of immune receptor diversity. Curr Opin Immunol 19(5):526–534. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Liu M, Zhang S, Liu Z, Li H, Xu A (2006) Characterization, organization and expression of AmphiLysC, an acidic c-type lysozyme gene in amphioxus Branchiostoma belcheri tsingtauense. Gene 367:110–117. CrossRefPubMedGoogle Scholar
  81. Liu N, Zhang S, Liu Z, Gaowa S, Wang Y (2007) Characterization and expression of gamma-interferon-inducible lysosomal thiol reductase (GILT) gene in amphioxus Branchiostoma belcheri with implications for GILT in innate immune response. Mol Immunol 44(10):2631–2637. CrossRefGoogle Scholar
  82. Liu J, Zhang S, Li L (2009) A transferrin-like homolog in amphioxus Branchiostoma belcheri: identification, expression and functional characterization. Mol Immunol 46(15):3117–3124. CrossRefPubMedGoogle Scholar
  83. Liu X, Xu N, Zhang S (2013) Calreticulin is a microbial-binding molecule with phagocytosis-enhancing capacity. Fish Shellfish Immunol 35(3):776–784. CrossRefGoogle Scholar
  84. Liu H, Lei M, Du X, Cui P, Zhang S (2015a) Identification of a novel antimicrobial peptide from amphioxus Branchiostoma japonicum by in silico and functional analyses. Sci Rep 5:18355. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Liu S, Liu Y, Yang S, Huang Y, Qin Q, Zhang S (2015b) Evolutionary conservation of molecular structure and antiviral function of a viral receptor, LGP2, in amphioxus Branchiostoma japonicum. Eur J Immunol 45(12):3404–3416. CrossRefPubMedGoogle Scholar
  86. Markiewski MM, DeAngelis RA, Lambris JD (2006) Liver inflammation and regeneration: two distinct biological phenomena or parallel pathophysiologic processes? Mol Immunol 43(1-2):45–56. CrossRefGoogle Scholar
  87. Matsushita M, Matsushita A, Endo Y, Nakata M, Kojima N, Mizuochi T, Fujita T (2004) Origin of the classical complement pathway: lamprey orthologue of mammalian C1q acts as a lectin. Proc Natl Acad Sci U S A 101(27):10127–10131. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Mayer WE, Uinuk-Ool T, Tichy H, Gartland LA, Klein J, Cooper MD (2002) Isolation and characterization of lymphocyte-like cells from a lamprey. Proc Natl Acad Sci U S A 99(22):14350–14355. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Metchnikoff E (1891) Lectures on the comparative pathology of inflammation. Dover Publications, New YorkGoogle Scholar
  90. Micheau O, Tschopp J (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114(2):181–190CrossRefGoogle Scholar
  91. Möller PC, Philpott CW (1973a) The circulatory system of amphioxus (Branchiostoma floridae). II. Uptake of exogenous proteins by endothelial cells. Z Zellforsch Mikrosk Anat 143(1):135–141CrossRefGoogle Scholar
  92. Möller PC, Philpott CW (1973b) The circulatory system of amphioxus (Branchiostoma floridae). I. Morphology of the major vessels of the pharyngeal area. J Morphol 139:389–406CrossRefGoogle Scholar
  93. Morgan BP, Gasque P (1997) Extrahepatic complement biosynthesis: where, when and why? Clin Exp Immunol 107(1):1–7CrossRefGoogle Scholar
  94. Motta V, Soares F, Sun T, Philpott DJ (2015) NOD-like receptors: versatile cytosolic sentinels. Physiol Rev 95(1):149–178. CrossRefPubMedGoogle Scholar
  95. Müller J (1844) Über den Bau und die Lebenserscheinungen des Branchiostoma lubricum Costa, Amphioxus lanceolatus Yarrell. Druckerei der Königliche Akademie der Wissenschaften zu Berlin, pp 186–204Google Scholar
  96. Mussabekova A, Daeffler L, Imler JL (2017) Innate and intrinsic antiviral immunity in Drosophila. Cell Mol Life Sci. CrossRefGoogle Scholar
  97. Nonaka M, Kimura A (2006) Genomic view of the evolution of the complement system. Immunogenetics 58(9):701–713. CrossRefPubMedPubMedCentralGoogle Scholar
  98. Nonaka M, Namikawa C, Kato Y, Sasaki M, Salter-Cid L, Flajnik MF (1997) Major histocompatibility complex gene mapping in the amphibian Xenopus implies a primordial organization. Proc Natl Acad Sci U S A 94(11):5789–5791CrossRefGoogle Scholar
  99. Nonaka M, Azumi K, Ji X, Namikawa-Yamada C, Sasaki M, Saiga H, Dodds AW, Sekine H, Homma MK, Matsushita M, Endo Y, Fujita T (1999) Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. J Immunol 162(1):387–391PubMedGoogle Scholar
  100. Pan J, Liu M, Zhang S (2011) Interplay between amphioxus complement with fish macrophages: evidence for vertebrate-like alternative complement activation in the protochordate. J Ocean Univ China 10(4):357–361CrossRefGoogle Scholar
  101. Park Y, Hahm KS (2005) Antimicrobial peptides (AMPs): peptide structure and mode of action. J Biochem Mol Biol 38(5):507–516PubMedGoogle Scholar
  102. Peng J, Tao X, Li R, Hu J, Ruan J, Wang R, Yang M, Yang R, Dong X, Chen S, Xu A, Yuan S (2015) Novel toll/IL-1 receptor homologous region adaptors act as negative regulators in Amphioxus TLR signaling. J Immunol 195(7):3110–3118. CrossRefPubMedGoogle Scholar
  103. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453(7198):1064–1071. CrossRefPubMedGoogle Scholar
  104. Qu B, Yang S, Ma Z, Gao Z, Zhang S (2016) A new LDLa domain-containing C-type lectin with bacterial agglutinating and binding activity in amphioxus. Gene 594(2):220–228. CrossRefPubMedGoogle Scholar
  105. Rabinovitch M (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol 5(3):85–87CrossRefGoogle Scholar
  106. Racanelli V, Rehermann B (2006) The liver as an immunological organ. Hepatology 43:S54–62. CrossRefGoogle Scholar
  107. Rada B, Leto TL (2008) Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib Microbiol 15:164–187. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Rähr (1979) The circulatory system of Amphioxus (Branchiostoma lanceolatum (Pallas)) : a light-microscopic investigation based on intravascular injection technique. Acta Zool 60(1):1–18CrossRefGoogle Scholar
  109. Rhodes CP, Ratcliffe NA, Rowley AF (1982) Presence of coelomocytes in the primitive chordate amphioxus (Branchiostoma lanceolatum). Science 217(4556):263–265CrossRefGoogle Scholar
  110. Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, Hood LE, Aderem A (2005) The evolution of vertebrate toll-like receptors. Proc Natl Acad Sci U S A 102(27):9577–9582. CrossRefPubMedPubMedCentralGoogle Scholar
  111. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, McClay DR, Coffman JA (2006) The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev Biol 300(1):321–334. CrossRefPubMedGoogle Scholar
  112. Rowley AF (1982) Ultrastructural and cytochemical studies on the blood cells of the sea squirt, Ciona intestinalis. I. Stem cells and amoebocytes. Cell Tissue Res 223(2):403–414CrossRefGoogle Scholar
  113. Royet J, Dziarski R (2007) Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5(4):264–277. CrossRefPubMedGoogle Scholar
  114. Russell S, Young KM, Smith M, Hayes MA, Lumsden JS (2008) Identification, cloning and tissue localization of a rainbow trout (Oncorhynchus mykiss) intelectin-like protein that binds bacteria and chitin. Fish Shellfish Immunol 25(1–2):91–105. CrossRefPubMedGoogle Scholar
  115. Saleh M (2011) The machinery of nod-like receptors: refining the paths to immunity and cell death. Immunol Rev 243(1):235–246. CrossRefPubMedGoogle Scholar
  116. Satoh T, Kato H, Kumagai Y, Yoneyama M, Sato S, Matsushita K, Tsujimura T, Fujita T, Akira S, Takeuchi O (2010) LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci U S A 107(4):1512–1517. CrossRefPubMedPubMedCentralGoogle Scholar
  117. Sekine H, Kenjo A, Azumi K, Ohi G, Takahashi M, Kasukawa R, Ichikawa N, Nakata M, Mizuochi T, Matsushita M, Endo Y, Fujita T (2001) An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 167(8):4504–4510CrossRefGoogle Scholar
  118. Seth RB, Sun L, Ea CK, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122(5):669–682. CrossRefPubMedGoogle Scholar
  119. Shoji H, Nishi N, Hirashima M, Nakamura T (2003) Characterization of the Xenopus galectin family. Three structurally different types as in mammals and regulated expression during embryogenesis. J Biol Chem 278(14):12285–12293. CrossRefPubMedGoogle Scholar
  120. Silva JR, Mendes EG, Mariano M (1995) Wound repair in the Amphioxus (Branchiostoma platae), an animal deprived of inflammatory phagocytes. J Invertebr Pathol 65(2):147–151. CrossRefPubMedGoogle Scholar
  121. Song X, Jin P, Hu J, Qin S, Chen L, Li-Ling J, Ma F (2012) Involvement of AmphiREL, a Rel-like gene identified in Brachiastoma belcheri, in LPS-induced response: implication for evolution of Rel subfamily genes. Genomics 99(6):361–369. CrossRefPubMedGoogle Scholar
  122. Sparkes A, De Baetselier P, Roelants K, De Trez C, Magez S, Van Ginderachter JA, Raes G, Bucala R, Stijlemans B (2017) The non-mammalian MIF superfamily. Immunobiology 222(3):473–482. CrossRefPubMedGoogle Scholar
  123. 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(5):671–679. CrossRefPubMedGoogle Scholar
  124. Takaoka A, Taniguchi T (2008) Cytosolic DNA recognition for triggering innate immune responses. Adv Drug Deliv Rev 60(7):847–857. CrossRefPubMedGoogle Scholar
  125. Teng L, Gao B, Zhang S (2012) The first chordate big defensin: identification, expression and bioactivity. Fish Shellfish Immunol 32(4):572–577. CrossRefPubMedGoogle Scholar
  126. Tessera V, Guida F, Juretic D, Tossi A (2012) Identification of antimicrobial peptides from teleosts and anurans in expressed sequence tag databases using conserved signal sequences. FEBS J 279(5):724–736. CrossRefPubMedGoogle Scholar
  127. Van Herreweghe JM, Michiels CW (2012) Invertebrate lysozymes: diversity and distribution, molecular mechanism and in vivo function. J Biosci 37(2):327–348CrossRefGoogle Scholar
  128. Wang Y, Zhang S (2011) Identification and expression of liver-specific genes after LPS challenge in amphioxus: the hepatic cecum as liver-like organ and "pre-hepatic" acute phase response. Funct Integr Genomics 11(1):111–118. CrossRefPubMedGoogle Scholar
  129. Wang WJ, Cheng W, Luo M, Yan Q, Yu HM, Li Q, Cao DD, Huang S, Xu A, Mariuzza RA, Chen Y, Zhou CZ (2015) Activity augmentation of Amphioxus peptidoglycan recognition protein BbtPGRP3 via fusion with a chitin binding domain. PLoS One 10(10):e0140953. CrossRefPubMedPubMedCentralGoogle Scholar
  130. Weitman E, Cuzzone D, Mehrara BJ (2013) Tissue engineering and regeneration of lymphatic structures. Future Oncol 9(9):1365–1374. CrossRefPubMedPubMedCentralGoogle Scholar
  131. Welsch U (1975) The fine structure of the pharynx, cryptopodocytes and digestive caecum of amphioxus (Branchiostoma lanceolatum). Symp Zool Soc Lond 36:17–41Google Scholar
  132. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC (1990) CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249(4975):1431–1433CrossRefGoogle Scholar
  133. Wu F, Chen L, Liu X, Wang H, Su P, Han Y, Feng B, Qiao X, Zhao J, Ma N, Liu H, Zheng Z, Li Q (2013) Lamprey variable lymphocyte receptors mediate complement-dependent cytotoxicity. J Immunol 190(3):922–930. CrossRefPubMedGoogle Scholar
  134. Xu AL (2011) Amphioxus immunity: tracing the origins of human immunity. Science Press, BeijingGoogle Scholar
  135. Xu N, Zhang S (2012) Identification, expression and bioactivity of a chitotriosidase-like homolog in amphioxus: dependence of enzymatic and antifungal activities on the chitin-binding domain. Mol Immunol 51(1):57–65. CrossRefPubMedGoogle Scholar
  136. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19(6):727–740. CrossRefPubMedGoogle Scholar
  137. Xu L, Yuan S, Li J, Ruan J, Huang S, Yang M, Huang H, Chen S, Ren Z, Xu A (2011) The conservation and uniqueness of the caspase family in the basal chordate, amphioxus. BMC Biol 9:60. CrossRefPubMedPubMedCentralGoogle Scholar
  138. Xu N, Pan J, Liu S, Xue Q, Zhang S (2014) Three in one: identification, expression and enzymatic activity of lysozymes in amphioxus. Dev Comp Immunol 46(2):508–517. CrossRefPubMedGoogle Scholar
  139. Yan J, Wang J, Zhao Y, Zhang J, Bai C, Zhang C, Li K, Zhang H, Du X, Feng L (2012) Identification of an amphioxus intelectin homolog that preferably agglutinates gram-positive over gram-negative bacteria likely due to different binding capacity to LPS and PGN. Fish Shellfish Immunol 33(1):11–20. CrossRefPubMedGoogle Scholar
  140. Yan J, Xu L, Zhang Y, Zhang C, Zhao F, Feng L (2013a) Comparative genomic and phylogenetic analyses of the intelectin gene family: implications for their origin and evolution. Dev Comp Immunol 41(2):189–199. CrossRefPubMedGoogle Scholar
  141. Yan J, Zhang C, Zhang Y, Li K, Xu L, Guo L, Kong Y, Feng L (2013b) Characterization and comparative analyses of two amphioxus intelectins involved in the innate immune response. Fish Shellfish Immunol 34(5):1139–1146. CrossRefPubMedGoogle Scholar
  142. Yang M, Yuan S, Huang S, Li J, Xu L, Huang H, Tao X, Peng J, Xu A (2011) Characterization of bbtTICAM from amphioxus suggests the emergence of a MyD88-independent pathway in basal chordates. Cell Res 21(10):1410–1423. CrossRefPubMedPubMedCentralGoogle Scholar
  143. Yang R, Zheng T, Cai X, Yu Y, Yu C, Guo L, Huang S, Zhu W, Zhu R, Yan Q, Ren Z, Chen S, Xu A (2013) Genome-wide analyses of amphioxus microRNAs reveal an immune regulation via miR-92d targeting C3. J Immunol 190(4):1491–1500. CrossRefPubMedGoogle Scholar
  144. Yang P, Huang S, Yan X, Huang G, Dong X, Zheng T, Yuan D, Wang R, Li R, Tan Y, Xu A (2014) Origin of the phagocytic respiratory burst and its role in gut epithelial phagocytosis in a basal chordate. Free Radic Biol Med 70:54–67. CrossRefPubMedGoogle Scholar
  145. Yao F, Li Z, Zhang Y, Zhang S (2012) A novel short peptidoglycan recognition protein in amphioxus: identification, expression and bioactivity. Dev Comp Immunol 38(2):332–341. CrossRefPubMedGoogle Scholar
  146. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9(1):47–59. CrossRefPubMedGoogle Scholar
  147. Yu C, Dong M, Wu X, Li S, Huang S, Su J, Wei J, Shen Y, Mou C, Xie X, Lin J, Yuan S, Yu X, Yu Y, Du J, Zhang S, Peng X, Xiang M, Xu A (2005) Genes "waiting" for recruitment by the adaptive immune system: the insights from amphioxus. J Immunol 174(6):3493–3500CrossRefGoogle Scholar
  148. Yu Y, Huang H, Feng K, Pan M, Yuan S, Huang S, Wu T, Guo L, Dong M, Chen S, Xu A (2007a) A short-form C-type lectin from amphioxus acts as a direct microbial killing protein via interaction with peptidoglycan and glucan. J Immunol 179(12):8425–8434CrossRefGoogle Scholar
  149. Yu Y, Yuan S, Huang H, Feng K, Pan M, Huang S, Dong M, Chen S, Xu A (2007b) Molecular and biochemical characterization of galectin from amphioxus: primitive galectin of chordates participated in the infection processes. Glycobiology 17(7):774–783. CrossRefPubMedGoogle Scholar
  150. Yu Y, Huang H, Wang Y, Yuan S, Huang S, Pan M, Feng K, Xu A (2008) A novel C1q family member of amphioxus was revealed to have a partial function of vertebrate C1q molecule. J Immunol 181(10):7024–7032. CrossRefGoogle Scholar
  151. Yuan S, Huang S, Zhang W, Wu T, Dong M, Yu Y, Liu T, Wu K, Liu H, Yang M, Zhang H, Xu A (2009a) An amphioxus TLR with dynamic embryonic expression pattern responses to pathogens and activates NF-kappaB pathway via MyD88. Mol Immunol 46(11–12):2348–2356. CrossRefPubMedGoogle Scholar
  152. Yuan S, Liu T, Huang S, Wu T, Huang L, Liu H, Tao X, Yang M, Wu K, Yu Y, Dong M, Xu A (2009b) Genomic and functional uniqueness of the TNF receptor-associated factor gene family in amphioxus, the basal chordate. J Immunol 183(7):4560–4568. CrossRefPubMedGoogle Scholar
  153. Yuan S, Liu H, Gu M, Xu L, Huang S, Ren Z, Xu A (2010a) Characterization of the extrinsic apoptotic pathway in the basal chordate amphioxus. Sci Signal 3(139):ra66. CrossRefPubMedGoogle Scholar
  154. Yuan S, Wu K, Yang M, Xu L, Huang L, Liu H, Tao X, Huang S, Xu A (2010b) Amphioxus SARM involved in neural development may function as a suppressor of TLR signaling. J Immunol 184(12):6874–6881. CrossRefPubMedGoogle Scholar
  155. Yuan S, Zhang J, Zhang L, Huang L, Peng J, Huang S, Chen S, Xu A (2013) The archaic roles of the amphioxus NF-kappaB/IkappaB complex in innate immune responses. J Immunol 191(3):1220–1230. CrossRefPubMedGoogle Scholar
  156. Yuan S, Dong X, Tao X, Xu L, Ruan J, Peng J, Xu A (2014a) Emergence of the A20/ABIN-mediated inhibition of NF-kappaB signaling via modifying the ubiquitinated proteins in a basal chordate. Proc Natl Acad Sci U S A 111(18):6720–6725. CrossRefPubMedPubMedCentralGoogle Scholar
  157. Yuan S, Tao X, Huang S, Chen S, Xu A (2014b) Comparative immune systems in animals. Annu Rev Anim Biosci 2:235–258. CrossRefPubMedGoogle Scholar
  158. Yuan S, Ruan J, Huang S, Chen S, Xu A (2015a) Amphioxus as a model for investigating evolution of the vertebrate immune system. Dev Comp Immunol 48(2):297–305. CrossRefPubMedGoogle Scholar
  159. Yuan S, Zheng T, Li P, Yang R, Ruan J, Huang S, Wu Z, Xu A (2015b) Characterization of Amphioxus IFN regulatory factor family reveals an archaic signaling framework for innate immune response. J Immunol 195(12):5657–5666. CrossRefPubMedGoogle Scholar
  160. Zhang S, Wang C, Wang Y, Wei R, Jiang G, Ju H (2003) Presence and characterization of complement-like activity in the amphioxus Branchiostoma belcheri tsingtauense. Zool Sci 20(10):1207–1214. CrossRefPubMedGoogle Scholar
  161. Zhang SM, Zeng Y, Loker ES (2007) Characterization of immune genes from the schistosome host snail Biomphalaria glabrata that encode peptidoglycan recognition proteins and gram-negative bacteria binding protein. Immunogenetics 59(11):883–898. CrossRefPubMedPubMedCentralGoogle Scholar
  162. Zhang Y, Xu K, Deng A, Fu X, Xu A, Liu X (2014) An amphioxus RAG1-like DNA fragment encodes a functional central domain of vertebrate core RAG1. Proc Natl Acad Sci U S A 111(1):397–402. CrossRefPubMedGoogle Scholar
  163. Zmasek CM, Zhang Q, Ye Y, Godzik A (2007) Surprising complexity of the ancestral apoptosis network. Genome Biol 8(10):R226. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine BiologyOcean University of ChinaQingdaoChina
  2. 2.Laboratory for Marine Biology and BiotechnologyQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

Personalised recommendations