Alternative adaptive immunity strategies: coelacanth, cod and shark immunity

Molecular Immunology

Volumn 69, Issue , 2016, Pages 157-169

  Buonocore, Francesco ^a   Gerdol, Marco ^b  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Adaptive immunity; CD4; Coelacanth; Immunoglobulin; Major histocompatibility complex; T helper cells.

Indexed keywords

IMMUNOGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; ARTICLE; ATLANTIC COD; CD4+ T LYMPHOCYTE; COELACANTH; HELPER CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; SHARK; TRANSCRIPTOMICS; VALIDATION STUDY; ANIMAL; EVOLUTION; IMMUNOLOGY; PHYLOGENY; VERTEBRATE;

ADAPTIVE IMMUNITY; ANIMALS; BIOLOGICAL EVOLUTION; GADUS MORHUA; PHYLOGENY; SHARKS; VERTEBRATES;

EID: 84966372768     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.09.003     Document Type: Article

References (102)

1. Alder, M.N., Rogozin, I.B., Iyer, L.M., Glazko, G.V., Cooper, M.D., Pancer, Z., Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310 (2005), 1970–1973, 10.1126/science.1119420.
2. Amemiya, C.T., Alföldi, J., Lee, A.P., Fan, S., Philippe, H., MacCallum, I., Braasch, I., Manousaki, T., Schneider, I., Rohner, N., Organ, C., Chalopin, D., Smith, J.J., Robinson, M., Dorrington, R.A., Gerdol, M., Aken, B., Biscotti, M.A., Barucca, M., Baurain, D., Berlin, A.M., Blatch, G.L., Buonocore, F., Burmester, T., Campbell, M.S., Canapa, A., Cannon, J.P., Christoffels, A., De Moro, G., Edkins, A.L., Fan, L., Fausto, A.M., Feiner, N., Forconi, M., Gamieldien, J., Gnerre, S., Gnirke, A., Goldstone, J.V., Haerty, W., Hahn, M.E., Hesse, U., Hoffmann, S., Johnson, J., Karchner, S.I., Kuraku, S., Lara, M., Levin, J.Z., Litman, G.W., Mauceli, E., Miyake, T., Mueller, M.G., Nelson, D.R., Nitsche, A., Olmo, E., Ota, T., Pallavicini, A., Panji, S., Picone, B., Ponting, C.P., Prohaska, S.J., Przybylski, D., Saha, N.R., Ravi, V., Ribeiro, F.J., Sauka-Spengler, T., Scapigliati, G., Searle, S.M.J., Sharpe, T., Simakov, O., Stadler, P.F., Stegeman, J.J., Sumiyama, K., Tabbaa, D., Tafer, H., Turner-Maier, J., van Heusden, P., White, S., Williams, L., Yandell, M., Brinkmann, H., Volff, J.-N., Tabin, C.J., Shubin, N., Schartl, M., Jaffe, D.B., Postlethwait, J.H., Venkatesh, B., Di Palma, F., Lander, E.S., Meyer, A., Lindblad-Toh, K., The African coelacanth genome provides insights into tetrapod evolution. Nature 496 (2013), 311–316, 10.1038/nature12027.
3. Amigorena, S., Savina, A., Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22 (2010), 109–117, 10.1016/j.coi.2010.01.022.
4. Andersen, K.G., Nissen, J.K., Betz, A.G., Comparative genomics reveals key gain-of-function events in foxp during regulatory T cell evolution. Front. Immunol., 3(113), 2012, 3, 10.3389/fimmu.2012.00113.
5. Bengtén, E., Clem, L.W., Miller, N.W., Warr, G.W., Wilson, M., Channel catfish immunoglobulins: repertoire and expression. Dev. Comp. Immunol. 30 (2006), 77–92, 10.1016/j.dci.2005.06.016.
6. Bengtén, E., Leanderson, T., Pilström, L., Immunoglobulin heavy chain cDNA from the teleost Atlantic cod (Gadus morhua L.): nucleotide sequences of secretory and membrane form show an unusual splicing pattern. Eur. J. Immunol. 21 (1991), 3027–3033, 10.1002/eji.1830211219.
7. Berstein, R.M., Schluter, S.F., Shen, S., Marchalonis, J.J., A new high molecular weight immunoglobulin class from the carcharhine shark: implications for the properties of the primordial immunoglobulin. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 3289–3293.
8. Boehm, T., Evolution of vertebrate immunity. Curr. Biol. CB 22 (2012), R722–R732, 10.1016/j.cub.2012.07.003.
9. Boniface, K., Blom, B., Liu, Y.-J., de Waal Malefyt, R., From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol. Rev. 226 (2008), 132–146, 10.1111/j.1600-065X.00714.x.
10. Boudinot, P., Zou, J., Ota, T., Buonocore, F., Scapigliati, G., Canapa, A., Cannon, J., Litman, G., Hansen, J.D., A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths. J. Exp. Zool. B Mol. Dev. Evol. 322 (2014), 415–437, 10.1002/jez.b.22559.
11. Burnet, F.M., The Clonal Selection Theory of Acquired Immunity. 1959, Cambridge University Press, Cambridge, UK.
12. Butler, J.E., Sun, J., Navarro, P., The swine Ig heavy chain locus has a single JH and no identifiable IgD. Int. Immunol. 8 (1996), 1897–1904.
13. Caipang, C.M.A., Expression of genes involved in the early immune response at the distal segment of the gut in Atlantic cod, Gadus morhua L. after vaccination with a bacterial antigen. Aquacult. Int. 21 (2012), 591–603, 10.1007/s10499-012-9591-8.
14. Caipang, C.M.A., Brinchmann, M.F., Kiron, V., Profiling gene expression in the spleen of Atlantic cod, Gadus morhua upon vaccination with Vibrio anguillarum antigen. Comp. Biochem. Physiol.—B Biochem. Mol. Biol. 153 (2009), 261–267, 10.1016/j.cbpb.2009.03.005.
15. Caipang, C.M.A., Lazado, C.C., Brinchmann, M.F., Kiron, V., Transcription of selected immune-related genes in spleen cells of cod, Gadus morhua following incubation with alginic acid and β-glucan. J. Exp. Mar. Biol. Ecol. 416–417 (2012), 202–207, 10.1016/j.jembe.2011.12.013.
16. Caipang, C.M.A., Lazado, C.C., Brinchmann, M.F., Kiron, V., Infection-induced changes in expression of antibacterial and cytokine genes in the gill epithelial cells of Atlantic cod, Gadus morhua during incubation with bacterial pathogens. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 156 (2010), 319–325, 10.1016/j.cbpb.2010.04.009.
17. Chen, K., Cerutti, A., New insights into the enigma of immunoglobulin D. Immunol. Rev. 237 (2010), 160–179, 10.1111/j.1600-065X.2010.00929.x.
18. Cooper, M.D., Alder, M.N., The evolution of adaptive immune systems. Cell 124 (2006), 815–822, 10.1016/j.cell.2006.02.001.
19. Cooper, M.D., Peterson, R.D.A., Good, R.A., Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205 (1965), 143–146, 10.1038/205143a0.
20. Daggfeldt, A., Bengtén, E., Pilström, L., A cluster type organization of the loci of the immunoglobulin light chain in Atlantic cod (Gadus morhua L.) and rainbow trout (Oncorhynchus mykiss Walbaum) indicated by nucleotide sequences of cDNAs and hybridization analysis. Immunogenetics 38 (1993), 199–209.
21. Desmyter, A., Transue, T.R., Ghahroudi, M.A., Dao Thi, M.-H., Poortmans, F., Hamers, R., Muyldermans, S., Wyns, L., Crystal structure of a camel single-domain VH antibody fragment in complex with lysozyme. Nat. Struct. Mol. Biol. 3 (1996), 803–811, 10.1038/nsb0996-803.
22. Dhanasiri, A.K., Brunvold, L., Brinchmann, M.F., Korsnes, K., Bergh, Ø., Kiron, V., Changes in the intestinal microbiota of wild Atlantic cod Gadus morhua L. upon captive rearing. Microb. Ecol. 61 (2011), 20–30.
23. Dijkstra, J.M., TH2 and Treg candidate genes in elephant shark. Nature 511 (2014), E7–E9, 10.1038/nature13446.
24. Dijkstra, J.M., Grimholt, U., Leong, J., Koop, B.F., Hashimoto, K., Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol. Biol., 13, 2013, 260, 10.1186/1471-2148-13-260.
25. Dooley, H., Flajnik, M.F., Shark immunity bites back: affinity maturation and memory response in the nurse shark, Ginglymostoma cirratum. Eur. J. Immunol. 35 (2005), 936–945, 10.1002/eji.200425760.
26. Edholm, E.-S., Bengten, E., Wilson, M., Insights into the function of IgD. Dev. Comp. Immunol. 35 (2011), 1309–1316, 10.1016/j.dci.2011.03.002.
27. Flajnik, M.F., Comparative analyses of immunoglobulin genes: surprises and portents. Nat. Rev. Immunol. 2 (2002), 688–698, 10.1038/nri889.
28. Flajnik, M.F., Du Pasquier, L., Evolution of innate and adaptive immunity: can we draw a line?. Trends Immunol. 25 (2004), 640–644, 10.1016/j.it.2004.10.001.
29. Flajnik, M.F., Kasahara, M., Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11 (2010), 47–59, 10.1038/nrg2703.
30. Flajnik, M.F., Rumfelt, L.L., The immune system of cartilaginous fish. Curr. Top. Microbiol. Immunol. 248 (2000), 249–270.
31. Fricke, H., Hissmann, K., Schauer, J., Reinicke, O., Kasang, L., Plante, R., Habitat and population size of the coelacanth Latimeria chalumnae at Grand Comoro. Environ. Biol. Fishes 32 (1991), 287–300, 10.1007/bf00007462.
32. Gellert, M., V(D)J recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 71 (2002), 101–132, 10.1146/annurev.biochem.71.090501.150203.
33. Gómez, D., Conejeros, P., Marshall, S.H., Consuegra, S., MHC evolution in three salmonid species: a comparison between class II alpha and beta genes. Immunogenetics 62 (2010), 531–542, 10.1007/s00251-010-0456-x.
34. Greenberg, A.S., Avila, D., Hughes, M., Hughes, A., McKinney, E.C., Flajnik, M.F., A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374 (1995), 168–173, 10.1038/374168a0.
35. Haase, D., Roth, O., Kalbe, M., Schmiedeskamp, G., Scharsack, J.P., Rosenstiel, P., Reusch, T.B.H., Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle: evidence from deep transcriptome sequencing. Biol. Lett., 9, 2013, 2013, 10.1098/rsbl.2013.0044.
36. Halldórsdóttir, K., Árnason, E., Trans-species polymorphism at antimicrobial innate immunity cathelicidin genes of Atlantic cod and related species. Peer J., 3, 2015, e976, 10.7717/peerj.976.
37. Hordvik, I., Identification of a novel immunoglobulin delta transcript and comparative analysis of the genes encoding IgD in Atlantic salmon and Atlantic halibut. Mol. Immunol. 39 (2002), 85–91.
38. Hughes, G.M., Itazawa, Y., The effect of temperature on the respiratory function of coelacanth blood. Experientia, 28, 1972, 1247.
39. Inoue, J.G., Miya, M., Lam, K., Tay, B.-H., Danks, J.A., Bell, J., Walker, T.I., Venkatesh, B., Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol. Biol. Evol. 27 (2010), 2576–2586, 10.1093/molbev/msq147.
40. Israelson, O., Petersson, A., Bengtén, E., Wiersma, E.J., Anderson, J., Gezelius, G., Pilstrom, L., Immunoglobulin concentration in Atlantic cod, Gadus morhua L., serum and cross-reactivity between anti-cod-antibodies and immunoglobulins from other species. J. Fish Biol. 39 (1991), 265–278, 10.1111/j.1095-8649.1991.tb04361.x.
41. Ivanov, I.I., McKenzie, B.S., Zhou, L., Tadokoro, C.E., Lepelley, A., Lafaille, J.J., Cua, D.J., Littman, D.R., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126 (2006), 1121–1133, 10.1016/j.cell.2006.07.035.
42. József, L., Khreiss, T., El Kebir, D., Filep, J.G., Activation of TLR-9 induces IL-8 secretion through peroxynitrite signaling in human neutrophils. J. Immunol. Baltim. Md 1950 176 (2006), 1195–1202.
43. King, B.L., Gillis, J.A., Carlisle, H.R., Dahn, R.D., A natural deletion of the HoxC cluster in elasmobranch fishes. Science, 334, 2011, 1517, 10.1126/science.1210912.
44. Kishishita, N., Nagawa, F., Evolution of adaptive immunity: implications of a third lymphocyte lineage in lampreys. Bioessays 36 (2014), 244–250, 10.1002/bies.201300145.
45. Krasnov, A., Kileng, O., Skugor, S., Jørgensen, S.M., Afanasyev, S., Timmerhaus, G., Sommer, A.-I., Jensen, I., Genomic analysis of the host response to nervous necrosis virus in atlantic cod (Gadus morhua) brain. Mol. Immunol. 54 (2013), 443–452, 10.1016/j.molimm.2013.01.010.
46. Krishnaswamy Gopalan, T., Gururaj, P., Gupta, R., Gopal, D.R., Rajesh, P., Chidambaram, B., Kalyanasundaram, A., Angamuthu, R., Transcriptome profiling reveals higher vertebrate orthologous of intra-cytoplasmic pattern recognition receptors in grey bamboo shark. PLoS One, 9, 2014, e100018, 10.1371/journal.pone.0100018.
47. Lampert, K.P., Fricke, H., Hissmann, K., Schauer, J., Blassmann, K., Ngatunga, B.P., Schartl, M., Population divergence in East African coelacanths. Curr. Biol. 22 (2012), R439–R440, 10.1016/j.cub.2012.04.053.
48. Lanier, L.L., Sun, J.C., Do the terms innate and adaptive immunity create conceptual barriers?. Nat. Rev. Immunol. 9 (2009), 302–303, 10.1038/nri2547.
49. Lazado, C.C., Caipang, C.M.A., Gallage, S., Brinchmann, M.F., Kiron, V., Expression profiles of genes associated with immune response and oxidative stress in Atlantic cod, Gadus morhua head kidney leukocytes modulated by live and heat-inactivated intestinal bacteria. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 155 (2010), 249–255, 10.1016/j.cbpb.2009.11.006.
50. Lee, Y.K., Mazmanian, S.K., Has the microbiota played a critical role in the evolution of the adaptive immune system?. Science 330 (2010), 1768–1773.
51. Litman, G.W., Cannon, J.P., Dishaw, L.J., Reconstructing immune phylogeny: new perspectives. Nat. Rev. Immunol. 5 (2005), 866–879, 10.1038/nri1712.
52. Litman, G.W., Rast, J.P., Fugmann, S.D., The origins of vertebrate adaptive immunity. Nat. Rev. Immunol. 10 (2010), 543–553, 10.1038/nri2807.
53. Magnadóttir, B., Jónsdóttir, H., Helgason, S., Björnsson, B., Jørgensen, T.Ø., Pilström, L., Humoral immune parameters in Atlantic cod (Gadus morhua L.): II. The effects of size and gender under different environmental conditions. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 122 (1999), 181–188, 10.1016/S0305-0491(98)10157-8.
54. Malagoli, D., Sacchi, S., Ottaviani, E. 2010. Lectins and cytokines in celomatic invertebrates: two tales with the same end.
55. Malmstrøm, M., Jentoft, S., Gregers, T.F., Jakobsen, K.S., Unraveling the evolution of the atlantic cod's (Gadus morhua L.) Alternative Immune Strategy. PLoS One, 8, 2013, e74004, 10.1371/journal.pone.0074004.
56. Mayer, W.E., Uinuk-ool, T., Tichy, H., Gartland, L.A., Klein, J., Cooper, M.D., Isolation and characterization of lymphocyte-like cells from a lamprey. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 14350–14355, 10.1073/pnas.212527499.
57. Mikkelsen, H., Lund, V., Larsen, R., Seppola, M., Vibriosis vaccines based on various sero-subgroups of Vibrio anguillarum O2 induce specific protection in Atlantic cod (Gadus morhua L.) juveniles. Fish Shellfish Immunol. 30 (2011), 330–339, 10.1016/j.fsi.2010.11.007.
58. Milano, I., Babbucci, M., Panitz, F., Ogden, R., Nielsen, R.O., Taylor, M.I., Helyar, S.J., Carvalho, G.R., Espiñeira, M., Atanassova, M., Tinti, F., Maes, G.E., Patarnello, T., Bargelloni, L., FishPopTrace Consortium, Novel tools for conservation genomics: comparing two high-throughput approaches for SNP discovery in the transcriptome of the European Hake. PLoS One, 6, 2011, e28008, 10.1371/journal.pone.0028008.
59. Miller, K.M., Kaukinen, K.H., Schulze, A.D., Expansion and contraction of major histocompatibility complex genes: a teleostean example. Immunogenetics 53 (2002), 941–963, 10.1007/s00251-001-0398-4.
60. Mulley, J.F., Hargreaves, A.D., Hegarty, M.J., Heller, R.S., Swain, M.T., Transcriptomic analysis of the lesser spotted catshark (Scyliorhinus canicula) pancreas, liver and brain reveals molecular level conservation of vertebrate pancreas function. BMC Genomics, 15, 2014, 1074, 10.1186/1471-2164-15-1074.
61. Mussmann, R., Du Pasquier, L., Hsu, E., Is Xenopus IgX an analog of IgA?. Eur. J. Immunol. 26 (1996), 2823–2830, 10.1002/eji.1830261205.
62. Nagawa, F., Kishishita, N., Shimizu, K., Hirose, S., Miyoshi, M., Nezu, J., Nishimura, T., Nishizumi, H., Takahashi, Y., Hashimoto, S., Takeuchi, M., Miyajima, A., Takemori, T., Otsuka, A.J., Sakano, H., Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat. Immunol. 8 (2007), 206–213, 10.1038/ni1419.
63. Nikaido, M., Noguchi, H., Nishihara, H., Toyoda, A., Suzuki, Y., Kajitani, R., Suzuki, H., Okuno, M., Aibara, M., Ngatunga, B.P., Mzighani, S.I., Kalombo, H.W.J., Masengi, K.W.A., Tuda, J., Nogami, S., Maeda, R., Iwata, M., Abe, Y., Fujimura, K., Okabe, M., Amano, T., Maeno, A., Shiroishi, T., Itoh, T., Sugano, S., Kohara, Y., Fujiyama, A., Okada, N., Coelacanth genomes reveal signatures for evolutionary transition from water to land. Genome Res., 2013, 10.1101/gr.158105.113.
64. Ohta, Y., Flajnik, M., IgD, like IgM, is a primordial immunoglobulin class perpetuated in most jawed vertebrates. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 10723–10728, 10.1073/pnas.0601407103.
65. Ota, T., Rast, J.P., Litman, G.W., Amemiya, C.T., Lineage-restricted retention of a primitive immunoglobulin heavy chain isotype within the Dipnoi reveals an evolutionary paradox. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 2501–2506, 10.1073/pnas.0538029100.
66. Ozsolak, F., Milos, P.M., RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet. 12 (2011), 87–98, 10.1038/nrg2934.
67. Pallavicini, A., Canapa, A., Barucca, M., Alfőldi, J., Biscotti, M.A., Buonocore, F., Moro, G.D., Palma, F.D., Fausto, A.M., Forconi, M., Gerdol, M., Makapedua, D.M., Turner-Meier, J., Olmo, E., Scapigliati, G., Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis. BMC Genomics, 14, 2013, 538, 10.1186/1471-2164-14-538.
68. Pancer, Z., Amemiya, C.T., Ehrhardt, G.R.A., Ceitlin, J., Gartland, G.L., Cooper, M.D., Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430 (2004), 174–180, 10.1038/nature02740.
69. Pancer, Z., Saha, N.R., Kasamatsu, J., Suzuki, T., Amemiya, C.T., Kasahara, M., Cooper, M.D., Variable lymphocyte receptors in hagfish. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9224–9229, 10.1073/pnas.0503792102.
70. Persson, A.-C., Stet, R.J.M., Pilström, L., Characterization of MHC class I and β2-microglobulin sequences in Atlantic cod reveals an unusually high number of expressed class I genes. Immunogenetics 50 (1999), 49–59, 10.1007/s002510050685.
71. Pilström, L., Petersson, A., Isolation and partial characterization of immunoglobulin from cod (Gadus morhua L.). Dev. Comp. Immunol. 15 (1991), 143–152.
72. Pilström, L., Warr, G.W., Strömberg, S., Why is the antibody response of Atlantic cod so poor? The search for a genetic explanation. Fish. Sci. 71 (2005), 961–971, 10.1111/j.1444-2906.2005.01052.x.
73. Richards, M.H., Nelson, J.L., The evolution of vertebrate antigen receptors: a phylogenetic approach. Mol. Biol. Evol. 17 (2000), 146–155.
74. Rogozin, I.B., Iyer, L.M., Liang, L., Glazko, G.V., Liston, V.G., Pavlov, Y.I., Aravind, L., Pancer, Z., Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat. Immunol. 8 (2007), 647–656, 10.1038/ni1463.
75. Rudensky, A.Y., Regulatory T cells and Foxp3. Immunol. Rev. 241 (2011), 260–268, 10.1111/j.1600-065X.2011.01018.x.
76. Saha, N.R., Ota, T., Litman, G.W., Hansen, J., Parra, Z., Hsu, E., Buonocore, F., Canapa, A., Cheng, J.-F., Amemiya, C.T., Genome complexity in the coelacanth is reflected in its adaptive immune system. J. Exp. Zool. B Mol. Dev. Evol. 322 (2014), 438–463, 10.1002/jez.b.22558.
77. Saha, N.R., Smith, J., Amemiya, C.T., Evolution of adaptive immune recognition in jawless vertebrates. Semin. Immunol. 22 (2010), 25–33, 10.1016/j.smim.2009.12.002.
78. Saha, N.R., Suetake, H., Kikuchi, K., Suzuki, Y., Fugu immunoglobulin D: a highly unusual gene with unprecedented duplications in its constant region. Immunogenetics 56 (2004), 438–447, 10.1007/s00251-004-0693-y.
79. Solem, S.T., Stenvik, J., Antibody repertoire development in teleosts—a review with emphasis on salmonids and Gadus morhua L. Dev. Comp. Immunol. 30 (2006), 57–76, 10.1016/j.dci.2005.06.007.
80. Star, B., Jentoft, S., Why does the immune system of Atlantic cod lack MHC II?. BioEssays News Rev. Mol. Cell. Dev. Biol. 34 (2012), 648–651, 10.1002/bies.201200005.
81. Star, B., Nederbragt, A.J., Jentoft, S., Grimholt, U., Malmstrøm, M., Gregers, T.F., Rounge, T.B., Paulsen, J., Solbakken, M.H., Sharma, A., Wetten, Ø.F., Lanzén, A., Winer, R., Knight, J., Vogel, J.-H., Aken, B., Andersen, Ø., Lagesen, K., Tooming-Klunderud, A., Edvardsen, R.B., Tina, K.G., Espelund, M., Nepal, C., Previti, C., Karlsen, B.Ø., Moum, T., Skage, M., Berg, P.R., Gjøen, T., Kuhl, H., Thorsen, J., Malde, K., Reinhardt, R., Du, L., Johansen, S.D., Searle, S., Lien, S., Nilsen, F., Jonassen, I., Omholt, S.W., Stenseth, N.C., Jakobsen, K.S., The genome sequence of Atlantic cod reveals a unique immune system. Nature 477 (2011), 207–210, 10.1038/nature10342.
82. Stenvik, J., Jørgensen, T.O., Immunoglobulin D (IgD) of Atlantic cod has a unique structure. Immunogenetics 51 (2000), 452–461.
83. Stenvik, J., Lundbäck, A.S., Jørgensen, T.O., Pilström, L., Variable region diversity of the Atlantic cod (Gadus morhua L.) immunoglobulin heavy chain. Immunogenetics 51 (2000), 670–680.
84. Tonegawa, S., Somatic generation of antibody diversity. Nature 302 (1983), 575–581, 10.1038/302575a0.
85. Tournefier, A., Laurens, V., Chapusot, C., Ducoroy, P., Padros, M.R., Salvadori, F., Sammut, B., Structure of MHC class I and class II cDNAs and possible immunodeficiency linked to class II expression in the Mexican axolotl. Immunol. Rev. 166 (1998), 259–277.
86. Venkatesh, B., Lee, A.P., Ravi, V., Maurya, A.K., Lian, M.M., Swann, J.B., Ohta, Y., Flajnik, M.F., Sutoh, Y., Kasahara, M., Hoon, S., Gangu, V., Roy, S.W., Irimia, M., Korzh, V., Kondrychyn, I., Lim, Z.W., Tay, B.-H., Tohari, S., Kong, K.W., Ho, S., Lorente-Galdos, B., Quilez, J., Marques-Bonet, T., Raney, B.J., Ingham, P.W., Tay, A., Hillier, L.W., Minx, P., Boehm, T., Wilson, R.K., Brenner, S., Warren, W.C., Elephant shark genome provides unique insights into gnathostome evolution. Nature 505 (2014), 174–179, 10.1038/nature12826.
87. Venkatesh, B., Lee, A.P., Swann, J.B., Ohta, Y., Flajnik, M.F., Kasahara, M., Boehm, T., Warren, W.C., Venkatesh et al. reply. Nature 511 (2014), E9–10, 10.1038/nature13447.
88. Wang, T., Huang, W., Costa, M.M., Secombes, C.J., The gamma-chain cytokine/receptor system in fish: more ligands and receptors. Fish Shellfish Immunol. 1st EOFFI Symp. 31 (2011), 673–687, 10.1016/j.fsi.2011.05.016.
89. Wang, T., Secombes, C.J., The evolution of IL-4 and IL-13 and their receptor subunits. Cytokine, 2015, 10.1016/j.cyto.2015.04.012.
90. Warr, G.W., Magor, K.E., Higgins, D.A., IgY: clues to the origins of modern antibodies. Immunol. Today 16 (1995), 392–398, 10.1016/0167-5699(95)800085-5.
91. Wen, Y., Fang, W., Xiang, L.-X., Pan, R.-L., Shao, J.-Z., Identification of Treg-like cells in Tetraodon: insight into the origin of regulatory T subsets during early vertebrate evolution. Cell. Mol. Life Sci. CMLS 68 (2011), 2615–2626, 10.1007/s00018-010-0574-5.
92. Whittaker K., 2014. Endangered Species Act—Draft status review report for the coelacanth Latimeria chalumnae.
93. Widholm, H., Lundbäck, A.-S., Daggfeldt, A., Magnadottir, B., Warr, G.W., Pilström, L., Light chain variable region diversity in Atlantic cod (Gadus morhua L.). Dev. Comp. Immunol. 23 (1999), 231–240, 10.1016/s0145-305x(99)3-8.
94. Wilson, A.B., Whittington, C.M., Bahr, A., High intralocus variability and interlocus recombination promote immunological diversity in a minimal major histocompatibility system. BMC Evol. Biol., 14, 2014, 273, 10.1186/s12862-014-0273-1.
95. Wilson, M., Bengtén, E., Miller, N.W., Clem, L.W., Du Pasquier, L., Warr, G.W., A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 4593–4597.
96. Xiao, F.S., Wang, Y.P., Yan, W., Chang, M.X., Yao, W.J., Xu, Q.Q., Wang, X.X., Gao, Q., Nie, P., Ig heavy chain genes and their locus in grass carp Ctenopharyngodon idella. Fish Shellfish Immunol. 29 (2010), 594–599, 10.1016/j.fsi.2010.06.004.
97. Zhang, Y.-A., Salinas, I., Li, J., Parra, D., Bjork, S., Xu, Z., LaPatra, S.E., Bartholomew, J., Sunyer, J.O., IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11 (2010), 827–835, 10.1038/ni.1913.
98. Zhang, T., Tacchi, L., Wei, Z., Zhao, Y., Salinas, I., Intraclass diversification of immunoglobulin heavy chain genes in the African lungfish. Immunogenetics 66 (2014), 335–351, 10.1007/s00251-014-0769-2.
99. Zhao, Y., Kacskovics, I., Pan, Q., Liberles, D.A., Geli, J., Davis, S.K., Rabbani, H., Hammarstrom, L., Artiodactyl IgD: the missing link. J. Immunol. Baltim. Md 1950 169 (2002), 4408–4416.
100. Zhao, Y., Pan-Hammarström, Q., Yu, S., Wertz, N., Zhang, X., Li, N., Butler, J.E., Hammarström, L., Identification of IgF, a hinge-region-containing Ig class, and IgD in Xenopus tropicalis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 12087–12092, 10.1073/pnas.0600291103.
101. Zhu, L., Yan, Z., Feng, M., Peng, D., Guo, Y., Hu, X., Ren, L., Sun, Y., Identification of sturgeon IgD bridges the evolutionary gap between elasmobranchs and teleosts. Dev. Comp. Immunol. 42 (2014), 138–147, 10.1016/j.dci.2013.08.020.
102. Zimmerman, A.M., Moustafa, F.M., Romanowski, K.E., Steiner, L.A., Zebrafish immunoglobulin IgD: unusual exon usage and quantitative expression profiles with IgM and IgZ/T heavy chain isotypes. Mol. Immunol. 48 (2011), 2220–2223, 10.1016/j.molimm.2011.06.441.