The immunoglobulins of cold-blooded vertebrates

Biomolecules

Volumn 4, Issue 4, 2014, Pages 1045-1069

  Pettinello, Rita ^a   Dooley, Helen ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Amphibians; Antibody; Bony fish; Cartilaginous fish; Ectotherms; Immunoglobulin; Reptiles

Indexed keywords

IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN D; IMMUNOGLOBULIN E; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN T; IMMUNOGLOBULIN W; IMMUNOGLOBULIN X; IMMUNOGLOBULIN Y; UNCLASSIFIED DRUG; AMPHIBIAN PROTEIN; IMMUNOGLOBULIN CLASS;

CARTILAGINOUS FISH; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SEQUENCE; HUMORAL IMMUNITY; IMMUNE RESPONSE; INTESTINE LYMPHATIC TISSUE; NONHUMAN; PHYLOGENY; PROTEIN EXPRESSION; REVIEW; SOMATIC HYPERMUTATION; TRANSCRIPTION REGULATION; VERTEBRATE; ADAPTIVE IMMUNITY; AMPHIBIA; ANIMAL; BLOOD; CHEMISTRY; FISH; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR EVOLUTION; REPTILE;

ADAPTIVE IMMUNITY; AMPHIBIAN PROTEINS; AMPHIBIANS; ANIMALS; EVOLUTION, MOLECULAR; FISHES; IMMUNOGLOBULIN ISOTYPES; IMMUNOGLOBULINS; PHYLOGENY; REPTILES; VERTEBRATES;

EID: 84964312932     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom4041045     Document Type: Review

References (140)

1. Flajnik, M.F.; Kasahara, M. Origin and evolution of the adaptive immune system: Genetic events and selective pressures. Nat. Rev. Genet. 2010, 11, 47-59.
2. Pancer, Z.; Amemiya, C.T.; Ehrhardt, G.R.; Ceitlin, J.; Gartland, G.L.; Cooper, M.D. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 2004, 430, 174-180.
3. 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. USA 2005, 102, 9224-9229.
4. 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. 2010, 27, 2576-2586.
5. Dooley, H.; Flajnik, M.F. Antibody repertoire development in cartilaginous fish. Dev. Comp. Immunol. 2006, 30, 43-56.
6. Miracle, A.L.; Anderson, M.K.; Litman, R.T.; Walsh, C.J.; Luer, C.A.; Rothenberg, E.V.; Litman, G.W. Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire. Int. Immunol. 2001, 13, 567-580.
7. Zapata, A.; Amemiya, C.T. Phylogeny of lower vertebrates and their immunological structures. Curr. Top. Microbiol. Immunol. 2000, 248, 67-107.
8. Hinds, K.R.; Litman, G.W. Major reorganization of immunoglobulin VH segmental elements during vertebrate evolution. Nature 1986, 320, 546-549.
9. Malecek, K.; Lee, V.; Feng, W.; Huang, J.L.; Flajnik, M.F.; Ohta, Y.; Hsu, E. Immunoglobulin heavy chain exclusion in the shark. PLoS Biol. 2008, 6, e157.
10. Kokubu, F.; Litman, R.; Shamblott, M.J.; Hinds, K.; Litman, G.W. Diverse organization of immunoglobulin VH gene loci in a primitive vertebrate. EMBO J. 1988, 7, 3413-3422.
11. Lee, S.S.; Fitch, D.; Flajnik, M.F.; Hsu, E. Rearrangement of immunoglobulin genes in shark germ cells. J. Exp. Med. 2000, 191, 1637-1648.
12. Diaz, M.; Stanfield, R.L.; Greenberg, A.S.; Flajnik, M.F. Structural analysis, selection, and ontogeny of the shark new antigen receptor (IgNAR): Identification of a new locus preferentially expressed in early development. Immunogenetics 2002, 54, 501-512.
13. Rumfelt, L.L.; Avila, D.; Diaz, M.; Bartl, S.; McKinney, E.C.; Flajnik, M.F. A shark antibody heavy chain encoded by a nonsomatically rearranged VDJ is preferentially expressed in early development and is convergent with mammalian IgG. Proc. Natl. Acad. Sci. USA 2001, 98, 1775-1780.
14. 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. 2007, 8, 647-656.
15. Warr, G.W.; Magor, K.E.; Higgins, D.A. IgY: Clues to the origins of modern antibodies. Immunol. Today 1995, 16, 392-398.
16. Mashoof, S.; Goodroe, A.; Du, C.C.; Eubanks, J.O.; Jacobs, N.; Steiner, J.M.; Tizard, I.; Suchodolski, J.S.; Criscitiello, M.F. Ancient T-independence of mucosal IgX/A: Gut microbiota unaffected by larval thymectomy in Xenopus laevis. Mucosal Immunol. 2013, 6, 358-368.
17. Saha, N.R.; Ota, T.; Litman, G.W.; Hansen, J.; Parra, Z.; Hsu, E.; Buonocore, F.; Canapa, A.; Cheng, J.F.; Amemiya, C.T.; et al. Genome complexity in the coelacanth is reflected in its adaptive immune system. J. Exp. Zool. B Mol. Dev. Evol. 2014, 322, 438-463.
18. Criscitiello, M.F.; Flajnik, M.F. Four primordial immunoglobulin light chain isotypes, including lambda and kappa, identified in the most primitive living jawed vertebrates. Eur. J. Immunol. 2007, 37, 2683-2694.
19. Zhu, C.; Lee, V.; Finn, A.; Senger, K.; Zarrin, A.A.; du Pasquier, L.; Hsu, E. Origin of immunoglobulin isotype switching. Curr. Biol. 2012, 22, 872-880.
20. Saunders, H.L.; Oko, A.L.; Scott, A.N.; Fan, C.W.; Magor, B.G. The cellular context of AID expressing cells in fish lymphoid tissues. Dev. Comp. Immunol. 2010, 34, 669-676.
21. Marchalonis, J.; Edelman, G.M. Polypeptide chains of immunoglobulins from the smooth dogfish (Mustelus canis). Science 1966, 154, 1567-1568.
22. Ohta, Y.; Flajnik, M. IgD, like IgM, is a primordial immunoglobulin class perpetuated in most jawed vertebrates. Proc. Natl. Acad. Sci. USA 2006, 103, 10723-10728.
23. Clem, I.W.; De, B.F.; Sigel, M.M. Phylogeny of immunoglobulin structure and function. II. Immunoglobulins of the nurse shark. J. Immunol. 1967, 99, 1226-1235.
24. Dooley, H.; Flajnik, M.F. Shark immunity bites back: Affinity maturation and memory response in the nurse shark, Ginglymostoma cirratum. Eur. J. Immunol. 2005, 35, 936-945.
25. Small, P.A., Jr.; Klapper, D.G.; Clem, L.W. Half-lives, body distribution and lack of interconversion of serum 19S and 7S IgM of sharks. J. Immunol. 1970, 105, 29-37.
26. Castro, C.D.; Ohta, Y.; Dooley, H.; Flajnik, M.F. Noncoordinate expression of J-chain and Blimp-1 define nurse shark plasma cell populations during ontogeny. Eur. J. Immunol. 2013, 43, 3061-3075.
27. Hohman, V.S.; Stewart, S.E.; Rumfelt, L.L.; Greenberg, A.S.; Avila, D.W.; Flajnik, M.F.; Steiner, L.A. J chain in the nurse shark: Implications for function in a lower vertebrate. J. Immunol. 2003, 170, 6016-6023.
28. Flajnik, M.F; Hsu, E. Department of Microbiology & Immunology, University of Maryland School of Medicine, Baltimore, MD, USA. Unpublished work. 2001.
29. Greenberg, A.S.; Hughes, A.L.; Guo, J.; Avila, D.; McKinney, E.C.; Flajnik, M.F. A novel "chimeric" antibody class in cartilaginous fish: IgM may not be the primordial immunoglobulin. Eur. J. Immunol. 1996, 26, 1123-1129.
30. Anderson, M.K.; Strong, S.J.; Litman, R.T.; Luer, C.A.; Amemiya, C.T.; Rast, J.P.; Litman, G.W. A long form of the skate IgX gene exhibits a striking resemblance to the new shark IgW and IgNARC genes. Immunogenetics 1999, 49, 56-67.
31. Kobayashi, K.; Tomonaga, S. The second immunoglobulin class is commonly present in cartilaginous fish belonging to the order Rajiformes. Mol. Immunol. 1988, 25, 115-120.
32. Rumfelt, L.L.; Diaz, M.; Lohr, R.L.; Mochon, E.; Flajnik, M.F. Unprecedented multiplicity of Ig transmembrane and secretory mRNA forms in the cartilaginous fish. J. Immunol. 2004, 173, 1129-1139.
33. Smith, L.E.; Crouch, K.; Cao, W.; Muller, M.R.; Wu, L.; Steven, J.; Lee, M.; Liang, M.; Flajnik, M.F.; Shih, H.H.; et al. Characterization of the immunoglobulin repertoire of the spiny dogfish (Squalus acanthias). Dev. Comp. Immunol. 2012, 36, 665-679.
34. Zhang, C.; du Pasquier, L.; Hsu, E. Shark IgW C region diversification through RNA processing and isotype switching. J. Immunol. 2013, 191, 3410-3418.
35. Eason, D.D.; Litman, R.T.; Luer, C.A.; Kerr, W.; Litman, G.W. Expression of individual immunoglobulin genes occurs in an unusual system consisting of multiple independent loci. Eur. J. Immunol. 2004, 34, 2551-2558.
36. 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 1995, 374, 168-173.
37. Stanfield, R.L.; Dooley, H.; Flajnik, M.F.; Wilson, I.A. Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 2004, 305, 1770-1773.
38. Criscitiello, M.F.; Saltis, M.; Flajnik, M.F. An evolutionarily mobile antigen receptor variable region gene: Doubly rearranging NAR-TcR genes in sharks. Proc. Natl. Acad. Sci. USA 2006, 103, 5036-5041.
39. Diaz, M.; Greenberg, A.S.; Flajnik, M.F. Somatic hypermutation of the new antigen receptor gene (NAR) in the nurse shark does not generate the repertoire: Possible role in antigen-driven reactions in the absence of germinal centers. Proc. Natl. Acad. Sci. USA 1998, 95, 14343-14348.
40. 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.; et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 2014, 505, 174-179.
41. Fidler, J.E.; Clem, L.W.; Small, P.A., Jr. Immunoglobulin synthesis in neonatal nurse sharks (Ginglymostoma cirratum). Comp. Biochem. Physiol. 1969, 31, 365-371.
42. Rumfelt, L.L.; McKinney, E.C.; Taylor, E.; Flajnik, M.F. The development of primary and secondary lymphoid tissues in the nurse shark Ginglymostoma cirratum: B-cell zones precede dendritic cell immigration and T-cell zone formation during ontogeny of the spleen. Scand. J. Immunol. 2002, 56, 130-148.
43. Dooley, H.; Flajnik, M.F. School of Biological Sciences, University of Aberdeen, Aberdeen, UK. Unpublished work. 2005.
44. Roux, K.H.; Greenberg, A.S.; Greene, L.; Strelets, L.; Avila, D.; McKinney, E.C.; Flajnik, M.F. Structural analysis of the nurse shark (new) antigen receptor (NAR): Molecular convergence of NAR and unusual mammalian immunoglobulins. Proc. Natl. Acad. Sci. USA 1998, 95, 11804-11809.
45. Crouch, K.; Smith, L.E.; Williams, R.; Cao, W.; Lee, M.; Jensen, A.; Dooley, H. Humoral immune response of the small-spotted catshark, Scyliorhinus canicula. Fish Shellfish Immunol. 2013, 34, 1158-1169.
46. Dooley, H.; Flajnik, M.F. School of Biological Sciences, University of Aberdeen, Aberdeen, UK. Unpublished work. 2004.
47. Lee, S.S.; Tranchina, D.; Ohta, Y.; Flajnik, M.F.; Hsu, E. Hypermutation in shark immunoglobulin light chain genes results in contiguous substitutions. Immunity 2002, 16, 571-582.
48. Diaz, M.; Velez, J.; Singh, M.; Cerny, J.; Flajnik, M.F. Mutational pattern of the nurse shark antigen receptor gene (NAR) is similar to that of mammalian Ig genes and to spontaneous mutations in evolution: The translesion synthesis model of somatic hypermutation. Int. Immunol. 1999, 11, 825-833.
49. Flajnik, M.F. Comparative analyses of immunoglobulin genes: Surprises and portents. Nat. Rev. Immunol. 2002, 2, 688-698.
50. Sunyer, J.O. Fishing for mammalian paradigms in the teleost immune system. Nat. Immunol. 2013, 14, 320-326.
51. Kaattari, S.; Evans, D.; Klemer, J. Varied redox forms of teleost IgM: An alternative to isotypic diversity? Immunol. Rev. 1998 166, 133-142.
52. Ye, J.; Bromage, E.; Kaattari, I.; Kaattari, S. Transduction of binding affinity by B lymphocytes: A new dimension in immunological regulation. Dev. Comp. Immunol. 2011, 35, 982-990.
53. Cain, K.D.; Jones, D.R.; Raison, R.L. Antibody-antigen kinetics following immunization of rainbow trout (Oncorhynchus mykiss) with a T-cell dependent antigen. Dev. Comp. Immunol. 2002, 26, 181-190.
54. Kaattari, S.L.; Zhang, H.L.; Khor, I.W.; Kaattari, I.M.; Shapiro, D.A. Affinity maturation in trout: Clonal dominance of high affinity antibodies late in the immune response. Dev. Comp. Immunol. 2002, 26, 191-200.
55. Ye, J.; Kaattari, I.M.; Ma, C.; Kaattari, S. The teleost humoral immune response. Fish Shellfish Immunol. 2013, 35, 1719-1728.
56. Wilson, M.; Bengten, 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. USA 1997, 94, 4593-4597.
57. + B cell populations in channel catfish, Ictalurus punctatus. J. Immunol. 2010, 185, 4082-4094.
58. Castro, R.; Bromage, E.; Abos, B.; Pignatelli, J.; Gonzalez, G.A.; Luque, A.; Tafalla, C. CCR7 is mainly expressed in teleost gills, where it defines an IgD+IgM- B lymphocyte subset. J. Immunol. 2014, 192, 1257-1266.
59. + B cell subset with phenotypical and functional characteristics of germinal center B cells. Eur. J. Immunol. 1996, 26, 1712-1719.
60. Edholm, E.S.; Bengten, E.; Wilson, M. Insights into the function of IgD. Dev. Comp. Immunol. 2011, 35, 1309-1316.
61. Ramirez-Gomez, F.; Greene, W.; Rego, K.; Hansen, J.D.; Costa, G.; Kataria, P.; Bromage, E.S. Discovery and characterization of secretory IgD in rainbow trout: Secretory IgD is produced through a novel splicing mechanism. J. Immunol. 2012, 188, 1341-1349.
62. Chen, K.; Xu, W.; Wilson, M.; He, B.; Miller, N.W.; Bengten, E.; Edholm, E.S.; Santini, P.A.; Rath, P.; Chiu, A.; et al. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils. Nat. Immunol. 2009, 10, 889-898.
63. Hansen, J.D.; Landis, E.D.; Phillips, R.B. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. Proc. Natl. Acad. Sci. USA 2005, 102, 6919-6924.
64. Danilova, N.; Bussmann, J.; Jekosch, K.; Steiner, L.A. The immunoglobulin heavy-chain locus in zebrafish: Identification and expression of a previously unknown isotype, immunoglobulin Z. Nat. Immunol. 2005, 6, 295-302.
65. Flajnik, M.F. All GOD’s creatures got dedicated mucosal immunity. Nat. Immunol. 2010, 11, 777-779.
66. Fillatreau, S.; Six, A.; Magadan, S.; Castro, R.; Sunyer, J.O.; Boudinot, P. The astonishing diversity of Ig classes and B cell repertoires in teleost fish. Front. Immunol. 2013, doi: 10.3389/fimmu.2013.00028.
67. 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. 2010, 11, 827-835.
68. Xu, Z.; Parra, D.; Gomez, D.; Salinas, I.; Zhang, Y.A.; von Gersdorff, J.L.; Heinecke, R.D.; Buchmann, K.; Lapatra, S.; Sunyer, J.O.; et al. Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proc. Natl. Acad. Sci. USA 2013, 110, 13097-13102.
69. 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. USA 2003, 100, 2501-2506.
70. Zhang, T.; Tacchi, L.; Wei, Z.; Zhao, Y.; Salinas, I. Intraclass diversification of immunoglobulin heavy chain genes in the African lungfish. Immunogenetics 2014, 66, 335-351.
71. Edholm, E.S.; Wilson, M.; Bengten, E. Immunoglobulin light (IgL) chains in ectothermic vertebrates. Dev. Comp. Immunol. 2011, 35, 906-915.
72. Edholm, E.S.; Wilson, M.; Sahoo, M.; Miller, N.W.; Pilstrom, L.; Wermenstam, N.E.; Bengten, E. Identification of Igsigma and Iglambda in channel catfish, Ictalurus punctatus, and Iglambda in Atlantic cod, Gadus morhua. Immunogenetics 2009, 61, 353-370.
73. Solem, S.T.; Stenvik, J. Antibody repertoire development in teleosts-A review with emphasis on salmonids and Gadus morhua L. Dev. Comp. Immunol. 2006, 30, 57-76.
74. Magnadottir, B.; Gudmundsdottir, S.; Gudmundsdottir, B.K.; Helgason, S. Natural antibodies of cod (Gadus morhua L.): Specificity, activity and affinity. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 154, 309-316.
75. Star, B.; Nederbragt, A.J.; Jentoft, S.; Grimholt, U.; Malmstrom, M.; Gregers, T.F.; Rounge, T.B.; Paulsen, J.; Solbakken, M.H.; Sharma, A.; et al. The genome sequence of Atlantic cod reveals a unique immune system. Nature 2011, 477, 207-210.
76. Malmstrom, 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 2013, 8, e74004.
77. Zhao, Y.; Pan-Hammarstrom, Q.; Yu, S.; Wertz, N.; Zhang, X.; Li, N.; Butler, J.E.; Hammarstrom, L. Identification of IgF, a hinge-region-containing Ig class, and IgD in Xenopus tropicalis. Proc. Natl. Acad. Sci. USA 2006, 103, 12087-12092.
78. Wei, Z.; Wu, Q.; Ren, L.; Hu, X.; Guo, Y.; Warr, G.W.; Hammarstrom, L.; Li, N.; Zhao, Y. Expression of IgM, IgD, and IgY in a reptile, Anolis carolinensis. J. Immunol. 2009, 183, 3858-3864.
79. Magadan-Mompo, S.; Sanchez-Espinel, C.; Gambon-Deza, F. Immunoglobulin genes of the turtles. Immunogenetics 2013, 65, 227-237.
80. Magadan-Mompo, S.; Sanchez-Espinel, C.; Gambon-Deza, F. IgH loci of American alligator and saltwater crocodile shed light on IgA evolution. Immunogenetics 2013, 65, 531-541.
81. Zhao, Y.; Rabbani, H.; Shimizu, A.; Hammarstrom, L. Mapping of the chicken immunoglobulin heavy-chain constant region gene locus reveals an inverted alpha gene upstream of a condensed upsilon gene. Immunology 2000, 101, 348-353.
82. Weinstein, J.A.; Jiang, N.; White, R.A., III; Fisher, D.S.; Quake, S.R. High-throughput sequencing of the zebrafish antibody repertoire. Science 2009, 324, 807-810.
83. Yasuike, M.; de Boer, J.; von Schalburg, K.R.; Cooper, G.A.; McKinnel, L.; Messmer, A.; So, S.; Davidson, W.S.; Koop, B.F. Evolution of duplicated IgH loci in Atlantic salmon, Salmo salar. BMC Genomics 2010, doi: 10.1186/1471-2164-11-486.
84. Castro, R.; Jouneau, L.; Pham, H.P.; Bouchez, O.; Giudicelli, V.; Lefranc, M.P.; Quillet, E.; Benmansour, A.; Cazals, F.; Six, A.; et al. Teleost fish mount complex clonal IgM and IgT responses in spleen upon systemic viral infection. PLoS Pathog. 2013, 9, e1003098.
85. Ye, J.; Kaattari, I.M.; Kaattari, S.L. The differential dynamics of antibody subpopulation expression during affinity maturation in a teleost. Fish Shellfish Immunol. 2011, 30, 372-377.
86. Yang, F.; Waldbieser, G.C.; Lobb, C.J. The nucleotide targets of somatic mutation and the role of selection in immunoglobulin heavy chains of a teleost fish. J. Immunol. 2006, 176, 1655-1667.
87. Zhao, Y.; Pan-Hammarstrom, Q.; Zhao, Z.; Hammarstrom, L. Identification of the activation-induced cytidine deaminase gene from zebrafish: An evolutionary analysis. Dev. Comp. Immunol. 2005, 29, 61-71.
88. Barreto, V.M.; Pan-Hammarstrom, Q.; Zhao, Y.; Hammarstrom, L.; Misulovin, Z.; Nussenzweig, M.C. AID from bony fish catalyzes class switch recombination. J. Exp. Med. 2005, 202, 733-738.
89. Wakae, K.; Magor, B.G.; Saunders, H.; Nagaoka, H.; Kawamura, A.; Kinoshita, K.; Honjo, T.; Muramatsu, M. Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID. Int. Immunol. 2006, 18, 41-47.
90. Steiner, L.A.; Mikoryak, C.A.; Lopes, A.D.; Green, C. Immunoglobulins in ranid frogs and tadpoles. Adv. Exp. Med. Biol. 1975, 64, 173-183.
91. Hadji-Azimi, I. Structural studies of the Xenopus 19S immunoglobulin and 7S immunoglobulin and two immunoglobulin-like proteins. Immunology 1975, 28, 419-429.
92. Qin, T.; Ren, L.; Hu, X.; Guo, Y.; Fei, J.; Zhu, Q.; Butler, J.E.; Wu, C.; Li, N.; Hammarstrom, L.; et al. Genomic organization of the immunoglobulin light chain gene loci in Xenopus tropicalis: Evolutionary implications. Dev. Comp. Immunol. 2008, 32, 156-165.
93. Du Pasquier, L.; Schwager, J.; Flajnik, M.F. The immune system of Xenopus. Annu. Rev. Immunol. 1989, 7, 251-275.
94. Hsu, E.; Flajnik, M.F.; du Pasquier, L. A third immunoglobulin class in amphibians. J. Immunol. 1985, 135, 1998-2004.
95. Zhu, R.; Chen, Z.Y.; Wang, J.; Yuan, J.D.; Liao, X.Y.; Gui, J.F.; Zhang, Q.Y. Thymus cDNA library survey uncovers novel features of immune molecules in Chinese giant salamander Andrias davidianus. Dev. Comp. Immunol. 2014, 46, 413-422.
96. Mussmann, R.; du Pasquier, L.; Hsu, E. Is Xenopus IgX an analog of IgA? Eur. J. Immunol. 1996, 26, 2823-2830.
97. Du, C.C.; Mashoof, S.M.; Criscitiello, M.F. Oral immunization of the African clawed frog (Xenopus laevis) upregulates the mucosal immunoglobulin IgX. Vet. Immunol. Immunopathol. 2012, 145, 493-498.
98. Macpherson, A.J.; Gatto, D.; Sainsbury, E.; Harriman, G.R.; Hengartner, H.; Zinkernagel, R.M. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000, 288, 2222-2226.
99. Mansikka, A. Chicken IgA H chains. Implications concerning the evolution of H chain genes. J. Immunol. 1992, 149, 855-861.
100. Marchalonis, J.; Edelman, G.M. Phylogenetic origins of antibody structure II. Immunoglobulins in the primary immune response of the bullfrog, Rana catesbiana. J. Exp. Med. 1966, 124, 901-913.
101. Schaerlinger, B.; Frippiat, J.P. IgX antibodies in the urodele amphibian Ambystoma mexicanum. Dev. Comp. Immunol. 2008, 32, 908-915.
102. Fellah, J.S.; Iscaki, S.; Vaerman, J.P.; Charlemagne, J. Transient developmental expression of IgY and secretory component like protein in the gut of the axolotl (Ambystoma mexicanum). Dev. Immunol. 1992, 2, 181-190.
103. Schaerlinger, B.; Bascove, M.; Frippiat, J.P. A new isotype of immunoglobulin heavy chain in the urodele amphibian Pleurodeles waltl predominantly expressed in larvae. Mol. Immunol. 2008, 45, 776-786.
104. Das, S.; Nikolaidis, N.; Klein, J.; Nei, M. Evolutionary redefinition of immunoglobulin light chain isotypes in tetrapods using molecular markers. Proc. Natl. Acad. Sci. USA 2008, 105, 16647-16652.
105. Mussmann, R.; Courtet, M.; Schwager, J.; du Pasquier, L. Microsites for immunoglobulin switch recombination breakpoints from Xenopus to mammals. Eur. J. Immunol. 1997, 27, 2610-2619.
106. Zarrin, A.A.; Alt, F.W.; Chaudhuri, J.; Stokes, N.; Kaushal, D.; du Pasquier, L.; Tian, M. An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nat. Immunol. 2004, 5, 1275-1281.
107. Du Pasquier, L.; Robert, J.; Courtet, M.; Mussmann, R. B-cell development in the amphibian Xenopus. Immunol. Rev. 2000, 175, 201-213.
108. Poorten, T.J.; Kuhn, R.E. Maternal transfer of antibodies to eggs in Xenopus laevis. Dev. Comp. Immunol. 2009, 33, 171-175.
109. Marr, S.; Morales, H.; Bottaro, A.; Cooper, M.; Flajnik, M.; Robert, J. Localization and differential expression of activation-induced cytidine deaminase in the amphibian Xenopus upon antigen stimulation and during early development. J. Immunol. 2007, 179, 6783-6789.
110. Wilson, M.; Hsu, E.; Marcuz, A.; Courtet, M.; du Pasquier, L.; Steinberg, C. What limits affinity maturation of antibodies in Xenopus-The rate of somatic mutation or the ability to select mutants? EMBO J. 1992, 11, 4337-4347.
111. Ramsey, J.P.; Reinert, L.K.; Harper, L.K.; Woodhams, D.C.; Rollins-Smith, L.A. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 2010, 78, 3981-3992.
112. Patel, H.M.; Hsu, E. Abbreviated junctional sequences impoverish antibody diversity in urodele amphibians. J. Immunol. 1997, 159, 3391-3399.
113. Frippiat, J.P. Contribution of the urodele amphibian Pleurodeles waltl to the analysis of spaceflight-associated immune system deregulation. Mol. Immunol. 2013, 56, 434-441.
114. Janes, D.E.; Organ, C.L.; Fujita, M.K.; Shedlock, A.M.; Edwards, S.V. Genome evolution in Reptilia, the sister group of mammals. Annu. Rev. Genomics Hum. Genet. 2010, 11, 239-264.
115. Marchalonis, J.J.; Ealey, E.H.; Diener, E. Immune response of the tuatara, Sphenodon punctatum. Aust. J. Exp. Biol. Med. Sci. 1969, 47, 367-380.
116. Gambon-Deza, F.; Sanchez-Espinel, C.; Mirete-Bachiller, S.; Magadan-Mompo, S. Snakes antibodies. Dev. Comp. Immunol. 2012, 38, 1-9.
117. Gambon, D.F.; Sanchez, E.C.; Magadan, M.S. The immunoglobulin heavy chain locus in the reptile Anolis carolinensis. Mol. Immunol. 2009, 46, 1679-1687.
118. Das, S.; Hirano, M.; Tako, R.; McCallister, C.; Nikolaidis, N. Evolutionary genomics of immunoglobulin-encoding Loci in vertebrates. Curr. Genomics 2012, 13, 95-102.
119. Turchin, A.; Hsu, E. The generation of antibody diversity in the turtle. J. Immunol. 1996, 156, 3797-3805.
120. Natarajan, K.; Muthukkaruppan, V.R. Immunoglobulin classes in the garden lizard, Calotes versicolor. Dev. Comp. Immunol. 1984, 8, 845-854.
121. Cheng, G.; Gao, Y.; Wang, T.; Sun, Y.; Wei, Z.; Li, L.; Ren, L.; Guo, Y.; Hu, X.; Lu, Y.; et al. Extensive diversification of IgH subclass-encoding genes and IgM subclass switching in crocodilians. Nat. Commun. 2013, doi: 10.1038/ncomms2317.
122. Leslie, G.A.; Clem, L.W. Phylogeny of immunoglobulin structure and function. VI. 17S, 7.5S and 5.7S anti-DNP of the turtle, Pseudamys scripta. J. Immunol. 1972, 108, 1656-1664.
123. Gambon-Deza, F.; Espinel, C.S. IgD in the reptile leopard gecko. Mol. Immunol. 2008, 45, 3470-3476.
124. Iwata, A.; Iwase, T.; Ogura, Y.; Takahashi, T.; Matsumoto, N.; Yoshida, T.; Kamei, N.; Kobayashi, K.; Mestecky, J.; Moro, I.; et al. Cloning and expression of the turtle (Trachemys scripta) immunoglobulin joining (J)-chain cDNA. Immunogenetics 2002, 54, 513-519.
125. Li, L.; Wang, T.; Sun, Y.; Cheng, G.; Yang, H.; Wei, Z.; Wang, P.; Hu, X.; Ren, L.; Meng, Q.; et al. Extensive diversification of IgD-, IgY-, and truncated IgY(deltaFc)-encoding genes in the red-eared turtle (Trachemys scripta elegans). J. Immunol. 2012, 189, 3995-4004.
126. Magor, K.E.; Higgins, D.A.; Middleton, D.L.; Warr, G.W. One gene encodes the heavy chains for three different forms of IgY in the duck. J. Immunol. 1994, 153, 5549-5555.
127. Humphrey, B.D.; Calvert, C.C.; Klasing, K.C. The ratio of full length IgY to truncated IgY in immune complexes affects macrophage phagocytosis and the acute phase response of mallard ducks (Anas platyrhynchos). Dev. Comp. Immunol. 2004, 28, 665-672.
128. Xu, Z.; Wang, G.L.; Nie, P. IgM, IgD and IgY and their expression pattern in the Chinese soft-shelled turtle Pelodiscus sinensis. Mol. Immunol. 2009, 46, 2124-2132.
129. Deza, F.G.; Espinel, C.S.; Beneitez, J.V. A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev. Comp. Immunol. 2007, 31, 596-605.
130. Wu, Q.; Wei, Z.; Yang, Z.; Wang, T.; Ren, L.; Hu, X.; Meng, Q.; Guo, Y.; Zhu, Q.; Robert, J.; et al. Phylogeny, genomic organization and expression of lambda and kappa immunoglobulin light chain genes in a reptile, Anolis carolinensis. Dev. Comp. Immunol. 2010, 34, 579-589.
131. Work, T.M.; Balazs, G.H.; Rameyer, R.A.; Chang, S.P.; Berestecky, J. Assessing humoral and cell-mediated immune response in Hawaiian green turtles, Chelonia mydas. Vet. Immunol. Immunopathol. 2000, 74, 179-194.
132. Grey, H.M. Phylogeny of the immune response. Studies on some physical chemical and serologic characteristics of antibody produced in the turtle. J. Immunol. 1963, 91, 819-825.
133. Cooper, E.L.; Klempau, A.E.; Zapata, A.G. Introduction to reptilian immunity. In Biology of the Reptilia;.Gans, C., Billett, F., Maderson, P.F.A., Eds.; John Wiley & Sons: New York, NY, USA, 1985; Volume 14, pp. 601-678.
134. Marschang, R.E.; Gravendyck, M.; Kaleta, E.F. Herpesviruses in tortoises: Investigations into virus isolation and the treatment of viral stomatitis in Testudo hermanni and T. graeca. Zentralbl Veterinarmed B 1997, 44, 385-394.
135. Merchant, M.E.; Roche, C.; Elsey, R.M.; Prudhomme, J. Antibacterial properties of serum from the American alligator (Alligator mississippiensis). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2003, 136, 505-513.
136. Pasmans, F.; Herdt, P.D.; Nerom, A.V.; Haesebrouck, F. Induction of the respiratory burst in turtle peritoneal macrophages by Salmonella muenchen. Dev. Comp. Immunol. 2001, 25, 159-168.
137. Cone, R.E.; Marchalonis, J.J. Cellular and humoral aspects of the influence of environmental temperature on the immune response of poikilothermic vertebrates. J. Immunol. 1972, 108, 952-957.
138. Zapata, A.G.; Varas, A.; Torroba, M. Seasonal variations in the immune system of lower vertebrates. Immunol. Today 1992, 13, 142-147.
139. Flajnik, M.F. Re-evaluation of the immunological Big Bang. Curr. Biol. 2014, 24, R1060-R1065.
140. Mestas, J.; Hughes, C.W. Of mice and not men: Differences between mouse and human immunology. J. Immunol. 2004, 172, 2731-2738.