Skip to main content

Advertisement

SpringerLink
Log in

Diversity of Immunoglobulin (Ig) Isotypes and the Role of Activation-Induced Cytidine Deaminase (AID) in Fish

  • Review
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

The disparate diversity in immunoglobulin (Ig) repertoire has been a subject of fascination since the emergence of prototypic adaptive immune system in vertebrates. The carboxy terminus region of activation-induced cytidine deaminase (AID) has been well established in tetrapod lineage and is crucial for its function in class switch recombination (CSR) event of Ig diversification. The absence of CSR in the paraphyletic group of fish is probably due to changes in catalytic domain of AID and lack of cis-elements in IgH locus. Therefore, understanding the arrangement of Ig genes in IgH locus and functional facets of fish AID opens up new realms of unravelling the alternative mechanisms of isotype switching and antibody diversity. Further, the teleost AID has been recently reported to have potential of catalyzing CSR in mammalian B cells by complementing AID deficiency in them. In that context, the present review focuses on the recent advances regarding the generation of diversity in Ig repertoire in the absence of AID-regulated class switching in teleosts and the possible role of T cell-independent pathway involving B cell activating factor and a proliferation-inducing ligand in activation of CSR machinery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

VLRs:

Variable lymphocyte receptors

Ig:

Immunoglobulin

SHM:

Somatic hypermutation

CSR:

Class-switch recombination

GC:

Gene conversion

AID:

Activation-induced cytidine deaminase

APOBEC:

Apolipoprotein B mRNA-editing catalytical component

BAFF:

B cell activating factor

APRIL:

A proliferation-inducing ligand

TLR:

Toll-like receptors

TNF:

Tumour necrosis factor

NF-κB:

Nuclear factor-κB

MHC:

Major histocompatibility complex

MDM2:

Mouse double minute 2 homolog

LPS:

Lipopolysaccharide

References

  1. Laird, D. J., De Tomaso, A. W., Cooper, M. D., & Weissman, I. L. (2000). 50 million years of chordate evolution: Seeking the origins of adaptive immunity. Proceedings of the National Academy of Sciences, 97, 6924–6926.

    Article  CAS  Google Scholar 

  2. Pancer, Z., Amemiya, C. T., Ehrhardt, G. R., Ceitlin, J., Gartland, G. L., & Cooper, M. D. (2004). Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature, 430, 174–180.

    Article  PubMed  CAS  Google Scholar 

  3. Cooper, M. D., & Alder, M. N. (2006). The evolution of adaptive immune systems. Cell, 124, 815–822.

    Article  PubMed  CAS  Google Scholar 

  4. Guo, P., Hirano, M., Herrin, B. R., Li, J., Yu, C., Sadlonova, A., et al. (2009). Dual nature of the adaptive immune system in lampreys. Nature, 459, 796–801.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Flajnik, M. F. (2002). Comparative analyses of immunoglobulin genes: Surprises and portents. Nature Reviews Immunology, 2, 688–698.

    Article  PubMed  CAS  Google Scholar 

  6. Sunyer, J. O. (2013). Fishing for mammalian paradigms in the teleost immune system. Nature Immunology, 14, 320–326.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Senger, K., Hackney, J., Payandeh, J., & Zarrin, A. A. (2015). Antibody isotype switching in vertebrates. In E. Hsu & L. D. Pasquier (Eds.), Pathogen–host interactions: antigenic variation v. somatic adaptations (pp. 295–324). Berlin: Springer.

    Chapter  Google Scholar 

  8. Hsu, E. (2016). Assembly and expression of shark Ig genes. The Journal of Immunology, 196, 3517–3523.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Poole, J. R. M., Paganini, J., & Pontarotti, P. (2017). Convergent evolution of the adaptive immune response in jawed vertebrates and cyclostomes: An evolutionary biology approach based study. Developmental & Comparative Immunology. https://doi.org/10.1016/j.dci.2017.02.011.

    Article  Google Scholar 

  10. Burnet, F. M. (1957). A modification of Jerne’s theory of antibody production using the concept of clonal selection. The Australian Journal of Science, 20, 67–69.

    Google Scholar 

  11. Hodgkin, P. D., Heath, W. R., & Baxter, A. G. (2007). The clonal selection theory: 50 years since the revolution. Nature Immunology, 8, 1019–1026.

    Article  PubMed  CAS  Google Scholar 

  12. Brack, C., Hirama, M., Lenhard-Schuller, R., & Tonegawa, S. (1978). A complete immunoglobulin gene is created by somatic recombination. Cell, 15, 1–14.

    Article  PubMed  CAS  Google Scholar 

  13. Seidman, J. G., Leder, A., Edgell, M. H., Polsky, F., Tilghman, S. M., Tiemeier, D. C., et al. (1978). Multiple related immunoglobulin variable-region genes identified by cloning and sequence analysis. Proceedings of the National Academy of Sciences of the United States of America, 75, 3881–3885.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Weigert, M. G., Cesari, I. M., Yonkovich, S. J., & Cohn, M. (1970). Variability in the lambda light chain sequences of mouse antibody. Nature, 228, 1045–1047.

    Article  PubMed  CAS  Google Scholar 

  15. Schilling, J., Clevinger, B., Davie, J. M., & Hood, L. (1980). Amino acid sequence of homogeneous antibodies to dextran and DNA rearrangments in heavy chain V-region gene segments. Nature, 283, 35–40.

    Article  PubMed  CAS  Google Scholar 

  16. Tonegawa, S. (1983). Somatic generation of antibody diversity. Nature, 302, 575–581.

    Article  PubMed  CAS  Google Scholar 

  17. Oettinger, M. A., Schatz, D. G., Gorka, C., & Baltimore, D. (1990). RAG-1 and RAG-2, adjacent genes that synergistically activate V (D) J recombination. Science, 248, 1517–1523.

    Article  PubMed  CAS  Google Scholar 

  18. Bassing, C. H., Swat, W., & Alt, F. W. (2002). The mechanism and regulation of chromosomal V (D) J recombination. Cell, 109, S45–S55.

    Article  PubMed  CAS  Google Scholar 

  19. Gellert, M. (2002). V(D)J recombination: RAG proteins, repair factors, and regulation. Annual Review of Biochemistry, 71, 101–132.

    Article  PubMed  CAS  Google Scholar 

  20. Kataoka, T., Kawakami, T., Takahashi, N., & Honjo, T. (1980). Rearrangement of immunoglobulin gamma 1-chain gene and mechanism for heavy-chain class switch. Proceedings of the National Academy of Sciences of the United States of America, 77, 919–923.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Reynaud, C. A., Anquez, V., Grimal, H., & Weill, J. C. (1987). A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell, 48, 379–388.

    Article  PubMed  CAS  Google Scholar 

  22. Reynaud, C. A., Mackay, C. R., Müller, R. G., & Weill, J. C. (1991). Somatic generation of diversity in a mammalian primary lymphoid organ: The sheep ileal Peyer’s patches. Cell, 64, 995–1005.

    Article  PubMed  CAS  Google Scholar 

  23. Litman, G. W., Rast, J. P., & Fugmann, S. D. (2010). The origins of vertebrate adaptive immunity. Nature Reviews Immunology, 10, 543–553.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Arakawa, H., Saribasak, H., & Buerstedde, J. M. (2004). Activation-induced cytidine deaminase initiates immunoglobulin gene conversion and hypermutation by a common intermediate. PLoS Biology, 2, 0967–0971.

    Article  Google Scholar 

  25. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., & Honjo, T. (2000). Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell, 102, 553–563.

    Article  PubMed  CAS  Google Scholar 

  26. Stavnezer, J., & Amemiya, C. T. (2004). Evolution of isotype switching. Seminars in Immunology, 16(4), 257–275.

    Article  PubMed  CAS  Google Scholar 

  27. Wakae, K., Magor, B. G., Saunders, H., Nagaoka, H., Kawamura, A., Kinoshita, K., et al. (2006). Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID. International Immunology, 18, 41–47.

    Article  PubMed  CAS  Google Scholar 

  28. Barreto, V. M., Pan-Hammarstrom, Q., Zhao, Y., Hammarstrom, L., Misulovin, Z., & Nussenzweig, M. C. (2005). AID from bony fish catalyzes class switch recombination. The Journal of Experimental Medicine, 202, 733–738.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Wilson, M., Bengtén, E., Miller, N. W., Clem, L. W., Du Pasquier, L., & Warr, G. W. (1997). A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proceedings of the National Academy of Sciences of the United States of America, 94, 4593–4597.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Flajnik, M. F., & Rumfelt, L. L. (2000). The immune system of cartilaginous fish. In L. Du Pasquier & G. W. Litman (Eds.), Origin and evolution of the vertebrate immune system (pp. 249–270). Berlin: Springer.

    Chapter  Google Scholar 

  31. Dooley, H., & Flajnik, M. F. (2006). Antibody repertoire development in cartilaginous fish. Developmental & Comparative Immunology, 30, 43–56.

    Article  CAS  Google Scholar 

  32. Danilova, N., Bussmann, J., Jekosch, K., & Steiner, L. A. (2005). The immunoglobulin heavy-chain locus in zebrafish: Identification and expression of a previously unknown isotype, immunoglobulin Z. Nature Immunology, 6, 295–302.

    Article  PubMed  CAS  Google Scholar 

  33. Zhang, Y. A., Salinas, I., Li, J., Parra, D., Bjork, S., Xu, Z., et al. (2010). IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nature Immunology, 11, 827–835.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Patel, B., Banerjee, R., Basu, M., Lenka, S., Samanta, M., & Das, S. (2016). Molecular cloning of IgZ heavy chain isotype in Catla catla and comparative expression profile of IgZ and IgM following pathogenic infection. Microbiology and Immunology, 60, 561–567.

    Article  PubMed  CAS  Google Scholar 

  35. Basu, M., Lenka, S. S., Paichha, M., Swain, B., Patel, B., Banerjee, R., et al. (2016). Immunoglobulin (Ig) D in Labeo rohita is widely expressed and differentially modulated in viral, bacterial and parasitic challenges. Veterinary Immunology and Immunopathology, 179, 77–84.

    Article  PubMed  CAS  Google Scholar 

  36. Castigli, E., Fuleihan, R., Ramesh, N., Tsitsikov, E., Tsytsykova, A., & Geha, R. S. (1995). CD40 ligand/CD40 deficiency. International Archives of Allergy and Immunology, 107, 37–39.

    Article  PubMed  CAS  Google Scholar 

  37. Stavnezer, J. (1996). Immunoglobulin class switching. Current Opinion in Immunology, 8, 199–205.

    Article  PubMed  CAS  Google Scholar 

  38. Geha, R. S., Jabara, H. H., & Brodeur, S. R. (2003). The regulation of immunoglobulin E class-switch recombination. Nature Reviews Immunology, 3, 721–732.

    Article  PubMed  CAS  Google Scholar 

  39. Litinskiy, M. B., Nardelli, B., Hilbert, D. M., He, B., Schaffer, A., Casali, P., et al. (2002). DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nature Immunology, 3, 822–829.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Basu, M., Lenka, S. S., Paichha, M., Patel, B., Banerjee, R., Das, S., et al. (2016). B cell activating factor is induced by toll-like receptor and NOD-like receptor ligands and plays critical role in IgM synthesis in Labeo rohita. Molecular Immunology, 78, 9–26.

    Article  PubMed  CAS  Google Scholar 

  41. Ramakrishnan, P., Wang, W., & Wallach, D. (2004). Receptor-specific signaling for both the alternative and the canonical NF-κB activation pathways by NF-κB-inducing kinase. Immunity, 21, 477–489.

    Article  PubMed  CAS  Google Scholar 

  42. Arakawa, H., Hauschild, J., & Buerstedde, J. M. (2002). Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science, 295, 1301–1306.

    Article  PubMed  CAS  Google Scholar 

  43. Honjo, T., Kinoshita, K., & Muramatsu, M. (2002). Molecular mechanism of class switch recombination: Linkage with somatic hypermutation. Annual Review of Immunology, 20, 165–196.

    Article  PubMed  CAS  Google Scholar 

  44. Harris, R. S., Sale, J. E., Petersen-Mahrt, S. K., & Neuberger, M. S. (2002). AID is essential for immunoglobulin V gene conversion in a cultured B cell line. Current Biology, 12, 435–438.

    Article  PubMed  CAS  Google Scholar 

  45. Delker, R. K., Fugmann, S. D., & Papavasiliou, F. N. (2009). A coming-of-age story: Activation-induced cytidine deaminase turns 10. Nature Immunology, 10, 1147–1153.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Gitlin, A. D., von Boehmer, L., Gazumyan, A., Shulman, Z., Oliveira, T. Y., & Nussenzweig, M. C. (2016). Independent roles of switching and hypermutation in the development and persistence of B lymphocyte memory. Immunity, 44, 769–781.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Parng, C. L., Hansal, S., Goldsby, R. A., & Osborne, B. A. (1996). Gene conversion contributes to Ig light chain diversity in cattle. The Journal of Immunology, 157, 5478–5486.

    PubMed  CAS  Google Scholar 

  48. Weinstein, P. D., Anderson, A. O., & Maget, R. G. (1994). Rabbit IgH sequences in appendix germinal centers: VH diversification by gene conversion-like and hypermutation mechanisms. Immunity, 1, 647–659.

    Article  PubMed  CAS  Google Scholar 

  49. Diaz, M., & Flajnik, M. E. (1998). Evolution of somatic hypermutation and gene conversion in adaptive immunity. Immunological Reviews, 162, 13–24.

    Article  PubMed  CAS  Google Scholar 

  50. Muramatsu, M., Sankaranand, V. S., Anant, S., Sugai, M., Kinoshita, K., Davidson, N. O., et al. (1999). Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. The Journal of Biological Chemistry, 274, 18470–18476.

    Article  PubMed  CAS  Google Scholar 

  51. Revy, P., Muto, T., Levy, Y., Geissmann, F., Plebani, A., Sanal, O., et al. (2000). Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell, 102, 565–575.

    Article  PubMed  CAS  Google Scholar 

  52. Magor, B. G. (2015). Antibody affinity maturation in fishes—Our current understanding. Biology, 4, 512–524.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Wilson, M., Hsu, E., Marcuz, A., Courtet, M., Du Pasquier, L., & Steinberg, C. (1992). What limits affinity maturation of antibodies in Xenopus—The rate of somatic mutation or the ability to select mutants? The EMBO Journal, 11, 4337–4347.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Greenberg, A. S., Avila, D., Hughes, M., Hughes, A., McKinney, E. C., & Flajnik, M. F. (1995). A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature, 374, 168–173.

    Article  PubMed  CAS  Google Scholar 

  55. Hinds-Frey, K. R., Nishikata, H., Litman, R. T., & Litman, G. W. (1993). Somatic variation precedes extensive diversification of germline sequences and combinatorial joining in the evolution of immunoglobulin heavy chain diversity. Journal of Experimental Medicine, 178(3), 815–824.

    Article  PubMed  CAS  Google Scholar 

  56. Diaz, M., Greenberg, A. S., & Flajnik, M. F. (1998). 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. Proceedings of the National Academy of Sciences, 95(24), 14343–14348.

    Article  CAS  Google Scholar 

  57. Lee, S. S., Tranchina, D., Ohta, Y., Flajnik, M. F., & Hsu, E. (2002). Hypermutation in shark immunoglobulin light chain genes results in contiguous substitutions. Immunity, 16, 571–582.

    Article  PubMed  CAS  Google Scholar 

  58. Cain, K. D., Jones, D. R., & Raison, R. L. (2002). Antibody–antigen kinetics following immunization of rainbow trout (Oncorhynchus mykiss) with a T-cell dependent antigen. Developmental & Comparative Immunology., 26(2), 181–190.

    Article  CAS  Google Scholar 

  59. Saunders, H. L., & Magor, B. G. (2004). Cloning and expression of the AID gene in the channel catfish. Developmental & Comparative Immunology, 28, 657–663.

    Article  CAS  Google Scholar 

  60. Yang, F., Waldbieser, G. C., & Lobb, C. J. (2006). The nucleotide targets of somatic mutation and the role of selection in immunoglobulin heavy chains of a teleost fish. The Journal of Immunology, 176(3), 1655–1667.

    Article  PubMed  CAS  Google Scholar 

  61. Marianes, A. E., & Zimmerman, A. M. (2011). Targets of somatic hypermutation within immunoglobulin light chain genes in zebrafish. Immunology, 132(2), 240–255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Matsumoto, M., Lo, S. F., Carruthers, C. J., Min, J., Mariathasan, S., Huang, G., et al. (1996). Affinity maturation without germinal centres in lymphotoxin-α-deficient mice. Nature, 382, 462.

    Article  PubMed  CAS  Google Scholar 

  63. William, J., Euler, C., Christensen, S., & Shlomchik, M. J. (2002). Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science, 297(5589), 2066–2070.

    Article  PubMed  Google Scholar 

  64. Peters, A., & Storb, U. (1996). Somatic hypermutation of immunoglobulin genes is linked to transcription initiation. Immunity, 4, 57–65.

    Article  PubMed  CAS  Google Scholar 

  65. Wiesendanger, M., Scharff, M. D., & Edelmann, W. (1998). Somatic hypermutation, transcription, and DNA mismatch repair. Cell, 94, 415–418.

    Article  PubMed  CAS  Google Scholar 

  66. Okazaki, I. M., Kinoshita, K., Muramatsu, M., Yoshikawa, K., & Honjo, T. (2002). The AID enzyme induces class switch recombination in fibroblasts. Nature, 416, 340–345.

    Article  PubMed  CAS  Google Scholar 

  67. Yoshikawa, K., Okazaki, I. M., Eto, T., Kinoshita, K., Muramatsu, M., Nagaoka, H., et al. (2002). AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science, 296, 2033–2036.

    Article  PubMed  CAS  Google Scholar 

  68. Martin, A., Bardwell, P. D., Woo, C. J., Fan, M., Shulman, M. J., & Scharff, M. D. (2002). Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature, 415, 802–806.

    Article  PubMed  CAS  Google Scholar 

  69. Petersen-Mahrt, S. K., Harris, R. S., & Neuberger, M. S. (2002). AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature, 418, 99–104.

    Article  PubMed  CAS  Google Scholar 

  70. Mayorov, V. I., Rogozin, I. B., Adkison, L. R., Frahm, C., Kunkel, T. A., & Pavlov, Y. I. (2005). Expression of human AID in yeast induces mutations in context similar to the context of somatic hypermutation at GC pairs in immunoglobulin genes. BMC Immunology, 6, 10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Dudley, D. D., Chaudhuri, J., Bassing, C. H., & Alt, F. W. (2005). Mechanism and control of V (D) J recombination versus class switch recombination: Similarities and differences. Advances in Immunology, 86, 43–112.

    Article  PubMed  CAS  Google Scholar 

  72. Mondal, S., Begum, N. A., Hu, W., & Honjo, T. (2016). Functional requirements of AID’s higher order structures and their interaction with RNA-binding proteins. Proceedings of the National Academy of Sciences of the United States of America, 113, E1545–E1554.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Di Noia, J., & Neuberger, M. S. (2002). Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature, 419, 43–48.

    Article  PubMed  CAS  Google Scholar 

  74. Bransteitter, R., Pham, P., Scharff, M. D., & Goodman, M. F. (2003). Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proceedings of the National Academy of Sciences of the United States of America, 100, 4102–4107.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Dickerson, S. K., Market, E., Besmer, E., & Papavasiliou, F. N. (2003). AID mediates hypermutation by deaminating single stranded DNA. The Journal of Experimental Medicine, 197, 1291–1296.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Conticello, S. G. (2008). The AID/APOBEC family of nucleic acid mutators. Genome Biology, 9, 229.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Larijani, M., & Martin, A. (2012). The biochemistry of activation-induced deaminase and its physiological functions. Seminars in Immunology, 24(4), 255–263.

    Article  PubMed  CAS  Google Scholar 

  78. Chester, A., Scott, J., Anant, S., & Navaratnam, N. (2000). RNA editing: Cytidine to uridine conversion in apolipoprotein B mRNA. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1494, 1–13.

    Article  CAS  Google Scholar 

  79. Kinoshita, K., & Honjo, T. (2001). Linking class-switch recombination with somatic hypermutation. Nature Reviews Molecular Cell Biology, 2, 493–503.

    Article  PubMed  CAS  Google Scholar 

  80. Chester, A., Weinreb, V., Carter, C. W., & Navaratnam, N. (2004). Optimization of apolipoprotein B mRNA editing by APOBEC1 apoenzyme and the role of its auxiliary factor, ACF. Rna, 10, 1399–1411.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Vonica, A., Rosa, A., Arduini, B. L., & Brivanlou, A. H. (2011). APOBEC2, a selective inhibitor of TGFβ signaling, regulates left–right axis specification during early embryogenesis. Developmental Biology, 350, 13–23.

    Article  PubMed  CAS  Google Scholar 

  82. Honjo, T., Muramatsu, M., & Fagarasan, S. (2004). AID: How does it aid antibody diversity? Immunity, 20, 659–668.

    Article  PubMed  CAS  Google Scholar 

  83. Conticello, S. G., Thomas, C. J., Petersen-Mahrt, S. K., & Neuberger, M. S. (2005). Evolution of the AID/APOBEC family of polynucleotide (deoxy) cytidine deaminases. Molecular Biology and Evolution, 22, 367–377.

    Article  PubMed  CAS  Google Scholar 

  84. Cullen, B. R. (2006). Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. Journal of Virology, 80, 1067–1076.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Gandhi, S. K., Siliciano, J. D., Bailey, J. R., Siliciano, R. F., & Blankson, J. N. (2008). Role of APOBEC3G/F-mediated hypermutation in the control of human immunodeficiency virus type 1 in elite suppressors. Journal of Virology, 82, 3125–3130.

    Article  PubMed  CAS  Google Scholar 

  86. Siriwardena, S., Chen, K., & Bhagwat, A. S. (2016). The functions and malfunctions of AID/APOBEC family deaminases: The known knowns and the known unknowns. Chemical Reviews, 116, 12688–12710.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Starrett, G. J., Luengas, E. M., McCann, J. L., Ebrahimi, D., Temiz, N. A., Love, R. P., et al. (2016). The DNA cytosine deaminase APOBEC3H haplotype I likely contributes to breast and lung cancer mutagenesis. Nature Communications, 7, 12918.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. King, J. J., & Larijani, M. (2017). A novel regulator of activation-induced cytidine deaminase/APOBeCs in immunity and cancer: Schrödinger’s CATalytic Pocket. Frontiers in Immunology, 8, 351. https://doi.org/10.3389/fimmu.2017.00351.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Rogozin, I. B., Basu, M. K., Jordan, I. K., Pavlov, Y. I., & Koonin, E. V. (2005). APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy) cytidine deaminases predicted by computational analysis. Cell Cycle, 4, 1281–1285.

    Article  PubMed  CAS  Google Scholar 

  90. Tacchi, L., Larragoite, E. T., Muñoz, P., Amemiya, C. T., & Salinas, I. (2015). African lungfish reveal the evolutionary origins of organized mucosal lymphoid tissue in vertebrates. Current Biology, 25(18), 2417–2424.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Saunders, H. L., Oko, A. L., Scott, A. N., Fan, C. W., & Magor, B. G. (2010). The cellular context of AID expressing cells in fish lymphoid tissues. Developmental & Comparative Immunology, 34, 669–676.

    Article  CAS  Google Scholar 

  92. Barreto, V. M., & Magor, B. G. (2011). Activation-induced cytidine deaminase structure and functions: A species comparative view. Developmental & Comparative Immunology, 35, 991–1007.

    Article  CAS  Google Scholar 

  93. King, J. J., Manuel, C. A., Barrett, C. V., Raber, S., Lucas, H., Sutter, P., et al. (2015). Catalytic pocket inaccessibility of activation-induced cytidine deaminase is a safeguard against excessive mutagenic activity. Structure, 23, 615–627.

    Article  PubMed  CAS  Google Scholar 

  94. Shinkura, R., Ito, S., Begum, N. A., Nagaoka, H., Muramatsu, M., Kinoshita, K., et al. (2004). Separate domains of AID are required for somatic hypermutation and class-switch recombination. Nature Immunology, 5, 707–712.

    Article  PubMed  CAS  Google Scholar 

  95. Geisberger, R., Rada, C., & Neuberger, M. S. (2009). The stability of AID and its function in class-switching are critically sensitive to the identity of its nuclear-export sequence. Proceedings of the National Academy of Sciences of the United States of America, 106, 6736–6741.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Xu, Z., Zan, H., Pone, E. J., Mai, T., & Casali, P. (2012). Immunoglobulin class-switch DNA recombination: Induction, targeting and beyond. Nature Reviews Immunology, 12, 517–531.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Zan, H., & Casali, P. (2013). Regulation of Aicda expression and AID activity. Autoimmunity, 46, 83–101.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Barreto, V., Reina-San-Martin, B., Ramiro, A. R., McBride, K. M., & Nussenzweig, M. C. (2003). C-terminal deletion of AID uncouples class switch recombination from somatic hypermutation and gene conversion. Molecular Cell, 12, 501–508.

    Article  PubMed  CAS  Google Scholar 

  99. Ta, V. T., Nagaoka, H., Catalan, N., Durandy, A., Fischer, A., Imai, K., et al. (2003). AID mutant analyses indicate requirement for class-switch-specific cofactors. Nature Immunology, 4, 843–848.

    Article  PubMed  CAS  Google Scholar 

  100. McBride, K. M., Barreto, V., Ramiro, A. R., Stavropoulos, P., & Nussenzweig, M. C. (2004). Somatic hypermutation is limited by CRM1-dependent nuclear export of activation-induced deaminase. The Journal of Experimental Medicine, 199, 1235–1244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Ichikawa, H. T., Sowden, M. P., Torelli, A. T., Bachl, J., Huang, P., Dance, G. S., et al. (2006). Structural phylogenetic analysis of activation-induced deaminase function. The Journal of Immunology, 177, 355–361.

    Article  PubMed  CAS  Google Scholar 

  102. Flajnik, M. F., & Kasahara, M. (2010). Origin and evolution of the adaptive immune system: Genetic events and selective pressures. Nature Reviews Genetics, 11, 47–59.

    Article  PubMed  CAS  Google Scholar 

  103. Ramsden, D. A., Weed, B. D., & Reddy, Y. V. (2010). V (D) J recombination: Born to be wild. Seminars in Cancer Biology, 20(4), 254–260.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Cooper, M. D., & Herrin, B. R. (2010). How did our complex immune system evolve? Nature Reviews Immunology, 10, 2–3.

    Article  PubMed  CAS  Google Scholar 

  105. Hirano, M., Das, S., Guo, P., & Cooper, M. D. (2011). The evolution of adaptive immunity in vertebrates. Advances in Immunology, 109, 125–157.

    Article  PubMed  CAS  Google Scholar 

  106. Dehal, P., Satou, Y., Campbell, R. K., Chapman, J., Degnan, B., De Tomaso, A., et al. (2002). The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science, 298, 2157–2167.

    Article  PubMed  CAS  Google Scholar 

  107. Cannon, J. P., Haire, R. N., & Litman, G. W. (2002). Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nature Immunology, 3, 1200–1207.

    Article  PubMed  CAS  Google Scholar 

  108. Kasahara, M., Suzuki, T., & Du Pasquier, L. (2004). On the origins of the adaptive immune system: Novel insights from invertebrates and cold-blooded vertebrates. Trends in Immunology, 25, 105–111.

    Article  PubMed  CAS  Google Scholar 

  109. Klein, J., Sato, A., & Mayer, W. E. (1999). The major histocompatibility complex: Evolution, structure and function (pp. 3–26). Tokyo: Springer.

    Google Scholar 

  110. Herrin, B. R., & Cooper, M. D. (2010). Alternative adaptive immunity in jawless vertebrates. The Journal of Immunology, 185, 1367–1374.

    Article  PubMed  CAS  Google Scholar 

  111. Pancer, Z., Mayer, W. E., Klein, J., & Cooper, M. D. (2004). Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proceedings of the National Academy of Sciences of the United States of America, 101, 13273–13278.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Pancer, Z., Saha, N. R., Kasamatsu, J., Suzuki, T., Amemiya, C. T., Kasahara, M., et al. (2005). Variable lymphocyte receptors in hagfish. Proceedings of the National Academy of Sciences of the United States of America, 102, 9224–9229.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Schatz, D. G. (2007). DNA deaminases converge on adaptive immunity. Nature Immunology, 8, 551–553.

    Article  PubMed  CAS  Google Scholar 

  114. Perey, D. Y., Finstad, J., Pollara, B., & Good, R. A. (1968). Evolution of the immune response. VI. First and second set skin homograft rejections in primitive fishes. Laboratory Investigation, 19, 591–597.

    PubMed  CAS  Google Scholar 

  115. Finstad, J., & Good, R. A. (1964). The evolution of the immune response: III. Immunologic responses in the lamprey. The Journal of Experimental Medicine, 120, 1151.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Marchalonis, J. J., & Edelman, G. M. (1968). Phylogenetic origins of antibody structure: III. Antibodies in the primary immune response of the sea lamprey, Petromyzon marinus. The Journal of Experimental Medicine, 127, 891–914.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Shintani, S., Terzic, J., Sato, A., Saraga-Babic, M., O’hUigin, C., Tichy, H., et al. (2000). Do lampreys have lymphocytes? The Spi evidence. Proceedings of the National Academy of Sciences of the United States of America, 97, 7417–7422.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Alder, M. N., Rogozin, I. B., Iyer, L. M., Glazko, G. V., Cooper, M. D., & Pancer, Z. (2005). Diversity and function of adaptive immune receptors in a jawless vertebrate. Science, 310, 1970–1973.

    Article  PubMed  CAS  Google Scholar 

  119. Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., et al. (2007). Evolution and diversification of lamprey antigen receptors: Evidence for involvement of an AID-APOBEC family cytosine deaminase. Nature Immunology, 8, 647–656.

    Article  PubMed  CAS  Google Scholar 

  120. Kishishita, N., & Nagawa, F. (2014). Evolution of adaptive immunity: Implications of a third lymphocyte lineage in lampreys. Bioessays, 36, 244–250.

    Article  PubMed  CAS  Google Scholar 

  121. Kim, H. M., Oh, S. C., Lim, K. J., Kasamatsu, J., Heo, J. Y., Park, B. S., et al. (2007). Structural diversity of the hagfish variable lymphocyte receptors. The Journal of Biological Chemistry, 282, 6726–6732.

    Article  PubMed  CAS  Google Scholar 

  122. Nagawa, F., Kishishita, N., Shimizu, K., Hirose, S., Miyoshi, M., Nezu, J., et al. (2007). Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nature Immunology, 8, 206–213.

    Article  PubMed  CAS  Google Scholar 

  123. Hirano, M., Guo, P., McCurley, N., Schorpp, M., Das, S., Boehm, T., et al. (2013). Evolutionary implications of a third lymphocyte lineage in lampreys. Nature, 501, 435–438.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Boehm, T., McCurley, N., Sutoh, Y., Schorpp, M., Kasahara, M., & Cooper, M. D. (2012). VLR-based adaptive immunity. Annual Review of Immunology, 30, 203–220.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. Zhu, C., Lee, V., Finn, A., Senger, K., Zarrin, A. A., Du Pasquier, L., et al. (2012). Origin of immunoglobulin isotype switching. Current Biology, 22, 872–880.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Rast, J. P., & Litman, G. W. (1998). Towards understanding the evolutionary origins and early diversification of rearranging antigen receptors. Immunological Reviews, 166, 79–86.

    Article  PubMed  CAS  Google Scholar 

  127. Lee, S. S., Fitch, D., Flajnik, M. F., & Hsu, E. (2000). Rearrangement of immunoglobulin genes in shark germ cells. The Journal of Experimental Medicine, 191, 1637–1648.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Eason, D. D., Cannon, J. P., Haire, R. N., Rast, J. P., Ostrov, D. A., & Litman, G. W. (2004). Mechanisms of antigen receptor evolution. Seminars in Immunology, 16(4), 215–226.

    Article  PubMed  CAS  Google Scholar 

  129. Hinds, K. R., & Litman, G. W. (1986). Major reorganization of immunoglobulin VH segmental elements during vertebrate evolution. Nature, 320, 546–549.

    Article  PubMed  CAS  Google Scholar 

  130. Rumfelt, L. L., McKinney, E. C., Taylor, E., & Flajnik, M. F. (2002). 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. Scandinavian Journal of Immunology, 56, 130–148.

    Article  PubMed  CAS  Google Scholar 

  131. Van Gent, D. C., Ramsden, D. A., & Gellert, M. (1996). The RAG1 and RAG2 proteins establish the 12/23 rule in V (D) J recombination. Cell, 85, 107–113.

    Article  PubMed  Google Scholar 

  132. Rumfelt, L. L., Avila, D., Diaz, M., Bartl, S., McKinney, E. C., & Flajnik, M. F. (2001). A shark antibody heavy chain encoded by a nonsomatically rearranged VDJ is preferentially expressed in early development and is convergent with mammalian IgG. Proceedings of the National Academy of Sciences of the United States of America, 98, 1775–1780.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Scapigliati, G. (2013). Functional aspects of fish lymphocytes. Developmental & Comparative Immunology, 41, 200–208.

    Article  CAS  Google Scholar 

  134. Malecek, K., Brandman, J., Brodsky, J. E., Ohta, Y., Flajnik, M. F., & Hsu, E. (2005). Somatic hypermutation and junctional diversification at Ig heavy chain loci in the nurse shark. The Journal of Immunology, 175, 8105–8115.

    Article  PubMed  CAS  Google Scholar 

  135. Kato, L., Stanlie, A., Begum, N. A., Kobayashi, M., Aida, M., & Honjo, T. (2012). An evolutionary view of the mechanism for immune and genome diversity. The Journal of Immunology, 188, 3559–3566.

    Article  PubMed  CAS  Google Scholar 

  136. Eason, D. D., Litman, R. T., Luer, C. A., Kerr, W., & Litman, G. W. (2004). Expression of individual immunoglobulin genes occurs in an unusual system consisting of multiple independent loci. European Journal of Immunology, 34, 2551–2558.

    Article  PubMed  CAS  Google Scholar 

  137. Zhang, C., Du Pasquier, L., & Hsu, E. (2013). Shark IgW C region diversification through RNA processing and isotype switching. The Journal of Immunology, 191, 3410–3418.

    Article  PubMed  CAS  Google Scholar 

  138. Ghaffari, S. H., & Lobb, C. J. (1997). Structure and genomic organization of a second class of immunoglobulin light chain genes in the channel catfish. The Journal of Immunology, 159, 250–258.

    PubMed  CAS  Google Scholar 

  139. Hansen, J. D., Landis, E. D., & Phillips, R. B. (2005). Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. Proceedings of the National Academy of Sciences of the United States of America, 102, 6919–6924.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  140. Jaillon, O., Aury, J. M., Brunet, F., Petit, J. L., Stange-Thomann, N., Mauceli, E., et al. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature, 431, 946–957.

    Article  PubMed  Google Scholar 

  141. Hsu, E., Pulham, N., Rumfelt, L. L., & Flajnik, M. F. (2006). The plasticity of immunoglobulin gene systems in evolution. Immunological Reviews, 210, 8–26.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Bengtén, E., Clem, L. W., Miller, N. W., Warr, G. W., & Wilson, M. (2006). Channel catfish immunoglobulins: Repertoire and expression. Developmental & Comparative Immunology, 30, 77–92.

    Article  CAS  Google Scholar 

  143. Fillatreau, S., Six, A., Magadan, S., Castro, R., Sunyer, J. O., & Boudinot, P. (2013). The astonishing diversity of Ig classes and B cell repertoires in teleost fish. Frontiers in immunology, 4, 28.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  144. Hikima, J. I., Jung, T. S., & Aoki, T. (2011). Immunoglobulin genes and their transcriptional control in teleosts. Developmental & Comparative Immunology, 35, 924–936.

    Article  CAS  Google Scholar 

  145. Vallur, A. C., Yabuki, M., Larson, E. D., & Maizels, N. (2007). AID in antibody perfection. Cellular and Molecular Life Sciences, 64, 555–565.

    Article  PubMed  CAS  Google Scholar 

  146. Sohail, A., Klapacz, J., Samaranayake, M., Ullah, A., & Bhagwat, A. S. (2003). Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Research, 31, 2990–2994.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  147. Pham, P., Bransteitter, R., Petruska, J., & Goodman, M. F. (2003). Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature, 424, 103–107.

    Article  PubMed  CAS  Google Scholar 

  148. DiMenna, L. J., & Chaudhuri, J. (2016). Regulating infidelity: RNA-mediated recruitment of AID to DNA during class switch recombination. European Journal of Immunology, 46, 523–530.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Hwang, J. K., Alt, F. W., & Yeap, L. S. (2015). Related mechanisms of antibody somatic hypermutation and class switch recombination. Microbiology Spectrum, 3, 1–35.

    Google Scholar 

  150. Chatterji, M., Unniraman, S., McBride, K. M., & Schatz, D. G. (2007). Role of activation-induced deaminase protein kinase A phosphorylation sites in Ig gene conversion and somatic hypermutation. The Journal of Immunology, 179, 5274–5280.

    Article  PubMed  CAS  Google Scholar 

  151. Matthews, A. J., Zheng, S., DiMenna, L. J., & Chaudhuri, J. (2014). Regulation of immunoglobulin class-switch recombination: Choreography of noncoding transcription, targeted DNA deamination, and long-range DNA repair. Advances in Immunology, 122, 1–57.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Patenaude, A. M., Orthwein, A., Hu, Y., Campo, V. A., Kavli, B., Buschiazzo, A., et al. (2009). Active nuclear import and cytoplasmic retention of activation-induced deaminase. Nature Structural & Molecular Biology, 16, 517–527.

    Article  CAS  Google Scholar 

  153. Pavri, R., Gazumyan, A., Jankovic, M., Di Virgilio, M., Klein, I., Ansarah-Sobrinho, C., et al. (2010). Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell, 143, 122–133.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  154. Stavnezer, J., & Schrader, C. E. (2014). IgH chain class switch recombination: Mechanism and regulation. The Journal of Immunology, 193, 5370–5378.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  155. Pham, P., Afif, S. A., Shimoda, M., Maeda, K., Sakaguchi, N., Pedersen, L. C., et al. (2016). Structural analysis of the activation-induced deoxycytidine deaminase required in immunoglobulin diversification. DNA Repair, 43, 48–56.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  156. Casellas, R., Nussenzweig, A., Wuerffel, R., Pelanda, R., Reichlin, A., Suh, H., et al. (1998). Ku80 is required for immunoglobulin isotype switching. The EMBO Journal, 17, 2404–2411.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  157. Manis, J. P., Gu, Y., Lansford, R., Sonoda, E., Ferrini, R., Davidson, L., et al. (1998). Ku70 is required for late B cell development and immunoglobulin heavy chain class switching. The Journal of Experimental Medicine, 187, 2081–2089.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  158. Reina-San-Martin, B., Difilippantonio, S., Hanitsch, L., Masilamani, R. F., Nussenzweig, A., & Nussenzweig, M. C. (2003). H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. The Journal of Experimental Medicine, 197, 1767–1778.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  159. Chandra, V., Bortnick, A., & Murre, C. (2015). AID targeting: Old mysteries and new challenges. Trends in Immunology, 36, 527–535.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  160. MacDuff, D. A., Neuberger, M. S., & Harris, R. S. (2006). MDM2 can interact with the C-terminus of AID but it is inessential for antibody diversification in DT40 B cells. Molecular Immunology, 43, 1099–1108.

    Article  PubMed  CAS  Google Scholar 

  161. Chaudhuri, J., Khuong, C., & Alt, F. W. (2004). Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature, 430, 992–998.

    Article  PubMed  CAS  Google Scholar 

  162. de Yébenes, V. G., & Ramiro, A. R. (2006). Activation-induced deaminase: Light and dark sides. Trends in Molecular Medicine, 12, 432–439.

    Article  PubMed  CAS  Google Scholar 

  163. Basu, U., Chaudhuri, J., Alpert, C., Dutt, S., Ranganath, S., Li, G., et al. (2005). The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation. Nature, 438, 508–511.

    Article  PubMed  CAS  Google Scholar 

  164. Basu, U., Wang, Y., & Alt, F. W. (2008). Evolution of phosphorylation-dependent regulation of activation-induced cytidine deaminase. Molecular Cell, 32, 285–291.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  165. Basu, U., Franklin, A., & Alt, F. W. (2009). Post-translational regulation of activation-induced cytidine deaminase. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 667–673.

    Article  PubMed  CAS  Google Scholar 

  166. Budzyńska, P. M., Kyläniemi, M. K., Kallonen, T., Soikkeli, A. I., Nera, K. P., Lassila, O., et al. (2017). Bach2 regulates AID-mediated immunoglobulin gene conversion and somatic hypermutation in DT40 B cells. European Journal of Immunology. https://doi.org/10.1002/eji.201646895.

    Article  PubMed  Google Scholar 

  167. Hu, W., Begum, N. A., Mondal, S., Stanlie, A., & Honjo, T. (2015). Identification of DNA cleavage-and recombination-specific hnRNP cofactors for activation-induced cytidine deaminase. Proceedings of the National Academy of Sciences of the United States of America, 112, 5791–5796.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  168. Dancyger, A. M., King, J. J., Quinlan, M. J., Fifield, H., Tucker, S., Saunders, H. L., et al. (2012). Differences in the enzymatic efficiency of human and bony fish AID are mediated by a single residue in the C terminus modulating single-stranded DNA binding. The FASEB Journal, 26(4), 1517–1525.

    Article  PubMed  CAS  Google Scholar 

  169. Villota-Herdoiza, D., Pila, E. A., Quiniou, S., Waldbieser, G. C., & Magor, B. G. (2013). Transcriptional regulation of teleost Aicda genes. Part 1—Suppressors of promiscuous promoters. Fish & Shellfish Immunology, 35(6), 1981–1987.

    Article  CAS  Google Scholar 

  170. Cerutti, A. (2008). The regulation of IgA class switching. Nature Reviews Immunology, 8, 421–434.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  171. Bekeredjian-Ding, I., & Jego, G. (2009). Toll-like receptors–sentries in the B-cell response. Immunology, 128, 311–323.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  172. Pone, E. J., Zan, H., Zhang, J. S., Al-Qahtani, A., Xu, Z., & Casali, P. (2010). Toll-like receptors and B-cell receptors synergize to induce immunoglobulin class-switch DNA recombination: Relevance to microbial antibody responses. Critical Reviews in Immunology, 30, 1–29.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  173. Xu, W., Santini, P. A., Matthews, A. J., Chiu, A., Plebani, A., He, B., et al. (2008). Viral double-stranded RNA triggers Ig class switching by activating upper respiratory mucosa B cells through an innate TLR3 pathway involving BAFF. The Journal of Immunology, 181, 276–287.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  174. Medzhitov, R., Preston-Hurlburt, P., & Janeway, C. A. (1997). A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature, 388, 394–397.

    Article  PubMed  CAS  Google Scholar 

  175. Rauta, P. R., Samanta, M., Dash, H. R., Nayak, B., & Das, S. (2014). Toll-like receptors (TLRs) in aquatic animals: Signaling pathways, expressions and immune responses. Immunology Letters, 158, 14–24.

    Article  PubMed  CAS  Google Scholar 

  176. Akira, S., Uematsu, S., & Takeuchi, O. (2006). Pattern recognition and innate immunity. Cell, 124, 783–801.

    Article  PubMed  CAS  Google Scholar 

  177. Bombardieri, M., Kam, N. W., Brentano, F., Choi, K., Filer, A., Kyburz, D., et al. (2011). A BAFF/APRIL-dependent TLR3-stimulated pathway enhances the capacity of rheumatoid synovial fibroblasts to induce AID expression and Ig class-switching in B cells. Annals of the Rheumatic Diseases, 70, 1857–1865.

    Article  PubMed  CAS  Google Scholar 

  178. Mandler, R., Finkelman, F. D., Levine, A. D., & Snapper, C. M. (1993). IL-4 induction of IgE class switching by lipopolysaccharide-activated murine B cells occurs predominantly through sequential switching. The Journal of Immunology, 150, 407–418.

    PubMed  CAS  Google Scholar 

  179. Castigli, E., Wilson, S. A., Scott, S., Dedeoglu, F., Xu, S., Lam, K. P., et al. (2005). TACI and BAFF-R mediate isotype switching in B cells. The Journal of Experimental Medicine, 201, 35–39.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  180. He, B., Qiao, X., & Cerutti, A. (2004). CpG DNA induces IgG class switch DNA recombination by activating human B cells through an innate pathway that requires TLR9 and cooperates with IL-10. The Journal of Immunology, 173, 4479–4491.

    Article  PubMed  CAS  Google Scholar 

  181. Schneider, P. (2005). The role of APRIL and BAFF in lymphocyte activation. Current Opinion in Immunology, 17, 282–289.

    Article  PubMed  CAS  Google Scholar 

  182. Thompson, J. S., Schneider, P., Kalled, S. L., Wang, L., Lefevre, E. A., Cachero, T. G., et al. (2000). BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population. The Journal of Experimental Medicine, 192, 129–136.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  183. Castigli, E., Scott, S., Dedeoglu, F., Bryce, P., Jabara, H., Bhan, A. K., et al. (2004). Impaired IgA class switching in APRIL-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 101, 3903–3908.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  184. Day, E. S., Cachero, T. G., Qian, F., Sun, Y., Wen, D., Pelletier, M., et al. (2005). Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry, 44, 1919–1931.

    Article  PubMed  CAS  Google Scholar 

  185. Barreto, V. M., Ramiro, A. R., & Nussenzweig, M. C. (2005). Activation-induced deaminase: Controversies and open questions. Trends in Immunology, 26, 90–96.

    Article  PubMed  CAS  Google Scholar 

  186. Moris, A., Murray, S., & Cardinaud, S. (2014). AID and APOBECs span the gap between innate and adaptive immunity. Frontiers in Microbiology, 5, 1–13.

    Article  Google Scholar 

  187. Abdouni, H., King, J. J., Suliman, M., Quinlan, M., Fifield, H., & Larijani, M. (2013). Zebrafish AID is capable of deaminating methylated deoxycytidines. Nucleic Acids Research, 41, 5457–5468.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Harris, R. S., Sheehy, A. M., Craig, H. M., Malim, M. H., & Neuberger, M. S. (2003). DNA deamination: Not just a trigger for antibody diversification but also a mechanism for defense against retroviruses. Nature Immunology, 4, 641–643.

    Article  PubMed  CAS  Google Scholar 

  189. Okazaki, I. M., Kotani, A., & Honjo, T. (2007). Role of AID in tumorigenesis. Advances in Immunology, 94, 245–273.

    Article  PubMed  CAS  Google Scholar 

  190. Liu, M., & Schatz, D. G. (2009). Balancing AID and DNA repair during somatic hypermutation. Trends in Immunology, 30, 173–181.

    Article  PubMed  CAS  Google Scholar 

  191. Robbiani, D. F., Bunting, S., Feldhahn, N., Bothmer, A., Camps, J., Deroubaix, S., et al. (2009). AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Molecular Cell, 36, 631–641.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  192. Guselnikov, S. V., Ramanayake, T., Erilova, A. Y., Mechetina, L. V., Najakshin, A. M., Robert, J., et al. (2008). The Xenopus FcR family demonstrates continually high diversification of paired receptors in vertebrate evolution. BMC Evolutionary Biology, 8, 148.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

Authors wish to thank the National Agricultural Science Fund (NASF/BS-4003) of the Indian Council of Agricultural Research (ICAR), Government of India, for providing the research grant.

Author information

Authors and Affiliations

  1. Laboratory of Environmental Microbiology and Ecology (LEnME), Department of Life Science, National Institute of Technology, Rourkela, Odisha, 769 008, India

    Bhakti Patel, Rajanya Banerjee & Surajit Das

  2. Immunology Laboratory, Fish Health Management Division, ICAR-Central Institute of Freshwater Aquaculture, Kausalyaganga, Bhubaneswar, Odisha, 751 002, India

    Mrinal Samanta

Authors
  1. Bhakti Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rajanya Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mrinal Samanta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Surajit Das
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Surajit Das.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patel, B., Banerjee, R., Samanta, M. et al. Diversity of Immunoglobulin (Ig) Isotypes and the Role of Activation-Induced Cytidine Deaminase (AID) in Fish. Mol Biotechnol 60, 435–453 (2018). https://doi.org/10.1007/s12033-018-0081-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-018-0081-8

Keywords

Search

Navigation