Extensive diversification of IgH subclass-encoding genes and IgM subclass switching in crocodilians

Nature Communications

Volumn 4, Issue , 2013, Pages

  Cheng, Gang ^a   Gao, Yang ^a   Wang, Tao ^a   Sun, Yi ^a   Wei, Zhiguo ^b   Li, Lingxiao ^a   Ren, Liming ^a   Guo, Ying ^a   Hu, Xiaoiang ^a   Lu, Ya ^c   Wang, Xumin ^d   Liu, Guiming ^d   Zhang, Chenglin ^c   Yu, Jun ^d   Pan Hammarström, Qiang ^e   Hammarström, Lennart ^e   Wu, Xiaobing ^f   Li, Ning ^a   Zhao, Yaofeng ^a,g  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b HENAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c Beijing Zoo   (China)

^d Chinese Academy of Sciences   (China)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^f ANHUI NORMAL UNIVERSITY   (China)

^g QINGDAO AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M1; IMMUNOGLOBULIN M2; IMMUNOGLOBULIN M3; IMMUNOGLOBULIN MU CHAIN; UNCLASSIFIED DRUG; MESSENGER RNA;

CROCODILIAN; GENE EXPRESSION; IDENTIFICATION METHOD; IMMUNE SYSTEM; RECOMBINATION;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CLONING; CONTROLLED STUDY; EXON; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; GENE MAPPING; GENE SEQUENCE; GENE STRUCTURE; HUMORAL IMMUNITY; INTRON; NONHUMAN; PROMOTER REGION; ANIMAL; BLOOD; CHROMOSOME MAP; CROCODILIAN; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; GENOME; GERM CELL; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY;

ALLIGATORS AND CROCODILES; ANIMALS; BASE SEQUENCE; EXONS; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETIC LOCI; GENETIC VARIATION; GENOME; GERM CELLS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN M; INTRONS; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PHYSICAL CHROMOSOME MAPPING; PROMOTER REGIONS, GENETIC; RECOMBINATION, GENETIC; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

MLCS; MLOWN;

EID: 84879182945     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2317     Document Type: Article

References (53)

1. Flajnik, M. F. Comparative analyses of immunoglobulin genes: surprises and portents. Nat. Rev. Immunol. 2, 688-698 (2002). (Pubitemid 37328726)
2. Flajnik, M. F. & Kasahara, M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11, 47-59 (2010).
3. Das, S., Hirano, M., McCallister, C., Tako, R. & Nikolaidis, N. Comparative genomics and evolution of immunoglobulin-encoding loci in tetrapods. Adv. Immunol. 111, 143-178 (2011).
4. Hirano, M., Das, S., Guo, P. & Cooper, M. D. The evolution of adaptive immunity in vertebrates. Adv. Immunol. 109, 125-157 (2011).
5. Cooper, M. D. & Herrin, B. R. How did our complex immune system evolve? Nat. Rev. Immunol. 10, 2-3 (2010).
6. Guo, P. et al. Dual nature of the adaptive immune system in lampreys. Nature 459, 796-801 (2009).
7. Alder, M. N. et al. Antibody responses of variable lymphocyte receptors in the lamprey. Nat. Immunol. 9, 319-327 (2008). (Pubitemid 351267329)
8. Reynaud, C. A., Anquez, V., Grimal, H. & Weill, J. C. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48, 379-388 (1987).
9. Reynaud, C. A., Dahan, A., Anquez, V. & Weill, J. C. Somatic hyperconversion diversifies the single Vh gene of the chicken with a high incidence in the D region. Cell 59, 171-183 (1989). (Pubitemid 19248567)
10. 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. USA 93, 3289-3293 (1996). (Pubitemid 26125611)
11. 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 100, 2501-2506 (2003). (Pubitemid 36297528)
12. Greenberg, A. S. et al. A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374, 168-173 (1995).
13. 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. 6, 295-302 (2005). (Pubitemid 41724767)
14. 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 102, 6919-6924 (2005). (Pubitemid 40675417)
15. Zhang, Y. A. et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11, 827-835 (2010).
16. Wilson, M. et al. A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc. Natl Acad. Sci. USA 94, 4593-4597 (1997). (Pubitemid 27194287)
17. Zhao, Y. et al. Identification of IgF, a hinge-region-containing Ig class, and IgD in Xenopus tropicalis. Proc. Natl Acad. Sci. USA 103, 12087-12092 (2006). (Pubitemid 44215815)
18. Zhao, Y. et al. Ornithorhynchus anatinus (platypus) links the evolution of immunoglobulin genes in eutherian mammals and nonmammalian tetrapods. J. Immunol. 183, 3285-3293 (2009).
19. Hsu, E., Flajnik, M. F. & Du Pasquier, L. A third immunoglobulin class in amphibians. J. Immunol. 135, 1998-2004 (1985). (Pubitemid 16243018)
20. Gambon-Deza, F., Sanchez-Espinel, C. & Magadan-Mompo, S. The immunoglobulin heavy chain locus in the platypus (Ornithorhynchus anatinus). Mol. Immunol. 46, 2515-2523 (2009).
21. Ohta, Y. & Flajnik, M. IgD, like IgM, is a primordial immunoglobulin class perpetuated in most jawed vertebrates. Proc. Natl Acad. Sci. USA 103, 10723-10728 (2006). (Pubitemid 44081629)
22. Sun, Y., Wei, Z., Hammarstrom, L. & Zhao, Y. The immunoglobulin delta gene in jawed vertebrates: a comparative overview. Dev. Comp. Immunol. 35, 975-981 (2011).
23. Litman, G. W., Anderson, M. K. & Rast, J. P. Evolution of antigen binding receptors. Annu. Rev. Immunol. 17, 109-147 (1999). (Pubitemid 29241121)
24. Deza, F. G., Espinel, C. S. & Beneitez, J. V. A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev. Comp. Immunol. 31, 596-605 (2007).
25. Wei, Z. et al. Expression of IgM, IgD, and IgY in a reptile, Anolis carolinensis. J. Immunol. 183, 3858-3864 (2009).
26. Warr, G. W., Magor, K. E. & Higgins, D. A. IgY: clues to the origins of modern antibodies. Immunol. Today 16, 392-398 (1995).
27. Lundqvist, M. L., Middleton, D. L., Hazard, S. & Warr, G. W. The immunoglobulin heavy chain locus of the duck. Genomic organization and expression of D, J, and C region genes. J. Biol. Chem. 276, 46729-46736 (2001).
28. Gambon Deza, F., Sanchez Espinel, C. & Magadan Mompo, S. The immunoglobulin heavy chain locus in the reptile Anolis carolinensis. Mol. Immunol. 46, 1679-1687 (2009).
29. Janke, A. & Arnason, U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles). Mol. Biol. Evol. 14, 1266-1272 (1997). (Pubitemid 27523140)
30. Darville, L. N., Merchant, M. E., Hasan, A. & Murray, K. K. Proteome analysis of the leukocytes from the American alligator (Alligator mississippiensis) using mass spectrometry. Comp. Biochem. Physiol. Part D Genomics Proteomics 5, 308-316 (2010).
31. Merchant, M. E. et al. Broad spectrum antimicrobial activity of leukocyte extracts from the American alligator (Alligator mississippiensis). Vet. Immunol. Immunopathol. 110, 221-228 (2006).
32. Zhao, Y., Kacskovics, I., Rabbani, H. & Hammarstrom, L. Physical mapping of the bovine immunoglobulin heavy chain constant region gene locus. J. Biol. Chem. 278, 35024-35032 (2003). (Pubitemid 37102263)
33. Stavnezer, J., Guikema, J. E. & Schrader, C. E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292 (2008). (Pubitemid 351600377)
34. Pan-Hammarstrom, Q., Zhao, Y. & Hammarstrom, L. Class switch recombination: a comparison between mouse and human. Adv. Immunol. 93, 1-61 (2007). (Pubitemid 46441428)
35. Pan-Hammarstrom, Q. et al. ATM is not required in somatic hypermutation of VH, but is involved in the introduction of mutations in the switch mu region. J. Immunol. 170, 3707-3716 (2003). (Pubitemid 36359241)
36. Litman, G. W. et al. Complete nucleotide sequences of three VH genes in Caiman, a phylogenetically ancient reptile: evolutionary diversification in coding segments and variation in the structure and organization of recombination elements. Proc. Natl Acad. Sci. USA 82, 844-848 (1985).
37. Turchin, A. & Hsu, E. The generation of antibody diversity in the turtle. J. Immunol. 156, 3797-3805 (1996). (Pubitemid 26137666)
38. Wu, Q. et al. Phylogeny, genomic organization and expression of lambda and kappa immunoglobulin light chain genes in a reptile, Anolis carolinensis. Dev. Comp. Immunol. 34, 579-589.
39. 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 105, 16647-16652 (2008).
40. Gambon-Deza, F. & Espinel, C. S. IgD in the reptile leopard gecko. Mol. Immunol. 45, 3470-3476 (2008).
41. 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. 46, 2124-2132 (2009).
42. Janke, A., Gullberg, A., Hughes, S., Aggarwal, R. K. & Arnason, U. Mitogenomic analyses place the gharial (Gavialis gangeticus) on the crocodile tree and provide pre-K/T divergence times for most crocodilians. J. Mol. Evol. 61, 620-626 (2005). (Pubitemid 41598608)
43. Gambon-Deza, F., Sanchez-Espinel, C., Mirete-Bachiller, S. & Magadan-Mompo, S. Snakes antibodies. Dev. Comp. Immunol. 38, 1-9 (2012).
44. Huang, T. et al. Analysis of immunoglobulin transcripts in the ostrich Struthio camelus, a primitive avian species. PLoS One 7, e34346.
45. 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 101, 348-353 (2000).
46. Lundqvist, M. L., Middleton, D. L., Radford, C., Warr, G. W. & Magor, K. E. Immunoglobulins of the non-galliform birds: antibody expression and repertoire in the duck. Dev. Comp. Immunol. 30, 93-100 (2006). (Pubitemid 41408492)
47. Barreto, V. M. et al. AID from bony fish catalyzes class switch recombination. J. Exp. Med. 202, 733-738 (2005). (Pubitemid 41345962)
48. 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. 29, 61-71 (2005). (Pubitemid 39119400)
49. Conticello, S. G., Thomas, C. J., Petersen-Mahrt, S. K. & Neuberger, M. S. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol. 22, 367-377 (2005). (Pubitemid 40130201)
50. Lundqvist, M. L., McElveen, B. R., Middleton, D. L. & Warr, G. W. Enhancer and promoter activity in the JH to IGHM intron of the Pekin duck, Anas platyrhynchos. Dev. Comp. Immunol. 31, 286-295 (2007). (Pubitemid 44894566)
51. Mussmann, R., Du Pasquier, L. & Hsu, E. Is Xenopus IgX an analog of IgA? Eur. J. Immunol. 26, 2823-2830 (1996). (Pubitemid 26411483)
52. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574 (2003). (Pubitemid 37038874)
53. Page, R. D. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358 (1996).