Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase (original) (raw)

References

  1. Alder, M.N. et al. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 310, 1970–1973 (2005).
    Article CAS Google Scholar
  2. Oettinger, M.A., Schatz, D.G., Gorka, C. & Baltimore, D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248, 1517–1523 (1990).
    Article CAS Google Scholar
  3. Arakawa, H., Hauschild, J. & Buerstedde, J.M. Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 295, 1301–1306 (2002).
    Article CAS Google Scholar
  4. Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553–563 (2000).
    Article CAS Google Scholar
  5. Pancer, Z. et al. Variable lymphocyte receptors in hagfish. Proc. Natl. Acad. Sci. USA 102, 9224–9229 (2005).
    Article CAS Google Scholar
  6. Pancer, Z. et al. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430, 174–180 (2004).
    Article CAS Google Scholar
  7. Kim, H.M. et al. Structural diversity of the hagfish variable lymphocyte receptors. J. Biol. Chem. 282, 6726–6732 (2007).
    Article CAS Google Scholar
  8. Schatz, D.G. Antigen receptor genes and the evolution of a recombinase. Semin. Immunol. 16, 245–256 (2004).
    Article CAS Google Scholar
  9. Fugmann, S.D., Messier, C., Novack, L.A., Cameron, R.A. & Rast, J.P. An ancient evolutionary origin of the Rag1/2 gene locus. Proc. Natl. Acad. Sci. USA 103, 3728–3733 (2006).
    Article CAS Google Scholar
  10. Kapitonov, V.V. & Jurka, J. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3, e181 (2005).
    Article Google Scholar
  11. 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).
    Article CAS Google Scholar
  12. Aravind, L. & Landsman, D. AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res. 26, 4413–4421 (1998).
    Article CAS Google Scholar
  13. Losey, H.C., Ruthenburg, A.J. & Verdine, G.L. Crystal structure of Staphylococcus aureus tRNA adenosine deaminase TadA in complex with RNA. Nat. Struct. Mol. Biol. 13, 153–159 (2006).
    Article CAS Google Scholar
  14. Petersen-Mahrt, S.K., Harris, R.S. & Neuberger, M.S. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99–103 (2002).
    Article CAS Google Scholar
  15. Garibyan, L. et al. Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair (Amst.) 2, 593–608 (2003).
    Article CAS Google Scholar
  16. Bransteitter, R., Pham, P., Calabrese, P. & Goodman, M.F. Biochemical analysis of hypermutational targeting by wild type and mutant activation-induced cytidine deaminase. J. Biol. Chem. 279, 51612–51621 (2004).
    Article CAS Google Scholar
  17. Mayorov, V.I. et al. Expression of human AID in yeast induces mutations in context similar to the context of somatic hypermutation at G-C pairs in immunoglobulin genes. BMC Immunol. 6, 10 (2005).
    Article Google Scholar
  18. Rogozin, I.B., Pavlov, Y.I., Bebenek, K., Matsuda, T. & Kunkel, T.A. Somatic mutation hotspots correlate with DNA polymerase η error spectrum. Nat. Immunol. 2, 530–536 (2001).
    Article CAS Google Scholar
  19. Milstein, C., Neuberger, M.S. & Staden, R. Both DNA strands of antibody genes are hypermutation targets. Proc. Natl. Acad. Sci. USA 95, 8791–8794 (1998).
    Article CAS Google Scholar
  20. Rogozin, I.B., Sredneva, N.E. & Kolchanov, N.A. Somatic hypermutagenesis in immunoglobulin genes. III. Somatic mutations in the chicken light chain locus. Biochim. Biophys. Acta 1306, 171–178 (1996).
    Article Google Scholar
  21. Wagner, S.D., Milstein, C. & Neuberger, M.S. Codon bias targets mutation. Nature 376, 732 (1995).
    Article CAS Google Scholar
  22. Pancer, Z. & Cooper, M.D. The evolution of adaptive immunity. Annu. Rev. Immunol. 24, 497–518 (2006).
    Article CAS Google Scholar
  23. Canobbio, I., Balduini, C. & Torti, M. Signalling through the platelet glycoprotein Ib-V-IX complex. Cell. Signal. 16, 1329–1344 (2004).
    Article CAS Google Scholar
  24. Meyers, B.C., Kozik, A., Griego, A., Kuang, H. & Michelmore, R.W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15, 809–834 (2003).
    Article CAS Google Scholar
  25. Hibino, T. et al. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 300, 349–365 (2006).
    Article CAS Google Scholar
  26. Huizinga, E.G. et al. Structures of glycoprotein Ibα and its complex with von Willebrand factor A1 domain. Science 297, 1176–1179 (2002).
    Article CAS Google Scholar
  27. Nagawa, F. et al. Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat. Immunol. 8, 206–213 (2007).
    Article CAS Google Scholar
  28. McCormack, W.T. & Thompson, C.B. Chicken IgL variable region gene conversions display pseudogene donor preference and 5′ to 3′ polarity. Genes Dev. 4, 548–558 (1990).
    Article CAS Google Scholar
  29. Arcangioli, B. & de Lahondes, R. Fission yeast switches mating type by a replication-recombination coupled process. EMBO J. 19, 1389–1396 (2000).
    Article CAS Google Scholar
  30. Viguera, E., Canceill, D. & Ehrlich, S.D. Replication slippage involves DNA polymerase pausing and dissociation. EMBO J. 20, 2587–2595 (2001).
    Article CAS Google Scholar
  31. Poltoratsky, V.P., Wilson, S.H., Kunkel, T.A. & Pavlov, Y.I. Recombinogenic phenotype of human activation-induced cytosine deaminase. J. Immunol. 172, 4308–4313 (2004).
    Article CAS Google Scholar
  32. Di Noia, J.M. & Neuberger, M.S. Immunoglobulin gene conversion in chicken DT40 cells largely proceeds through an abasic site intermediate generated by excision of the uracil produced by AID-mediated deoxycytidine deamination. Eur. J. Immunol. 34, 504–548 (2004).
    Article CAS Google Scholar
  33. Butler, J.E. Immunoglobulin diversity, B-cell and antibody repertoire development in large farm animals. Rev. Sci. Tech. 17, 43–70 (1998).
    Article CAS Google Scholar
  34. 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).
    Article CAS Google Scholar
  35. Thompson, C.B. & Neiman, P.E. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell 48, 369–378 (1987).
    Article CAS Google Scholar
  36. Rogozin, I.B., Basu, M.K., Jordan, I.K., Pavlov, Y.I. & Koonin, E.V. APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 4, 1281–1285 (2005).
    Article CAS Google Scholar
  37. Gourzi, P., Leonova, T. & Papavasiliou, F.N. A role for activation-induced cytidine deaminase in the host response against a transforming retrovirus. Immunity 24, 779–786 (2006).
    Article CAS Google Scholar
  38. Flajnik, M.F. Comparative analyses of immunoglobulin genes: surprises and portents. Nat. Rev. Immunol. 2, 688–698 (2002).
    Article CAS Google Scholar
  39. Li, J. et al. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7, 1116–1124 (2006).
    Article CAS Google Scholar
  40. Kuraku, S. & Kuratani, S. Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zoolog. Sci. 23, 1053–1064 (2006).
    Article CAS Google Scholar
  41. Litman, G.W., Cannon, J.P. & Rast, J.P. New insights into alternative mechanisms of immune receptor diversification. Adv. Immunol. 87, 209–236 (2005).
    Article CAS Google Scholar
  42. Huang, X., Wang, J., Aluru, S., Yang, S.P. & Hillier, L. PCAP: a whole-genome assembly program. Genome Res. 13, 2164–2170 (2003).
    Article CAS Google Scholar
  43. Altschul, S.F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
    Article CAS Google Scholar
  44. Notredame, C., Higgins, D.G. & Heringa, J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205–217 (2000).
    Article CAS Google Scholar
  45. Cuff, J.A., Clamp, M.E., Siddiqui, A.S., Finlay, M. & Barton, G.J. JPred: a consensus secondary structure prediction server. Bioinformatics 14, 892–893 (1998).
    Article CAS Google Scholar
  46. Holm, L. & Sander, C. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20, 478–480 (1995).
    Article CAS Google Scholar
  47. Bruno, W.J., Socci, N.D. & Halpern, A.L. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol. 17, 189–197 (2000).
    Article CAS Google Scholar
  48. Hasegawa, M., Kishino, H. & Saitou, N. On the maximum likelihood method in molecular phylogenetics. J. Mol. Evol. 32, 443–445 (1991).
    Article CAS Google Scholar
  49. Adams, W.T. & Skopek, T.R. Statistical test for the comparison of samples from mutational spectra. J. Mol. Biol. 194, 391–396 (1987).
    Article CAS Google Scholar

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