Ancient evolutionary origin of diversified variable regions demonstrated by crystal structures of an immune-type receptor in amphioxus (original) (raw)

References

  1. Orengo, C.A. & Thornton, J.M. Protein families and their evolution—a structural perspective. Annu. Rev. Biochem. 74, 867–900 (2005).
    Article CAS Google Scholar
  2. Bork, P., Holm, L. & Sander, C. The immunoglobulin fold. Structural classification, sequence patterns and common core. J. Mol. Biol. 242, 309–320 (1994).
    CAS Google Scholar
  3. Barclay, A.N. Membrane proteins with immunoglobulin-like domains–a master superfamily of interaction molecules. Semin. Immunol. 15, 215–223 (2003).
    Article CAS Google Scholar
  4. Hunkapiller, T. & Hood, L. Diversity of the immunoglobulin gene superfamily. Adv. Immunol. 44, 1–62 (1989).
    Article CAS Google Scholar
  5. Eason, D.D. et al. Mechanisms of antigen receptor evolution. Semin. Immunol. 16, 215–226 (2004).
    Article CAS Google Scholar
  6. Chothia, C., Gelfand, I. & Kister, A. Structural determinants in the sequences of immunoglobulin variable domains. J. Mol. Biol. 278, 457–479 (1998).
    Article CAS Google Scholar
  7. Garrett, T.P., Wang, J., Yan, Y., Liu, J. & Harrison, S.C. Refinement and analysis of the structure of the first two domains of human CD4. J. Mol. Biol. 234, 763–778 (1993).
    Article CAS Google Scholar
  8. Leahy, D.J., Axel, R. & Hendrickson, W.A. Crystal structure of a soluble form of the human T cell coreceptor CD8 at 2.6 Å resolution. Cell 68, 1145–1162 (1992).
    Article CAS Google Scholar
  9. Cantoni, C. et al. The three-dimensional structure of the human NK cell receptor NKp44, a triggering partner in natural cytotoxicity. Structure (Camb.) 11, 725–734 (2003).
    Article CAS Google Scholar
  10. Laird, D.J., De Tomaso, A.W., Cooper, M.D. & Weissman, I.L. 50 million years of chordate evolution: seeking the origins of adaptive immunity. Proc. Natl. Acad. Sci. USA 97, 6924–6926 (2000).
    Article CAS Google Scholar
  11. Litman, G.W., Cannon, J.P. & Dishaw, L.J. Reconstructing immune phylogeny: new perspectives. Nat. Rev. Immunol. 5, 866–879 (2005).
    Article CAS Google Scholar
  12. Desmyter, A. et al. Crystal structure of a camel single-domain VH antibody fragment in complex with lysozyme. Nat. Struct. Biol. 3, 803–811 (1996).
    Article CAS Google Scholar
  13. 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 305, 1770–1773 (2004).
    Article CAS Google Scholar
  14. Garcia, K.C. et al. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166–1172 (1998).
    Article CAS Google Scholar
  15. Cannon, J.P., Haire, R.N. & Litman, G.W. Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat. Immunol. 3, 1200–1207 (2002).
    Article CAS Google Scholar
  16. Cannon, J.P., Haire, R.N., Schnitker, N., Mueller, M.G. & Litman, G.W. Individual protochordates possess unique immune-type receptor repertoires. Curr. Biol. 14, R465–R466 (2004).
    Article CAS Google Scholar
  17. Davis, M.M. & Bjorkman, P.J. T-cell antigen receptor genes and T-cell recognition. Nature 334, 395–402 (1988).
    Article CAS Google Scholar
  18. Medzhitov, R. & Janeway, C.A., Jr Advances in immunology: innate immunity. N. Engl. J. Med. 343, 338–344 (2000).
    Article CAS Google Scholar
  19. Zhang, S-M., Adema, C.M., Kepler, T.B. & Loker, E.S. Diversification of Ig superfamily genes in an invertebrate. Science 305, 251–254 (2004).
    Article CAS Google Scholar
  20. Watson, F.L. et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309, 1874–1878 (2005).
    Article CAS Google Scholar
  21. Wang, J.W. et al. SAD phasing by combination of direct methods with the SOLVE/RESOLVE procedure. Acta Crystallogr. D Biol. Crystallogr. 60, 1244–1253 (2004).
    Article CAS Google Scholar
  22. Schneider, T.R. & Sheldrick, G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772–1779 (2002).
    Article Google Scholar
  23. Carter, P., Andersen, C.A. & Rost, B. DSSPcont: Continuous secondary structure assignments for proteins. Nucl. Acids Res. 31, 3293–3295 (2003).
    Article CAS Google Scholar
  24. Holm, L. & Sander, C. Protein folds and families: sequence and structure alignments. Nucl. Acids Res. 27, 244–247 (1999).
    Article CAS Google Scholar
  25. Dauter, Z., Lamzin, V.S. & Wilson, K.S. The benefits of atomic resolution. Curr. Opin. Struct. Biol. 7, 681–688 (1997).
    Article CAS Google Scholar
  26. Babu, M.M. NCI: A server to identify non-canonical interactions in protein structures. Nucl. Acids Res. 31, 3345–3348 (2003).
    Article CAS Google Scholar
  27. Kolodny, R., Koehl, P. & Levitt, M. Comprehensive evaluation of protein structure alignment methods: scoring by geometric measures. J. Mol. Biol. 346, 1173–1188 (2005).
    Article CAS Google Scholar
  28. Li, H. et al. Structure of the Vδ domain of a human γδ T-cell antigen receptor. Nature 391, 502–506 (1998).
    Article CAS Google Scholar
  29. Clements, C.S. et al. The crystal structure of myelin oligodendrocyte glycoprotein, a key autoantigen in multiple sclerosis. Proc. Natl. Acad. Sci. USA 100, 11059–11064 (2003).
    Article CAS Google Scholar
  30. van Raaij, M.J., Chouin, E., van der Zandt, H., Bergelson, J.M. & Cusack, S. Dimeric structure of the coxsackievirus and adenovirus receptor D1 domain at 1.7 Å resolution. Structure 8, 1147–1155 (2000).
    Article CAS Google Scholar
  31. Ostrov, D.A., Shi, W., Schwartz, J.C., Almo, S.C. & Nathenson, S.G. Structure of murine CTLA-4 and its role in modulating T cell responsiveness. Science 290, 816–819 (2000).
    Article CAS Google Scholar
  32. Kaufman, J. The origins of the adaptive immune system: whatever next? Nat. Immunol. 3, 1124–1125 (2002).
    Article CAS Google Scholar
  33. Rudolph, M.G., Luz, J.G. & Wilson, I.A. Structural and thermodynamic correlates of T cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31, 121–149 (2002).
    Article CAS Google Scholar
  34. Luz, J.G. et al. Structural comparison of allogeneic and syngeneic T cell receptor-peptide-major histocompatibility complex complexes: a buried alloreactive mutation subtly alters peptide presentation substantially increasing V(β) Interactions. J. Exp. Med. 195, 1175–1186 (2002).
    Article CAS Google Scholar
  35. Lo Conte, L., Chothia, C. & Janin, J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177–2198 (1999).
    Article Google Scholar
  36. Suzuki, T., Shin, I., Fujiyama, A., Kohara, Y. & Kasahara, M. Hagfish leukocytes express a paired receptor family with a variable domain resembling those of antigen receptors. J. Immunol. 174, 2885–2891 (2005).
    Article CAS Google Scholar
  37. Haruta, C., Suzuki, T. & Kasahara, M. Variable domains in hagfish: NICIR is a polymorphic multigene family expressed preferentially in leukocytes and is related to lamprey TCR-like. Immunogenetics 58, 216–225 (2006).
    Article CAS Google Scholar
  38. Seeger, M.A. & Kaufman, T.C. Characterization of amalgam: a member of the immunoglobulin superfamily from Drosophila. Cell 55, 589–600 (1988).
    Article CAS Google Scholar
  39. Streltsov, V.A. et al. Structural evidence for evolution of shark Ig new antigen receptor variable domain antibodies from a cell-surface receptor. Proc. Nat. Acad. Sci. USA 101, 12444–12449 (2004).
    Article CAS Google Scholar
  40. Cannon, J.P., Haire, R.N., Rast, J.P. & Litman, G.W. The phylogenetic origins of the antigen binding receptors and somatic diversification mechanisms. Immunol. Rev. 200, 12–22 (2004).
    Article CAS Google Scholar
  41. Raskin, D.M., Seshadri, R., Pukatzki, S.U. & Mekalanos, J.J. Bacterial genomics and pathogen evolution. Cell 124, 703–714 (2006).
    Article CAS Google Scholar
  42. Chatterji, M., Tsai, C.L. & Schatz, D.G. New concepts in the regulation of an ancient reaction: transposition by RAG1/RAG2. Immunol. Rev. 200, 261–271 (2004).
    Article CAS Google Scholar
  43. 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
  44. Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006).
    Article CAS Google Scholar
  45. Hernandez Prada, J.A., Haire, R.N., Cannon, J.P., Litman, G.W. & Ostrov, D.A. Crystallization and preliminary x-ray analysis of VCBP3 from Branchiostoma floridae. Acta Crystallogr. D Biol. Crystallogr. 60, 2022–2024 (2004).
    Article Google Scholar
  46. Weeks, C.M. et al. Automatic solution of heavy-atom substructures. Methods Enzymol. 374, 37–83 (2003).
    Article CAS Google Scholar
  47. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997).
    Article CAS Google Scholar
  48. Kantardjieff, K.A. & Rupp, B. Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals. Protein Sci. 12, 1865–1871 (2003).
    Article CAS Google Scholar
  49. Terwilliger, T.C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849–861 (1999).
    Article CAS Google Scholar
  50. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47, 110–119 (1991).
    Article Google Scholar
  51. Brunger, A.T. et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921 (1998).
    Article CAS Google Scholar
  52. Laskowski, R.A., Moss, D.S. & Thornton, J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049–1067 (1993).
    Article CAS Google Scholar
  53. McRee, D.E. XtalView/Xfit–A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156–165 (1999).
    Article CAS Google Scholar
  54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
    Article Google Scholar
  55. Lefranc, M.P. et al. IMGT-ONTOLOGY for immunogenetics and immunoinformatics. In Silico Biol. 4, 17–29 (2004).
    CAS Google Scholar

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