Skip to main content
Log in

Antigen-specific receptors. Generation of the diversity from lamprey to human

  • Reviews
  • Published:
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

In the last century it was established that the diversity of the antigen-recognizing receptors of Band T-lymphocytes and Ig/antibodies in mice and humans is due to the random recombination of DNA segments organized in clusters and located in fetal genome far apart. During somatic rearrangement of genome these segments combine and form functional V-genes, coding antigen-specific receptors. In birds and some other animals the diversity is provided or increased by gene conversion, which leads to the diversification of nucleotide sequences in pre-rearranged functional V-genes. Recently it was shown that the generation of the diversity might be realized by an entirely different way. In most primitive and living now agnathan vertebrates, lamprey and hagfishes, Ig-genes are absent, and somatic diversification of the antigen-specific receptors is due to a stepwise assembly of functional V-genes from separate modules. These modules coding leucine-rich repeats (LRR) adjust to a single (or two) “incomplete” germ-line V-gene and insert into it by gene conversion. LRR modules lodge in so called DNA “cassettes”. The number of LRR in the agnathan genome reaches 2–3 thousands; primary structure of LRR is very variable. The properties of lamprey and hagfish antibodies differ from that of other vertebrates. It is extremely interesting that similar LRR are found in Toll-like receptors of insects, mollusks and even plants, where they provide the resistance to different diseases. The data obtained are very important for the evolutionary immunology. The review deals with the mechanisms of generation of diversity of the antigen-specific receptors in vertebrates, insects, and plants.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Edelman, G.M., Cunningham, B.A., Gall, W.E., Gottlieb, P.D., Rutishauser, U., and Waxdal, M.J., The Covalent Structure of an Entire Gamma G Immunoglobulin Molecule, Proc. Natl. Acad. Sci. USA, 1969, vol. 63,no. 1, pp. 78–85.

    Article  PubMed  CAS  Google Scholar 

  2. Porter, R.R., The Hydrolysis of Rabbit γ-Globulin and Antibodies with Crystalline Papain, Biochem. J., 1959, vol. 73, pp. 119–126.

    PubMed  CAS  Google Scholar 

  3. Wu, T.T. and Kabat, E.A., An Analysis of the Sequences oBottom of Formf the Variable Regions of Bence-Jones Protein and myeloma Light Chains and Their Implications for Antibody Complementarity, J. Exp. Med., 1970, vol. 132, no. 2, pp. 211–250.

    Article  PubMed  CAS  Google Scholar 

  4. Dreyer, W.J. and Bennett, J.C., the Molecular Basis of Antibody Formation: A Paradox, Proc. Natl. Acad. Sci. USA, 1965, vol. 54, no. 3, pp. 864–869.

    Article  PubMed  CAS  Google Scholar 

  5. Hozumi, N. and Tonegawa, S., Evidence for Somatic Rearrangement of Immunoglobulin Genes Coding for Variable and Constant Regions, Proc. Natl. Acad. Sci. USA, 1976, vol.73, pp. 3628–3634.

    Article  PubMed  CAS  Google Scholar 

  6. Leder, P., Honjo, T., Packman, S., Swan, D., Nau, M., and Norman, B., The Organization and Diversity of Immunoglobulin Genes, Proc. Natl. Acad. Sci. USA, 1974, vol. 71, no. 12, pp. 5109–5115.

    Article  PubMed  CAS  Google Scholar 

  7. Tonegawa, S., Somatic Generation of Antibody Diversity, Nature, 1983, vol. 302, no. 5909, pp. 575–578.

    Article  PubMed  CAS  Google Scholar 

  8. Gourvich, A.E. and Nezlin, R.S., DNA and Antibody and Gamma-Globulin Biosynthesis, Uspekhi Biol. Khimii (Rus.), 1969, vol.7, pp. 150–175.

    Google Scholar 

  9. Kabat, E.A., Origins of Antibody Complementarity, and Specificity-Hypervariable Regions and Minigene Hypothesis, J. Imunol., 1980, vol. 125, no. 3, pp. 961–969.

    CAS  Google Scholar 

  10. Wu, T.T. and Kabat, E.A., Fourteen Nucleotides in the Second Complementarity-Determining Region of a Human Heavy-Chain Variable Region Gene Are Identical with a Sequence in a Human D Minigene, Proc. Natl. Acad. Sci. USA, 1982, vol.79, no. 16, pp. 5031–5042.

    Article  PubMed  CAS  Google Scholar 

  11. Hammers-Casterman, C., Atarbouch, T., Muyldermans, S., Robinson, G., Hamers, C., Songa, E.B., Bendahman, N., and Hamers, R., Naturally Occurring Antibodies Devoid of Light Chains, Nature, 1993, vol. 363, no. 6428, pp. 446–448.

    Article  Google Scholar 

  12. Nguyen, V.K., and Hamers, R., Camel Heavy-Chain Antibodies: Diverse Germline VHH and Specific Mechanisms Enlarge the Antigen-Binding Repertoire, EMBO J., 2000, vol. 19, no. 5, pp. 921–930.

    Article  PubMed  CAS  Google Scholar 

  13. Spinelli, S., Frenken, L., Bourgeois, D., De Ron, L., Bos, W., Verrips, T., Anguille, C., Cambillau, C., and Tegoni, M., The Crystal Structure of a Lama Heavy Chain Variable Domain, Nat. Struct. Biol., 1996, vol. 3, no. 9, pp. 752–757.

    Article  PubMed  CAS  Google Scholar 

  14. Sidorova, E.V., Molecular Mechanisms of Generation of Immunoglobulin Diversity, Uspekhi Sovr. Biol. (Rus.), 1988, vol. 106, pp. 369–381.

    Google Scholar 

  15. Baltimore, D., Gene Conversion: Some Implications for Immunoglobulin Genes, Cell, 1981, vol. 26, no. 3, pp. 295–296.

    Article  PubMed  CAS  Google Scholar 

  16. Meselson, M.S. and Radding, C.M., A General Model for Genetic Recombination, Proc. Natl. Acad. Sci. USA, 1975, vol. 72, no. 1, pp. 358–361.

    Article  PubMed  CAS  Google Scholar 

  17. Kolchanov, N.A., Soloviev, V.V., and Rogozin I.B., Molecular Mechanisms of Somatic Hypermutagenesis in Immunoglobulin Genes, Doklady Akademii Nauk SSSR, (Rus.), 1985, vol. 281, pp. 994–999.

    CAS  Google Scholar 

  18. Cummings, W.J., Yabuki, M., Ordinaro, E.C., Bednarski, D.W., Quay, S., and Maizels N., Chromatin Structure Regulates Gene Conversion, Plos Biol., 2007, vol. 5, no. 10, pp. 246.

    Article  CAS  Google Scholar 

  19. Zimmermann, F.K., Tests for Recombinagenes in Fungi, Mutat. Res., 1992, vol. 284, no. 1, pp. 147–158.

    PubMed  CAS  Google Scholar 

  20. Papadakis, M.N. and Patrinos, G.P., Contribution of Gene Conversion in the Evolution of the Human Beta-Like Globin Gene Family, Hum. Genet., 1999, vol. 104, no. 2, pp. 117–125.

    Article  PubMed  CAS  Google Scholar 

  21. Reynaud, C.A., Dahan, A., Anquez, V., and Weill, J.C., Somatic Hyperconversion Diversifies the Single VH Gene of the Chicken with a High Incidence in the D Regions, Cell, 1989, vol. 59, no. 1, pp. 171–183.

    Article  PubMed  CAS  Google Scholar 

  22. Reynaud, C.A., Anquez, V., Grimal H., and Weill, J.C., A Hyperconversion Mechanism Generates the Chicken Light Chain Preimmune Repertoire, Cell, 1987, vol. 48, no. 3, pp. 379–388.

    Article  PubMed  CAS  Google Scholar 

  23. Thompson, C.B. and Neiman, O.E., Somatic Diversification of the Chicken Immunoglobulin Light Chain Gene Is Limited to the Rearranged Variable Gene Segment, Cell, 1987, vol. 48, no. 3, pp. 369–378.

    Article  PubMed  CAS  Google Scholar 

  24. Ota, T. and Nei, M., Evolution of Immunoglobulin VH Pseudogenes in Chickens, Mol. Biol. Evol., 1995, vol. 12, no. 1, pp. 94–102.

    PubMed  CAS  Google Scholar 

  25. Blanden, R.V., Lendly, R.A., and Steel, E.G., Chto esli Lamark prav? Immunogenetika I Evolutsija (What if Lamark Is Right? Immunogenetics and Evolution), Moscow, Mir, 2002.

    Google Scholar 

  26. Ratcliffe, M.J., Antibodies, Immunoglobulin Genes and the Bursa of Fabricius in Chicken B Cell Development, Dev. Comp. Immunol., 2006, vol. 30, nos. 1–2, pp. 101–118.

    Article  PubMed  CAS  Google Scholar 

  27. Masteller, E.L., Pharr, G.T., Funk, P.E., and Thompson, C.B., Avian B Cell Development, Int. Rev. Immunol., 1997, vol. 15, nos. 3–4, pp. 185–206.

    PubMed  CAS  Google Scholar 

  28. Arakawa, H. and Buerstedde, J.-M., Immunoglobulin Gene Conversion: Insight from Bursa B Cells and DT40 Cell Line, Development Dynamics, 2004, vol. 229, pp. 458–464.

    Article  CAS  Google Scholar 

  29. Kruithof, E.K., Satta, N., Liu, J.W., Dunoyergeindre, S., and Fish, R.J., Gene Conversion Limits Divergence of Mammalian TLR1 and TLR6, BMC Evol. Biol., 2007, vol. 7, pp. 148–158.

    Article  PubMed  CAS  Google Scholar 

  30. Conticello, S.G., The AID/APOBEC Family of Nucleic Acid Mutators, Genome Biol., 2008, vol. 9, no. 6, pp. 229–244.

    Article  PubMed  CAS  Google Scholar 

  31. Conticello, S.G., Thomas C.J., Petersen-Mahrt, S.K., and Neuberger, M.S., Evolution of AID/APOBEC Family of Polynucleotide (Deoxy)Cytidine Deaminases, Mol. Biol. Evol., 2005, vol. 22, no. 2, pp. 367–377.

    Article  PubMed  CAS  Google Scholar 

  32. Gopal, A.R. and Fugmann, S.D., AID-Mediated Diversification within the Igl Locus of Chicken DT40 Cells Is Restricted to the Transcribed IgL Gene, Mol. Immunol., 2008, vol. 45, no. 7, pp. 2062–2068.

    Article  PubMed  CAS  Google Scholar 

  33. Kothapalli, N., Norton, D.D., and Fumgann, S.D., Cutting Edge: A cis-Acting LNA Element Targets AIDMediated Sequence Diversification the Chicken Ig Light Chain Gene Locus, J. Immunol., 2008, vol. 180, no. 4, pp. 2019–2023.

    PubMed  CAS  Google Scholar 

  34. Muramatsu, M., Sankaranand, V.S., Anant, S., Sugai, M., Kinoshita, K., Davidson, N.O., and Honjo, T., Specific Expression of Activation-Induced Cytidine Deaminase (AID), a Novel Member of the RNA-Specific Editing Deaminase Family in Germinal Center B Cells, J. Biol. Chem., 1999, vol. 274, no. 26, pp. 18470–18476.

    Article  PubMed  CAS  Google Scholar 

  35. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T., Class Switch Recombination and Hypermutation Require Activation-Induced Cytidine Deaminase (AID), a Potential RNA Editing Enzyme, Cell, 2000, vol. 102, no. 5, pp. 553–563.

    Article  PubMed  CAS  Google Scholar 

  36. Saribasak, H., Saribasak, N.N., Ipek, F.M., Ellwart, J.W., Arakawa, H., and Buerstedde, J.M., Uracil DNA Glycosilase Disruption Blocks Ig Gene Conversion and Induces Transition Mutations, J. Immunol., 2006, vol. 176., no. 1, pp. 365–371.

    PubMed  Google Scholar 

  37. Navaratnam, N. and Sarwar, R., An Overview of Cytidine Deaminases, Int. J. Hematol., 2006, vol. 83, no. 3, pp. 195–200.

    Article  PubMed  CAS  Google Scholar 

  38. Chaudhuri, J., Basu, U., Zarrin, A., Yan, C., Franco, S., Perlot, T., Vuong, B., Phan, R.T., Datta, A., Manis, J., and Ält, F.W., Evolution of the Immunoglobulin Heavy Chain Class Switch Combination Mechanism, Adv. Immunol., 2007, vol. 94, pp. 157–214.

    Article  PubMed  CAS  Google Scholar 

  39. Arakawa, Y., Saribasak, H., and Buerstedde, J.M., Activation-Induced Cytidine Deaminase Initiates Immunoglobulin Gene Conversion and Hypermutation by a Common Intermediate, Plos, 2004, vol. 2, no. 7, pp. E179.

    Article  Google Scholar 

  40. Arakawa, Y., Hauschild, J., and Buerstedde J.M., Requirement of the Activation-Induced Deaminase (AID) Gene for Immunoglobulin Gene Conversion, Science, 2002, vol. 295, pp. 1301–1306.

    Article  PubMed  CAS  Google Scholar 

  41. Stavnezer, J. and Amemiya, C.T., Evolution of Isotype Switching, Semin. Immunol., 2004, vol. 16, no. 4, pp. 257–275.

    Article  PubMed  CAS  Google Scholar 

  42. Sitnikova, T. and Su, C., Coevolution of Immunoglobulin Heavy- and Light-Chain Variable-Region Gene Families, Mol. Biol. Evol., 1998, vol.15, no. 6, pp. 617–625.

    PubMed  CAS  Google Scholar 

  43. Hinds-Frey, K.R., Nishikata, H., Lirman, R.T., and Litman, G.W., Somatic Variation Precedes Extensive Diversification of Germline Sequences and Combinatorial Joining in the Evolution of Immunoglobulin Heavy Chain Diversity, J. Exp. Med.,, 1993, vol.178, no. 3, pp. 815–824.

    Article  PubMed  CAS  Google Scholar 

  44. Kokubo, F., Litman, R., Shamblott, M.J., Hinds, K., and Litman G.W., Diverse Organization of Immunoglobulin VH Gene Loci in A Primitive Vertebrate, EMBO J., 1988, vol. 7, no. 1, pp. 3413–3422.

    Google Scholar 

  45. Fleurant, M., Changchien, L., Chtn, C.T., Flajnik, V.F., and Hsu E., Shark Ig Light Chain Functions Are As Diverse As in Heavy Chains, J. Immunol., 2004, vol. 173, no. 9, pp. 5574–5582.

    PubMed  CAS  Google Scholar 

  46. Adler, M.N., Herrin, B.R., Sadionova, A., Stockard, C.R., Grizzle, W.E., Gartland, L.A., Gartland, G.L., Boydston, J.A., Turnbough, C.L., Jr., and Cooper, M.D., Antibody Responses of Variable Lymphocyte Receptors in He Lamprey, Nat. Immunol., 2008, vol. 9, pp. 319–327.

    Article  CAS  Google Scholar 

  47. Adler, M.N., Rogozin I. B., and Lyer, L.M., Diversity and Function of Adaptive Immune Receptors in a Jawless Vertebrate, Science, 2005, vol. 310, pp. 309–319.

    Article  Google Scholar 

  48. Cooper, M.D. and Adler, M.N., The Evolution of Adaptive Immune Systems, Cell, 2006, vol. 124, no. 4, pp. 815–822.

    Article  PubMed  CAS  Google Scholar 

  49. Anastassiou, D., Liu, H., and Varadan, V., Variable Window Binding for Mutually Exclusive Alternative Splicing, Genome Biol., 2006, vol. 7, no. 1, p. R2.

  50. Pancer, Z., Saha, N.R., Kasamatsu, J., Suzuki, T., Amemiya, C., Kasahara, M., and Cooper, M.D., Variable Lymphocyte Receptors in Hagfish, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 26, pp. 9224–9229.

    Article  PubMed  CAS  Google Scholar 

  51. Pancer, Z., Amemiya, C.T., Ehrhardt, G.R., Ceitlin, J., Gartland, G.L., and Cooper M.D., Somatic Diversification of Variable Lymphocyte Receptors in the Agnathan Sea Lamprey, Nature, 2004, vol. 430, no. 6996, pp. 174–180.

    Article  PubMed  CAS  Google Scholar 

  52. Kim, Ho Min, Oh, S.C., Lim, K.J., Kasamatsu, J., Heo, Y., Park, B.S., Lee, H., Yoo, O.J., Kasayara, M., and Lee, J.-O., Structural Diversity of the Hagfish Variable Lymphocyte Receptors, J. Biol. Chem., 2007, vol. 282, no. 9, pp. 6726–6732.

    Article  PubMed  CAS  Google Scholar 

  53. Kasamatsu, J., Suzuki, T., Ishijima, J., Matsuda, Y., and Kasahara, M., Two Variable Lymphocyte Receptor Genes of the Inshore Hagfish Are Located Far Apart on the Same Chromosome, Immunogenetics, 2007, vol. 59, no. 4, pp. 329–331.

    Article  PubMed  CAS  Google Scholar 

  54. Rogozin, I.B., Iyer, L.M., Liang, L., Glazko, G.V., Liston, V.G., Pavlov, Y.I., Aravind L., and Pancer, Z., Evolution and Diversification of Lamprey Antigen Receptors: Evidence for Involvement of an AID-APOBEC Family Cytosine Deaminase, Nat. Immunol., 2007, vol. 8, pp. 647–656.

    Article  PubMed  CAS  Google Scholar 

  55. Nagawa, F., Kishishita, N., Shimizu, K., Hirose, S., Miyoshi, M., Nezu, J., Nishimura, T., Nishizumi, H., Takahashi Y., Hashimoto, S-I., Takeuchi, M., Atsushi, M., Takemori, T., Otsuka, A.J., and Sakano H., Antigen-Receptor Genes of the Agnathan Lamprey Are Assembled by a Process Involving Copy Choice, Nat. Immunol., 2006, vol. 8, pp. 206–213.

    Article  PubMed  CAS  Google Scholar 

  56. Lada, A.G., Iyer, L.M., Rogozin, I.B., Aravind, L., and Pavlov I., Vertebrate Immunity: Mutator Proteins and Their Evolution, Genetika (Rus.), 2007, vol. 43, no. 10, pp.1311–1327.

    CAS  Google Scholar 

  57. Han, B.W., Herrin, B.R., Cooper, M.D., and Wilson I.A., Antigen Recognition by Variable Lymphocyte Receptors, Science, 2008, vol. 321, no. 5897, pp. 1834–1837.

    Article  PubMed  CAS  Google Scholar 

  58. Herrin, B.R., Adler, M.N., Rou, K.H., Sina, C., Ehrhardt, G.R.A., Boydston, J.A., Turnbough, C.L.,Jr., and Cooper M.D., Structure and Specificity of Lamprey Monoclonal Antibodies, Proc. Natl. Acad. Sci. USA, 2008, vol.105, no. 6, pp. 2040–2045.

    Article  PubMed  Google Scholar 

  59. Iwasaki, A. and Medzhitov, R., Toll-Like Receptor Control of the Adaptive Immune Responses, Nat. Immunol., 2004, vol.5, no. 10, pp. 987–995.

    Article  PubMed  CAS  Google Scholar 

  60. Ishii, A., Matsuo, A., Sawa, H., Tsujita, T., Shida, K., Matsumoto, M., and Seya, T., Lamprey TLRs with Properties Distinct from Those of the Variable Lymphocyte Receptors, J. Immunol., 2007, vol. 178, pp. 397–406.

    PubMed  CAS  Google Scholar 

  61. Takeuchi, O. and Akira, S., Toll-Like Receptors: Their Physiological Role and Signal Transduction System, Int. Immunopharmacol., 2001, vol.1, no. 4, pp. 625–635.

    Article  PubMed  CAS  Google Scholar 

  62. Xu, H., An, H., Yu, Y., Zhang, M., Qi, R., and Cao, X., Ras Participates in CPG Oligodeoxynucleotide Signaling through Association with Toll-Like Receptor 9 and Promotion of Interleukine-1 Receptor-Associated Kinase/Tumor Necrosis Factor Receptor-Associated Factor 6 Complex Formation in Macrophages, J. Biol. Chem., 2003, vol. 278, no. 38, pp. 36334–36340.

    Article  PubMed  CAS  Google Scholar 

  63. Muzio, M., Polentarutti, N., Bosisio, D., Prahladan, M.K.P., and Manovani, A., Toll-Like Receptors: A Growing Family of Immune Receptors That Are Differentially Expressed and Regulated by Different Leukocytes, J. Leukoc. Biol., 2000, vol. 67, pp. 450–456.

    PubMed  CAS  Google Scholar 

  64. Gurujan, M., Jacob, J., and Pulendran, B., Toll-Like Receptor Expression and Responsiveness of Distinct Murine Splenic and Mucosal B-Cell Subsets, Plos One, 2007, vol. 2, no. 9, p. E863.

    Article  CAS  Google Scholar 

  65. Huang, S., Yuan, S., Guo, L., Yu, Y., Li, J., Wu, T., Liu, T., Yang, M., Wu, K., Liu, H., Ge, J., Yu, Y., Huang, H., Dong, M., Yu, C., Chen, S., and Xu, A., Genomic Analysis of the Immune Gene Repertoire of Amphioxus Reveals Extraordinary Innate Complexity and Diversity, Genome Res., 2008, vol. 18, no. 7, pp. 1112–1126.

    Article  PubMed  CAS  Google Scholar 

  66. Pasare, C. and Medzhitov, R., Control of B-Cell Responses by Toll-Like Receptors, Nature, 2005, vol. 438, pp. 364–368.

    Article  PubMed  CAS  Google Scholar 

  67. Edry, E., Azualay-Debby Y., and Melamed, D., Toll-Like Receptor Ligands Stimulate Aberrant Class Switch Recombination in Early B Cell Precursors, Int. Immunol., 2008, vol. 20, no. 12, pp. 1575–1585.

    Article  PubMed  CAS  Google Scholar 

  68. Salaun, B., Romero, P., and Lebecque, S., Toll-Like Receptors Two-Edged Sword: When Immunity Meets Apoptosis, Eur. J. Immunol., 2007, vol. 37, pp. 3311–3318.

    Article  PubMed  CAS  Google Scholar 

  69. Rock, F.L., Hardiman, G., Timans, J.C., Kastelein, R.A., and Bazan J.F., A Family of Human Receptors Structurally Related to Drosophila Toll, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, no. 2, pp. 588–593.

    Article  PubMed  CAS  Google Scholar 

  70. Jin, M.S. and Lee, J.O., Structure of TLR-Ligand Complexes, Curr. Opin. Immunol., 2008, vol.20, N.4, pp. 414–419.

    Article  PubMed  CAS  Google Scholar 

  71. Jin, M.S. and Lee J.O., Structures of the Toll-Like Receptor Family and Its Ligand Complexes, Immunity, 2008, vol. 29, no. 2, pp. 182–191.

    Article  PubMed  CAS  Google Scholar 

  72. Bell, J.K., Mullen, G.E., Leifer, C.A., Davis, D.R., and Segal, D.M., Leucine-Rich Repeats and Pathogen Recognition in Toll-Like Receptors, Trends Immunol., 2003, vol. 24, pp. 528–533.

    Article  PubMed  CAS  Google Scholar 

  73. Matsushima, N., Tanaka, T., Enkhbayar, P., Mikami, T., Taga, M., Yamada, K., and Kuroki, Y., Comparative Sequence Analysis of Leucine-Rich Repeats (LRRs) within Vertebrate Toll-Like Receptors, BMC Genomics, 2007, vol. 8, pp. 124–144.

    Article  PubMed  CAS  Google Scholar 

  74. Yang, L.S., Yin Z.X., Liao, J.X., Huang, X.D., Guo, C.J., Weng, S.P., Chan, S.M., Yu, X.Q., and He, J.G., A Toll Receptor in Shrimp, Mol. Immunol., 2007, vol. 44, no. 8, pp. 1999–2008.

    Article  PubMed  CAS  Google Scholar 

  75. Heguy, A., Baldari, C.T., Vacchia, G., Telford, J.L., and Melli, M., Amino Acids Conserved in Interleukin-1 Receptors (IL-1Rs) and the Drosophila Toll-Protein Are Essential for IL-1R Signal Transduction, J. Biol. Chem., 1992, vol. 267, no. 4, pp. 2605–2609.

    PubMed  CAS  Google Scholar 

  76. Bosh, T.C., Augustin, R., Anton-Erxleben, F., and Fraune, S., Uncovering the Evolutionary History of Innate Immunity: The Simple Metazoan Hydra Uses Epithelial Cells for Host Defense, Dev. Comp. Immunol., 2009, vol. 33, no. 4, pp. 559–569.

    Article  CAS  Google Scholar 

  77. Qiu, L., Song, L., Xu, W., Ni, D., and Yu, Y., Molecular Cloning and Expression of a Toll Receptor Gene Homologue from Zhikong Scallop, Chiamys farreri, Fish Shellfish Immunol., 2007, vol. 22, no. 5, pp. 451–456.

    Article  CAS  Google Scholar 

  78. Ting, J.P. and Davis, B.K., CATERPILLER: A Novel Gene Family Important in Immunity, Cell Death and Diseases, Annu. Rev. Immunol., 2005, vol. 23, pp. 387–414.

    Article  PubMed  CAS  Google Scholar 

  79. He, C.Y., Tian, A.G., Zhang, J.S., Zhang, Z.Y., Gai, J.Y., and Chen, S.Y., Isolation and Characterization of a Full-Length Resistance Gene Homolog from Soybean, Theor. Appl. Genet., 2003, vol. 106, no. 5, pp. 786–793.

    PubMed  CAS  Google Scholar 

  80. Baumgarten, A., Cannon, S., Spangler, R., and May, G., Genome-Level Evolution of Resistance Genes in Arabidopsis thaliana, Genetics, 2003, vol.165, pp. 309–319.

    PubMed  CAS  Google Scholar 

  81. Walker, J.C. and Zhang, R., Relationship of a Putative Receptor Protein Kinase from Maize to the S-Locus Glycoproteins of Brassica, Nature, 1990, vol. 6277, pp. 743–746.

    Article  Google Scholar 

  82. Dievart, A. and Clark, S., LRR-Containing Receptors Regulating Plant Development and Defense, Development, 2004, vol. 131, pp. 251–261.

    Article  PubMed  CAS  Google Scholar 

  83. Padmanabhan, M., Cournoyer, P., and Dinesh-Kumar S.P., The Leucine-Rich Repeat Domain in Plant Innate Immunity: A Wealth of Possibilities, Cell. Microbiol., 2009, vol. 11, no. 2, pp. 191–198.

    Article  PubMed  CAS  Google Scholar 

  84. Richter, T.E. and Ronald, P.C., The Evolution of Disease Resistance Genes, Plant Mol. Biol., 2000, vol. 42, no. 1, pp. 195–204.

    Article  PubMed  CAS  Google Scholar 

  85. Mondragon-Palomino, M. and Gaut, B.S., Gene Conversion and the Evolution of Three Leucine-Rich Repeat Gene Families in Arabidopsis thaliana, Mol. Biol. Evol., 2005, vol. 22, no. 12, pp. 2444–2456.

    Article  PubMed  CAS  Google Scholar 

  86. Rogozin, I.B., Wulf, Yu. I., Babenko, V.I., and Kunin, E.V., Genome Evolution and the Principle of Maximal Parsimony, Vestnik VOG i S (Rus.), 2005, vol. 9, no. 2, p. 141.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. V. Sidorova.

Additional information

Original Russian Text © E.V. Sidorova, 2009, published in Biologicheskie Membrany, 2009, Vol. 26, No. 5, pp. 339–351.

The article was translated by the author.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sidorova, E.V. Antigen-specific receptors. Generation of the diversity from lamprey to human. Biochem. Moscow Suppl. Ser. A 3, 345–355 (2009). https://doi.org/10.1134/S1990747809040011

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747809040011

Key words

Navigation