Advertisement

The Evolution of Adaptive Immunity

  • Nadia Danilova
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 738)

Abstract

The concept of adaptive immunity suggests de novo generation in each individual of extremely large repertoires of diversified receptors and selective expansion of receptors that match the antigen/pathogen. Accordingly, adaptive immune system is also called “anticipatory”. It allows each individual to have a unique repertoire of immune receptors corresponding to its life history. The memory of an antigen gets encoded in the clonal composition of the organism’s immune cells instead of being encoded in the genome. Consequently, the immune response to repeated encounter with the same antigen becomes stronger, a phenomenon called immunological memory. Elements of adaptive immunity are found at all taxonomical levels, whereas in vertebrates, adaptive mechanisms have become the cornerstone of the immune system. In jaw vertebrates, adaptive immune receptors of T and B lymphoid cells belong to immunoglobulin superfamily and are created by rearrangement of gene segments. In jawless vertebrates lamprey and hagfish, recombination of leucine-rich repeat modules is used to form variable lymphocyte receptors. Striking functional similarity of the cellular and humoral branches of these systems suggests similar driving forces underlying their development.

Keywords

Migration Inhibitory Factor Adaptive Immunity Adaptive Immune System Whole Genome Duplication Class Switch Recombination 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20:197–216.PubMedGoogle Scholar
  2. 2.
    Matzinger P. The danger model: a renewed sense of self. Science 2002; 296:301–305.PubMedGoogle Scholar
  3. 3.
    F rank M, Kirkman L, Costantini D et al. Frequent recombination events generate diversity within the multi-copy variant antigen gene families of Plasmodium falciparum. Int J Parasitol 2008; 38:1099–1109.PubMedGoogle Scholar
  4. 4.
    L azzaro BP, Sceurman BK, Clark AG. Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 2004; 303:1873–1876.PubMedGoogle Scholar
  5. 5.
    Messier-Solek C, Buckley KM, Rast JP. Highly diversified innate receptor systems and new forms of animal immunity. Semin Immunol 2010; 22:39–47.PubMedGoogle Scholar
  6. 6.
    Pal S, Wu LP. Lessons from the fly: pattern recognition in Drosophila melanogaster. Adv Exp Med Biol 2009; 653:162–174.PubMedGoogle Scholar
  7. 7.
    Watson FL, Puttmann-Holgado R, Thomas F et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005; 309:1874–1878.PubMedGoogle Scholar
  8. 8.
    Brites D, McTaggart S, Morris K et al. The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Mol Biol Evol 2008; 25:1429–1439.PubMedGoogle Scholar
  9. 9.
    Buckley KM, Terwilliger DP, Smith LC. Sequence variations in 185/333 messages from the purple sea urchin suggest posttranscriptional modifications to increase immune diversity. J Immunol 2008; 181:8585–8594.PubMedGoogle Scholar
  10. 10.
    Waterhouse PM, Wang MB, Lough T. Gene silencing as an adaptive defence against viruses. Nature 2001; 411:834–842.PubMedGoogle Scholar
  11. 11.
    Brouns SJ, Jore MM, Lundgren M et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008; 321:960–964.PubMedGoogle Scholar
  12. 12.
    Tonegawa S. Somatic generation of antibody diversity. Nature 1983; 302:575–581.PubMedGoogle Scholar
  13. 13.
    Schatz DG. V(D)J recombination. Immunol Rev 2004; 200:5–11.PubMedGoogle Scholar
  14. 14.
    Burnet FM. A modification of Jerne’s theory of antibody production using the concept of clonal selection. Aust J Sci 1957; 20:67–69.Google Scholar
  15. 15.
    Maizels N. Immunoglobulin gene diversification. Annu Rev Genet 2005; 39:23–46.PubMedGoogle Scholar
  16. 16.
    Paul WE. Fundamental Immunology. 5 ed. Philadelphia: Lippincott Williams and Wilkins 2008.Google Scholar
  17. 17.
    Pancer Z, Amemiya CT, Ehrhardt GRC et al. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 2004; 430:174–180.PubMedGoogle Scholar
  18. 18.
    Guo P, Hirano M, Herrin BR et al. Dual nature of the adaptive immune system in lampreys. Nature 2009; 459:796–801.PubMedGoogle Scholar
  19. 19.
    Rogozin IB, Iyer LM, Liang L et al. Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 2007; 8:647–656.PubMedGoogle Scholar
  20. 20.
    Litman GW, Cannon JP, Rast JP. New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 2005; 87:209–236.PubMedGoogle Scholar
  21. 21.
    Kasahara M. The 2R hypothesis: an update. Curr Opin Immunol 2007; 19:547–552.PubMedGoogle Scholar
  22. 22.
    Fugmann SD. The origins of the Rag genes-From transposition to V(D)J recombination. Semin Immunol 2010; 22:10–16.PubMedGoogle Scholar
  23. 23.
    Abram CL, Lowell CA. The expanding role for ITAM-based signaling pathways in immune cells. Sci STKE 2007; 2007:re2.PubMedGoogle Scholar
  24. 24.
    Alt FW, Baltimore D. Joining of immunoglobulin heavy chain gene segments: implications from a chromosome with evidence of three D-JH fusions. Proc Natl Acad Sci USA 1982; 79:4118–4122.PubMedGoogle Scholar
  25. 25.
    Cedar H, Bergman Y. Choreography of Ig allelic exclusion. Curr Opin Immunol 2008; 20:308–317.PubMedGoogle Scholar
  26. 26.
    Muramatsu M, Kinoshita K, Fagarasan S et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000; 102:553–563.PubMedGoogle Scholar
  27. 27.
    Liu M, Schatz DG. Balancing AID and DNA repair during somatic hypermutation. Trends Immunol 2009; 30:173–181.PubMedGoogle Scholar
  28. 28.
    Rogozin IB, Kolchanov NA. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim Biophys Acta 1992; 1171:11–18.PubMedGoogle Scholar
  29. 29.
    Chaudhuri J, Basu U, Zarrin A et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 2007; 94:157–214.PubMedGoogle Scholar
  30. 30.
    Chang B, Casali P. The CDR1 sequences of a major proportion of human germline Ig VH genes are inherently susceptible to amino acid replacement. Immunol Today 1994; 15:367–373.PubMedGoogle Scholar
  31. 31.
    Danilova N, Amemiya CT. Going adaptive: the saga of antibodies. Ann N Y Acad Sci 2009; 1168:130–155.PubMedGoogle Scholar
  32. 32.
    Gay D, Saunders T, Camper S et al. Receptor editing: an approach by autoreactive B-cells to escape tolerance. J Exp Med 1993; 177:999–1008.PubMedGoogle Scholar
  33. 33.
    Tiegs SL, Russell DM, Nemazee D. Receptor editing in self-reactive bone marrow B-cells. J Exp Med 1993; 177:1009–1020.PubMedGoogle Scholar
  34. 34.
    Ota T, Nei M. Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol Biol Evol 1994; 11:469–482.PubMedGoogle Scholar
  35. 35.
    Uche UN, Huber CR, Raulet DH et al. Recombination signal sequence-associated restriction on TCRdelta gene rearrangement affects the development of tissue-specific gammadelta T-cells. J Immunol 2009; 183:4931–4939.PubMedGoogle Scholar
  36. 36.
    Elliott JF, Rock EP, Patten PA et al. The adult T-cell receptor delta-chain is diverse and distinct from that of fetal thymocytes. Nature 1988; 331:627–631.PubMedGoogle Scholar
  37. 37.
    Rumfelt LL, Marilyn Diaz M, Lohr RL et al. Unprecedented Multiplicity of Ig Transmembrane and Secretory mRNA Forms in the Cartilaginous Fish. J Immunol 2004; 173:1129–1139.PubMedGoogle Scholar
  38. 38.
    Criscitiello MF, Flajnik MF. Four primordial immunoglobulin light chain isotypes, including lambda and kappa, identified in the most primitive living jawed vertebrates. Eur J Immunol 2007; 37:2683–2694.PubMedGoogle Scholar
  39. 39.
    Danilova N, Bussmann J, Jekosch K et al. The immunoglobulin heavy-chain locus in zebrafish:identification and expression of a previously unknown isotype, immunoglobulin Z. Nat Immunol. 2005; 6:295–302.PubMedGoogle Scholar
  40. 40.
    Wilson M, Bengten E, Miller NW et al. A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc Natl Acad Sci USA 1997; 94:4593–4597.PubMedGoogle Scholar
  41. 41.
    Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol 2008; 26:261–292.PubMedGoogle Scholar
  42. 42.
    Fagarasan S. Evolution, development, mechanism and function of IgA in the gut. Curr Opin Immunol 2008; 20:170–177.PubMedGoogle Scholar
  43. 43.
    Criscitiello MF, Saltis M, Flajnik MF. An evolutionarily mobile antigen receptor variable region gene: doubly rearranging NAR-TcR genes in sharks. Proc Natl Acad Sci USA 2006; 103:5036–5041.PubMedGoogle Scholar
  44. 44.
    Parra ZE, Baker ML, Schwarz RS et al. A unique T-cell receptor discovered in marsupials. Proc Natl Acad Sci USA 2007; 104:9776–9781.PubMedGoogle Scholar
  45. 45.
    Boehm T, Bleul CC. The evolutionary history of lymphoid organs. Nat Immunol 2007; 8:131–135.PubMedGoogle Scholar
  46. 46.
    Martinez-Borra J, Lopez-Larrea C. The emergence of Major Histocompatibility Complex In: Lopez-Larrea C, ed. Self and Nonself. Austin: Landes Bioscience; 2011.Google Scholar
  47. 47.
    Amemiya CT, Saha NR, Zapata A. Evolution and development of immunological structures in the lamprey. Curr Opin Immunol 2007; 19(5):535–541.PubMedGoogle Scholar
  48. 48.
    Alder MN, Rogozin IB, Iyer LM et al. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science 2005; 310:1970–1973.PubMedGoogle Scholar
  49. 49.
    Han BW, Herrin BR, Cooper MD et al. Antigen recognition by variable lymphocyte receptors. Science 2008; 321:1834–1837.PubMedGoogle Scholar
  50. 50.
    Pollara B, Litman GW, Finstad J et al. The evolution of the immune response. VII. Antibody to human “O” cells and properties of the immunoglobulin in lamprey. J Immunol 1970; 105:738–745.PubMedGoogle Scholar
  51. 51.
    Velikovsky CA, Deng L, Tasumi S et al. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen. Nat Struct Mol Biol 2009; 16:725–730.PubMedGoogle Scholar
  52. 52.
    Alder MN, Herrin BR, Sadlonova A et al. Antibody responses of variable lymphocyte receptors in the lamprey. Nat Immunol 2008; 9:319–327.PubMedGoogle Scholar
  53. 53.
    Tasumi S, Velikovsky CA, Xu G et al. High-affinity lamprey VLRA and VLRB monoclonal antibodies. Proc Natl Acad Sci USA 2009; 106:12891–12896.PubMedGoogle Scholar
  54. 54.
    Flajnik MF, Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 2009; 11:47–59.PubMedGoogle Scholar
  55. 55.
    Saha NR, Smith J, Amemiya CT. Evolution of adaptive immune recognition in jawless vertebrates. Semin Immunol 2010; 22:25–33.PubMedGoogle Scholar
  56. 56.
    Spanopoulou E, Zaitseva F, Wang FH et al. The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 1996; 87:263–276.PubMedGoogle Scholar
  57. 57.
    van Gent DC, Mizuuchi K, Gellert M. Similarities between initiation of V(D)J recombination and retroviral integration. Science 1996; 271:1592–1594.PubMedGoogle Scholar
  58. 58.
    Sakano H, Huppi K, Heinrich G et al. Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature 1979; 280:288–294.PubMedGoogle Scholar
  59. 59.
    Schatz DG. Antigen receptor genes and the evolution of a recombinase. Semin Immunol 2004; 16:245–256.PubMedGoogle Scholar
  60. 60.
    Kapitonov VV, Jurka J. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 2005; 3:e181.PubMedGoogle Scholar
  61. 61.
    Panchin Y, Moroz LL. Molluscan mobile elements similar to the vertebrate Recombination-Activating Genes. Biochem Biophys Res Commun 2008; 369:818–823.PubMedGoogle Scholar
  62. 62.
    Fugmann SD, Messier C, Novack LA et al. An ancient evolutionary origin of the Rag1/2 gene locus. Proc Natl Acad Sci USA 2006; 103:3728–3733.PubMedGoogle Scholar
  63. 63.
    Dreyfus DH. Paleo-immunology: evidence consistent with insertion of a primordial herpes virus-like element in the origins of acquired immunity. PLoS One 2009; 4:e5778.PubMedGoogle Scholar
  64. 64.
    Conticello SG. The AID/APOBEC family of nucleic acid mutators. Genome Biol 2008; 9:229.PubMedGoogle Scholar
  65. 65.
    Holland LZ, Albalat R, Azumi K et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 2008; 18:1100–1111.PubMedGoogle Scholar
  66. 66.
    Flajnik MF. Comparative analyses of immunoglobulin genes: surprises and portents. Nat Rev Immunol 2002; 2:688–698.PubMedGoogle Scholar
  67. 67.
    Gourzi P, Leonova T, Papavasiliou FN. Viral induction of AID is independent of the interferon and the Toll-like receptor signaling pathways but requires NF-kappaB. J Exp Med 2007; 204:259–265.PubMedGoogle Scholar
  68. 68.
    Davis BJ, Havener JM, Ramsden DA. End-bridging is required for pol mu to efficiently promote repair of noncomplementary ends by nonhomologous end joining. Nucleic Acids Res 2008; 36:3085–3094.PubMedGoogle Scholar
  69. 69.
    Rast JP, Messier-Solek C. Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biol Bull 2008; 214:274–283.PubMedGoogle Scholar
  70. 70.
    Du Pasquier L. Speculations on the origin of the vertebrate immune system. Immunol Lett 2004; 92:3–9.PubMedGoogle Scholar
  71. 71.
    van den Berg TK. On the origin and function of immune’ self’ recognition. Immunol Lett 2009; 128:24–25.PubMedGoogle Scholar
  72. 72.
    Tsai RK, Discher DE. Inhibition of’ self’ engulfment through deactivation of myosin-II at the phagocytic synapse between human cells. J Cell Biol 2008; 180:989–1003.PubMedGoogle Scholar
  73. 73.
    Olinski RP, Lundin LG, Hallbook F. Conserved synteny between the Ciona genome and human paralogons identifies large duplication events in the molecular evolution of the insulin-relaxin gene family. Mol Biol Evol 2006; 23:10–22.PubMedGoogle Scholar
  74. 74.
    Canobbio I, Balduini C, Torti M. Signalling through the platelet glycoprotein Ib-V-IX complex. Cell Signal 2004; 16:1329–1344.PubMedGoogle Scholar
  75. 75.
    Kuraku S, Meyer A, Kuratani S. Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Mol Biol Evol 2009; 26:47–59.PubMedGoogle Scholar
  76. 76.
    Pancer Z, Mayer WE, Klein J et al. Prototypic T-cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc Natl Acad Sci USA 2004; 101:13273–13278.PubMedGoogle Scholar
  77. 77.
    Cannon JP, Haire RN, Pancer Z et al. Variable domains and a VpreB-like molecule are present in a jawless vertebrate. Immunogenetics 2005; 56:924–929.PubMedGoogle Scholar
  78. 78.
    Chen G, Zhuchenko O, Kuspa A. Immune-like phagocyte activity in the social amoeba. Science 2007; 317:678–681.PubMedGoogle Scholar
  79. 79.
    Hagerstrand H, Danieluk M, Bobrowska-Hagerstrand M et al. The lamprey (Lampetra fluviatilis) erythrocyte; morphology, ultrastructure, major plasma membrane proteins and phospholipids and cytoskeletal organization. Mol Membr Biol 1999; 16:195–204.PubMedGoogle Scholar
  80. 80.
    Le Foll F, Rioult D, Boussa S et al. Characterisation of Mytilus edulis hemocyte subpopulations by single cell time-lapse motility imaging. Fish Shellfish Immunol 2010; 28:372–386.PubMedGoogle Scholar
  81. 81.
    de Barros CM, de Carvalho DR, Andrade LRP et al. Nitric oxide production by hemocytes of the ascidian Styela plicata. Cell Tissue Res 2009; 338:117–128.PubMedGoogle Scholar
  82. 82.
    Cooper MA, Colonna M, Yokoyama WM. Hidden talents of natural killers: NK cells in innate and adaptive immunity. EMBO Rep 2009; 10:1103–1110.PubMedGoogle Scholar
  83. 83.
    Dokun AO, Kim S, Smith HR et al. Specific and nonspecific NK cell activation during virus infection. Nat Immunol 2001; 2:951–956.PubMedGoogle Scholar
  84. 84.
    Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009; 457:557–561.PubMedGoogle Scholar
  85. 85.
    Cooper MA, Elliott JM, Keyel PA, Y et al. Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 2009; 106:1915–1919.PubMedGoogle Scholar
  86. 86.
    Nicotra ML, Powell AE, Rosengarten RD et al. A hypervariable invertebrate allodeterminant. Curr Biol 2009; 19:583–589.PubMedGoogle Scholar
  87. 87.
    Khalturin K, Becker M, Rinkevich B et al. Urochordates and the origin of natural killer cells: identification of a CD94/NKR-P1-related receptor in blood cells of Botryllus. Proc Natl Acad Sci USA 2003; 100:622–627.PubMedGoogle Scholar
  88. 88.
    Arizza V, Giaramita FT, Parrinello D et al. Cell cooperation in coelomocyte cytotoxic activity of Paracentrotus lividus coelomocytes. Comp Biochem Physiol A Mol Integr Physiol 2007; 147:389–394.PubMedGoogle Scholar
  89. 89.
    Brockton V, Henson JH, Raftos DA et al. Localization and diversity of 185/333 proteins from the purple sea urchin-unexpected protein-size range and protein expression in a new coelomocyte type. J Cell Sci 2008; 121:339–348.PubMedGoogle Scholar
  90. 90.
    Pancer Z. Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc Natl Acad Sci USA 2000; 97:13156–13161.PubMedGoogle Scholar
  91. 91.
    Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997; 91:661–672.PubMedGoogle Scholar
  92. 92.
    Inlay MA, Bhattacharya D, Sahoo D et al. Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development. Genes Dev 2009; 23:2376–2381.PubMedGoogle Scholar
  93. 93.
    Wada H, Masuda K, Satoh R et al. Adult T-cell progenitors retain myeloid potential. Nature 2008; 452:768–772.PubMedGoogle Scholar
  94. 94.
    Bell JJ, Bhandoola A. The earliest thymic progenitors for T-cells possess myeloid lineage potential. Nature2008; 452:764–767.PubMedGoogle Scholar
  95. 95.
    L i J, Barreda DR, Zhang YA et al. B-lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 2006; 7:1116–1124.PubMedGoogle Scholar
  96. 96.
    Wu Y, Wu W, Wong WM et al. Human gamma delta T-cells: a lymphoid lineage cell capable of professional phagocytosis. J Immunol 2009; 183:5622–5629.PubMedGoogle Scholar
  97. 97.
    Laslo P, Pongubala JM, Lancki DW et al. Gene regulatory networks directing myeloid and lymphoid cell fates within the immune system. Semin Immunol 2008; 20:228–235.PubMedGoogle Scholar
  98. 98.
    Kawamoto H, Katsura Y. A new paradigm for hematopoietic cell lineages: revision of the classical concept of the myeloid-lymphoid dichotomy. Trends Immunol 2009; 30:193–200.PubMedGoogle Scholar
  99. 99.
    Spooner CJ, Cheng JX, Pujadas E et al. A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 2009; 31:576–586.PubMedGoogle Scholar
  100. 100.
    Benne C, Lelievre JD, Balbo MH et al. Notch increases T/NK potential of human hematopoietic progenitors and inhibits B-cell differentiation at a pro-B stage. Stem Cells 2009; 27:1676–1685.PubMedGoogle Scholar
  101. 101.
    Bajoghli B, Aghaallaei N, Hess I et al. Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell 2009; 138:186–197.PubMedGoogle Scholar
  102. 102.
    Glick B, Chang TS, Jaap RG. The bursa of Fabricius and antibody production. Poult. Sci 1956; 35:224.Google Scholar
  103. 103.
    Pospisil R, Mage RG. Rabbit appendix: a site of development and selection of the B-cell repertoire. Curr Top Microbiol Immunol 1998; 229:59–70.PubMedGoogle Scholar
  104. 104.
    Palm NW, Medzhitov R. Pattern recognition receptors and control of adaptive immunity. Immunol Rev 2009; 227:221–233.PubMedGoogle Scholar
  105. 105.
    Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T-cell lineage differentiation. Immunity 2009; 30:646–655.PubMedGoogle Scholar
  106. 106.
    Batista FD, Harwood NE. The who, how and where of antigen presentation to B-cells. Nat Rev Immunol 2009; 9:15–27.PubMedGoogle Scholar
  107. 107.
    Denzel A, Maus UA, Rodriguez Gomez M et al. Basophils enhance immunological memory responses. Nat Immunol 2008; 9(7):733–742.PubMedGoogle Scholar
  108. 108.
    Leadbetter EA, Rifkin IR, Hohlbaum AM et al. Chromatin-IgG complexes activate B-cells by dual engagement of IgM and Toll-like receptors. Nature 2002; 416:603–607.PubMedGoogle Scholar
  109. 109.
    Rast JP, Smith LC, Loza-Coll M et al. Genomic insights into the immune system of the sea urchin. Science 2006; 314:952–956.PubMedGoogle Scholar
  110. 110.
    Jima DD, Shah RN, Orcutt TM et al. Enhanced transcription of complement and coagulation genes in the absence of adaptive immunity. Mol Immunol 2009; 46:1505–1516.PubMedGoogle Scholar
  111. 111.
    Wienholds E, Schulte-Merker S, Walderich B et al. Target-selected inactivation of the zebrafish rag1 gene. Science 2002; 297:99–102.PubMedGoogle Scholar
  112. 112.
    K araca NE, Aksu G, Genel F et al. Diverse phenotypic and genotypic presentation of RAG1 mutations in two cases with SCID. Clin Exp Med 2009; 9:339–342.PubMedGoogle Scholar
  113. 113.
    Jackson JA, Friberg IM, Little S et al. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 2009; 126:18–27.PubMedGoogle Scholar
  114. 114.
    Steinfelder S, Andersen JF, Cannons JL et al. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med 2009; 206:1681–1690.PubMedGoogle Scholar
  115. 115.
    Matsunaga T, Rahman A. What brought the adaptive immune system to vertebrates?-The jaw hypothesis and the seahorse. Immunol Rev 1998; 166:177–186.PubMedGoogle Scholar
  116. 116.
    McFall-Ngai M. Adaptive immunity: care for the community. Nature 2007; 445:153.PubMedGoogle Scholar
  117. 117.
    Sansonetti PJ, Medzhitov R. Learning tolerance while fighting ignorance. Cell 2009; 138:416–420.PubMedGoogle Scholar
  118. 118.
    Pancer Z, Cooper MD. The Evolution of Adaptive Immunity. Annu. Rev. Immunol 2006; 24:497–518.PubMedGoogle Scholar
  119. 119.
    Hedrick SM. The acquired immune system: a vantage from beneath. Immunity 2004; 21:607–615.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2012

Authors and Affiliations

  • Nadia Danilova
    • 1
  1. 1.Department of Molecular, Cell and Developmental BiologyUniversity of California; Los AngelesLos AngelesUSA

Personalised recommendations