Evolution of Adaptive Immunity

Nadia Danilova, University of California, Los Angeles, California, USA

Published online: April 2013

DOI: 10.1002/9780470015902.a0024598

Historically, two components of immunity were identified, innate and adaptive. Innate receptors recognise molecular patterns common for groups of pathogens or for common pathological changes in host cells. All animals are protected by innate immunity. In addition, in vertebrates, adaptive immunity evolved that is based on the limitless somatic diversification of lymphoid receptors and selective expansion of those receptors that match the antigen/pathogen. Moreover, somatic hypermutation of antibodies combined with antigen selection allows fine-tuning of an antibody sequence to match the antigen.

The repertoire of adaptive immune receptors in each individual differs in dependence on its life history and provides a basis for a strong memory response. Adaptive immune systems in jaw and jawless vertebrates are built on completely different receptors; immunoglobulin superfamily in jaw vertebrates and molecules with leucine-rich repeats in jawless vertebrates. However, they are strikingly similar functionally pointing to similar evolutionary forces shaping these systems.

Key Concepts:

  • Both adaptive and innate strategies are used in organisms from bacteria to humans.
  • Innate mechanisms provide basic protection based on evolutionary conserved features of pathogens whereas adaptive mechanisms provide immunity that is shaped by the life history of every individual.
  • Adaptive immunity of jaw and jawless vertebrates is based on different receptors but functionally similar pointing to the same evolutionary driving forces.
  • Combination of adaptive and innate mechanisms is necessary to provide the most comprehensive immune protection.
  • Genome duplications played a crucial role in the origin of the adaptive immune system.
  • Adaptive immune system coevolve with innate immune mechanisms.

Keywords: T cell; B cell; antibody; rags; AID; VLR; rearrangement; diversification; thymus

Figure 1. The organisation of a hypothetical mammalian immunoglobulin heavy chain locus is shown. At the first step, one of the D segments rearranges to one of J segments. Next, one of V segments rearranges to DJ. All intervening sequences are excised. The resulting recombined gene is expressed as VDJCC message and it is alternatively spliced producing or chain. After antigen exposure, any of the downstream constant regions can replace Cmu through class switch recombination.
Figure 2. VLR receptors are encoded as an empty cassette containing only flanking gene segments. Alongside it, hundreds of LRR modules are encoded in different orientations. They are brought into the cassette in stepwise fashion by gene conversion, which presumably is mediated by the enzymes of cytosine deaminase family. CP, connecting peptide; LRR, leucine rich repeat modules; SP, signal peptide.
Figure 3. Two whole genome duplication events are thought to play a vital role in the evolution of vertebrate adaptive immunity. The most accepted view is that the first duplication took place before splitting of vertebrate lineages whereas the second took place in jaw lineage. However it may be that both duplications happened before the split. Genes similar to components of TCR and BCR are present in lamprey whereas genes similar to VLR are found in zebrafish suggesting that elements of both systems were present in the vertebrate ancestors.
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 References
    Bajoghli B, Guo P, Aghaallaei N et al. (2011) A thymus candidate in lampreys. Nature 470(7332): 90–94.
    Barrangou R, Fremaux C, Deveau H et al. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819): 1709–1712.
    Cannon JP, Haire RN, Pancer Z et al. (2005) Variable domains and a VpreB-like molecule are present in a jawless vertebrate. Immunogenetics 56(12): 924–929.
    Capalbo D, Giardino G, Martino LD et al. (2012) Genetic basis of altered central tolerance and autoimmune diseases: a lesson from AIRE mutations. International Reviews of Immunology 31(5): 344–362.
    Cyster JG (2012) B cell follicles and antigen encounters of the third kind. Nature Immunology 11(11): 989–996.
    Danilova N and Amemiya CT (2009) Going adaptive: the saga of antibodies. Annals of the New York Academy of Sciences 1168: 130–155.
    Denzel A, Maus UA, Rodriguez Gomez M et al. (2008) Basophils enhance immunological memory responses. Nature Immunology 9(7): 733–742.
    Dresch C, Leverrier Y, Marvel J and Shortman K (2012) Development of antigen cross-presentation capacity in dendritic cells. Trends Immunology 33(8): 381–388.
    Elliott DE and Weinstock JV (2012) Where are we on worms? Current Opinion in Gastroenterology 28(6): 551–556.
    Flajnik MF and Kasahara M (2009) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nature Reviews Genetics 11(1): 47–59.
    Fugmann SD (2010) The origins of the Rag genes – From transposition to V(D)J recombination. Seminars in Immunology 22(1): 10–16.
    Ghosh J, Lun CM, Majeske AJ et al. (2011) Invertebrate immune diversity. Developmental and Comparative Immunology 35(9): 959–974.
    Guo P, Hirano M, Herrin BR et al. (2009) Dual nature of the adaptive immune system in lampreys. Nature 459(7248): 796–801.
    Han BW, Herrin BR, Cooper MD and Wilson IA (2008) Antigen recognition by variable lymphocyte receptors. Science 321(5897): 1834–1837.
    Hedrick SM (2004) The acquired immune system: a vantage from beneath. Immunity 21(5): 607–615.
    Hohn C and Petrie-Hanson L (2012) Rag1-/- mutant zebrafish demonstrate specific protection following bacterial re-exposure. PLoS One 7(9): e44451.
    Holland LZ, Albalat R, Azumi K et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Research 18: 1100–1111.
    Hsu E (1996) Canonical VH CDR1 nucleotide sequences are conserved in all jawed vertebrates. International Immunology 8(6): 847–854.
    book Janeway CA (2005) Immunobiology: the Immune System in Health and Disease. New York: Garland Science.
    Kapitonov VV and Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biology 3(6): e181.
    Karaca NE, Aksu G, Genel F et al. (2009) Diverse phenotypic and genotypic presentation of RAG1 mutations in two cases with SCID. Clinical and Experimental Medicine 9(4): 339–342.
    Kasahara M (2007) The 2R hypothesis: an update. Current Opinions in Immunology 19(5): 547–552.
    Kato L, Stanlie A, Begum NA et al. (2012) An evolutionary view of the mechanism for immune and genome diversity. Journal of Immunology 188(8): 3559–3566.
    Kauffman SA and Weinberger ED (1989) The NK model of rugged fitness landscapes and its application to maturation of the immune response. Journal of Theoretical Biology 141(2): 211–245.
    Kuraku S (2010) Palaeophylogenomics of the vertebrate ancestor – impact of hidden paralogy on hagfish and lamprey gene phylogeny. Integrative and Comparative Biology 50(1): 124–129.
    Leadbetter EA, Rifkin IR, Hohlbaum AM et al. (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416(6881): 603–607.
    Lee YK and Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330(6012): 1768–1773.
    Malecek K, Lee V, Feng W et al. (2008) Immunoglobulin heavy chain exclusion in the shark. PLoS Biology 6(6): e157.
    Matsunaga T and Rahman A (1998) What brought the adaptive immune system to vertebrates? – The jaw hypothesis and the seahorse. Immunological Reviews 166: 177–186.
    Medzhitov R and Janeway CA Jr (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296(5566): 298–300.
    Munoz-Fontela C, Pazos M, Delgado I et al. (2011) p53 serves as a host antiviral factor that enhances innate and adaptive immune responses to influenza A virus. Journal of Immunology 187(12): 6428–6436.
    Netea MG, Quintin J and van der Meer JW (2011) Trained immunity: a memory for innate host defense. Cell Host and Microbe 9(5): 355–361.
    Pancer Z, Amemiya CT, Ehrhardt GR et al. (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430(6996): 174–180.
    Pancer Z and Cooper MD (2006) The evolution of adaptive immunity. Annual Reviews of Immunology 24: 497–518.
    Petrie-Hanson L, Hohn C and Hanson L (2009) Characterization of rag1 mutant zebrafish leukocytes. BMC Immunology 10(8): 8.
    Rast JP and Messier-Solek C (2008) Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biological Bulletin 214(3): 274–283.
    Rast JP, Smith LC, Loza-Coll M, Hibino T and Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314(5801): 952–956.
    Reynaud CA, Anquez V, Grimal H and Weill JC (1987) A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48(3): 379–388.
    Rogozin IB, Iyer LM, Liang L et al. (2007) Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nature Immunology 8(6): 647–656.
    Saha NR, Smith J and Amemiya CT (2010) Evolution of adaptive immune recognition in jawless vertebrates. Seminars in Immunology 22(1): 25–33.
    Schatz DG and Ji Y (2011) Recombination centres and the orchestration of V(D)J recombination. Nature Reviews Immunology 11(4): 251–263.
    Shlomchik MJ and Weisel F (2012) Germinal center selection and the development of memory B and plasma cells. Immunological Reviews 247(1): 52–63.
    Storb U and Stavnezer J (2002) Immunoglobulin genes: generating diversity with AID and UNG. Current Biology 12(21): R725–R727.
    Sun JC, Beilke JN and Lanier LL (2009) Adaptive immune features of natural killer cells. Nature 457: 557–561.
    Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302(5909): 575–581.
    Waterhouse PM, Wang MB and Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411(6839): 834–842.
    Wienholds E, Schulte-Merker S, Walderich B and Plasterk RH (2002) Target-selected inactivation of the zebrafish rag1 gene. Science 297(5578): 99–102.
    Xu Z, Zan H, Pone EJ, Mai T and Casali P (2012) Immunoglobulin class-switch DNA recombination: induction, targeting and beyond. Nature Reviews Immunology 12(7): 517–531.
 Further Reading
    Boehm T, McCurley N, Sutoh Y et al. (2012) VLR-based adaptive immunity. Annual Review of Immunology 30: 203–220.
    Hsu E (2011) The invention of lymphocytes. Current Opinion in Immunology 23(2): 156–162.
    book Larrea CL (ed.) (2011) Self and Non-self. Austin, TX: Landers Bioscience.
    Litman GW, Rast JP and Fugmann SD (2010) The origins of vertebrate adaptive immunity. Nature Reviews Immunology 10(8): 543–553.
    Ohta Y, Shiina T, Lohr, RL et al. (2011) Primordial linkage of beta2-microglobulin to the MHC. Journal of Immunology 186(6): 3563–3571.
    book Paul WE (2008) Fundamental Immunology. Philadelphia: Lippincott Williams & Wilkins.

Related Sub-Topics:

Acquired (Adaptive) Immunity | Antibodies | Adaptive Evolution | Evolution of Novelty | Molecular Evolution | Protein Evolution
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Article Title: Evolution of Adaptive Immunity
 
How to Cite close
Danilova, Nadia(Apr 2013) Evolution of Adaptive Immunity. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024598]