Design principles of adaptive immune systems (original) (raw)
Heimberg, A. M., Cowper-Sal-lari, R., Sémon, M., Donoghue, P. C. J. & Peterson, K. J. microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc. Natl Acad. Sci. USA107, 19379–19383 (2010). ArticleCASPubMedPubMed Central Google Scholar
Janvier, P. Early jawless vertebrates and cyclostome origins. Zool. Sci.25, 1045–1056 (2008). Article Google Scholar
Schaffer, J. Ueber die Thymusanlage bei Petromyzon Planeri. Zweite vorläufige Mittheilung über den feineren Bau des Thymus. Sitzungsberichte der K. Akad. der Wissenschaften Math. Nat. Klasse Abth. III103, 149–156 (1894). Google Scholar
Finstad, J. & Good, R. A. The evolution of the immune response. III. Immunologic responses in the lamprey. J. Exp. Med.120, 1151–1168 (1964). ArticleCASPubMedPubMed Central Google Scholar
Mayer, W. E. et al. Isolation and characterization of lymphocyte-like cells from a lamprey. Proc. Natl Acad. Sci. USA99, 14350–14355 (2002). ArticleCASPubMedPubMed Central Google Scholar
Guo, P. et al. Dual nature of the adaptive immune system in lampreys. Nature459, 796–801 (2009). This study identified two distinct lymphocyte lineages in lamprey larvae, indicating that the functional dichotomy of B and T cells is common to all vertebrates. ArticleCASPubMedPubMed Central Google Scholar
Pancer, Z. et al. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature430, 174–180 (2004). This paper describes a novel somatic diversification system for antigen receptors in lampreys. CASPubMed Google Scholar
Cooper, M. D. & Alder, M. N. The evolution of adaptive immune systems. Cell124, 815–822 (2006). ArticleCASPubMed Google Scholar
Cooper, M. D. & Herrin, B. R. How did our complex immune system evolve? Nature Rev. Immunol.10, 2–3 (2010). ArticleCAS Google Scholar
Du Pasquier, L. Meeting the demand for innate and adaptive immunities during evolution. Scand. J. Immunol.62 (Suppl. 1), 39–48 (2005). ArticleCASPubMed Google Scholar
Flajnik, M. F. & Kasahara, M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nature Rev. Genet.11, 47–59 (2010). ArticleCASPubMed Google Scholar
Herrin, B. R. & Cooper, M. D. Alternative adaptive immunity in jawless vertebrates. J. Immunol.185, 1367–1374 (2010). ArticleCASPubMed Google Scholar
Litman, G. W., Rast, J. P. & Fugmann, S. D. The origins of vertebrate adaptive immunity. Nature Rev. Immunol.10, 543–553 (2010). ArticleCAS Google Scholar
Pancer, Z. & Cooper, M. D. The evolution of adaptive immunity. Annu. Rev. Immunol.24, 497–518 (2006). ArticleCASPubMed Google Scholar
Cannon, J. P. et al. Recognition of additional roles for immunoglobulin domains in immune function. Semin. Immunol.22, 17–24 (2010). ArticleCASPubMed Google Scholar
Flajnik, M. F. & Du Pasquier, L. Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol.25, 640–644 (2004). ArticleCASPubMed Google Scholar
Litman, G. W., Dishaw, L. J., Cannon, J. P., Haire, R. N. & Rast, J. P. Alternative mechanisms of immune receptor diversity. Curr. Opin. Immunol.19, 526–534 (2007). ArticleCASPubMedPubMed Central Google Scholar
Rast, J. P., Smith, L. C., Loza-Coll, M., Hibino, T. & Litman, G. W. Genomic insights into the immune system of the sea urchin. Science314, 952–956 (2006). ArticleCASPubMedPubMed Central Google Scholar
Bajoghli, B. et al. A thymus candidate in lampreys. Nature470, 90–94 (2011). This paper shows that the sites of development of the two lymphocyte lineages in lampreys are anatomically distinct and suggests that a thymus equivalent is situated in the gill basket. ArticleCASPubMed Google Scholar
Alder, M. N. et al. Diversity and function of adaptive immune receptors in a jawless vertebrate. Science310, 1970–1973 (2005). ArticleCASPubMed Google Scholar
Nagawa, F. et al. Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nature Immunol.8, 206–213 (2007). ArticleCAS Google Scholar
Rogozin, I. B. et al. Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nature Immunol.8, 647–656 (2007). ArticleCAS Google Scholar
Kasamatsu, J. et al. Identification of a third variable lymphocyte receptor in the lamprey. Proc. Natl Acad. Sci. USA107, 14304–14308 (2010). ArticleCASPubMedPubMed Central Google Scholar
Cooper, M. D., Peterson, R. D. & Good, R. A. Delineation of the thymic and bursal lymphoid systems in the chicken. Nature205, 143–146 (1965). This paper introduced the concept of the dual nature of the vertebrate immune system, that is, the presence of functionally distinct B and T cell lineages. ArticleCASPubMed Google Scholar
Dias, S., Xu, W., McGregor, S. & Kee, B. Transcriptional regulation of lymphocyte development. Curr. Opin. Genet. Dev.18, 441–448 (2008). ArticleCASPubMedPubMed Central Google Scholar
Ramírez, J., Lukin, K. & Hagman, J. From hematopoietic progenitors to B cells: mechanisms of lineage restriction and commitment. Curr. Opin. Immunol.22, 177–184 (2010). ArticlePubMedPubMed CentralCAS Google Scholar
Martin, F. & Kearney, J. F. B1 cells: similarities and differences with other B cell subsets. Curr. Opin. Immunol.13, 195–201 (2001). ArticleCASPubMed Google Scholar
Yamagata, T., Benoist, C. & Mathis, D. A shared gene-expression signature in innate-like lymphocytes. Immunol. Rev.210, 52–66 (2006). ArticleCASPubMed Google Scholar
Yoshimoto, M. et al. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc. Natl Acad. Sci. USA108, 1468–1473 (2011). ArticleCASPubMedPubMed Central Google Scholar
Schorpp, M. et al. Conserved functions of Ikaros in vertebrate lymphocyte development: genetic evidence for distinct larval and adult phases of T cell development and two lineages of B cells in zebrafish. J. Immunol.177, 2463–2476 (2006). ArticleCASPubMed Google Scholar
Zhang, Y. A. et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nature Immunol.11, 827–835 (2010). ArticleCAS Google Scholar
Dooley, H. & Flajnik, M. F. Shark immunity bites back: affinity maturation and memory response in the nurse shark, Ginglymostoma cirratum. Eur. J. Immunol.35, 936–945 (2005). ArticleCASPubMed Google Scholar
Ciofani, M. & Zúñiga-Pflücker, J. C. Determining γδ versus αβ T cell development. Nature Rev. Immunol.10, 657–663 (2010). ArticleCAS Google Scholar
Kreslavsky, T., Gleimer, M. & von Boehmer, H. αβ versus γδ lineage choice at the first TCR-controlled checkpoint. Curr. Opin. Immunol.22, 185–192 (2010). ArticleCASPubMedPubMed Central Google Scholar
Höglund, P. & Brodin, P. Current perspectives of natural killer cell education by MHC class I molecules. Nature Rev. Immunol.10, 724–734 (2010). ArticleCAS Google Scholar
Raulet, D. H., Vance, R. E. & McMahon, C. W. Regulation of the natural killer cell receptor repertoire. Annu. Rev. Immunol.19, 291–330 (2001). ArticleCASPubMed Google Scholar
Sun, J. C., Beilke, J. N. & Lanier, L. L. Immune memory redefined: characterizing the longevity of natural killer cells. Immunol. Rev.236, 83–94 (2010). ArticleCASPubMedPubMed Central Google Scholar
Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nature Rev. Genet.10, 725–732 (2009). ArticleCASPubMed Google Scholar
Okada, K. & Asai, K. Expansion of signaling genes for adaptive immune system evolution in early vertebrates. BMC Genomics9, 218 (2008). ArticlePubMedPubMed CentralCAS Google Scholar
Boehm, T. & Bleul, C. C. The evolutionary history of lymphoid organs. Nature Immunol.8, 131–135 (2007). ArticleCAS Google Scholar
Kawamoto, H. & Katsura, Y. A new paradigm for hematopoietic cell lineages: revision of the classical concept of the myeloid–lymphoid dichotomy. Trends Immunol.30, 193–200 (2009). ArticleCASPubMed Google Scholar
Han, Y. et al. The primitive immune system of amphioxus provides insights into the ancestral structure of the vertebrate immune system. Dev. Comp. Immunol.34, 791–796 (2010). ArticleCASPubMed Google Scholar
Ballarin, L. & Cima, F. Cytochemical properties of Botryllus schlosseri haemocytes: indications for morpho-functional characterisation. Eur. J. Histochem.49, 255–264 (2005). CASPubMed Google Scholar
Leclerc, M., Brillouet, C. & Luquet, G. The starfish axial organ: an ancestral lymphoid organ. Dev. Comp. Immunol.4, 605–615 (1980). ArticleCASPubMed Google Scholar
Davis, M. M. & Bjorkman, P. J. T-cell antigen receptor genes and T-cell recognition. Nature334, 395–402 (1988). Based on the structure of peptide–MHC–TCR complexes, this paper proposes a model of how TCRs and BCRs have evolved. ArticleCASPubMed Google Scholar
Sakano, H., Hüppi, K., Heinrich, G. & Tonegawa, S. Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature280, 288–294 (1979). ArticleCASPubMed Google Scholar
Alder, M. N. et al. Antibody responses of variable lymphocyte receptors in the lamprey. Nature Immunol.9, 319–327 (2008). ArticleCAS Google Scholar
Reynaud, C. A., Bertocci, B., Dahan, A. & Weill, J. C. Formation of the chicken B-cell repertoire: ontogenesis, regulation of Ig gene rearrangement, and diversification by gene conversion. Adv. Immunol.57, 353–378 (1994). ArticleCASPubMed Google Scholar
Chaudhuri, J. et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv. Immunol.94, 157–214 (2007). ArticleCASPubMed Google Scholar
Di Noia, J. M. & Neuberger, M. S. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem.76, 1–22 (2007). ArticleCASPubMed Google Scholar
Zhang, S.-M., Adema, C. M., Kepler, T. B. & Loker, E. S. Diversification of Ig superfamily genes in an invertebrate. Science305, 251–254 (2004). This paper provides evidence for somatic diversification of immune-related receptors in an invertebrate. ArticleCASPubMed Google Scholar
Hamilton, C. E., Papavasiliou, F. N. & Rosenberg, B. R. Diverse functions for DNA and RNA editing in the immune system. RNA Biol.7, 220–228 (2010). ArticleCASPubMed Google Scholar
Ghosh, J. et al. Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev. Comp. Immunol.34, 235–245 (2010). ArticleCASPubMed Google Scholar
van Meerwijk, J. P. M. et al. Quantitative impact of thymic clonal deletion on the T cell repertoire. J. Exp. Med.185, 377–383 (1997). ArticleCASPubMedPubMed Central Google Scholar
Wardemann, H. et al. Predominant autoantibody production by early human B cell precursors. Science301, 1374–1377 (2003). ArticleCASPubMed Google Scholar
Chen, H. et al. Characterization of arrangement and expression of the T cell receptor γ locus in the sandbar shark. Proc. Natl Acad. Sci. USA106, 8591–8596 (2009). ArticleCASPubMedPubMed Central Google Scholar
Rast, J. P. et al. α, β, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity6, 1–11 (1997). ArticleCASPubMed Google Scholar
Cho, J.-H., Kim, H.-O., Surh, C. D. & Sprent, J. T cell receptor-dependent regulation of lipid rafts controls naive CD8+ T cell homeostasis. Immunity32, 214–226 (2010). ArticleCASPubMedPubMed Central Google Scholar
Anderson, G., Lane, P. J. L. & Jenkinson, E. J. Generating intrathymic microenvironments to establish T-cell tolerance. Nature Rev. Immunol.7, 954–963 (2007). ArticleCAS Google Scholar
Bleul, C. C. et al. Formation of a functional thymus initiated by a postnatal epithelial progenitor cell. Nature441, 992–996 (2006). ArticleCASPubMed Google Scholar
Rossi, S. W., Jenkinson, W. E., Anderson, G. & Jenkinson, E. J. Clonal analysis reveals a common progenitor for thymic cortical and medullary epithelium. Nature441, 988–991 (2006). ArticleCASPubMed Google Scholar
Jenkins, M. K., Chu, H. H., McLachlan, J. B. & Moon, J. J. On the composition of the preimmune repertoire of T cells specific for peptide–major histocompatibility complex ligands. Annu. Rev. Immunol.28, 275–294 (2010). ArticleCASPubMed Google Scholar
Richards, M. H. & Nelson, J. L. The evolution of vertebrate antigen receptors: a phylogenetic approach. Mol. Biol. Evol.17, 146–155 (2000). ArticleCASPubMed Google Scholar
Deng, L. et al. A structural basis for antigen recognition by the T cell-like lymphocytes of sea lamprey. Proc. Natl Acad. Sci. USA107, 13408–13413 (2010). This study usedin vitroselection to identify VLRA proteins that directly bind to unprocessed protein antigens with high affinity. ArticleCASPubMedPubMed Central Google Scholar
Dervovi, D. & Zúñiga-Pflücker, J. C. Positive selection of T cells, an in vitro view. Semin. Immunol.22, 276–286 (2010). ArticleCAS Google Scholar
Huseby, E. S. et al. How the T cell repertoire becomes peptide and MHC specific. Cell122, 247–260 (2005). ArticleCASPubMed Google Scholar
Scott-Browne, J. P., White, J., Kappler, J. W., Gapin, L. & Marrack, P. Germline-encoded amino acids in the αβ T-cell receptor control thymic selection. Nature458, 1043–1046 (2009). ArticleCASPubMedPubMed Central Google Scholar
Wang, B. et al. A single peptide–MHC complex positively selects a diverse and specific CD8 T cell repertoire. Science326, 871–874 (2009). ArticleCASPubMedPubMed Central Google Scholar
Palmer, E. Negative selection — clearing out the bad apples from the T-cell repertoire. Nature Rev. Immunol.3, 383–391 (2003). ArticleCAS Google Scholar
Derbinski, J. & Kyewski, B. How thymic antigen presenting cells sample the body's self-antigens. Curr. Opin. Immunol.22, 592–600 (2010). ArticleCASPubMed Google Scholar
Bajoghli, B. et al. Evolution of genetic networks underlying the emergence of thymopoiesis in vertebrates. Cell138, 186–197 (2009). ArticleCASPubMed Google Scholar
Corbeaux, T. et al. Thymopoiesis in mice depends on a _Foxn1_-positive thymic epithelial cell lineage. Proc. Natl Acad. Sci. USA107, 16613–16618 (2010). ArticleCASPubMedPubMed Central Google Scholar
Nehls, M. et al. Two genetically separable steps in the differentiation of thymic epithelium. Science272, 886–889 (1996). This paper shows that the FOXN1 transcription factor is required for the differentiation of thymic epithelial cells. ArticleCASPubMed Google Scholar
Bleul, C. C. & Boehm, T. Chemokines define distinct microenvironments in the developing thymus. Eur. J. Immunol.30, 3371–3379 (2000). ArticleCASPubMed Google Scholar
Klein, J. & Nikolaidis, N. The descent of the antibody-based immune system by gradual evolution. Proc. Natl Acad. Sci. USA102, 169–174 (2005). ArticleCASPubMed Google Scholar
McKitrick, T. R. & De Tomaso, A. W. Molecular mechanisms of allorecognition in a basal chordate. Semin. Immunol.22, 34–38 (2010). ArticleCASPubMed Google Scholar
Rosengarten, R. D. & Nicotra, M. L. Model systems of invertebrate allorecognition. Curr. Biol.21, R82–R92 (2011). ArticleCASPubMed Google Scholar
Perlot, T. & Alt, F. W. _Cis_-regulatory elements and epigenetic changes control genomic rearrangements of the IgH locus. Adv. Immunol.99, 1–32 (2008). ArticleCASPubMedPubMed Central Google Scholar
Spicuglia, S., Pekowska, A., Zacarias-Cabeza, J. & Ferrier, P. Epigenetic control of Tcrb gene rearrangement. Semin. Immunol.22, 330–336 (2010). ArticleCASPubMed Google Scholar
Kaufman, J., Skjoedt, K. & Salomonsen, J. The MHC molecules of nonmammalian vertebrates. Immunol. Rev.113, 83–117 (1990). ArticleCASPubMed Google Scholar
Boehm, T. Co-evolution of a primordial peptide-presentation system and cellular immunity. Nature Rev. Immunol.6, 79–84 (2006). ArticleCAS Google Scholar
Leinders-Zufall, T. et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science306, 1033–1037 (2004). ArticleCASPubMed Google Scholar
Leinders-Zufall, T., Ishii, T., Mombaerts, P., Zufall, F. & Boehm, T. Structural requirements for the activation of mouse vomeronasal sensory neurons by MHC peptides. Nature Neurosci.12, 1551–1558 (2009). ArticleCASPubMed Google Scholar
Milinski, M. et al. Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc. Natl Acad. Sci. USA102, 4414–4418 (2005). ArticleCASPubMedPubMed Central Google Scholar
Jin, M. S. & Lee, J.-O. Structures of TLR–ligand complexes. Curr. Opin. Immunol.20, 414–419 (2008). ArticleCASPubMed Google Scholar
Kim, H. M. et al. Crystal structure of the TLR4–MD-2 complex with bound endotoxin antagonist Eritoran. Cell130, 906–917 (2007). ArticleCASPubMed Google Scholar
Han, B. W., Herrin, B. R., Cooper, M. D. & Wilson, I. A. Antigen recognition by variable lymphocyte receptors. Science321, 1834–1837 (2008). ArticleCASPubMedPubMed Central Google Scholar
Kim, H. M. et al. Structural diversity of the hagfish variable lymphocyte receptors. J. Biol. Chem.282, 6726–6732 (2007). CASPubMed Google Scholar
Vyas, J. M., Van der Veen, A. G. & Ploegh, H. L. The known unknowns of antigen processing and presentation. Nature Rev. Immunol.8, 607–618 (2008). ArticleCAS Google Scholar