Generation of individual diversity: A too neglected fundamental property of adaptive immune system

Frontiers in Immunology

Volumn 5, Issue MAY, 2014, Pages

  Muraille, Eric ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Adaptive immune system; Convergent evolution; Group selection; Immune repertoire; Individual diversity; Major histocompatibility complex

Indexed keywords

PATTERN RECOGNITION RECEPTOR;

ADAPTIVE IMMUNITY; ARTICLE; CONVERGENT EVOLUTION; ECHINODERM; FITNESS; GENE; GENETIC VARIABILITY; HETEROZYGOSITY; HOST PATHOGEN INTERACTION; HUMAN; HYPOTHESIS; IMMUNE EVASION; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MAMMAL; MICROFLORA; NONHUMAN; PARSIMONY ANALYSIS; PHENOTYPIC VARIATION; SYMBIOSIS;

EID: 84937697108     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00208     Document Type: Article

References (78)

1. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos (2000) 88:87-98. doi:10.1034/j.1600-0706.2000. 880110.x.
2. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE. Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc Biol Sci (2004) 271:925-30. doi:10.1098/rspb.2004.2678.
3. Gregersen PK, Behrens TW. Genetics of autoimmune diseases-disorders of immune homeostasis. Nat Rev Genet (2006) 7:917-28. doi:10.1038/nrg1944.
4. Medzhitov R, Janeway CA. Innate immunity: the virtues of a nonclonal system of recognition. Cell (1997) 91:295-8. doi:10.1016/S0092-8674(00)80412-2.
5. Matsunaga T, Rahman A. What brought the adaptive immune system to vertebrates-the jaw hypothesis and the seahorse.pdf. Immunol Rev (1998) 166:177-86. doi:10.1111/j.1600-065X.1998.tb01262.x.
6. Flajnik M, Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures.pdf. Nat Rev Genet (2010) 11:47-59. doi:10.1038/nrg2703.
7. Pancer Z, Amemiya CT, Ehrhardt GRA, Ceitlin J, Gartland GL, Cooper MD. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature (2004) 430:174-80. doi:10.1038/nature02740.
8. Watson FL, Püttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, et al. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science (2005) 309:1874-8. doi:10.1126/science.1116887.
9. Zhang SM, Adema CM, Kepler TB, Loker ES. Diversification of Ig superfamily genes in an invertebrate. Science (2004) 305:251-4. doi:10.1126/science.1088069.
10. Cannon JP, Haire RN, Litman GW. Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nat Immunol (2002) 3:1200-7. doi:10.1038/ni849.
11. Smith LC. Innate immune complexity in the purple sea urchin: diversity of the sp185/333 system. Front Immunol (2012) 3:70. doi:10.3389/fimmu.2012.00070.
12. Hedrick SM. The acquired immune system: a vantage from beneath.pdf. Immunity (2004) 21:607-15. doi:10.1016/j.immuni.2004.08.020.
13. Van Valen L. A new evolutionary law. Evol Theory (1973) 1:1-30.
14. Monack DM, Mueller A, Falkow S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol (2004) 2:747-65. doi:10.1038/nrmicro955.
15. Kaye P, Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol (2011) 9:604-15. doi:10.1038/nrmicro2608.
16. Cooper MD, Alder MN. The evolution of adaptive immune systems. Cell (2006) 124:815-22. doi:10.1016/j.cell.2006.02.001.
17. Schneider DS, Ayres JS. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol (2008) 8:889-95. doi:10.1038/nri2432.
18. Muraille E. Redefining the immune system as a social interface for cooperative processes. PLoS Pathog (2013) 9:e1003203. doi:10.1371/journal.ppat. 1003203.
19. Stewart J. Immunoglobulins did not arise in evolution to fight infection. Immunol Today (1992) 13:396-9. doi:10.1016/0167-5699(92)90088-O.
20. Klimovich VB. Actual problems of evolutionary immunology. J Evol Biochem Physiol (2002) 38:562-74. doi:10.1023/A:1022060916099.
21. McFall-Ngai M. Adaptive immunity: care for the community. Nature (2007) 445:153. doi:10.1038/445153a.
22. Boehm T. Evolution of vertebrate immunity. Curr Biol (2012) 22:R722-32. doi:10.1016/j.cub.2012.07.003.
23. Bosch TCG. Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annu Rev Microbiol (2013) 67:499-518. doi:10.1146/annurevmicro-092412-155626.
24. Davis MM, Bjorkman PJ. T-cell antigen receptor genes and T-cell recognition. Nature (1988) 334:395-402. doi:10.1038/334395a0.
25. Oudin J, Michel M. Idiotypy of rabbit antibodies. I. Comparison of idiotypy of antibodies against Salmonella typhi with that of antibodies against other bacteria in the same rabbits, or of antibodies against Salmonella typhi in various rabbits. J Exp Med (1969) 1956:595-617. doi:10.1084/jem.130.3.595.
26. Fuschiotti P, Pasqual N, Hierle V, Borel E, London J, Marche PN, et al. Analysis of the TCR alpha-chain rearrangement profile in human T lymphocytes. Mol Immunol (2007) 44:3380-8. doi:10.1016/j.molimm.2007.02.017.
27. Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P. A direct estimate of the human alphabeta T cell receptor diversity. Science (1999) 286:958-61. doi:10.1126/science.286.5441.958.
28. Casrouge A, Beaudoing E, Dalle S, Pannetier C, Kanellopoulos J, Kourilsky P. Size estimate of the alphabeta TCR repertoire of naive mouse splenocytes. J Immunol (2000) 164:5782-7. doi:10.4049/jimmunol.164.11.5782.
29. Bousso P, Casrouge A, Altman JD, Haury M, Kanellopoulos J, Abastado JP, et al. Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. Immunity (1998) 9:169-78. doi:10.1016/S1074-7613(00)80599-3.
30. Maryanski JL, Attuil V, Hamrouni A, Mutin M, Rossi M, Aublin A, et al. Individuality of Ag-selected and preimmune TCR repertoires. Immunol Res (2001) 23:75-84. doi:10.1385/IR:23:1:75.
31. Avrameas S, Ternynck T, Tsonis IA, Lymberi P. Naturally occurring B-cell autoreactivity: a critical overview. J Autoimmun (2007) 29:213-8. doi:10.1016/j.jaut. 2007.07.010.
32. Panda S, Zhang J, Tan NS, Ho B, Ding JL. Natural IgG antibodies provide innate protection against ficolin-opsonized bacteria. EMBO J (2013) 32:2905-19. doi:10.1038/emboj.2013.199.
33. Lindner C, Wahl B, Föhse L, Suerbaum S, Macpherson AJ, Prinz I, et al. Age, microbiota, and T cells shape diverse individual IgA repertoires in the intestine. J Exp Med (2012) 209:365-77. doi:10.1084/jem.20111980.
34. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol (2013) 13:790-801. doi:10.1038/nri3535.
35. Nagele EP, Han M, Acharya NK, DeMarshall C, Kosciuk MC, Nagele RG. Natural IgG autoantibodies are abundant and ubiquitous in human sera, and their number is influenced by age, gender, and disease. PLoS One (2013) 8:e60726. doi:10.1371/journal.pone.0060726.
36. Wooldridge L, Ekeruche-Makinde J, van den Berg HA, Skowera A, Miles JJ, Tan MP, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem (2012) 287:1168-77. doi:10.1074/jbc. M111.289488.
37. Lin MY, Welsh RM. Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice. J Exp Med (1998) 188:1993-2005. doi:10.1084/jem.188.11.1993.
38. Gopinath S, Hotson A, Johns J, Nolan G, Monack D. The systemic immune state of super-shedder mice is characterized by a unique neutrophil-dependent blunting of TH1 responses. PLoS Pathog (2013) 9:e1003408. doi:10.1371/journal. ppat.1003408.
39. Julia V, Rassoulzadegan M, Glaichenhaus N. Resistance to Leishmania major induced by tolerance to a single antigen. Science (1996) 274:421-3. doi:10.1126/science.274.5286.421.
40. Suzuki K, Meek B, DoiY, Muramatsu M, Chiba T, Honjo T, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci USA (2004) 101:1981-6. doi:10.1073/pnas.0307317101.
41. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature (2011) 474:327-36. doi:10.1038/nature10213.
42. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell (2012) 148:1258-70. doi:10.1016/j. cell.2012.01.035.
43. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA (2010) 107:20051-6. doi:10.1073/pnas.1009906107.
44. Bravo J, Forsythe P. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA (2011) 108:16050-5. doi:10.1073/pnas.1102999108.
45. Fine P, Eames K, Heymann DL. "Herd immunity": a rough guide. Clin Infect Dis (2011) 52:911-6. doi:10.1093/cid/cir007.
46. Stein RA. Super-spreaders in infectious diseases. Int J Infect Dis (2011) 15:e510-3. doi:10.1016/j.ijid.2010.06.020.
47. Joo J, Gunny M, Cases M, Hudson P, Albert R, Harvill E. Bacteriophagemediated competition in Bordetella bacteria. Proc Biol Sci (2006) 273:1843-8. doi:10.1098/rspb.2006.3512.
48. Tompkins DM, Sainsbury AW, Nettleton P, Buxton D, Gurnell J. Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proc Biol Sci (2002) 269:529-33. doi:10.1098/rspb.2001.1897.
49. Sessa R, Palagiano C, Scifoni MG, Di Pietro M, Del Piano M. The major epidemic infections: a gift from the old world to the new? Panminerva Med (1999) 41:78-84.
50. Collins FM, Mackaness GB, Blanden RV. Infection-immunity in experimental Salmonellosis. J Exp Med (1966) 124:601-19. doi:10.1084/jem.124.4.601.
51. Strassmann JE, Queller DC. Evolution of cooperation and control of cheating in a social microbe. Proc Natl Acad Sci USA (2011) 108(Suppl):10855-62. doi:10.1073/pnas.1102451108.
52. Schluter SF, Bernstein RM, Bernstein H, Marchalonis JJ. "Big Bang" emergence of the combinatorial immune system. Dev Comp Immunol (1999) 23:107-11.
53. Du Pasquier L. Speculations on the origin of the vertebrate immune system. Immunol Lett (2004) 92:3-9. doi:10.1016/j.imlet.2003.10.012.
54. Dermody TS, Kirchner E, Guglielmi KM, Stehle T. Immunoglobulin superfamily virus receptors and the evolution of adaptive immunity. PLoS Pathog (2009) 5:e1000481. doi:10.1371/journal.ppat.1000481.
55. Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP. An ancient evolutionary origin of the Rag1/2 gene locus. Proc Natl Acad Sci USA (2006) 103:3728-33. doi:10.1073/pnas.0509720103.
56. Jeffery KJ, Bangham CR. Do infectious diseases drive MHC diversity? Microb Infect (2000) 2:1335-41. doi:10.1016/S1286-4579(00)01287-9.
57. Wegner KM, Kalbe M, Schaschl H, Reusch TBH. Parasites and individual major histocompatibility complex diversity-an optimal choice? Microb Infect (2004) 6:1110-6. doi:10.1016/j.micinf.2004.05.025.
58. Radwan J, Biedrzycka A, Babik W. Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv (2010) 143:537-44. doi:10.1016/j. biocon.2009.07.026.
59. Vercelli D. Discovering susceptibility genes for asthma and allergy. Nat Rev Immunol (2008) 8:169-82. doi:10.1038/nri2257.
60. Fernando MMA, Stevens CR, Walsh EC, De Jager PL, Goyette P, Plenge RM, et al. Defining the role of the MHC in autoimmunity: a review and pooled analysis. PLoS Genet (2008) 4:e1000024. doi:10.1371/journal.pgen.1000024.
61. Richards MH, Nelson JL. The evolution of vertebrate antigen receptors: a phylogenetic approach. Mol Biol Evol (2000) 17:146-55. doi:10.1093/oxfordjournals. molbev.a026227.
62. Van Laethem F, Tikhonova AN, Pobezinsky LA, Tai X, Kimura MY, Le Saout C, et al. Lck availability during thymic selection determines the recognition specificity of the T cell repertoire. Cell (2013) 154:1326-41. doi:10.1016/j.cell.2013. 08.009.
63. Leinders-Zufall T, Brennan P, Widmayer P, PC S, Maul-Pavicic A, Jäger M, et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science (2004) 306:1033-7. doi:10.1126/science.1102818.
64. Proulx R, Wirth C, Voigt W, Weigelt A, Roscher C, Attinger S, et al. Diversity promotes temporal stability across levels of ecosystem organization in experimental grasslands. PLoS One (2010) 5:e13382. doi:10.1371/journal.pone.0013382.
65. Jousset A, Schulz W, Scheu S, Eisenhauer N. Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J (2011) 5:1108-14. doi:10.1038/ismej.2011.9.
66. Roger F, Godhe A, Gamfeldt L. Genetic diversity and ecosystem functioning in the face of multiple stressors. PLoS One (2012) 7:e45007. doi:10.1371/journal. pone.0045007.
67. Cordero OX, Polz MF. Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol (2014) 12:263-73. doi:10.1038/nrmicro3218.
68. Kitano H. Biological robustness. Nat Rev Genet (2004) 5:826-37. doi:10.1038/nrg1471.
69. Más A, López-Galíndez C, Cacho I, Gómez J, Martínez MA. Unfinished stories on viral quasispecies and Darwinian views of evolution. J Mol Biol (2010) 397:865-77. doi:10.1016/j.jmb.2010.02.005.
70. Domingo E, Sheldon J, Perales C. Viral quasispecies evolution. Microbiol Mol Biol Rev (2012) 76:159-216. doi:10.1128/MMBR.05023-11.
71. Costerton JW. Bacterial biofilms: a common cause of persistent infections. Science (1999) 284:1318-22. doi:10.1126/science.284.5418.1318.
72. Madsen JS, Burmølle M, Hansen LH, Sørensen SJ. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol (2012) 65:183-95. doi:10.1111/j.1574-695X.2012.00960.x.
73. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Ferrer-Admettla A, Pattini L, et al. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet (2011) 7:e1002355. doi:10.1371/journal.pgen.1002355.
74. Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science (2010) 327:167-70. doi:10.1126/science.1179555.
75. Baer B, Schmid-Hempel P, Ecology E, Nw E, Zu C. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature (1999) 397:151-4. doi:10.1038/16451.
76. Penn DJ, Damjanovich K, Potts WK. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc Natl Acad Sci USA (2002) 99:11260-4. doi:10.1073/pnas.162006499.
77. Worley K, Collet J, Spurgin LG, Cornwallis C, Pizzari T, Richardson DS. MHC heterozygosity and survival in red junglefowl. Mol Ecol (2010) 19:3064-75. doi:10.1111/j.1365-294X.2010.04724.x.
78. Morris K, Austin JJ, Belov K. Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics. Biol Lett (2012) 9:1-6. doi:10.1098/rsbl.2012. 0900.