The hygiene hypothesis: an evolutionary perspective

Microbes and Infection

Volumn 12, Issue 6, 2010, Pages 421-427

  Sironi, Manuela ^a   Clerici, Mario ^b  

^a SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Host pathogen interactions; Natural selection; Population genetics

Indexed keywords

ADAPTIVE IMMUNITY; COEVOLUTION; ENVIRONMENTAL SANITATION; GENETIC ASSOCIATION; GENETIC REGULATION; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOGENETICS; IMMUNOREGULATION; LIFE EXPECTANCY; MOLECULAR EVOLUTION; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; SHORT SURVEY; SINGLE NUCLEOTIDE POLYMORPHISM; EVOLUTION; GENETIC SELECTION; HYGIENE;

EVOLUTION; GENETICS, POPULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; HYGIENE; SELECTION, GENETIC; BIOLOGICAL EVOLUTION;

EID: 77952671750     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2010.02.002     Document Type: Short Survey

References (68)

1. Strachan D.P. Hay fever, hygiene, and household size. BMJ 299 (1989) 1259-1260
2. Strachan D.P. Allergy and family size: a riddle worth solving. Clin. Exp. Allergy 27 (1997) 235-236
3. Lemanske Jr. R.F. The childhood origins of asthma (COAST) study. Pediatr. Allergy Immunol. 13 Suppl. 15 (2002) 38-43
4. Celedon J.C., Wright R.J., Litonjua A.A., Sredl D., Ryan L., Weiss S.T., and Gold D.R. Day care attendance in early life, maternal history of asthma, and asthma at the age of 6 years. Am. J. Respir. Crit. Care Med. 167 (2003) 1239-1243
5. Hoffjan S., and Epplen J.T. The genetics of atopic dermatitis: recent findings and future options. J. Mol. Med. 83 (2005) 682-692
6. Riedler J., Braun-Fahrlander C., Eder W., Schreuer M., Waser M., Maisch S., Carr D., Schierl R., Nowak D., von Mutius E., and ALEX Study Team. Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 358 (2001) 1129-1133
7. Braun-Fahrlander C., Riedler J., Herz U., Eder W., Waser M., Grize L., Maisch S., Carr D., Gerlach F., Bufe A., Lauener R.P., Schierl R., Renz H., Nowak D., von Mutius E., and Allergy and Endotoxin Study Team. Environmental exposure to endotoxin and its relation to asthma in school-age children. N. Engl. J. Med. 347 (2002) 869-877
8. Lucey D.R., Clerici M., and Shearer G.M. Type 1 and type 2 cytokine dysregulation in human infectious, neoplastic, and inflammatory diseases. Clin. Microbiol. Rev. 9 (1996) 532-562
9. Vercelli D. Mechanisms of the hygiene hypothesis-molecular and otherwise. Curr. Opin. Immunol. 18 (2006) 733-737
10. Garn H., and Renz H. Epidemiological and immunological evidence for the hygiene hypothesis. Immunobiology 212 (2007) 441-452
11. Rook G.A. Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 126 (2009) 3-11
12. Krug N., Madden J., Redington A.E., Lackie P., Djukanovic R., Schauer U., Holgate S.T., Frew A.J., and Howarth P.H. T-cell cytokine profile evaluated at the single cell level in BAL and blood in allergic asthma. Am. J. Respir. Cell Mol. Biol. 14 (1996) 319-326
13. Lammas D.A., Casanova J.L., and Kumararatne D.S. Clinical consequences of defects in the IL-12-dependent interferon-gamma (IFN-gamma) pathway. Clin. Exp. Immunol. 121 (2000) 417-425
14. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., and Yamaguchi T. Regulatory T cells: how do they suppress immune responses?. Int. Immunol. 21 (2009) 1105-1111
15. Rook G.A., and Lowry C.A. The hygiene hypothesis and psychiatric disorders. Trends Immunol. 29 (2008) 150-158
16. Dobson A. In: Jones S., Martin R., and Pilbeam D. (Eds). The Cambridge Encyclopedia of Human Evolution (1992), Cambridge University Press, Cambridge 411-420
17. Wolfe N.D., Dunavan C.P., and Diamond J. Origins of major human infectious diseases. Nature 447 (2007) 279-283
18. Casanova J.L., and Abel L. Inborn errors of immunity to infection: the rule rather than the exception. J. Exp. Med. 202 (2005) 197-201
19. Kapp C. WHO warns of microbial threat. Lancet 353 (1999) 2222
20. Haldane J.B.S. Anonymous Selected Genetic Papers of J.B.S. Haldane (1949), Garland Publ. Inc., New York and London 325-334
21. Pozzoli U., Fumagalli M., Cagliani R., Comi G.P., Bresolin N., Clerici M., and Sironi M. The role of protozoa-driven selection in shaping human genetic variability. Trends Genet. (2010) 10.1016/j.tig.2009.12.010
22. Castillo-Davis C.I., Kondrashov F.A., Hartl D.L., and Kulathinal R.J. The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res. 14 (2004) 802-811
23. Sironi M., Menozzi G., Comi G.P., Cagliani R., Bresolin N., and Pozzoli U. Analysis of intronic conserved elements indicates that functional complexity might represent a major source of negative selection on non-coding sequences. Hum. Mol. Genet. 14 (2005) 2533-2546
24. Kosiol C., Vinar T., da Fonseca R.R., Hubisz M.J., Bustamante C.D., Nielsen R., and Siepel A. Patterns of positive selection in six mammalian genomes. PLoS Genet. 4 (2008) e1000144
25. Voight B.F., Kudaravalli S., Wen X., and Pritchard J.K. A map of recent positive selection in the human genome. PLoS Biol. 4 (2006) e72
26. Wang E.T., Kodama G., Baldi P., and Moyzis R.K. Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 135-140
27. Prugnolle F., Manica A., Charpentier M., Guegan J.F., Guernier V., and Balloux F. Pathogen-driven selection and worldwide HLA class I diversity. Curr. Biol. 15 (2005) 1022-1027
28. Fumagalli M., Cagliani R., Pozzoli U., Riva S., Comi G.P., Menozzi G., Bresolin N., and Sironi M. Widespread balancing selection and pathogen-driven selection at blood group antigen genes. Genome Res. 19 (2009) 199-212
29. Fumagalli M., Pozzoli U., Cagliani R., Comi G.P., Riva S., Clerici M., Bresolin N., and Sironi M. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J. Exp. Med. 206 (2009) 1395-1408
30. Cagliani R., Fumagalli M., Riva S., Pozzoli U., Comi G.P., Menozzi G., Bresolin N., and Sironi M. The signature of long-standing balancing selection at the human defensin beta-1 promoter. Genome Biol. 9 (2008) R143
31. Andres A.M., Hubisz M.J., Indap A., Torgerson D.G., Degenhardt J.D., Boyko A.R., Gutenkunst R.N., White T.J., Green E.D., Bustamante C.D., Clark A.G., and Nielsen R. Targets of balancing selection in the human genome. Mol. Biol. Evol. 26 (2009) 2755-2764
32. Ferrer-Admetlla A., Bosch E., Sikora M., Marques-Bonet T., Ramirez-Soriano A., Muntasell A., Navarro A., Lazarus R., Calafell F., Bertranpetit J., and Casals F. Balancing selection is the main force shaping the evolution of innate immunity genes. J. Immunol. 181 (2008) 1315-1322
33. Barreiro L.B., Ben-Ali M., Quach H., Laval G., Patin E., Pickrell J.K., Bouchier C., Tichit M., Neyrolles O., Gicquel B., Kidd J.R., Kidd K.K., Alcais A., Ragimbeau J., Pellegrini S., Abel L., Casanova J.L., and Quintana-Murci L. Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet. 5 (2009) e1000562
34. Fumagalli M., Pozzoli U., Cagliani R., Comi G.P., Bresolin N., Clerici M., and Sironi M. Genome-wide identification of susceptibility alleles for viral infections through a population genetics approach. PLoS Genet. 6 (2010) e1000849
35. Dunne D.W., and Cooke A. A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol. 5 (2005) 420-426
36. Maizels R.M., Balic A., Gomez-Escobar N., Nair M., Taylor M.D., and Allen J.E. Helminth parasites-masters of regulation. Immunol. Rev. 201 (2004) 89-116
37. Hotez P.J., Brindley P.J., Bethony J.M., King C.H., Pearce E.J., and Jacobson J. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 118 (2008) 1311-1321
38. Jackson J.A., Friberg I.M., Little S., and Bradley J.E. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies?. Immunology 126 (2009) 18-27
39. McIntire J.J., Umetsu S.E., Macaubas C., Hoyte E.G., Cinnioglu C., Cavalli-Sforza L.L., Barsh G.S., Hallmayer J.F., Underhill P.A., Risch N.J., Freeman G.J., DeKruyff R.H., and Umetsu D.T. Immunology: hepatitis A virus link to atopic disease. Nature 425 (2003) 576
40. Bach J.F. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347 (2002) 911-920
41. Nakajima T., Wooding S., Satta Y., Jinnai N., Goto S., Hayasaka I., Saitou N., Guan-Jun J., Tokunaga K., Jorde L.B., Emi M., and Inoue I. Evidence for natural selection in the HAVCR1 gene: high degree of amino-acid variability in the mucin domain of human HAVCR1 protein. Genes Immun. 6 (2005) 398-406
42. Barreiro L.B., and Quintana-Murci L. From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat. Rev. Genet. 11 (2010) 17-30
43. Kivity S., Agmon-Levin N., Blank M., and Shoenfeld Y. Infections and autoimmunity-friends or foes?. Trends Immunol. 30 (2009) 409-414
44. Hunt K.A., Zhernakova A., Turner G., Heap G.A., Franke L., Bruinenberg M., Romanos J., Dinesen L.C., Ryan A.W., Panesar D., Gwilliam R., Takeuchi F., McLaren W.M., Holmes G.K., Howdle P.D., Walters J.R., Sanders D.S., Playford R.J., Trynka G., Mulder C.J., Mearin M.L., Verbeek W.H., Trimble V., Stevens F.M., O'Morain C., Kennedy N.P., Kelleher D., Pennington D.J., Strachan D.P., McArdle W.L., Mein C.A., Wapenaar M.C., Deloukas P., McGinnis R., McManus R., Wijmenga C., and van Heel D.A. Newly identified genetic risk variants for celiac disease related to the immune response. Nat. Genet. 40 (2008) 395-402
45. Sirota M., Schaub M.A., Batzoglou S., Robinson W.H., and Butte A.J. Autoimmune disease classification by inverse association with SNP alleles. PLoS Genet. 5 (2009) e1000792
46. Dethlefsen L., McFall-Ngai M., and Relman D.A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 (2007) 811-818
47. Ley R.E., Lozupone C.A., Hamady M., Knight R., and Gordon J.I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6 (2008) 776-788
48. Ley R.E., Peterson D.A., and Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124 (2006) 837-848
49. McFall-Ngai M. Adaptive immunity: care for the community. Nature 445 (2007) 153
50. Peterson D.A., McNulty N.P., Guruge J.L., and Gordon J.I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell. Host Microbe 2 (2007) 328-339
51. Fagarasan S., Muramatsu M., Suzuki K., Nagaoka H., Hiai H., and Honjo T. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 298 (2002) 1424-1427
52. Toivanen P., Vaahtovuo J., and Eerola E. Influence of major histocompatibility complex on bacterial composition of fecal flora. Infect. Immun. 69 (2001) 2372-2377
53. Lanyon C.V., Rushton S.P., O'donnell A.G., Goodfellow M., Ward A.C., Petrie M., Jensen S.P., Morris Gosling L., and Penn D.J. Murine scent mark microbial communities are genetically determined. FEMS Microbiol. Ecol. 59 (2007) 576-583
54. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., Hu C., Wong F.S., Szot G.L., Bluestone J.A., Gordon J.I., and Chervonsky A.V. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455 (2008) 1109-1113
55. Stewart J.A., Chadwick V.S., and Murray A. Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children. J. Med. Microbiol. 54 (2005) 1239-1242
56. Zoetendal E.G., Akkermans A.D.L., Akkermans-van Vliet W.M., de Visser J.A.G.M., and de Vos W.M. The host genotype affects the bacterial community in the human gastronintestinal tract. Microb. Ecol. Health Dis. 13 (2001) 129-134
57. Turnbaugh P.J., Hamady M., Yatsunenko T., Cantarel B.L., Duncan A., Ley R.E., Sogin M.L., Jones W.J., Roe B.A., Affourtit J.P., Egholm M., Henrissat B., Heath A.C., Knight R., and Gordon J.I. A core gut microbiome in obese and lean twins. Nature 457 (2009) 480-484
58. Penders J., Thijs C., Vink C., Stelma F.F., Snijders B., Kummeling I., van den Brandt P.A., and Stobberingh E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118 (2006) 511-521
59. Mazmanian S.K., Liu C.H., Tzianabos A.O., and Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122 (2005) 107-118
60. Strauch U.G., Obermeier F., Grunwald N., Gurster S., Dunger N., Schultz M., Griese D.P., Mahler M., Scholmerich J., and Rath H.C. Influence of intestinal bacteria on induction of regulatory T cells: lessons from a transfer model of colitis. Gut 54 (2005) 1546-1552
61. Ivanov I.I., Frutos Rde L., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., and Littman D.R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell. Host Microbe 4 (2008) 337-349
62. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., and Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 13780-13785
63. Sjogren Y.M., Jenmalm M.C., Bottcher M.F., Bjorksten B., and Sverremark-Ekstrom E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin. Exp. Allergy 39 (2009) 518-526
64. Mah K.W., Bjorksten B., Lee B.W., van Bever H.P., Shek L.P., Tan T.N., Lee Y.K., and Chua K.Y. Distinct pattern of commensal gut microbiota in toddlers with eczema. Int. Arch. Allergy Immunol. 140 (2006) 157-163
65. Watanabe S., Narisawa Y., Arase S., Okamatsu H., Ikenaga T., Tajiri Y., and Kumemura M. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J. Allergy Clin. Immunol. 111 (2003) 587-591
66. Marra F., Marra C.A., Richardson K., Lynd L.D., Kozyrskyj A., Patrick D.M., Bowie W.R., and Fitzgerald J.M. Antibiotic use in children is associated with increased risk of asthma. Pediatrics 123 (2009) 1003-1010
67. Kozyrskyj A.L., Ernst P., and Becker A.B. Increased risk of childhood asthma from antibiotic use in early life. Chest 131 (2007) 1753-1759
68. Lederberg J. Infectious history. Science 288 (2000) 287-293