The commensal microbiota drives immune homeostasis

Frontiers in Immunology

Volumn 3, Issue MAR, 2012, Pages

  Arrieta, Marie Claire ^a   Finlay, Barton Brett ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Immune homeostasis; Intestinal microbiota

Indexed keywords

EID: 84874172901     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00033     Document Type: Short Survey

References (60)

1. Abrams, G. D., Bauer, H., and Sprinz, H. (1963). Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab. Invest. 12, 355-364.
2. Adlerberth, I. (2008). Factors influencing the establishment of the intestinal microbiota in infancy. Nestle Nutr. Workshop Ser. Pediatr. Program. 62, 13-29; discussion 29-33.
3. Agrawal,A.,Eastman,Q. M.,and Schatz, D. G. (1998). Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394, 744-751.
4. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J. M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Kurokawa, K., Leclerc, M., Levenez, F., Manichanh, C., Nielsen, H. B., Nielsen, T., Pons, N., Poulain, J., Qin, J., Sicheritz-Ponten, T., Tims, S., Torrents, D., Ugarte, E., Zoetendal, E. G., Wang, J., Guarner, F., Pedersen, O., De Vos, W. M., Brunak, S., Dore, J., Antolin, M., Artiguenave, F., Blottiere, H. M., Almeida, M., Brechot, C., Cara, C., Chervaux, C.,Cultrone,A.,Delorme,C.,Denariaz, G., Dervyn, R., Foerstner, K. U., Friss, C., Van De Guchte, M., Guedon, E., Haimet, F., Huber, W., Van Hylckama-Vlieg, J., Jamet, A., Juste, C., Kaci, G., Knol, J., Lakhdari, O., Layec, S., Le Roux, K., Maguin, E., Merieux, A., Melo Minardi, R., M'Rini, C., Muller, J., Oozeer, R., Parkhill, J., Renault, P., Rescigno, M., Sanchez, N., Sunagawa, S., Torrejon, A., Turner, K., Vandemeulebrouck, G.,Varela,E.,Winogradsky,Y.,Zeller, G., Weissenbach, J., Ehrlich, S. D., and Bork, P. (2011). Enterotypes of the human gut microbiome. Nature 473, 174-180.
5. Atarashi, K., Nishimura, J., Shima, T., Umesaki, Y., Yamamoto, M., Onoue, M., Yagita, H., Ishii, N., Evans, R., Honda, K., and Takeda, K. (2008). ATP drives lamina propria T(H)17 cell differentiation. Nature 455, 808-812.
6. Ather, J. L., Ckless, K., Martin, R., Foley, K. L., Suratt, B. T., Boyson, J. E., Fitzgerald, K. A., Flavell, R. A., Eisenbarth, S. C., and Poynter, M. E. (2011). Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J. Immunol. 187, 64-73.
7. Benson, A. K., Kelly, S. A., Legge, R., Ma, F., Low, S. J., Kim, J., Zhang, M., Oh, P. L., Nehrenberg, D., Hua, K., Kachman, S. D., Moriyama, E. N., Walter, J., Peterson, D. A., and Pomp,D. (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl. Acad. Sci. U.S.A. 107, 18933-18938.
8. Bouskra, D., Brezillon, C., Berard, M., Werts, C., Varona, R., Boneca, I. G., and Eberl, G. (2008). Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456, 507-510.
9. Buonocore, S., Ahern, P. P., Uhlig, H. H., Ivanov, Ii, Littman, D. R., Maloy, K. J., and Powrie, F. (2010). Innate lymphoid cells drive interleukin-23dependent innate intestinal pathology. Nature 464, 1371-1375.
10. Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., and Weiser, J. N. (2010). Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16, 228-231.
11. Dobber, R., Hertogh-Huijbregts, A., Rozing, J., Bottomly, K., and Nagelkerken, L. (1992). The involvement of the intestinal microflora in the expansion of CD4+ T cells with a naive phenotype in the periphery. Dev. Immunol. 2, 141-150.
12. Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent,M.,Gill,S. R.,Nelson,K. E.,and Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science 308, 1635-1638.
13. Endt, K., Stecher, B., Chaffron, S., Slack, E., Tchitchek, N., Benecke, A., Van Maele, L., Sirard, J. C., Mueller, A. J., Heikenwalder, M., Macpherson, A. J., Strugnell, R., Von Mering, C., and Hardt, W. D. (2010). The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog. 6, e1001097. doi:10.1371/journal.ppat.1001097
14. Ferreira, R. B., Gill, N., Willing, B. P., Antunes, L. C., Russell, S. L., Croxen, M. A., and Finlay, B. B. (2011). The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PLoS ONE 6, e20338. doi:10.1371/journal.pone.0020338
15. Gaboriau-Routhiau, V., Rakotobe, S., Lecuyer, E., Mulder, I., Lan, A., Bridonneau, C., Rochet, V., Pisi, A., De Paepe, M., Brandi, G., Eberl, G., Snel, J., Kelly, D., and CerfBensussan, N. (2009). The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677-689.
16. Geuking, M. B., Cahenzli, J., Lawson, M. A., Ng, D. C., Slack, E., Hapfelmeier, S., Mccoy, K. D., and Macpherson, A. J. (2011). Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34, 794-806.
17. Gill, N., Wlodarska, M., and Finlay, B. B. (2010). The future of mucosal immunology: studying an integrated system-wide organ. Nat. Immunol. 11, 558-560.
18. Hansson, G. C., and Johansson, M. E. (2010). The inner of the two Muc2 mucin-dependent mucus layers in colonisdevoidofbacteria.Gut Microbes 1, 51-54.
19. Hooper, L. V., and Macpherson, A. J. (2010). Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10, 159-169.
20. Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., and Littman, D. R. (2009). Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498.
21. Ivanov, I. I., Frutos Rde, L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., Finlay, B. B., and Littman, D. R. (2008). Specific microbiota direct the differentiation of IL17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349.
22. Kinnebrew, M. A., Ubeda, C., Zenewicz, L. A., Smith, N., Flavell, R. A., and Pamer, E. G. (2010). Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201,534-543.
23. Lathrop, S. K., Bloom, S. M., Rao, S. M., Nutsch, K., Lio, C. W., Santacruz, N., Peterson, D. A., Stappenbeck, T. S., and Hsieh, C. S. (2011). Peripheral education of the immune system by colonic commensal microbiota. Nature 478, 250-254.
24. Lee,Y. K., and Mazmanian, S. K. (2010). Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330, 1768-1773.
25. Lee, Y. K., Menezes, J. S., Umesaki, Y., and Mazmanian, S. K. (2010). Microbes and health Sackler colloquium: proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl. 1), 4615-4622.
26. Ley,R. E.,Peterson,D. A.,and Gordon,J. I. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848.
27. Matsunaga, T., and Rahman, A. (1998). What brought the adaptive immune system to vertebrates? The jaw hypothesis and the seahorse. Immunol. Rev. 166, 177-186.
28. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., and Kasper, D. L. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107-118.
29. Mazmanian, S. K., Round, J. L., and Kasper, D. L. (2008). A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625.
30. McFall-Ngai, M. (2007). Adaptive immunity: care for the community. Nature 445, 153.
31. Moreau, M. C., Ducluzeau, R., GuyGrand, D., and Muller, M. C. (1978). Increase in the population of duodenal immunoglobulin A plasmocytes in axenic mice associated with different living or dead bacterial strains of intestinal origin. Infect. Immun. 21, 532-539.
32. Nardi, R. M., Silva, M. E., Vieira, E. C., Bambirra, E. A., and Nicoli, J. R. (1989). Intragastric infection of germfree and conventional mice with Salmonella typhimurium. Braz. J. Med. Biol. Res. 22, 1389-1392.
33. Niess, J. H., Leithauser, F., Adler, G., and Reimann, J. (2008). Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. J. Immunol. 180, 559-568.
34. Ochoa-Reparaz, J., Mielcarz, D. W., Wang, Y., Begum-Haque, S., Dasgupta,S.,Kasper,D. L.,and Kasper,L. H. (2010).A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 3, 487-495.
35. Penders, J., Thijs, C., Vink, C., Stelma, F. F., Snijders, B., Kummeling, I., Van Den Brandt, P. A., and Stobberingh, E. E. (2006). Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511-521.
36. Rask, C., Evertsson, S., Telemo, E., and Wold, A. E. (2005). A full flora, but not monocolonization by Escherichia coli or lactobacilli, supports tolerogenic processing of a fed antigen. Scand. J. Immunol. 61, 529-535.
37. Rescigno, M. (2011). The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol. 32, 256-264.
38. Round, J. L., and Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323.
39. Sekirov, I., and Finlay, B. B. (2009). The role of the intestinal microbiota in enteric infection. J. Physiol. (Lond.) 587, 4159-4167.
40. Sekirov, I., Tam, N. M., Jogova, M., Robertson, M. L., Li, Y. L., Lupp, C., and Finlay, B. B. (2008). Antibioticinduced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect. Immun. 76, 4726-4736.
41. Smith, K., Mccoy, K. D., and Macpherson, A. J. (2007). Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19, 59-69.
42. Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermudez-Humaran, L. G., Gratadoux, J. J., Blugeon, S., Bridonneau, C., Furet, J. P., Corthier, G., Grangette, C., Vasquez, N., Pochart,P.,Trugnan,G.,Thomas,G., Blottiere, H. M., Dore, J., Marteau, P., Seksik, P., and Langella, P. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U.S.A. 105, 16731-16736.
43. Sprinz, H., Kundel, D. W., Dammin, G. J.,Horowitz,R. E.,Schneider,H.,and Formal,S. B. (1961). The response of the germfree guinea pig to oral bacterial challenge with Escherichia coli and Shigella flexneri. Am. J. Pathol. 39, 681-695.
44. Strauch, U. G., Obermeier, F., Grunwald, N., Gurster, S., Dunger, N., Schultz, M., Griese, D. P., Mahler, M., Scholmerich, J., and Rath, H. C. (2005). Influence of intestinal bacteria on induction of regulatory T cells: lessons from a transfer model of colitis. Gut 54, 1546-1552.
45. Swidsinski, A., Loening-Baucke, V., Vaneechoutte, M., and Doerffel, Y. (2008). Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm. Bowel Dis. 14, 147-161.
46. Tap, J., Mondot, S., Levenez, F., Pelletier, E., Caron, C., Furet, J. P., Ugarte, E., Munoz-Tamayo, R., Paslier, D. L., Nalin, R., Dore, J., and Leclerc, M. (2009). Towards the human intestinal microbiota phylogenetic core. Environ. Microbiol. 11, 2574-2584.
47. 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. (2009). A core gut microbiome in obese and lean twins. Nature 457, 480-484.
48. Uematsu, S., Fujimoto, K., Jang, M. H., Yang,B. G.,Jung,Y. J.,Nishiyama,M., Sato, S., Tsujimura, T., Yamamoto, M., Yokota, Y., Kiyono, H., Miyasaka, M., Ishii, K. J., and Akira, S. (2008). Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Tolllikereceptor5.Nat. Immunol. 9, 769-776.
49. Umesaki, Y., Okada, Y., Matsumoto, S., Imaoka, A., and Setoyama, H. (1995). Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class-II molecules and fucosyl asialo Gm1 glycolipids on the small-intestinal epithelial-cells in the ex-germ-free mouse. Microbiol. Immunol. 39, 555-562.
50. van der Waaij, D., Berghuis-De Vries, J. M., and Lekkerkerk, L.-V. (1971). Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.) 69, 405-411.
51. Wen, L., Ley, R. E., Volchkov, P. Y., Stranges, P. B., Avanesyan, L., Stonebraker, A. C., Hu, C. Y., Wong, F. S., Szot, G. L., Bluestone, J. A., Gordon, J. I., and Chervonsky, A. V. (2008). Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455, 1109-1113.
52. Willing, B., Halfvarson, J., Dicksved, J., Rosenquist, M., Jarnerot, G., Engstrand, L., Tysk, C., and Jansson, J. K. (2009). Twin studies reveal specific imbalances in the mucosaassociated microbiota of patients with ileal Crohn's disease. Inflamm. Bowel Dis. 15, 653-660.
53. Willing, B. P., Gill, N., and Finlay, B. B. (2010). The role of the immune system in regulating the microbiota. Gut Microbes 1, 213-223.
54. Willing, B. P., Vacharaksa, A., Croxen, M., Thanachayanont, T., and Finlay, B. B. (2011). Altering host resistance to infections through microbial transplantation. PLoS ONE 6, e26988. doi:10.1371/journal.pone.0026988
55. Willing, B. P., and Van Kessel, A. G. (2007). Enterocyte proliferation and apoptosis in the caudal small intestine is influenced by the composition of colonizing commensal bacteria in the neonatal gnotobiotic pig. J. Anim. Sci. 85, 3256-3266.
56. Wlodarska, M., Willing, B., Keeney, K. M., Menendez, A., Bergstrom, K. S., Gill, N., Russell, S. L., Vallance, B. A., and Finlay, B. B. (2011). Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentiuminduced colitis. Infect. Immun. 79, 1536-1545.
57. Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y. Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., Sinha, R., Gilroy, E., Gupta, K., Baldassano,R., Nessel, L., Li, H., Bushman, F. D., and Lewis, J. D. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108.
58. Wu, H. J., Ivanov, Ii, Darce, J., Hattori, K., Shima, T., Umesaki, Y., Littman, D. R., Benoist, C., and Mathis, D. (2010). Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32, 815-827.
59. Zachar, Z., and Savage, D. C. (1979). Microbial interference and colonization of the murine gastrointestinal tract by Listeria monocytogenes. Infect. Immun. 23, 168-174.
60. Zaph, C., Du, Y., Saenz, S. A., Nair, M. G., Perrigoue, J. G., Taylor, B. C., Troy, A. E., Kobuley, D. E., Kastelein, R. A., Cua, D. J., Yu, Y., and Artis, D. (2008). Commensal-dependent expression of IL-25 regulates the IL23-IL-17 axis in the intestine. J. Exp. Med. 205, 2191-2198.