Deciphering the tête-è-tête between the microbiota and the immune system

Journal of Clinical Investigation

Volumn 124, Issue 10, 2014, Pages 4197-4203

  Surana, Neeraj K ^a,b   Kasper, Dennis L ^b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTEROIDES FRAGILIS; CLOSTRIDIUM; COMMENSAL; DYSBIOSIS; FAECALIBACTERIUM PRAUSNITZII; GNOTOBIOTICS; HOST RANGE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOMODULATION; INTESTINE FLORA; MATURATION; MICROBIAL COMMUNITY; NONHUMAN; PREVOTELLA; REVIEW; STAPHYLOCOCCUS EPIDERMIDIS; ANIMAL; BACTERIUM; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE; PHYSIOLOGY;

ANIMALS; BACTERIA; HUMANS; IMMUNE SYSTEM; INTESTINES; MICE; MICROBIOTA;

EID: 84907494648     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI72332     Document Type: Review

References (84)

1. De Kruif P. Microbe Hunters. New York, New York, USA: Harcourt, Inc.; 1926.
2. Kendall AI. Some observations on the study of the intestinal bacteria. J Biol Chem. 1909;6:499-507.
3. Hooper LV, Gordon JI. Commensal hostbacterial relationships in the gut. Science. 2001;292(5519):1115-1118.
4. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science. 2001;291(5505):881-884.
5. Luckey TD. Introduction to intestinal microecology. Am J Clin Nutr. 1972;25(12):1292-1294.
6. Smith MI, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339(6119):548-554.
7. Van der Waaij D, Berghuis-de Vries JM. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond). 1971;69(3):405-411.
8. Chung H, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149(7):1578-1593.
9. Bhatt AS, et al. Sequence-based discovery of Bradyrhizobium enterica in cord colitis syndrome. N Engl J Med. 2013;369(6):517-528.
10. De Goffau MC, et al. Fecal microbiota composition differs between children with beta-cell autoimmunity and those without. Diabetes. 2013;62(4):1238-1244.
11. Ege MJ, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364(8):701-709.
12. Huang YJ, et al. The airway microbiome in severe asthma. Ann Am Thorac Soc. 2014;11 (suppl 1):S78.
13. Morgan XC, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79.
14. Wang Y, Kasper LH. The role of microbiome in central nervous system disorders. Brain Behav Immun. 2014;38:1-12.
15. Wong BC, et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004;291(2):187-194.
16. Xuan C, et al. Microbial dysbiosis is associated with human breast cancer. PLoS One. 2014;9(1):e83744.
17. Sokol H, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105(43):16731-16736.
18. Scher JU, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.
19. Metchnikoff E. The Prolongation Of Life: Optimistic Studies. New York, New York, USA: G. P. Putnam's Sons; 1908.
20. Pamer EG. Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns. Mucosal Immunol. 2014;7(2):210-214.
21. Van Nood E, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407-415.
22. Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ. Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn's disease. World J Gastroenterol. 2013;19(41):7213-7216.
23. Glimstedt G. Bakterienfreie Meerscheinchen. Ac ta Pathol Microbiol Scand. 1936;30(1):1-295.
24. Gordon HA. Morphological and physiological characterization of germfree life. Ann N Y Acad Sci. 1959;78:208-220.
25. Hill DA, et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 2010;3(2):148-158.
26. Honda K, Littman DR. The microbiome in infectious disease and inflammation. Annu Rev Immunol. 2012;30:759-795.
27. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268-1273.
28. Ivanov II, Honda K. Intestinal commensal microbes as immune modulators. Cell Host Microbe. 2012;12(4):496-508.
29. Kamada N, Nunez G. Role of the gut microbiota in the development and function of lymphoid cells. J Immunol. 2013;190(4):1389-1395.
30. Surana NK, Kasper DL. The yin yang of bacterial polysaccharides: lessons learned from B.fragilis PSA. Immunol Rev. 2012;245(1):13-26.
31. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122(1):107-118.
32. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620-625.
33. Ochoa-Reparaz J, et al. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression. J Immunol. 2010;185(7):4101-4108.
34. Ochoa-Reparaz J, et al. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 2010;3(5):487-495.
35. Round JL, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332(6032):974-977.
36. Wang Q, et al. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J Exp Med. 2006;203(13):2853-2863.
37. An D, et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell. 2014;156(1-2):123-133.
38. Wieland Brown LC, et al. Production of α-galactosylceramide by a prominent member of the human gut microbiota. PLoS Biol. 2013;11(7):e1001610.
39. Atarashi K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500(7461):232-236.
40. Atarashi K, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331(6015):337-341.
41. Faith JJ, Ahern PP, Ridaura VK, Cheng J, Gordon JI. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci Transl Med. 2014;6(220):220ra211.
42. Gaboriau-Routhiau V, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31(4):677-689.
43. Ivanov II, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139(3):485-498.
44. Chappert P, Bouladoux N, Naik S, Schwartz RH. Specific gut commensal flora locally alters T cell tuning to endogenous ligands. Immunity. 2013;38(6):1198-1210.
45. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229-241.
46. Wen L, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455(7216):1109-1113.
47. Jiang W, et al. Recognition of gut microbiota by NOD2 is essential for the homeostasis of intestinal intraepithelial lymphocytes. J Exp Med. 2013;210(11):2465-2476.
48. Yu Q, Tang C, Xun S, Yajima T, Takeda K, Yoshikai Y. MyD88-dependent signaling for IL-15 production plays an important role in maintenance of CD8 alpha alpha TCR alpha beta and TCR gamma delta intestinal intraepithelial lymphocytes. J Immunol. 2006;176(10):6180-6185.
49. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature. 2013;501(7467):426-429.
50. + regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107(27):12204-12209.
51. Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC, Kasper DL. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe. 2014;15(4):413-423.
52. Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe. 2012;12(4):509-520.
53. Guy-Grand D, Griscelli C, Vassalli P. The gut-associated lymphoid system: nature and properties of the large dividing cells. Eur J Immunol. 1974;4(6):435-443.
54. Guy-Grand D, Griscelli C, Vassalli P. The mouse gut T lymphocyte, a novel type of T cell. Nature, origin, and traffic in mice in normal and graft-versus-host conditions. J Exp Med. 1978;148(6):1661-1677.
55. Williams AM, et al. Intestinal alpha beta T cells differentiate and rearrange antigen receptor genes in situ in the human infant. J Immunol. 2004;173(12):7190-7199.
56. Olszak T, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336(6080):489-493.
57. Arpaia N, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-455.
58. Furusawa Y, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446-450.
59. Smith PM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569-573.
60. Davis CP, Savage DC. Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect Immun. 1974;10(4):948-956.
61. Fraher MH, O'Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol. 2012;9(6):312-322.
62. Vujkovic-Cvijin I, et al. Dysbiosis of the gut microbiota is associated with hiv disease progression and tryptophan catabolism. Sci Transl Med. 2013;5(193):193ra191.
63. Eckburg PB, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638.
64. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011;108(suppl 1):4615-4622.
65. Noverr MC, Falkowski NR, McDonald RA, McKenzie AN, Huffnagle GB. Development of allergic airway disease in mice following antibiotic therapy and fungal microbiota increase: role of host genetics, antigen, and interleukin-13. Infec t Immun. 2005;73(1):30-38.
66. Wu HJ, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32(6):815-827.
67. Naik S, et al. Compartmentalized control of skin immunity by resident commensals. Science. 2012;337(6098):1115-1119.
68. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med. 2002;347(12):911-920.
69. Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299(6710):1259-1260.
70. Ege MJ, et al. Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children. J Allergy Clin Immunol. 2006;117(4):817-823.
71. Ege MJ, et al. Specific IgE to allergens in cord blood is associated with maternal immunity to Toxoplasma gondii and rubella virus. Allergy. 2008;63(11):1505-1511.
72. Aagaaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra265.
73. Chen VL, Surana NK, Duan J, Kasper DL. Role of murine intestinal interleukin-1 receptor 1-expressing lymphoid tissue inducer-like cells in salmonella infection. PLoS One. 2013;8(6):e65405.
74. Gorbach SL, Bartlett JG. Anaerobic infections (second of three parts). N Engl J Med. 1974;290(22):1237-1245.
75. Polk BF, Kasper DL. Bacteroides fragilis subspecies in clinical isolates. Ann Intern Med. 1977;86(5):569-571.
76. Tzianabos AO, Onderdonk AB, Rosner B, Cisneros RL, Kasper DL. Structural features of polysaccharides that induce intra-abdominal abscesses. Science. 1993;262(5132):416-419.
77. Mathis D, Benoist C. Microbiota and autoimmune disease: the hosted self. Cell Host Microbe. 2011;10(4):297-301.
78. Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, Mathis D. Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad Sci U S A. 2011;108(28):11548-11553.
79. Cadwell K, et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell. 2010;141(7):1135-1145.
80. Caliskan M, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med. 2013;368(15):1398-1407.
81. Yatsunenko T, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222-227.
82. Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell. 2013;152(4):884-894.
83. Lysenko ES, Ratner AJ, Nelson AL, Weiser JN. The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog. 2005;1(1):e1.
84. Winter SE, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426-429.