Immune and genetic gardening of the intestinal microbiome

FEBS Letters

Volumn 588, Issue 22, 2014, Pages 4102-4111

  Jacobs, Jonathan P ^a   Braun, Jonathan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crohn's disease; Epithelium; Immune system; Inflammatory bowel disease; Innate lymphoid cell; Intestine; Microbial ecology; Microbiome; Mucosal immunology; Pattern recognition receptor; Ulcerative colitis

Indexed keywords

GLYCOPROTEIN; INFLAMMASOME; INTERLEUKIN 18 BINDING PROTEIN; TOLL LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; COLON; COMMUNITY STRUCTURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DYSBIOSIS; EPITHELIUM CELL; GENETIC ANALYSIS; GENETIC VARIABILITY; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LONGITUDINAL STUDY; LYMPHOID CELL; MICROBIAL COMMUNITY; MICROBIOME; MOUSE; MUCOSAL IMMUNITY; NATURAL KILLER T CELL; NONHUMAN; PATTERN RECOGNITION; SMALL INTESTINE; T LYMPHOCYTE; ANIMAL; GENETIC VARIATION; IMMUNITY; IMMUNOLOGY; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; GENETIC VARIATION; HUMANS; IMMUNITY; INTESTINAL MUCOSA; INTESTINES; MICROBIOTA; RECEPTORS, PATTERN RECOGNITION;

EID: 84908354373     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.02.052     Document Type: Review

References (150)

1. J. Braun Unsettling facts of life: bacterial commensalism, epithelial adherence, and inflammatory bowel disease Gastroenterology 122 2002 228 230
2. F. Backhed, J.K. Manchester, C.F. Semenkovich, and J.I. Gordon Mechanisms underlying the resistance to diet-induced obesity in germ-free mice Proc. Natl. Acad. Sci. USA 104 2007 979 984
3. J. Petersson Importance and regulation of the colonic mucus barrier in a mouse model of colitis Am. J. Physiol. Gastrointest. Liver Physiol. 300 2011 G327 G333
4. C. Reinhardt, M. Bergentall, T.U. Greiner, F. Schaffner, G. Ostergren-Lunden, L.C. Petersen, W. Ruf, and F. Backhed Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling Nature 483 2012 627 631
5. J. Swann Gut microbiome modulates the toxicity of hydrazine: a metabonomic study Mol. BioSyst. 5 2009 351 355
6. T.D. Lawley, and A.W. Walker Intestinal colonization resistance Immunology 138 2013 1 11
7. R.E. Ley, D.A. Peterson, and J.I. Gordon Ecological and evolutionary forces shaping microbial diversity in the human intestine Cell 124 2006 837 848
8. L. Dethlefsen, M. McFall-Ngai, and D.A. Relman An ecological and evolutionary perspective on human-microbe mutualism and disease Nature 449 2007 811 818
9. R.E. Ley Evolution of mammals and their gut microbes Science 320 2008 1647 1651
10. B.D. Muegge Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans Science 332 2011 970 974
11. M.J. Claesson Gut microbiota composition correlates with diet and health in the elderly Nature 488 2012 178 184
12. G.D. Wu Linking long-term dietary patterns with gut microbial enterotypes Science 334 2011 105 108
13. Y. Moodley The peopling of the Pacific from a bacterial perspective Science 323 2009 527 530
14. M.G. Dominguez-Bello, E.K. Costello, M. Contreras, M. Magris, G. Hidalgo, N. Fierer, and R. Knight Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns Proc. Natl. Acad. Sci. USA 107 2010 11971 11975
15. P.A. Vaishampayan, J.V. Kuehl, J.L. Froula, J.L. Morgan, H. Ochman, and M.P. Francino Comparative metagenomics and population dynamics of the gut microbiota in mother and infant Genome Biol. Evol. 2 2010 53 66
16. J.E. Koenig, A. Spor, N. Scalfone, A.D. Fricker, J. Stombaugh, R. Knight, L.T. Angenent, and R.E. Ley Succession of microbial consortia in the developing infant gut microbiome Proc. Natl. Acad. Sci. USA 108 Suppl. 1 2011 4578 4585
17. J. McCafferty, M. Muhlbauer, R.Z. Gharaibeh, J.C. Arthur, E. Perez-Chanona, W. Sha, C. Jobin, and A.A. Fodor Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model ISME J. 7 2013 2116 2125
18. O. Takeuchi, and S. Akira Pattern recognition receptors and inflammation Cell 140 2010 805 820
19. H. von Bernuth Pyogenic bacterial infections in humans with MyD88 deficiency Science 321 2008 691 696
20. L. Wen Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
21. A.L. Frantz, E.W. Rogier, C.R. Weber, L. Shen, D.A. Cohen, L.A. Fenton, M.E. Bruno, and C.S. Kaetzel Targeted deletion of MyD88 in intestinal epithelial cells results in compromised antibacterial immunity associated with downregulation of polymeric immunoglobulin receptor, mucin-2, and antibacterial peptides Mucosal Immunol. 5 2012 501 512
22. S. Vaishnava The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine Science 334 2011 255 258
23. M. Vijay-Kumar Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
24. M. Vijay-Kumar Deletion of TLR5 results in spontaneous colitis in mice J. Clin. Invest. 117 2007 3909 3921
25. F.A. Carvalho Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice Cell Host Microbe 12 2012 139 152
26. R. Kellermayer Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice FASEB J. 25 2011 1449 1460
27. C. Ubeda, L. Lipuma, A. Gobourne, A. Viale, I. Leiner, M. Equinda, R. Khanin, and E.G. Pamer Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice J. Exp. Med. 209 2012 1445 1456
28. L. Franchi, N. Warner, K. Viani, and G. Nunez Function of Nod-like receptors in microbial recognition and host defense Immunol. Rev. 227 2009 106 128
29. J.P. Ting, J.A. Duncan, and Y. Lei How the noninflammasome NLRs function in the innate immune system Science 327 2010 286 290
30. L.H. Travassos Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry Nat. Immunol. 11 2010 55 62
31. A. Couturier-Maillard NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer J. Clin. Invest. 123 2013 700 711
32. A. Rehman, C. Sina, O. Gavrilova, R. Hasler, S. Ott, J.F. Baines, S. Schreiber, and P. Rosenstiel Nod2 is essential for temporal development of intestinal microbial communities Gut 60 2011 1354 1362
33. T. Petnicki-Ocwieja, T. Hrncir, Y.J. Liu, A. Biswas, T. Hudcovic, H. Tlaskalova-Hogenova, and K.S. Kobayashi Nod2 is required for the regulation of commensal microbiota in the intestine Proc. Natl. Acad. Sci. USA 106 2009 15813 15818
34. E. Li Inflammatory bowel diseases phenotype, C. difficile and NOD2 genotype are associated with shifts in human ileum associated microbial composition PLoS ONE 7 2012 e26284
35. S.J. Robertson, J.Y. Zhou, K. Geddes, S.J. Rubino, J.H. Cho, S.E. Girardin, and D.J. Philpott Nod1 and Nod2 signaling does not alter the composition of intestinal bacterial communities at homeostasis Gut Microbes 4 2013 222 231
36. L. Franchi, R. Munoz-Planillo, and G. Nunez Sensing and reacting to microbes through the inflammasomes Nat. Immunol. 13 2012 325 332
37. R. Zhou, A.S. Yazdi, P. Menu, and J. Tschopp A role for mitochondria in NLRP3 inflammasome activation Nature 469 2011 221 225
38. E. Elinav NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis Cell 145 2011 745 757
39. J. Henao-Mejia Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 482 2012 179 185
40. Y. Sun Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice Gastroenterology 144 2013 1478 1487 1487e1-1487e8
41. W.P. Arend, G. Palmer, and C. Gabay IL-1, IL-18, and IL-33 families of cytokines Immunol. Rev. 223 2008 20 38
42. A. Cederlund, G.H. Gudmundsson, and B. Agerberth Antimicrobial peptides important in innate immunity FEBS J. 278 2011 3942 3951
43. P. Vora Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells J. Immunol. 173 2004 5398 5405
44. S. Ghannam CCL20 and beta-defensin-2 induce arrest of human Th17 cells on inflamed endothelium in vitro under flow conditions J. Immunol. 186 2011 1411 1420
45. H.C. Clevers, and C.L. Bevins Paneth cells: maestros of the small intestinal crypts Annu. Rev. Physiol. 75 2013 289 311
46. N.H. Salzman Enteric defensins are essential regulators of intestinal microbial ecology Nat. Immunol. 11 2010 76 83
47. I.I. Ivanov Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 2009 485 498
48. T. Hashimoto ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation Nature 487 2012 477 481
49. Y. De, Q. Chen, A.P. Schmidt, G.M. Anderson, J.M. Wang, J. Wooters, J.J. Oppenheim, and O. Chertov LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells J. Exp. Med. 192 2000 1069 1074
50. J. Schauber Expression of the cathelicidin LL-37 is modulated by short chain fatty acids in colonocytes: relevance of signalling pathways Gut 52 2003 735 741
51. R. Raqib Improved outcome in shigellosis associated with butyrate induction of an endogenous peptide antibiotic Proc. Natl. Acad. Sci. USA 103 2006 9178 9183
52. P.T. Liu Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response Science 311 2006 1770 1773
53. J.H. Ooi, Y. Li, C.J. Rogers, and M.T. Cantorna Vitamin D regulates the gut microbiome and protects mice from dextran sodium sulfate-induced colitis J. Nutr. 143 2013 1679 1686
54. A. Mukherji, A. Kobiita, T. Ye, and P. Chambon Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs Cell 153 2013 812 827
55. N. Liu Altered endocrine and autocrine metabolism of vitamin D in a mouse model of gastrointestinal inflammation Endocrinology 149 2008 4799 4808
56. J. Kong, Z. Zhang, M.W. Musch, G. Ning, J. Sun, J. Hart, M. Bissonnette, and Y.C. Li Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier Am. J. Physiol. Gastrointest. Liver Physiol. 294 2008 G208 G216
57. W. Liu Intestinal epithelial vitamin D receptor signaling inhibits experimental colitis J. Clin. Invest. 123 2013 3983 3996
58. D. Bruce, and M.T. Cantorna Intrinsic requirement for the vitamin D receptor in the development of CD8alphaalpha-expressing T cells J. Immunol. 186 2011 2819 2825
59. S. Yu, D. Bruce, M. Froicu, V. Weaver, and M.T. Cantorna Failure of T cell homing, reduced CD4/CD8alphaalpha intraepithelial lymphocytes, and inflammation in the gut of vitamin D receptor KO mice Proc. Natl. Acad. Sci. USA 105 2008 20834 20839
60. S. Yu, and M.T. Cantorna The vitamin D receptor is required for iNKT cell development Proc. Natl. Acad. Sci. USA 105 2008 5207 5212
61. H.L. Cash, C.V. Whitham, C.L. Behrendt, and L.V. Hooper Symbiotic bacteria direct expression of an intestinal bactericidal lectin Science 313 2006 1126 1130
62. K. Brandl Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits Nature 455 2008 804 807
63. L.D. McVay Absence of bacterially induced RELMbeta reduces injury in the dextran sodium sulfate model of colitis J. Clin. Invest. 116 2006 2914 2923
64. S.L. Barnes, A. Vidrich, M.L. Wang, G.D. Wu, F. Cominelli, J. Rivera-Nieves, G. Bamias, and S.M. Cohn Resistin-like molecule beta (RELMbeta/FIZZ2) is highly expressed in the ileum of SAMP1/YitFc mice and is associated with initiation of ileitis J. Immunol. 179 2007 7012 7020
65. D.R. Herbert Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection J. Exp. Med. 206 2009 2947 2957
66. W. He Bacterial colonization leads to the colonic secretion of RELMbeta/FIZZ2, a novel goblet cell-specific protein Gastroenterology 125 2003 1388 1397
67. M.G. Nair Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFN-gamma and infection-induced intestinal inflammation J. Immunol. 181 2008 4709 4715
68. M.A. Hildebrandt High-fat diet determines the composition of the murine gut microbiome independently of obesity Gastroenterology 137 2009 1716 1724 e1-e2
69. E.C. Martens Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts PLoS Biol. 9 2011 e1001221
70. A.R. Pacheco, M.M. Curtis, J.M. Ritchie, D. Munera, M.K. Waldor, C.G. Moreira, and V. Sperandio Fucose sensing regulates bacterial intestinal colonization Nature 492 2012 113 117
71. K.M. Ng Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens Nature 502 2013 96 99
72. M.J. Coyne, B. Reinap, M.M. Lee, and L.E. Comstock Human symbionts use a host-like pathway for surface fucosylation Science 307 2005 1778 1781
73. L. Lindesmith Human susceptibility and resistance to Norwalk virus infection Nat. Med. 9 2003 548 553
74. G.M. Ruiz-Palacios, L.E. Cervantes, P. Ramos, B. Chavez-Munguia, and D.S. Newburg Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection J. Biol. Chem. 278 2003 14112 14120
75. L. Bry, P.G. Falk, T. Midtvedt, and J.I. Gordon A model of host-microbial interactions in an open mammalian ecosystem Science 273 1996 1380 1383
76. L.V. Hooper, J. Xu, P.G. Falk, T. Midtvedt, and J.I. Gordon A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem Proc. Natl. Acad. Sci. USA 96 1999 9833 9838
77. P.C. Kashyap Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota Proc. Natl. Acad. Sci. USA 110 2013 17059 17064
78. P. Rausch Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype Proc. Natl. Acad. Sci. USA 108 2011 19030 19035
79. P. Wacklin Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine PLoS ONE 6 2011 e20113
80. T. Folseraas Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci J. Hepatol. 57 2012 366 375
81. D.P. McGovern Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease Hum. Mol. Genet. 19 2010 3468 3476
82. D. Ellinghaus Combined analysis of genome-wide association studies for Crohn disease and psoriasis identifies seven shared susceptibility loci Am. J. Hum. Genet. 90 2012 636 647
83. D.J. Smyth FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection Diabetes 60 2011 3081 3084
84. A. Fuhrer, N. Sprenger, E. Kurakevich, L. Borsig, C. Chassard, and T. Hennet Milk sialyllactose influences colitis in mice through selective intestinal bacterial colonization J. Exp. Med. 207 2010 2843 2854
85. C. Zhang Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice ISME J. 4 2010 232 241
86. J. Fu Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice J. Clin. Invest. 121 2011 1657 1666
87. E.L. Stone Glycosyltransferase function in core 2-type protein O glycosylation Mol. Cell. Biol. 29 2009 3770 3782
88. G. An, B. Wei, B. Xia, J.M. McDaniel, T. Ju, R.D. Cummings, J. Braun, and L. Xia Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans J. Exp. Med. 204 2007 1417 1429
89. G.F. Sonnenberg, and D. Artis Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease Immunity 37 2012 601 610
90. S. Sawa RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota Nat. Immunol. 12 2011 320 326
91. Y. Zheng Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens Nat. Med. 14 2008 282 289
92. G.F. Sonnenberg Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria Science 336 2012 1321 1325
93. S.L. Sanos, C. Vonarbourg, A. Mortha, and A. Diefenbach Control of epithelial cell function by interleukin-22-producing RORgammat+ innate lymphoid cells Immunology 132 2011 453 465
94. M.A. Kinnebrew Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense Immunity 36 2012 276 287
95. J. Qiu, X. Guo, Z.M. Chen, L. He, G.F. Sonnenberg, D. Artis, Y.X. Fu, and L. Zhou Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora Immunity 39 2013 386 399
96. C.S. Klose A T-bet gradient controls the fate and function of CCR6(-)RORgammat(+) innate lymphoid cells Nature 494 2013 261 265
97. W.S. Garrett, G.M. Lord, S. Punit, G. Lugo-Villarino, S.K. Mazmanian, S. Ito, J.N. Glickman, and L.H. Glimcher Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system Cell 131 2007 33 45
98. N. Powell The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells Immunity 37 2012 674 684
99. W.S. Garrett Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis Cell Host Microbe 8 2010 292 300
100. S. Buonocore, P.P. Ahern, H.H. Uhlig, I.I. Ivanov, D.R. Littman, K.J. Maloy, and F. Powrie Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology Nature 464 2010 1371 1375
101. N.E. Welty, C. Staley, N. Ghilardi, M.J. Sadowsky, B.Z. Igyarto, and D.H. Kaplan Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism J. Exp. Med. 210 2013 2011 2024
102. S. Fagarasan, S. Kawamoto, O. Kanagawa, and K. Suzuki Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis Annu. Rev. Immunol. 28 2010 243 273
103. M. Tsuji Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut Immunity 29 2008 261 271
104. J. Hansson Influence of gut microbiota on mouse B2 B cell ontogeny and function Mol. Immunol. 48 2011 1091 1101
105. S. Hapfelmeier Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses Science 328 2010 1705 1709
106. N. Shulzhenko Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut Nat. Med. 17 2011 1585 1593
107. S. Fagarasan, M. Muramatsu, K. Suzuki, H. Nagaoka, H. Hiai, and T. Honjo Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora Science 298 2002 1424 1427
108. K. Suzuki, B. Meek, Y. Doi, M. Muramatsu, T. Chiba, T. Honjo, and S. Fagarasan Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut Proc. Natl. Acad. Sci. USA 101 2004 1981 1986
109. M. Wei, R. Shinkura, Y. Doi, M. Maruya, S. Fagarasan, and T. Honjo Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense Nat. Immunol. 12 2011 264 270
110. J.H. Fritz Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut Nature 481 2012 199 203
111. L.M. Kato, S. Kawamoto, M. Maruya, and S. Fagarasan Gut T and IgA: key players for regulation of bacterial communities and immune homeostasis Immunol. Cell Biol. 92 2013 49 56
112. H. Nishimura, M. Nose, H. Hiai, N. Minato, and T. Honjo Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor Immunity 11 1999 141 151
113. H. Nishimura Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice Science 291 2001 319 322
114. M. Maruya, S. Kawamoto, L.M. Kato, and S. Fagarasan Impaired selection of IgA and intestinal dysbiosis associated with PD-1-deficiency Gut Microbes 4 2013 165 171
115. S. Kawamoto, T.H. Tran, M. Maruya, K. Suzuki, Y. Doi, Y. Tsutsui, L.M. Kato, and S. Fagarasan The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut Science 336 2012 485 489
116. S.Z. Josefowicz, R.E. Niec, H.Y. Kim, P. Treuting, T. Chinen, Y. Zheng, D.T. Umetsu, and A.Y. Rudensky Extrathymically generated regulatory T cells control mucosal TH2 inflammation Nature 482 2012 395 399
117. P.J. Brennan, M. Brigl, and M.B. Brenner Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions Nat. Rev. Immunol. 13 2013 101 117
118. T. Olszak Microbial exposure during early life has persistent effects on natural killer T cell function Science 336 2012 489 493
119. G. Wingender Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice Gastroenterology 143 2012 418 428
120. B. Wei Commensal microbiota and CD8+ T cells shape the formation of invariant NKT cells J. Immunol. 184 2010 1218 1226
121. E. Tupin, Y. Kinjo, and M. Kronenberg The unique role of natural killer T cells in the response to microorganisms Nat. Rev. Microbiol. 5 2007 405 417
122. E.E. Nieuwenhuis Cd1d-dependent regulation of bacterial colonization in the intestine of mice J. Clin. Invest. 119 2009 1241 1250
123. H. Cheroutre, F. Lambolez, and D. Mucida The light and dark sides of intestinal intraepithelial lymphocytes Nat. Rev. Immunol. 11 2011 445 456
124. A.S. Ismail, C.L. Behrendt, and L.V. Hooper Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury J. Immunol. 182 2009 3047 3054
125. A.S. Ismail Gammadelta intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface Proc. Natl. Acad. Sci. USA 108 2011 8743 8748
126. J.H. Campbell Host genetic and environmental effects on mouse intestinal microbiota ISME J. 6 2012 2033 2044
127. A.K. Benson Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors Proc. Natl. Acad. Sci. USA 107 2010 18933 18938
128. A.M. McKnite Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits PLoS ONE 7 2012 e39191
129. B.W. Parks Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice Cell Metab. 17 2013 141 152
130. J.A. Stewart, V.S. Chadwick, and A. Murray Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children J. Med. Microbiol. 54 2005 1239 1242
131. P.J. Turnbaugh A core gut microbiome in obese and lean twins Nature 457 2009 480 484
132. T. Yatsunenko Human gut microbiome viewed across age and geography Nature 486 2012 222 227
133. P. Lepage Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis Gastroenterology 141 2011 227 236
134. S. Tims, C. Derom, D.M. Jonkers, R. Vlietinck, W.H. Saris, M. Kleerebezem, W.M. de Vos, and E.G. Zoetendal Microbiota conservation and BMI signatures in adult monozygotic twins ISME J. 7 2013 707 717
135. C. Quince The impact of Crohn's disease genes on healthy human gut microbiota: a pilot study Gut 62 2013 952 954
136. J.C. Barrett Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease Nat. Genet. 40 2008 955 962
137. V. Deretic, T. Saitoh, and S. Akira Autophagy in infection, inflammation and immunity Nat. Rev. Immunol. 13 2013 722 737
138. P. Brest A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease Nat. Genet. 43 2011 242 245
139. B.R. Dorn, K.L. Leung, and A. Progulske-Fox Invasion of human oral epithelial cells by Prevotella intermedia Infect. Immun. 66 1998 6054 6057
140. L. Strombeck, J. Sandros, E. Holst, P. Madianos, U. Nannmark, P. Papapanou, and I. Mattsby-Baltzer Prevotella bivia can invade human cervix epithelial (HeLa) cells APMIS 115 2007 241 251
141. R.S. Veazey, and A.A. Lackner HIV swiftly guts the immune system Nat. Med. 11 2005 469 470
142. C.T. Costiniuk, and J.B. Angel Human immunodeficiency virus and the gastrointestinal immune system: does highly active antiretroviral therapy restore gut immunity? Mucosal Immunol. 5 2012 596 604
143. N.G. Sandler, and D.C. Douek Microbial translocation in HIV infection: causes, consequences and treatment opportunities Nat. Rev. Microbiol. 10 2012 655 666
144. S. Mehandru Lack of mucosal immune reconstitution during prolonged treatment of acute and early HIV-1 infection PLoS Med. 3 2006 e484
145. A.H. Moeller SIV-induced instability of the chimpanzee gut microbiome Cell Host Microbe 14 2013 340 345
146. I. Vujkovic-Cvijin Dysbiosis of the gut microbiota is associated with hiv disease progression and tryptophan catabolism Sci. Transl. Med. 5 2013 193ra91
147. C.A. Lozupone Alterations in the gut microbiota associated with HIV-1 infection Cell Host Microbe 14 2013 329 339
148. I.H. McHardy HIV Infection is associated with compositional and functional shifts in the rectal mucosal microbiota Microbiome 1 2013 26
149. M. Castellarin Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma Genome Res. 22 2012 299 306
150. P.I. Diaz Transplantation-associated long-term immunosuppression promotes oral colonization by potentially opportunistic pathogens without impacting other members of the salivary bacteriome Clin. Vaccine Immunol. 20 2013 920 930