The microbiota, the immune system and the allograft

American Journal of Transplantation

Volumn 14, Issue 6, 2014, Pages 1236-1248

  Alegre, M L ^a   Mannon, R B ^b   Mannon, P J ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Acute rejection; alloimmunity; chronic rejection; microbiota; pattern recognition receptor

Indexed keywords

IMMUNOSUPPRESSIVE AGENT;

ALLOGRAFT; CELL DIFFERENTIATION; DISEASE PREDISPOSITION; DYSBIOSIS; ENVIRONMENTAL EXPOSURE; GRAFT RECIPIENT; HOMEOSTASIS; HUMAN; IMMUNE DYSREGULATION; IMMUNE SYSTEM; IMMUNOMODULATION; INFLAMMATION; INTESTINE FLORA; METABOLOME; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; TRANSPLANTATION; AUTOTRANSPLANTATION; IMMUNOLOGY;

HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; MICROBIOTA; TRANSPLANTATION, AUTOLOGOUS;

EID: 84901358255     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12760     Document Type: Review

References (116)

1. Charlson ES, Bittinger K, Haas AR, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011; 184: 957-963.
2. Tremaroli V, Backhed F., Functional interactions between the gut microbiota and host metabolism. Nature 2012; 489: 242-249.
3. Weinstock GM., Genomic approaches to studying the human microbiota. Nature 2012; 489: 250-256.
4. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207-214.
5. Segata N, Haake SK, Mannon P, et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 2012; 13: R42.
6. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-180.
7. Koren O, Knights D, Gonzalez A, et al. A guide to enterotypes across the human body: Meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 2013; 9: e1002863.
8. Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 2011; 108 (Suppl 1): 4578-4585.
9. Sekirov I, Russell SL, Antunes LC, Finlay BB., Gut microbiota in health and disease. Physiol Rev 2010; 90: 859-904.
10. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP., Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2010; 2: 53-66.
11. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO., Development of the human infant intestinal microbiota. PLoS Biol 2007; 5: e177.
12. Faith JJ, Guruge JL, Charbonneau M, et al. The long-term stability of the human gut microbiota. Science 2013; 341: 1237439.
13. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R., Bacterial community variation in human body habitats across space and time. Science 2009; 326: 1694-1697.
14. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-484.
15. Bager P, Wohlfahrt J, Westergaard T., Caesarean delivery and risk of atopy and allergic disease: Meta-analyses. Clin Exp Allergy 2008; 38: 634-642. (Pubitemid 351406069)
16. Russell SL, Gold MJ, Willing BP, Thorson L, McNagny KM, Finlay BB., Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes 2013; 4: 158-164.
17. Joossens M, Huys G, Cnockaert M, et al. Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives. Gut 2011; 60: 631-637.
18. Knights D, Lassen KG, Xavier RJ., Advances in inflammatory bowel disease pathogenesis: Linking host genetics and the microbiome. Gut 2013; 62: 1505-1510.
19. Mondot S, Kang S, Furet JP, et al. Highlighting new phylogenetic specificities of Crohn's disease microbiota. Inflamm Bowel Dis 2011; 17: 185-192.
20. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13: R79.
21. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008; 105: 16731-16736.
22. Zhao L., The gut microbiota and obesity: From correlation to causality. Nat Rev Microbiol 2013; 11: 639-647.
23. Karlsson F, Tremaroli V, Nielsen J, Backhed F., Assessing the human gut microbiota in metabolic diseases. Diabetes 2013; 62: 3341-3349.
24. Ridaura V., Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013; 341: 1241214.
25. Smith MI, Yatsunenko T, Manary MJ, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013; 339: 548-554.
26. Yurkovetskiy L, Burrows M, Khan AA, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity 2013; 39: 400-412.
27. Round JL, Lee SM,., Li J, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011; 332: 974-977.
28. Wang Y, Kasper LH., The role of microbiome in central nervous system disorders. Brain Behav Immun 2014; 38C: 1-12.
29. Bultman SJ., Emerging roles of the microbiome in cancer. Carcinogenesis 2014; 35: 249-255.
30. Ussher JR, Lopaschuk GD, Arduini A., Gut microbiota metabolism of L-carnitine and cardiovascular risk. Atherosclerosis 2013; 231: 456-461.
31. Sanford JA, Gallo RL., Functions of the skin microbiota in health and disease. Semin Immunol 2013; 25: 370-377.
32. Bouskra D, Brezillon C, Berard M, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008; 456: 507-510. (Pubitemid 352759006)
33. Pabst O., New concepts in the generation and functions of IgA. Nat Rev Immunol 2012; 12: 821-832.
34. Kawamoto S, Tran TH, Maruya M, et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 2012; 336: 485-489.
35. Kirkland D, Benson A, Mirpuri J, et al. B cell-intrinsic MyD88 signaling prevents the lethal dissemination of commensal bacteria during colonic damage. Immunity 2012; 36: 228-238.
36. Wen L, Ley RE, Volchkov PY., AC et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008; 455: 1109-1113.
37. Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145: 745-757.
38. Henao-Mejia J, Elinav E, Jin C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-185.
39. Garrett WS, Gallini CA, Yatsunenko T, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010; 8: 292-300.
40. Upadhyay V, Poroyko V, Kim TJ, et al. Lymphotoxin regulates commensal responses to enable diet-induced obesity. Nat Immunol 2012; 13: 947-953.
41. Ubeda C, Lipuma L, Gobourne A, et al. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J Exp Med 2012; 209: 1445-1456.
42. Spits H, Artis D, Colonna M, et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat Rev Immunol 2013; 13: 145-149.
43. Sonnenberg GF, Monticelli LA, Alenghat T, et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012; 336: 1321-1325.
44. Hepworth MR, Monticelli LA, Fung TC, et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013; 498: 113-117.
45. Rook GA, Hygiene hypothesis, autoimmune diseases., Clin Rev Allergy Immunol 2012; 42: 5-15.
46. Brown EM, Arrieta MC, Finlay BB., A fresh look at the hygiene hypothesis: How intestinal microbial exposure drives immune effector responses in atopic disease. Semin Immunol 2013; 25: 378-387.
47. Kawai T, Akira S., Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011; 34: 637-650.
48. Alegre ML, Leemans J, Le Moine A, et al. The multiple facets of Toll-like receptors in transplantation biology. Transplantation 2008; 86: 1-9.
49. Mukherji A, Kobiita A, Ye T, Chambon P., Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 2013; 153: 812-827.
50. Brandtzaeg P., Secretory IgA: Designed for anti-microbial defense. Front Immunol 2013; 4: 222.
51. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009; 31: 677-689.
52. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139: 485-498.
53. Lau K, Benitez P, Ardissone A, et al. Inhibition of type 1 diabetes correlated to a Lactobacillus johnsonii N6.2-mediated Th17 bias. J Immunol 2011; 186: 3538-3546.
54. Geuking MB, Cahenzli J, Lawson MA, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 2011; 34: 794-806.
55. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337-341.
56. Atarashi K, Tanoue T, Oshima K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500: 232-236.
57. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL., An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122: 107-118. (Pubitemid 40977944)
58. Mazmanian SK, Round JL, Kasper DL., A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008; 453: 620-625. (Pubitemid 351769307)
59. Round JL, Mazmanian SK., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 2010; 107: 12204-12209.
60. Han D, Walsh MC, Cejas PJ, et al. Dendritic cell expression of the signaling molecule TRAF6 is critical for gut microbiota-dependent immune tolerance. Immunity 2013; 38: 1211-1222.
61. Josefowicz SZ, Niec RE, Kim HY, et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 2012; 482: 395-399.
62. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341: 569-573.
63. Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504: 451-455.
64. Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504: 446-450.
65. Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009; 461: 1282-1286.
66. Lathrop SK, Bloom SM, Rao SM, et al. Peripheral education of the immune system by colonic commensal microbiota. Nature 2011; 478: 250-254.
67. Cebula A, Seweryn M, Rempala GA, et al. Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 2013; 497: 258-262.
68. Alegre ML, Chen L, Wang T, Ahmed E, Wang CR, Chong A., Antagonistic effect of toll-like receptor signaling and bacterial infections on transplantation tolerance. Transplantation 2009; 87 (9 Suppl): S77-S79.
69. Porrett PM, Yuan X, LaRosa DF, et al. Mechanisms underlying blockade of allograft acceptance by TLR ligands. J Immunol 2008; 181: 1692-1699.
70. Gras S, Kjer-Nielsen L, Chen Z, Rossjohn J, McCluskey J., The structural bases of direct T-cell allorecognition: Implications for T-cell-mediated transplant rejection. Immunol Cell Biol 2011; 89: 388-395.
71. Kuhn KA, Stappenbeck TS., Peripheral education of the immune system by the colonic microbiota. Semin Immunol 2013; 25: 364-369.
72. Wu HJ, Ivanov II, Darce J, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32: 815-827.
73. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK., Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2011; 108 (Suppl 1): 4615-4622.
74. Chappert P, Bouladoux N, Naik S, Schwartz RH., Specific gut commensal flora locally alters T cell tuning to endogenous ligands. Immunity 2013; 38: 1198-1210.
75. Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013; 2: e01202.
76. Kim SV, Xiang WV, Kwak C, et al. GPR15-mediated homing controls immune homeostasis in the large intestine mucosa. Science 2013; 340: 1456-1459.
77. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN., Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 2010; 16: 228-231.
78. Ganal SC, Sanos SL, Kallfass C, et al. Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 2012; 37: 171-186.
79. Abt MC, Osborne LC, Monticelli LA, et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 2012; 37: 158-170.
80. 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 USA 2011; 108: 11548-11553.
81. Hand TW, Dos Santos LM, Bouladoux N, et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 2012; 337: 1553-1556.
82. Adams AB, Pearson TC, Larsen CP., Heterologous immunity: An overlooked barrier to tolerance. Immunol Rev 2003; 196: 147-160. (Pubitemid 37468109)
83. Naik S, Bouladoux N, Wilhelm C, et al. Compartmentalized control of skin immunity by resident commensals. Science 2012; 337: 1115-1119.
84. Grice EA, Segre JA., The skin microbiome. Nat Rev Microbiol 2011; 9: 244-253.
85. Findley K, Oh J, Yang J, et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 2013; 498: 367-370.
86. Yoshitomi H, Sakaguchi N, Kobayashi K, et al. A role for fungal {beta}-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005; 201: 949-960. (Pubitemid 40524464)
87. Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD., Intestinal Microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 2013; 14: 559-570.
88. Duerkop BA, Hooper LV., Resident viruses and their interactions with the immune system. Nat Immunol 2013; 14: 654-659.
89. Reyes A, Haynes M, Hanson N, et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010; 466: 334-338.
90. Kuss SK, Best GT, Etheredge CA, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 2011; 334: 249-252.
91. Kane M, Case LK, Kopaskie K, et al. Successful transmission of a retrovirus depends on the commensal microbiota. Science 2011; 334: 245-249.
92. Young GR, Eksmond U, Salcedo R, Alexopoulou L, Stoye JP, Kassiotis G., Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 2012; 491: 774-778.
93. Goldstein DR, Tesar BM, Akira S, Lakkis FG., Critical role of the Toll-like receptor signal adaptor protein MyD88 in acute allograft rejection. J Clin Invest 2003; 111: 1571-1578. (Pubitemid 38063290)
94. Shen H, Song Y, Colangelo CM, et al. Haptoglobin activates innate immunity to enhance acute transplant rejection in mice. J Clin Invest 2012; 122: 383-387.
95. Eriguchi Y, Takashima S, Oka H, et al. Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of alpha-defensins. Blood 2012; 120: 223-231.
96. Jenq RR, Ubeda C, Taur Y, et al. Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. J Exp Med 2012; 209: 903-911.
97. Tawara I, Liu C, Tamaki H, et al. Influence of donor microbiota on the severity of experimental graft-versus-host-disease. Biol Blood Marrow Transplant 2013; 19: 164-168.
98. Corbitt N, Kimura S, Isse K, et al. Gut bacteria drive Kupffer cell expansion via MAMP-mediated ICAM-1 induction on sinusoidal endothelium and influence preservation-reperfusion injury after orthotopic liver transplantation. Am J Path 2013; 182: 180-191.
99. Li QR, Wang CY, Tang C., He Q, Li N, Li JS. Reciprocal interaction between intestinal microbiota and mucosal lymphocyte in cynomolgus monkeys after alemtuzumab treatment. Am J Transplant 2013; 13: 899-910.
100. Fricke WF, Maddox C, Song Y, Bromberg JS., Human microbiota characterization in the course of renal transplantation. Am J Transplant 2014; 14: 416-427.
101. Lu H, He J, Wu Z, et al. Assessment of microbiome variation during the perioperative period in liver transplant patients: A retrospective analysis. Microb Ecol 2013; 65: 781-791.
102. Wu ZW, Ling ZX, Lu HF, et al. Changes of gut bacteria and immune parameters in liver transplant recipients. Hepatobiliary Pancreat Dis Int 2012; 11: 40-50.
103. Oh PL, Martinez I, Sun Y, Walter J, Peterson DA, Mercer DF., Characterization of the ileal microbiota in rejecting and nonrejecting recipients of small bowel transplants. Am J Transplant 2012; 12: 753-762.
104. Charlson ES, Diamond JM, Bittinger K, et al. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med 2012; 186: 536-545.
105. Borewicz K, Pragman AA, Kim HB, Hertz M, Wendt C, Isaacson RE., Longitudinal analysis of the lung microbiome in lung transplantation. FEMS Microbiol Lett 2013; 339: 57-65.
106. Willner DL, Hugenholtz P, Yerkovich ST, et al. Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2013; 187: 640-647.
107. Dethlefsen L, Relman DA., Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA 2011; 108(Suppl 1): 4554-4561.
108. Jakobsson HE, Jernberg C, Andersson AF, Sjolund-Karlsson M, Jansson JK, Engstrand L., Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PloS One 2010; 5: e9836.
109. Jernberg C, Lofmark S, Edlund C, Jansson JK., Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 2010; 156: 3216-3223.
110. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2013; 505: 559-563.
111. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-108.
112. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010; 107: 14691-14696.
113. Viaud S, Saccheri F, Mignot G, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013; 342: 971-976.
114. Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013; 342: 967-970.
115. Haiser HJ, Gootenberg DB, Chatman K, Sirasani G, Balskus EP, Turnbaugh PJ., Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 2013; 341: 295-298.
116. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013; 368: 407-415.