Microbiota-Dependent Sequelae of Acute Infection Compromise Tissue-Specific Immunity

Cell

Volumn 163, Issue 2, 2015, Pages 354-366

  Fonseca, Denise Morais Da ^a,b   Hand, Timothy W ^a   Han, Seong Ji ^a   Gerner, Michael Y ^a   Zaretsky, Arielle Glatman ^a   Byrd, Allyson L ^a,c,d   Harrison, Oliver J ^a   Ortiz, Alexandra M ^a   Quinones, Mariam ^a   Trinchieri, Giorgio ^e   Brenchley, Jason M ^a   Brodsky, Igor E ^f   Germain, Ronald N ^a   Randolph, Gwendalyn J ^g   Belkaid, Yasmine ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d BOSTON UNIVERSITY   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; CONTROLLED STUDY; DENDRITIC CELL; HISTOCOMPATIBILITY; HOMEOSTASIS; IMMUNOLOGICAL TOLERANCE; INFECTION; INFLAMMATION; MESENTERIC FAT; MESENTERIC LYMPHADENITIS; MESENTERY LYMPH NODE; MICROFLORA; MOUSE; MOUTH INFECTION; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TISSUES; YERSINIA PSEUDOTUBERCULOSIS; CELL MOTION; CHRONIC DISEASE; FEMALE; GERMFREE ANIMAL; HUMAN; IMMUNOLOGY; IMMUNOPATHOLOGY; INTESTINE FLORA; LYMPHATIC SYSTEM DISEASE; LYMPHOID TISSUE; MALE; MESENTERY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; YERSINIA PSEUDOTUBERCULOSIS INFECTION;

CELL MOVEMENT; CHRONIC DISEASE; DENDRITIC CELLS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNE SYSTEM DISEASES; LYMPHATIC DISEASES; LYMPHOID TISSUE; MALE; MESENTERY; SPECIFIC PATHOGEN-FREE ORGANISMS; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 84943653785     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.08.030     Document Type: Article

References (72)

1. M.B. Aldrich, and E.M. Sevick-Muraca Cytokines are systemic effectors of lymphatic function in acute inflammation Cytokine 64 2013 362 369
2. S. Asano Granulomatous lymphadenitis J. Clin. Exp. Hematop. 52 2012 1 16
3. E.S. Barton, D.W. White, J.S. Cathelyn, K.A. Brett-McClellan, M. Engle, M.S. Diamond, V.L. Miller, and H.W. Virgin 4th Herpesvirus latency confers symbiotic protection from bacterial infection Nature 447 2007 326 329
4. M.A. Behr The path to Crohn's disease: is mucosal pathology a secondary event? Inflamm. Bowel Dis. 16 2010 896 902
5. V. Bekiaris, E.K. Persson, and W.W. Agace Intestinal dendritic cells in the regulation of mucosal immunity Immunol. Rev. 260 2014 86 101
6. Y. Belkaid, and T.W. Hand Role of the microbiota in immunity and inflammation Cell 157 2014 121 141
7. Y. Belkaid, and J.A. Segre Dialogue between skin microbiota and immunity Science 346 2014 954 959
8. M.A. Bergman, W.P. Loomis, J. Mecsas, M.N. Starnbach, and R.R. Isberg CD8(+) T cells restrict Yersinia pseudotuberculosis infection: bypass of anti-phagocytosis by targeting antigen-presenting cells PLoS Pathog. 5 2009 e1000573
9. T. Bergsbaken, and M.J. Bevan Proinflammatory microenvironments within the intestine regulate the differentiation of tissue-resident CD8 T cells responding to infection Nat Immunol 2015
10. M.J. Blaser, and S. Falkow What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7 2009 887 894
11. M. Bogunovic, F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M.A. Ingersoll, M. Leboeuf, and et al. Origin of the lamina propria dendritic cell network Immunity 31 2009 513 525
12. E.N. Bou Ghanem, G.S. Jones, T. Myers-Morales, P.D. Patil, A.N. Hidayatullah, and S.E. D'Orazio InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice PLoS Pathog. 8 2012 e1003015
13. C.G. Buffie, and E.G. Pamer Microbiota-mediated colonization resistance against intestinal pathogens Nat. Rev. Immunol. 13 2013 790 801
14. K. Cadwell, K.K. Patel, N.S. Maloney, T.C. Liu, A.C. Ng, C.E. Storer, R.D. Head, R. Xavier, T.S. Stappenbeck, and H.W. Virgin Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine Cell 141 2010 1135 1145
15. J.L. Coombes, K.R. Siddiqui, C.V. Arancibia-Carcamo, J. Hall, C.M. Sun, Y. Belkaid, and F. Powrie A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-{beta}- and retinoic acid-dependent mechanism J Exp Med 2007
16. W.E. Cromer, S.D. Zawieja, B. Tharakan, E.W. Childs, M.K. Newell, and D.C. Zawieja The effects of inflammatory cytokines on lymphatic endothelial barrier function Angiogenesis 17 2014 395 406
17. M.A. Curotto de Lafaille, N. Kutchukhidze, S. Shen, Y. Ding, H. Yee, and J.J. Lafaille Adaptive Foxp3+ regulatory T cell-dependent and -independent control of allergic inflammation Immunity 29 2008 114 126
18. R.W. DePaolo, V. Abadie, F. Tang, H. Fehlner-Peach, J.A. Hall, W. Wang, E.V. Marietta, D.D. Kasarda, T.A. Waldmann, J.A. Murray, and et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens Nature 471 2011 220 224
19. G.E. Diehl, R.S. Longman, J.X. Zhang, B. Breart, C. Galan, A. Cuesta, S.R. Schwab, and D.R. Littman Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells Nature 494 2013 116 120
20. J. Estes, J.V. Baker, J.M. Brenchley, A. Khoruts, J.L. Barthold, A. Bantle, C.S. Reilly, G.J. Beilman, M.E. George, D.C. Douek, and et al. Collagen deposition limits immune reconstitution in the gut J. Infect. Dis. 198 2008 456 464
21. A. Fahlgren, K. Avican, L. Westermark, R. Nordfelth, and M. Fällman Colonization of cecum is important for development of persistent infection by Yersinia pseudotuberculosis Infect. Immun. 82 2014 3471 3482
22. J. Farache, I. Koren, I. Milo, I. Gurevich, K.W. Kim, E. Zigmond, G.C. Furtado, S.A. Lira, and G. Shakhar Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation Immunity 38 2013 581 595
23. A.M. Fendrick, A.S. Monto, B. Nightengale, and M. Sarnes The economic burden of non-influenza-related viral respiratory tract infection in the United States Arch. Intern. Med. 163 2003 487 494
24. W.C. Gause, T.A. Wynn, and J.E. Allen Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths Nat. Rev. Immunol. 13 2013 607 614
25. M. Gaya, A. Castello, B. Montaner, N. Rogers, C. Reis e Sousa, A. Bruckbauer, and F.D. Batista Host response. Inflammation-induced disruption of SCS macrophages impairs B cell responses to secondary infection Science 347 2015 667 672
26. M.Y. Gerner, W. Kastenmuller, I. Ifrim, J. Kabat, and R.N. Germain Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes Immunity 37 2012 364 376
27. J.R. Grainger, M.H. Askenase, F. Guimont-Desrochers, D.M. da Fonseca, and Y. Belkaid Contextual functions of antigen-presenting cells in the gastrointestinal tract Immunol. Rev. 259 2014 75 87
28. U. Hadis, B. Wahl, O. Schulz, M. Hardtke-Wolenski, A. Schippers, N. Wagner, W. Müller, T. Sparwasser, R. Förster, and O. Pabst Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria Immunity 34 2011 237 246
29. J.A. Hall, N. Bouladoux, C.M. Sun, E.A. Wohlfert, R.B. Blank, Q. Zhu, M.E. Grigg, J.A. Berzofsky, and Y. Belkaid Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses Immunity 29 2008 637 649
30. T.W. Hand, L.M. Dos Santos, N. Bouladoux, M.J. Molloy, A.J. Pagán, M. Pepper, C.L. Maynard, C.O. Elson 3rd, and Y. Belkaid Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses Science 337 2012 1553 1556
31. L.V. Hooper, and A.J. Macpherson Immune adaptations that maintain homeostasis with the intestinal microbiota Nat. Rev. Immunol. 10 2010 159 169
32. B.J. Huppert, M.A. Farrell, A. Kawashima, and J.A. Murray Diagnosis of cavitating mesenteric lymph node syndrome in celiac disease using MRI AJR Am. J. Roentgenol. 183 2004 1375 1377
33. A.M. Jamieson, L. Pasman, S. Yu, P. Gamradt, R.J. Homer, T. Decker, and R. Medzhitov Role of tissue protection in lethal respiratory viral-bacterial coinfection Science 340 2013 1230 1234
34. C.J. Johnston, H.J. McSorley, S.M. Anderton, S.J. Wigmore, and R.M. Maizels Helminths and immunological tolerance Transplantation 97 2014 127 132
35. T. Katakai, T. Hara, M. Sugai, H. Gonda, and A. Shimizu Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes J. Exp. Med. 200 2004 783 795
36. A. Khalifeh-Soltani, W. McKleroy, S. Sakuma, Y.Y. Cheung, K. Tharp, Y. Qiu, S.M. Turner, A. Chawla, A. Stahl, and K. Atabai Mfge8 promotes obesity by mediating the uptake of dietary fats and serum fatty acids Nat. Med. 20 2014 175 183
37. A. Kissenpfennig, S. Henri, B. Dubois, C. Laplace-Builhé, P. Perrin, N. Romani, C.H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, and et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells Immunity 22 2005 643 654
38. P.S. Korpe, and W.A. Petri Jr. Environmental enteropathy: critical implications of a poorly understood condition Trends Mol. Med. 18 2012 328 336
39. M. Kosek, C. Bern, and R.L. Guerrant The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000 Bull. World Health Organ. 81 2003 197 204
40. E.L. Kuan, S. Ivanov, E.A. Bridenbaugh, G. Victora, W. Wang, E.W. Childs, A.M. Platt, C.V. Jakubzick, R.J. Mason, A.A. Gashev, and et al. Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node-homing adipose tissue dendritic cells J. Immunol. 194 2015 5200 5210
41. M.M. Levine Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine BMC Biol. 8 2010 129
42. J. Lindenbaum, J.W. Harmon, and C.D. Gerson Subclinical malabsorption in developing countries Am. J. Clin. Nutr. 25 1972 1056 1061
43. B.C. Lucey, J.W. Stuhlfaut, and J.A. Soto Mesenteric lymph nodes seen at imaging: causes and significance Radiographics 25 2005 351 365
44. K.J. Maloy, and F. Powrie Intestinal homeostasis and its breakdown in inflammatory bowel disease Nature 474 2011 298 306
45. J.B. McPhee, P. Mena, Y. Zhang, and J.B. Bliska Interleukin-10 induction is an important virulence function of the Yersinia pseudotuberculosis type III effector YopM Infect. Immun. 80 2012 2519 2527
46. M. Merad, P. Sathe, J. Helft, J. Miller, and A. Mortha The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting Annu. Rev. Immunol. 31 2013 563 604
47. N.A. Molodecky, I.S. Soon, D.M. Rabi, W.A. Ghali, M. Ferris, G. Chernoff, E.I. Benchimol, R. Panaccione, S. Ghosh, H.W. Barkema, and et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review Gastroenterology 142 2012 46 54 e42; quiz e30
48. A.M. Mowat, and W.W. Agace Regional specialization within the intestinal immune system Nat. Rev. Immunol. 14 2014 667 685
49. S.N. Mueller, M. Matloubian, D.M. Clemens, A.H. Sharpe, G.J. Freeman, S. Gangappa, C.P. Larsen, and R. Ahmed Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection Proc. Natl. Acad. Sci. USA 104 2007 15430 15435
50. G. Oldenhove, N. Bouladoux, E.A. Wohlfert, J.A. Hall, D. Chou, L. Dos Santos, S. O'Brien, R. Blank, E. Lamb, S. Natarajan, and et al. Decrease of Foxp3(+) Treg Cell Number and Acquisition of Effector Cell Phenotype during Lethal Infection Immunity 2009
51. L.C. Osborne, L.A. Monticelli, T.J. Nice, T.E. Sutherland, M.C. Siracusa, M.R. Hepworth, V.T. Tomov, D. Kobuley, S.V. Tran, K. Bittinger, and et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation Science 345 2014 578 582
52. L. Peyrin-Biroulet, F. Gonzalez, L. Dubuquoy, C. Rousseaux, C. Dubuquoy, C. Decourcelle, A. Saudemont, M. Tachon, E. Béclin, M.F. Odou, and et al. Mesenteric fat as a source of C reactive protein and as a target for bacterial translocation in Crohn's disease Gut 61 2012 78 85
53. G.J. Randolph, and N.E. Miller Lymphatic transport of high-density lipoproteins and chylomicrons J. Clin. Invest. 124 2014 929 935
54. P. Salgame, G.S. Yap, and W.C. Gause Effect of helminth-induced immunity on infections with microbial pathogens Nat. Immunol. 14 2013 1118 1126
55. A.T. Satpathy, C.G. Briseño, J.S. Lee, D. Ng, N.A. Manieri, W. Kc, X. Wu, S.R. Thomas, W.L. Lee, M. Turkoz, and et al. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens Nat. Immunol. 14 2013 937 948
56. J.P. Scallan, M.J. Davis, and V.H. Huxley Permeability and contractile responses of collecting lymphatic vessels elicited by atrial and brain natriuretic peptides J. Physiol. 591 2013 5071 5081
57. B. Schaub, R. Lauener, and E. von Mutius The many faces of the hygiene hypothesis J. Allergy Clin. Immunol. 117 2006 969 977 quiz 978
58. A. Schlitzer, N. McGovern, P. Teo, T. Zelante, K. Atarashi, D. Low, A.W. Ho, P. See, A. Shin, P.S. Wasan, and et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses Immunity 38 2013 970 983
59. O. Schulz, E. Jaensson, E.K. Persson, X. Liu, T. Worbs, W.W. Agace, and O. Pabst Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions J. Exp. Med. 206 2009 3101 3114
60. M. Simonet, and S. Falkow Invasin expression in Yersinia pseudotuberculosis Infect. Immun. 60 1992 4414 4417
61. A.L. St John, W.X. Ang, M.N. Huang, C.A. Kunder, E.W. Chan, M.D. Gunn, and S.N. Abraham S1P-Dependent trafficking of intracellular yersinia pestis through lymph nodes establishes Buboes and systemic infection Immunity 41 2014 440 450
62. C.M. Sun, J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid J. Exp. Med. 204 2007 1775 1785
63. C. Varol, A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H.J. Fehling, W.D. Hardt, G. Shakhar, and S. Jung Intestinal lamina propria dendritic cell subsets have different origin and functions Immunity 31 2009 502 512
64. L. Vernacchio, R.M. Vezina, A.A. Mitchell, S.M. Lesko, A.G. Plaut, and D.W. Acheson Diarrhea in American infants and young children in the community setting: incidence, clinical presentation and microbiology Pediatr. Infect. Dis. J. 25 2006 2 7
65. Y. Wang, M.A. Su, and Y.Y. Wan An essential role of the transcription factor GATA-3 for the function of regulatory T cells Immunity 35 2011 337 348
66. H.L. Weiner, A.P. da Cunha, F. Quintana, and H. Wu Oral tolerance Immunol. Rev. 241 2011 241 259
67. J.V. Weinstock, R. Summers, and D.E. Elliott Helminths and harmony Gut 53 2004 7 9
68. + regulatory T cell fate during inflammation in mice J. Clin. Invest. 121 2011 4503 4515
69. T. Worbs, U. Bode, S. Yan, M.W. Hoffmann, G. Hintzen, G. Bernhardt, R. Förster, and O. Pabst Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells J. Exp. Med. 203 2006 519 527
70. B.W. Wren The yersiniae - a model genus to study the rapid evolution of bacterial pathogens Nat. Rev. Microbiol. 1 2003 55 64
71. Y. Zhang, P. Mena, G. Romanov, J.S. Lin, S.T. Smiley, and J.B. Bliska A protective epitope in type III effector YopE is a major CD8 T cell antigen during primary infection with Yersinia pseudotuberculosis Infect. Immun. 80 2012 206 214
72. A. Zulian, R. Cancello, C. Ruocco, D. Gentilini, A.M. Di Blasio, P. Danelli, G. Micheletto, E. Cesana, and C. Invitti Differences in visceral fat and fat bacterial colonization between ulcerative colitis and Crohn's disease. An in vivo and in vitro study PLoS ONE 8 2013 e78495