Emerging roles for antigen presentation in establishing host–microbiome symbiosis

Immunological Reviews

Volumn 272, Issue 1, 2016, Pages 139-150

  Bessman, Nicholas J ^a   Sonnenberg, Gregory F ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

bacterial infection; IgA; IL 22; innate lymphoid cells; microbiota

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL ANTIGEN; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR1; CXCL16 CHEMOKINE; FUCOSYLTRANSFERASE; IMMUNOGLOBULIN A; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 25; LYMPHOTOXIN ALPHA BETA; LYMPHOTOXIN BETA; OSTEOCLAST DIFFERENTIATION FACTOR;

ADAPTIVE IMMUNITY; ANTIBIOTIC THERAPY; ANTIGEN PRESENTATION; CD4+ T LYMPHOCYTE; COMMENSAL; CYTOKINE PRODUCTION; DENDRITIC CELL; GLYCOSYLATION; HOST; HUMAN; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; MACROPHAGE; MICROBIOME; MONOCYTE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYMBIOSIS; TOXOPLASMOSIS;

EID: 84975495674     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12425     Document Type: Review

References (104)

1. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. BioRxiv 2016;doi:10.1101/036103.
2. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 2012;336:1268–1273.
3. Huttenhower C, Kostic AD, Xavier RJ. Inflammatory bowel disease as a model for translating the microbiome. Immunity 2014;40:843–854.
4. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature 2011;474:327–336.
5. Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 2016;14:20–32.
6. Fung TC, et al. Lymphoid tissue-resident commensal bacteria promote IL-10 family cytokines to establish mutualism. Immunity 2016;44:634–646.
7. Zeng H, Chi H. Metabolic control of regulatory T cell development and function. Trends Immunol 2015;36:3–12.
8. Macpherson AJ, Koller Y, McCoy KD. The bilateral responsiveness between intestinal microbes and IgA. Trends Immunol 2015;36:460–470.
9. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011;12:383–390.
10. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008;29:947–957.
11. Hanash AM, et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 2012;37:339–350.
12. Lindemans CA, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 2015;528:560–564.
13. Pickert G, et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 2009;206:1465–1472.
14. Sugimoto K, et al. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 2008;118:534–544.
15. Aparicio-Domingo P, et al. Type 3 innate lymphoid cells maintain intestinal epithelial stem cells after tissue damage. J Exp Med 2015;212:1783–1791.
16. Munoz M, et al. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 2009;206:3047–3059.
17. + ILC3s in models of intestinal inflammation. J Exp Med 2015;212:1869–1882.
18. Hue S, et al. Interleukin-23 drives innate and T cell–mediated intestinal inflammation. J Exp Med 2006;203:2473–2483.
19. Stefka AT, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci 2014;111:13145–13150.
20. Sonnenberg GF, Nair MG, Kirn TJ, Zaph C, Fouser LA, Artis D. Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J Exp Med 2010;207:1293–1305.
21. Geremia A, et al. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J Exp Med 2011;208:1127–1133.
22. Kelsen JR, Baldassano RN, Artis D, Sonnenberg GF. Maintaining intestinal health: the genetics and immunology of very early onset inflammatory bowel disease. Cell Mol Gastroenterol Hepatol 2015;1:462–476.
23. Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011;474:298–306.
24. Sonnenberg GF, et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012;336:1321–1325.
25. Zenewicz LA, et al. IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic. J Immunol 2013;190:5306–5312.
26. Zheng Y, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008;14:282–289.
27. Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D. CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 2011;34:122–134.
28. Rankin LC, et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol 2016;17:179–186.
29. Aychek T, et al. IL-23-mediated mononuclear phagocyte crosstalk protects mice from Citrobacter rodentium-induced colon immunopathology. Nat Commun 2015;6.
30. + dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 2012;36:276–287.
31. Manta C, et al. CX(3)CR1(+) macrophages support IL-22 production by innate lymphoid cells during infection with Citrobacter rodentium. Mucosal Immunol 2013;6:177–188.
32. + mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J Exp Med 2014;211:1571–1583.
33. Ota N, et al. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat Immunol 2011;12:941–948.
34. Tumanov AV, et al. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 2011;10:44–53.
35. Munoz M, et al. Interleukin-22 induces interleukin-18 expression from epithelial cells during intestinal infection. Immunity 2015;42:321–331.
36. Wagage S, Harms Pritchard G, Dawson L, Buza EL, Sonnenberg GF, Hunter CA. The group 3 innate lymphoid cell defect in aryl hydrocarbon receptor deficient mice is associated with T cell hyperactivation during intestinal infection. PLoS ONE 2015;10:e0128335.
37. Hepworth MR, et al. Immune tolerance. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4(+) T cells. Science 2015;348:1031–1035.
38. Hasegawa M, et al. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage. Immunity 2014;41:620–632.
39. Gauguet S, et al. Intestinal microbiota of mice influences resistance to Staphylococcus aureus pneumonia. Infect Immun 2015;83:4003–4014.
40. Sanos SL, et al. RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22–producing NKp46(+) cells. Nat Immunol 2009;10:83–91.
41. + innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 2011;12:320–326.
42. Satoh-Takayama N, et al. The chemokine receptor CXCR6 controls the functional topography of interleukin-22 producing intestinal innate lymphoid cells. Immunity 2014;41:776–788.
43. Cella M, et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009;457:722–725.
44. Allan DS, et al. An in vitro model of innate lymphoid cell function and differentiation. Mucosal Immunol 2015;8:340–351.
45. Hernández PP, et al. Interferon-λ and interleukin-22 cooperate for the induction of interferon-stimulated genes and control of rotavirus infection. Nat Immunol 2015;16:698–707.
46. Giacomin PR, et al. Epithelial-intrinsic IKKalpha expression regulates group 3 innate lymphoid cell responses and antibacterial immunity. J Exp Med 2015;212:1513–1528.
47. Guo X, Liang Y, Zhang Y, Lasorella A, Kee BL, Fu YX. Innate lymphoid cells control early colonization resistance against intestinal pathogens through ID2-dependent regulation of the microbiota. Immunity 2015;42:731–743.
48. Obata T, et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc Natl Acad Sci USA 2010;107:7419–7424.
49. Qiu J, et al. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 2013;39:386–399.
50. Sano T, et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell 2015;163:381–393.
51. Atarashi K, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 2015;163:367–380.
52. Upadhyay V, et al. Lymphotoxin regulates commensal responses to enable diet-induced obesity. Nat Immunol 2012;13:947–953.
53. Wang X, et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature 2014;514:237–241.
54. Pham TA, et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe 2014;16:504–516.
55. Goto Y, et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science 2014;345:1254009.
56. Pickard JM, et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 2014;514:638–641.
57. Johansson ME, et al. Normalization of host intestinal mucus layers requires long-term microbial colonization. Cell Host Microbe 2015;18:582–592.
58. Earle KA, et al. Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 2015;18:478–488.
59. Shan M, et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 2013;342:447–453.
60. Pelaseyed T, et al. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol Rev 2014;260:8–20.
61. Conley ME, Delacroix DL. Intravascular and mucosal immunoglobulin A: two separate but related systems of immune defense? Ann Intern Med 1987;106:892–899.
62. Rogier EW, et al. Lessons from mother: long-term impact of antibodies in breast milk on the gut microbiota and intestinal immune system of breastfed offspring. Gut Microbes 2014;5:663–668.
63. Gommerman JL, Rojas OL, Fritz JH. Re-thinking the functions of IgA(+) plasma cells. Gut Microbes 2014;5:652–662.
64. Rogier EW, et al. Secretory antibodies in breast milk promote long-term intestinal homeostasis by regulating the gut microbiota and host gene expression. Proc Natl Acad Sci USA 2014;111:3074–3079.
65. Moon C, Baldridge MT, Wallace MA, Burnham C-AD, Virgin HW, Stappenbeck TS. Vertically transmitted faecal IgA levels determine extra-chromosomal phenotypic variation. Nature 2015;521:90–93.
66. Palm NW, et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 2014;158:1000–1010.
67. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000;288:2222–2226.
68. + plasmablasts in the human gut are antigen-specific. J Clin Investig 2011;121:1946–1955.
69. Koenig JE, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci 2011;108:4578–4585.
70. Lindner C, et al. Diversification of memory B cells drives the continuous adaptation of secretory antibodies to gut microbiota. Nat Immunol 2015;16:880–888.
71. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662–1665.
72. + plasma cell phenotype in the gut. Nature 2012;481:199–203.
73. Tezuka H, et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 2007;448:929–933.
74. Wang S, et al. MyD88 adaptor-dependent microbial sensing by regulatory T cells promotes mucosal tolerance and enforces commensalism. Immunity 2015;43:289–303.
75. Kubinak Jason L, et al. MyD88 signaling in T cells directs IgA-mediated control of the microbiota to promote health. Cell Host Microbe 2015;17:153–163.
76. Cao AT, Yao S, Gong B, Nurieva RI, Elson CO, Cong Y. Interleukin (IL)-21 promotes intestinal IgA response to microbiota. Mucosal Immunol 2015;8:1072–1082.
77. Hirota K, et al. Plasticity of TH17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol 2013;14:372–379.
78. Chu VT, et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity 2014;40:582–593.
79. Bunker J J, et al. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 2015;43:541–553.
80. + plasma cells mediate robust early-phase intestinal IgA responses in mice. Nat Commun 2013;4:1772.
81. Lécuyer E, et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 2014;40:608–620.
82. Fransen F, et al. BALB/c and C57BL/6 mice differ in polyreactive IgA abundance, which impacts the generation of antigen-specific IgA and microbiota diversity. Immunity 2015;43:527–540.
83. Mirpuri J, et al. Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microbes 2014;5:28–39.
84. Kau AL, et al. Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy. Sci Transl Med 2015;7:276ra224.
85. Charbonneau MR, et al. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 2016;164:859–871.
86. Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med 2015;21:698–708.
87. Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 2004;5:64–73.
88. − cells in relation to B- and T-zone stroma in spleen. Blood 2007;109:1602–1610.
89. van de Pavert SA, Mebius RE. New insights into the development of lymphoid tissues. Nat Rev Immunol 2010;10:664–674.
90. White A, et al. Lymphotoxin a-dependent and -independent signals regulate stromal organizer cell homeostasis during lymph node organogenesis. Blood 2007;110:1950–1959.
91. Bouskra D, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008;456:507–510.
92. Kruglov AA, et al. Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 2013;342:1243–1246.
93. Mortha A, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014;343:1449–1477.
94. Withers DR, et al. Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J Immunol 2012;189:2094–2098.
95. von Burg N, et al. Activated group 3 innate lymphoid cells promote T-cell–mediated immune responses. Proc Natl Acad Sci USA 2014;111:12835–12840.
96. Goto Y, et al. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 2014;40:594–607.
97. + T-cell responses to intestinal commensal bacteria. Nature 2013;498:113–117.
98. Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc Natl Acad Sci USA 2009;106:19256–19261.
99. + innate lymphoid cells revealed by single-cell RNA sequencing. Nat Immunol 2016;17:451–460.
100. Goc J, Hepworth MR, Sonnenberg GF. Group 3 innate lymphoid cells: regulating host-commensal bacteria interactions in inflammation and cancer. Int Immunol 2016;28:43–52.
101. Xu H, Wang X, Lackner AA, Veazey RS. Type 3 innate lymphoid cell depletion is mediated by TLRs in lymphoid tissues of simian immunodeficiency virus–infected macaques. FASEB J 2015;29:5072–5080.
102. Zhang Z, et al. Plasmacytoid dendritic cells promote HIV-1–induced group 3 innate lymphoid cell depletion. J Clin Investig 2015;125:3692–3703.
103. Kubinak JL, et al. MHC variation sculpts individualized microbial communities that control susceptibility to enteric infection. Nat Commun 2015;6.
104. Withers DR, et al. Transient inhibition of ROR-[gamma]t therapeutically limits intestinal inflammation by reducing TH17 cells and preserving group 3 innate lymphoid cells. Nat Med 2016;22:319–323.