Recent advances in gut immunology

Parasite Immunology

Volumn 39, Issue 6, 2017, Pages

  Powell, N ^a   MacDonald, T T ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

adaptive immunity; Innate immunity; Mucosal immunity

Indexed keywords

RETINOIC ACID;

CELL DIFFERENTIATION; CELL INTERACTION; HELMINTHIASIS; HOMEOSTASIS; HUMAN; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASE; INTESTINE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE FUNCTION; LYMPHOID CELL; MACROPHAGE; MONONUCLEAR PHAGOCYTE; MUCOSAL IMMUNITY; MUCOSAL-ASSOCIATED INVARIANT T CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GASTROINTESTINAL TRACT; INNATE IMMUNITY; INTESTINE MUCOSA; LYMPHOCYTE;

ANIMALS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INTESTINAL MUCOSA; INTESTINES; LYMPHOCYTES;

EID: 85019191990     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12430     Document Type: Review

References (94)

1. Sender R, Fichs S, Milo R. Revised estimates for the number of human and bacterial cells in the body. PLoS Biol. 2016;14:e1002533.
2. Gagliani N, Amezcua Vesely C, Iseppon A, et al. Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature. 2015;523:221-225.
3. Abt MC, Lewis BB, Caballero S, et al. Innate immune defenses mediated by two ILC subsets are critical for protection against acute Clostridium difficile infection. Cell Host Microbe. 2015;18:27-37.
4. Klose CS, Flach M, Mohle L, et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 2014;157:340-356.
5. Reynders A, Yessaad N, Vu Manh TP, et al. Identity, regulation and in vivo function of gut NKp46+RORgammat+ and NKp46+RORgammat- lymphoid cells. EMBO J. 2011;2011:2934-2947.
6. Neill DR, Wong SH, Bellosi A, et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010;464:1367-1370.
7. Huang Y, Guo L, Qiu J, et al. IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential ‘inflammatory’ type 2 innate lymphoid cells. Nat Immunol. 2015;16:161-169.
8. Sanos SL, Bui VL, Mortha A, et al. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nature Immunol. 2009;10:83-91.
9. Glatzer T, Killig M, Meisig J, et al. RORgammat(+) innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity. 2013;38:1223-1235.
10. Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity. 2008;29:958-970.
11. Zheng Y, Valdez PA, Danilenko DM, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14:282-289.
12. Zook EC, Kee BL. Development of innate lymphoid cells. Nature Immunol. 2016;17:775-782.
13. Yagi R, Zhong C, Northrup DL, et al. The transcription factor GATA3 is critical for the development of all IL-7Rα-expressing innate lymphoid cells. Immunity. 2014;40:378-388.
14. Moretta F, Petronelli F, Lucarelli B, et al. The generation of human innate lymphoid cells is influenced by the source of hematopoietic stem cells and by the use of G-CSF. Eur J Immunol. 2016;46:1271-1278.
15. Harbour SN, Maynard CL, Zindl CL, Schoeb TR, Weaver CT. Th17 cells give rise to Th1 cells that are required for the pathogenesis of colitis. Proc Natl Acad Sci USA. 2015;112:7061-7066.
16. Hirota K, Duarte JH, Veldhoen M, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nature Immunol. 2011;12:255-263.
17. Bal SM, Bernin JH, Nagasawa M, et al. IL-1beta, IL-4 and IL-12 control the fate of group 2 innate lymphoid cells in human airway inflammation in the lungs. Nature Immunol. 2016;17:636-645.
18. Ohne Y, Silver JS, Thompson-Snipes L, et al. IL-1 is a critical regulator of group 2 innate lymphoid cell function and plasticity. Nature Immunol. 2016;17:646-655.
19. Bernink JH, Krabbendam L, Germar K, et al. Interleukin-12 and -23 control plasticity of CD127(+) group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity. 2015;43:146-160.
20. Lim AI, Menegatti S, Bustamante J, et al. IL-12 drives functional plasticity of human group 2 innate lymphoid cells. J Exp Med. 2016;213:569-583.
21. Jenner RG, Townsend MJ, Jackson I, et al. The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes. Proc Natl Acad Sci USA. 2009;106:17876-17881.
22. Silver JS, Kearley J, Copenhaver AM, et al. Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nature Immunol. 2016;17:626-635.
23. von Burg N, Chappaz S, Baerenwaldt A, et al. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci USA. 2014;111:12835-12840.
24. 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.
25. Oliphant CJ, Hwang YY, Walker JA, et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4(+) T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity. 2014;41:283-295.
26. Halim TY, Hwang YY, Scanlon ST, et al. Group 2 innate lymphoid cells license dendritic cells to potentiate memory TH2 cell responses. Nature Immunol. 2016;17:57-64.
27. Goto Y, Obata T, Kunisawa J, et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science. 2014;345:1254009.
28. Pham TA, Clare S, Goulding D, et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe. 2014;16:504-516.
29. Lindemans CA, Calafiore M, Mertelsmann AM, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature. 2015;528:560-564.
30. Buonocore S, Ahern PP, Uhlig HH, et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature. 2010;464:1371-1375.
31. Powell N, Walker AW, Stolarczyk E, et al. The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor(+) innate lymphoid cells. Immunity. 2012;37:674-684.
32. Powell N, Lo JW, Biancheri P, et al. Interleukin 6 increases production of cytokines by colonic innate lymphoid cells in mice and patients with chronic intestinal inflammation. Gastro. 2015;149:456-467.
33. Ermann J, Staton T, Glickman JN, et al. Nod/Ripk2 signaling in dendritic cells activates IL-17A-secreting innate lymphoid cells and drives colitis in T-bet-/-.Rag2-/- (TRUC) mice. Proc Natl Acad Sci USA. 2014; 111: E2559-E2566.
34. Geremia A, Arancibia-Carcamo CV, Fleming MP, et al. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J Exp Med. 2011;208:1127-1133.
35. Mizuno S, Mikami Y, Kamada N, et al. Cross-talk between RORgammat+ innate lymphoid cells and intestinal macrophages induces mucosal IL-22 production in Crohn's disease. Inflamm Bowel Dis. 2014;20:1426-1434.
36. Song C, Lee JS, Gilfillan S, et al. Unique and redundant functions of NKp46+ ILC3s in models of intestinal inflammation. J Exp Med. 2015;212:1869-1882.
37. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-124.
38. Feagan BG, Sandborn WJ, Gasink C, et al. Ustekinumab as induction and maintenance therapy for Crohn's disease. N Engl J Med. 2016;375:1946-1960.
39. Awasthi A, Riol-Blanco L, Jager A, et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol. 2009;182:5904-5908.
40. Saenz SA, Siracusa MC, Perrigoue JG, et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010;464:1362-1366.
41. Grencis RK, Humphreys NE, Bancroft AJ. Immunity to gastrointestinal nematodes: mechanisms and myths. Immunol Rev. 2014;260:183-205.
42. Gerbe F, Sidot E, Smyth DJ, et al. Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites. Nature. 2016;529:226-230.
43. von Moltke J, Ji M, Liang HE, Locksley RM. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature. 2016;529:221-225.
44. Howitt MR, Lavoie S, Michaud M, et al. Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science. 2016;351:1329-1333.
45. Hsieh CS, Macatonia SE, O'Garra A, Murphy KM. T cell genetic background determines default T helper phenotype development in vitro. J Exp Med. 1995;181:713-721.
46. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. New Engl J Med. 2016;375:2369-2379.
47. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485-498.
48. 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.
49. 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.
50. Atarashi K, Tanoue T, Ando M, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell. 2015;163:367-380.
51. Sano T, Huang W, Hall JA, et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 Responses. Cell. 2015;163:381-393.
52. 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.
53. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620-625.
54. 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.
55. Shen Y, Giardino Torchia ML, Lawson GW, et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe. 2012;12:509-520.
56. Chu H, Khosravi A, Kusumawardhani IP, et al. Gene-microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science. 2016;352:1116-1120.
57. Holm JB, Sorobetea D, Kiilerich P, et al. Chronic Trichuris muris infection decreases diversity of the intestinal microbiota and concomitantly increases the abundance of lactobacilli. PLoS One. 2015;10:e0125495.
58. Walk ST, Blum AM, Ewing SA, et al. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm Bowel Dis. 2010;16:1841-1849.
59. Rausch S, Held J, Fischer A, et al. Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLoS One. 2013 Sep 10;8:e74026.
60. McKenney EA, Williamson L, Yoder AD, et al. Alteration of the rat cecal microbiome during colonization with the helminth Hymenolepis diminuta. Gut Microbes. 2015;6:182-193.
61. Kay GL, Millard A, Sergeant MJ, et al. Differences in the faecal microbiome in Schistosoma haematobium infected children vs. uninfected Children. PLoS Negl Trop Dis. 2015;9:e0003861.
62. Li RW, Wu S, Li W, et al. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect Immun. 2012;80:2150-2157.
63. Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos Trans R Soc Lond B Biol Sci. 2015; 370: 20140295.
64. Gorkiewicz G, Thallinger GG, Trajanoski S, et al. Alterations in the colonic microbiota in response to osmotic diarrhea. PLoS One. 2013;8:e55817.
65. Reynolds LA, Finlay BB. Worming their way into the picture: microbiota help helminths modulate host immunity. Immunity. 2015;43:840-842.
66. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330:841-845.
67. Schulz C, Perdiguero EG, Chorro L, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336:86-90.
68. Bain CC, Bravo-Blas A, Scott CL, et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol. 2014;15:929-937.
69. Niess JH, Brand S, Gu X, et al. A CX3CR1- mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005;307:254-258.
70. Cerovic V, Bain CC, Mowat AM, Milling SWF. Intestinal macrophages and dendritic cells: what's the difference. Trends Immunol. 2014;35:270-77.
71. Lelouard H, Fallet M, de Bovis B, et al. Peyer's patch dendritic cells sample antigens by extending dendrites through M-cell specific transcellular pores. Gastro. 2012;142:592-601.
72. Smythies LE, Sellers M, Clements RH, et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest. 2005;115:66-75.
73. Bain CC, Scott CL, Uronen-Hansson U, et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 2013;6:498-510.
74. Kamada N, Hisamatsu T, Okamoto S, et al. Unique CD14+ intestinal macrophages contribute to the pathogenesis of Crohn's disease via IL-23/IFN-gamma axis. J Clin Invest. 2008;118:2269-2280.
75. Kamada N, Hisamitsu T, Honda H, et al. Human CD14+ macrophages in intestinal lamina propria exhibit potent antigen-presenting ability. J Immunol. 2009;183:1724-1731.
76. Rugtveit J, Nilsen EM, Bakka A, et al. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastro. 1997;112:1493-1505.
77. Jenkins SJ, Ruckerl D, Cook PC, et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science. 2011;10:1284-1288.
78. Iwata M. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin Immunol. 2009;21:8-13.
79. Sanders TJ, McCarthy NE, Giles EM, et al. Increased production of retinoic acid by intestinal macrophages contributes to their inflammatory phenotype in patients with Crohn's disease. Gastro. 2014;146:1278-1288.
80. Sun CM, Hall JA, Blank RB, et al. Small intestine lamina propria dendritic cells promote de nove generation of Focp3 T reg cells via retinoic acid. J Exp Med. 2007;204:1775-1785.
81. Mucida D, Park Y, Gisen K, et al. Reciprocal Th17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317:256-260.
82. Brown CC, Esterhazy D, Sarde A, et al. Retinoic acid is essential for Th1 lineage stability and prevents transition to a Th17 program. Immunity. 2015;42:499-511.
83. Treiner E, Duban L, Bahram S, et al. Selection of evolutionary conserved mucosal-associated invariant T cells by MR1. Nature. 2003;422:164-169.
84. Kjer-Nielsen L, Patel O, Corbett AO, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 2012;491:717-723.
85. Godfrey DI, Uldrich AP, McCluskey J, et al. The burgeoning family of unconventional T cells. Nature Immunol. 2015;16:1114-1123.
86. Reantragoon R, Corbett AJ, Salaka IG, et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med. 2013;210:2305-2320.
87. Koay H-F, Gherardin NA, Enders A, et al. A three-stage intrathymic developmental pathway for the mucosal-associated invariant T cell lineage. Nat Immunol. 2016;17:1300-1311.
88. Cui Y, Franciszkiewicz K, Mburu YK, et al. Mucosal associated invariant T cell-rich congenic mouse strain allows functional evaluation. J Clin Invest. 2015;125:4171-4185.
89. Le Bourhis L, Martin E, Peguillet I, et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol. 2010;11:701-708.
90. Le Bourhis L, Dusseaux M, Bohineust A, et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 2013;9:e1003681.
91. Van Wigenburg B, Scherwitzl I, Hutchinson EC, et al. MAIT cells are activated during human viral infections. Nat Commun. 2016;6:11653.
92. Greene JM, Dash P, Roy S, et al. MR-1 restricted mucosal-associated invariant T (MAIT) cells respond to mycobacterial vaccination and infection in nonhuman primates. Mucosal Immunol. 2016;10:802-813.
93. Heijima E, Kawai T, Nakase H, et al. Reduced numbers and proapoptotic features of mucosal-associated invariant T cells as a characteristic finding in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21:1529-1540.
94. Serriari NE, Eoche M, Lamotte L, et al. Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel disease. Clin Exp Immunol. 2014;176:266-274.