Pathogen Resistance Mediated by IL-22 Signaling at the Epithelial-Microbiota Interface

Journal of Molecular Biology

Volumn 427, Issue 23, 2015, Pages 3676-3682

  Schreiber, Fernanda ^a   Arasteh, Julia Maryam ^a   Lawley, Trevor D ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Abbreviations ILC innate lymphoid cell; IBD inflammatory bowel disease; SCFA short chain fatty acid; SFB segmented filamentous bacteria

Indexed keywords

INTERLEUKIN 22; IL22RA2 PROTEIN, HUMAN; INTERLEUKIN RECEPTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; EPITHELIUM CELL; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HYDRATION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INTESTINE EPITHELIUM; INTESTINE FLORA; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION; BACTERIAL INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MUCOSAL IMMUNITY; PHYSIOLOGY;

BACTERIAL INFECTIONS; EPITHELIAL CELLS; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION;

EID: 84947569140     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.10.013     Document Type: Review

References (55)

1. I. Sekirov, S.L. Russell, L.C.M. Antunes, and B.B. Finlay Gut microbiota in health and disease Physiol. Rev. 90 2010 859 904
2. C.M. Guinane, and P.D. Cotter Role of the gut microbiota in health and chronic gastrointestinal disease: Understanding a hidden metabolic organ Ther. Adv. Gastroenterol. 6 2013 295 308
3. B.O. Adamu, and T.D. Lawley Bacteriotherapy for the treatment of intestinal dysbiosis caused by Clostridium difficile infection Curr. Opin. Microbiol. 16 2013 596 601
4. B. Stecher, D. Berry, and A. Loy Colonization resistance and microbial ecophysiology: Using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle FEMS Microbiol. Rev. 37 2013 793 829
5. H.E. Jakobsson, A.M. RodríguezPiñeiro, A. Schütte, A. Ermund, P. Boysen, M. Bemark, and et al. The composition of the gut microbiota shapes the colon mucus barrier EMBO Rep. 16 2015 164 177
6. M.E.V. Johansson, M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G.C. Hansson The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria Proc. Natl. Acad. Sci. 105 2008 15064 15069
7. M.V. Johansson, D. Ambort, T. Pelaseyed, A. Schütte, J. Gustafsson, A. Ermund, and et al. Composition and functional role of the mucus layers in the intestine Cell. Mol. Life Sci. 68 2011 3635 3641
8. B.D. Simons, and H. Clevers Stem cell self-renewal in intestinal crypt Exp. Cell Res. 317 2011 2719 2724
9. A.M. Mowat, and W.W. Agace Regional specialization within the intestinal immune system Nat. Rev. Immunol. 14 2014 667 685
10. H. Kumar, T. Kawai, and S. Akira Pathogen recognition by the innate immune system Int. Rev. Immunol. 30 2011 16 34
11. P.J. Sansonetti The innate signaling of dangers and the dangers of innate signaling Nat. Immunol. 7 2006 1237 1242
12. D.F. McCole IBD candidate genes and intestinal barrier regulation Inflamm. Bowel Dis. 20 2014 1829 1849
13. K. Wolk, E. Witte, K. Witte, K. Warszawska, and R. Sabat Biology of interleukin-22 Semin. Immunopathol. 32 2010 17 31
14. E. Witte, K. Witte, K. Warszawska, R. Sabat, and K. Wolk Interleukin-22: A cytokine produced by T, NK and NKT cell subsets, with importance in the innate immune defense and tissue protection Cytokine Growth Factor Rev. 21 2010 365 379
15. K. Wolk, S. Kunz, E. Witte, M. Friedrich, K. Asadullah, and R. Sabat IL-22 increases the innate immunity of tissues Immunity 21 2004 241 254
16. M. Colonna Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity Immunity 31 2009 15 23
17. N. Pham Tu Anh, S. Clare, D. Goulding, M. Arasteh Julia, D. Stares Mark, P. Browne Hilary, and et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen Cell Host Microbe 16 2014 504 516
18. R. Basu, B. O'Quinn Darrell, J. Silberger Daniel, R. Schoeb Trenton, L. Fouser, W. Ouyang, and et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria Immunity 37 2012 1061 1075
19. J. Behnsen, S. Jellbauer, P. Wong Christina, A. Edwards Robert, D. George Michael, W. Ouyang, and et al. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria Immunity 40 2014 262 273
20. M. Hasegawa, S. Yada, Z. Liu Meng, N. Kamada, R. Muñoz-Planillo, N. Do, and et al. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage Immunity 41 2014 620 632
21. M.S. Silverberg, J.H. Cho, J.D. Rioux, D.P.B. McGovern, J. Wu, V. Annese, and et al. Ulcerative colitis-risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study Nat. Genet. 41 2009 216 220
22. L. Jostins, S. Ripke, R.K. Weersma, R.H. Duerr, D.P. McGovern, K.Y. Hui, and et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease Nature 491 2012 119 124
23. F. Sommer, and F. Backhed The gut microbiota - Masters of host development and physiology Nat. Rev. Microbiol. 11 2013 227 238
24. P.J. Turnbaugh, V.K. Ridaura, J.J. Faith, F.E. Rey, R. Knight, and J.I. Gordon The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice Sci. Transl. Med. 1 2009 1 12
25. A. Spor, O. Koren, and R. Ley Unravelling the effects of the environment and host genotype on the gut microbiome Nat. Rev. Microbiol. 9 2011 279 290
26. J.L. Round, and S.K. Mazmanian The gut microbiota shapes intestinal immune responses during health and disease Nat. Rev. Immunol. 9 2009 313 323
27. N. Satoh-Takayama, C.A. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, and F. Rattis Microbial flora drives interleukin 22 production in intestinal NKp46 + cells that provide innate mucosal immune defense Immunity 29 2008 958 970
28. M. Coccia, O.J. Harrison, C. Schiering, M.J. Asquith, B. Becher, F. Powrie, and et al. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4 + Th17 cells J. Exp. Med. 209 2012 1595 1609
29. S. Buonocore, P.P. Ahern, H.H. Uhlig, I.I. Ivanov, D.R. Littman, K.J. Maloy, and et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology Nature 464 2010 1371 1375
30. N.K. Crellin, S. Trifari, C.D. Kaplan, N. Satoh-Takayama, J.P. Di Santo, and H. Spits Regulation of cytokine secretion in human CD127 + LTi-like innate lymphoid cells by Toll-like receptor 2 Immunity 33 2010 752 764
31. J. Qiu, X. Guo, Z-mE Chen, L. He, G.F. Sonnenberg, D. Artis, and et al. 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
32. T. Zelante, G. Iannitti Rossana, C. Cunha, A. De Luca, G. Giovannini, G. Pieraccini, and et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22 Immunity 39 2013 372 385
33. I.I. Ivanov, K. Atarashi, N. Manel, E.L. Brodie, T. Shima, U. Karaoz, and et al. Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 2009 485 498
34. T. Mitsuma, H. Odajima, Z. Momiyama, K. Watanabe, M. Masuguchi, T. Sekine, and et al. Enhancement of gene expression by a peptide p(CHWPR) produced by Bifidobacterium lactis BB-12 Microbiol. Immunol. 52 2008 144 155
35. I.A. Finnie, A.D. Dwarakanath, B.A. Taylor, and J.M. Rhodes Colonic mucin synthesis is increased by sodium butyrate Gut 36 1995 93 99
36. Y. Furusawa, Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, D. Takahashi, and et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells Nature 504 2013 446 450
37. B. Sovran, L.M.P. Loonen, P. Lu, F. Hugenholtz, C. Belzer, E.H. Stolte, and et al. IL-22-STAT3 pathway plays a key role in the maintenance of ileal homeostasis in mice lacking secreted mucus barrier Inflamm. Bowel Dis. 21 2015 531 542
38. S. Keely, C.J. Kelly, T. Weissmueller, A. Burgess, B.D. Wagner, C.E. Robertson, and et al. Activated fluid transport regulates bacterial-epithelial interactions and significantly shifts the murine colonic microbiome Gut Microbes 3 2012 250 260
39. 2 +-dependent chloride secretion across colonic epithelial cells via distinct kinase signaling pathways and ion transport proteins FASEB J. 22 2008 2023 2036
40. A.P. Moran, A. Gupta, and L. Joshi Sweet-talk: Role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract Gut 60 2011 1412 1425
41. K. Kuespert, S. Pils, and C.R. Hauck CEACAMs: Their role in physiology and pathophysiology Curr. Opin. Cell Biol. 18 2006 565 571
42. S. Nutten, P. Sansonetti, G. Huet, C. Bourdon-Bisiaux, B. Meresse, J.-F. Colombel, and et al. Epithelial inflammation response induced by Shigella flexneri depends on mucin gene expression Microbes Infect. 4 2002 1121 1124
43. D.J. Becker, and J.B. Lowe Fucose: Biosynthesis and biological function in mammals Glycobiology 13 2003 41R 53R
44. J.M. Pickard, C.F. Maurice, M.A. Kinnebrew, M.C. Abt, D. Schenten, T.V. Golovkina, and et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness Nature 514 2014 638 641
45. Y. Goto, T. Obata, J. Kunisawa, S. Sato, I.I. Ivanov, A. Lamichhane, and et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation Science 345 2014 1254009
46. D.J. Smyth, J.D. Cooper, J.M.M. Howson, P. Clarke, K. Downes, T. Mistry, and et al. FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection Diabetes 60 2011 3081 3084
47. D.P.B. McGovern, M.R. Jones, K.D. Taylor, K. Marciante, X. Yan, M. Dubinsky, and et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease Hum. Mol. Genet. 19 2010 3468 3476
48. E.A. Hurd, and S.E. Domino Increased susceptibility of secretor factor gene Fut2-null mice to experimental vaginal candidiasis Infect. Immun. 72 2004 4279 4281
49. S.H. Lee Intestinal permeability regulation by tight junction: Implication on inflammatory bowel diseases Intest. Res. 13 2015 11 18
50. G. Eberl, M. Colonna, J.P. Di Santo, and A.N.J. McKenzie Innate lymphoid cells: A new paradigm in immunology Science 348 2015 aaa6566
51. V. Tumanov Alexei, P. Koroleva Ekaterina, X. Guo, Y. Wang, A. Kruglov, S. Nedospasov, and et al. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge Cell Host Microbe 10 2011 44 53
52. N.K. Crellin, S. Trifari, C.D. Kaplan, T. Cupedo, and H. Spits Human NKp44+IL-22 + cells and LTi-like cells constitute a stable RORC + lineage distinct from conventional natural killer cells J. Exp. Med. 207 2010 281 290
53. A. Mortha, A. Chudnovskiy, D. Hashimoto, M. Bogunovic, S.P. Spencer, Y. Belkaid, and et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis Science 343 2014 1249288
54. M. Cella, A. Fuchs, W. Vermi, F. Facchetti, K. Otero, J.K.M. Lennerz, and et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity Nature 457 2009 722 725
55. A. Andoh, Z. Zhang, O. Inatomi, S. Fujino, Y. Deguchi, Y. Araki, and et al. Interleukin-22, a member of the IL-10 subfamily, induces inflammatory responses in colonic subepithelial myofibroblasts Gastroenterology 129 2005 969 984