Innate lymphoid cells in inflammatory bowel diseases

Immunology Letters

Volumn 172, Issue , 2016, Pages 124-131

  Peters, C P ^a   Mjosberg J M ^b   Bernink, J H ^a   Spits, H ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Anti TNF; Crohn's disease; IBD; IFN ; ILC; Innate lymphoid cells; Ulcerative colitis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; BLOCKING ANTIBODY; TUMOR NECROSIS FACTOR;

CELL FUNCTION; CLINICAL FEATURE; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; GASTRITIS; GASTROINTESTINAL ENDOSCOPY; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE SYSTEM; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE FLORA; LYMPHOID CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; ULCERATIVE COLITIS; ANIMAL; DISEASE PREDISPOSITION; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE; METABOLISM; PROCEDURES;

ANIMALS; ANTIBODIES, BLOCKING; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY; INFLAMMATORY BOWEL DISEASES; INTERFERON-GAMMA; LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84949439020     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2015.10.004     Document Type: Review

References (101)

1. Jostins L., Ripke S., Weersma R.K., Duerr R.H., McGovern D.P., Hui K.Y., et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012, 491:119-124.
2. Frolkis A., Dieleman L.A., Barkema H.W., Panaccione R., Ghosh S., Fedorak R.N., et al. Environment and the inflammatory bowel diseases. Can. J. Gastroenterol. 2013, 27:e18-e24.
3. Ng S.C., Bernstein C.N., Vatn M.H., Lakatos P.L., Loftus E.V., Tysk C., et al. Geographical variability and environmental risk factors in inflammatory bowel disease. Gut 2013, 62:630-649.
4. Abraham C., Cho J.H. Inflammatory bowel disease. N. Engl. J. Med. 2009, 361:2066-2078.
5. Bernstein C.N., Wajda A., Blanchard J.F. The clustering of other chronic inflammatory diseases in inflammatory bowel disease: a population-based study. Gastroenterology 2005, 129:827-836.
6. Xavier R.J., Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
7. Glocker E.O., Kotlarz D., Boztug K., Gertz E.M., Schäffer A.A., Noyan F., et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 2009, 361:2033-2045.
8. Desai H.G., Gupte P.A. Increasing incidence of Crohn's disease in India: is it related to improved sanitation. Indian J. Gastroenterol. 2005, 24:23-24.
9. Zheng J.J., Zhu X.S., Huangfu Z., Gao Z.X., Guo Z.R., Wang Z. Crohn's disease in mainland China: a systematic analysis of 50 years of research. Chin. J. Dig. Dis. 2005, 6:175-181.
10. Aldhous M.C., Drummond H.E., Anderson N., Baneshi M.R., Smith L.A., Arnott I.D., et al. Smoking habit and load influence age at diagnosis and disease extent in ulcerative colitis. Am. J. Gastroenterol. 2007, 102:589-597.
11. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13780-13785.
12. Gevers D., Kugathasan S., Denson L.A., Vázquez-Baeza Y., Van Treuren W., Ren B., et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014, 15:382-392.
13. + lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease Crohn's disease LP cells manifest increased secretion of IFN-γ, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 1996, 157:1261-1270.
14. Kobayashi T., Okamoto S., Hisamatsu T., Kamada N., Chinen H., Saito R., et al. IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 2008, 57:1682-1689.
15. + T cells. Immunity 1994, 1:553-562.
16. Fujino S., Andoh A., Bamba S., Ogawa A., Hata K., Araki Y., et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003, 52:65-70.
17. Sarra M., Pallone F., MacDonald T.T., Monteleone G. IL-23/IL-17 axis in IBD. Inflamm. Bowel Dis. 2010, 16:1808-1813.
18. Fuss I.J., Heller F., Boirivant M., Leon F., Yoshida M., Fichtner-Feigl S., et al. Nonclassical CD1d-restricted NK T. cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J. Clin. Invest. 2004, 113:1490-1497.
19. Inoue S., Matsumoto T., Iida M., Mizuno M., Kuroki F., Hoshika K., et al. Characterization of cytokine expression in the rectal mucosa of ulcerative colitis: correlation with disease activity. Am. J. Gastroenterol. 1999, 94:2441-2446.
20. Danese S., Fiocchi C. Ulcerative colitis. N. Engl. J. Med. 2011, 365:1713-1725.
21. + T cells in the inflamed mucosa of patients with ulcerative colitis. World J. Gastroenterol. 2007, 13:5995-6002.
22. Beltran C.J., Nunez L.E., Diaz-Jimenez D., Farfan N., Candia E., Heine C., et al. Characterization of the novel ST2/IL-33 system in patients with inflammatory bowel disease. Inflamm. Bowel Dis. 2010, 16:1097-1107.
23. Kobori A., Yagi Y., Imaeda H., Ban H., Bamba S., Tsujikawa T., et al. Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis. J. Gastroenterol. 2010, 45:999-1007.
24. Diaz-Jimenez D., Nunez L.E., Beltran C.J., Candia E., Suazo C., Alvarez-Lobos M., et al. Soluble ST2: a new and promising activity marker in ulcerative colitis. World J. Gastroenterol. 2011, 17:2181-2190.
25. Danese S., Rudzinski J., Brandt W., Dupas J.L., Peyrin-Biroulet L., Bouhnik Y., et al. Tralokinumab for moderate-to-severe UC: a randomised, double-blind, placebo-controlled, phase IIa study. Gut 2015, 64:243-249.
26. Halim T.Y., Krauss R.H., Sun A.C., Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 2012, 36:451-463.
27. Klein Wolterink R.G., Kleinjan A., van Nimwegen M., Bergen I., de Bruijn M., Levani Y., et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur. J. Immunol. 2012, 42:1106-1116.
28. Monticelli L.A., Sonnenberg G.F., Abt M.C., Alenghat T., Ziegler C.G., Doering T.A., et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 2011, 12:1045-1054.
29. Kim B.S., Siracusa M.C., Saenz S.A., Noti M., Monticelli L.A., Sonnenberg G.F., et al. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci. Transl. Med. 2013, 5:170ra16.
30. Salimi M., Barlow J.L., Saunders S.P., Xue L., Gutowska-Owsiak D., Wang X., et al. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J. Exp. Med. 2013, 210:2939-2950.
31. + ILC3 in lesional skin and blood of psoriasis patients. J. Invest. Dermatol. 2014, 134:2351-2360.
32. McHedlidze T., Waldner M., Zopf S., Walker J., Rankin A.L., Schuchmann M., et al. Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 2013, 39:357-371.
33. Fuchs A., Vermi W., Lee J.S., Lonardi S., Gilfillan S., Newberry R.D., et al. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity 2013, 38:769-781.
34. Mjösberg J.M., Trifari S., Crellin N.K., Peters C.P., van Drunen C.M., Piet B., et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat. Immunol. 2011, 12:1055-1062.
35. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722-725.
36. Dudakov J.A., Hanash A.M., Jenq R.R., Young L.F., Ghosh A., Singer N.V., et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science 2012, 336:91-95.
37. Gentek R., Munneke J.M., Helbig C., Blom B., Hazenberg M.D., Spits H., Amsen D. Modulation of signal strength switches notch from an inducer of T cells to an inducer of ILC2. Front. Immunol. 2013, 4:334.
38. Male V., Hughes T., McClory S., Colucci F., Caligiuri M.A., Moffett Immature A.N.K. cells, capable of producing IL-22, are present in human uterine mucosa. J. Immunol. 2010, 185:3913-3918.
39. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
40. Klose C.S., Flach M., Möhle L., Rogell L., Hoyler T., Ebert K., et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014, 157:340-356.
41. Spits H., Artis D., Colonna M., Diefenbach A., Di Santo J.P., Eberl G., et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013, 13:145-149.
42. Mebius R.E. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 2003, 3:292-303.
43. Spits H., Di Santo J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 2011, 12:21-27.
44. + lineage distinct from conventional natural killer cells. J. Exp. Med. 2010, 207:281-290.
45. + innate lymphoid cells. Immunity 2014, 41:988-1000.
46. + innate lymphoid cells and conventional natural killer cells. Blood 2013, 121:2234-2243.
47. Artis D., Spits H. The biology of innate lymphoid cells. Nature 2015, 517:293-301.
48. + innate lymphoid cells and intraepithelial lymphocytes. Front. Immunol. 2012, 3:124.
49. + group 3 ILCs and controls intestinal immunity and inflammation. Semin. Immunopathol. 2013, 35:657-670.
50. Cella M., Otero K., Colonna M. Expansion of human NK-22 cells with IL-7, IL-2, and IL-1β reveals intrinsic functional plasticity. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10961-10966.
51. + immature human natural killer cells in secondary lymphoid tissue. Immunity 2010, 32:803-814.
52. + LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 2010, 33:752-764.
53. + innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 2013, 38:1223-1235.
54. Colonna M. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity. Immunity 2009, 31:15-23.
55. Wolk K., Kunz S., Witte E., Friedrich M., Asadullah K., Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004, 21:241-254.
56. Gasteiger G., Rudensky A.Y. Interactions between innate and adaptive lymphocytes. Nat. Rev. Immunol. 2014, 14:631-639.
57. + innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 2011, 12:320-326.
58. + Innate Lymphoid Cells. Front. Immunol. 2012, 3:72.
59. + cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
60. Zenewicz L.A., Yancopoulos G.D., Valenzuela D.M., Murphy A.J., Stevens S., Flavell R.A. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008, 29:947-957.
61. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008, 14:282-289.
62. Mielke L.A., Jones S.A., Raverdeau M., Higgs R., Stefanska A., Groom J.R., et al. Retinoic acid expression associates with enhanced IL-22 production by γδ T cells and innate lymphoid cells and attenuation of intestinal inflammation. J. Exp. Med. 2013, 210:1117-1124.
63. Sonnenberg G.F., Monticelli L.A., Alenghat T., Fung T.C., Hutnick N.A., Kunisawa J., et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012, 336:1321-1325.
64. Huber S., Gagliani N., Zenewicz L.A., Huber F.J., Bosurgi L., Hu B., et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 2012, 491:259-263.
65. Kirchberger S., Royston D.J., Boulard O., Thornton E., Franchini F., Szabady R.L., et al. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013, 210:917-931.
66. + immune precursors reside in human adult intestine and differentiate into natural killer cells. Gastroenterology 2007, 133:559-573.
67. Fehniger T.A., Cooper M.A., Nuovo G.J., Cella M., Facchetti F., Colonna M., et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003, 101:3052-3057.
68. Ferlazzo G., Thomas D., Lin S.L., Goodman K., Morandi B., Muller W.A., et al. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J. Immunol. 2004, 172:1455-1462.
69. + NK cells in the colonic lamina propria of inflammatory bowel disease patients, but not after azathioprine treatment. Aliment. Pharmacol. Ther. 2011, 33:115-126.
70. Colonna T., Korelitz B.I. The role of leukopenia in the 6-mercaptopurine-induced remission of refractory Crohn's disease. Am. J. Gastroenterol. 1994, 89:362-366.
71. Bernink J.H., Peters C.P., Munneke M., te Velde A.A., Meijer S.L., Weijer K., et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 2013, 14:221-229.
72. + innate lymphoid cells. Nature 2013, 494:261-265.
73. + innate lymphocytes. Immunity 2010, 33:736-751.
74. + group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 2015, 43:146-160.
75. Adams R.B., Planchon S.M., Roche J.K. IFN-γ modulation of epithelial barrier function time course, reversibility, and site of cytokine binding. J Immunol 1993, 150:2356-2363.
76. Boehm U., Klamp T., Groot M., Howard J.C. Cellular responses to interferon-γ. Annu. Rev. Immunol. 1997, 15:749-795.
77. -/-- mice: functional inactivation of p53 in developing T cells. Blood 2004, 104:3886-3893.
78. Buonocore S., Ahern P.P., Uhlig H.H., Ivanov I.I., Littman D.R., Maloy K.J., et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010, 464:1371-1375.
79. Mannon P.J., Fuss I.J., Mayer L., Elson C.O., Sandborn W.J., Present D., et al. Anti-interleukin-12 antibody for active Crohn's disease. N. Engl. J. Med. 2004, 351:2069-2079.
80. Agnholt J., Kaltoft K. Infliximab downregulates interferon-γ production in activated gut T-lymphocytes from patients with Crohn's disease. Cytokine 2001, 15:212-222.
81. Cuffari C., Li D.Y., Mahoney J., Barnes Y., Bayless T.M. Peripheral blood mononuclear cell DNA 6-thioguanine metabolite levels correlate with decreased interferon-γ production in patients with Crohn's disease on AZA therapy. Dig. Dis. Sci. 2004, 49:133-137.
82. Reinisch W., de Villiers W., Bene L., Simon L., Rácz I., Katz S., et al. Fontolizumab in moderate to severe Crohn's disease: a phase 2, randomized, double-blind, placebo-controlled, multiple-dose study. Inflamm. Bowel. Dis. 2010, 16:233-242.
83. Hommes D.W., Mikhajlova T.L., Stoinov S., Stimac D., Vucelic B., Lonovics J., et al. Fontolizumab, a humanised anti-interferon γ antibody, demonstrates safety and clinical activity in patients with moderate to severe Crohn's disease. Gut 2006, 55:1131-1137.
84. Geremia A., Arancibia-Carcamo C.V., Fleming M.P., Rust N., Singh B., Mortensen N.J., et al. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 2011, 208:1127-1133.
85. Hueber W., Sands B.E., Lewitzky S., Vandemeulebroecke M., Reinisch W., Higgins P.D., et al. Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut 2012, 61:1693-1700.
86. Gordon K.B., Leonardi C.L., Lebwohl M., Blauvelt A., Cameron G.S., Braun D., et al. A 52-week, open-label study of the efficacy and safety of ixekizumab, an anti-interleukin-17A monoclonal antibody, in patients with chronic plaque psoriasis. J. Am. Acad. Dermatol. 2014, 71:1176-1182.
87. Baeten D., Baraliakos X., Braun J., Sieper J., Emery P., van der Heijde D., et al. Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 2013, 382:1705-1713.
88. O'Connor W., Kamanaka M., Booth C.J., Town T., Nakae S., Iwakura Y., et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 2009, 10:603-609.
89. Mikami Y., Kanai T., Sujino T., Ono Y., Hayashi A., Okazawa A., et al. Competition between colitogenic Th1 and Th17 cells contributes to the amelioration of colitis. Eur. J. Immunol. 2010, 40:2409-2422.
90. + T-cell responses to intestinal commensal bacteria. Nature 2013, 498:113-117.
91. + T cells. Science 2015, 348:1031-1035.
92. Nussbaum J.C., Van Dyken S.J., von Dyken J., Cheng L.E., Mohapatra A., Molofsky A.B., et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 2013, 502:245-248.
93. Mjösberg J., Bernink J., Golebski K., Karrich J.J., Peters C.P., Blom B., et al. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012, 37:649-659.
94. Wong S.H., Walker J.A., Jolin H.E., Drynan L.F., Hams E., Camelo A., et al. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 2012, 13:229-236.
95. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., et al. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
96. Fallon P.G., Ballantyne S.J., Mangan N.E., Barlow J.L., Dasvarma A., Hewett D.R., et al. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 2006, 203:1105-1116.
97. + lymphoid cells. Nature 2010, 463:540-544.
98. Neill D.R., Wong S.H., Bellosi A., Flynn R.J., Daly M., Langford T.K., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
99. hi cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat. Immunol. 2015, 16:161-169.
100. Heller F., Fuss I.J., Nieuwenhuis E.E., Blumberg R.S., Strober W. Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity 2002, 17:629-638.
101. + innate lymphoid cells. Immunity 2012, 37:674-684.