Skip to main content
Top
Published in: Seminars in Immunopathology 4/2018

Open Access 01-07-2018 | Review

Orchestration of intestinal homeostasis and tolerance by group 3 innate lymphoid cells

Published in: Seminars in Immunopathology | Issue 4/2018

Login to get access

Abstract

The gastrointestinal tract is the primary site of exposure to a multitude of microbial, environmental, and dietary challenges. As a result, immune responses in the intestine need to be tightly regulated in order to prevent inappropriate inflammatory responses to exogenous stimuli. Intestinal homeostasis and tolerance are mediated through a multitude of immune mechanisms that act to reinforce barrier integrity, maintain the segregation and balance of commensal microbes, and ensure tissue health and regeneration. Here, we discuss the role of group 3 innate lymphoid cells (ILC3) as key regulators of intestinal health and highlight how increasing evidence implicates dysregulation of this innate immune cell population in the onset or progression of a broad range of clinically relevant pathologies. Finally, we discuss how the next generation of immunotherapeutics may be utilized to target ILC3 in disease and restore gastrointestinal tolerance and tissue health.
Literature
8.
go back to reference Eberl G, Colonna M, Di Santo JP, McKenzie AN (2015) Innate lymphoid cells: a new paradigm in immunology. Science 348 (6237):aaa6566 Eberl G, Colonna M, Di Santo JP, McKenzie AN (2015) Innate lymphoid cells: a new paradigm in immunology. Science 348 (6237):aaa6566
9.
go back to reference Klose CS, Artis D (2016) Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat Immunol 17(7):765–774PubMedCrossRef Klose CS, Artis D (2016) Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat Immunol 17(7):765–774PubMedCrossRef
11.
go back to reference Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol 13(2):145–149PubMedCrossRef Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol 13(2):145–149PubMedCrossRef
12.
go back to reference Wang S, Xia P, Chen Y, Qu Y, Xiong Z, Ye B, Du Y, Tian Y, Yin Z, Xu Z, Fan Z (2017) Regulatory innate lymphoid cells control innate intestinal inflammation. Cell 171:201–216.e18PubMedCrossRef Wang S, Xia P, Chen Y, Qu Y, Xiong Z, Ye B, Du Y, Tian Y, Yin Z, Xu Z, Fan Z (2017) Regulatory innate lymphoid cells control innate intestinal inflammation. Cell 171:201–216.e18PubMedCrossRef
13.
go back to reference Sonnenberg GF, Fouser LA, Artis D (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12(5):383–390PubMedCrossRef Sonnenberg GF, Fouser LA, Artis D (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12(5):383–390PubMedCrossRef
15.
go back to reference Bar-Ephraim YE, Cornelissen F, Papazian N, Konijn T, Hoogenboezem RM, Sanders MA, Westerman BA, Gonultas M, Kwekkeboom J, Den Haan JMM, Reijmers RM, Mebius RE, Cupedo T (2017) Cross-tissue transcriptomic analysis of human secondary lymphoid organ-residing ILC3s reveals a quiescent state in the absence of inflammation. Cell Rep 21(3):823–833. https://doi.org/10.1016/j.celrep.2017.09.070 PubMedCrossRef Bar-Ephraim YE, Cornelissen F, Papazian N, Konijn T, Hoogenboezem RM, Sanders MA, Westerman BA, Gonultas M, Kwekkeboom J, Den Haan JMM, Reijmers RM, Mebius RE, Cupedo T (2017) Cross-tissue transcriptomic analysis of human secondary lymphoid organ-residing ILC3s reveals a quiescent state in the absence of inflammation. Cell Rep 21(3):823–833. https://​doi.​org/​10.​1016/​j.​celrep.​2017.​09.​070 PubMedCrossRef
20.
go back to reference Finke D, Acha-Orbea H, Mattis A, Lipp M, Kraehenbuhl J (2002) CD4+CD3- cells induce Peyer’s patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 17(3):363–373PubMedCrossRef Finke D, Acha-Orbea H, Mattis A, Lipp M, Kraehenbuhl J (2002) CD4+CD3- cells induce Peyer’s patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 17(3):363–373PubMedCrossRef
21.
go back to reference Mackley EC, Houston S, Marriott CL, Halford EE, Lucas B, Cerovic V, Filbey KJ, Maizels RM, Hepworth MR, Sonnenberg GF, Milling S, Withers DR (2015) CCR7-dependent trafficking of RORgamma(+) ILCs creates a unique microenvironment within mucosal draining lymph nodes. Nat Commun 6:5862PubMedPubMedCentralCrossRef Mackley EC, Houston S, Marriott CL, Halford EE, Lucas B, Cerovic V, Filbey KJ, Maizels RM, Hepworth MR, Sonnenberg GF, Milling S, Withers DR (2015) CCR7-dependent trafficking of RORgamma(+) ILCs creates a unique microenvironment within mucosal draining lymph nodes. Nat Commun 6:5862PubMedPubMedCentralCrossRef
22.
go back to reference Ohl L, Henning G, Krautwald S, Lipp M, Hardtke S, Bernhardt G, Pabst O, Forster R (2003) Cooperating mechanisms of CXCR5 and CCR7 in development and organization of secondary lymphoid organs. J Exp Med 197(9):1199–1204PubMedPubMedCentralCrossRef Ohl L, Henning G, Krautwald S, Lipp M, Hardtke S, Bernhardt G, Pabst O, Forster R (2003) Cooperating mechanisms of CXCR5 and CCR7 in development and organization of secondary lymphoid organs. J Exp Med 197(9):1199–1204PubMedPubMedCentralCrossRef
23.
go back to reference Emgard J, Kammoun H, Garcia-Cassani B, Chesne J, Parigi SM, Jacob JM, Cheng HW, Evren E, Das S, Czarnewski P, Sleiers N, Melo-Gonzalez F, Kvedaraite E, Svensson M, Scandella E, Hepworth MR, Huber S, Ludewig B, Peduto L, Villablanca EJ, Veiga-Fernandes H, Pereira JP, Flavell RA, Willinger T (2018) Oxysterol sensing through the receptor GPR183 promotes the lymphoid-tissue-inducing function of innate lymphoid cells and colonic inflammation. Immunity 48(1):120–132 e128. https://doi.org/10.1016/j.immuni.2017.11.020 PubMedPubMedCentralCrossRef Emgard J, Kammoun H, Garcia-Cassani B, Chesne J, Parigi SM, Jacob JM, Cheng HW, Evren E, Das S, Czarnewski P, Sleiers N, Melo-Gonzalez F, Kvedaraite E, Svensson M, Scandella E, Hepworth MR, Huber S, Ludewig B, Peduto L, Villablanca EJ, Veiga-Fernandes H, Pereira JP, Flavell RA, Willinger T (2018) Oxysterol sensing through the receptor GPR183 promotes the lymphoid-tissue-inducing function of innate lymphoid cells and colonic inflammation. Immunity 48(1):120–132 e128. https://​doi.​org/​10.​1016/​j.​immuni.​2017.​11.​020 PubMedPubMedCentralCrossRef
25.
go back to reference Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, Mention JJ, Thiam K, Cerf-Bensussan N, Mandelboim O, Eberl G, Di Santo JP (2008) Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29(6):958–970PubMedCrossRef Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M, Rattis F, Mention JJ, Thiam K, Cerf-Bensussan N, Mandelboim O, Eberl G, Di Santo JP (2008) Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29(6):958–970PubMedCrossRef
26.
go back to reference Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, Doherty JM, Mills JC, Colonna M (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457(7230):722–725PubMedCrossRef Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz JK, Doherty JM, Mills JC, Colonna M (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457(7230):722–725PubMedCrossRef
27.
go back to reference Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov, II, Littman DR, O'Shea JJ (2009) Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206 (1):35–41 Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov, II, Littman DR, O'Shea JJ (2009) Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206 (1):35–41
29.
go back to reference Sonnenberg GF, Monticelli LA, Alenghat T, Fung TC, Hutnick NA, Kunisawa J, Shibata N, Grunberg S, Sinha R, Zahm AM, Tardif MR, Sathaliyawala T, Kubota M, Farber DL, Collman RG, Shaked A, Fouser LA, Weiner DB, Tessier PA, Friedman JR, Kiyono H, Bushman FD, Chang KM, Artis D (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336(6086):1321–1325PubMedPubMedCentralCrossRef Sonnenberg GF, Monticelli LA, Alenghat T, Fung TC, Hutnick NA, Kunisawa J, Shibata N, Grunberg S, Sinha R, Zahm AM, Tardif MR, Sathaliyawala T, Kubota M, Farber DL, Collman RG, Shaked A, Fouser LA, Weiner DB, Tessier PA, Friedman JR, Kiyono H, Bushman FD, Chang KM, Artis D (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336(6086):1321–1325PubMedPubMedCentralCrossRef
31.
33.
go back to reference Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y, Fenis A, Wieduwild E, Putoczki T, Mondot S, Lantz O, Demon D, Papenfuss AT, Smyth GK, Lamkanfi M, Carotta S, Renauld JC, Shi W, Carpentier S, Soos T, Arendt C, Ugolini S, Huntington ND, Belz GT, Vivier E (2016) Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol 17(2):179–186. https://doi.org/10.1038/ni.3332 PubMedCrossRef Rankin LC, Girard-Madoux MJ, Seillet C, Mielke LA, Kerdiles Y, Fenis A, Wieduwild E, Putoczki T, Mondot S, Lantz O, Demon D, Papenfuss AT, Smyth GK, Lamkanfi M, Carotta S, Renauld JC, Shi W, Carpentier S, Soos T, Arendt C, Ugolini S, Huntington ND, Belz GT, Vivier E (2016) Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat Immunol 17(2):179–186. https://​doi.​org/​10.​1038/​ni.​3332 PubMedCrossRef
35.
go back to reference Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, Diefenbach A (2009) RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 10(1):83–91PubMedCrossRef Sanos SL, Bui VL, Mortha A, Oberle K, Heners C, Johner C, Diefenbach A (2009) RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 10(1):83–91PubMedCrossRef
38.
go back to reference Hanash AM, Dudakov JA, Hua G, O'Connor MH, Young LF, Singer NV, West ML, Jenq RR, Holland AM, Kappel LW, Ghosh A, Tsai JJ, Rao UK, Yim NL, Smith OM, Velardi E, Hawryluk EB, Murphy GF, Liu C, Fouser LA, Kolesnick R, Blazar BR, van den Brink MR (2012) Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37(2):339–350. https://doi.org/10.1016/j.immuni.2012.05.028 PubMedPubMedCentralCrossRef Hanash AM, Dudakov JA, Hua G, O'Connor MH, Young LF, Singer NV, West ML, Jenq RR, Holland AM, Kappel LW, Ghosh A, Tsai JJ, Rao UK, Yim NL, Smith OM, Velardi E, Hawryluk EB, Murphy GF, Liu C, Fouser LA, Kolesnick R, Blazar BR, van den Brink MR (2012) Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37(2):339–350. https://​doi.​org/​10.​1016/​j.​immuni.​2012.​05.​028 PubMedPubMedCentralCrossRef
40.
go back to reference Lindemans CA, Calafiore M, Mertelsmann AM, O'Connor MH, Dudakov JA, Jenq RR, Velardi E, Young LF, Smith OM, Lawrence G, Ivanov JA, Fu YY, Takashima S, Hua G, Martin ML, O'Rourke KP, Lo YH, Mokry M, Romera-Hernandez M, Cupedo T, Dow LE, Nieuwenhuis EE, Shroyer NF, Liu C, Kolesnick R, van den Brink MR, Hanash AM (2015) Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528(7583):560–564. https://doi.org/10.1038/nature16460 PubMedPubMedCentralCrossRef Lindemans CA, Calafiore M, Mertelsmann AM, O'Connor MH, Dudakov JA, Jenq RR, Velardi E, Young LF, Smith OM, Lawrence G, Ivanov JA, Fu YY, Takashima S, Hua G, Martin ML, O'Rourke KP, Lo YH, Mokry M, Romera-Hernandez M, Cupedo T, Dow LE, Nieuwenhuis EE, Shroyer NF, Liu C, Kolesnick R, van den Brink MR, Hanash AM (2015) Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528(7583):560–564. https://​doi.​org/​10.​1038/​nature16460 PubMedPubMedCentralCrossRef
45.
go back to reference Sonnenberg GF, Fouser LA, Artis D (2010) Functional biology of the IL-22-IL-22R pathway in regulating immunity and inflammation at barrier surfaces. Adv Immunol 107:1–29PubMedCrossRef Sonnenberg GF, Fouser LA, Artis D (2010) Functional biology of the IL-22-IL-22R pathway in regulating immunity and inflammation at barrier surfaces. Adv Immunol 107:1–29PubMedCrossRef
47.
48.
51.
go back to reference Gladiator A, Wangler N, Trautwein-Weidner K, LeibundGut-Landmann S (2013) Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol 190(2):521–525PubMedCrossRef Gladiator A, Wangler N, Trautwein-Weidner K, LeibundGut-Landmann S (2013) Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J Immunol 190(2):521–525PubMedCrossRef
55.
go back to reference Goverse G, Labao-Almeida C, Ferreira M, Molenaar R, Wahlen S, Konijn T, Koning J, Veiga-Fernandes H, Mebius RE (2016) Vitamin A controls the presence of RORgamma+ innate lymphoid cells and lymphoid tissue in the small intestine. J Immunol 196(12):5148–5155PubMedCrossRef Goverse G, Labao-Almeida C, Ferreira M, Molenaar R, Wahlen S, Konijn T, Koning J, Veiga-Fernandes H, Mebius RE (2016) Vitamin A controls the presence of RORgamma+ innate lymphoid cells and lymphoid tissue in the small intestine. J Immunol 196(12):5148–5155PubMedCrossRef
56.
go back to reference Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N, Boyd A, Nutman TB, Urban JF Jr, Wang J, Ramalingam TR, Bhandoola A, Wynn TA, Belkaid Y (2014) Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343(6169):432–437PubMedPubMedCentralCrossRef Spencer SP, Wilhelm C, Yang Q, Hall JA, Bouladoux N, Boyd A, Nutman TB, Urban JF Jr, Wang J, Ramalingam TR, Bhandoola A, Wynn TA, Belkaid Y (2014) Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343(6169):432–437PubMedPubMedCentralCrossRef
57.
go back to reference van de Pavert SA, Ferreira M, Domingues RG, Ribeiro H, Molenaar R, Moreira-Santos L, Almeida FF, Ibiza S, Barbosa I, Goverse G, Labao-Almeida C, Godinho-Silva C, Konijn T, Schooneman D, O'Toole T, Mizee MR, Habani Y, Haak E, Santori FR, Littman DR, Schulte-Merker S, Dzierzak E, Simas JP, Mebius RE, Veiga-Fernandes H (2014) Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508(7494):123–127PubMedPubMedCentralCrossRef van de Pavert SA, Ferreira M, Domingues RG, Ribeiro H, Molenaar R, Moreira-Santos L, Almeida FF, Ibiza S, Barbosa I, Goverse G, Labao-Almeida C, Godinho-Silva C, Konijn T, Schooneman D, O'Toole T, Mizee MR, Habani Y, Haak E, Santori FR, Littman DR, Schulte-Merker S, Dzierzak E, Simas JP, Mebius RE, Veiga-Fernandes H (2014) Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508(7494):123–127PubMedPubMedCentralCrossRef
58.
go back to reference Konya V, Czarnewski P, Forkel M, Rao A, Kokkinou E, Villablanca EJ, Almer S, Lindforss U, Friberg D, Hoog C, Bergman P, Mjosberg J (2017) Vitamin D downregulates the IL-23 receptor pathway in human mucosal group 3 innate lymphoid cells. J Allergy Clin Immunol Konya V, Czarnewski P, Forkel M, Rao A, Kokkinou E, Villablanca EJ, Almer S, Lindforss U, Friberg D, Hoog C, Bergman P, Mjosberg J (2017) Vitamin D downregulates the IL-23 receptor pathway in human mucosal group 3 innate lymphoid cells. J Allergy Clin Immunol
59.
go back to reference Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334(6062):1561–1565PubMedCrossRef Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334(6062):1561–1565PubMedCrossRef
60.
go back to reference Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD, Nukaya M, Mantovani A, Kopan R, Bradfield CA, Newberry RD, Colonna M (2012) AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol 13(2):144–151. https://doi.org/10.1038/ni.2187 CrossRef Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD, Nukaya M, Mantovani A, Kopan R, Bradfield CA, Newberry RD, Colonna M (2012) AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol 13(2):144–151. https://​doi.​org/​10.​1038/​ni.​2187 CrossRef
61.
go back to reference Qiu J, Guo X, Chen ZM, He L, Sonnenberg GF, Artis D, Fu YX, Zhou L (2013) Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39(2):386–399PubMedCrossRef Qiu J, Guo X, Chen ZM, He L, Sonnenberg GF, Artis D, Fu YX, Zhou L (2013) Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39(2):386–399PubMedCrossRef
62.
go back to reference Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, McCoy KD, Macpherson AJ (2016) The maternal microbiota drives early postnatal innate immune development. Science 351(6279):1296–1302PubMedCrossRef Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, McCoy KD, Macpherson AJ (2016) The maternal microbiota drives early postnatal innate immune development. Science 351(6279):1296–1302PubMedCrossRef
63.
go back to reference Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling HJ, Langa F, Di Santo JP, Eberl G (2010) Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330(6004):665–669PubMedCrossRef Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling HJ, Langa F, Di Santo JP, Eberl G (2010) Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330(6004):665–669PubMedCrossRef
66.
go back to reference Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343(6178):1249288PubMedPubMedCentralCrossRef Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, Merad M (2014) Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343(6178):1249288PubMedPubMedCentralCrossRef
67.
go back to reference Hepworth MR, Sonnenberg GF (2014) Regulation of the adaptive immune system by innate lymphoid cells. Curr Opin Immunol 27C:75–82CrossRef Hepworth MR, Sonnenberg GF (2014) Regulation of the adaptive immune system by innate lymphoid cells. Curr Opin Immunol 27C:75–82CrossRef
69.
70.
71.
go back to reference von Burg N, Chappaz S, Baerenwaldt A, Horvath E, Bose Dasgupta S, Ashok D, Pieters J, Tacchini-Cottier F, Rolink A, Acha-Orbea H, Finke D (2014) Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci U S A 111(35):12835–12840CrossRef von Burg N, Chappaz S, Baerenwaldt A, Horvath E, Bose Dasgupta S, Ashok D, Pieters J, Tacchini-Cottier F, Rolink A, Acha-Orbea H, Finke D (2014) Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci U S A 111(35):12835–12840CrossRef
72.
go back to reference Withers DR, Gaspal FM, Bekiaris V, McConnell FM, Kim M, Anderson G, Lane PJ (2011) OX40 and CD30 signals in CD4(+) T-cell effector and memory function: a distinct role for lymphoid tissue inducer cells in maintaining CD4(+) T-cell memory but not effector function. Immunol Rev 244(1):134–148PubMedCrossRef Withers DR, Gaspal FM, Bekiaris V, McConnell FM, Kim M, Anderson G, Lane PJ (2011) OX40 and CD30 signals in CD4(+) T-cell effector and memory function: a distinct role for lymphoid tissue inducer cells in maintaining CD4(+) T-cell memory but not effector function. Immunol Rev 244(1):134–148PubMedCrossRef
74.
go back to reference Withers DR, Jaensson E, Gaspal F, McConnell FM, Eksteen B, Anderson G, Agace WW, Lane PJ (2009) The survival of memory CD4+ T cells within the gut lamina propria requires OX40 and CD30 signals. J Immunol 183(8):5079–5084PubMedCrossRef Withers DR, Jaensson E, Gaspal F, McConnell FM, Eksteen B, Anderson G, Agace WW, Lane PJ (2009) The survival of memory CD4+ T cells within the gut lamina propria requires OX40 and CD30 signals. J Immunol 183(8):5079–5084PubMedCrossRef
79.
go back to reference Kruglov AA, Grivennikov SI, Kuprash DV, Winsauer C, Prepens S, Seleznik GM, Eberl G, Littman DR, Heikenwalder M, Tumanov AV, Nedospasov SA (2013) Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 342(6163):1243–1246PubMedCrossRef Kruglov AA, Grivennikov SI, Kuprash DV, Winsauer C, Prepens S, Seleznik GM, Eberl G, Littman DR, Heikenwalder M, Tumanov AV, Nedospasov SA (2013) Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 342(6163):1243–1246PubMedCrossRef
81.
go back to reference Tsuji M, Suzuki K, Kitamura H, Maruya M, Kinoshita K, Ivanov, II, Itoh K, Littman DR, Fagarasan S (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29 (2):261–271 Tsuji M, Suzuki K, Kitamura H, Maruya M, Kinoshita K, Ivanov, II, Itoh K, Littman DR, Fagarasan S (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 29 (2):261–271
82.
go back to reference Magri G, Miyajima M, Bascones S, Mortha A, Puga I, Cassis L, Barra CM, Comerma L, Chudnovskiy A, Gentile M, Llige D, Cols M, Serrano S, Arostegui JI, Juan M, Yague J, Merad M, Fagarasan S, Cerutti A (2014) Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat Immunol 15(4):354–364PubMedPubMedCentralCrossRef Magri G, Miyajima M, Bascones S, Mortha A, Puga I, Cassis L, Barra CM, Comerma L, Chudnovskiy A, Gentile M, Llige D, Cols M, Serrano S, Arostegui JI, Juan M, Yague J, Merad M, Fagarasan S, Cerutti A (2014) Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nat Immunol 15(4):354–364PubMedPubMedCentralCrossRef
83.
go back to reference Komlosi ZI, Kovacs N, van de Veen W, Kirsch AI, Fahrner HB, Wawrzyniak M, Rebane A, Stanic B, Palomares O, Ruckert B, Menz G, Akdis M, Losonczy G, Akdis CA (2017) Human CD40 ligand-expressing type 3 innate lymphoid cells induce IL-10-producing immature transitional regulatory B cells. J Allergy Clin Immunol doi:https://doi.org/10.1016/j.jaci.2017.07.046 Komlosi ZI, Kovacs N, van de Veen W, Kirsch AI, Fahrner HB, Wawrzyniak M, Rebane A, Stanic B, Palomares O, Ruckert B, Menz G, Akdis M, Losonczy G, Akdis CA (2017) Human CD40 ligand-expressing type 3 innate lymphoid cells induce IL-10-producing immature transitional regulatory B cells. J Allergy Clin Immunol doi:https://​doi.​org/​10.​1016/​j.​jaci.​2017.​07.​046
86.
go back to reference Maloy KJ, Powrie F (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474(7351):298–306PubMedCrossRef Maloy KJ, Powrie F (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474(7351):298–306PubMedCrossRef
87.
go back to reference Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A, Boucher G, Brand S, Buning C, Cohain A, Cichon S, D'Amato M, De Jong D, Devaney KL, Dubinsky M, Edwards C, Ellinghaus D, Ferguson LR, Franchimont D, Fransen K, Gearry R, Georges M, Gieger C, Glas J, Haritunians T, Hart A, Hawkey C, Hedl M, Hu X, Karlsen TH, Kupcinskas L, Kugathasan S, Latiano A, Laukens D, Lawrance IC, Lees CW, Louis E, Mahy G, Mansfield J, Morgan AR, Mowat C, Newman W, Palmieri O, Ponsioen CY, Potocnik U, Prescott NJ, Regueiro M, Rotter JI, Russell RK, Sanderson JD, Sans M, Satsangi J, Schreiber S, Simms LA, Sventoraityte J, Targan SR, Taylor KD, Tremelling M, Verspaget HW, De Vos M, Wijmenga C, Wilson DC, Winkelmann J, Xavier RJ, Zeissig S, Zhang B, Zhang CK, Zhao H, Silverberg MS, Annese V, Hakonarson H, Brant SR, Radford-Smith G, Mathew CG, Rioux JD, Schadt EE, Daly MJ, Franke A, Parkes M, Vermeire S, Barrett JC, Cho JH (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491 (7422):119–124. doi:https://doi.org/10.1038/nature11582 Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A, Boucher G, Brand S, Buning C, Cohain A, Cichon S, D'Amato M, De Jong D, Devaney KL, Dubinsky M, Edwards C, Ellinghaus D, Ferguson LR, Franchimont D, Fransen K, Gearry R, Georges M, Gieger C, Glas J, Haritunians T, Hart A, Hawkey C, Hedl M, Hu X, Karlsen TH, Kupcinskas L, Kugathasan S, Latiano A, Laukens D, Lawrance IC, Lees CW, Louis E, Mahy G, Mansfield J, Morgan AR, Mowat C, Newman W, Palmieri O, Ponsioen CY, Potocnik U, Prescott NJ, Regueiro M, Rotter JI, Russell RK, Sanderson JD, Sans M, Satsangi J, Schreiber S, Simms LA, Sventoraityte J, Targan SR, Taylor KD, Tremelling M, Verspaget HW, De Vos M, Wijmenga C, Wilson DC, Winkelmann J, Xavier RJ, Zeissig S, Zhang B, Zhang CK, Zhao H, Silverberg MS, Annese V, Hakonarson H, Brant SR, Radford-Smith G, Mathew CG, Rioux JD, Schadt EE, Daly MJ, Franke A, Parkes M, Vermeire S, Barrett JC, Cho JH (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491 (7422):119–124. doi:https://​doi.​org/​10.​1038/​nature11582
89.
go back to reference Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, Hreggvidsdottir HS, Heinsbroek SE, Legrand N, Buskens CJ, Bemelman WA, Mjosberg JM, Spits H (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 14(3):221–229PubMedCrossRef Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL, Weijer K, Hreggvidsdottir HS, Heinsbroek SE, Legrand N, Buskens CJ, Bemelman WA, Mjosberg JM, Spits H (2013) Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 14(3):221–229PubMedCrossRef
90.
go back to reference Takayama T, Kamada N, Chinen H, Okamoto S, Kitazume MT, Chang J, Matuzaki Y, Suzuki S, Sugita A, Koganei K, Hisamatsu T, Kanai T, Hibi T (2010) Imbalance of NKp44(+)NKp46(−) and NKp44(−)NKp46(+) natural killer cells in the intestinal mucosa of patients with Crohn’s disease. Gastroenterology 139 (3):882–892, 892.e881–883 doi:https://doi.org/10.1053/j.gastro.2010.05.040 Takayama T, Kamada N, Chinen H, Okamoto S, Kitazume MT, Chang J, Matuzaki Y, Suzuki S, Sugita A, Koganei K, Hisamatsu T, Kanai T, Hibi T (2010) Imbalance of NKp44(+)NKp46(−) and NKp44(−)NKp46(+) natural killer cells in the intestinal mucosa of patients with Crohn’s disease. Gastroenterology 139 (3):882–892, 892.e881–883 doi:https://​doi.​org/​10.​1053/​j.​gastro.​2010.​05.​040
94.
go back to reference Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, Fabiunke C, Pfeifer D, Sexl V, Fonseca-Pereira D, Domingues RG, Veiga-Fernandes H, Arnold SJ, Busslinger M, Dunay IR, Tanriver Y, Diefenbach A (2014) Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157(2):340–356PubMedCrossRef Klose CS, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K, Fabiunke C, Pfeifer D, Sexl V, Fonseca-Pereira D, Domingues RG, Veiga-Fernandes H, Arnold SJ, Busslinger M, Dunay IR, Tanriver Y, Diefenbach A (2014) Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157(2):340–356PubMedCrossRef
95.
go back to reference Bernink JH, Krabbendam L, Germar K, de Jong E, Gronke K, Kofoed-Nielsen M, Munneke JM, Hazenberg MD, Villaudy J, Buskens CJ, Bemelman WA, Diefenbach A, Blom B, Spits H (2015) Interleukin-12 and -23 control plasticity of CD127(+) group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 43(1):146–160. https://doi.org/10.1016/j.immuni.2015.06.019 PubMedCrossRef Bernink JH, Krabbendam L, Germar K, de Jong E, Gronke K, Kofoed-Nielsen M, Munneke JM, Hazenberg MD, Villaudy J, Buskens CJ, Bemelman WA, Diefenbach A, Blom B, Spits H (2015) Interleukin-12 and -23 control plasticity of CD127(+) group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 43(1):146–160. https://​doi.​org/​10.​1016/​j.​immuni.​2015.​06.​019 PubMedCrossRef
97.
go back to reference Viant C, Rankin LC, Girard-Madoux MJ, Seillet C, Shi W, Smyth MJ, Bartholin L, Walzer T, Huntington ND, Vivier E, Belz GT (2016) Transforming growth factor-beta and Notch ligands act as opposing environmental cues in regulating the plasticity of type 3 innate lymphoid cells. Sci Signal 9(426):ra46. https://doi.org/10.1126/scisignal.aaf2176 PubMedCrossRef Viant C, Rankin LC, Girard-Madoux MJ, Seillet C, Shi W, Smyth MJ, Bartholin L, Walzer T, Huntington ND, Vivier E, Belz GT (2016) Transforming growth factor-beta and Notch ligands act as opposing environmental cues in regulating the plasticity of type 3 innate lymphoid cells. Sci Signal 9(426):ra46. https://​doi.​org/​10.​1126/​scisignal.​aaf2176 PubMedCrossRef
99.
101.
go back to reference Xiao S, Yosef N, Yang J, Wang Y, Zhou L, Zhu C, Wu C, Baloglu E, Schmidt D, Ramesh R, Lobera M, Sundrud MS, Tsai PY, Xiang Z, Wang J, Xu Y, Lin X, Kretschmer K, Rahl PB, Young RA, Zhong Z, Hafler DA, Regev A, Ghosh S, Marson A, Kuchroo VK (2014) Small-molecule RORgammat antagonists inhibit T helper 17 cell transcriptional network by divergent mechanisms. Immunity 40(4):477–489. https://doi.org/10.1016/j.immuni.2014.04.004 PubMedPubMedCentralCrossRef Xiao S, Yosef N, Yang J, Wang Y, Zhou L, Zhu C, Wu C, Baloglu E, Schmidt D, Ramesh R, Lobera M, Sundrud MS, Tsai PY, Xiang Z, Wang J, Xu Y, Lin X, Kretschmer K, Rahl PB, Young RA, Zhong Z, Hafler DA, Regev A, Ghosh S, Marson A, Kuchroo VK (2014) Small-molecule RORgammat antagonists inhibit T helper 17 cell transcriptional network by divergent mechanisms. Immunity 40(4):477–489. https://​doi.​org/​10.​1016/​j.​immuni.​2014.​04.​004 PubMedPubMedCentralCrossRef
102.
go back to reference Withers DR, Hepworth MR, Wang X, Mackley EC, Halford EE, Dutton EE, Marriott CL, Brucklacher-Waldert V, Veldhoen M, Kelsen J, Baldassano RN, Sonnenberg GF (2016) Transient inhibition of ROR-gammat therapeutically limits intestinal inflammation by reducing TH17 cells and preserving group 3 innate lymphoid cells. Nat Med 22(3):319–323. https://doi.org/10.1038/nm.4046 PubMedPubMedCentralCrossRef Withers DR, Hepworth MR, Wang X, Mackley EC, Halford EE, Dutton EE, Marriott CL, Brucklacher-Waldert V, Veldhoen M, Kelsen J, Baldassano RN, Sonnenberg GF (2016) Transient inhibition of ROR-gammat therapeutically limits intestinal inflammation by reducing TH17 cells and preserving group 3 innate lymphoid cells. Nat Med 22(3):319–323. https://​doi.​org/​10.​1038/​nm.​4046 PubMedPubMedCentralCrossRef
103.
go back to reference Hueber W, Sands BE, Lewitzky S, Vandemeulebroecke M, Reinisch W, Higgins PD, Wehkamp J, Feagan BG, Yao MD, Karczewski M, Karczewski J, Pezous N, Bek S, Bruin G, Mellgard B, Berger C, Londei M, Bertolino AP, Tougas G, Travis SP (2012) 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 61(12):1693–1700PubMedPubMedCentralCrossRef Hueber W, Sands BE, Lewitzky S, Vandemeulebroecke M, Reinisch W, Higgins PD, Wehkamp J, Feagan BG, Yao MD, Karczewski M, Karczewski J, Pezous N, Bek S, Bruin G, Mellgard B, Berger C, Londei M, Bertolino AP, Tougas G, Travis SP (2012) 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 61(12):1693–1700PubMedPubMedCentralCrossRef
105.
go back to reference Sandborn WJ, Gasink C, Gao LL, Blank MA, Johanns J, Guzzo C, Sands BE, Hanauer SB, Targan S, Rutgeerts P, Ghosh S, de Villiers WJ, Panaccione R, Greenberg G, Schreiber S, Lichtiger S, Feagan BG (2012) Ustekinumab induction and maintenance therapy in refractory Crohn’s disease. N Engl J Med 367(16):1519–1528. https://doi.org/10.1056/NEJMoa1203572 PubMedCrossRef Sandborn WJ, Gasink C, Gao LL, Blank MA, Johanns J, Guzzo C, Sands BE, Hanauer SB, Targan S, Rutgeerts P, Ghosh S, de Villiers WJ, Panaccione R, Greenberg G, Schreiber S, Lichtiger S, Feagan BG (2012) Ustekinumab induction and maintenance therapy in refractory Crohn’s disease. N Engl J Med 367(16):1519–1528. https://​doi.​org/​10.​1056/​NEJMoa1203572 PubMedCrossRef
110.
go back to reference Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, Taniguchi K, Yu GY, Osterreicher CH, Hung KE, Datz C, Feng Y, Fearon ER, Oukka M, Tessarollo L, Coppola V, Yarovinsky F, Cheroutre H, Eckmann L, Trinchieri G, Karin M (2012) Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491(7423):254–258. https://doi.org/10.1038/nature11465 PubMedPubMedCentralCrossRef Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, Taniguchi K, Yu GY, Osterreicher CH, Hung KE, Datz C, Feng Y, Fearon ER, Oukka M, Tessarollo L, Coppola V, Yarovinsky F, Cheroutre H, Eckmann L, Trinchieri G, Karin M (2012) Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491(7423):254–258. https://​doi.​org/​10.​1038/​nature11465 PubMedPubMedCentralCrossRef
112.
go back to reference Chan IH, Jain R, Tessmer MS, Gorman D, Mangadu R, Sathe M, Vives F, Moon C, Penaflor E, Turner S, Ayanoglu G, Chang C, Basham B, Mumm JB, Pierce RH, Yearley JH, McClanahan TK, Phillips JH, Cua DJ, Bowman EP, Kastelein RA, LaFace D (2014) Interleukin-23 is sufficient to induce rapid de novo gut tumorigenesis, independent of carcinogens, through activation of innate lymphoid cells. Mucosal Immunol 7(4):842–856. https://doi.org/10.1038/mi.2013.101 PubMedCrossRef Chan IH, Jain R, Tessmer MS, Gorman D, Mangadu R, Sathe M, Vives F, Moon C, Penaflor E, Turner S, Ayanoglu G, Chang C, Basham B, Mumm JB, Pierce RH, Yearley JH, McClanahan TK, Phillips JH, Cua DJ, Bowman EP, Kastelein RA, LaFace D (2014) Interleukin-23 is sufficient to induce rapid de novo gut tumorigenesis, independent of carcinogens, through activation of innate lymphoid cells. Mucosal Immunol 7(4):842–856. https://​doi.​org/​10.​1038/​mi.​2013.​101 PubMedCrossRef
118.
go back to reference Huber S, Gagliani N, Zenewicz LA, Huber FJ, Bosurgi L, Hu B, Hedl M, Zhang W, O'Connor W, Jr., Murphy AJ, Valenzuela DM, Yancopoulos GD, Booth CJ, Cho JH, Ouyang W, Abraham C, Flavell RA (2012) IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491 (7423):259–263. doi:https://doi.org/10.1038/nature11535 Huber S, Gagliani N, Zenewicz LA, Huber FJ, Bosurgi L, Hu B, Hedl M, Zhang W, O'Connor W, Jr., Murphy AJ, Valenzuela DM, Yancopoulos GD, Booth CJ, Cho JH, Ouyang W, Abraham C, Flavell RA (2012) IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491 (7423):259–263. doi:https://​doi.​org/​10.​1038/​nature11535
119.
go back to reference Carrega P, Loiacono F, Di Carlo E, Scaramuccia A, Mora M, Conte R, Benelli R, Spaggiari GM, Cantoni C, Campana S, Bonaccorsi I, Morandi B, Truini M, Mingari MC, Moretta L, Ferlazzo G (2015) NCR(+)ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat Commun 6:8280. https://doi.org/10.1038/ncomms9280 PubMedCrossRef Carrega P, Loiacono F, Di Carlo E, Scaramuccia A, Mora M, Conte R, Benelli R, Spaggiari GM, Cantoni C, Campana S, Bonaccorsi I, Morandi B, Truini M, Mingari MC, Moretta L, Ferlazzo G (2015) NCR(+)ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat Commun 6:8280. https://​doi.​org/​10.​1038/​ncomms9280 PubMedCrossRef
120.
go back to reference Irshad S, Flores-Borja F, Lawler K, Monypenny J, Evans R, Male V, Gordon P, Cheung A, Gazinska P, Noor F, Wong F, Grigoriadis A, Fruhwirth GO, Barber PR, Woodman N, Patel D, Rodriguez-Justo M, Owen J, Martin SG, Pinder SE, Gillett CE, Poland SP, Ameer-Beg S, McCaughan F, Carlin LM, Hasan U, Withers DR, Lane P, Vojnovic B, Quezada SA, Ellis P, Tutt AN, Ng T (2017) RORgammat(+) innate lymphoid cells promote lymph node metastasis of breast cancers. Cancer Res 77(5):1083–1096. https://doi.org/10.1158/0008-5472.CAN-16-0598 PubMedCrossRef Irshad S, Flores-Borja F, Lawler K, Monypenny J, Evans R, Male V, Gordon P, Cheung A, Gazinska P, Noor F, Wong F, Grigoriadis A, Fruhwirth GO, Barber PR, Woodman N, Patel D, Rodriguez-Justo M, Owen J, Martin SG, Pinder SE, Gillett CE, Poland SP, Ameer-Beg S, McCaughan F, Carlin LM, Hasan U, Withers DR, Lane P, Vojnovic B, Quezada SA, Ellis P, Tutt AN, Ng T (2017) RORgammat(+) innate lymphoid cells promote lymph node metastasis of breast cancers. Cancer Res 77(5):1083–1096. https://​doi.​org/​10.​1158/​0008-5472.​CAN-16-0598 PubMedCrossRef
127.
go back to reference Couturier M, Lamarthee B, Arbez J, Renauld JC, Bossard C, Malard F, Bonnefoy F, Mohty M, Perruche S, Tiberghien P, Saas P, Gaugler B (2013) IL-22 deficiency in donor T cells attenuates murine acute graft-versus-host disease mortality while sparing the graft-versus-leukemia effect. Leukemia 27(7):1527–1537. https://doi.org/10.1038/leu.2013.39 PubMedCrossRef Couturier M, Lamarthee B, Arbez J, Renauld JC, Bossard C, Malard F, Bonnefoy F, Mohty M, Perruche S, Tiberghien P, Saas P, Gaugler B (2013) IL-22 deficiency in donor T cells attenuates murine acute graft-versus-host disease mortality while sparing the graft-versus-leukemia effect. Leukemia 27(7):1527–1537. https://​doi.​org/​10.​1038/​leu.​2013.​39 PubMedCrossRef
128.
go back to reference Bouziat R, Hinterleitner R, Brown JJ, Stencel-Baerenwald JE, Ikizler M, Mayassi T, Meisel M, Kim SM, Discepolo V, Pruijssers AJ, Ernest JD, Iskarpatyoti JA, Costes LM, Lawrence I, Palanski BA, Varma M, Zurenski MA, Khomandiak S, McAllister N, Aravamudhan P, Boehme KW, Hu F, Samsom JN, Reinecker HC, Kupfer SS, Guandalini S, Semrad CE, Abadie V, Khosla C, Barreiro LB, Xavier RJ, Ng A, Dermody TS, Jabri B (2017) Reovirus infection triggers inflammatory responses to dietary antigens and development of celiac disease. Science 356(6333):44–50. https://doi.org/10.1126/science.aah5298 PubMedPubMedCentralCrossRef Bouziat R, Hinterleitner R, Brown JJ, Stencel-Baerenwald JE, Ikizler M, Mayassi T, Meisel M, Kim SM, Discepolo V, Pruijssers AJ, Ernest JD, Iskarpatyoti JA, Costes LM, Lawrence I, Palanski BA, Varma M, Zurenski MA, Khomandiak S, McAllister N, Aravamudhan P, Boehme KW, Hu F, Samsom JN, Reinecker HC, Kupfer SS, Guandalini S, Semrad CE, Abadie V, Khosla C, Barreiro LB, Xavier RJ, Ng A, Dermody TS, Jabri B (2017) Reovirus infection triggers inflammatory responses to dietary antigens and development of celiac disease. Science 356(6333):44–50. https://​doi.​org/​10.​1126/​science.​aah5298 PubMedPubMedCentralCrossRef
129.
go back to reference Klatt NR, Estes JD, Sun X, Ortiz AM, Barber JS, Harris LD, Cervasi B, Yokomizo LK, Pan L, Vinton CL, Tabb B, Canary LA, Dang Q, Hirsch VM, Alter G, Belkaid Y, Lifson JD, Silvestri G, Milner JD, Paiardini M, Haddad EK, Brenchley JM (2012) Loss of mucosal CD103+ DCs and IL-17+ and IL-22+ lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol 5(6):646–657PubMedPubMedCentralCrossRef Klatt NR, Estes JD, Sun X, Ortiz AM, Barber JS, Harris LD, Cervasi B, Yokomizo LK, Pan L, Vinton CL, Tabb B, Canary LA, Dang Q, Hirsch VM, Alter G, Belkaid Y, Lifson JD, Silvestri G, Milner JD, Paiardini M, Haddad EK, Brenchley JM (2012) Loss of mucosal CD103+ DCs and IL-17+ and IL-22+ lymphocytes is associated with mucosal damage in SIV infection. Mucosal Immunol 5(6):646–657PubMedPubMedCentralCrossRef
130.
go back to reference Kloverpris HN, Kazer SW, Mjosberg J, Mabuka JM, Wellmann A, Ndhlovu Z, Yadon MC, Nhamoyebonde S, Muenchhoff M, Simoni Y, Andersson F, Kuhn W, Garrett N, Burgers WA, Kamya P, Pretorius K, Dong K, Moodley A, Newell EW, Kasprowicz V, Abdool Karim SS, Goulder P, Shalek AK, Walker BD, Ndung'u T, Leslie A (2016) Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity 44(2):391–405. https://doi.org/10.1016/j.immuni.2016.01.006 PubMedCrossRef Kloverpris HN, Kazer SW, Mjosberg J, Mabuka JM, Wellmann A, Ndhlovu Z, Yadon MC, Nhamoyebonde S, Muenchhoff M, Simoni Y, Andersson F, Kuhn W, Garrett N, Burgers WA, Kamya P, Pretorius K, Dong K, Moodley A, Newell EW, Kasprowicz V, Abdool Karim SS, Goulder P, Shalek AK, Walker BD, Ndung'u T, Leslie A (2016) Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity 44(2):391–405. https://​doi.​org/​10.​1016/​j.​immuni.​2016.​01.​006 PubMedCrossRef
131.
go back to reference Li H, Richert-Spuhler LE, Evans TI, Gillis J, Connole M, Estes JD, Keele BF, Klatt NR, Reeves RK (2014) Hypercytotoxicity and rapid loss of NKp44+ innate lymphoid cells during acute SIV infection. PLoS Pathog 10(12):e1004551PubMedPubMedCentralCrossRef Li H, Richert-Spuhler LE, Evans TI, Gillis J, Connole M, Estes JD, Keele BF, Klatt NR, Reeves RK (2014) Hypercytotoxicity and rapid loss of NKp44+ innate lymphoid cells during acute SIV infection. PLoS Pathog 10(12):e1004551PubMedPubMedCentralCrossRef
132.
go back to reference Xu H, Wang X, Liu DX, Moroney-Rasmussen T, Lackner AA, Veazey RS (2012) IL-17-producing innate lymphoid cells are restricted to mucosal tissues and are depleted in SIV-infected macaques. Mucosal Immunol 5(6):658–669PubMedPubMedCentralCrossRef Xu H, Wang X, Liu DX, Moroney-Rasmussen T, Lackner AA, Veazey RS (2012) IL-17-producing innate lymphoid cells are restricted to mucosal tissues and are depleted in SIV-infected macaques. Mucosal Immunol 5(6):658–669PubMedPubMedCentralCrossRef
133.
go back to reference Zhang Z, Cheng L, Zhao J, Li G, Zhang L, Chen W, Nie W, Reszka-Blanco NJ, Wang FS, Su L (2015) Plasmacytoid dendritic cells promote HIV-1-induced group 3 innate lymphoid cell depletion. J Clin Invest 125(9):3692–3703PubMedPubMedCentralCrossRef Zhang Z, Cheng L, Zhao J, Li G, Zhang L, Chen W, Nie W, Reszka-Blanco NJ, Wang FS, Su L (2015) Plasmacytoid dendritic cells promote HIV-1-induced group 3 innate lymphoid cell depletion. J Clin Invest 125(9):3692–3703PubMedPubMedCentralCrossRef
140.
go back to reference Xu H, Feely SL, Wang X, Liu DX, Borda JT, Dufour J, Li W, Aye PP, Doxiadis GG, Khosla C, Veazey RS, Sestak K (2013) Gluten-sensitive enteropathy coincides with decreased capability of intestinal T cells to secrete IL-17 and IL-22 in a macaque model for celiac disease. Clinical immunology (Orlando, Fla) 147(1):40–49. https://doi.org/10.1016/j.clim.2013.02.012 CrossRef Xu H, Feely SL, Wang X, Liu DX, Borda JT, Dufour J, Li W, Aye PP, Doxiadis GG, Khosla C, Veazey RS, Sestak K (2013) Gluten-sensitive enteropathy coincides with decreased capability of intestinal T cells to secrete IL-17 and IL-22 in a macaque model for celiac disease. Clinical immunology (Orlando, Fla) 147(1):40–49. https://​doi.​org/​10.​1016/​j.​clim.​2013.​02.​012 CrossRef
Metadata
Title
Orchestration of intestinal homeostasis and tolerance by group 3 innate lymphoid cells
Publication date
01-07-2018
Published in
Seminars in Immunopathology / Issue 4/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-018-0687-8

Other articles of this Issue 4/2018

Seminars in Immunopathology 4/2018 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.