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Published in: Seminars in Immunopathology 4/2018

01-07-2018 | Review

Innate lymphoid cells in autoimmunity and chronic inflammatory diseases

Authors: Tingting Xiong, Jan-Eric Turner

Published in: Seminars in Immunopathology | Issue 4/2018

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Abstract

Abnormal activation of the innate immune system is a common feature of autoimmune and chronic inflammatory diseases. Since their identification as a separate family of leukocytes, innate lymphoid cells (ILCs) have emerged as important effector cells of the innate immune system. Alterations in ILC function and subtype distribution have been observed in a variety of immune-mediated diseases in humans and evidence from experimental models suggests a subtype specific role of ILCs in the pathophysiology of autoimmune inflammation. In this review, we discuss recent advances in the understanding of ILC biology in autoimmune and chronic inflammatory disorders, including multiple sclerosis, inflammatory bowel diseases, psoriasis, and rheumatic diseases, with a special focus on the potential of ILCs as therapeutic targets for the development of novel treatment strategies in humans.
Literature
9.
go back to reference Klose CSN, 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 157:340–356. https://doi.org/10.1016/j.cell.2014.03.030 CrossRefPubMed Klose CSN, 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 157:340–356. https://​doi.​org/​10.​1016/​j.​cell.​2014.​03.​030 CrossRefPubMed
12.
go back to reference Papp KA, Blauvelt A, Bukhalo M, Gooderham M, Krueger JG, Lacour JP, Menter A, Philipp S, Sofen H, Tyring S, Berner BR, Visvanathan S, Pamulapati C, Bennett N, Flack M, Scholl P, Padula SJ (2017) Risankizumab versus ustekinumab for moderate-to-severe plaque psoriasis. N Engl J Med 376:1551–1560. https://doi.org/10.1056/NEJMoa1607017 CrossRefPubMed Papp KA, Blauvelt A, Bukhalo M, Gooderham M, Krueger JG, Lacour JP, Menter A, Philipp S, Sofen H, Tyring S, Berner BR, Visvanathan S, Pamulapati C, Bennett N, Flack M, Scholl P, Padula SJ (2017) Risankizumab versus ustekinumab for moderate-to-severe plaque psoriasis. N Engl J Med 376:1551–1560. https://​doi.​org/​10.​1056/​NEJMoa1607017 CrossRefPubMed
13.
14.
go back to reference Baeten D, Baraliakos X, Braun J, Sieper J, Emery P, van der Heijde D, McInnes I, van Laar JM, Landewe R, Wordsworth P, Wollenhaupt J, Kellner H, Paramarta J, Wei J, Brachat A, Bek S, Laurent D, Li Y, Wang YA, Bertolino AP, Gsteiger S, Wright AM, Hueber W (2013) Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 382:1705–1713. https://doi.org/10.1016/S0140-6736(13)61134-4 CrossRefPubMed Baeten D, Baraliakos X, Braun J, Sieper J, Emery P, van der Heijde D, McInnes I, van Laar JM, Landewe R, Wordsworth P, Wollenhaupt J, Kellner H, Paramarta J, Wei J, Brachat A, Bek S, Laurent D, Li Y, Wang YA, Bertolino AP, Gsteiger S, Wright AM, Hueber W (2013) Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 382:1705–1713. https://​doi.​org/​10.​1016/​S0140-6736(13)61134-4 CrossRefPubMed
15.
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 336:1321–1325. https://doi.org/10.1126/science.1222551 CrossRefPubMedPubMedCentral 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 336:1321–1325. https://​doi.​org/​10.​1126/​science.​1222551 CrossRefPubMedPubMedCentral
19.
go back to reference Lim AI, Li Y, Lopez-Lastra S, Stadhouders R, Paul F, Casrouge A, Serafini N, Puel A, Bustamante J, Surace L, Masse-Ranson G, David E, Strick-Marchand H, Le Bourhis L, Cocchi R, Topazio D, Graziano P, Muscarella LA, Rogge L, Norel X, Sallenave JM, Allez M, Graf T, Hendriks RW, Casanova JL, Amit I, Yssel H, Di Santo JP (2017) Systemic human ILC precursors provide a substrate for tissue ILC differentiation. Cell 168:1086–1100.e10. https://doi.org/10.1016/j.cell.2017.02.021 CrossRefPubMed Lim AI, Li Y, Lopez-Lastra S, Stadhouders R, Paul F, Casrouge A, Serafini N, Puel A, Bustamante J, Surace L, Masse-Ranson G, David E, Strick-Marchand H, Le Bourhis L, Cocchi R, Topazio D, Graziano P, Muscarella LA, Rogge L, Norel X, Sallenave JM, Allez M, Graf T, Hendriks RW, Casanova JL, Amit I, Yssel H, Di Santo JP (2017) Systemic human ILC precursors provide a substrate for tissue ILC differentiation. Cell 168:1086–1100.e10. https://​doi.​org/​10.​1016/​j.​cell.​2017.​02.​021 CrossRefPubMed
25.
go back to reference Jiang HR, Milovanovic M, Allan D, Niedbala W, Besnard AG, Fukada SY, Alves-Filho JC, Togbe D, Goodyear CS, Linington C, Xu D, Lukic ML, Liew FY (2012) IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur J Immunol 42:1804–1814. https://doi.org/10.1002/eji.201141947 CrossRefPubMed Jiang HR, Milovanovic M, Allan D, Niedbala W, Besnard AG, Fukada SY, Alves-Filho JC, Togbe D, Goodyear CS, Linington C, Xu D, Lukic ML, Liew FY (2012) IL-33 attenuates EAE by suppressing IL-17 and IFN-gamma production and inducing alternatively activated macrophages. Eur J Immunol 42:1804–1814. https://​doi.​org/​10.​1002/​eji.​201141947 CrossRefPubMed
29.
go back to reference Gross CC, Schulte-Mecklenbeck A, Hanning U, Posevitz-Fejfar A, Korsukewitz C, Schwab N, Meuth SG, Wiendl H, Klotz L (2017) Distinct pattern of lesion distribution in multiple sclerosis is associated with different circulating T-helper and helper-like innate lymphoid cell subsets. Mult Scler 23:1025–1030. https://doi.org/10.1177/1352458516662726 CrossRefPubMed Gross CC, Schulte-Mecklenbeck A, Hanning U, Posevitz-Fejfar A, Korsukewitz C, Schwab N, Meuth SG, Wiendl H, Klotz L (2017) Distinct pattern of lesion distribution in multiple sclerosis is associated with different circulating T-helper and helper-like innate lymphoid cell subsets. Mult Scler 23:1025–1030. https://​doi.​org/​10.​1177/​1352458516662726​ CrossRefPubMed
38.
go back to reference Luci C, Reynders A, Ivanov II, Cognet C, Chiche L, Chasson L, Hardwigsen J, Anguiano E, Banchereau J, Chaussabel D, Dalod M, Littman DR, Vivier E, Tomasello E (2009) Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol 10:75–82. https://doi.org/10.1038/ni.1681 CrossRefPubMed Luci C, Reynders A, Ivanov II, Cognet C, Chiche L, Chasson L, Hardwigsen J, Anguiano E, Banchereau J, Chaussabel D, Dalod M, Littman DR, Vivier E, Tomasello E (2009) Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol 10:75–82. https://​doi.​org/​10.​1038/​ni.​1681 CrossRefPubMed
40.
go back to reference Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, Kleinschek M, Cua D, Di Santo JP, Eberl G (2011) RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 12:320–326. https://doi.org/10.1038/ni.2002 CrossRefPubMed Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, Kleinschek M, Cua D, Di Santo JP, Eberl G (2011) RORgammat+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 12:320–326. https://​doi.​org/​10.​1038/​ni.​2002 CrossRefPubMed
46.
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 17:179–186. https://doi.org/10.1038/ni.3332 CrossRefPubMed 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 17:179–186. https://​doi.​org/​10.​1038/​ni.​3332 CrossRefPubMed
47.
go back to reference Vely F, Barlogis V, Vallentin B, Neven B, Piperoglou C, Ebbo M, Perchet T, Petit M, Yessaad N, Touzot F, Bruneau J, Mahlaoui N, Zucchini N, Farnarier C, Michel G, Moshous D, Blanche S, Dujardin A, Spits H, Distler JH, Ramming A, Picard C, Golub R, Fischer A, Vivier E (2016) Evidence of innate lymphoid cell redundancy in humans. Nat Immunol 17:1291–1299. https://doi.org/10.1038/ni.3553 CrossRefPubMedPubMedCentral Vely F, Barlogis V, Vallentin B, Neven B, Piperoglou C, Ebbo M, Perchet T, Petit M, Yessaad N, Touzot F, Bruneau J, Mahlaoui N, Zucchini N, Farnarier C, Michel G, Moshous D, Blanche S, Dujardin A, Spits H, Distler JH, Ramming A, Picard C, Golub R, Fischer A, Vivier E (2016) Evidence of innate lymphoid cell redundancy in humans. Nat Immunol 17:1291–1299. https://​doi.​org/​10.​1038/​ni.​3553 CrossRefPubMedPubMedCentral
48.
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 139:882–892, 892 e881–883. https://doi.org/10.1053/j.gastro.2010.05.040 CrossRefPubMed 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 139:882–892, 892 e881–883. https://​doi.​org/​10.​1053/​j.​gastro.​2010.​05.​040 CrossRefPubMed
49.
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 14:221–229. https://doi.org/10.1038/ni.2534 CrossRefPubMed 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 14:221–229. https://​doi.​org/​10.​1038/​ni.​2534 CrossRefPubMed
50.
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 43:146–160. https://doi.org/10.1016/j.immuni.2015.06.019 CrossRefPubMed 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 43:146–160. https://​doi.​org/​10.​1016/​j.​immuni.​2015.​06.​019 CrossRefPubMed
53.
go back to reference Powell N, Lo JW, Biancheri P, Vossenkamper A, Pantazi E, Walker AW, Stolarczyk E, Ammoscato F, Goldberg R, Scott P, Canavan JB, Perucha E, Garrido-Mesa N, Irving PM, Sanderson JD, Hayee B, Howard JK, Parkhill J, MacDonald TT, Lord GM (2015) Interleukin 6 increases production of cytokines by colonic innate lymphoid cells in mice and patients with chronic intestinal inflammation. Gastroenterology 149:456–467e415. https://doi.org/10.1053/j.gastro.2015.04.017 CrossRefPubMedPubMedCentral Powell N, Lo JW, Biancheri P, Vossenkamper A, Pantazi E, Walker AW, Stolarczyk E, Ammoscato F, Goldberg R, Scott P, Canavan JB, Perucha E, Garrido-Mesa N, Irving PM, Sanderson JD, Hayee B, Howard JK, Parkhill J, MacDonald TT, Lord GM (2015) Interleukin 6 increases production of cytokines by colonic innate lymphoid cells in mice and patients with chronic intestinal inflammation. Gastroenterology 149:456–467e415. https://​doi.​org/​10.​1053/​j.​gastro.​2015.​04.​017 CrossRefPubMedPubMedCentral
56.
57.
go back to reference Alwan W, Nestle FO (2015) Pathogenesis and treatment of psoriasis: exploiting pathophysiological pathways for precision medicine. Clin Exp Rheumatol 33:S2–S6PubMed Alwan W, Nestle FO (2015) Pathogenesis and treatment of psoriasis: exploiting pathophysiological pathways for precision medicine. Clin Exp Rheumatol 33:S2–S6PubMed
61.
go back to reference Teunissen MBM, Munneke JM, Bernink JH, Spuls PI, Res PCM, Te Velde A, Cheuk S, Brouwer MWD, Menting SP, Eidsmo L, Spits H, Hazenberg MD, Mjosberg J (2014) Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR(+) ILC3 in lesional skin and blood of psoriasis patients. J Invest Dermatol 134:2351–2360. https://doi.org/10.1038/jid.2014.146 CrossRefPubMed Teunissen MBM, Munneke JM, Bernink JH, Spuls PI, Res PCM, Te Velde A, Cheuk S, Brouwer MWD, Menting SP, Eidsmo L, Spits H, Hazenberg MD, Mjosberg J (2014) Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR(+) ILC3 in lesional skin and blood of psoriasis patients. J Invest Dermatol 134:2351–2360. https://​doi.​org/​10.​1038/​jid.​2014.​146 CrossRefPubMed
64.
go back to reference Mora-Velandia LM, Castro-Escamilla O, Mendez AG, Aguilar-Flores C, Velazquez-Avila M, Tussie-Luna MI, Tellez-Sosa J, Maldonado-Garcia C, Jurado-Santacruz F, Ferat-Osorio E, Martinez-Barnetche J, Pelayo R, Bonifaz LC (2017) A human Lin− CD123+ CD127low population endowed with ILC features and migratory capabilities contributes to immunopathological hallmarks of psoriasis. Front Immunol 8:176. https://doi.org/10.3389/fimmu.2017.00176 CrossRefPubMedPubMedCentral Mora-Velandia LM, Castro-Escamilla O, Mendez AG, Aguilar-Flores C, Velazquez-Avila M, Tussie-Luna MI, Tellez-Sosa J, Maldonado-Garcia C, Jurado-Santacruz F, Ferat-Osorio E, Martinez-Barnetche J, Pelayo R, Bonifaz LC (2017) A human Lin− CD123+ CD127low population endowed with ILC features and migratory capabilities contributes to immunopathological hallmarks of psoriasis. Front Immunol 8:176. https://​doi.​org/​10.​3389/​fimmu.​2017.​00176 CrossRefPubMedPubMedCentral
68.
go back to reference Ciccia F, Guggino G, Rizzo A, Saieva L, Peralta S, Giardina A, Cannizzaro A, Sireci G, De Leo G, Alessandro R, Triolo G (2015) Type 3 innate lymphoid cells producing IL-17 and IL-22 are expanded in the gut, in the peripheral blood, synovial fluid and bone marrow of patients with ankylosing spondylitis. Ann Rheum Dis 74:1739–1747. https://doi.org/10.1136/annrheumdis-2014-206323 CrossRefPubMed Ciccia F, Guggino G, Rizzo A, Saieva L, Peralta S, Giardina A, Cannizzaro A, Sireci G, De Leo G, Alessandro R, Triolo G (2015) Type 3 innate lymphoid cells producing IL-17 and IL-22 are expanded in the gut, in the peripheral blood, synovial fluid and bone marrow of patients with ankylosing spondylitis. Ann Rheum Dis 74:1739–1747. https://​doi.​org/​10.​1136/​annrheumdis-2014-206323 CrossRefPubMed
69.
go back to reference Leijten EF, van Kempen TS, Boes M, Michels-van Amelsfort JM, Hijnen D, Hartgring SA, van Roon JA, Wenink MH, Radstake TR (2015) Brief report: enrichment of activated group 3 innate lymphoid cells in psoriatic arthritis synovial fluid. Arthritis Rheumatol 67:2673–2678. https://doi.org/10.1002/art.39261 CrossRefPubMed Leijten EF, van Kempen TS, Boes M, Michels-van Amelsfort JM, Hijnen D, Hartgring SA, van Roon JA, Wenink MH, Radstake TR (2015) Brief report: enrichment of activated group 3 innate lymphoid cells in psoriatic arthritis synovial fluid. Arthritis Rheumatol 67:2673–2678. https://​doi.​org/​10.​1002/​art.​39261 CrossRefPubMed
70.
go back to reference Triggianese P, Conigliaro P, Chimenti MS, Biancone L, Monteleone G, Perricone R, Monteleone I (2016) Evidence of IL-17 producing innate lymphoid cells in peripheral blood from patients with enteropathic spondyloarthritis. Clin Exp Rheumatol 34:1085–1093PubMed Triggianese P, Conigliaro P, Chimenti MS, Biancone L, Monteleone G, Perricone R, Monteleone I (2016) Evidence of IL-17 producing innate lymphoid cells in peripheral blood from patients with enteropathic spondyloarthritis. Clin Exp Rheumatol 34:1085–1093PubMed
72.
go back to reference Rodriguez-Carrio J, Hahnlein JS, Ramwadhdoebe TH, Semmelink JF, Choi IY, van Lienden KP, Maas M, Gerlag DM, Tak PP, Geijtenbeek TB, van Baarsen LG (2017) Brief report: altered innate lymphoid cell subsets in human lymph node biopsy specimens obtained during the at-risk and earliest phases of rheumatoid arthritis. Arthritis Rheumatol 69:70–76. https://doi.org/10.1002/art.39811 CrossRefPubMed Rodriguez-Carrio J, Hahnlein JS, Ramwadhdoebe TH, Semmelink JF, Choi IY, van Lienden KP, Maas M, Gerlag DM, Tak PP, Geijtenbeek TB, van Baarsen LG (2017) Brief report: altered innate lymphoid cell subsets in human lymph node biopsy specimens obtained during the at-risk and earliest phases of rheumatoid arthritis. Arthritis Rheumatol 69:70–76. https://​doi.​org/​10.​1002/​art.​39811 CrossRefPubMed
76.
go back to reference Rauber S, Luber M, Weber S, Maul L, Soare A, Wohlfahrt T, Lin NY, Dietel K, Bozec A, Herrmann M, Kaplan MH, Weigmann B, Zaiss MM, Fearon U, Veale DJ, Canete JD, Distler O, Rivellese F, Pitzalis C, Neurath MF, McKenzie ANJ, Wirtz S, Schett G, Distler JHW, Ramming A (2017) Resolution of inflammation by interleukin-9-producing type 2 innate lymphoid cells. Nat Med 23:938–944. https://doi.org/10.1038/nm.4373 PubMedPubMedCentralCrossRef Rauber S, Luber M, Weber S, Maul L, Soare A, Wohlfahrt T, Lin NY, Dietel K, Bozec A, Herrmann M, Kaplan MH, Weigmann B, Zaiss MM, Fearon U, Veale DJ, Canete JD, Distler O, Rivellese F, Pitzalis C, Neurath MF, McKenzie ANJ, Wirtz S, Schett G, Distler JHW, Ramming A (2017) Resolution of inflammation by interleukin-9-producing type 2 innate lymphoid cells. Nat Med 23:938–944. https://​doi.​org/​10.​1038/​nm.​4373 PubMedPubMedCentralCrossRef
78.
go back to reference Biton J, Khaleghparast Athari S, Thiolat A, Santinon F, Lemeiter D, Herve R, Delavallee L, Levescot A, Roga S, Decker P, Girard JP, Herbelin A, Boissier MC, Bessis N (2016) In vivo expansion of activated Foxp3+ regulatory T cells and establishment of a type 2 immune response upon IL-33 treatment protect against experimental arthritis. J Immunol 197:1708–1719. https://doi.org/10.4049/jimmunol.1502124 CrossRefPubMed Biton J, Khaleghparast Athari S, Thiolat A, Santinon F, Lemeiter D, Herve R, Delavallee L, Levescot A, Roga S, Decker P, Girard JP, Herbelin A, Boissier MC, Bessis N (2016) In vivo expansion of activated Foxp3+ regulatory T cells and establishment of a type 2 immune response upon IL-33 treatment protect against experimental arthritis. J Immunol 197:1708–1719. https://​doi.​org/​10.​4049/​jimmunol.​1502124 CrossRefPubMed
80.
go back to reference Fazekas B, Moreno-Olivera A, Kelly Y, O'Hara P, Murray S, Kennedy A, Conlon N, Scott J, Melo AM, Hickey FB, Dooley D, O'Brien EC, Moran S, Doherty DG, Little MA (2017) Alterations in circulating lymphoid cell populations in systemic small vessel vasculitis are non-specific manifestations of renal injury. Clin Exp Immunol 191:180–188. https://doi.org/10.1111/cei.13058 CrossRefPubMed Fazekas B, Moreno-Olivera A, Kelly Y, O'Hara P, Murray S, Kennedy A, Conlon N, Scott J, Melo AM, Hickey FB, Dooley D, O'Brien EC, Moran S, Doherty DG, Little MA (2017) Alterations in circulating lymphoid cell populations in systemic small vessel vasculitis are non-specific manifestations of renal injury. Clin Exp Immunol 191:180–188. https://​doi.​org/​10.​1111/​cei.​13058 CrossRefPubMed
Metadata
Title
Innate lymphoid cells in autoimmunity and chronic inflammatory diseases
Authors
Tingting Xiong
Jan-Eric Turner
Publication date
01-07-2018
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 4/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-018-0670-4

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