nach oben

Seminars in Immunopathology

Erschienen in:

22.03.2018 | Review

Innate lymphoid cells in autoimmunity and chronic inflammatory diseases

verfasst von: Tingting Xiong, Jan-Eric Turner

Erschienen in: Seminars in Immunopathology | Ausgabe 4/2018

Einloggen, um Zugang zu erhalten

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.

Cho JH, Gregersen PK (2011) Genomics and the multifactorial nature of human autoimmune disease. N Engl J Med 365:1612–1623. https://doi.org/10.1056/NEJMra1100030 CrossRefPubMed

Park H, Bourla AB, Kastner DL, Colbert RA, Siegel RM (2012) Lighting the fires within: the cell biology of autoinflammatory diseases. Nat Rev Immunol 12:570–580. https://doi.org/10.1038/nri3261 CrossRefPubMedPubMedCentral

Artis D, Spits H (2015) The biology of innate lymphoid cells. Nature 517:293–301. https://doi.org/10.1038/nature14189 CrossRefPubMed

Eberl G, Colonna M, Di Santo JP, McKenzie AN (2015) Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 348:aaa6566. https://doi.org/10.1126/science.aaa6566 CrossRefPubMedPubMedCentral

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 13:145–149. https://doi.org/10.1038/nri3365 CrossRefPubMed

Eberl G, Di Santo JP, Vivier E (2015) The brave new world of innate lymphoid cells. Nat Immunol 16:1–5. https://doi.org/10.1038/ni.3059 CrossRefPubMed

Mebius RE, Rennert P, Weissman IL (1997) Developing lymph nodes collect CD4+CD3- LTbeta+ cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7:493–504 https://doi.org/S1074-7613(00)80371-4 CrossRefPubMed

Spits H, Bernink JH, Lanier L (2016) NK cells and type 1 innate lymphoid cells: partners in host defense. Nat Immunol 17:758–764. https://doi.org/10.1038/ni.3482 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

10.

Fuchs A, Vermi W, Lee JS, Lonardi S, Gilfillan S, Newberry RD, Cella M, Colonna M (2013) Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-gamma-producing cells. Immunity 38:769–781. https://doi.org/10.1016/j.immuni.2013.02.010 CrossRefPubMedPubMedCentral

11.

Gasteiger G, Rudensky AY (2014) Interactions between innate and adaptive lymphocytes. Nat Rev Immunol 14:631–639. https://doi.org/10.1038/nri3726 CrossRefPubMedPubMedCentral

12.

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.

Blanco FJ, Moricke R, Dokoupilova E, Codding C, Neal J, Andersson M, Rohrer S, Richards H (2017) Secukinumab in active rheumatoid arthritis: a phase III randomized, double-blind, active comparator- and placebo-controlled study. Arthritis Rheumatol 69:1144–1153. https://doi.org/10.1002/art.40070 CrossRefPubMed

14.

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.

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

16.

Papi A, Brightling C, Pedersen SE, Reddel HK (2017) Asthma. Lancet. https://doi.org/10.1016/S0140-6736(17)33311-1 CrossRef

17.

Gieseck RL 3rd, Wilson MS, Wynn TA (2017) Type 2 immunity in tissue repair and fibrosis. Nat Rev Immunol 18:62–76. https://doi.org/10.1038/nri.2017.90 CrossRefPubMed

18.

Mjosberg JM, Trifari S, Crellin NK, Peters CP, van Drunen CM, Piet B, Fokkens WJ, Cupedo T, Spits H (2011) Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 12:1055–1062. https://doi.org/10.1038/ni.2104 CrossRefPubMed

19.

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

20.

Dendrou CA, Fugger L, Friese MA (2015) Immunopathology of multiple sclerosis. Nat Rev Immunol 15:545–558. https://doi.org/10.1038/nri3871 CrossRefPubMed

21.

Mair F, Becher B (2014) Thy1+ Sca1+ innate lymphoid cells infiltrate the CNS during autoimmune inflammation, but do not contribute to disease development. Eur J Immunol 44:37–45. https://doi.org/10.1002/eji.201343653 CrossRefPubMed

22.

Hatfield JK, Brown MA (2015) Group 3 innate lymphoid cells accumulate and exhibit disease-induced activation in the meninges in EAE. Cell Immunol 297:69–79. https://doi.org/10.1016/j.cellimm.2015.06.006 CrossRefPubMed

23.

Kwong B, Rua R, Gao Y, Flickinger J Jr, Wang Y, Kruhlak MJ, Zhu J, Vivier E, McGavern DB, Lazarevic V (2017) T-bet-dependent NKp46+ innate lymphoid cells regulate the onset of TH17-induced neuroinflammation. Nat Immunol 18:1117–1127. https://doi.org/10.1038/ni.3816 CrossRefPubMedPubMedCentral

24.

Russi AE, Walker-Caulfield ME, Ebel ME, Brown MA (2015) Cutting edge: c-kit signaling differentially regulates type 2 innate lymphoid cell accumulation and susceptibility to central nervous system demyelination in male and female SJL mice. J Immunol 194:5609–5613. https://doi.org/10.4049/jimmunol.1500068 CrossRefPubMedPubMedCentral

25.

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

26.

Milovanovic M, Volarevic V, Ljujic B, Radosavljevic G, Jovanovic I, Arsenijevic N, Lukic ML (2012) Deletion of IL-33R (ST2) abrogates resistance to EAE in BALB/C mice by enhancing polarization of APC to inflammatory phenotype. PLoS One 7:e45225. https://doi.org/10.1371/journal.pone.0045225 CrossRefPubMedPubMedCentral

27.

Gadani SP, Smirnov I, Smith AT, Overall CC, Kipnis J (2017) Characterization of meningeal type 2 innate lymphocytes and their response to CNS injury. J Exp Med 214:285–296. https://doi.org/10.1084/jem.20161982 CrossRefPubMedPubMedCentral

28.

Perry JS, Han S, Xu Q, Herman ML, Kennedy LB, Csako G, Bielekova B (2012) Inhibition of LTi cell development by CD25 blockade is associated with decreased intrathecal inflammation in multiple sclerosis. Sci Transl Med 4:145ra106. https://doi.org/10.1126/scitranslmed.3004140 CrossRefPubMed

29.

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

30.

Gross CC, Ahmetspahic D, Ruck T, Schulte-Mecklenbeck A, Schwarte K, Jorgens S, Scheu S, Windhagen S, Graefe B, Melzer N, Klotz L, Arolt V, Wiendl H, Meuth SG, Alferink J (2016) Alemtuzumab treatment alters circulating innate immune cells in multiple sclerosis. Neurol Neuroimmunol Neuroinflamm 3:e289. https://doi.org/10.1212/NXI.0000000000000289 CrossRefPubMedPubMedCentral

31.

Gillard GO, Saenz SA, Huss DJ, Fontenot JD (2016) Circulating innate lymphoid cells are unchanged in response to DAC HYP therapy. J Neuroimmunol 294:41–45. https://doi.org/10.1016/j.jneuroim.2016.03.008 CrossRefPubMed

32.

Lin YC, Winokur P, Blake A, Wu T, Romm E, Bielekova B (2015) Daclizumab reverses intrathecal immune cell abnormalities in multiple sclerosis. Ann Clin Transl Neurol 2:445–455. https://doi.org/10.1002/acn3.181 CrossRefPubMedPubMedCentral

33.

Abraham C, Cho JH (2009) Inflammatory bowel disease. N Engl J Med 361:2066–2078. https://doi.org/10.1056/NEJMra0804647 CrossRefPubMedPubMedCentral

34.

Neurath MF (2014) Cytokines in inflammatory bowel disease. Nat Rev Immunol 14:329–342. https://doi.org/10.1038/nri3661 CrossRefPubMed

35.

Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA (2008) Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 29:947–957. https://doi.org/10.1016/j.immuni.2008.11.003 CrossRefPubMedPubMedCentral

36.

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 29:958–970. https://doi.org/10.1016/j.immuni.2008.11.001 CrossRefPubMed

37.

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 10:83–91. https://doi.org/10.1038/ni.1684 CrossRefPubMed

38.

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

39.

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 457:722–725. https://doi.org/10.1038/nature07537 CrossRefPubMed

40.

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

41.

Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA, Hoyler T, Flach M, Bengsch B, Thimme R, Holscher C, Honig M, Pannicke U, Schwarz K, Ware CF, Finke D, Diefenbach A (2010) Regulated expression of nuclear receptor RORgammat confers distinct functional fates to NK cell receptor-expressing RORgammat(+) innate lymphocytes. Immunity 33:736–751. https://doi.org/10.1016/j.immuni.2010.10.017 CrossRefPubMedPubMedCentral

42.

Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, Maloy KJ, Powrie F (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464:1371–1375. https://doi.org/10.1038/nature08949 CrossRefPubMedPubMedCentral

43.

Pearson C, Thornton EE, McKenzie B, Schaupp AL, Huskens N, Griseri T, West N, Tung S, Seddon BP, Uhlig HH, Powrie F (2016) ILC3 GM-CSF production and mobilisation orchestrate acute intestinal inflammation. elife 5:e10066. https://doi.org/10.7554/eLife.10066 PubMedPubMedCentralCrossRef

44.

Powell N, Walker AW, Stolarczyk E, Canavan JB, Gokmen MR, Marks E, Jackson I, Hashim A, Curtis MA, Jenner RG, Howard JK, Parkhill J, MacDonald TT, Lord GM (2012) The transcription factor T-bet regulates intestinal inflammation mediated by interleukin-7 receptor+ innate lymphoid cells. Immunity 37:674–684. https://doi.org/10.1016/j.immuni.2012.09.008 CrossRefPubMedPubMedCentral

45.

Monticelli LA, Osborne LC, Noti M, Tran SV, Zaiss DM, Artis D (2015) IL-33 promotes an innate immune pathway of intestinal tissue protection dependent on amphiregulin-EGFR interactions. Proc Natl Acad Sci U S A 112:10762–10767. https://doi.org/10.1073/pnas.1509070112 CrossRefPubMedPubMedCentral

46.

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.

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.

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.

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.

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

51.

Geremia A, Arancibia-Carcamo CV, Fleming MP, Rust N, Singh B, Mortensen NJ, Travis SP, Powrie F (2011) IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J Exp Med 208:1127–1133. https://doi.org/10.1084/jem.20101712 CrossRefPubMedPubMedCentral

52.

Longman RS, Diehl GE, Victorio DA, Huh JR, Galan C, Miraldi ER, Swaminath A, Bonneau R, Scherl EJ, Littman DR (2014) CX(3)CR1(+) mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J Exp Med 211:1571–1583. https://doi.org/10.1084/jem.20140678 CrossRefPubMedPubMedCentral

53.

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

54.

Ohne Y, Silver JS, Thompson-Snipes L, Collet MA, Blanck JP, Cantarel BL, Copenhaver AM, Humbles AA, Liu YJ (2016) IL-1 is a critical regulator of group 2 innate lymphoid cell function and plasticity. Nat Immunol 17:646–655. https://doi.org/10.1038/ni.3447 CrossRefPubMed

55.

Lim AI, Menegatti S, Bustamante J, Le Bourhis L, Allez M, Rogge L, Casanova JL, Yssel H, Di Santo JP (2016) IL-12 drives functional plasticity of human group 2 innate lymphoid cells. J Exp Med 213:569–583. https://doi.org/10.1084/jem.20151750 CrossRefPubMedPubMedCentral

56.

Silver JS, Kearley J, Copenhaver AM, Sanden C, Mori M, Yu L, Pritchard GH, Berlin AA, Hunter CA, Bowler R, Erjefalt JS, Kolbeck R, Humbles AA (2016) Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nat Immunol 17:626–635. https://doi.org/10.1038/ni.3443 CrossRefPubMedPubMedCentral

57.

Alwan W, Nestle FO (2015) Pathogenesis and treatment of psoriasis: exploiting pathophysiological pathways for precision medicine. Clin Exp Rheumatol 33:S2–S6PubMed

58.

Hawkes JE, Chan TC, Krueger JG (2017) Psoriasis pathogenesis and the development of novel targeted immune therapies. J Allergy Clin Immunol 140:645–653. https://doi.org/10.1016/j.jaci.2017.07.004 CrossRefPubMedPubMedCentral

59.

Pantelyushin S, Haak S, Ingold B, Kulig P, Heppner FL, Navarini AA, Becher B (2012) Rorgammat+ innate lymphocytes and gammadelta T cells initiate psoriasiform plaque formation in mice. J Clin Invest 122:2252–2256. https://doi.org/10.1172/JCI61862 CrossRefPubMedPubMedCentral

60.

Villanova F, Flutter B, Tosi I, Grys K, Sreeneebus H, Perera GK, Chapman A, Smith CH, Di Meglio P, Nestle FO (2014) Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J Invest Dermatol 134:984–991. https://doi.org/10.1038/jid.2013.477 CrossRefPubMed

61.

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

62.

Bruggen MC, Bauer WM, Reininger B, Clim E, Captarencu C, Steiner GE, Brunner PM, Meier B, French LE, Stingl G (2016) In situ mapping of innate lymphoid cells in human skin: evidence for remarkable differences between normal and inflamed skin. J Invest Dermatol 136:2396–2405. https://doi.org/10.1016/j.jid.2016.07.017 CrossRefPubMed

63.

Dyring-Andersen B, Geisler C, Agerbeck C, Lauritsen JP, Gudjonsdottir SD, Skov L, Bonefeld CM (2014) Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br J Dermatol 170:609–616. https://doi.org/10.1111/bjd.12658 CrossRefPubMed

64.

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

65.

Rak GD, Osborne LC, Siracusa MC, Kim BS, Wang K, Bayat A, Artis D, Volk SW (2016) IL-33-dependent group 2 innate lymphoid cells promote cutaneous wound healing. J Invest Dermatol 136:487–496. https://doi.org/10.1038/JID.2015.406 CrossRefPubMedPubMedCentral

66.

Sieper J, Poddubnyy D (2017) Axial spondyloarthritis. Lancet 390:73–84. https://doi.org/10.1016/S0140-6736(16)31591-4 CrossRefPubMed

67.

Cuthbert RJ, Fragkakis EM, Dunsmuir R, Li Z, Coles M, Marzo-Ortega H, Giannoudis PV, Jones E, El-Sherbiny YM, McGonagle D (2017) Brief report: group 3 innate lymphoid cells in human enthesis. Arthritis Rheumatol 69:1816–1822. https://doi.org/10.1002/art.40150 CrossRefPubMed

68.

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.

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.

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

71.

Malmstrom V, Catrina AI, Klareskog L (2017) The immunopathogenesis of seropositive rheumatoid arthritis: from triggering to targeting. Nat Rev Immunol 17:60–75. https://doi.org/10.1038/nri.2016.124 CrossRefPubMed

72.

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

73.

Ren J, Feng Z, Lv Z, Chen X, Li J (2011) Natural killer-22 cells in the synovial fluid of patients with rheumatoid arthritis are an innate source of interleukin 22 and tumor necrosis factor-alpha. J Rheumatol 38:2112–2118. https://doi.org/10.3899/jrheum.101377 CrossRefPubMed

74.

Koo J, Kim S, Jung WJ, Lee YE, Song GG, Kim KS, Kim MY (2013) Increased lymphocyte infiltration in rheumatoid arthritis is correlated with an increase in LTi-like cells in synovial fluid. Immune Netw 13:240–248. https://doi.org/10.4110/in.2013.13.6.240 CrossRefPubMedPubMedCentral

75.

Pineda MA, Rodgers DT, Al-Riyami L, Harnett W, Harnett MM (2014) ES-62 protects against collagen-induced arthritis by resetting interleukin-22 toward resolution of inflammation in the joints. Arthritis Rheumatol 66:1492–1503. https://doi.org/10.1002/art.38392 CrossRefPubMedPubMedCentral

76.

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

77.

Turner JE, Morrison PJ, Wilhelm C, Wilson M, Ahlfors H, Renauld JC, Panzer U, Helmby H, Stockinger B (2013) IL-9-mediated survival of type 2 innate lymphoid cells promotes damage control in helminth-induced lung inflammation. J Exp Med 210:2951–2965. https://doi.org/10.1084/jem.20130071 CrossRefPubMedPubMedCentral

78.

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

79.

Braudeau C, Amouriaux K, Neel A, Herbreteau G, Salabert N, Rimbert M, Martin JC, Hemont C, Hamidou M, Josien R (2016) Persistent deficiency of circulating mucosal-associated invariant T (MAIT) cells in ANCA-associated vasculitis. J Autoimmun 70:73–79. https://doi.org/10.1016/j.jaut.2016.03.015 CrossRefPubMed

80.

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

81.

Asano Y (2017) Systemic sclerosis. J Dermatol 45:128–138. https://doi.org/10.1111/1346-8138.14153 CrossRefPubMed

82.

Roan F, Stoklasek TA, Whalen E, Molitor JA, Bluestone JA, Buckner JH, Ziegler SF (2016) CD4+ group 1 innate lymphoid cells (ILC) form a functionally distinct ILC subset that is increased in systemic sclerosis. J Immunol 196:2051–2062. https://doi.org/10.4049/jimmunol.1501491 CrossRefPubMedPubMedCentral

83.

Wohlfahrt T, Usherenko S, Englbrecht M, Dees C, Weber S, Beyer C, Gelse K, Distler O, Schett G, Distler JH, Ramming A (2016) Type 2 innate lymphoid cell counts are increased in patients with systemic sclerosis and correlate with the extent of fibrosis. Ann Rheum Dis 75:623–626. https://doi.org/10.1136/annrheumdis-2015-207388 CrossRefPubMed

84.

McHedlidze T, Waldner M, Zopf S, Walker J, Rankin AL, Schuchmann M, Voehringer D, McKenzie AN, Neurath MF, Pflanz S, Wirtz S (2013) Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 39:357–371. https://doi.org/10.1016/j.immuni.2013.07.018 CrossRefPubMedPubMedCentral

85.

Hams E, Armstrong ME, Barlow JL, Saunders SP, Schwartz C, Cooke G, Fahy RJ, Crotty TB, Hirani N, Flynn RJ, Voehringer D, McKenzie AN, Donnelly SC, Fallon PG (2014) IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci U S A 111:367–372. https://doi.org/10.1073/pnas.1315854111 CrossRefPubMed

86.

Gaffen SL, Jain R, Garg AV, Cua DJ (2014) The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol 14:585–600. https://doi.org/10.1038/nri3707 CrossRefPubMedPubMedCentral

87.

Riedel JH, Becker M, Kopp K, Duster M, Brix SR, Meyer-Schwesinger C, Kluth LA, Gnirck AC, Attar M, Krohn S, Fehse B, Stahl RAK, Panzer U, Turner JE (2017) IL-33-mediated expansion of type 2 innate lymphoid cells protects from progressive glomerulosclerosis. J Am Soc Nephrol 28:2068–2080. https://doi.org/10.1681/ASN.2016080877 CrossRefPubMedPubMedCentral

88.

Kiss EA, Diefenbach A (2012) Role of the aryl hydrocarbon receptor in controlling maintenance and functional programs of RORgammat(+) innate lymphoid cells and intraepithelial lymphocytes. Front Immunol 3:124. https://doi.org/10.3389/fimmu.2012.00124 CrossRefPubMedPubMedCentral

89.

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 343:432–437. https://doi.org/10.1126/science.1247606 CrossRefPubMedPubMedCentral

Titel: Innate lymphoid cells in autoimmunity and chronic inflammatory diseases
verfasst von: Tingting Xiong
Jan-Eric Turner
Publikationsdatum: 22.03.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Seminars in Immunopathology / Ausgabe 4/2018
Print ISSN: 1863-2297
Elektronische ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-018-0670-4

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

Echinokokkose medikamentös behandeln oder operieren?

06.05.2024 DCK 2024 Kongressbericht

Die Therapie von Echinokokkosen sollte immer in spezialisierten Zentren erfolgen. Eine symptomlose Echinokokkose kann – egal ob von Hunde- oder Fuchsbandwurm ausgelöst – konservativ erfolgen. Wenn eine Op. nötig ist, kann es sinnvoll sein, vorher Zysten zu leeren und zu desinfizieren.

Aquatherapie bei Fibromyalgie wirksamer als Trockenübungen

03.05.2024 Fibromyalgiesyndrom Nachrichten

Bewegungs-, Dehnungs- und Entspannungsübungen im Wasser lindern die Beschwerden von Patientinnen mit Fibromyalgie besser als das Üben auf trockenem Land. Das geht aus einer spanisch-brasilianischen Vergleichsstudie hervor.

Wo hapert es noch bei der Umsetzung der POMGAT-Leitlinie?

03.05.2024 DCK 2024 Kongressbericht

Seit November 2023 gibt es evidenzbasierte Empfehlungen zum perioperativen Management bei gastrointestinalen Tumoren (POMGAT) auf S3-Niveau. Vieles wird schon entsprechend der Empfehlungen durchgeführt. Wo es im Alltag noch hapert, zeigt eine Umfrage in einem Klinikverbund.

Das Risiko für Vorhofflimmern in der Bevölkerung steigt

02.05.2024 Vorhofflimmern Nachrichten

Das Risiko, im Lauf des Lebens an Vorhofflimmern zu erkranken, ist in den vergangenen 20 Jahren gestiegen: Laut dänischen Zahlen wird es drei von zehn Personen treffen. Das hat Folgen weit über die Schlaganfallgefährdung hinaus.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2018

ILC2s in infectious diseases and organ-specific fibrosis

Memory responses of innate lymphocytes and parallels with T cells

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

Innate lymphoid cells: key players in tissue-specific immunity

AHR signaling in the development and function of intestinal immune cells and beyond