Skip to main content
Erschienen in: Seminars in Immunopathology 3/2019

15.04.2019 | Review

The role of invariant T cells in inflammation of the skin and airways

verfasst von: Kwok Ho Yip, Magdalene Papadopoulos, Harshita Pant, Damon J. Tumes

Erschienen in: Seminars in Immunopathology | Ausgabe 3/2019

Einloggen, um Zugang zu erhalten

Abstract

Invariant and semi-invariant T cells are emerging as important regulators of host environment interactions at barrier tissues such as the airway and skin. In contrast to conventional T cells, invariant natural killer T (iNKT) cells and mucosal associated invariant T (MAIT) cells express T cell receptors of very limited diversity. iNKT and MAIT cells recognise antigens presented by the MHC class 1-like monomorphic molecules CD1d and MR1, respectively. Both iNKT cells and MAIT cells have been identified in the skin and airways and can rapidly produce cytokines after activation. Numerous studies have implicated iNKT cells in the pathology of both skin and airway disease, but conflicting evidence in human disease means that more studies are necessary to resolve the exact roles of iNKT in inflammation. The functions of MAIT cells in skin and lung inflammation are even less well defined. We herein describe the current literature on iNKT and MAIT cells in allergic and non-allergic skin diseases (dermatitis and psoriasis) and airway diseases (asthma, chronic obstructive pulmonary disease, rhinitis, and chronic rhinosinusitis).
Literatur
1.
Zurück zum Zitat Tumes DJ, Papadopoulos M, Endo Y, Onodera A, Hirahara K, Nakayama T (2017) Epigenetic regulation of T-helper cell differentiation, memory, and plasticity in allergic asthma. Immunol Rev 278(1):8–19CrossRefPubMed Tumes DJ, Papadopoulos M, Endo Y, Onodera A, Hirahara K, Nakayama T (2017) Epigenetic regulation of T-helper cell differentiation, memory, and plasticity in allergic asthma. Immunol Rev 278(1):8–19CrossRefPubMed
2.
Zurück zum Zitat Arase H, Arase N, Ogasawara K, Good RA, Onoe K (1992) An NK1.1+ CD4+8- single-positive thymocyte subpopulation that expresses a highly skewed T-cell antigen receptor V beta family. Proc Natl Acad Sci U S A 89(14):6506–6510CrossRefPubMedPubMedCentral Arase H, Arase N, Ogasawara K, Good RA, Onoe K (1992) An NK1.1+ CD4+8- single-positive thymocyte subpopulation that expresses a highly skewed T-cell antigen receptor V beta family. Proc Natl Acad Sci U S A 89(14):6506–6510CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Hayakawa K, Lin BT, Hardy RR (1992) Murine thymic CD4+ T cell subsets: a subset (Thy0) that secretes diverse cytokines and overexpresses the V beta 8 T cell receptor gene family. J Exp Med 176(1):269–274CrossRefPubMed Hayakawa K, Lin BT, Hardy RR (1992) Murine thymic CD4+ T cell subsets: a subset (Thy0) that secretes diverse cytokines and overexpresses the V beta 8 T cell receptor gene family. J Exp Med 176(1):269–274CrossRefPubMed
4.
Zurück zum Zitat Koseki H, Asano H, Inaba T, Miyashita N, Moriwaki K, Lindahl KF, Mizutani Y, Imai K, Taniguchi M (1991) Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice. Proc Natl Acad Sci U S A 88(17):7518–7522CrossRefPubMedPubMedCentral Koseki H, Asano H, Inaba T, Miyashita N, Moriwaki K, Lindahl KF, Mizutani Y, Imai K, Taniguchi M (1991) Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice. Proc Natl Acad Sci U S A 88(17):7518–7522CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Lantz O, Bendelac A (1994) An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med 180(3):1097–1106CrossRefPubMed Lantz O, Bendelac A (1994) An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med 180(3):1097–1106CrossRefPubMed
6.
Zurück zum Zitat Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, Ohmi Y, Sato M, Takeda K, Okumura K, van Kaer L, Kawano T, Taniguchi M, Nishimura T (1999) The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 189(7):1121–1128CrossRefPubMedPubMedCentral Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, Ohmi Y, Sato M, Takeda K, Okumura K, van Kaer L, Kawano T, Taniguchi M, Nishimura T (1999) The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 189(7):1121–1128CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat de Leit-Moraes MC, Hameg A, Arnould A, Machavoine F, Koezuka Y, Schneider E et al (1999) A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement. J Immunol 163(11):5871–5876 de Leit-Moraes MC, Hameg A, Arnould A, Machavoine F, Koezuka Y, Schneider E et al (1999) A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement. J Immunol 163(11):5871–5876
8.
Zurück zum Zitat Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D, Nussenblatt RB, Caspi RR (2008) Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol 180(8):5167–5171CrossRefPubMed Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D, Nussenblatt RB, Caspi RR (2008) Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol 180(8):5167–5171CrossRefPubMed
9.
Zurück zum Zitat Terashima A, Watarai H, Inoue S, Sekine E, Nakagawa R, Hase K, Iwamura C, Nakajima H, Nakayama T, Taniguchi M (2008) A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity. J Exp Med 205(12):2727–2733CrossRefPubMedPubMedCentral Terashima A, Watarai H, Inoue S, Sekine E, Nakagawa R, Hase K, Iwamura C, Nakajima H, Nakayama T, Taniguchi M (2008) A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity. J Exp Med 205(12):2727–2733CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Bourgeois E, Van LP, Samson M, Diem S, Barra A, Roga S et al (2009) The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39(4):1046–1055CrossRefPubMed Bourgeois E, Van LP, Samson M, Diem S, Barra A, Roga S et al (2009) The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39(4):1046–1055CrossRefPubMed
11.
Zurück zum Zitat Kim CH, Johnston B, Butcher EC (2002) Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among V alpha 24(+)V beta 11(+) NKT cell subsets with distinct cytokine-producing capacity. Blood. 100(1):11–16CrossRefPubMed Kim CH, Johnston B, Butcher EC (2002) Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among V alpha 24(+)V beta 11(+) NKT cell subsets with distinct cytokine-producing capacity. Blood. 100(1):11–16CrossRefPubMed
12.
Zurück zum Zitat Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E, Koseki H, Taniguchi M (1997) CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 278(5343):1626–1629CrossRefPubMed Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E, Koseki H, Taniguchi M (1997) CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 278(5343):1626–1629CrossRefPubMed
13.
Zurück zum Zitat Meyer EH, Goya S, Akbari O, Berry GJ, Savage PB, Kronenberg M, Nakayama T, DeKruyff RH, Umetsu DT (2006) Glycolipid activation of invariant T cell receptor+ NK T cells is sufficient to induce airway hyperreactivity independent of conventional CD4+ T cells. Proc Natl Acad Sci U S A 103(8):2782–2787CrossRefPubMedPubMedCentral Meyer EH, Goya S, Akbari O, Berry GJ, Savage PB, Kronenberg M, Nakayama T, DeKruyff RH, Umetsu DT (2006) Glycolipid activation of invariant T cell receptor+ NK T cells is sufficient to induce airway hyperreactivity independent of conventional CD4+ T cells. Proc Natl Acad Sci U S A 103(8):2782–2787CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Albacker LA, Chaudhary V, Chang YJ, Kim HY, Chuang YT, Pichavant M, DeKruyff RH, Savage PB, Umetsu DT (2013) Invariant natural killer T cells recognize a fungal glycosphingolipid that can induce airway hyperreactivity. Nat Med 19(10):1297–1304CrossRefPubMedPubMedCentral Albacker LA, Chaudhary V, Chang YJ, Kim HY, Chuang YT, Pichavant M, DeKruyff RH, Savage PB, Umetsu DT (2013) Invariant natural killer T cells recognize a fungal glycosphingolipid that can induce airway hyperreactivity. Nat Med 19(10):1297–1304CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Kinjo Y, Illarionov P, Vela JL, Pei B, Girardi E, Li X, Li Y, Imamura M, Kaneko Y, Okawara A, Miyazaki Y, Gómez-Velasco A, Rogers P, Dahesh S, Uchiyama S, Khurana A, Kawahara K, Yesilkaya H, Andrew PW, Wong CH, Kawakami K, Nizet V, Besra GS, Tsuji M, Zajonc DM, Kronenberg M (2011) Invariant natural killer T cells recognize glycolipids from pathogenic gram-positive bacteria. Nat Immunol 12(10):966–974CrossRefPubMedPubMedCentral Kinjo Y, Illarionov P, Vela JL, Pei B, Girardi E, Li X, Li Y, Imamura M, Kaneko Y, Okawara A, Miyazaki Y, Gómez-Velasco A, Rogers P, Dahesh S, Uchiyama S, Khurana A, Kawahara K, Yesilkaya H, Andrew PW, Wong CH, Kawakami K, Nizet V, Besra GS, Tsuji M, Zajonc DM, Kronenberg M (2011) Invariant natural killer T cells recognize glycolipids from pathogenic gram-positive bacteria. Nat Immunol 12(10):966–974CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 336(6080):489–493CrossRefPubMedPubMedCentral Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 336(6080):489–493CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Savage AK, Constantinides MG, Han J, Picard D, Martin E, Li B, Lantz O, Bendelac A (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity. 29(3):391–403CrossRefPubMedPubMedCentral Savage AK, Constantinides MG, Han J, Picard D, Martin E, Li B, Lantz O, Bendelac A (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity. 29(3):391–403CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Seiler MP, Mathew R, Liszewski MK, Spooner CJ, Barr K, Meng F, Singh H, Bendelac A (2012) Elevated and sustained expression of the transcription factors Egr1 and Egr2 controls NKT lineage differentiation in response to TCR signaling. Nat Immunol 13(3):264–271CrossRefPubMedPubMedCentral Seiler MP, Mathew R, Liszewski MK, Spooner CJ, Barr K, Meng F, Singh H, Bendelac A (2012) Elevated and sustained expression of the transcription factors Egr1 and Egr2 controls NKT lineage differentiation in response to TCR signaling. Nat Immunol 13(3):264–271CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH (2004) T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity. 20(4):477–494CrossRefPubMed Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH (2004) T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity. 20(4):477–494CrossRefPubMed
20.
Zurück zum Zitat Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA (2013) Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 14(11):1146–1154CrossRefPubMed Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA (2013) Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 14(11):1146–1154CrossRefPubMed
21.
Zurück zum Zitat Coquet JM, Chakravarti S, Kyparissoudis K, McNab FW, Pitt LA, McKenzie BS et al (2008) Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc Natl Acad Sci U S A 105(32):11287–11292CrossRefPubMedPubMedCentral Coquet JM, Chakravarti S, Kyparissoudis K, McNab FW, Pitt LA, McKenzie BS et al (2008) Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc Natl Acad Sci U S A 105(32):11287–11292CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Kim PJ, Pai SY, Brigl M, Besra GS, Gumperz J, Ho IC (2006) GATA-3 regulates the development and function of invariant NKT cells. J Immunol 177(10):6650–6659CrossRefPubMed Kim PJ, Pai SY, Brigl M, Besra GS, Gumperz J, Ho IC (2006) GATA-3 regulates the development and function of invariant NKT cells. J Immunol 177(10):6650–6659CrossRefPubMed
23.
Zurück zum Zitat Michel ML, Mendes-da-Cruz D, Keller AC, Lochner M, Schneider E, Dy M, Eberl G, Leite-de-Moraes MC (2008) Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci U S A 105(50):19845–19850CrossRefPubMedPubMedCentral Michel ML, Mendes-da-Cruz D, Keller AC, Lochner M, Schneider E, Dy M, Eberl G, Leite-de-Moraes MC (2008) Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci U S A 105(50):19845–19850CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Pobezinsky LA, Etzensperger R, Jeurling S, Alag A, Kadakia T, McCaughtry TM et al (2015) Let-7 microRNAs target the lineage-specific transcription factor PLZF to regulate terminal NKT cell differentiation and effector function. Nat Immunol 16(5):517–524CrossRefPubMedPubMedCentral Pobezinsky LA, Etzensperger R, Jeurling S, Alag A, Kadakia T, McCaughtry TM et al (2015) Let-7 microRNAs target the lineage-specific transcription factor PLZF to regulate terminal NKT cell differentiation and effector function. Nat Immunol 16(5):517–524CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Engel I, Seumois G, Chavez L, Samaniego-Castruita D, White B, Chawla A, Mock D, Vijayanand P, Kronenberg M (2016) Innate-like functions of natural killer T cell subsets result from highly divergent gene programs. Nat Immunol 17(6):728–739CrossRefPubMedPubMedCentral Engel I, Seumois G, Chavez L, Samaniego-Castruita D, White B, Chawla A, Mock D, Vijayanand P, Kronenberg M (2016) Innate-like functions of natural killer T cell subsets result from highly divergent gene programs. Nat Immunol 17(6):728–739CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Chang PP, Barral P, Fitch J, Pratama A, Ma CS, Kallies A, Hogan JJ, Cerundolo V, Tangye SG, Bittman R, Nutt SL, Brink R, Godfrey DI, Batista FD, Vinuesa CG (2011) Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat Immunol 13(1):35–43CrossRefPubMed Chang PP, Barral P, Fitch J, Pratama A, Ma CS, Kallies A, Hogan JJ, Cerundolo V, Tangye SG, Bittman R, Nutt SL, Brink R, Godfrey DI, Batista FD, Vinuesa CG (2011) Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat Immunol 13(1):35–43CrossRefPubMed
27.
Zurück zum Zitat Galli G, Nuti S, Tavarini S, Galli-Stampino L, De Lalla C, Casorati G et al (2003) CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J Exp Med 197(8):1051–1057CrossRefPubMedPubMedCentral Galli G, Nuti S, Tavarini S, Galli-Stampino L, De Lalla C, Casorati G et al (2003) CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J Exp Med 197(8):1051–1057CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Barral P, Eckl-Dorna J, Harwood NE, De Santo C, Salio M, Illarionov P et al (2008) B cell receptor-mediated uptake of CD1d-restricted antigen augments antibody responses by recruiting invariant NKT cell help in vivo. Proc Natl Acad Sci U S A 105(24):8345–8350CrossRefPubMedPubMedCentral Barral P, Eckl-Dorna J, Harwood NE, De Santo C, Salio M, Illarionov P et al (2008) B cell receptor-mediated uptake of CD1d-restricted antigen augments antibody responses by recruiting invariant NKT cell help in vivo. Proc Natl Acad Sci U S A 105(24):8345–8350CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat King IL, Fortier A, Tighe M, Dibble J, Watts GF, Veerapen N, Haberman AM, Besra GS, Mohrs M, Brenner MB, Leadbetter EA (2011) Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat Immunol 13(1):44–50CrossRefPubMed King IL, Fortier A, Tighe M, Dibble J, Watts GF, Veerapen N, Haberman AM, Besra GS, Mohrs M, Brenner MB, Leadbetter EA (2011) Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat Immunol 13(1):44–50CrossRefPubMed
30.
Zurück zum Zitat Gaya M, Barral P, Burbage M, Aggarwal S, Montaner B, Warren Navia A, Aid M, Tsui C, Maldonado P, Nair U, Ghneim K, Fallon PG, Sekaly RP, Barouch DH, Shalek AK, Bruckbauer A, Strid J, Batista FD (2018) Initiation of antiviral B cell immunity relies on innate signals from spatially positioned NKT cells. Cell. 172(3):517–533 e20CrossRefPubMedPubMedCentral Gaya M, Barral P, Burbage M, Aggarwal S, Montaner B, Warren Navia A, Aid M, Tsui C, Maldonado P, Nair U, Ghneim K, Fallon PG, Sekaly RP, Barouch DH, Shalek AK, Bruckbauer A, Strid J, Batista FD (2018) Initiation of antiviral B cell immunity relies on innate signals from spatially positioned NKT cells. Cell. 172(3):517–533 e20CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, Affaticati P, Gilfillan S, Lantz O (2003) Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 422(6928):164–169CrossRefPubMed Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, Affaticati P, Gilfillan S, Lantz O (2003) Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 422(6928):164–169CrossRefPubMed
32.
Zurück zum Zitat Lepore M, Kalinichenko A, Colone A, Paleja B, Singhal A, Tschumi A, Lee B, Poidinger M, Zolezzi F, Quagliata L, Sander P, Newell E, Bertoletti A, Terracciano L, de Libero G, Mori L (2014) Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat Commun 5:3866CrossRefPubMed Lepore M, Kalinichenko A, Colone A, Paleja B, Singhal A, Tschumi A, Lee B, Poidinger M, Zolezzi F, Quagliata L, Sander P, Newell E, Bertoletti A, Terracciano L, de Libero G, Mori L (2014) Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat Commun 5:3866CrossRefPubMed
33.
Zurück zum Zitat Reantragoon R, Corbett AJ, Sakala IG, Gherardin NA, Furness JB, Chen Z, Eckle SBG, Uldrich AP, Birkinshaw RW, Patel O, Kostenko L, Meehan B, Kedzierska K, Liu L, Fairlie DP, Hansen TH, Godfrey DI, Rossjohn J, McCluskey J, Kjer-Nielsen L (2013) Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med 210(11):2305–2320CrossRefPubMedPubMedCentral Reantragoon R, Corbett AJ, Sakala IG, Gherardin NA, Furness JB, Chen Z, Eckle SBG, Uldrich AP, Birkinshaw RW, Patel O, Kostenko L, Meehan B, Kedzierska K, Liu L, Fairlie DP, Hansen TH, Godfrey DI, Rossjohn J, McCluskey J, Kjer-Nielsen L (2013) Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med 210(11):2305–2320CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Tilloy F, Treiner E, Park SH, Garcia C, Lemonnier F, de la Salle H, Bendelac A, Bonneville M, Lantz O (1999) An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med 189(12):1907–1921CrossRefPubMedPubMedCentral Tilloy F, Treiner E, Park SH, Garcia C, Lemonnier F, de la Salle H, Bendelac A, Bonneville M, Lantz O (1999) An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med 189(12):1907–1921CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, Winata E, Swarbrick GM, Chua WJ, Yu YYL, Lantz O, Cook MS, Null MD, Jacoby DB, Harriff MJ, Lewinsohn DA, Hansen TH, Lewinsohn DM (2010) Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8(6):e1000407CrossRefPubMedPubMedCentral Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, Winata E, Swarbrick GM, Chua WJ, Yu YYL, Lantz O, Cook MS, Null MD, Jacoby DB, Harriff MJ, Lewinsohn DA, Hansen TH, Lewinsohn DM (2010) Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8(6):e1000407CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Teunissen MBM, Yeremenko NG, Baeten DLP, Chielie S, Spuls PI, de Rie MA, Lantz O, Res PCM (2014) The IL-17A-producing CD8+ T-cell population in psoriatic lesional skin comprises mucosa-associated invariant T cells and conventional T cells. J Invest Dermatol 134(12):2898–2907CrossRefPubMed Teunissen MBM, Yeremenko NG, Baeten DLP, Chielie S, Spuls PI, de Rie MA, Lantz O, Res PCM (2014) The IL-17A-producing CD8+ T-cell population in psoriatic lesional skin comprises mucosa-associated invariant T cells and conventional T cells. J Invest Dermatol 134(12):2898–2907CrossRefPubMed
37.
Zurück zum Zitat Martin E, Treiner E, Duban L, Guerri L, Laude H, Toly C, Premel V, Devys A, Moura IC, Tilloy F, Cherif S, Vera G, Latour S, Soudais C, Lantz O (2009) Stepwise development of MAIT cells in mouse and human. PLoS Biol 7(3):e54CrossRefPubMed Martin E, Treiner E, Duban L, Guerri L, Laude H, Toly C, Premel V, Devys A, Moura IC, Tilloy F, Cherif S, Vera G, Latour S, Soudais C, Lantz O (2009) Stepwise development of MAIT cells in mouse and human. PLoS Biol 7(3):e54CrossRefPubMed
38.
Zurück zum Zitat Porcelli S, Yockey CE, Brenner MB, Balk SP (1993) Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 178(1):1–16CrossRefPubMed Porcelli S, Yockey CE, Brenner MB, Balk SP (1993) Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 178(1):1–16CrossRefPubMed
39.
Zurück zum Zitat Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, Milder M, le Bourhis L, Soudais C, Treiner E, Lantz O (2011) Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 117(4):1250–1259CrossRefPubMed Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, Milder M, le Bourhis L, Soudais C, Treiner E, Lantz O (2011) Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 117(4):1250–1259CrossRefPubMed
40.
Zurück zum Zitat Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, Core M et al (2010) Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11(8):701–708CrossRefPubMed Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, Core M et al (2010) Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11(8):701–708CrossRefPubMed
41.
Zurück zum Zitat Leeansyah E, Loh L, Nixon DF, Sandberg JK (2014) Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat Commun 5:3143CrossRefPubMed Leeansyah E, Loh L, Nixon DF, Sandberg JK (2014) Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat Commun 5:3143CrossRefPubMed
42.
Zurück zum Zitat Walker LJ, Kang YH, Smith MO, Tharmalingham H, Ramamurthy N, Fleming VM, Sahgal N, Leslie A, Oo Y, Geremia A, Scriba TJ, Hanekom WA, Lauer GM, Lantz O, Adams DH, Powrie F, Barnes E, Klenerman P (2012) Human MAIT and CD8alphaalpha cells develop from a pool of type-17 precommitted CD8+ T cells. Blood. 119(2):422–433CrossRefPubMedPubMedCentral Walker LJ, Kang YH, Smith MO, Tharmalingham H, Ramamurthy N, Fleming VM, Sahgal N, Leslie A, Oo Y, Geremia A, Scriba TJ, Hanekom WA, Lauer GM, Lantz O, Adams DH, Powrie F, Barnes E, Klenerman P (2012) Human MAIT and CD8alphaalpha cells develop from a pool of type-17 precommitted CD8+ T cells. Blood. 119(2):422–433CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Dias J, Leeansyah E, Sandberg JK (2017) Multiple layers of heterogeneity and subset diversity in human MAIT cell responses to distinct microorganisms and to innate cytokines. Proc Natl Acad Sci U S A 114(27):E5434–E5E43CrossRefPubMedPubMedCentral Dias J, Leeansyah E, Sandberg JK (2017) Multiple layers of heterogeneity and subset diversity in human MAIT cell responses to distinct microorganisms and to innate cytokines. Proc Natl Acad Sci U S A 114(27):E5434–E5E43CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Rahimpour A, Koay HF, Enders A, Clanchy R, Eckle SB, Meehan B et al (2015) Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J Exp Med 212(7):1095–1108CrossRefPubMedPubMedCentral Rahimpour A, Koay HF, Enders A, Clanchy R, Eckle SB, Meehan B et al (2015) Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J Exp Med 212(7):1095–1108CrossRefPubMedPubMedCentral
45.
Zurück zum Zitat Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L et al (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 491(7426):717–723CrossRefPubMed Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L et al (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 491(7426):717–723CrossRefPubMed
47.
Zurück zum Zitat Finkelman FD, Hogan SP, Hershey GK, Rothenberg ME, Wills-Karp M (2010) Importance of cytokines in murine allergic airway disease and human asthma. J Immunol 184(4):1663–1674CrossRefPubMed Finkelman FD, Hogan SP, Hershey GK, Rothenberg ME, Wills-Karp M (2010) Importance of cytokines in murine allergic airway disease and human asthma. J Immunol 184(4):1663–1674CrossRefPubMed
48.
Zurück zum Zitat Nakayama T, Hirahara K, Onodera A, Endo Y, Hosokawa H, Shinoda K, Tumes DJ, Okamoto Y (2017) Th2 cells in health and disease. Annu Rev Immunol 35:53–84CrossRefPubMed Nakayama T, Hirahara K, Onodera A, Endo Y, Hosokawa H, Shinoda K, Tumes DJ, Okamoto Y (2017) Th2 cells in health and disease. Annu Rev Immunol 35:53–84CrossRefPubMed
49.
Zurück zum Zitat Brown DR, Fowell DJ, Corry DB, Wynn TA, Moskowitz NH, Cheever AW, Locksley RM, Reiner SL (1996) Beta 2-microglobulin-dependent NK1.1+ T cells are not essential for T helper cell 2 immune responses. J Exp Med 184(4):1295–1304CrossRefPubMed Brown DR, Fowell DJ, Corry DB, Wynn TA, Moskowitz NH, Cheever AW, Locksley RM, Reiner SL (1996) Beta 2-microglobulin-dependent NK1.1+ T cells are not essential for T helper cell 2 immune responses. J Exp Med 184(4):1295–1304CrossRefPubMed
50.
Zurück zum Zitat Korsgren M, Persson CG, Sundler F, Bjerke T, Hansson T, Chambers BJ et al (1999) Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J Exp Med 189(3):553–562CrossRefPubMedPubMedCentral Korsgren M, Persson CG, Sundler F, Bjerke T, Hansson T, Chambers BJ et al (1999) Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J Exp Med 189(3):553–562CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat McKnight CG, Morris SC, Perkins C, Zhu Z, Hildeman DA, Bendelac A et al (2017) NKT cells contribute to basal IL-4 production but are not required to induce experimental asthma. PLoS One 12(11):e0188221CrossRefPubMedPubMedCentral McKnight CG, Morris SC, Perkins C, Zhu Z, Hildeman DA, Bendelac A et al (2017) NKT cells contribute to basal IL-4 production but are not required to induce experimental asthma. PLoS One 12(11):e0188221CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Zhang Y, Rogers KH, Lewis DB (1996) Beta 2-microglobulin-dependent T cells are dispensable for allergen-induced T helper 2 responses. J Exp Med 184(4):1507–1512CrossRefPubMed Zhang Y, Rogers KH, Lewis DB (1996) Beta 2-microglobulin-dependent T cells are dispensable for allergen-induced T helper 2 responses. J Exp Med 184(4):1507–1512CrossRefPubMed
53.
Zurück zum Zitat Akbari O, Stock P, Meyer E, Kronenberg M, Sidobre S, Nakayama T, Taniguchi M, Grusby MJ, DeKruyff RH, Umetsu DT (2003) Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 9(5):582–588CrossRefPubMed Akbari O, Stock P, Meyer E, Kronenberg M, Sidobre S, Nakayama T, Taniguchi M, Grusby MJ, DeKruyff RH, Umetsu DT (2003) Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 9(5):582–588CrossRefPubMed
54.
Zurück zum Zitat Lisbonne M, Diem S, de Castro KA, Lefort J, Araujo LM, Hachem P et al (2003) Cutting edge: invariant V alpha 14 NKT cells are required for allergen-induced airway inflammation and hyperreactivity in an experimental asthma model. J Immunol 171(4):1637–1641CrossRefPubMed Lisbonne M, Diem S, de Castro KA, Lefort J, Araujo LM, Hachem P et al (2003) Cutting edge: invariant V alpha 14 NKT cells are required for allergen-induced airway inflammation and hyperreactivity in an experimental asthma model. J Immunol 171(4):1637–1641CrossRefPubMed
55.
Zurück zum Zitat Chandra S, Zhao M, Budelsky A, de Mingo PA, Day J, Fu Z et al (2015) A new mouse strain for the analysis of invariant NKT cell function. Nat Immunol 16(8):799–800CrossRefPubMedPubMedCentral Chandra S, Zhao M, Budelsky A, de Mingo PA, Day J, Fu Z et al (2015) A new mouse strain for the analysis of invariant NKT cell function. Nat Immunol 16(8):799–800CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Hachem P, Lisbonne M, Michel ML, Diem S, Roongapinun S, Lefort J, Marchal G, Herbelin A, Askenase PW, Dy M, de Leite-Moraes MC (2005) Alpha-galactosylceramide-induced iNKT cells suppress experimental allergic asthma in sensitized mice: role of IFN-gamma. Eur J Immunol 35(10):2793–2802CrossRefPubMed Hachem P, Lisbonne M, Michel ML, Diem S, Roongapinun S, Lefort J, Marchal G, Herbelin A, Askenase PW, Dy M, de Leite-Moraes MC (2005) Alpha-galactosylceramide-induced iNKT cells suppress experimental allergic asthma in sensitized mice: role of IFN-gamma. Eur J Immunol 35(10):2793–2802CrossRefPubMed
57.
Zurück zum Zitat Matangkasombut P, Pichavant M, Yasumi T, Hendricks C, Savage PB, Dekruyff RH et al (2008) Direct activation of natural killer T cells induces airway hyperreactivity in nonhuman primates. J Allergy Clin Immunol 121(5):1287–1289CrossRefPubMedPubMedCentral Matangkasombut P, Pichavant M, Yasumi T, Hendricks C, Savage PB, Dekruyff RH et al (2008) Direct activation of natural killer T cells induces airway hyperreactivity in nonhuman primates. J Allergy Clin Immunol 121(5):1287–1289CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Michel ML, Keller AC, Paget C, Fujio M, Trottein F, Savage PB, Wong CH, Schneider E, Dy M, Leite-de-Moraes MC (2007) Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 204(5):995–1001CrossRefPubMedPubMedCentral Michel ML, Keller AC, Paget C, Fujio M, Trottein F, Savage PB, Wong CH, Schneider E, Dy M, Leite-de-Moraes MC (2007) Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 204(5):995–1001CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat Scanlon ST, Thomas SY, Ferreira CM, Bai L, Krausz T, Savage PB, Bendelac A (2011) Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation. J Exp Med 208(10):2113–2124CrossRefPubMedPubMedCentral Scanlon ST, Thomas SY, Ferreira CM, Bai L, Krausz T, Savage PB, Bendelac A (2011) Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation. J Exp Med 208(10):2113–2124CrossRefPubMedPubMedCentral
60.
Zurück zum Zitat Tumes DJ, Hirahara K, Papadopoulos M, Shinoda K, Onodera A, Kumagai J, et al. (2019) Ezh2 controls development of natural killer T cells that cause spontaneous asthma-like pathology. J Allergy Clin Immunol. Advance online Tumes DJ, Hirahara K, Papadopoulos M, Shinoda K, Onodera A, Kumagai J, et al. (2019) Ezh2 controls development of natural killer T cells that cause spontaneous asthma-like pathology. J Allergy Clin Immunol. Advance online
61.
Zurück zum Zitat Tumes DJ, Onodera A, Suzuki A, Shinoda K, Endo Y, Iwamura C, Hosokawa H, Koseki H, Tokoyoda K, Suzuki Y, Motohashi S, Nakayama T (2013) The polycomb protein Ezh2 regulates differentiation and plasticity of CD4(+) T helper type 1 and type 2 cells. Immunity. 39(5):819–832CrossRefPubMed Tumes DJ, Onodera A, Suzuki A, Shinoda K, Endo Y, Iwamura C, Hosokawa H, Koseki H, Tokoyoda K, Suzuki Y, Motohashi S, Nakayama T (2013) The polycomb protein Ezh2 regulates differentiation and plasticity of CD4(+) T helper type 1 and type 2 cells. Immunity. 39(5):819–832CrossRefPubMed
62.
Zurück zum Zitat Pichavant M, Goya S, Meyer EH, Johnston RA, Kim HY, Matangkasombut P, Zhu M, Iwakura Y, Savage PB, DeKruyff RH, Shore SA, Umetsu DT (2008) Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J Exp Med 205(2):385–393CrossRefPubMedPubMedCentral Pichavant M, Goya S, Meyer EH, Johnston RA, Kim HY, Matangkasombut P, Zhu M, Iwakura Y, Savage PB, DeKruyff RH, Shore SA, Umetsu DT (2008) Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J Exp Med 205(2):385–393CrossRefPubMedPubMedCentral
63.
Zurück zum Zitat Divekar R, Kita H (2015) Recent advances in epithelium-derived cytokines (IL-33, IL-25, and thymic stromal lymphopoietin) and allergic inflammation. Curr Opin Allergy Clin Immunol 15(1):98–103CrossRefPubMedPubMedCentral Divekar R, Kita H (2015) Recent advances in epithelium-derived cytokines (IL-33, IL-25, and thymic stromal lymphopoietin) and allergic inflammation. Curr Opin Allergy Clin Immunol 15(1):98–103CrossRefPubMedPubMedCentral
64.
Zurück zum Zitat Stock P, Lombardi V, Kohlrautz V, Akbari O (2009) Induction of airway hyperreactivity by IL-25 is dependent on a subset of invariant NKT cells expressing IL-17RB. J Immunol 182(8):5116–5122CrossRefPubMed Stock P, Lombardi V, Kohlrautz V, Akbari O (2009) Induction of airway hyperreactivity by IL-25 is dependent on a subset of invariant NKT cells expressing IL-17RB. J Immunol 182(8):5116–5122CrossRefPubMed
65.
Zurück zum Zitat Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE (2008) IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol 20(8):1019–1030CrossRefPubMed Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE (2008) IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol 20(8):1019–1030CrossRefPubMed
66.
Zurück zum Zitat Nagata Y, Kamijuku H, Taniguchi M, Ziegler S, Seino K (2007) Differential role of thymic stromal lymphopoietin in the induction of airway hyperreactivity and Th2 immune response in antigen-induced asthma with respect to natural killer T cell function. Int Arch Allergy Immunol 144(4):305–314CrossRefPubMed Nagata Y, Kamijuku H, Taniguchi M, Ziegler S, Seino K (2007) Differential role of thymic stromal lymphopoietin in the induction of airway hyperreactivity and Th2 immune response in antigen-induced asthma with respect to natural killer T cell function. Int Arch Allergy Immunol 144(4):305–314CrossRefPubMed
67.
Zurück zum Zitat Vultaggio A, Nencini F, Pratesi S, Petroni G, Romagnani S, Maggi E (2012) Poly(I:C) promotes the production of IL-17A by murine CD1d-driven invariant NKT cells in airway inflammation. Allergy. 67(10):1223–1232CrossRefPubMed Vultaggio A, Nencini F, Pratesi S, Petroni G, Romagnani S, Maggi E (2012) Poly(I:C) promotes the production of IL-17A by murine CD1d-driven invariant NKT cells in airway inflammation. Allergy. 67(10):1223–1232CrossRefPubMed
68.
Zurück zum Zitat Akbari O, Faul JL, Hoyte EG, Berry GJ, Wahlstrom J, Kronenberg M et al (2006) CD4+ invariant T-cell-receptor+ natural killer T cells in bronchial asthma. N Engl J Med 354(11):1117–1129CrossRefPubMed Akbari O, Faul JL, Hoyte EG, Berry GJ, Wahlstrom J, Kronenberg M et al (2006) CD4+ invariant T-cell-receptor+ natural killer T cells in bronchial asthma. N Engl J Med 354(11):1117–1129CrossRefPubMed
69.
Zurück zum Zitat Koh YI, Shim JU (2010) Association between sputum natural killer T cells and eosinophilic airway inflammation in human asthma. Int Arch Allergy Immunol 153(3):239–248CrossRefPubMed Koh YI, Shim JU (2010) Association between sputum natural killer T cells and eosinophilic airway inflammation in human asthma. Int Arch Allergy Immunol 153(3):239–248CrossRefPubMed
70.
Zurück zum Zitat Matangkasombut P, Marigowda G, Ervine A, Idris L, Pichavant M, Kim HY, Yasumi T, Wilson SB, DeKruyff RH, Faul JL, Israel E, Akbari O, Umetsu DT (2009) Natural killer T cells in the lungs of patients with asthma. J Allergy Clin Immunol 123(5):1181–1185CrossRefPubMedPubMedCentral Matangkasombut P, Marigowda G, Ervine A, Idris L, Pichavant M, Kim HY, Yasumi T, Wilson SB, DeKruyff RH, Faul JL, Israel E, Akbari O, Umetsu DT (2009) Natural killer T cells in the lungs of patients with asthma. J Allergy Clin Immunol 123(5):1181–1185CrossRefPubMedPubMedCentral
71.
Zurück zum Zitat Reynolds C, Barkans J, Clark P, Kariyawasam H, Altmann D, Kay B, Boyton R (2009) Natural killer T cells in bronchial biopsies from human allergen challenge model of allergic asthma. J Allergy Clin Immunol 124(4):860–862 author reply 2CrossRefPubMed Reynolds C, Barkans J, Clark P, Kariyawasam H, Altmann D, Kay B, Boyton R (2009) Natural killer T cells in bronchial biopsies from human allergen challenge model of allergic asthma. J Allergy Clin Immunol 124(4):860–862 author reply 2CrossRefPubMed
72.
Zurück zum Zitat Brooks CR, Weinkove R, Hermans IF, van Dalen CJ, Douwes J (2010) Invariant natural killer T cells and asthma: immunologic reality or methodologic artifact? J Allergy Clin Immunol 126(4):882–885CrossRefPubMed Brooks CR, Weinkove R, Hermans IF, van Dalen CJ, Douwes J (2010) Invariant natural killer T cells and asthma: immunologic reality or methodologic artifact? J Allergy Clin Immunol 126(4):882–885CrossRefPubMed
73.
Zurück zum Zitat Vijayanand P, Seumois G, Pickard C, Powell RM, Angco G, Sammut D, Gadola SD, Friedmann PS, Djukanović R (2007) Invariant natural killer T cells in asthma and chronic obstructive pulmonary disease. N Engl J Med 356(14):1410–1422CrossRefPubMed Vijayanand P, Seumois G, Pickard C, Powell RM, Angco G, Sammut D, Gadola SD, Friedmann PS, Djukanović R (2007) Invariant natural killer T cells in asthma and chronic obstructive pulmonary disease. N Engl J Med 356(14):1410–1422CrossRefPubMed
74.
Zurück zum Zitat Chandra S, Wingender G, Greenbaum JA, Khurana A, Gholami AM, Ganesan AP, Rosenbach M, Jaffee K, Gern JE, Wood R, O’Connor G, Sandel M, Kattan M, Bacharier L, Togias A, Horner AA, Kronenberg M (2018) Development of asthma in Inner-City children: possible roles of MAIT cells and variation in the home environment. J Immunol 200(6):1995–2003CrossRefPubMed Chandra S, Wingender G, Greenbaum JA, Khurana A, Gholami AM, Ganesan AP, Rosenbach M, Jaffee K, Gern JE, Wood R, O’Connor G, Sandel M, Kattan M, Bacharier L, Togias A, Horner AA, Kronenberg M (2018) Development of asthma in Inner-City children: possible roles of MAIT cells and variation in the home environment. J Immunol 200(6):1995–2003CrossRefPubMed
75.
Zurück zum Zitat Lezmi G, Abou Taam R, Dietrich C, Chatenoud L, de Blic J, Leite-de-Moraes M (2018) Circulating IL-17-producing mucosal-associated invariant T cells (MAIT) are associated with symptoms in children with asthma. Clin Immunol 188:7–11CrossRefPubMed Lezmi G, Abou Taam R, Dietrich C, Chatenoud L, de Blic J, Leite-de-Moraes M (2018) Circulating IL-17-producing mucosal-associated invariant T cells (MAIT) are associated with symptoms in children with asthma. Clin Immunol 188:7–11CrossRefPubMed
76.
Zurück zum Zitat Shim JU, Koh YI (2014) Increased Th2-like invariant natural killer T cells in peripheral blood from patients with asthma. Allergy, Asthma Immunol Res 6(5):444–448CrossRef Shim JU, Koh YI (2014) Increased Th2-like invariant natural killer T cells in peripheral blood from patients with asthma. Allergy, Asthma Immunol Res 6(5):444–448CrossRef
77.
Zurück zum Zitat Hinks TS, Zhou X, Staples KJ, Dimitrov BD, Manta A, Petrossian T et al (2015) Innate and adaptive T cells in asthmatic patients: relationship to severity and disease mechanisms. J Allergy Clin Immunol 136(2):323–333CrossRefPubMedPubMedCentral Hinks TS, Zhou X, Staples KJ, Dimitrov BD, Manta A, Petrossian T et al (2015) Innate and adaptive T cells in asthmatic patients: relationship to severity and disease mechanisms. J Allergy Clin Immunol 136(2):323–333CrossRefPubMedPubMedCentral
78.
Zurück zum Zitat Shinoda K, Hirahara K, Iinuma T, Ichikawa T, Suzuki AS, Sugaya K, Tumes DJ, Yamamoto H, Hara T, Tani-ichi S, Ikuta K, Okamoto Y, Nakayama T (2016) Thy1+IL-7+ lymphatic endothelial cells in iBALT provide a survival niche for memory T-helper cells in allergic airway inflammation. Proc Natl Acad Sci U S A 113(20):E2842–E2851CrossRefPubMedPubMedCentral Shinoda K, Hirahara K, Iinuma T, Ichikawa T, Suzuki AS, Sugaya K, Tumes DJ, Yamamoto H, Hara T, Tani-ichi S, Ikuta K, Okamoto Y, Nakayama T (2016) Thy1+IL-7+ lymphatic endothelial cells in iBALT provide a survival niche for memory T-helper cells in allergic airway inflammation. Proc Natl Acad Sci U S A 113(20):E2842–E2851CrossRefPubMedPubMedCentral
79.
Zurück zum Zitat Pant H, Hughes A, Miljkovic D, Schembri M, Wormald P, Macardle P, Grose R, Zola H, Krumbiegel D (2013) Accumulation of effector memory CD8+ T cells in nasal polyps. Am J Rhinol Allergy 27(5):e117–e126CrossRefPubMed Pant H, Hughes A, Miljkovic D, Schembri M, Wormald P, Macardle P, Grose R, Zola H, Krumbiegel D (2013) Accumulation of effector memory CD8+ T cells in nasal polyps. Am J Rhinol Allergy 27(5):e117–e126CrossRefPubMed
80.
Zurück zum Zitat Yamamoto H, Okamoto Y, Horiguchi S, Kunii N, Yonekura S, Nakayama T (2007) Detection of natural killer T cells in the sinus mucosa from asthmatics with chronic sinusitis. Allergy. 62(12):1451–1455CrossRefPubMed Yamamoto H, Okamoto Y, Horiguchi S, Kunii N, Yonekura S, Nakayama T (2007) Detection of natural killer T cells in the sinus mucosa from asthmatics with chronic sinusitis. Allergy. 62(12):1451–1455CrossRefPubMed
81.
Zurück zum Zitat Tsao CC, Tsao PN, Chen YG, Chuang YH (2016) Repeated activation of lung invariant NKT cells results in chronic obstructive pulmonary disease-like symptoms. PLoS One 11(1):e0147710CrossRefPubMedPubMedCentral Tsao CC, Tsao PN, Chen YG, Chuang YH (2016) Repeated activation of lung invariant NKT cells results in chronic obstructive pulmonary disease-like symptoms. PLoS One 11(1):e0147710CrossRefPubMedPubMedCentral
82.
Zurück zum Zitat Kim EY, Battaile JT, Patel AC, You Y, Agapov E, Grayson MH, Benoit LA, Byers DE, Alevy Y, Tucker J, Swanson S, Tidwell R, Tyner JW, Morton JD, Castro M, Polineni D, Patterson GA, Schwendener RA, Allard JD, Peltz G, Holtzman MJ (2008) Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med 14(6):633–640CrossRefPubMedPubMedCentral Kim EY, Battaile JT, Patel AC, You Y, Agapov E, Grayson MH, Benoit LA, Byers DE, Alevy Y, Tucker J, Swanson S, Tidwell R, Tyner JW, Morton JD, Castro M, Polineni D, Patterson GA, Schwendener RA, Allard JD, Peltz G, Holtzman MJ (2008) Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med 14(6):633–640CrossRefPubMedPubMedCentral
83.
Zurück zum Zitat Szabo M, Sarosi V, Baliko Z, Bodo K, Farkas N, Berki T et al (2017) Deficiency of innate-like T lymphocytes in chronic obstructive pulmonary disease. Respir Res 18(1):197CrossRefPubMedPubMedCentral Szabo M, Sarosi V, Baliko Z, Bodo K, Farkas N, Berki T et al (2017) Deficiency of innate-like T lymphocytes in chronic obstructive pulmonary disease. Respir Res 18(1):197CrossRefPubMedPubMedCentral
84.
85.
Zurück zum Zitat Hinks TS, Wallington JC, Williams AP, Djukanovic R, Staples KJ, Wilkinson TM (2016) Steroid-induced deficiency of mucosal-associated invariant T cells in the chronic obstructive pulmonary disease lung. Implications for Nontypeable Haemophilus influenzae infection. Am J Respir Crit Care Med 194(10):1208–1218CrossRefPubMedPubMedCentral Hinks TS, Wallington JC, Williams AP, Djukanovic R, Staples KJ, Wilkinson TM (2016) Steroid-induced deficiency of mucosal-associated invariant T cells in the chronic obstructive pulmonary disease lung. Implications for Nontypeable Haemophilus influenzae infection. Am J Respir Crit Care Med 194(10):1208–1218CrossRefPubMedPubMedCentral
86.
Zurück zum Zitat Van Eldere J, Slack MP, Ladhani S, Cripps AW (2014) Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 14(12):1281–1292CrossRefPubMed Van Eldere J, Slack MP, Ladhani S, Cripps AW (2014) Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 14(12):1281–1292CrossRefPubMed
87.
Zurück zum Zitat Heath WR, Carbone FR (2013) The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat Immunol 14(10):978–985CrossRefPubMed Heath WR, Carbone FR (2013) The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat Immunol 14(10):978–985CrossRefPubMed
88.
Zurück zum Zitat Di Meglio P, Perera GK, Nestle FO (2011) The multitasking organ: recent insights into skin immune function. Immunity. 35(6):857–869CrossRefPubMed Di Meglio P, Perera GK, Nestle FO (2011) The multitasking organ: recent insights into skin immune function. Immunity. 35(6):857–869CrossRefPubMed
90.
Zurück zum Zitat Cavani A, Pennino D, Eyerich K (2012) Th17 and Th22 in skin allergy. Chem Immunol Allergy 96:39–44CrossRefPubMed Cavani A, Pennino D, Eyerich K (2012) Th17 and Th22 in skin allergy. Chem Immunol Allergy 96:39–44CrossRefPubMed
91.
Zurück zum Zitat Novak N, Bieber T (2003) Allergic and nonallergic forms of atopic diseases. J Allergy Clin Immunol 112(2):252–262CrossRefPubMed Novak N, Bieber T (2003) Allergic and nonallergic forms of atopic diseases. J Allergy Clin Immunol 112(2):252–262CrossRefPubMed
92.
Zurück zum Zitat Wu WH, Park CO, Oh SH, Kim HJ, Kwon YS, Bae BG et al (2010) Thymic stromal lymphopoietin-activated invariant natural killer T cells trigger an innate allergic immune response in atopic dermatitis. J Allergy Clin Immunol 126(2):290–299 9 e1–4CrossRefPubMed Wu WH, Park CO, Oh SH, Kim HJ, Kwon YS, Bae BG et al (2010) Thymic stromal lymphopoietin-activated invariant natural killer T cells trigger an innate allergic immune response in atopic dermatitis. J Allergy Clin Immunol 126(2):290–299 9 e1–4CrossRefPubMed
93.
Zurück zum Zitat Takahashi T, Nakamura K, Chiba S, Kanda Y, Tamaki K, Hirai H (2003) V alpha 24+ natural killer T cells are markedly decreased in atopic dermatitis patients. Hum Immunol 64(6):586–592CrossRefPubMed Takahashi T, Nakamura K, Chiba S, Kanda Y, Tamaki K, Hirai H (2003) V alpha 24+ natural killer T cells are markedly decreased in atopic dermatitis patients. Hum Immunol 64(6):586–592CrossRefPubMed
94.
Zurück zum Zitat Gyimesi E, Nagy G, Remenyik E, Sipka S, Zeher M, Biro T et al (2011) Altered peripheral invariant natural killer T cells in atopic dermatitis. J Clin Immunol 31(5):864–872CrossRefPubMed Gyimesi E, Nagy G, Remenyik E, Sipka S, Zeher M, Biro T et al (2011) Altered peripheral invariant natural killer T cells in atopic dermatitis. J Clin Immunol 31(5):864–872CrossRefPubMed
95.
Zurück zum Zitat Simon D, Kozlowski E, Simon H (2009) Natural killer T cells expressing IFN-gamma and IL-4 in lesional skin of atopic eczema. Allergy. 64(11):1681–1684CrossRefPubMed Simon D, Kozlowski E, Simon H (2009) Natural killer T cells expressing IFN-gamma and IL-4 in lesional skin of atopic eczema. Allergy. 64(11):1681–1684CrossRefPubMed
96.
Zurück zum Zitat Gober MD, Fishelevich R, Zhao Y, Unutmaz D, Gaspari AA (2008) Human natural killer T cells infiltrate into the skin at elicitation sites of allergic contact dermatitis. J Invest Dermatol 128(6):1460–1469CrossRefPubMed Gober MD, Fishelevich R, Zhao Y, Unutmaz D, Gaspari AA (2008) Human natural killer T cells infiltrate into the skin at elicitation sites of allergic contact dermatitis. J Invest Dermatol 128(6):1460–1469CrossRefPubMed
97.
Zurück zum Zitat Kronenberg M, Gapin L (2002) The unconventional lifestyle of NKT cells. Nat Rev Immunol 2(8):557–568CrossRefPubMed Kronenberg M, Gapin L (2002) The unconventional lifestyle of NKT cells. Nat Rev Immunol 2(8):557–568CrossRefPubMed
98.
Zurück zum Zitat Nieuwenhuis EE, Gillessen S, Scheper RJ, Exley MA, Taniguchi M, Balk SP et al (2005) CD1d and CD1d-restricted iNKT-cells play a pivotal role in contact hypersensitivity. Exp Dermatol 14(4):250–258CrossRefPubMed Nieuwenhuis EE, Gillessen S, Scheper RJ, Exley MA, Taniguchi M, Balk SP et al (2005) CD1d and CD1d-restricted iNKT-cells play a pivotal role in contact hypersensitivity. Exp Dermatol 14(4):250–258CrossRefPubMed
99.
Zurück zum Zitat Shimizuhira C, Otsuka A, Honda T, Kitoh A, Egawa G, Nakajima S, Nakashima C, Watarai H, Miyachi Y, Kabashima K (2014) Natural killer T cells are essential for the development of contact hypersensitivity in BALB/c mice. J Invest Dermatol 134(11):2709–2718CrossRefPubMed Shimizuhira C, Otsuka A, Honda T, Kitoh A, Egawa G, Nakajima S, Nakashima C, Watarai H, Miyachi Y, Kabashima K (2014) Natural killer T cells are essential for the development of contact hypersensitivity in BALB/c mice. J Invest Dermatol 134(11):2709–2718CrossRefPubMed
100.
Zurück zum Zitat Askenase PW, Majewska-Szczepanik M, Kerfoot S, Szczepanik M (2011) Participation of iNKT cells in the early and late components of Tc1-mediated DNFB contact sensitivity: cooperative role of gammadelta-T cells. Scand J Immunol 73(5):465–477CrossRefPubMed Askenase PW, Majewska-Szczepanik M, Kerfoot S, Szczepanik M (2011) Participation of iNKT cells in the early and late components of Tc1-mediated DNFB contact sensitivity: cooperative role of gammadelta-T cells. Scand J Immunol 73(5):465–477CrossRefPubMed
101.
Zurück zum Zitat Curzytek K, Kubera M, Majewska-Szczepanik M, Szczepanik M, Ptak W, Duda W, Leśkiewicz M, Basta-Kaim A, Budziszewska B, Regulska M, Korzeniak B, Głombik K, Maes M, Lasoń W (2015) Inhibitory effect of antidepressant drugs on contact hypersensitivity reaction is connected with their suppressive effect on NKT and CD8(+) T cells but not on TCR delta T cells. Int Immunopharmacol 28(2):1091–1096CrossRefPubMed Curzytek K, Kubera M, Majewska-Szczepanik M, Szczepanik M, Ptak W, Duda W, Leśkiewicz M, Basta-Kaim A, Budziszewska B, Regulska M, Korzeniak B, Głombik K, Maes M, Lasoń W (2015) Inhibitory effect of antidepressant drugs on contact hypersensitivity reaction is connected with their suppressive effect on NKT and CD8(+) T cells but not on TCR delta T cells. Int Immunopharmacol 28(2):1091–1096CrossRefPubMed
102.
Zurück zum Zitat Campos RA, Szczepanik M, Itakura A, Akahira-Azuma M, Sidobre S, Kronenberg M, Askenase PW (2003) Cutaneous immunization rapidly activates liver invariant Valpha14 NKT cells stimulating B-1 B cells to initiate T cell recruitment for elicitation of contact sensitivity. J Exp Med 198(12):1785–1796CrossRefPubMedPubMedCentral Campos RA, Szczepanik M, Itakura A, Akahira-Azuma M, Sidobre S, Kronenberg M, Askenase PW (2003) Cutaneous immunization rapidly activates liver invariant Valpha14 NKT cells stimulating B-1 B cells to initiate T cell recruitment for elicitation of contact sensitivity. J Exp Med 198(12):1785–1796CrossRefPubMedPubMedCentral
103.
Zurück zum Zitat Askenase PW, Itakura A, Leite-de-Moraes MC, Lisbonne M, Roongapinun S, Goldstein DR, Szczepanik M (2005) TLR-dependent IL-4 production by invariant Valpha14+Jalpha18+ NKT cells to initiate contact sensitivity in vivo. J Immunol 175(10):6390–6401CrossRefPubMed Askenase PW, Itakura A, Leite-de-Moraes MC, Lisbonne M, Roongapinun S, Goldstein DR, Szczepanik M (2005) TLR-dependent IL-4 production by invariant Valpha14+Jalpha18+ NKT cells to initiate contact sensitivity in vivo. J Immunol 175(10):6390–6401CrossRefPubMed
104.
Zurück zum Zitat Askenase PW, Szczepanik M, Itakura A, Kiener C, Campos RA (2004) Extravascular T-cell recruitment requires initiation begun by Valpha14+ NKT cells and B-1 B cells. Trends Immunol 25(8):441–449CrossRefPubMed Askenase PW, Szczepanik M, Itakura A, Kiener C, Campos RA (2004) Extravascular T-cell recruitment requires initiation begun by Valpha14+ NKT cells and B-1 B cells. Trends Immunol 25(8):441–449CrossRefPubMed
105.
Zurück zum Zitat Goubier A, Vocanson M, Macari C, Poyet G, Herbelin A, Nicolas JF, Dubois B, Kaiserlian D (2013) Invariant NKT cells suppress CD8(+) T-cell-mediated allergic contact dermatitis independently of regulatory CD4(+) T cells. J Invest Dermatol 133(4):980–987CrossRefPubMed Goubier A, Vocanson M, Macari C, Poyet G, Herbelin A, Nicolas JF, Dubois B, Kaiserlian D (2013) Invariant NKT cells suppress CD8(+) T-cell-mediated allergic contact dermatitis independently of regulatory CD4(+) T cells. J Invest Dermatol 133(4):980–987CrossRefPubMed
106.
Zurück zum Zitat Fjelbye J, Antvorskov JC, Buschard K, Issazadeh-Navikas S, Engkilde K (2015) CD1d knockout mice exhibit aggravated contact hypersensitivity responses due to reduced interleukin-10 production predominantly by regulatory B cells. Exp Dermatol 24(11):853–856CrossRefPubMed Fjelbye J, Antvorskov JC, Buschard K, Issazadeh-Navikas S, Engkilde K (2015) CD1d knockout mice exhibit aggravated contact hypersensitivity responses due to reduced interleukin-10 production predominantly by regulatory B cells. Exp Dermatol 24(11):853–856CrossRefPubMed
107.
Zurück zum Zitat Benhadou F, Mintoff D, Del Marmol V (2018) Psoriasis: keratinocytes or immune cells—which is the trigger? Dermatology. 235:91–100CrossRefPubMed Benhadou F, Mintoff D, Del Marmol V (2018) Psoriasis: keratinocytes or immune cells—which is the trigger? Dermatology. 235:91–100CrossRefPubMed
108.
Zurück zum Zitat Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A (2010) Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 130(5):1373–1383CrossRefPubMed Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A (2010) Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 130(5):1373–1383CrossRefPubMed
109.
Zurück zum Zitat Nickoloff BJ, Wrone-Smith T, Bonish B, Porcelli SA (1999) Response of murine and normal human skin to injection of allogeneic blood-derived psoriatic immunocytes: detection of T cells expressing receptors typically present on natural killer cells, including CD94, CD158, and CD161. Arch Dermatol 135(5):546–552CrossRefPubMed Nickoloff BJ, Wrone-Smith T, Bonish B, Porcelli SA (1999) Response of murine and normal human skin to injection of allogeneic blood-derived psoriatic immunocytes: detection of T cells expressing receptors typically present on natural killer cells, including CD94, CD158, and CD161. Arch Dermatol 135(5):546–552CrossRefPubMed
110.
Zurück zum Zitat Gilhar A, Ullmann Y, Kerner H, Assy B, Shalaginov R, Serafimovich S et al (2002) Psoriasis is mediated by a cutaneous defect triggered by activated immunocytes: induction of psoriasis by cells with natural killer receptors. J Invest Dermatol 119(2):384–391CrossRefPubMed Gilhar A, Ullmann Y, Kerner H, Assy B, Shalaginov R, Serafimovich S et al (2002) Psoriasis is mediated by a cutaneous defect triggered by activated immunocytes: induction of psoriasis by cells with natural killer receptors. J Invest Dermatol 119(2):384–391CrossRefPubMed
111.
Zurück zum Zitat Bonish B, Jullien D, Dutronc Y, Huang BB, Modlin R, Spada FM, Porcelli SA, Nickoloff BJ (2000) Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-gamma production by NK-T cells. J Immunol 165(7):4076–4085CrossRefPubMed Bonish B, Jullien D, Dutronc Y, Huang BB, Modlin R, Spada FM, Porcelli SA, Nickoloff BJ (2000) Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-gamma production by NK-T cells. J Immunol 165(7):4076–4085CrossRefPubMed
112.
Zurück zum Zitat Curry JL, Qin JZ, Robinson J, Nickoloff BJ (2003) Reactivity of resident immunocytes in normal and prepsoriatic skin using an ex vivo skin-explant model system. Arch Pathol Lab Med 127(3):289–296PubMed Curry JL, Qin JZ, Robinson J, Nickoloff BJ (2003) Reactivity of resident immunocytes in normal and prepsoriatic skin using an ex vivo skin-explant model system. Arch Pathol Lab Med 127(3):289–296PubMed
113.
Zurück zum Zitat McWilliam HE, Villadangos JA (2018) MR1 antigen presentation to MAIT cells: new ligands, diverse pathways? Curr Opin Immunol 52:108–113CrossRefPubMed McWilliam HE, Villadangos JA (2018) MR1 antigen presentation to MAIT cells: new ligands, diverse pathways? Curr Opin Immunol 52:108–113CrossRefPubMed
114.
Zurück zum Zitat Ortega C, Fernandez AS, Carrillo JM, Romero P, Molina IJ, Moreno JC et al (2009) IL-17-producing CD8+ T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17-related cytokines. J Leukoc Biol 86(2):435–443CrossRefPubMed Ortega C, Fernandez AS, Carrillo JM, Romero P, Molina IJ, Moreno JC et al (2009) IL-17-producing CD8+ T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17-related cytokines. J Leukoc Biol 86(2):435–443CrossRefPubMed
Metadaten
Titel
The role of invariant T cells in inflammation of the skin and airways
verfasst von
Kwok Ho Yip
Magdalene Papadopoulos
Harshita Pant
Damon J. Tumes
Publikationsdatum
15.04.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
Seminars in Immunopathology / Ausgabe 3/2019
Print ISSN: 1863-2297
Elektronische ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-019-00740-9

Weitere Artikel der Ausgabe 3/2019

Seminars in Immunopathology 3/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

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