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Inflammation Research

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04-07-2022 | Graft-Versus-Host Disease | Review

MAIT cells and their implication in human oral diseases

Authors: Qin Jiang, Fang Wang, Jing-Ya Yang, Gang Zhou

Published in: Inflammation Research | Issue 9/2022

Abstract

Objective

Mucosal-associated invariant T (MAIT) cells are unique innate-like T cells that are abundant in humans, accounting for 1-10% of circulating T cells and about 2% of total T cells in human oral cavity. MAIT cells can mount a strong immune response quickly without exogenous antigens and undergo a phenotypic transformation in the development of diseases. They produce cytokines involved in the Th1 and Th17 immune response and cytotoxic proteins, promote the dysfunction of autoreactive B cell and inhibit the function of NK cells. MAIT cells have been widely explored in autoimmune diseases, inflammatory diseases and tumors, and these mechanisms may also be involved in the pathogenesis of some oral diseases, while MAIT cells have not been systematically discussed in oral diseases.

Methods

We searched PubMed/MEDLINE, EMBASE and Microsoft Bing databases to review and analyze relevant literatures on the impact of MAIT cells in the pathogenesis of human oral diseases.

Conclusion

Collected evidence elucidated the characteristics of MAIT cells and emphasized the potential roles of MAIT cells in oral lichen planus (OLP), chronic graft-versus-host disease (cGVHD), oral squamous cell carcinoma (OSCC), apical periodontitis (AP) and primary Sjogren's syndrome (pSS).

Nel I, Bertrand L, Toubal A, Lehuen A. MAIT cells, guardians of skin and mucosa? Mucosal Immunol. 2021;14(4):803–14. https://doi.org/10.1038/s41385-021-00391-w.CrossRefPubMedPubMedCentral

Porcelli S, Yockey CE, Brenner MB, Balk SP. 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. 1993;178(1):1–16. https://doi.org/10.1084/jem.178.1.1.CrossRefPubMed

Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 2003;422(6928):164–9. https://doi.org/10.1038/nature01433.CrossRefPubMed

Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53. https://doi.org/10.1038/ni.3123.CrossRefPubMedPubMedCentral

Chandra S, Kronenberg M. Activation and function of iNKT and MAIT Cells. Adv Immunol. 2015;127:145–201. https://doi.org/10.1016/bs.ai.2015.03.003.CrossRefPubMed

Schmaler M, Colone A, Spagnuolo J, Zimmermann M, Lepore M, Kalinichenko A, et al. Modulation of bacterial metabolism by the microenvironment controls MAIT cell stimulation. Mucosal Immunol. 2018;11(4):1060–70. https://doi.org/10.1038/s41385-018-0020-9.CrossRefPubMed

Kumar V, Ahmad A. Role of MAIT cells in the immunopathogenesis of inflammatory diseases: new players in old game. Int Rev Immunol. 2018;37(2):90–110. https://doi.org/10.1080/08830185.2017.1380199. CrossRefPubMed

Zumwalde NA, Gumperz JE. Mucosal-associated invariant T cells in tumors of epithelial origin. Adv Exp Med Biol. 2020;1224:63–77. https://doi.org/10.1007/978-3-030-35723-8_5.CrossRefPubMed

Marie L, Angelis D. The role of Candida in oral lichen planus (OLP). In: The University of Melbourne Library, Minerva Access, 2019; https://hdl.handle.net/11343/241240. Accessed 23 May 2022.

10.

Konuma T, Kohara C, Watanabe E, Takahashi S, Ozawa G, Suzuki K, et al. Reconstitution of circulating mucosal-associated invariant T cells after allogeneic hematopoietic cell transplantation: its association with the riboflavin synthetic pathway of gut microbiota in cord blood transplant recipients. J Immunol. 2020;204(6):1462–73. https://doi.org/10.4049/jimmunol.1900681.CrossRefPubMed

11.

Petley EV, Koay HF, Henderson MA, Sek K, Todd KL, Keam SP, et al. MAIT cells regulate NK cell-mediated tumor immunity. Nat Commun. 2021;12(1):4746. https://doi.org/10.1038/s41467-021-25009-4.CrossRefPubMedPubMedCentral

12.

Jewett A, Kos J, Fong Y, Ko MW, Safaei T, Perišić Nanut M, et al. NK cells shape pancreatic and oral tumor microenvironments; role in inhibition of tumor growth and metastasis. Semin Cancer Biol. 2018;53:178–88. https://doi.org/10.1016/j.semcancer.2018.08.001.CrossRefPubMed

13.

Lee JJ, Yeh CY, Jung CJ, Chen CW, Du MK, Yu HM, et al. Skewed distribution of IL-7 receptor-alpha-expressing effector memory CD8⁺ T cells with distinct functional characteristics in oral squamous cell carcinoma. PLoS ONE. 2014;9(1): e85521. https://doi.org/10.1371/journal.pone.0085521.CrossRefPubMedPubMedCentral

14.

Sundström P, Szeponik L, Ahlmanner F, Sundquist M, Wong JSB, Lindskog EB, et al. Tumor-infiltrating mucosal-associated invariant T (MAIT) cells retain expression of cytotoxic effector molecules. Oncotarget. 2019;10(29):2810–23. https://doi.org/10.18632/oncotarget.26866.CrossRefPubMedPubMedCentral

15.

Davanian H, Gaiser RA, Silfverberg M, Hugerth LW, Sobkowiak MJ, Lu L, et al. Mucosal-associated invariant T cells and oral microbiome in persistent apical periodontitis. Int J Oral Sci. 2019;11(2):16. https://doi.org/10.1038/s41368-019-0049-y.CrossRefPubMedPubMedCentral

16.

Wang JJ, Macardle C, Weedon H, Beroukas D, Banovic T. Mucosal-associated invariant T cells are reduced and functionally immature in the peripheral blood of primary Sjögren’s syndrome patients. Eur J Immunol. 2016;46(10):2444–53. https://doi.org/10.1002/eji.201646300.CrossRefPubMed

17.

Guggino G, Liberto DD, Pizzo ML, Saieva L, Alessandro R, Dieli F, Triolo G, Cacciatore F. IL-17 polarization of MAIT cells is derived from the activation of two different pathways. Eur J Immunol. 2017;47(11):2002–3. https://doi.org/10.1002/eji.201747140.CrossRefPubMed

18.

Dusseaux M, Martin E, Serriari N, Péguillet I, Premel V, Louis D, et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 2011;117(4):1250–9. https://doi.org/10.1182/blood-2010-08-303339.CrossRefPubMed

19.

Wang SR, Zhong N, Zhang XM, Zhao ZB, Balderas R, Li L, et al. OMIP 071: a 31-parameter flow cytometry panel for in-depth immunophenotyping of human T-cell subsets using surface markers. Cytometry A. 2021;99(3):273–7. https://doi.org/10.1002/cyto.a.24272.CrossRefPubMed

20.

Acquaviva M, Bassani C, Sarno N, Dalla Costa G, Romeo M, Sangalli F, et al. Loss of circulating CD8⁺CD161 high T cells in primary progressive multiple sclerosis. Front Immunol. 2019;10:1922. https://doi.org/10.3389/fimmu.2019.01922.CrossRefPubMedPubMedCentral

21.

Leeansyah E, Loh L, Nixon DF, Sandberg JK. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat Commun. 2014;5:3143. https://doi.org/10.1038/ncomms4143.CrossRefPubMed

22.

Koay H-F, Gherardin NA, Enders A, Loh L, Mackay LK, Almeida CF, et al. A three-stage intrathymic development pathway for the mucosal-associated invariant T cell lineage. Nat Immunol. 2016;17(11):1300–11. https://doi.org/10.1038/ni.3565.CrossRefPubMed

23.

Koay H-F, Godfrey DI. MicroRNA-managing the development of MAIT cells. Immunol Cell Biol. 2019;97(2):121–3. https://doi.org/10.1111/imcb.12232.CrossRefPubMed

24.

Legoux F, Bellet D, Daviaud C, Morr YE, Darbois A, Niort K. Microbial metabolites control the thymic development of mucosal-associated invariant T cells. Science. 2019;366(6464):494–9. https://doi.org/10.1126/science.aaw2719.CrossRefPubMed

25.

Walker LJ, Tharmalingam H, Klenerman P. The rise and fall of MAIT cells with age. Scand J Immunol. 2014;80(6):462–3. https://doi.org/10.1111/sji.12237.CrossRefPubMedPubMedCentral

26.

Keller AN, Eckle SB, Xu W, Liu L, Hughes VA, Mak JY, et al. Drugs and drug-like molecules can modulate the function of mucosal-associated invariant T cells. Nat Immunol. 2017;18(4):402–11. https://doi.org/10.1038/ni.3679.CrossRefPubMed

27.

Jiang J, Chen X, An H, Yang B, Zhang F, Cheng X. Enhanced immune response of MAIT cells in tuberculous pleural effusions depends on cytokine signaling. Sci Rep. 2016;6:32320. https://doi.org/10.1038/srep32320.CrossRefPubMedPubMedCentral

28.

Ussher JE, van Wilgenburg B, Hannaway RF, Ruustal K, Phalora P, Kurioka A, et al. TLR signaling in human antigen-presenting cells regulates MR1-dependent activation of MAIT cells. Eur J Immunol. 2016;46(7):1600–14. https://doi.org/10.1002/eji.201545969.CrossRefPubMedPubMedCentral

29.

Sattler A, Dang-Heine C, Reinke P, Babel N. IL-15 dependent induction of IL-18 secretion as a feedback mechanism controlling human MAIT-cell effector functions. Eur J Immunol. 2015;45(8):2286–98. https://doi.org/10.1002/eji.201445313.CrossRefPubMed

30.

Willing A, Jäger J, Reinhardt S, Kursawe N, Friese MA. Production of IL-17 by MAIT cells is increased in multiple sclerosis and is associated with IL-7 receptor expression. J Immunol. 2018;200(3):974–82. https://doi.org/10.4049/jimmunol.1701213.CrossRefPubMed

31.

Cole S, Murray J, Simpson C, Okoye R, Tyson K, Griffiths M, et al. Interleukin (IL)-12 and IL-18 synergize to promote MAIT cell IL-17A and IL-17F production independently of IL-23 signaling. Front Immunol. 2020;11: 585134. https://doi.org/10.3389/fimmu.2020.585134.CrossRefPubMedPubMedCentral

32.

van Wilgenburg B, Scherwitzl I, Hutchinson EC, Leng T, Kurioka A, Kulicke C, et al. MAIT cells are activated during human viral infections. Nat Commun. 2016;7:11653. https://doi.org/10.1038/ncomms11653.CrossRefPubMedPubMedCentral

33.

Wilgenburg BV, Loh L, Chen Z, Pediongco TJ, Wang H, Shi M, et al. MAIT cells contribute to protection against lethal influenza infection in vivo. Nat Commun. 2018;9(1):4706. https://doi.org/10.1038/s41467-018-07207-9.CrossRefPubMedPubMedCentral

34.

Sobkowiak MJ, Davanian H, Heymann R, Gibbs A, Emgård J, Dias J, et al. Tissue-resident MAIT cell populations in human oral mucosa exhibit an activated profile and produce IL-17. Eur J Immunol. 2019;49(1):133–43. https://doi.org/10.1002/eji.201847759.CrossRefPubMed

35.

Ichimura M, Hiratsuka K, Ogura N, Utsunomiya T, Sakamaki H, Kondoh T, et al. Expression profile of chemokines and chemokine receptors in epithelial cell layers of oral lichen planus. J Oral Pathol Med. 2006;35(3):167–74. https://doi.org/10.1111/j.1600-0714.2006.00402.x.CrossRefPubMed

36.

Yang JY, Wang F, Zhou G. Characterization and function of circulating mucosal-associated invariant T cells and γδ T cells in oral lichen planus. J Oral Pathol Med. 2022;51(1):74–85. https://doi.org/10.1111/jop.13250.CrossRefPubMed

37.

Tastan C, Karhan E, Zhou W, Fleming E, Voigt AY, Yao X, et al. Tuning of human MAIT cell activation by commensal bacteria species and MR1-dependent T-cell presentation. Mucosal Immunol. 2018;11(6):1591–605. https://doi.org/10.1038/s41385-018-0072-x.CrossRefPubMedPubMedCentral

38.

Ohno S, Tateishi Y, Tatemoto Y, Morishita K, Sasabe E, Yamamoto T. Enhanced expression of toll-like receptor 2 in lesional tissues and peripheral blood monocytes of patients with oral lichen planus. J Dermatol. 2011;38(4):335–44. https://doi.org/10.1111/j.1346-8138.2010.00956.x.CrossRefPubMed

39.

Zhang Y, Liu W, Zhang S, Dan H, Lu R, Wang F, et al. Salivary and serum interleukin-18 in patients with oral lichen planus: a study in an ethnic Chinese population. Inflammation. 2012;35(2):399–404. https://doi.org/10.1007/s10753-011-9327-3.CrossRefPubMed

40.

Fairweather D, Yusung S, Frisancho S, Barrett M, Gatewood S, Steele R, et al. Differential expression of TLR-2 and TLR-4 in the epithelial cells in oral lichen planus. J Immunol. 2003;170(9):4731–7. https://doi.org/10.1016/j.archoralbio.2011.10.013.CrossRefPubMed

41.

He Y, Gong D, Shi C, Shao F, Shi J, Fei J. Dysbiosis of oral buccal mucosa microbiota in patients with oral lichen planus. Oral Dis. 2017;23(5):674–82. https://doi.org/10.1111/odi.12657.CrossRefPubMed

42.

Zhang J, Tan YQ, Wei MH, Ye XJ, Chen GY, Lu R, et al. TLR4-induced B7–H1 on keratinocytes negatively regulates CD4⁺ T cells and CD8⁺ T cells responses in oral lichen planus. Exp Dermatol. 2017;26(5):409–15. https://doi.org/10.1111/exd.13244.CrossRefPubMed

43.

Wang Y, Shang S, Sun Q, Chen J, Du G, Nie H, et al. Increased infiltration of CD11 c⁺/CD123⁺ dendritic cell subsets and upregulation of TLR/IFN-α signaling participate in pathogenesis of oral lichen planus. Oral Surg Oral Med Oral Pathol Oral Radiol. 2018;125(5):459–67. https://doi.org/10.1016/j.oooo.2017.12.003.CrossRefPubMed

44.

Weaver CT, Elson CO, Fouser LA, Kolls JK. The Th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu Rev Pathol. 2013;8:477–512. https://doi.org/10.1146/annurev-pathol-011110-130318.CrossRefPubMed

45.

Veldhoen M. Interleukin 17 is a chief orchestrator of immunity. Nat Immunol. 2017;18(6):612–21. https://doi.org/10.1038/ni.3742.CrossRefPubMed

46.

Parks OB, Pociask DA, Hodzic Z, Kolls JK, Good M. Interleukin-22 signaling in the regulation of intestinal health and disease. Front Cell Dev Biol. 2016;3:85. https://doi.org/10.3389/fcell.2015.00085.CrossRefPubMedPubMedCentral

47.

Fujita H. The role of IL-22 and Th22 cells in human skin diseases. J Dermatol Sci. 2013;72(1):3–8. https://doi.org/10.1016/j.jdermsci.2013.04.028.CrossRefPubMed

48.

Gibbs A, Leeansyah E, Introit A, Paquin-Proulx D, Hasselrot K, Andersson E, et al. MAIT cells reside in the female genital mucosa and are biased towards IL-17 and IL-22 production in response to bacterial stimulation. Mucosal Immunol. 2017;10(1):35–45. https://doi.org/10.1038/mi.2016.30.CrossRefPubMed

49.

Rouxel O, Lehuen A. Mucosal-associated invariant T cells in autoimmune and immune-mediated diseases. Immunol Cell Biol. 2018;96(6):618–29. https://doi.org/10.1111/imcb.12011.CrossRefPubMed

50.

Lu R, Zeng X, Han Q, Lin M, Long L, Dan H, et al. Overexpression and selectively regulatory roles of IL-23/IL-17 axis in the lesions of oral lichen planus. Mediators Inflamm. 2014;2014: 701094. https://doi.org/10.1155/2014/701094.CrossRefPubMedPubMedCentral

51.

Chen J, Feng J, Chen X, Xu H, Zhou Z, Shen X, et al. Immunoexpression of interleukin-22 and interleukin-23 in oral and cutaneous lichen planus lesions: a preliminary study. Mediators Inflamm. 2013;2013: 801974. https://doi.org/10.1155/2013/801974.CrossRefPubMedPubMedCentral

52.

Arora S, Verma M, Gupta SR, Urs AB, Dhakad MS, Kaur R. Phenotypic variability and therapeutic implications of Candida species in patients with oral lichen planus. Biotech Histochem. 2016;91(4):237–41. https://doi.org/10.3109/10520295.2015.1127425.CrossRefPubMed

53.

Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 2010;8(6): e1000407. https://doi.org/10.1371/journal.pbio.1000407.CrossRefPubMedPubMedCentral

54.

Pouralibaba F, Babaloo Z, Pakdel F, Aghazadeh M. Serum level of interleukin 17 in patients with erosive and non erosive oral lichen planus. J Dent Res Dent Clin Dent Prospects. 2013;7(2):91–4. https://doi.org/10.5681/joddd.2013.016.CrossRefPubMedPubMedCentral

55.

Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E, Premel V, et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cell. PLoS Pathog. 2013;9(10): e1003681. https://doi.org/10.1371/journal.ppat.1003681.CrossRefPubMedPubMedCentral

56.

Kurioka A, Ussher JE, Cosgrove C, Clough C, Fergusson JR, Smith K, et al. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol. 2015;8(2):429–40. https://doi.org/10.1038/mi.2014.81.CrossRefPubMed

57.

Shimizu M, Higaki Y, Higaki M, Kawashima M. The role of granzyme B-expressing CD8-positive T cells in apoptosis of keratinocytes in lichen planus. Arch Dermatol Res. 1997;289(9):527–32. https://doi.org/10.1007/s004030050234.CrossRefPubMed

58.

Gade P, Ramachandran G, Maachani UB, Rizzo MA, Okada T, Prywes R, et al. An IFN-γ-stimulated ATF6-C/EBP-β-signaling pathway critical for the expression of death associated protein kinase 1 and induction of autophagy. Proc Natl Acad Sci U S A. 2012;109(26):10316–21. https://doi.org/10.1073/pnas.1119273109.CrossRefPubMedPubMedCentral

59.

MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci U S A. 1997;94(10):5243–8. https://doi.org/10.1073/pnas.94.10.5243.CrossRefPubMedPubMedCentral

60.

Le Bourhis L, Martin E, Péguillet I, Guihot A, Froux N, Coré M, et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol. 2010;11(8):701–8. https://doi.org/10.1038/ni.1890.CrossRefPubMed

61.

Khan A, Farah CS, Savage NW, Walsh LJ, Harbrow DJ, Sugerman PB. Th1 cytokines in oral lichen planus. J Oral Pathol Med. 2003;32(2):77–83. https://doi.org/10.1034/j.1600-0714.2003.00077.x.CrossRefPubMed

62.

Malarkodi T, Sathasivasubramanian S. Quantitative analysis of salivary TNF-α in oral lichen planus patients. Int J Dent. 2015;2015: 283465. https://doi.org/10.1155/2015/283465.CrossRefPubMedPubMedCentral

63.

Ghallab NA, el-Wakeel N, Shaker OG. Levels of salivary IFN-gamma, TNF-alfa, and TNF receptor-2 as prognostic markers in (erosive) oral lichen planus. Mediators Inflamm. 2010;2010: 847632. https://doi.org/10.1155/2010/847632.CrossRefPubMed

64.

Lu R, Zhou G, Du G, Xu X, Yang J, Hu J. Expression of T-bet and GATA-3 in peripheral blood mononuclear cells of patients with oral lichen planus. Arch Oral Biol. 2011;56(5):499–505. https://doi.org/10.1016/j.archoralbio.2010.11.006.CrossRefPubMed

65.

Fall-Dickson JM, Pavletic SZ, Mays JW, Schubert MM. Oral complications of chronic graft-versus-host disease. J Natl Cancer Inst Monogr. 2019;2019(53):lgz007. https://doi.org/10.1093/jncimonographs/lgz007.CrossRefPubMedPubMedCentral

66.

Weng X, Xing Y, Cheng B. Multiple and recurrent squamous cell carcinoma of the oral cavity after graft-versus-host disease. J Oral Maxillofac Surg. 2017;75(9):1899–905. https://doi.org/10.1016/j.joms.2017.02.012.CrossRefPubMed

67.

Blazar BR, Murphy WJ, Abedi M. Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol. 2012;12(6):443–58. https://doi.org/10.1038/nri3212.CrossRefPubMedPubMedCentral

68.

Stikvoort A, Chen Y, Rådestad E, Törlén J, Lakshmikanth T, Björklund A, et al. Combining flow and mass cytometry in the search for biomarkers in chronic graft-versus-host disease. Front Immunol. 2017;8:717. https://doi.org/10.3389/fimmu.2017.00717.CrossRefPubMedPubMedCentral

69.

Bhattacharyya A, Hanafi LA, Sheih A, Golob JL, Srinivasan S, Boeckh MJ, et al. Graft-derived reconstitution of mucosal-associated invariant T cells after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2018;24(2):242–51. https://doi.org/10.1016/j.bbmt.2017.10.003.CrossRefPubMed

70.

van der Waart AB, van der Velden WJ, van Halteren AG, Leenders MJ, Feuth T, Blijlevens NM, et al. Decreased levels of circulating IL17-producing CD161⁺CCR6⁺ T cells are associated with graft-versus-host disease after allogeneic stem cell transplantation. PLoS ONE. 2012;7(12): e50896. https://doi.org/10.1371/journal.pone.0050896.CrossRefPubMedPubMedCentral

71.

Zhao XY, Lv M, Xu LL, Qian X, Huang XJ. Donor Th17 cells and IL-21 may contribute to the development of chronic graft-versus-host disease after allogeneic transplantation. Eur J Immunol. 2013;43(3):838–50. https://doi.org/10.1002/eji.201242816.CrossRefPubMed

72.

Miyazaki Y, Miyake S, Chiba A, Lantz O, Yamamura T. Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int Immunol. 2011;23(9):529–35. https://doi.org/10.1093/intimm/dxr047.CrossRefPubMed

73.

Hiejima E, Kawai T, Nakase H, Tsuruyama T, Morimoto T, Yasumi T, et al. Reduced numbers and proapoptotic features of mucosal-associated invariant T cells as a characteristic finding in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(7):1529–40. https://doi.org/10.1097/MIB.0000000000000397.CrossRefPubMed

74.

Zhang L, Chu J, Yu J, Wei W. Cellular and molecular mechanisms in graft-versus-host disease. J Leukoc Biol. 2016;99(2):279–87. https://doi.org/10.1189/jlb.4RU0615-254RR.CrossRefPubMed

75.

Okamoto S, Fujiwara H, Nishimori H, Matsuoka K, Fujii N, Kondo E, et al. Anti-IL-12/23 p40 antibody attenuates experimental chronic graft-versus-host disease via suppression of IFN-γ/IL-17-producing cells. J Immunol. 2015;194(3):1357–63. https://doi.org/10.4049/jimmunol.1400973.CrossRefPubMed

76.

Wu Y, Bastian D, Schutt S, Nguyen H, Fu J, Heinrichs J, et al. Essential role of interleukin-12/23p40 in the development of graft-versus-host disease in mice. Biol Blood Marrow Transplant. 2015;21(7):1195–204. https://doi.org/10.1016/j.bbmt.2015.03.016.CrossRefPubMedPubMedCentral

77.

Hegde P, Weiss E, Paradis V, Wan J, Mabire M, Sukriti S, et al. Mucosal-associated invariant T cells are a profibrogenic immune cell population in the liver. Nat Commun. 2018;9(1):2146. https://doi.org/10.1038/s41467-018-04450-y.CrossRefPubMedPubMedCentral

78.

Kurioka A, Walker LJ, Klenerman P, Willberg CB. MAIT cells: new guardians of the liver. Clin Transl Immunology. 2016;5(8): e98. https://doi.org/10.1038/cti.2016.51.CrossRefPubMedPubMedCentral

79.

Böttcher K, Rombouts K, Saffioti F, Roccarina D, Rosselli M, Hall A, et al. MAIT cells are chronically activated in patients with autoimmune liver disease and promote profibrogenic hepatic stellate cell activation. Hepatology. 2018;68(1):172–86. https://doi.org/10.1002/hep.29782.CrossRefPubMed

80.

Kyrcz-Krzemień S, Helbig G, Zielińska P, Markiewicz M. The kinetics of mRNA transforming growth factor beta1 expression and its serum concentration in graft-versus-host disease after allogeneic hemopoietic stem cell transplantation for myeloid leukemias. Med Sci Monit. 2011;17(6):CR322-328; https://doi.org/10.12659/msm.881804

81.

Zhang Y, McCormick LL, Gilliam AC. Latency-associated peptide prevents skin fibrosis in murine sclerodermatous graft-versus-host disease, a model for human scleroderma. J Invest Dermatol. 2003;121(4):713–9. https://doi.org/10.1046/j.1523-1747.2003.12517.x.CrossRefPubMed

82.

Park MJ, Moon SJ, Lee EJ, Jung KA, Kim EK, Kim DS, et al. IL-1-IL-17 signaling axis contributes to fibrosis and inflammation in two different murine models of systemic sclerosis. Front Immunol. 2018;9:1611. https://doi.org/10.3389/fimmu.2018.01611.CrossRefPubMedPubMedCentral

83.

Pedersen SJ, Maksymowych WP. The pathogenesis of ankylosing spondylitis: an update. Curr Rheumatol Rep. 2019;21(10):58. https://doi.org/10.1007/s11926-019-0856-3.CrossRefPubMed

84.

Sanz I, Lee FE. B cells as therapeutic targets in SLE. Nat Rev Rheumatol. 2010;6(6):326–37. https://doi.org/10.1038/nrrheum.2010.68.CrossRefPubMedPubMedCentral

85.

Manzel L, Macfarlane DE. CpG-oligodeoxynucleotide supports growth of IL-6-dependent 7TD1 murine hybridoma cells. Life Sci. 1998;62(1):23–7. https://doi.org/10.1016/s0024-3205(97)01034-5.CrossRefPubMed

86.

Korn T, Bettelli E, Gao W, Awasthi A, Jäger A, Strom TB, et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature. 2007;448(7152):484–7. https://doi.org/10.1038/nature05970.CrossRefPubMedPubMedCentral

87.

Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev. 2008;223:87–113. https://doi.org/10.1111/j.1600-065X.2008.00628.x.CrossRefPubMedPubMedCentral

88.

Bennett MS, Trivedi S, Iyer AS, Hale JS, Leung DT. Human mucosal-associated invariant T (MAIT) cells possess capacity for B cell help. J Leukoc Biol. 2017;102(5):1261–9. https://doi.org/10.1189/jlb.4A0317-116R.CrossRefPubMedPubMedCentral

89.

Chiba A, Tamura N, Yoshikiyo K, Murayama G, Kitagaichi M, Yamaji K, et al. Activation status of mucosal-associated invariant T cells reflects disease activity and pathology of systemic lupus erythematosus. Arthritis Res Ther. 2017;19(1):58. https://doi.org/10.1186/s13075-017-1257-5.CrossRefPubMedPubMedCentral

90.

Le Huu D, Matsushita T, Jin G, Hamaguchi Y, Hasegawa M, Takehara K, et al. IL-6 blockade attenuates the development of murine sclerodermatous chronic graft-versus-host disease. J Invest Dermatol. 2012;132(12):2752–61. https://doi.org/10.1038/jid.2012.226.CrossRefPubMed

91.

Markopoulos AK. Current aspects on oral squamous cell carcinoma. Open Dent J. 2012;6:126–30. https://doi.org/10.2174/1874210601206010126.CrossRefPubMedPubMedCentral

92.

Choi S, Myers JN. Molecular pathogenesis of oral squamous cell carcinoma: implications for therapy. J Dent Res. 2008;87(1):14–32. https://doi.org/10.1177/154405910808700104.CrossRefPubMed

93.

Saloura V, Izumchenko E, Zuo Z, Bao R, Korzinkin M, Ozerov I, et al. Immune profiles in primary squamous cell carcinoma of head and neck. Oral Oncol. 2019;96:77–88. https://doi.org/10.1016/j.oraloncology.2019.06.032.CrossRefPubMedPubMedCentral

94.

Ling L, Lin Y, Zheng W, Hong S, Tang X, Zhao P, et al. Circulating and tumor-infiltrating mucosal associated invariant T (MAIT) cells in colorectal cancer patients. Sci Rep. 2016;6:20358. https://doi.org/10.1038/srep20358.CrossRefPubMedPubMedCentral

95.

Won EJ, Ju JK, Cho YN, Jin HM, Park KJ, Kim TJ, et al. Clinical relevance of circulating mucosal-associated invariant T cell levels and their anti-cancer activity in patients with mucosal-associated cancer. Oncotarget 2016;7(46):76274–76290;https://doi.org/10.18632/oncotarget.11187

96.

Kelly J, Minoda Y, Meredith T, Cameron G, Philipp MS, Pellicci DG, et al. Chronically stimulated human MAIT cells are unexpectedly potent IL-13 producers. Immunol Cell Biol. 2019;97(8):689–99. https://doi.org/10.1111/imcb.12281.CrossRefPubMedPubMedCentral

97.

Melo AM, O’Brien AM, Phelan JJ, Kennedy SA, Wood NAW, Veerapen N, et al. Mucosal-associated invariant T cells display diminished effector capacity in oesophageal adenocarcinoma. Front Immunol. 2019;10:1580. https://doi.org/10.3389/fimmu.2019.01580.CrossRefPubMedPubMedCentral

98.

Zabijak L, Attencourt C, Guignant C, Chatelain D, Marcelo P, Marolleau JP, et al. Increased tumor infiltration by mucosal-associated invariant T cells correlates with poor survival in colorectal cancer patients. Cancer Immunol Immunother. 2015;64(12):1601–8. https://doi.org/10.1007/s00262-015-1764-7.CrossRefPubMed

99.

Zhao Y, Shao Q, Peng G. Exhaustion and senescence: two crucial dysfunctional states of T cells in the tumor microenvironment. Cell Mol Immunol. 2020;17(1):27–35. https://doi.org/10.1038/s41423-019-0344-8.CrossRefPubMed

100.

Sakata J, Hirosue A, Yoshida R, Kawahara K, Matsuoka Y, Yamamoto T, et al. HMGA2 contributes to distant metastasis and poor prognosis by promoting angiogenesis in oral squamous cell carcinoma. Int J Mol Sci. 2019;20(10):2473. https://doi.org/10.3390/ijms20102473.CrossRefPubMedCentral

101.

Shivamallappa SM, Venkatraman NT, Shreedhar B, Mohanty L, Shenoy S. Role of angiogenesis in oral squamous cell carcinoma development and metastasis: an immunohistochemical study. Int J Oral Sci. 2011;3(4):216–24. https://doi.org/10.4248/IJOS11077.CrossRefPubMedPubMedCentral

102.

Robinson CJ, Stringer SE. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci. 2001;114(Pt 5):853–65. https://doi.org/10.1242/jcs.114.5.853.CrossRefPubMed

103.

Sahibzada HA, Khurshid Z, Khan RS, Naseem M, Siddique KM, Mali M, et al. Salivary IL-8, IL-6 and TNF-α as potential diagnostic biomarkers for oral cancer. Diagnostics (Basel). 2017;7(2):21. https://doi.org/10.3390/diagnostics7020021.CrossRef

104.

Duan M, Goswami S, Shi JY, Wu LJ, Wang XY, Ma JQ, et al. Activated and exhausted MAIT cells foster disease progression and indicate poor outcome in hepatocellular carcinoma. Clin Cancer Res. 2019;25(11):3304–16. https://doi.org/10.1158/1078-0432.CCR-18-3040.CrossRefPubMed

105.

Ioannidis M, Cerundolo V, Salio M. The immune modulating properties of mucosal-associated invariant T Cells. Front Immunol. 2020;11:1556. https://doi.org/10.3389/fimmu.2020.01556.CrossRefPubMedPubMedCentral

106.

Yan J, Allen S, McDonald E, Das I, Mak JYW, Liu L, et al. MAIT cells promote tumor initiation, growth, and metastases via tumor MR1. Cancer Discov. 2020;10(1):124–41. https://doi.org/10.1158/2159-8290.CD-19-0569.CrossRefPubMed

107.

Jewett A, Head C, Cacalano NA. Emerging mechanisms of immunosuppression in oral cancers. J Dent Res. 2006;85(12):1061–73. https://doi.org/10.1177/154405910608501201.CrossRefPubMed

108.

López-Soto A, Huergo-Zapico L, Acebes-Huerta A, Villa-Alvarez M, Gonzalez S. NKG2D signaling in cancer immunosurveillance. Int J Cancer. 2015;136(8):1741–50. https://doi.org/10.1002/ijc.28775.CrossRefPubMed

109.

Haeryfar SMM, Shaler CR, Rudak PT. Mucosa-associated invariant T cells in malignancies: a faithful friend or formidable foe? Cancer Immunol Immunother. 2018;67(12):1885–96. https://doi.org/10.1007/s00262-018-2132-1.CrossRefPubMed

110.

Zumwalde NA, Haag JD, Gould MN, Gumperz JE. Mucosal associated invariant T cells from human breast ducts mediate a Th17-skewed response to bacterially exposed breast carcinoma cells. Breast Cancer Res. 2018;20(1):111. https://doi.org/10.1186/s13058-018-1036-5.CrossRefPubMedPubMedCentral

111.

McGilvray RW, Eagle RA, Watson NF, Al-Attar A, Ball G, Jafferji I, et al. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res. 2009;15(22):6993–7002. https://doi.org/10.1158/1078-0432.CCR-09-0991.CrossRefPubMedPubMedCentral

112.

Tamaki S, Sanefuzi N, Kawasaki M, Aoki K, Imani Y, Yamasaki Y, et al. Association between soluble MICA levels and disease stage IV oral squamous cell carcinoma in Japanese patients. Hum Immunol. 2008;69(2):88–93. https://doi.org/10.1016/j.humimm.2008.01.010.CrossRefPubMed

113.

Chen S, Ying M, Lin X, Zheng X, Liu C, Liu H. Expression of MICA in oral squamous carcinoma cells and its effect on NK cells. Int J Clin Exp Med. 2015;8(10):18208–12.PubMedPubMedCentral

114.

Flores-Villanueva P, Sobhani N, Wang X, Li Y. MR1-restricted T cells in cancer immunotherapy. Cancers (Basel). 2020;12(8):2145. https://doi.org/10.3390/cancers12082145.CrossRef

115.

Godfrey DI, Koay HF, McCluskey J, Gherardin NA. The biology and functional importance of MAIT cells. Nat Immunol. 2019;20(9):1110–28. https://doi.org/10.1038/s41590-019-0444-8.CrossRefPubMed

116.

Paydarnia N, Khoshtinat Nikkhoi S, Fakhravar A, Mehdiabdol M, Heydarzadeh H, Ranjbar S. Synergistic effect of granzyme B-azurin fusion protein on breast cancer cells. Mol Biol Rep. 2019;46(3):3129–40. https://doi.org/10.1007/s11033-019-04767-x.CrossRefPubMed

117.

Chen XJ, Zhang XQ, Tang MX, Liu Q, Zhou G. Anti-PD-L1-modified and ATRA-loaded nanoparticles for immuno-treatment of oral dysplasia and oral squamous cell carcinoma. Nanomedicine (Lond). 2020;15(10):951–68. https://doi.org/10.2217/nnm-2019-0397.CrossRef

118.

Belai EB, de Oliveira CE, Gasparoto TH, Ramos RN, Torres SA, Garlet GP, et al. PD-1 blockage delays murine squamous cell carcinoma development. Carcinogenesis. 2014;35(2):424–31. https://doi.org/10.1093/carcin/bgt305.CrossRefPubMed

119.

Márton IJ, Kiss C. Overlapping protective and destructive regulatory pathways in apical periodontitis. J Endod. 2014;40(2):155–63. https://doi.org/10.1016/j.joen.2013.10.036.CrossRefPubMed

120.

Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. The inflammasome: a caspase-1 activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009;10(3):241–7. https://doi.org/10.1038/ni.1703.CrossRefPubMedPubMedCentral

121.

Anthony OE, Rachel O. The assessment of CD4 lymphocyte counts in patients with chronic periodontitis in Benin City. Nigeria Asian Pac J Trop Dis. 2012;2:S639–41. https://doi.org/10.1016/S2222-1808(12)60236-9.CrossRef

122.

Ajuz NC, Antunes H, Mendonça TA, Pires FR, Siqueira JF Jr, Armada L. Immunoexpression of interleukin 17 in apical periodontitis lesions. J Endod. 2014;40(9):1400–3. https://doi.org/10.1016/j.joen.2014.03.024.CrossRefPubMed

123.

Hinks TS. Mucosal-associated invariant T cells in autoimmunity, immune-mediated diseases and airways disease. Immunology. 2016;148(1):1–12. https://doi.org/10.1111/imm.12582.CrossRefPubMedPubMedCentral

124.

Figueredo CM, Lira-Junior R, Love RM. T and B cells in periodontal disease: new functions in a complex scenario. Int J Mol Sci. 2019;20(16):3949. https://doi.org/10.3390/ijms20163949.CrossRefPubMedCentral

125.

Nair PN. Pathogenesis of apical periodontitis and the causes of endodontic failures. Crit Rev Oral Biol Med. 2004;15(6):348–81. https://doi.org/10.1177/154411130401500604.CrossRefPubMed

126.

Bowman SJ. Primary Sjogren’s syndrome. Lupus. 2018;27(1):32–5. https://doi.org/10.1177/0961203318801673.CrossRefPubMed

127.

Gan Y, Zhao X, He J, Liu X, Li Y, Sun X, et al. Increased interleukin-17F is associated with elevated autoantibody levels and more clinically relevant than interleukin-17A in primary Sjögren’s syndrome. J Immunol Res. 2017;2017:4768408. https://doi.org/10.1155/2017/4768408.CrossRefPubMedPubMedCentral

Title: MAIT cells and their implication in human oral diseases
Authors: Qin Jiang
Fang Wang
Jing-Ya Yang
Gang Zhou
Publication date: 04-07-2022
Publisher: Springer International Publishing
Keywords: Graft-Versus-Host Disease
Lichen Planus
Cytokines
Graft-Versus-Host Disease
Published in: Inflammation Research / Issue 9/2022
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI: https://doi.org/10.1007/s00011-022-01600-3

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