Mucosal-associated invariant T cells are reduced and functionally immature in the peripheral blood of primary Sjögren's syndrome patients

European Journal of Immunology

Volumn 46, Issue 10, 2016, Pages 2444-2453

  Wang, Jing J ^a,b   Macardle, Cindy ^a,b   Weedon, Helen ^c   Beroukas, Dimitra ^a,b   Banovic, Tatjana ^a,b,d,e,f  

^a FLINDERS MEDICAL CENTRE   (Australia)

^b FLINDERS UNIVERSITY   (Australia)

^c REPATRIATION GENERAL HOSPITAL   (Australia)

^d INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^e ROYAL ADELAIDE HOSPITAL   (Australia)

^f UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Immunity; Mucosal associated invariant T cell; Primary Sj gren syndrome

Indexed keywords

CD4 ANTIGEN; CD40 LIGAND; CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; TUMOR NECROSIS FACTOR;

ADULT; ANTIGEN EXPRESSION; ARTICLE; BLOOD ANALYSIS; CELL MIGRATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; LYMPHOCYTE FUNCTION; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MUCOSAL ASSOCIATED INVARIANT T CELL; PRIORITY JOURNAL; SALIVARY GLAND; SJOEGREN SYNDROME; T LYMPHOCYTE;

EID: 84990853014     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201646300     Document Type: Article

References (53)

1. Moutsopoulos, H. M., Chused, T. M., Mann, D. L., Klippel, J. H., Fauci, A. S., Frank, M. M., Lawley, T. J. et al., Sjogren's syndrome (Sicca syndrome): current issues. Ann. Intern. Med. 1980. 92: 212–226.
2. Brito-Zeron, P. and Ramos-Casals, M., Advances in the understanding and treatment of systemic complications in Sjogren's syndrome. Curr. Opin. Rheumatol. 2014. 26: 520–527.
3. Moreira, I., Teixeira, F., Martins Silva, A., Vasconcelos, C., Farinha, F. and Santos, E., Frequent involvement of central nervous system in primary Sjogren syndrome. Rheumatol. Int. 2015. 35: 289–294.
4. Skopouli, F. N., Fox, P. C., Galanopoulou, V., Atkinson, J. C., Jaffe, E. S. and Moutsopoulos, H. M., T cell subpopulations in the labial minor salivary gland histopathologic lesion of Sjogren's syndrome. J. Rheumatol. 1991. 18: 210–214.
5. Moriyama, M., Tanaka, A., Maehara, T., Furukawa, S., Nakashima, H. and Nakamura, S., T helper subsets in Sjogren's syndrome and IgG4-related dacryoadenitis and sialoadenitis: a critical review. J. Autoimmun. 2014. 51: 81–88.
6. Sudzius, G., Mieliauskaite, D., Butrimiene, I., Siaurys, A., Mackiewicz, Z. and Dumalakiene, I., Activity of T-helper cells in patients with primary Sjogren's syndrome. In Vivo 2013. 27: 263–268.
7. Caretto, A., Ostuni, P. A., Chieco-Bianchi, F., Pedini, B., Spadaccino, A. C., Bagnasco, M., Todesco, S. et al., An immunohistochemical study of immunological phenomena in minor salivary glands in patients with Sjogren's syndrome. Rheumatol. Int. 1995. 15: 51–55.
8. Margulies, D. H., The in-betweeners: MAIT cells join the innate-like lymphocytes gang. J. Exp. Med. 2014. 211: 1501–1502.
9. Lee, O. J., Cho, Y. N., Kee, S. J., Kim, M. J., Jin, H. M., Lee, S. J., Park, K. J. et al., Circulating mucosal-associated invariant T cell levels and their cytokine levels in healthy adults. Exp. Gerontol. 2014. 49: 47–54.
10. Gold, M. C., McLaren, J. E., Reistetter, J. A., Smyk-Pearson, S., Ladell, K., Swarbrick, G. M., Yu, Y. Y. et al., MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J. Exp. Med. 2014. 211: 1601–1610.
11. Lopez-Sagaseta, J., Dulberger, C. L., Crooks, J. E., Parks, C. D., Luoma, A. M., McFedries, A., Van Rhijn, I. et al., The molecular basis for mucosal-associated invariant T cell recognition of MR1 proteins. Proc. Natl. Acad. Sci. U S A 2013. 110: E1771–1778.
12. Eckle, S. B., Birkinshaw, R. W., Kostenko, L., Corbett, A. J., McWilliam, H. E., Reantragoon, R., Chen, Z. et al., A molecular basis underpinning the T cell receptor heterogeneity of mucosal-associated invariant T cells. J. Exp. Med. 2014. 211: 1585–1600.
13. Patel, O., Kjer-Nielsen, L., Le Nours, J., Eckle, S. B., Birkinshaw, R., Beddoe, T., Corbett, A. J. et al., Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat. Commun. 2013. 4: 2142.
14. Grimaldi, D., Le Bourhis, L., Sauneuf, B., Dechartres, A., Rousseau, C., Ouaaz, F., Milder, M. et al., Specific MAIT cell behaviour among innate-like T lymphocytes in critically ill patients with severe infections. Intensive Care Med. 2014. 40: 192–201.
15. Meierovics, A., Yankelevich, W. J. and Cowley, S. C., MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc. Natl. Acad. Sci. U S A 2013. 110: E3119–3128.
16. Reantragoon, R., Kjer-Nielsen, L., Patel, O., Chen, Z., Illing, P. T., Bhati, M., Kostenko, L. et al., Structural insight into MR1-mediated recognition of the mucosal associated invariant T cell receptor. J. Exp. Med. 2012. 209: 761–774.
17. Fernandez, C. S., Amarasena, T., Kelleher, A. D., Rossjohn, J., McCluskey, J., Godfrey, D. I. and Kent, S. J., MAIT cells are depleted early but retain functional cytokine expression in HIV infection. Immunol. Cell Biol. 2015. 93: 177–188.
18. Le Bourhis, L., Dusseaux, M., Bohineust, A., Bessoles, S., Martin, E., Premel, V., Core, M. et al., MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 2013. 9: e1003681.
19. Le Bourhis, L., Martin, E., Peguillet, I., Guihot, A., Froux, N., Core, M., Levy, E. et al., Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 2010. 11: 701–708.
20. Leeansyah, E., Ganesh, A., Quigley, M. F., Sonnerborg, A., Andersson, J., Hunt, P. W., Somsouk, M. et al., Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 2013. 121: 1124–1135.
21. Leung, D. T., Bhuiyan, T. R., Nishat, N. S., Hoq, M. R., Aktar, A., Rahman, M. A., Uddin, T. et al., Circulating mucosal associated invariant T cells are activated in Vibrio cholerae O1 infection and associated with lipopolysaccharide antibody responses. PLoS Negl. Trop. Dis. 2014. 8: e3076.
22. Willing, A., Leach, O. A., Ufer, F., Attfield, K. E., Steinbach, K., Kursawe, N., Piedavent, M. and Friese, M. A., CD8(+) MAIT cells infiltrate into the CNS and alterations in their blood frequencies correlate with IL-18 serum levels in multiple sclerosis. Eur. J. Immunol. 2014. 44: 3119–3128.
23. Brennan, F., Plater-Zyberk, C., Maini, R. N. and Feldmann, M., Coordinate expansion of 'fetal type' lymphocytes (TCR gamma delta+T and CD5+B) in rheumatoid arthritis and primary Sjogren's syndrome. Clin. Exp. Immunol. 1989. 77: 175–178.
24. Caielli, S., Sorini, C. and Falcone, M., The dangerous liaison between iNKT cells and dendritic cells: does it prevent or promote autoimmune diseases? Autoimmunity 2011. 44: 11–22.
25. Dusseaux, M., Martin, E., Serriari, N., Peguillet, I., Premel, V., Louis, D., Milder, M. et al., Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 2011. 117: 1250–1259.
26. Martin, E., Treiner, E., Duban, L., Guerri, L., Laude, H., Toly, C., Premel, V. et al., Stepwise development of MAIT cells in mouse and human. PLoS Biol. 2009. 7: e54.
27. Napier, R. J., Adams, E. J., Gold, M. C. and Lewinsohn, D. M., The role of mucosal associated invariant T cells in antimicrobial immunity. Front. Immunol. 2015. 6: 344.
28. Gold, M. C., Cerri, S., Smyk-Pearson, S., Cansler, M. E., Vogt, T. M., Delepine, J., Winata, E. et al., Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 2010. 8: e1000407.
29. Gao, Y. and Williams, A. P., Role of innate T cells in anti-bacterial immunity. Front. Immunol. 2015. 6: 302.
30. Miyazaki, Y., Miyake, S., Chiba, A., Lantz, O. and Yamamura, T., Mucosal-associated invariant T cells regulate Th1 response in multiple sclerosis. Int. Immunol. 2011. 23: 529–535.
31. Serriari, N. E., Eoche, M., Lamotte, L., Lion, J., Fumery, M., Marcelo, P., Chatelain, D. et al., Innate mucosal-associated invariant T (MAIT) cells are activated in inflammatory bowel diseases. Clin. Exp. Immunol. 2014. 176: 266–274.
32. Eberhard, J. M., Hartjen, P., Kummer, S., Schmidt, R. E., Bockhorn, M., Lehmann, C., Balagopal, A. et al., CD161+ MAIT cells are severely reduced in peripheral blood and lymph nodes of HIV-infected individuals independently of disease progression. PLoS One 2014. 9: e111323.
33. Jiang, J., Wang, X., An, H., Yang, B., Cao, Z., Liu, Y., Su, J. et al., Mucosal-associated invariant T-cell function is modulated by programmed death-1 signaling in patients with active tuberculosis. Am. J. Respir. Crit. Care Med. 2014. 190: 329–339.
34. Huang, S., Martin, E., Kim, S., Yu, L., Soudais, C., Fremont, D. H., Lantz, O. et al., MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution. Proc. Natl. Acad. Sci. U S A 2009. 106: 8290–8295.
35. Huang, S., Gilfillan, S., Kim, S., Thompson, B., Wang, X., Sant, A. J., Fremont, D. H. et al., MR1 uses an endocytic pathway to activate mucosal-associated invariant T cells. J. Exp. Med. 2008. 205: 1201–1211.
36. Huang, S., Gilfillan, S., Cella, M., Miley, M. J., Lantz, O., Lybarger, L., Fremont, D. H. et al., Evidence for MR1 antigen presentation to mucosal-associated invariant T cells. J. Biol. Chem. 2005. 280: 21183–21193.
37. Fleischer, B., Schrezenmeier, H. and Wagner, H., Function of the CD4 and CD8 molecules on human cytotoxic T lymphocytes: regulation of T cell triggering. J. Immunol. 1986. 136: 1625–1628.
38. Gay, D., Maddon, P., Sekaly, R., Talle, M. A., Godfrey, M., Long, E., Goldstein, G. et al., Functional interaction between human T-cell protein CD4 and the major histocompatibility complex HLA-DR antigen. Nature 1987. 328: 626–629.
39. Matsui, Y., Shapiro, H. M., Sheehy, M. J., Christenson, L., Staunton, D. E., Eynon, E. E. and Yunis, E. J., Differential expression of T cell differentiation antigens and major histocompatibility antigens on activated T cells during the cell cycle. Eur. J. Immunol. 1986. 16: 248–251.
40. Beringer, D. X., Kleijwegt, F. S., Wiede, F., van der Slik, A. R., Loh, K. L., Petersen, J., Dudek, N. L. et al., T cell receptor reversed polarity recognition of a self-antigen major histocompatibility complex. Nat. Immunol. 2015. 16: 1153–1161.
41. Miles, J. J., McCluskey, J., Rossjohn, J. and Gras, S., Understanding the complexity and malleability of T-cell recognition. Immunol. Cell Biol. 2015. 93: 433–441.
42. Rist, M. J., Theodossis, A., Croft, N. P., Neller, M. A., Welland, A., Chen, Z., Sullivan, L. C. et al., HLA peptide length preferences control CD8+ T cell responses. J. Immunol. 2013. 191: 561–571.
43. Rossjohn, J., Gras, S., Miles, J. J., Turner, S. J., Godfrey, D. I. and McCluskey, J., T cell antigen receptor recognition of antigen-presenting molecules. Annu. Rev. Immunol. 2015. 33: 169–200.
44. Treiner, E., Duban, L., Moura, I. C., Hansen, T., Gilfillan, S. and Lantz, O., Mucosal-associated invariant T (MAIT) cells: an evolutionarily conserved T cell subset. Microbes Infect. 2005. 7: 552–559.
45. Ussher, J. E., Bilton, M., Attwod, E., Shadwell, J., Richardson, R., de Lara, C., Mettke, E. et al., CD161++ CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur. J. Immunol. 2014. 44: 195–203.
46. Tang, X. Z., Jo, J., Tan, A. T., Sandalova, E., Chia, A., Tan, K. C., Lee, K. H. et al., IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 2013. 190: 3142–3152.
47. Teunissen, M. B., Yeremenko, N. G., Baeten, D. L., Chielie, S., Spuls, P. I., de Rie, M. A., Lantz, O. et al., 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. 2014. 134: 2898–2907.
48. Salerno-Goncalves, R., Rezwan, T. and Sztein, M. B., B cells modulate mucosal associated invariant T cell immune responses. Front. Immunol. 2014. 4: 511.
49. Simoni, Y., Diana, J., Ghazarian, L., Beaudoin, L. and Lehuen, A., Therapeutic manipulation of natural killer (NK) T cells in autoimmunity: are we close to reality? Clin. Exp. Immunol. 2013. 171: 8–19.
50. Germain, C., Meier, A., Jensen, T., Knapnougel, P., Poupon, G., Lazzari, A., Neisig, A. et al., Induction of lectin-like transcript 1 (LLT1) protein cell surface expression by pathogens and interferon-gamma contributes to modulate immune responses. J. Biol. Chem. 2011. 286: 37964–37975.
51. Chua, W. J., Truscott, S. M., Eickhoff, C. S., Blazevic, A., Hoft, D. F. and Hansen, T. H., Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect. Immun. 2012. 80: 3256–3267.
52. Reantragoon, R., Corbett, A. J., Sakala, I. G., Gherardin, N. A., Furness, J. B., Chen, Z., Eckle, S. B. et al., Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 2013. 210: 2305–2320.
53. Smith, M. D., Weedon, H., Papangelis, V., Walker, J., Roberts-Thomson, P. J. and Ahern, M. J., Apoptosis in the rheumatoid arthritis synovial membrane: modulation by disease-modifying anti-rheumatic drug treatment. Rheumatology (Oxford) 2010. 49: 862–875.