Increased CD226 expression on CD8+ T cells is associated with upregulated cytokine production and endothelial cell injury in patients with systemic sclerosis

Journal of Immunology

Volumn 195, Issue 3, 2015, Pages 892-900

  Ayano, Masahiro ^a   Tsukamoto, Hiroshi ^a   Kohno, Kentaro ^b   Ueda, Naoyasu ^c   Tanaka, Atsushi ^a   Mitoma, Hiroki ^a   Akahoshi, Mitsuteru ^a   Arinobu, Yojiro ^a   Niiro, Hiroaki ^d   Horiuchi, Takahiko ^e   Akashi, Koichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION KYUSHU MEDICAL CENTER   (Japan)

^c MIYAZAKI PREFECTURAL MIYAZAKI HOSPITAL   (Japan)

^d KYUSHU UNIVERSITY HOSPITAL   (Japan)

^e KYUSHU UNIVERSITY BEPPU HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD155 ANTIGEN; CD226 ANTIGEN; CD8 ANTIGEN; COMPLEMENTARY DNA; INTERLEUKIN 13; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; CYTOKINE; T LYMPHOCYTE ANTIGEN;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD226 GENE; CD8+ T LYMPHOCYTE; CELL ADHESION; CELL DAMAGE; CELL MEDIATED CYTOTOXICITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; DISEASE ASSOCIATION; DISEASE SEVERITY; EFFECTOR CELL; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; INTERSTITIAL LUNG DISEASE; MALE; MEMORY T LYMPHOCYTE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYSTEMIC SCLEROSIS; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; COCULTURE; CYTOTOXICITY; DNA MICROARRAY; GENETICS; IMMUNOLOGY; JAPAN; METABOLISM; MIDDLE AGED; PATHOLOGY; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERLEUKIN-13; JAPAN; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SCLERODERMA, SYSTEMIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84937682050     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1403046     Document Type: Article

References (50)

1. Gabrielli, A., E. V. Avvedimento, and T. Krieg. 2009. Scleroderma. N. Engl. J. Med. 360: 1989-2003.
2. Gu, Y. S., J. Kong, G. S. Cheema, C. L. Keen, G. Wick, and M. E. Gershwin. 2008. The immunobiology of systemic sclerosis. Semin. Arthritis Rheum. 38: 132-160.
3. Abraham, D. J., and J. Varga. 2005. Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol. 26: 587-595.
4. Sgonc, R., M. S. Gruschwitz, H. Dietrich, H. Recheis, M. E. Gershwin, and G. Wick. 1996. Endothelial cell apoptosis is a primary pathogenetic event underlying skin lesions in avian and human scleroderma. J. Clin. Invest. 98: 785-792.
5. Baraut, J., L. Michel, F. Verrecchia, and D. Farge. 2010. Relationship between cytokine profiles and clinical outcomes in patients with systemic sclerosis. Autoimmun. Rev. 10: 65-73.
6. Fuschiotti, P., A. T. Larregina, J. Ho, C. Feghali-Bostwick, and T. A. Medsger, Jr. 2013. Interleukin-13-producing CD8+ T cells mediate dermal fibrosis in patients with systemic sclerosis. Arthritis Rheum. 65: 236-246.
7. Luzina, I. G., S. P. Atamas, R. Wise, F. M. Wigley, J. Choi, H. Q. Xiao, and B. White. 2003. Occurrence of an activated, profibrotic pattern of gene expression in lung CD8+ T cells from scleroderma patients. Arthritis Rheum. 48: 2262-2274.
8. Lympany, P. A., A. M. Southcott, K. I. Welsh, C. M. Black, A. W. Boylston, and R. M. du Bois. 1999. T-cell receptor gene usage in patients with fibrosing alveolitis and control subjects. Eur. J. Clin. Invest. 29: 173-181.
9. Gustafsson, R., T. H. Tötterman, L. Klareskog, and R. Hällgren. 1990. Increase in activated T cells and reduction in suppressor inducer T cells in systemic sclerosis. Ann. Rheum. Dis. 49: 40-45.
10. Tiev, K. P., J. Abriol, M. C. Burland, D. Antonelli, D. Klatzmann, J. Cabane, and O. Boyer. 2005. T cell repertoire in patients with stable scleroderma. Clin. Exp. Immunol. 139: 348-354.
11. Sakkas, L. I., and C. D. Platsoucas. 2004. Is systemic sclerosis an antigen-driven T cell disease? Arthritis Rheum. 50: 1721-1733.
12. Fuschiotti, P., T. A. Medsger, Jr., and P. A. Morel. 2009. Effector CD8+ T cells in systemic sclerosis patients produce abnormally high levels of interleukin-13 associated with increased skin fibrosis. Arthritis Rheum. 60: 1119-1128.
13. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
14. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
15. Oertelt, S., C. Selmi, P. Invernizzi, M. Podda, and M. E. Gershwin. 2005. Genes and goals: an approach to microarray analysis in autoimmunity. Autoimmun. Rev. 4: 414-422.
16. Lyons, P. A., M. Koukoulaki, A. Hatton, K. Doggett, H. B. Woffendin, A. N. Chaudhry, and K. G. C. Smith. 2007. Microarray analysis of human leucocyte subsets: the advantages of positive selection and rapid purification. BMC Genomics 8: 64.
17. Masi, A. T., G. P. Rodnan, and T. A. Medsger. 1980. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Arthritis Rheum. 23: 581-590.
18. LeRoy, E. C., C. Black, R. Fleischmajer, S. Jablonska, T. Krieg, T. A. Medsger, Jr., N. Rowell, and F. Wollheim. 1988. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J. Rheumatol. 15: 202-205.
19. Clements, P. J., P. A. Lachenbruch, J. R. Seibold, B. Zee, V. D. Steen, P. Brennan, A. J. Silman, N. Allegar, J. Varga, M. Massa, et al. 1993. Skin thickness score in systemic sclerosis: an assessment of interobserver variability in 3 independent studies. J. Rheumatol. 20: 1892-1896.
20. Medsger, T. A., Jr., S. Bombardieri, L. Czirjak, R. Scorza, A. Della Rossa, and W. Bencivelli. 2003. Assessment of disease severity and prognosis. Clin. Exp. Rheumatol. 21(3, Suppl 29)S42-S46.
21. Goh, N. S. L., S. R. Desai, S. Veeraraghavan, D. M. Hansell, S. J. Copley, T. M. Maher, T. J. Corte, C. R. Sander, J. Ratoff, A. Devaraj, et al. 2008. Interstitial lung disease in systemic sclerosis: a simple staging system. Am. J. Respir. Crit. Care Med. 177: 1248-1254.
22. Sasaki, E., M. Nakamura, and K. Kida. 2001. Reference values for spirogram and blood gas analysis in Japanese non-smoking healthy adults. J. Jpn. Respir. Soc. 39: 383-399.
23. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
24. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
25. Smyth, G. K. 2005. Limma: linear models for microarray data. In Bioinformatics and computational biology solutions using R and Bioconductor. R. Gentleman, V. J. Carey, W. Huber, R. A. Irizarry, and S. Dudoit, eds. Springer, New York, NY, p. 397-420.
26. Huang, D. W., B. T. Sherman, Q. Tan, J. R. Collins, W. G. Alvord, J. Roayaei, R. Stephens, M. W. Baseler, H. C. Lane, and R. A. Lempicki. 2007. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 8: R183.
27. Huang, W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
28. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
29. Lecoeur, H., M. Février, S. Garcia, Y. Rivière, and M. L. Gougeon. 2001. A novel flow cytometric assay for quantitation and multiparametric characterization of cell-mediated cytotoxicity. J. Immunol. Methods 253: 177-187.
30. Dieudé, P., M. Guedj, M. E. Truchetet, J. Wipff, L. Revillod, G. Riemekasten, M. Matucci-Cerinic, I. Melchers, E. Hachulla, P. Airo, et al. 2011. Association of the CD226 Ser(307) variant with systemic sclerosis: evidence of a contribution of costimulation pathways in systemic sclerosis pathogenesis. Arthritis Rheum. 63: 1097-1105.
31. Cosmi, L., F. Annunziato, M. Galli, R. Maggi, K. Nagata, and S. Romagnani. 2000. CRTH2 is the most reliable marker for the detection of circulating human type 2 Th and type 2 T cytotoxic cells in health and disease. Eur. J. Immunol. 30: 2972-2979.
32. Wynn, T. A. 2003. IL-13 effector functions. Annu. Rev. Immunol. 21: 425-456.
33. Shibuya, A., D. Campbell, C. Hannum, H. Yssel, K. Franz-Bacon, T. McClanahan, T. Kitamura, J. Nicholl, G. R. Sutherland, L. L. Lanier, and J. H. Phillips. 1996. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4: 573-581.
34. Shibuya, A., S. Tahara-Hanaoka, and K. Shibuya. 2005. DNAM-1 (CD226): A Two-Sword Fencer for Innate and Adaptive Immunity. Curr. Med. Chem. 4: 53-58.
35. Bottino, C., R. Castriconi, D. Pende, P. Rivera, M. Nanni, B. Carnemolla, C. Cantoni, J. Grassi, S. Marcenaro, N. Reymond, et al. 2003. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198: 557-567.
36. Tahara-Hanaoka, S., K. Shibuya, Y. Onoda, H. Zhang, S. Yamazaki, A. Miyamoto, S. Honda, L. L. Lanier, and A. Shibuya. 2004. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). Int. Immunol. 16: 533-538.
37. Chan, C. J., D. M. Andrews, and M. J. Smyth. 2012. Receptors that interact with nectin and nectin-like proteins in the immunosurveillance and immunotherapy of cancer. Curr. Opin. Immunol. 24: 246-251.
38. Bossini-Castillo, L., C. P. Simeon, L. Beretta, J. C. Broen, M. C. Vonk, R. Ríos-Fernández, G. Espinosa, P. Carreira, M. T. Camps, M. J. Castillo, et al; Spanish Scleroderma Group. 2012. A multicenter study confirms CD226 gene association with systemic sclerosis-related pulmonary fibrosis. Arthritis Res. Ther. 14: R85.
39. Avouac, J., M. Elhai, M. Tomcik, B. Ruiz, M. Friese, M. Piedavent, M. Colonna, G. Bernhardt, A. Kahan, G. Chiocchia, et al. 2013. Critical role of the adhesion receptor DNAX accessory molecule-1 (DNAM-1) in the development of inflammation-driven dermal fibrosis in a mouse model of systemic sclerosis. Ann. Rheum. Dis. 72: 1089-1098.
40. Maier, L. M., and D. A. Hafler. 2009. Autoimmunity risk alleles in costimulation pathways. Immunol. Rev. 229: 322-336.
41. Wynn, T. A. 2008. Cellular and molecular mechanisms of fibrosis. J. Pathol. 214: 199-210.
42. Fuschiotti, P. 2011. Role of IL-13 in systemic sclerosis. Cytokine 56: 544-549.
43. Greenblatt, M. B., and A. O. Aliprantis. 2013. The immune pathogenesis of scleroderma: context is everything. Curr. Rheumatol. Rep. 15: 297.
44. Shibuya, K., J. Shirakawa, T. Kameyama, S. Honda, S. Tahara-Hanaoka, A. Miyamoto, M. Onodera, T. Sumida, H. Nakauchi, H. Miyoshi, and A. Shibuya. 2003. CD226 (DNAM-1) is involved in lymphocyte functionassociated antigen 1 costimulatory signal for naive T cell differentiation and proliferation. J. Exp. Med. 198: 1829-1839.
45. Dardalhon, V., A. S. Schubart, J. Reddy, J. H. Meyers, L. Monney, C. A. Sabatos, R. Ahuja, K. Nguyen, G. J. Freeman, E. A. Greenfield, et al. 2005. CD226 is specifically expressed on the surface of Th1 cells and regulates their expansion and effector functions. J. Immunol. 175: 1558-1565.
46. Lozano, E., N. Joller, Y. Cao, V. K. Kuchroo, and D. A. Hafler. 2013. The CD226/CD155 interaction regulates the proinflammatory (Th1/Th17)/antiinflammatory (Th2) balance in humans. J. Immunol. 191: 3673-3680.
47. Sgonc, R., M. S. Gruschwitz, G. Boeck, N. Sepp, J. Gruber, and G. Wick. 2000. Endothelial cell apoptosis in systemic sclerosis is induced by antibody-dependent cell-mediated cytotoxicity via CD95. Arthritis Rheum. 43: 2550-2562.
48. Kahaleh, M. B., P. S. Fan, and T. Otsuka. 1999. Gammadelta receptor bearing T cells in scleroderma: enhanced interaction with vascular endothelial cells in vitro. Clin. Immunol. 91: 188-195.
49. Ramsbottom, K. M., E. D. Hawkins, R. Shimoni, M. McGrath, C. J. Chan, S. M. Russell, M. J. Smyth, and J. Oliaro. 2014. Cutting edge: DNAX accessory molecule 1-deficient CD8+ T cells display immunological synapse defects that impair antitumor immunity. J. Immunol. 192: 553-557.
50. Gilfillan, S., C. J. Chan, M. Cella, N. M. Haynes, A. S. Rapaport, K. S. Boles, D. M. Andrews, M. J. Smyth, and M. Colonna. 2008. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J. Exp. Med. 205: 2965-2973.