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Mediators of Inflammation
Volume 2017, Article ID 2513829, 9 pages
https://doi.org/10.1155/2017/2513829
Research Article

Patients with Systemic Lupus Erythematosus Show Increased Levels and Defective Function of CD69+ T Regulatory Cells

1Department of Immunology, Faculty of Medicine, UASLP, San Luis Potosí, SLP, Mexico
2Research Center for Health Sciences and Biomedicine, UASLP, San Luis Potosí, SLP, Mexico
3Laboratory of Genetics and Molecular Diagnostics, Faculty of Chemical Sciences, UASLP, San Luis Potosí, SLP, Mexico
4Regional Unit of Rheumatology and Osteoporosis, Hospital Central Dr. Ignacio Morones Prieto, San Luis Potosí, SLP, Mexico

Correspondence should be addressed to Roberto González-Amaro; xm.plsau@elaznogr

Received 30 March 2017; Revised 1 August 2017; Accepted 16 August 2017; Published 6 September 2017

Academic Editor: Alex Kleinjan

Copyright © 2017 Marlen Vitales-Noyola et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. G. Puranik and T. B. Niewold, “Immunogenetics of systemic lupus erythematosus: a comprehensive review,” Journal of Autoimmunity, vol. 30, pp. 1–12, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. M. J. Podolska, M. H. Biermann, C. Maueröder, J. Hahn, and M. Hermann, “Inflammatory etiopathogenesis of systemic lupus erythematosus: an update,” Journal of Inflammation Research, vol. 8, pp. 161–171, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Miyara, Y. Ito, and S. Sakaguchi, “Treg-cell therapies for autoimmune rheumatic diseases,” Nature Reviews Rheumatology, vol. 10, no. 9, pp. 543–551, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Schmidt, N. Oberle, and P. H. Krammer, “Molecular mechanisms of Treg-mediated T cell suppression,” Frontiers in Immunology, vol. 3, pp. 1–20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Sakaguchi, K. Wing, Y. Onishi, P. Prieto-Martin, and T. Yamaguchi, “Regulatory T cells: how do they suppress immune responses?” International Immunology, vol. 21, no. 10, pp. 1105–1111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Miyara and S. Sakaguchi, “Natural regulatory T cells: mechanisms of suppression,” Trends in Molecular Medicine, vol. 13, no. 3, pp. 108–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. L. W. Collison, V. Chaturvedi, A. L. Henderson et al., “IL-35-mediated induction of a potent regulatory T cell population,” Nature Immunology, vol. 11, no. 12, pp. 1093–1101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Bin Dhuban and C. A. Piccirillo, “The immunological and genetic basis of immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome,” Current Opinion in Allergy and Clinical Immunology, vol. 15, no. 6, pp. 525–532, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. B. Alvarado-Sánchez, B. Hernández-Castro, D. Portales-Pérez et al., “Regulatory T cells in patients with systemic lupus erythematosus,” Journal of Autoimmunity, vol. 27, no. 2, pp. 110–118, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Battaglia, S. Gregori, R. Bacchetta, and M. G. Roncarolo, “Tr1 cells: from discovery to their clinical application,” Seminars in Immunology, vol. 18, no. 2, pp. 120–127, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. G. Roncarolo, S. Gregori, R. Bacchetta, and M. Battaglia, “Tr1 cells and the counter-regulation of immunity: natural mechanisms and therapeutic applications,” Current Topics in Microbiology and Immunology, vol. 380, pp. 39–68, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. R. K. Dinesh, B. J. Skaggs, A. La Cava, B. H. Hahn, and R. P. Singh, “CD8+ Tregs in lupus, autoimmunity, and beyond,” Autoimmunity Reviews, vol. 9, no. 8, pp. 560–568, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Cebrián, E. Yagüe, M. Rincón, M. López-Botet, M. O. de Landázuri, and F. Sánchez-Madrid, “Triggering of T cell proliferation through AIM, an activation inducer molecule expressed on activated human lymphocytes,” Journal of Experimental Medicine, vol. 168, no. 5, pp. 1621–1637, 1988. View at Google Scholar
  14. Y. Han, Q. Guo, M. Zhang, Z. Chen, and X. Cao, “CD69+ CD4+ CD25- T cells, a new subset of regulatory T cells, suppress T cell proliferation through membrane-bound TGF-β1,” Journal of Immunology, vol. 182, no. 1, pp. 111–120, 2009. View at Google Scholar
  15. M. Vitales-Noyola, L. Doníz-Padilla, C. Alvarez-Quiroga, A. Monsiváis-Urenda, H. Portillo-Salazar, and R. González-Amaro, “Quantitative and functional analysis of CD69+ NKG2D+ T regulatory cells in healthy subjects,” Human Immunology, vol. 76, no. 7, pp. 511–518, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Muñoz-Rodríguez, M. Vitales-Noyola, A. Ramos-Levi, A. Serrano-Somavilla, R. González-Amaro, and M. Marazuela, “Levels of regulatory T cells CD69+NKG2D+IL-10+ are increased in patients with autoimmune thyroid disorders,” Endocrine, vol. 51, no. 3, pp. 478–489, 2016. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Vitales-Noyola, R. Martínez-Martínez, J. P. Loyola-Rodríguez, L. Baranda, P. Niño-Moreno, and R. González-Amaro, “Quantitative and functional analysis of CD69+ T regulatory lymphocytes in patients with periodontal disease,” Journal of Oral Pathology and Medicine, vol. 46, no. 7, pp. 549–557, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Zhu, A. Feng, J. Sun et al., “Increased CD4+CD69+CD25- T cells in patients with hepatocellular carcinoma are associated with tumor progression,” Journal of Gastroenterology and Hepatology, vol. 26, no. 10, pp. 1519–1526, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Bauer, V. Groh, J. Wu et al., “Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA,” Science, vol. 285, no. 5428, pp. 727–729, 1999. View at Google Scholar
  20. Z. Dai, C. J. Turtle, G. C. Booth et al., “Normally occurring NKG2D+ CD4+ T cells are immunosuppressive and inversely correlated with disease activity in juvenile-onset lupus,” Journal of Experimental Medicine, vol. 206, no. 4, pp. 793–805, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. J. B. Canavan, B. Afzali, C. Scottà et al., “A rapid diagnostic test for human regulatory T-cell function to enable regulatory T-cell therapy,” Blood, vol. 119, no. 8, pp. e57–e66, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Sancho, M. Gómez, F. Viedma et al., “CD69 downregulates autoimmune reactivity through active transforming growth factor-beta production in collagen-induced arthritis,” Journal of Clinical Investigation, vol. 112, no. 6, pp. 872–882, 2003. View at Publisher · View at Google Scholar
  23. P. Martín, M. Gómez, A. Lamana et al., “CD69 association with Jak3/Stat5 proteins regulates Th17 cell differentiation,” Molecular and Cellular Biology, vol. 30, no. 20, pp. 4877–4889, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Liappas, G. T. González-Mateo, R. Sánchez-Díaz et al., “Immune-regulatory molecule CD69 controls peritoneal fibrosis,” Journal of the American Society of Nephrology, vol. 27, no. 12, pp. 3561–3576, 2016. View at Publisher · View at Google Scholar
  25. A. Cruz-Adalia, L. J. Jiménez-Borreguero, M. Ramírez-Huesca et al., “CD69 limits the severity of cardiomyopathy after autoimmune myocarditis,” Circulation, vol. 122, no. 14, pp. 1396–1404, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. P. Martín, M. Gómez, A. Lamana et al., “The leukocyte activation antigen CD69 limits allergic asthma and skin contact hypersensitivity,” Journal of Allergy and Clinical Immunology, vol. 126, no. 2, pp. 355–365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. González-Amaro, J. R. Cortés, F. Sánchez-Madrid, and P. Martín, “Is CD69 an effective brake to control inflammatory diseases?” Trends in Molecular Medicine, vol. 19, no. 10, pp. 625–632, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. D. Portales-Pérez, R. González-Amaro, C. Abud-Mendoza, and S. Sánchez-Armáss, “Abnormalities in CD69 expression, cytosolic pH and Ca2+ during activation of lymphocytes from patients with systemic lupus erythematosus,” Lupus, vol. 6, no. 1, pp. 48–56, 1997. View at Publisher · View at Google Scholar
  29. R. González-Amaro and M. Marazuela, “T regulatory (Treg) and T helper 17 (Th17) lymphocytes in thyroid autoimmunity,” Endocrine, vol. 52, no. 1, pp. 30–38, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Facciotti, N. Gagliani, B. Häringer et al., “IL-10-producing forkhead box protein 3-negative regulatory T cells inhibit B-cell responses and are involved in systemic lupus erythematosus,” Journal of Allergy and Clinical Immunology, vol. 137, no. 1, pp. 318–321, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Geginat, P. Larghi, M. Paroni et al., “The light and the dark sides of Interleukin-10 in immune-mediated diseases and cancer,” Cytokine & Growth Factor Reviews, vol. 30, pp. 87–93, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Llorente, W. Zou, Y. Levy et al., “Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus,” Journal of Experimental Medicine, vol. 181, no. 3, pp. 839–844, 1995. View at Google Scholar
  33. J. Alcocer-Varela and D. Alarcón-Segovia, “Decreased production of and response to interleukin-2 by cultured lymphocytes from patients with systemic lupus erythematosus,” Journal of Clinical Investigation, vol. 69, no. 6, pp. 1388–1392, 1982. View at Publisher · View at Google Scholar
  34. S. Sakaguchi, D. A. Vignali, A. Y. Rudensky, R. E. Niec, and H. Waldmann, “The plasticity and stability of regulatory T cells,” Nature Reviews Immunology, vol. 13, no. 6, pp. 461–467, 2013. View at Publisher · View at Google Scholar · View at Scopus