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Journal of Immunology Research
Volume 2015, Article ID 307453, 15 pages
http://dx.doi.org/10.1155/2015/307453
Research Article

The Clinical Relevance of IL-17-Producing CD4+CD161+ Cell and Its Subpopulations in Primary Sjögren’s Syndrome

Department of Rheumatology & Immunology, Clinical Immunology Center, Peking University People’s Hospital, 11 Xizhimen South Street, Beijing 100044, China

Received 15 April 2015; Revised 12 August 2015; Accepted 12 August 2015

Academic Editor: Ethan M. Shevach

Copyright © 2015 Linbo Li 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. C. Vitali, S. Bombardieri, R. Jonsson et al., “Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group,” Annals of the Rheumatic Diseases, vol. 61, no. 6, pp. 554–558, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Brito-Zerón and M. Ramos-Casals, “Advances in the understanding and treatment of systemic complications in Sjögren's syndrome,” Current Opinion in Rheumatology, vol. 26, no. 5, pp. 520–527, 2014. View at Publisher · View at Google Scholar
  3. A. Karabiyik, A. B. Peck, and C. Q. Nguyen, “The important role of T cells and receptor expression in Sjögren’s syndrome,” Scandinavian Journal of Immunology, vol. 78, no. 2, pp. 157–166, 2013. View at Publisher · View at Google Scholar
  4. D. Zhou and N. A. McNamara, “Macrophages: important players in primary Sjögren's syndrome?” Expert Review of Clinical Immunology, vol. 10, no. 4, pp. 513–520, 2014. View at Publisher · View at Google Scholar
  5. S. C. A. van Blokland, A. F. Wierenga-Wolf, C. G. van Helden-Meeuwsen et al., “Professional antigen presenting cells in minor salivary glands in Sjögren's syndrome: potential contribution to the histopathological diagnosis?” Laboratory Investigation, vol. 80, no. 12, pp. 1935–1941, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. T. C. Adamson III, R. I. Fox, D. M. Frisman, and F. V. Howell, “Immunohistologic analysis of lymphoid infiltrates in primary Sjogren's syndrome using monoclonal antibodies,” Journal of Immunology, vol. 130, no. 1, pp. 203–208, 1983. View at Google Scholar · View at Scopus
  7. S. Salomonsson, M. V. Jonsson, K. Skarstein et al., “Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjögren’s syndrome,” Arthritis & Rheumatism, vol. 48, no. 11, pp. 3187–3201, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. D. J. Cua, J. Sherlock, Y. Chen et al., “Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain,” Nature, vol. 421, no. 6924, pp. 744–748, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. C. G. Nguyen, H. Yin, B. H. Lee, W. C. Carcamo, J. A. Chiorini, and A. B. Peck, “Pathogenic effect of interleukin-17A in induction of Sjögren's syndrome-like disease using adenovirus-mediated gene transfer,” Arthritis Research and Therapy, vol. 12, no. 6, article R220, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. W. H. Abdulahad, A. M. H. Boots, and C. G. M. Kallenberg, “FoxP3+ CD4+ T cells in systemic autoimmune diseases: the delicate balance between true regulatory T cells and effector Th-17 cells,” Rheumatology, vol. 50, no. 4, pp. 646–656, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Lin, J. Tian, K. Rui et al., “The role of T helper 17 cell subsets in Sjögren's syndrome: similarities and differences between mouse model and humans,” Annals of the Rheumatic Diseases, vol. 73, no. 7, article e43, 2014. View at Publisher · View at Google Scholar
  12. A. Sakai, Y. Sugawara, T. Kuroishi, T. Sasano, and S. Sugawara, “Identification of IL-18 and Th17 cells in salivary glands of patients with Sjögren's syndrome, and amplification of IL-17-mediated secretion of inflammatory cytokines from salivary gland cells by IL-18,” Journal of Immunology, vol. 181, no. 4, pp. 2898–2906, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. G. E. Katsifis, S. Rekka, N. M. Moutsopoulos, S. Pillemer, and S. M. Wahl, “Systemic and local interleukin-17 and linked cytokines associated with Sjögren's syndrome immunopathogenesis,” The American Journal of Pathology, vol. 175, no. 3, pp. 1167–1177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Pozo, M. Valés-Gómez, N. Mavaddat, S. C. Williamson, S. E. Chisholm, and H. Reyburn, “CD161 (human NKR-P1A) signaling in NK cells involves the activation of acid sphingomyelinase,” The Journal of Immunology, vol. 176, no. 4, pp. 2397–2406, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. E. Gulbins and R. Kolesnick, “Raft ceramide in molecular medicine,” Oncogene, vol. 22, no. 45, pp. 7070–7077, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Cosmi, R. De Palma, V. Santarlasci et al., “Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor,” The Journal of Experimental Medicine, vol. 205, no. 8, pp. 1903–1916, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Maggi, V. Santarlasci, M. Capone et al., “CD161 is a marker of all human IL-17-producing T-cell subsets and is induced by RORC,” European Journal of Immunology, vol. 40, no. 8, pp. 2174–2181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Cosmi, R. Cimaz, L. Maggi et al., “Evidence of the transient nature of the Th17 phenotype of CD4+CD161+ T cells in the synovial fluid of patients with juvenile idiopathic arthritis,” Arthritis and Rheumatism, vol. 63, no. 8, pp. 2504–2515, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Miao, J. Geng, K. Zhang et al., “Frequencies of circulating IL-17-producing CD4+CD161+ T cells and CD4+CD161+ T cells correlate with disease activity in rheumatoid arthritis,” Modern Rheumatology, vol. 24, no. 2, pp. 265–570, 2014. View at Publisher · View at Google Scholar
  20. Y. Gernez, R. Tirouvanziam, K. D. Nguyen, L. A. Herzenberg, A. M. Krensky, and K. C. Nadeau, “Altered phosphorylated signal transducer and activator of transcription profile of CD4+CD161+ T cells in asthma: modulation by allergic status and oral corticosteroids,” The Journal of Allergy and Clinical Immunology, vol. 120, no. 6, pp. 1441–1448, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Maggi, M. Capone, F. Giudici et al., “CD4+CD161+ T lymphocytes infiltrate Crohn's disease-associated perianal fistulas and are reduced by anti-TNF-α local therapy,” International Archives of Allergy and Immunology, vol. 161, no. 1, pp. 81–86, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Wang, X. Sun, J. Zhao et al., “Regulatory T cells in rheumatoid arthritis showed increased plasticity toward Th17 but retained suppressive function in peripheral bloodis,” Annals of the Rheumatic Diseases, vol. 74, no. 6, pp. 1293–1301, 2015. View at Publisher · View at Google Scholar
  23. B. Afzali, P. J. Mitchell, F. C. Edozie et al., “CD161 expression characterizes a subpopulation of human regulatory T cells that produces IL-17 in a STAT3-dependent manner,” European Journal of Immunology, vol. 43, no. 8, pp. 2043–2054, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Dong, “TH17 cells in development: an updated view of their molecular identity and genetic programming,” Nature Reviews Immunology, vol. 8, no. 5, pp. 337–348, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. M. S. Maddur, P. Miossec, S. V. Kaveri, and J. Bayry, “Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies,” The American Journal of Pathology, vol. 181, no. 1, pp. 8–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Lin, K. Rui, J. Deng et al., “Th17 cells play a critical role in the development of experimental Sjögren's syndrome,” Annals of the Rheumatic Diseases, vol. 74, no. 6, pp. 1302–1310, 2015. View at Publisher · View at Google Scholar
  27. F. Ciccia, G. Guggino, A. Rizzo et al., “Potential involvement of IL-22 and IL-22-producing cells in the inflamed salivary glands of patients with Sjögren's syndrome,” Annals of the Rheumatic Diseases, vol. 71, no. 2, pp. 295–301, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Fei, W. Zhang, D. Lin et al., “Clinical parameter and Th17 related to lymphocytes infiltrating degree of labial salivary gland in primary Sjögren's syndrome,” Clinical Rheumatology, vol. 33, no. 4, pp. 523–529, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. J. B. Brayer, S. Cha, H. Nagashima et al., “IL-4-dependent effector phase in autoimmune exocrinopathy as defined by the NOD.IL-4-gene knockout mouse model of Sjögren's syndrome,” Scandinavian Journal of Immunology, vol. 54, no. 1-2, pp. 133–140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Gao, S. Killedar, J. G. Cornelius, C. Nguyen, S. Cha, and A. B. Peck, “Sjögren's syndrome in the NOD mouse model is an interleukin-4 time-dependent, antibody isotype-specific autoimmune disease,” Journal of Autoimmunity, vol. 26, no. 2, pp. 90–103, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Q. Nguyen, J.-H. Gao, H. Kim, D. R. Saban, J. G. Cornelius, and A. B. Peck, “IL-4-STAT6 signal transduction-dependent induction of the clinical phase of Sjögren's syndrome-like disease of the nonobese diabetic mouse,” Journal of Immunology, vol. 179, no. 1, pp. 382–390, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Gao, S. Cha, R. Jonsson, J. Opalko, and A. B. Peck, “Detection of anti-type 3 muscarinic acetylcholine receptor autoantibodies in the sera of Sjögren's syndrome patients by use of a transfected cell line assay,” Arthritis & Rheumatism, vol. 50, no. 8, pp. 2615–2621, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Gliozzi, T. Greenwell-Wild, W. Jin et al., “A link between interferon and augmented plasmin generation in exocrine gland damage in Sjögren's syndrome,” Journal of Autoimmunity, vol. 40, no. 1, pp. 122–133, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. X. Zhang, C. S. Schaumburg, T. G. Coursey et al., “CD8+ cells regulate the T helper-17 response in an experimental murine model of sjögren syndrome,” Mucosal Immunology, vol. 7, no. 2, pp. 417–427, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. T. N. Lavoie, C. M. Stewart, K. M. Berg, Y. Li, and C. Q. Nguyen, “Expression of Interleukin-22 in Sjögren's syndrome: significant correlation with disease parameters,” Scandinavian Journal of Immunology, vol. 74, no. 4, pp. 377–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Mitsdoerffer, Y. Lee, A. Jäger et al., “Proinflammatory T helper type 17 cells are effective B-cell helpers,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 32, pp. 14292–14297, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Alunno, F. Carubbi, S. Caterbi et al., “The role of T helper 17 cell subsets in Sjögren's syndrome: similarities and differences between mouse model and humans,” Annals of the Rheumatic Diseases, vol. 73, no. 7, article e42, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. F. B. Vincent, D. Saulep-Easton, W. A. Figgett, K. A. Fairfax, and F. Mackay, “The BAFF/APRIL system: emerging functions beyond B cell biology and autoimmunity,” Cytokine and Growth Factor Reviews, vol. 24, no. 3, pp. 203–215, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Deng, J. Chen, J. Zheng et al., “Association of BAFF and IL-17A with subphenotypes of primary Sjögren's syndrome,” International Journal of Rheumatic Diseases, 2015. View at Publisher · View at Google Scholar
  40. Y. González-Hernández, S. Pedraza-Sánchez, V. Blandón-Vijil et al., “Peripheral blood CD161+ T cells from asthmatic patients are activated during asthma attack and predominantly produce IFN-γ,” Scandinavian Journal of Immunology, vol. 65, no. 4, pp. 368–375, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Y. Kang, H.-O. Kim, S.-K. Kwok et al., “Impact of interleukin-21 in the pathogenesis of primary Sjögren's syndrome: increased serum levels of interleukin-21 and its expression in the labial salivary glands.,” Arthritis Research & Therapy, vol. 13, no. 5, article R179, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Poggi, P. Costa, M. R. Zocchi, and L. Moretta, “NKRP1A molecule is involved in transendothelial migration of CD4+ human T lymphocytes,” Immunology Letters, vol. 57, no. 1–3, pp. 121–123, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. J. J. Campbell, C. E. Brightling, F. A. Symon et al., “Expression of chemokine receptors by lung T cells from normal and asthmatic subjects,” The Journal of Immunology, vol. 166, no. 4, pp. 2842–2848, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. S. A. Basdeo, B. Moran, D. Cluxton et al., “Polyfunctional, pathogenic CD161+ Th17 lineage cells are resistant to regulatory T cell-mediated suppression in the context of autoimmunity,” The Journal of Immunology, vol. 195, no. 2, pp. 528–540, 2015. View at Publisher · View at Google Scholar
  45. M.-F. Liu, L.-H. Lin, C.-T. Weng, and M.-Y. Weng, “Decreased CD4+CD25+bright T cells in peripheral blood of patients with primary Sjögren's syndrome,” Lupus, vol. 17, no. 1, pp. 34–39, 2008. View at Publisher · View at Google Scholar · View at Scopus