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Journal of Immunology Research
Volume 2016, Article ID 2932531, 8 pages
http://dx.doi.org/10.1155/2016/2932531
Review Article

The Role of γδ T Cells in Systemic Lupus Erythematosus

Department of Rheumatology, The Second Hospital of Shanxi Medical University, Shanxi, Taiyuan 030001, China

Received 3 November 2015; Accepted 13 January 2016

Academic Editor: Baojun Zhang

Copyright © 2016 Meng Wu 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. S. Beetz, D. Wesch, L. Marischen, S. Welte, H.-H. Oberg, and D. Kabelitz, “Innate immune functions of human γδ T cells,” Immunobiology, vol. 213, no. 3-4, pp. 173–182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. M. B. Brenner, J. McLean, D. P. Dialynas et al., “Identification of a putative second T-cell receptor,” Nature, vol. 322, no. 6075, pp. 145–149, 1986. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Tanaka, C. T. Morita, Y. Tanaka, E. Nieves, M. B. Brenner, and B. R. Bloom, “Natural and synthetic non-peptide antigens recognized by human γδ T cells,” Nature, vol. 375, no. 6527, pp. 155–158, 1995. View at Publisher · View at Google Scholar · View at Scopus
  4. 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 Publisher · View at Google Scholar · View at Scopus
  5. J. F. Bukowski, C. T. Morita, and M. B. Brenner, “Human γδ T cells recognize alkylamines derived from microbes, edible plants, and tea: implications for innate immunity,” Immunity, vol. 11, no. 1, pp. 57–65, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. A. C. Hayday, “γδ Cells: a right time and a right place for a conserved third way of protection,” Annual Review of Immunology, vol. 18, pp. 975–1026, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Lawetzky, G. Tiefenthaler, R. Kubo, and T. Hunig, “Identification and characterization of rat T cell subpopulations expressing T cell receptors α/β and γ/δ,” European Journal of Immunology, vol. 20, no. 2, pp. 343–349, 1990. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Itohara, A. G. Farr, J. J. Lafaille et al., “Homing of a γδ thymocyte subset with homogeneous T-cell receptors to mucosal epithelia,” Nature, vol. 343, no. 6260, pp. 754–757, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Goodman and L. Lefrancois, “Expression of the γ-δ T-cell receptor on intestinal CD8+ intraepithelial lymphocytes,” Nature, vol. 333, no. 6176, pp. 855–858, 1988. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Stingl, F. Koning, H. Yamada et al., “Thy-1+ dendritic epidermal cells express T3 antigen and the T-cell receptor γ chain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 13, pp. 4586–4590, 1987. View at Publisher · View at Google Scholar · View at Scopus
  11. P. W. Heald, P. Buckley, A. Gilliam et al., “Correlations of unique clinical, immunotypic, and histologic findings in cutaneous γ/δ T-cell lymphoma,” Journal of the American Academy of Dermatology, vol. 26, no. 5, part 2, pp. 865–870, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. U. Laggner, P. Di Meglio, G. K. Perera et al., “Identification of a novel proinflammatory human skin-homing Vγ9Vδ2 T cell subset with a potential role in psoriasis,” The Journal of Immunology, vol. 187, no. 5, pp. 2783–2793, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Deusch, F. Lüling, K. Reich, M. Classen, H. Wagner, and K. Pfeffer, “A major fraction of human intraepithelial lymphocytes simultaneously expresses the γ/δ T cell receptor, the CD8 accessory molecule and preferentially uses the Vδ1 gene segment,” European Journal of Immunology, vol. 21, no. 4, pp. 1053–1059, 1991. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Groh, A. Brühl, H. El-Gabalawy, J. L. Nelson, and T. Spies, “Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 16, pp. 9452–9457, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. A. R. Kazen and E. J. Adams, “Evolution of the V, D, and J gene segments used in the primate γδ T-cell receptor reveals a dichotomy of conservation and diversity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 29, pp. E332–E340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. H.-J. Gober, M. Kistowska, L. Angman, P. Jenö, L. Mori, and G. De Libero, “Human T cell receptor γ-δ cells recognize endogenous mevalonate metabolites in tumor cells,” Journal of Experimental Medicine, vol. 197, no. 2, pp. 163–168, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Rakasz, A. V. MacDougall, M. T. Zayas et al., “γδ T cell receptor repertoire in blood and colonic mucosa of rhesus macaques,” Journal of Medical Primatology, vol. 29, no. 6, pp. 387–396, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Moser and M. Eberl, “γδ T-APCs: a novel tool for immunotherapy?” Cellular and Molecular Life Sciences, vol. 68, no. 14, pp. 2443–2452, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Li and C. D. Pauza, “Rapamycin increases the yield and effector function of human γδ T cells stimulated in vitro,” Cancer Immunology, Immunotherapy, vol. 60, no. 3, pp. 361–370, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. B. A. Mangan, M. R. Dunne, V. P. O'Reilly et al., “Cutting edge: CD1d restriction and Th1/Th2/Th17 cytokine secretion by human Vδ3 T cells,” The Journal of Immunology, vol. 191, no. 1, pp. 30–34, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Zheng, Y. Liu, Y.-L. Lau, and W. Tu, “γδ-T cells: an unpolished sword in human anti-infection immunity,” Cellular and Molecular Immunology, vol. 10, no. 1, pp. 50–57, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. C. E. Rudd, A. Taylor, and H. Schneider, “CD28 and CTLA-4 coreceptor expression and signal transduction,” Immunological Reviews, vol. 229, no. 1, pp. 12–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. J. E. Smith-Garvin, G. A. Koretzky, and M. S. Jordan, “T cell activation,” Annual Review of Immunology, vol. 27, pp. 591–619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. J. C. Ribot, A. DeBarros, and B. Silva-Santos, “Searching for ‘signal 2’: costimulation requirements of γδ T cells,” Cellular and Molecular Life Sciences, vol. 68, no. 14, pp. 2345–2355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. J. C. Ribot and B. Silva-Santos, “Differentiation and activation of γδ T Lymphocytes: focus on CD27 and CD28 costimulatory receptors,” in Crossroads Between Innate and Adaptive Immunity IV, vol. 785 of Advances in Experimental Medicine and Biology, pp. 95–105, Springer, New York, NY, USA, 2013. View at Publisher · View at Google Scholar
  26. J. C. Ribot, A. Debarros, L. Mancio-Silva, A. Pamplona, and B. Silva-Santos, “B7-CD28 costimulatory signals control the survival and proliferation of murine and human γδ T cells via IL-2 production,” The Journal of Immunology, vol. 189, no. 3, pp. 1202–1208, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Zhang, J.-C. D. Schwartz, X. Guo et al., “Structural and functional analysis of the costimulatory receptor programmed death-1,” Immunity, vol. 20, no. 3, pp. 337–347, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. G. J. Freeman, A. J. Long, Y. Iwai et al., “Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation,” Journal of Experimental Medicine, vol. 192, no. 7, pp. 1027–1034, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. L. M. Francisco, P. T. Sage, and A. H. Sharpe, “The PD-1 pathway in tolerance and autoimmunity,” Immunological Reviews, vol. 236, no. 1, pp. 219–242, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. A. H. Sharpe, E. J. Wherry, R. Ahmed, and G. J. Freeman, “The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection,” Nature Immunology, vol. 8, no. 3, pp. 239–245, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. R. V. Parry, J. M. Chemnitz, K. A. Frauwirth et al., “CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms,” Molecular and Cellular Biology, vol. 25, no. 21, pp. 9543–9553, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Iwasaki, Y. Tanaka, H. Kobayashi et al., “Expression and function of PD-1 in human γδ T cells that recognize phosphoantigens,” European Journal of Immunology, vol. 41, no. 2, pp. 345–355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. F. Ware and J. R. Šedý, “TNF Superfamily Networks: bidirectional and interference pathways of the herpesvirus entry mediator (TNFSF14),” Current Opinion in Immunology, vol. 23, no. 5, pp. 627–631, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Gertner-Dardenne, C. Fauriat, F. Orlanducci et al., “The co-receptor BTLA negatively regulates human Vγ9Vδ2 T-cell proliferation: a potential way of immune escape for lymphoma cells,” Blood, vol. 122, no. 6, pp. 922–931, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Chen, K. Chou, E. Fuchs, W. L. Havran, and R. Boismenu, “Protection of the intestinal mucosa by intraepithelial γδ T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 22, pp. 14338–14343, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. D. A. Pociask, K. Chen, S. M. Choi, T. D. Oury, C. Steele, and J. K. Kolls, “γδ T cells attenuate bleomycin-induced fibrosis through the production of CXCL10,” The American Journal of Pathology, vol. 178, no. 3, pp. 1167–1176, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Li, A. R. Burns, R. E. Rumbaut, and C. W. Smith, “γδ T cells are necessary for platelet and neutrophil accumulation in limbal vessels and efficient epithelial repair after corneal abrasion,” The American Journal of Pathology, vol. 171, no. 3, pp. 838–845, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. R. K. Braun, C. Ferrick, P. Neubauer et al., “IL-17 producing γδ T cells are required for a controlled inflammatory response after bleomycin-induced lung injury,” Inflammation, vol. 31, no. 3, pp. 167–179, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Hao, X. Wu, S. Xia et al., “Current progress in γδ T-cell biology,” Cellular and Molecular Immunology, vol. 7, no. 6, pp. 409–413, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Viey, G. Fromont, B. Escudier et al., “Phosphostim-activated γδ T cells kill autologous metastatic renal cell carcinoma,” The Journal of Immunology, vol. 174, no. 3, pp. 1338–1347, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Boismenu, L. Feng, Y. Y. Xia, J. C. C. Chang, and W. L. Havran, “Chemokine expression by intraepithelial γδ T cells. Implications for the recruitment of inflammatory cells to damaged epithelia,” Journal of Immunology, vol. 157, no. 3, pp. 985–992, 1996. View at Google Scholar · View at Scopus
  42. K. Hudspeth, M. Fogli, D. V. Correia et al., “Engagement of NKp30 on Vδ1 T cells induces the production of CCL3, CCL4, and CCL5 and suppresses HIV-1 replication,” Blood, vol. 119, no. 17, pp. 4013–4016, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Dieli, F. Poccia, M. Lipp et al., “Differentiation of effector/memory Vδ2 T cells and migratory routes in lymph nodes or inflammatory sites,” Journal of Experimental Medicine, vol. 198, no. 3, pp. 391–397, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Sciammas, P. Kodukula, Q. Tang, R. L. Hendricks, and J. A. Bluestone, “T cell receptor-γ/δ cells protect mice from herpes simplex virus type 1-induced lethal encephalitis,” The Journal of Experimental Medicine, vol. 185, no. 11, pp. 1969–1975, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Y. Chen, S. Yao, D. Huang et al., “Phosphoantigen/IL2 expansion and differentiation of Vγ2Vδ2 T cells increase resistance to tuberculosis in nonhuman primates,” PLoS Pathogens, vol. 9, no. 8, Article ID e1003501, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Paul, A. K. Singh, Shilpi, and G. Lal, “Phenotypic and functional plasticity of gamma-delta (γδ) T cells in inflammation and tolerance,” International Reviews of Immunology, vol. 33, no. 6, pp. 537–558, 2014. View at Publisher · View at Google Scholar
  47. H. Li, K. Luo, and C. D. Pauza, “TNF-α is a positive regulatory factor for human Vγ2Vδ2 T cells,” The Journal of Immunology, vol. 181, no. 10, pp. 7131–7137, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Duhindan, A. J. Farley, S. Humphreys, C. Parker, B. Rossiter, and C. G. Brooks, “Patterns of lymphokine secretion amongst mouse γδ T cell clones,” European Journal of Immunology, vol. 27, no. 7, pp. 1704–1712, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. H. M. Ashour and J. Y. Niederkorn, “γδ T cells promote anterior chamber-associated immune deviation and immune privilege through their production of IL-10,” Journal of Immunology, vol. 177, no. 12, pp. 8331–8337, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. K. A. Rhodes, E. M. Andrew, D. J. Newton, D. Tramonti, and S. R. Carding, “A subset of IL-10-producing γδ T cells protect the liver from Listeria-elicited, CD8+ T cell-mediated injury,” European Journal of Immunology, vol. 38, no. 8, pp. 2274–2283, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. J. C. Ribot, A. deBarros, D. J. Pang et al., “CD27 is a thymic determinant of the balance between interferon-γ- and interleukin 17-producing γδ T cell subsets,” Nature Immunology, vol. 10, no. 4, pp. 427–436, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. C. E. Sutton, S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, and K. H. G. Mills, “Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity,” Immunity, vol. 31, no. 2, pp. 331–341, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. B. Martin, K. Hirota, D. J. Cua, B. Stockinger, and M. Veldhoen, “Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals,” Immunity, vol. 31, no. 2, pp. 321–330, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Brandes, K. Willimann, and B. Moser, “Professional antigen-presentation function by human γδ T cells,” Science, vol. 309, no. 5732, pp. 264–268, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. D. S. Leslie, M. S. Vincent, F. M. Spada et al., “CD1-mediated γ/δ T cell maturation of dendritic cells,” Journal of Experimental Medicine, vol. 196, no. 12, pp. 1575–1584, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Collins, J. Wolfe, K. Roessner, C. Shi, L. H. Sigal, and R. C. Budd, “Lyme arthritis synovial γδ T cells instruct dendritic cells via Fas ligand,” The Journal of Immunology, vol. 175, no. 9, pp. 5656–5665, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Conti, R. Casetti, M. Cardone et al., “Reciprocal activating interaction between dendritic cells and pamidronate-stimulated γδ T cells: role of CD86 and inflammatory cytokines,” The Journal of Immunology, vol. 174, no. 1, pp. 252–260, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Dieli, N. Caccamo, S. Meraviglia et al., “Reciprocal stimulation of γδ T cells and dendritic cells during the anti-mycobacterial immune response,” European Journal of Immunology, vol. 34, no. 11, pp. 3227–3235, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. P. Vantourout and A. Hayday, “Six-of-the-best: unique contributions of γδ T cells to immunology,” Nature Reviews Immunology, vol. 13, no. 2, pp. 88–100, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Caccamo, L. Battistini, M. Bonneville et al., “CXCR5 identifies a subset of Vγ9Vδ2 T cells which secrete IL-4 and IL-10 and help B cells for antibody production,” The Journal of Immunology, vol. 177, no. 8, pp. 5290–5295, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Peng, H. Y. Wang, W. Peng, Y. Kiniwa, K. H. Seo, and R.-F. Wang, “Tumor-infiltrating γδ T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway,” Immunity, vol. 27, no. 2, pp. 334–348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. A. A. Kühl, N. N. Pawlowski, K. Grollich et al., “Human peripheral γδ T cells possess regulatory potential,” Immunology, vol. 128, no. 4, pp. 580–588, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Casetti, C. Agrati, M. Wallace et al., “Cutting edge: TGF-β1 and IL-15 induce FOXP3+γδ regulatory T cells in the presence of antigen stimulation,” The Journal of Immunology, vol. 183, no. 6, pp. 3574–3577, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Su, M. Shen, X. Li, and L. Sun, “Roles of γδ T cells in the pathogenesis of autoimmune diseases,” Clinical and Developmental Immunology, vol. 2013, Article ID 985753, 6 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. Y.-H. Chien, C. Meyer, and M. Bonneville, “γδ T cells: first line of defense and beyond,” Annual Review of Immunology, vol. 32, pp. 121–155, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. L. L. Sharp, J. M. Jameson, G. Cauvi, and W. L. Havran, “Dendritic epidermal T cells regulate skin homeostasis through local production of insulin-like growth factor 1,” Nature Immunology, vol. 6, no. 1, pp. 73–79, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Ippolito, D. J. Wallace, D. Gladman et al., “Autoantibodies in systemic lupus erythematosus: comparison of historical and current assessment of seropositivity,” Lupus, vol. 20, no. 3, pp. 250–255, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. B. Volc-Platzer, B. Anegg, S. Milota, W. Pickl, and G. Fischer, “Accumulation of γδ T cells in chronic cutaneous lupus erythematosus,” Journal of Investigative Dermatology, vol. 100, no. 1, pp. S84–S91, 1993. View at Publisher · View at Google Scholar · View at Scopus
  69. S. L. Peng, M. P. Madaio, A. C. Hayday, and J. Craft, “Propagation and regulation of systemic autoimmunity by γδ T cells,” Journal of Immunology, vol. 157, no. 12, pp. 5689–5698, 1996. View at Google Scholar · View at Scopus
  70. E. Robak, H. Niewiadomska, T. Robak et al., “Lymphocytes Tγδ in clinically normal skin and peripheral blood of patients with systemic lupus erythematosus and their correlation with disease activity,” Mediators of Inflammation, vol. 10, no. 4, pp. 179–189, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. Z. Lu, D. Su, D. Wang, X. Li, X. Feng, and L. Sun, “Elevated apoptosis and impaired proliferation contribute to downregulated peripheral γδ T cells in patients with systemic lupus erythematosus,” Clinical and Developmental Immunology, vol. 2013, Article ID 405395, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Lunardi, C. Marguerie, P. Bowness, M. J. Walport, and A. K. So, “Reduction in T γδ cell numbers and alteration in subset distribution in systemic lupus erythematosus,” Clinical and Experimental Immunology, vol. 86, no. 2, pp. 203–206, 1991. View at Google Scholar · View at Scopus
  73. E. Robak, J. Z. Błoński, J. Bartkowiak, H. Niewiadomska, A. Sysa-Jȩdrzejowska, and T. Robak, “Circulating TCR γδ cells in the patients with systemic lupus erythematosus,” Mediators of Inflammation, vol. 8, no. 6, pp. 305–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. L. Wang, N. Kang, J. Zhou et al., “Downregulation of CD94/NKG2A inhibitory receptor on decreased γδ T cells in patients with systemic lupus erythematosus,” Scandinavian Journal of Immunology, vol. 76, no. 1, pp. 62–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Spinozzi, E. Agea, O. Bistoni et al., “T lymphocytes bearing the γδ T cell receptor are susceptible to steroid-induced programmed cell death,” Scandinavian Journal of Immunology, vol. 41, no. 5, pp. 504–508, 1995. View at Publisher · View at Google Scholar · View at Scopus
  76. D.-L. Su, Z.-M. Lu, M.-N. Shen, X. Li, and L.-Y. Sun, “Roles of pro- and anti-inflammatory cytokines in the pathogenesis of SLE,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 347141, 15 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. G. Sireci, E. Champagne, J. J. Fourniè, F. Dieli, and A. Salerno, “Patterns of phosphoantigen stimulation of human Vγ9/Vδ2 T cell clones include Th0 cytokines,” Human Immunology, vol. 58, no. 2, pp. 70–82, 1997. View at Publisher · View at Google Scholar · View at Scopus
  78. D. Wesch, A. Glatzel, and D. Kabelitz, “Differentiation of resting human peripheral blood γδ T cells toward Th1- or Th2-phenotype,” Cellular Immunology, vol. 212, no. 2, pp. 110–117, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. K. J. Ness-Schwickerath, C. Jin, and C. T. Morita, “Cytokine requirements for the differentiation and expansion of IL-17A- and IL-22-producing human Vγ2Vδ2 T cells,” The Journal of Immunology, vol. 184, no. 12, pp. 7268–7280, 2010. View at Publisher · View at Google Scholar
  80. N. Caccamo, C. La Mendola, V. Orlando et al., “Differentiation, phenotype, and function of interleukin-17-producing human Vγ9Vδ2 T cells,” Blood, vol. 118, no. 1, pp. 129–138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Miyake, M. Akahoshi, and H. Nakashima, “Th subset balance in lupus nephritis,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 980286, 7 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. R. R. Bansal, C. R. Mackay, B. Moser, and M. Eberl, “IL-21 enhances the potential of human γδ T cells to provide B-cell help,” European Journal of Immunology, vol. 42, no. 1, pp. 110–119, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Petrasca and D. G. Doherty, “Human Vδ2+γδ T cells differentially induce maturation, cytokine production, and alloreactive T cell stimulation by dendritic cells and B cells,” Frontiers in Immunology, vol. 5, article 650, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. D. A. Ferrick, M. D. Schrenzel, T. Mulvania, B. Hsieh, W. C. Ferlin, and H. Lepper, “Differential production of interferon-γ and interleukin-4 in response to Th1- and Th2-stimulating pathogens by γδ T cells in vivo,” Nature, vol. 373, no. 6511, pp. 255–257, 1995. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Yin, Y. Mao, X. Li et al., “Hyperactivation and in situ recruitment of inflammatory Vδ2 T cells contributes to disease pathogenesis in systemic lupus erythematosus,” Scientific Reports, vol. 5, Article ID 14432, 2015. View at Publisher · View at Google Scholar
  86. C. Albanesi, A. Cavani, and G. Girolomoni, “IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: Synergistic or antagonist effects with IFN-γ and TNF-α,” The Journal of Immunology, vol. 162, no. 1, pp. 494–502, 1999. View at Google Scholar · View at Scopus
  87. A. Doreau, A. Belot, J. Bastid et al., “Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus,” Nature Immunology, vol. 10, no. 7, pp. 778–785, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. D. Kabelitz, A. Glatzel, and D. Wesch, “Antigen recognition by human γδ T lymphocytes,” International Archives of Allergy and Immunology, vol. 122, no. 1, pp. 1–7, 2000. View at Google Scholar · View at Scopus
  89. J. Wu, V. Groh, and T. Spies, “T cell antigen receptor engagement and specificity in the recognition of stress-inducible MHC class I-related chains by human epithelial γδ T cells,” The Journal of Immunology, vol. 169, no. 3, pp. 1236–1240, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Li, N. Kang, X. Zhang et al., “Generation of human regulatory γδ T cells by TCRγδ stimulation in the presence of TGF-β and their involvement in the pathogenesis of systemic lupus erythematosus,” The Journal of Immunology, vol. 186, no. 12, pp. 6693–6700, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Decker, I. Kötter, R. Klein, B. Berner, and H.-G. Rammensee, “Monocyte-derived dendritic cells over-express CD86 in patients with systemic lupus erythematosus,” Rheumatology, vol. 45, no. 9, pp. 1087–1095, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Ding, H. Mehta, W. J. McCune, and M. J. Kaplan, “Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus,” The Journal of Immunology, vol. 177, no. 9, pp. 5878–5889, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. N. Mozaffarian, A. E. Wiedeman, and A. M. Stevens, “Active systemic lupus erythematosus is associated with failure of antigen-presenting cells to express programmed death ligand-1,” Rheumatology, vol. 47, no. 9, pp. 1335–1341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Mak and N. Y. Kow, “The pathology of t cells in systemic lupus erythematosus,” Journal of Immunology Research, vol. 2014, Article ID 419029, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  95. M. J. Shlomchik, J. E. Craft, and M. J. Mamula, “From T to B and back again: positive feedback in systemic autoimmune disease,” Nature Reviews Immunology, vol. 1, no. 2, pp. 147–153, 2001. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Fujihara, J. A. Williams, M. Watanabe, H. Jeon, S. O. Sharrow, and R. J. Hodes, “T cell-B cell thymic cross-talk: maintenance and function of thymic B cells requires cognate CD40-CD40 ligand interaction,” Journal of Immunology, vol. 193, no. 11, pp. 5534–5544, 2014. View at Publisher · View at Google Scholar · View at Scopus
  97. A. D. Henn, J. Rebhahn, M. A. Brown et al., “Modulation of single-cell IgG secretion frequency and rates in human memory B cells by CpG DNA, CD40L, IL-21, and cell division,” The Journal of Immunology, vol. 183, no. 5, pp. 3177–3187, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Nakou, E. D. Papadimitraki, A. Fanouriakis et al., “Interleukin-21 is increased in active systemic lupus erythematosus patients and contributes to the generation of plasma B cells,” Clinical and Experimental Rheumatology, vol. 31, no. 2, pp. 172–179, 2013. View at Google Scholar · View at Scopus
  99. S. Dolff, W. H. Abdulahad, J. Westra et al., “Increase in IL-21 producing T-cells in patients with systemic lupus erythematosus,” Arthritis Research and Therapy, vol. 13, no. 5, article R157, 2011. View at Publisher · View at Google Scholar · View at Scopus