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Clinical and Developmental Immunology
Volume 2013, Article ID 459210, 11 pages
http://dx.doi.org/10.1155/2013/459210
Research Article

Decreased CD127 Expression on CD4+ T-Cells and Elevated Frequencies of CD4+CD25+CD127− T-Cells in Children with Long-Lasting Type 1 Diabetes

1Department of Regenerative Medicine and Immune Regulation, Medical University of Bialystok, 15-269 Bialystok, Poland
2Department of Allergology and Internal Medicine, University of Bialystok, 15-276 Bialystok, Poland
3Department of Pediatrics, Endocrinology, Diabetology with Cardiology Division, Medical University of Bialystok, 15-274 Bialystok, Poland
4Department of Hematological Diagnostics, Medical University of Bialystok, 15-274 Bialystok, Poland
5Department of Immunology, Medical University of Bialystok, 15-276 Bialystok, Poland
6Department of Endocrinology, Diabetology and Internal Medicine, Medical University of Bialystok, 15-276 Bialystok, Poland
7Department of Statistics and Medical Informatics, Medical University of Bialystok, 15-295 Bialystok, Poland

Received 24 July 2013; Revised 28 September 2013; Accepted 1 October 2013

Academic Editor: Mario Clerici

Copyright © 2013 Marcin Moniuszko 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. M. Cnop, N. Welsh, J. C. Jonas, A. Jorns, S. Lenzen, and D. L. Eizirik, “Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities,” Diabetes, vol. 54, no. 2, pp. S97–S107, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Faideau, E. Larger, F. Lepault, J. C. Carel, and C. Boitard, “Role of beta-cells in type 1 diabetes pathogenesis,” Diabetes, vol. 54, no. 2, pp. S87–S96, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. K. S. Schluns, W. C. Kieper, S. C. Jameson, and L. Lefrançois, “Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo,” Nature Immunology, vol. 1, no. 5, pp. 426–432, 2000. View at Google Scholar · View at Scopus
  4. N. Chetoui, M. Boisvert, S. Gendron, and F. Aoudjit, “Interleukin-7 promotes the survival of human CD4+ effector/memory T cells by up-regulating Bcl-2 proteins and activating the JAK/STAT signalling pathway,” Immunology, vol. 130, no. 3, pp. 418–426, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. T. J. Fry and C. L. Mackall, “The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance,” Journal of Immunology, vol. 174, no. 11, pp. 6571–6576, 2005. View at Google Scholar · View at Scopus
  6. S. A. Koesters, J. B. Alimonti, C. Wachihi et al., “IL-7R alpha expression on CD4+ T lymphocytes decreases with HIV disease progression and inversely correlates with immune activation,” European Journal of Immunology, vol. 36, no. 2, pp. 336–344, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. D. J. Hartigan-O'Connor, C. Poon, E. Sinclair, and J. M. McCune, “Human CD4+ regulatory T cells express lower levels of the IL-7 receptor alpha chain (CD127), allowing consistent identification and sorting of live cells,” Journal of Immunological Methods, vol. 319, no. 1–2, pp. 41–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Sakaguchi, M. Miyara, C. M. Costantino, and D. A. Hafler, “FOXP3 + regulatory T cells in the human immune system,” Nature Reviews Immunology, vol. 10, no. 7, pp. 490–500, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Kukreja, G. Cost, J. Marker et al., “Multiple immuno-regulatory defects in type-1 diabetes,” Journal of Clinical Investigation, vol. 109, no. 1, pp. 131–140, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. W. Luczynski, N. Wawrusiewicz-Kurylonek, A. Stasiak-Barmuta et al., “Diminished expression of ICOS, GITR and CTLA-4 at the mRNA level in T regulatory cells of children with newly diagnosed type 1 diabetes,” Acta Biochimica Polonica, vol. 56, no. 2, pp. 361–370, 2009. View at Google Scholar · View at Scopus
  11. M. Ryba, N. Marek, L. Hak et al., “Anti-TNF rescue CD4(+)Foxp3(+) regulatory T cells in patients with type 1 diabetes from effects mediated by TNF,” Cytokine, vol. 55, no. 3, pp. 353–361, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Ryba, L. Hak, K. Zorena, M. Myoeliwiec, and J. Myoeliwska, “CD4+Foxp3+ regulatory T lymphocytes expressing CD62L in patients with long-standing diabetes type 1,” Central-European Journal of Immunology, vol. 34, no. 2, pp. 90–93, 2009. View at Google Scholar · View at Scopus
  13. N. Marek-Trzonkowska, M. Mysliwiec, A. Dobyszuk et al., “Administration of CD4+CD25highCD127(−) regulatory T cells preserves beta-cell function in type 1 diabetes in children,” Diabetes Care, vol. 35, pp. 1817–1820, 2012. View at Google Scholar
  14. A. M. Crawley and J. B. Angel, “The influence of HIV on CD127 expression and its potential implications for IL-7 therapy,” Seminars in Immunology, vol. 24, pp. 231–240, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Moniuszko, Y. Edghill-Smith, D. Venzon et al., “Decreased number of CD4+ and CD8+ T cells that express the interleukin-7 receptor in blood and tissues of SIV-infected macaques,” Virology, vol. 356, no. 1–2, pp. 188–197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. E. M. Faller, S. M. Sugden, M. J. McVey, J. A. Kakal, and P. A. MacPherson, “Soluble HIV Tat protein removes the IL-7 receptor alpha-chain from the surface of resting CD8 T cells and targets it for degradation,” Journal of Immunology, vol. 185, no. 5, pp. 2854–2866, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. S. A. K. Kiazyk and K. R. Fowke, “Loss of CD127 expression links immune activation and CD4+ T cell loss in HIV infection,” Trends in Microbiology, vol. 16, no. 12, pp. 567–573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Nemes, E. Lugli, M. Nasi et al., “Immunophenotype of HIV+ patients during CD4 cell-monitored treatment interruption: role of the IL-7/IL-7 receptor system,” AIDS, vol. 20, no. 16, pp. 2021–2032, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Rethi, C. Fluur, A. Atlas et al., “Loss of IL-7R alpha is associated with CD4 T-cell depletion, high interleukin-7 levels and CD28 down-regulation in HIV infected patients,” AIDS, vol. 19, no. 18, pp. 2077–2086, 2005. View at Google Scholar · View at Scopus
  20. M. Moniuszko, K. Kowal, M. Jeznach et al., “Phenotypic correlations between monocytes and CD4+ T cells in allergic patients,” International Archives of Allergy and Immunology, vol. 161, pp. 131–141, 2013. View at Google Scholar
  21. N. E. Aerts, E. J. Dombrecht, D. G. Ebo, C. H. Bridts, W. J. Stevens, and L. S. De Clerck, “Activated T cells complicate the identification of regulatory T cells in rheumatoid arthritis,” Cellular Immunology, vol. 251, no. 2, pp. 109–115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. S. A. Y. Hartgring, C. R. Willis, D. Alcorn et al., “Blockade of the interleukin-7 receptor inhibits collagen-induced arthritis and is associated with reduction of T cell activity and proinflammatory mediators,” Arthritis and Rheumatism, vol. 62, no. 9, pp. 2716–2725, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Penaranda, W. Kuswanto, J. Hofmann et al., “IL-7 receptor blockade reverses autoimmune diabetes by promoting inhibition of effector/memory T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 12668–12673, 2012. View at Google Scholar
  24. L. F. Lee, K. Logronio, G. H. Tu et al., “Anti-IL-7 receptor-alpha reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 12674–12679, 2012. View at Google Scholar
  25. J. Nilsson and G. K. Hansson, “Autoimmunity in atherosclerosis: a protective response losing control?” Journal of Internal Medicine, vol. 263, no. 5, pp. 464–478, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Blasi, “The autoimmune origin of atherosclerosis,” Atherosclerosis, vol. 201, no. 1, pp. 17–32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Nilsson, E. Bengtsson, G. N. Fredrikson, and H. Björkbacka, “Inflammation and immunity in diabetic vascular complications,” Current Opinion in Lipidology, vol. 19, no. 5, pp. 519–524, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. T. M. Triolo, T. K. Armstrong, K. McFann et al., “Additional autoimmune disease found in 33% of patients at type 1 diabetes onset,” Diabetes Care, vol. 34, no. 5, pp. 1211–1213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Warncke, E. E. Fröhlich-Reiterer, A. Thon, S. E. Hofer, D. Wiemann, and R. W. Holl, “Polyendocrinopathy in children, adolescents, and young adults with type 1 diabetes: a multicenter analysis of 28,671 patients from the German/Austrian DPV-Wiss database,” Diabetes Care, vol. 33, no. 9, pp. 2010–2012, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Glowinska-Olszewska, M. Moniuszko, A. Hryniewicz et al., “Relationship between circulating endothelial progenitor cells and endothelial dysfunction in children with type 1 diabetes: a novel paradigm of early atherosclerosis in high-risk young patients,” European Journal of Endocrinology, vol. 168, pp. 153–161, 2013. View at Google Scholar
  31. M. C. Corretti, T. J. Anderson, E. J. Benjamin et al., “International Brachial Artery Reactivity Task Force. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force,” Journal of the American College of Cardiology, vol. 39, pp. 257–265, 2002. View at Google Scholar
  32. R. Mallone and P. Van Endert, “T cells in the pathogenesis of type 1 diabetes,” Current Diabetes Reports, vol. 8, no. 2, pp. 101–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Hedman, M. Faresjo, S. Axelsson, J. Ludvigsson, and R. Casas, “Impaired CD4(+) and CD8(+) T cell phenotype and reduced chemokine secretion in recent-onset type 1 diabetic children,” Clinical and Experimental Immunology, vol. 152, no. 3, pp. 360–368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Lindley, C. M. Dayan, A. Bishop, B. O. Roep, M. Peatman, and T. I. M. Tree, “Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes,” Diabetes, vol. 54, no. 1, pp. 92–99, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Viglietta, C. Baecher-Allan, H. L. Weiner, and D. A. Hafler, “Loss of functional suppression by CD4(+)CD25(+) regulatory T-cells in patients with multiple sclerosis,” Journal of Experimental Medicine, vol. 199, no. 7, pp. 971–979, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Holmen, A. Lundgren, S. Lundin et al., “Functional CD4(+)CD25(high) regulatory T cells are enriched in the colonic mucosa of patients with active ulcerative colitis and increase with disease activity,” Inflammatory Bowel Diseases, vol. 12, no. 6, pp. 447–456, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Taflin, M. Miyara, D. Nochy et al., “FoxP3(+) regulatory T cells suppress early stages of granuloma formation but have little impact on sarcoidosis lesions,” American Journal of Pathology, vol. 174, no. 2, pp. 497–508, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Ryba-Stanisławowska, M. Skrzypkowska, M. Myśliwiec et al., “Loss of the balance between CD4(+)Foxp3(+) regulatory T cells and CD4(+)IL17A(+) Th17 cells in patients with type 1 diabetes,” Human Immunology, vol. 74, pp. 701–707, 2013. View at Google Scholar
  39. C. Zeng, X. Shi, B. Zhang et al., “The imbalance of Th17/Th1/Tregs in patients with type 2 diabetes: relationship with metabolic factors and complications,” Journal of Molecular Medicine, vol. 90, no. 2, pp. 175–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Schwartzenberg, A. Mor, G. Luboshits et al., “Association between circulating early endothelial progenitors and CD4+CD25+ regulatory T cells: a possible cross-talk between immunity and angiogenesis?” American Journal of Immunology, vol. 1, pp. 143–147, 2005. View at Google Scholar
  41. M. A. Zimmerman and S. C. Flores, “Autoimmune-mediated oxidative stress and endothelial dysfunction: implications of accelerated vascular injury in type I diabetes,” Journal of Surgical Research, vol. 155, no. 1, pp. 173–178, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. X. J. Pan, X. L. Yuan, Y. X. Zheng et al., “Increased CD45RA+FOXP3low regulatory T cells with impaired suppressive function in patients with systemic lupus erythematosus,” Plos ONE, vol. 7, no. 4, Article ID e34662, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Cao, R. van Vollenhoven, L. Klareskog, C. Trollmo, and V. Malmström, “CD25(bright)CD4(+) regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease,” Arthritis Research and Therapy, vol. 6, no. 4, pp. R335–346, 2004. View at Google Scholar · View at Scopus
  44. B. Alvarado-Sanchez, B. Hernandez-Castro, D. Portales-Perez et al., “Regulatory T cells in patients with systemic lupus erythematosus,” Journal of Autoimmunity, vol. 27, pp. 110–118, 2006. View at Google Scholar
  45. T. Brusko, C. Wasserfall, K. McGrail et al., “No alterations in the frequency of FOXP3(+) regulatory T-cells in type 1 diabetes,” Diabetes, vol. 56, no. 3, pp. 604–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Nilsson, M. Wigren, and P. K. Shah, “Regulatory T cells and the control of modified lipoprotein autoimmunity-driven atherosclerosis,” Trends in Cardiovascular Medicine, vol. 19, no. 8, pp. 272–276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Nilsson, G. N. Fredrikson, H. Björkbacka, K.-Y. Chyu, and P. K. Shah, “Vaccines modulating lipoprotein autoimmunity as a possible future therapy for cardiovascular disease,” Journal of Internal Medicine, vol. 266, no. 3, pp. 221–231, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. B. Yang, N. Danke, M. Roti et al., “CD4+ T cells from type 1 diabetic and healthy subjects exhibit different thresholds of activation to a naturally processed proinsulin epitope,” Journal of Autoimmunity, vol. 31, no. 1, pp. 30–41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Aarnisalo, A. Treszl, P. Svec et al., “Reduced CD4(+)T cell activation in children with type 1 diabetes carrying the PTPN22/Lyp 620Trp variant,” Journal of Autoimmunity, vol. 31, no. 1, pp. 13–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Baker, L. Chang, K. A. Elsegood et al., “Activated T cell subsets in human type 1 diabetes: evidence for expansion of the DR+ CD30(+) subpopulation in new-onset disease,” Clinical and Experimental Immunology, vol. 147, no. 3, pp. 472–482, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Ming, Q. Zhang, X. Qiu, and E. Wang, “Interleukin 7/interleukin 7 receptor induce c-Fos/c-Jun-dependent vascular endothelial growth factor-D up-regulation: a mechanism of lymphangiogenesis in lung cancer,” European Journal of Cancer, vol. 45, no. 5, pp. 866–873, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. A. K. Yadav, A. Lal, and V. Jha, “Association of circulating fractalkine (CX3CL1) and CX3CR1(+)CD4(+) T cells with common carotid artery intima-media thickness in patients with chronic kidney disease,” Journal of Atherosclerosis and Thrombosis, vol. 18, no. 11, pp. 958–965, 2011. View at Google Scholar · View at Scopus