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Journal of Transplantation
Volume 2013, Article ID 841430, 8 pages
http://dx.doi.org/10.1155/2013/841430
Clinical Study

Circulating CD4+CD28null T Cells May Increase the Risk of an Atherosclerotic Vascular Event Shortly after Kidney Transplantation

Erasmus Medical Center, Department of Internal Medicine, Division of Nephrology & Transplantation, D414, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands

Received 26 June 2013; Accepted 29 August 2013

Academic Editor: Parmjeet Randhawa

Copyright © 2013 Michiel G. H. Betjes 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. G. Shlipak, L. F. Fried, M. Cushman et al., “Cardiovascular mortality risk in chronic kidney disease: comparison of traditional and novel risk factors,” Journal of the American Medical Association, vol. 293, no. 14, pp. 1737–1745, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Aull-Watschinger, H. Konstantin, D. Demetriou et al., “Pre-transplant predictors of cerebrovascular events after kidney transplantation,” Nephrology Dialysis Transplantation, vol. 23, no. 4, pp. 1429–1435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Muntner, J. He, B. C. Astor, A. R. Folsom, and J. Coresh, “Traditional and nontraditional risk factors predict coronary heart disease in chronic kidney disease: results from the atherosclerosis risk in communities study,” Journal of the American Society of Nephrology, vol. 16, no. 2, pp. 529–538, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. de Mattos, J. Prather, A. J. Olyaei et al., “Cardiovascular events following renal transplantation: role of traditional and transplant-specific risk factors,” Kidney International, vol. 70, no. 4, pp. 757–764, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. B. C. Fellstrom, A. G. Jardine, R. E. Schmieder, H. Holdaas, K. Bannister, J. Beutler et al., “Rosuvastatin and cardiovascular events in patients undergoing hemodialysis,” The New England Journal of Medicine, vol. 360, no. 14, pp. 1395–1407, 2009. View at Google Scholar
  6. S. D. Navaneethan, S. U. Nigwekar, V. Perkovic, D. W. Johnson, J. C. Craig, and G. F. Strippoli, “HMG CoA reductase inhibitors (statins) for dialysis patients,” Cochrane Database of Systematic Reviews, no. 3, Article ID CD004289, 2009. View at Google Scholar · View at Scopus
  7. C. Wanner, V. Krane, W. März et al., “Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis,” The New England Journal of Medicine, vol. 353, no. 3, pp. 238–248, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Holdaas, B. Fellström, A. G. Jardine et al., “Effect of fluvastatin on cardiac outcomes in renal transplant recipients: a multicentre, randomised, placebo-controlled trial,” The Lancet, vol. 361, no. 9374, pp. 2024–2031, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. M. G. Betjes, R. W. Meijers, L. E. de Wit, and N. H. Litjens, “A killer on the road: circulating CD4(+)CD28null T cells as cardiovascular risk factor in ESRD patients,” Journal of Nephrology, vol. 25, no. 2, pp. 183–191, 2012. View at Google Scholar
  10. M. G. H. Betjes, M. Huisman, W. Weimar, and N. H. R. Litjens, “Expansion of cytolytic CD4+CD28- T cells in end-stage renal disease,” Kidney International, vol. 74, no. 6, pp. 760–767, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. Z. G. Nadareishvili, H. Li, V. Wright et al., “Elevated pro-inflammatory CD4+CD28- lymphocytes and stroke recurrence and death,” Neurology, vol. 63, no. 8, pp. 1446–1451, 2004. View at Google Scholar · View at Scopus
  12. M. Nowik, P. Nowacki, J. Grabarek et al., “Can we talk about CD4+CD28- lymphocytes as a risk factor for ischemic stroke?” European Neurology, vol. 58, no. 1, pp. 26–33, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Zal, J. C. Kaski, G. Arno et al., “Heat-shock protein 60-reactive CD4+CD28null T cells in patients with acute coronary syndromes,” Circulation, vol. 109, no. 10, pp. 1230–1235, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Liuzzo, L. M. Biasucci, G. Trotta et al., “Unusual CD4+CD28null T lymphocytes and recurrence of acute coronary events,” Journal of the American College of Cardiology, vol. 50, no. 15, pp. 1450–1458, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Liuzzo, J. J. Goronzy, H. Yang et al., “Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes,” Circulation, vol. 101, no. 25, pp. 2883–2888, 2000. View at Google Scholar · View at Scopus
  16. K. Sato, A. Niessner, S. L. Kopecky, R. L. Frye, J. J. Goronzy, and C. M. Weyand, “TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque,” Journal of Experimental Medicine, vol. 203, no. 1, pp. 239–250, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. M. G. H. Betjes, E. E. A. de Wit, W. Weimar, and N. H. R. Litjens, “Circulating pro-inflammatory CD4posCD28null T cells are independently associated with cardiovascular disease in ESRD patients,” Nephrology, Dialysis, Transplantation, vol. 25, no. 11, pp. 3640–3646, 2010. View at Google Scholar · View at Scopus
  18. N. H. R. Litjens, M. Huisman, D. Hijdra, B. M. N. Lambrecht, K. J. Stittelaar, and M. G. H. Betjes, “IL-2 producing memory CD4+ T lymphocytes are closely associated with the generation of IgG-secreting plasma cells,” Journal of Immunology, vol. 181, no. 5, pp. 3665–3673, 2008. View at Google Scholar · View at Scopus
  19. N. H. R. Litjens, M. Huisman, M. van den Dorpel, and M. G. H. Betjes, “Impaired immune responses and antigen-specific memory CD4+ T cells in hemodialysis patients,” Journal of the American Society of Nephrology, vol. 19, no. 8, pp. 1483–1490, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. G. H. Betjes, W. Weimar, and N. H. R. Litjens, “CMV seropositivity determines epoetin dose and hemoglobin levels in patients with CKD,” Journal of the American Society of Nephrology, vol. 20, no. 12, pp. 2661–2666, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Aalten, E. K. Hoogeveen, J. I. Roodnat et al., “Associations between pre-kidney-transplant risk factors and post-transplant cardiovascular events and death,” Transplant International, vol. 21, no. 10, pp. 985–991, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Boschiero, F. Fior, and F. Nacchia, “Bimodal distribution of major cardiovascular events in kidney allograft recipients,” Transplantation Proceedings, vol. 41, no. 4, pp. 1183–1186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. G. Betjes, “Immune cell dysfunction and inflammation in end-stage renal disease,” Nature Reviews Nephrology, vol. 9, no. 5, pp. 255–265, 2013. View at Google Scholar
  24. E. Pingiotti, P. Cipriani, A. Marrelli et al., “Surface expression of fractalkine receptor (CX3CR1) on CD4+/CD28- T cells in RA patients and correlation with atherosclerotic damage,” Annals of the New York Academy of Sciences, vol. 1107, pp. 32–41, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Kobayashi, S. Okamoto, Y. Iwakami et al., “Exclusive increase of CX3CR1+CD28-CD4+ T cells in inflammatory bowel disease and their recruitment as intraepithelial lymphocytes,” Inflammatory Bowel Diseases, vol. 13, no. 7, pp. 837–846, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. P. B. Martens, J. J. Goronzy, D. Schaid, and C. M. Weyand, “Expansion of unusual CD4+ T cells in severe rheumatoid arthritis,” Arthritis and Rheumatism, vol. 40, no. 6, pp. 1106–1114, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. A. E. R. Fasth, M. Dastmalchi, A. Rahbar et al., “T cell infiltrates in the muscles of patients with dermatomyositis and polymyositis are dominated by CD28null T cells,” Journal of Immunology, vol. 183, no. 7, pp. 4792–4799, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. L. E. Gamadia, E. B. M. Remmerswaal, J. F. Weel, F. Bemelman, R. A. W. van Lier, and I. J. M. Ten Berge, “Primary immune responses to human CMV: a critical role for IFN-γ-producing CD4+ T cells in protection against CMV disease,” Blood, vol. 101, no. 7, pp. 2686–2692, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. Q. Xu, R. Kleindienst, W. Waitz, H. Dietrich, and G. Wick, “Increased expression of heat shock protein 65 coincides with a population of infiltrating T lymphocytes in atherosclerotic lesions of rabbits specifically responding to heat shock protein 65,” Journal of Clinical Investigation, vol. 91, no. 6, pp. 2693–2702, 1993. View at Google Scholar · View at Scopus
  30. I. Avalos, Y. H. Rho, C. P. Chung, and C. M. Stein, “Atherosclerosis in rheumatoid arthritis and systemic lupus erythematosus,” Clinical and Experimental Rheumatology, vol. 26, supplement 51, no. 5, pp. S5–S13, 2008. View at Google Scholar · View at Scopus
  31. L. E. Full, C. Ruisanchez, and C. Monaco, “The inextricable link between atherosclerosis and prototypical inflammatory diseases rheumatoid arthritis and systemic lupus erythematosus,” Arthritis Research & Therapy, vol. 11, no. 2, article 217, 2009. View at Google Scholar · View at Scopus
  32. K. J. Warrington, P. D. Kent, R. L. Frye et al., “Rheumatoid arthritis is an independent risk factor for multi-vessel coronary artery disease: a case control study,” Arthritis Research & Therapy, vol. 7, no. 5, pp. R984–R991, 2005. View at Google Scholar · View at Scopus
  33. L. Calza, R. Manfredi, D. Pocaterra, and F. Chiodo, “Risk of premature atherosclerosis and ischemic heart disease associated with HIV infection and antiretroviral therapy,” Journal of Infection, vol. 57, no. 1, pp. 16–32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Gerli, G. Schillaci, A. Giordano et al., “CD4+CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients,” Circulation, vol. 109, no. 22, pp. 2744–2748, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. A. Ambrose, M. A. Tannenbaum, D. Alexopoulos et al., “Angiographic progression of coronary artery disease and the development of myocardial infarction,” Journal of the American College of Cardiology, vol. 12, no. 1, pp. 56–62, 1988. View at Google Scholar · View at Scopus
  36. M. M. Dawood, D. K. Gutpa, J. Southern, A. Walia, J. B. Atkinson, and K. A. Eagle, “Pathology of fatal perioperative myocardial infarction: implications regarding pathophysiology and prevention,” International Journal of Cardiology, vol. 57, no. 1, pp. 37–44, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. O. Schouten, E. Boersma, S. E. Hoeks et al., “Fluvastatin and perioperative events in patients undergoing vascular surgery,” The New England Journal of Medicine, vol. 361, no. 10, pp. 980–989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Distelmaier, C. Adlbrecht, J. Jakowitsch et al., “Local complement activation triggers neutrophil recruitment to the site of thrombus formation in acute myocardial infarction,” Thrombosis and Haemostasis, vol. 102, no. 3, pp. 564–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. S. I. van Leuven, D. F. van Wijk, O. L. Volger et al., “Mycophenolate mofetil attenuates plaque inflammation in patients with symptomatic carotid artery stenosis,” Atherosclerosis, vol. 211, no. 1, pp. 231–236, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. V. Rizzello, G. Liuzzo, S. Brugaletta, A. Rebuzzi, L. M. Biasucci, and F. Crea, “Modulation of CD4+CD28null T lymphocytes by tumor necrosis factor-α blockade in patients with unstable angina,” Circulation, vol. 113, no. 19, pp. 2272–2277, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Brugaletta, L. M. Biasucci, M. Pinnelli et al., “Novel anti-inflammatory effect of statins: reduction of CD4 +CD28null T lymphocyte frequency in patients with unstable angina,” Heart, vol. 92, no. 2, pp. 249–250, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Thewissen, V. Somers, N. Hellings, J. Fraussen, J. Damoiseaux, and P. Stinissen, “CD4+CD28null T cells in autoimmune disease: pathogenic features and decreased susceptibility to immunoregulation,” Journal of Immunology, vol. 179, no. 10, pp. 6514–6523, 2007. View at Google Scholar · View at Scopus
  43. S. N. Nadig, J. Wickiewicz, D. C. Wu et al., “In vivo prevention of transplant arteriosclerosis by ex vivo-expanded human regulatory T cells,” Nature Medicine, vol. 16, no. 7, pp. 809–813, 2010. View at Publisher · View at Google Scholar · View at Scopus