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Journal of Transplantation
Volume 2012 (2012), Article ID 210210, 10 pages
http://dx.doi.org/10.1155/2012/210210
Review Article

Antibody-Mediated Rejection: An Evolving Entity in Heart Transplantation

1Division of Cardiology, University Health Network, Toronto General Hospital, Toronto, ON, Canada M5G 2C4
2Multi-Organ Transplant, University Health Network, Toronto General Hospital, Toronto, ON, Canada M5G 2N2
3Histocompatibility Laboratory, University Health Network, Toronto General Hospital, Toronto, ON, Canada M5G 2M1
4Department of Pathology, University Health Network, Toronto General Hospital, Toronto, ON, Canada M5G 2C4
5Division of Cardiac Surgery, University Health Network, Toronto General Hospital, Toronto, ON, Canada M5G 2C4

Received 15 October 2011; Revised 19 December 2011; Accepted 21 December 2011

Academic Editor: Mark Haas

Copyright © 2012 Sharon Chih 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. P. J. Michaels, M. L. Espejo, J. Kobashigawa et al., “Humoral rejection in cardiac transplantation: risk factors, hemodynamic consequences and relationship to transplant coronary artery disease,” Journal of Heart and Lung Transplantation, vol. 22, no. 1, pp. 58–69, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. G. W. Wu, J. A. Kobashigawa, M. C. Fishbein et al., “Asymptomatic antibody-mediated rejection after heart transplantation predicts poor outcomes,” Journal of Heart and Lung Transplantation, vol. 28, no. 5, pp. 417–422, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Nair, T. Ball, P. A. Uber, and M. R. Mehra, “Current and future challenges in therapy for antibody-mediated rejection,” Journal of Heart and Lung Transplantation, vol. 30, no. 6, pp. 612–617, 2011. View at Publisher · View at Google Scholar
  4. A. Herskowitz, L. M. Soule, K. Ueda, et al., “Arteriolar vasculitis on endomyocardial biopsy: a histologic predictor of poor outcome in cyclosporine-treated heart transplant recipients,” Journal of Heart Transplantation, vol. 6, no. 3, pp. 127–136, 1987. View at Scopus
  5. E. H. Hammond, R. L. Yowell, S. Nunoda et al., “Vascular (humoral) rejection in heart transplantation: pathologic observations and clinical implications,” Journal of Heart Transplantation, vol. 8, no. 6, pp. 430–443, 1989. View at Scopus
  6. S. Stewart, G. L. Winters, M. C. Fishbein et al., “Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection,” Journal of Heart and Lung Transplantation, vol. 24, no. 11, pp. 1710–1720, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Kobashigawa, M. G. Crespo-Leiro, S. M. Ensminger et al., “Report from a consensus conference on antibody-mediated rejection in heart transplantation,” Journal of Heart and Lung Transplantation, vol. 30, no. 3, pp. 252–269, 2011. View at Publisher · View at Google Scholar
  8. G. J. Berry, A. Angelini, M. M. Burke et al., “The ISHLT working formulation for pathologic diagnosis of antibody-mediated rejection in heart transplantation: evolution and current status (2005–2011),” Journal of Heart and Lung Transplantation, vol. 30, no. 6, pp. 601–611, 2011. View at Publisher · View at Google Scholar
  9. K. Murata and W. M. Baldwin III, “Mechanisms of complement activation, C4d deposition, and their contribution to the pathogenesis of antibody-mediated rejection,” Transplantation Reviews, vol. 23, no. 3, pp. 139–150, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. K. S. Kilgore, E. Schmidt, T. P. Shanley et al., “Sublytic concentrations of the membrane attack complex of complement induce endothelial interleukin-8 and monocyte chemoattractant protein-1 through nuclear factor-κB activation,” American Journal of Pathology, vol. 150, no. 6, pp. 2019–2031, 1997. View at Scopus
  11. R. Snyderman, M. C. Pike, D. McCarley, and L. Lang, “Quantification of mouse macrophage chemotoxis in vitro: role of C5 for the production of chemotactic activity,” Infection and Immunity, vol. 11, no. 3, pp. 488–492, 1975. View at Scopus
  12. B. A. Wasowska, “Mechanisms involved in antibody- and complement-mediated allograft rejection,” Immunologic Research, vol. 47, no. 1–3, pp. 25–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. J. D. Smith, C. Lawson, M. H. Yacoub, and M. L. Rose, “Activation of NF-κB in human endothelial cells induced by monoclonal and allospecific HLA antibodies,” International Immunology, vol. 12, no. 4, pp. 563–571, 2000. View at Scopus
  14. P. D. Hughes and S. J. Cohney, “Modifiers of complement activation for prevention of antibody-mediated injury to allografts,” Current Opinion in Organ Transplantation, vol. 16, no. 4, pp. 425–433, 2011. View at Publisher · View at Google Scholar
  15. D. O. Taylor, R. L. Yowell, A. G. Kfoury, E. H. Hammond, and D. G. Renlund, “Allograft coronary artery disease: clinical correlations with circulating anti-HLA antibodies and the immunohistopathologic pattern of vascular rejection,” Journal of Heart and Lung Transplantation, vol. 19, no. 6, pp. 518–521, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Soleimani, R. I. Lechler, P. I. Hornick, and A. J. T. George, “Role of alloantibodies in the pathogenesis of graft arteriosclerosis in cardiac transplantation,” American Journal of Transplantation, vol. 6, no. 8, pp. 1781–1785, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Wehner, C. N. Morrell, T. Reynolds, E. R. Rodriguez, and W. M. Baldwin, “Antibody and complement in transplant vasculopathy,” Circulation Research, vol. 100, no. 2, pp. 191–203, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. D. S. Nath, H. Ilias Basha, V. Tiriveedhi et al., “Characterization of immune responses to cardiac self-antigens myosin and vimentin in human cardiac allograft recipients with antibody-mediated rejection and cardiac allograft vasculopathy,” Journal of Heart and Lung Transplantation, vol. 29, no. 11, pp. 1277–1285, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. S. Nath, V. Tiriveedhi, H. I. Basha et al., “A role for antibodies to human leukocyte antigens, collagen-V, and K-α1-tubulin in antibody-mediated rejection and cardiac allograft vasculopathy,” Transplantation, vol. 91, no. 9, pp. 1036–1043, 2011. View at Publisher · View at Google Scholar
  20. J. D. Smith, V. M. Brunner, S. Jigjidsuren et al., “Lack of effect of MICA antibodies on graft survival following heart transplantation,” American Journal of Transplantation, vol. 9, no. 8, pp. 1912–1919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. G. Kfoury, M. E. H. Hammond, G. L. Snow et al., “Cardiovascular mortality among heart transplant recipients with asymptomatic antibody-mediated or stable mixed cellular and antibody-mediated rejection,” Journal of Heart and Lung Transplantation, vol. 28, no. 8, pp. 781–784, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Tinckam, “Histocompatibility methods,” Transplantation Reviews, vol. 23, no. 2, pp. 80–93, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. A. Koch, Z. I. Khalpey, and J. L. Platt, “Accommodation: preventing injury in transplantation and disease,” Journal of Immunology, vol. 172, no. 9, pp. 5143–5148, 2004. View at Scopus
  24. O. Bocrie, A. A. Hussein Aly, F. Guignier et al., “Distribution of donor-specific antibodies in the cortex and the medulla of renal transplants with chronic allograft nephropathy,” Transplant Immunology, vol. 17, no. 3, pp. 227–229, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. E. H. Hammond, J. Stehlik, G. Snow et al., “Utility of histologic parameters in screening for antibody-mediated rejection of the cardiac allograft: a study of 3,170 biopsies,” Journal of Heart and Lung Transplantation, vol. 24, no. 12, pp. 2015–2021, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Fedrigo, A. Gambino, E. Benazzi et al., “Role of morphologic parameters on endomyocardial biopsy to detect sub-clinical antibody-mediated rejection in heart transplantation,” Journal of Heart and Lung Transplantation, vol. 30, no. 12, pp. 1381–1388, 2011. View at Publisher · View at Google Scholar
  27. S. Gupta, J. D. Mitchell, B. Lavingia et al., “Utility of Routine Immunofluorescence Staining for C4d in Cardiac Transplant Recipients,” Journal of Heart and Lung Transplantation, vol. 28, no. 8, pp. 776–780, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. E. R. Rodriguez, D. V. Skojec, C. D. Tan et al., “Antibody-mediated rejection in human cardiac allografts: evaluation of immunoglobulins and complement activation products C4d and C3d as markers,” American Journal of Transplantation, vol. 5, no. 11, pp. 2778–2785, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. C. D. Tan, G. G. Sokos, D. J. Pidwell et al., “Correlation of donor-specific antibodies, complement and its regulators with graft dysfunction in cardiac antibody-mediated rejection,” American Journal of Transplantation, vol. 9, no. 9, pp. 2075–2084, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Lones, L. S. C. Czer, A. Trento, D. Harasty, J. M. Miller, and M. C. Fishbein, “Clinical-pathologic features of humoral rejection in cardiac allografts: a study in 81 consecutive patients,” Journal of Heart and Lung Transplantation, vol. 14, no. 1, pp. 151–162, 1995. View at Scopus
  31. N. B. Ratliff and J. T. McMahon, “Activation of intravascular macrophages within myocardial small vessels is a feature of acute vascular rejection in human heart transplants,” Journal of Heart and Lung Transplantation, vol. 14, no. 2, pp. 338–345, 1995. View at Scopus
  32. B. Sis and P. F. Halloran, “Endothelial transcripts uncover a previously unknown phenotype: C4d-negative antibody-mediated rejection,” Current Opinion in Organ Transplantation, vol. 15, no. 1, pp. 42–48, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Sis, G. S. Jhangri, S. Bunnag, K. Allanach, B. Kaplan, and P. F. Halloran, “Endothelial gene expression in kidney transplants with alloantibody indicates Antibody-mediated damage despite lack of C4d staining,” American Journal of Transplantation, vol. 9, no. 10, pp. 2312–2323, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. J. D. Smith, N. R. Banner, I. M. Hamour et al., “De novo donor HLA-specific antibodies after heart transplantation are an independent predictor of poor patient survival,” American Journal of Transplantation, vol. 11, no. 2, pp. 312–319, 2011. View at Publisher · View at Google Scholar
  35. M. S. Zand, “B-cell activity of polyclonal antithymocyte globulins,” Transplantation, vol. 82, no. 11, pp. 1387–1395, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. A. C. Allison and E. M. Eugui, “Mechanisms of action of mycophenolate mofetil in preventing acute and chronic allograft rejection,” Transplantation, vol. 80, no. 2, pp. S181–S190, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Heidt, D. L. Roelen, C. Eijsink, C. Van Kooten, F. H. J. Claas, and A. Mulder, “Effects of immunosuppressive drugs on purified human b cells: evidence supporting the use of mmf and rapamycin,” Transplantation, vol. 86, no. 9, pp. 1292–1300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. O. Grauhan, C. Knosalla, R. Ewert et al., “Plasmapheresis and cyclophosphamide in the treatment of humoral rejection after heart transplantation,” Journal of Heart and Lung Transplantation, vol. 20, no. 3, pp. 316–321, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. S. C. Jordan, M. Toyoda, J. Kahwaji, and A. A. Vo, “Clinical aspects of intravenous immunoglobulin use in solid organ transplant recipients,” American Journal of Transplantation, vol. 11, no. 2, pp. 196–202, 2011. View at Publisher · View at Google Scholar
  40. N. Shehata, V. A. Palda, R. M. Meyer et al., “The use of immunoglobulin therapy for patients undergoing solid organ transplantation: an evidence-based practice guideline,” Transfusion Medicine Reviews, vol. 24, no. 1, pp. S7–S27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. R. A. Montgomery, B. E. Lonze, K. E. King et al., “Desensitization in HLA-incompatible kidney recipients and survival,” The New England Journal of Medicine, vol. 365, no. 4, pp. 318–326, 2011. View at Publisher · View at Google Scholar
  42. R. W. Lehrich, P. N. Rocha, N. Reinsmoen et al., “Intravenous immunoglobulin and plasmapheresis in acute humoral rejection: experience in renal allograft transplantation,” Human Immunology, vol. 66, no. 4, pp. 350–358, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. P. N. Rocha, D. W. Butterly, A. Greenberg et al., “Beneficial effect of plasmapheresis and intravenous immunoglobulin on renal allograft survival of patients with acute humoral rejection,” Transplantation, vol. 75, no. 9, pp. 1490–1495, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. R. A. Montgomery, A. A. Zachary, L. C. Racusen et al., “Plasmapheresis and intravenous immune globulin provides effective rescue therapy for refractory humoral rejection and allows kidneys to be successfully transplanted into cross-match-positive recipients,” Transplantation, vol. 70, no. 6, pp. 887–895, 2000. View at Scopus
  45. S. C. Jordan, A. W. Quartel, L. S. C. Czer et al., “Posttransplant therapy using high-dose human immunoglobulin (intravenous gammaglobulin) to control acute humoral reaction in renal and cardiac allograft recipients and potential mechanism of action,” Transplantation, vol. 66, no. 6, pp. 800–808, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Cerny, B. Borisch, M. Introna, P. Johnson, and A. L. Rose, “Mechanism of action of rituximab,” Anti-Cancer Drugs, vol. 13, no. 2, pp. S3–S10, 2002. View at Scopus
  47. I. Kaczmarek, M. A. Deutsch, S. Sadoni et al., “Successful management of antibody-mediated cardiac allograft rejection with combined immunoadsorption and anti-CD20 monoclonal antibody treatment: case report and literature review,” Journal of Heart and Lung Transplantation, vol. 26, no. 5, pp. 511–515, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. G. L. Plosker and D. P. Figgitt, “Rituximab: a review of its use in non-Hodgkin's lymphoma and chronic lymphocytic leukaemia,” Drugs, vol. 63, no. 8, pp. 803–843, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. C. A. Vieira, A. Agarwal, B. K. Book et al., “Rituximab for reduction of anti-HLA antibodies in patients awaiting renal transplantation: 1. Safety, pharmacodynamics, and pharmacokinetics,” Transplantation, vol. 77, no. 4, pp. 542–548, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. W. K. Weng and R. Levy, “Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma,” Journal of Clinical Oncology, vol. 21, no. 21, pp. 3940–3947, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. G. Cartron, L. Dacheux, G. Salles et al., “Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcγrIIIa gene,” Blood, vol. 99, no. 3, pp. 754–758, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Rostaing, C. Guilbeau-Frugier, and N. Kamar, “Rituximab for humoral rejection after kidney transplantation: an update,” Transplantation, vol. 87, no. 8, p. 1261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. J. Everly, R. C. Walsh, R. R. Alloway, and E. S. Woodle, “Proteasome inhibition for antibody-mediated rejection,” Current Opinion in Organ Transplantation, vol. 14, no. 6, pp. 662–666, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Nencioni, F. Grünebach, F. Patrone, A. Ballestrero, and P. Brossart, “Proteasome inhibitors: antitumor effects and beyond,” Leukemia, vol. 21, no. 1, pp. 30–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Everly, J. J. Everly, B. Susskind et al., “Bortezomib provides effective therapy for antibody- and cell-mediated acute rejection,” Transplantation, vol. 86, no. 12, pp. 1754–1761, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. H. L. Trivedi, P. I. Terasaki, A. Feroz et al., “Abrogation of Anti-HLA antibodies via proteasome inhibition,” Transplantation, vol. 87, no. 10, pp. 1555–1561, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. M. J. Everly, J. J. Everly, B. Susskind et al., “Proteasome inhibition reduces donor-specific antibody levels,” Transplantation Proceedings, vol. 41, no. 1, pp. 105–107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. D. K. Perry, J. M. Burns, H. S. Pollinger et al., “Proteasome inhibition causes apoptosis of normal human plasma cells preventing alloantibody production,” American Journal of Transplantation, vol. 9, no. 1, pp. 201–209, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. R. C. Walsh, J. J. Everly, P. Brailey et al., “Proteasome inhibitor-based primary therapy for antibody-mediated renal allograft rejection,” Transplantation, vol. 89, no. 3, pp. 277–284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. E. S. Woodle, J. Light, W. Franklin, et al., “A multicenter prospective, collaborative evaluation of proteosome inhibition for the treatment of antibody mediated rejection in solid organ transplantation,” American Journal of Transplantion, vol. 10, supplement 4, p. 159, 2011.
  61. H. Wang, J. Arp, W. Liu et al., “Inhibition of terminal complement components in presensitized transplant recipients prevents antibody-mediated rejection leading to long-term graft survival and accommodation,” Journal of Immunology, vol. 179, no. 7, pp. 4451–4463, 2007. View at Scopus
  62. M. D. Stegall, T. Diwan, S. Raghavaiah et al., “Terminal complement inhibition decreases antibody-mediated rejection in sensitized renal transplant recipients,” American Journal of Transplantation, vol. 11, no. 11, pp. 2405–2413, 2011. View at Publisher · View at Google Scholar
  63. J. E. Locke, C. M. Magro, A. L. Singer et al., “The use of antibody to complement protein C5 for salvage treatment of severe antibody-mediated rejection,” American Journal of Transplantation, vol. 9, no. 1, pp. 231–235, 2009. View at Publisher · View at Google Scholar · View at Scopus