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Ann Thorac Surg 2004;77:2247-2249
© 2004 The Society of Thoracic Surgeons
Division of Cardiac Surgery, Transplantation Biology Research Center, and Division of Thoracic Surgery, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
* Address reprint requests to Dr Madsen, EDR 105, Department of Surgery, Massachusetts General Hospital, Boston, MA 02114, USA
e-mail: madsen{at}helix.mgh.harvard.edu
Clinical immunosuppression in thoracic organ transplantation
21st century immunosuppressive agents—heart
1. Baran DA, Segura L, Kushwaha S, et al. Tacrolimus monotherapy in adult cardiac transplant recipients: intermediate-term results. J Heart Lung Transplant 2001;20:59–70.
2. Reichart B, Meiser B, Vigano M, et al. European multicenter tacrolimus heart pilot study: three year follow-up. J Heart Lung Transplant 2001;20:249–50.
3. Kobashigawa J, Miller L, Renlund D, et al. A randomized active-controlled trial of mycophenolate mofetil in heart transplant recipients. Mycophenolate Mofetil Investigators. Transplantation 1998;66:507–15.
4. Meiser BM, Pfeiffer M, Schmidt D, et al. Combination therapy with tacrolimus and mycophenolate mofetil following cardiac transplantation: importance of mycophenolic acid therapeutic drug monitoring. J Heart Lung Transplant 1999;18:143–9.
5. Keogh AM, (The Sirolimus Cardiac Trial Group). Progression of graft vessel disease in cardiac allograft recipients is significantly reduced by sirolimus immunotherapy: 6 month results from a phase 2, open-label study. Am J Transplant 2002:2(suppl 3):246 [Abstract].
6. Mancini D, Vigano M, Pulpon LA, et al. 24-month results of a multicenter study of everolimus for the prevention of allograft rejection and vasculopathy in de novo cardiac transplant recipients. Am J Transplant 2003:S5;550 [Abstract].
7. Kobashigawa JA, Katznelson S, Laks H, et al. Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med 1995;333:621–27.
8. Koshiba T, Van Damme B, Rutgeerts O, et al. FTY720, an immunosuppressant that alters lymphocyte trafficking, abrogates chronic rejection in combination with cyclosporine A. Transplantation. 2003;75:945–52.
21st century immunosuppressive agents—lung
1. Palmer SM, Baz MA, Sanders L, et al. Results of a randomized, prospective, multicenter trial of mycophenolate mofetil versus azathioprine in the prevention of acute lung allograft rejection. Transplantation 2001;71:1772–6.
2. Zuckermann A, Reichenspurner H, Birsan T, et al. Cyclosporine A versus tacrolimus in combination with mycophenolate mofetil and steroids as primary immunosuppression after lung transplantation: one-year results of a 2-center prospective randomized trial. J Thorac Cardiovasc Surg 2003;125:891–900.
3. Zuckerman A, Reichenspurner H, Jaksch P, et al. Long term follow-up of a prospective randomized trial comparing tacrolimus versus cyclosporine in combination with MMF after lung transplantation. J Heart Lung Transplant 2003;22:s26 [Abstract].
Induction therapy
1. Beniaminovitz A, Itescu S, Lietz K, et al. Prevention of rejection in cardiac transplantation by blockade of the interleukin-2 receptor with a monoclonal antibody. N Engl J Med 2000;342:613–19.
2. Lietz K, John R, Beniaminovitz A, et al. Interleukin-2 receptor blockade in cardiac transplantation: influence of HLA-DR locus incompatibility on treatment efficacy. Transplantation 2003;75:781–7.
3. Krasinskas AM, Acker MA, Bavaria JE, et al. CD3 monitoring of antithymocyte globulin therapy in thoracic organ transplantation. Transplantation 2002;73:1339–41.
Alternative immunosuppressive strategies
1. Barr ML, Meiser BM, Eisen HJ, et al. Photopheresis for the prevention of rejection in cardiac transplantation. Photopheresis Transplantation Study Group. N Engl J Med 1998;339:1744–51.
2. Trachiotis GD, Johnston TS, Vega JD, et al. Single-field total lymphoid irradiation in the treatment of refractory rejection after heart transplantation. J Heart Lung Transplant 1998;17:1045–8.
Sensitized recipients
1. Pisani BA, Mullen GM, Malinowska K, et al. Plasmapheresis with intravenous immunoglobulin G is effective in patients with elevated panel reactive antibody prior to cardiac transplantation. J Heart Lung Transplant 1999;18:701–6.
2. Itescu S, Burke E, Lietz K, et al. Intravenous pulse administration of cyclophosphamide is an effective and safe treatment for sensitized cardiac allograft recipients. Circulation 2002;105(10):214–9.
3. John R, Lietz K, Burke E, et al. Intravenous immunoglobulin reduces anti-HLA alloreactivity and shortens waiting time to cardiac transplantation in highly sensitized left ventricular assist device recipients. Circulation 1999;100(19 Suppl):II229–35.
Steroid withdrawal
1. Taylor DO, Bristow MR, O'Connell JB, et al. Improved long-term survival after heart transplantation predicted by successful early withdrawal from maintenance corticosteroid therapy. J Heart Lung Transplant 1996;15:1039–46.
2. Kobashigawa JA, Stevenson LW, Brownfield ED, et al. Corticosteroid weaning late after heart transplantation: relation to HLA-DR mismatching and long-term metabolic benefits. J Heart Lung Transplant 1995;14:963–7.
3. Felkel TO, Smith AL, Reichenspurner HC, et al. Survival and incidence of acute rejection in heart transplant recipients undergoing successful withdrawal from steroid therapy. J Heart Lung Transplant 2002;21:530–39.
Transplantation immunology
Experimental studies in humans
1. Spitzer TR, Delmonico F, Tolkoff-Rubin N, et al. Combined histocompatibility leukocyte antigen-matched donor bone marrow and renal transplantation for multiple myeloma with end stage renal disease: the induction of allograft tolerance through mixed lymphohematopoietic chimerism. Transplantation 1999;68:480–4.
2. West LJ, Pollock-Barziv SM, Dipchand AI, et al. ABO-incompatible heart transplantation in infants. N Engl J Med 2001;344:793–800.
3. Pham SM, Rao AS, Zeevi A, et al. A clinical trial combining donor bone marrow infusion and heart transplantation: intermediate-term results. J Thorac Cardiovasc Surg 2000;119:673–81.
4. Jaramillo A, Smith CR, Maruyama T, et al. Anti-HLA class I antibody binding to airway epithelial cells induces production of fibrogenic growth factors and apoptotic cell death: a possible mechanism for bronchiolitis obliterans syndrome. Hum Immunol 2003;64:521–29.
5. SivaSai KS, Smith MA, Poindexter NJ, et al. Indirect recognition of donor HLA class I peptides in lung transplant recipients with bronchiolitis obliterans syndrome. Transplantation 1999;67:1094–8.
6. Ciubotariu R, Liu Z, Colovai AI, et al. Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts. J Clin Invest 1998:101:398–405.
7. Mancini D, Pinney S, Burkhoff D, et al. Use of rapamycin slows progression of cardiac transplantation vasculopathy. Circulation 2003;108:48–53.
8. Quaini F, Urbanek K, Beltrami AP, et al. Chimerism of the transplanted heart. N Engl J Med 2002;346:5–15.
9. Dhodapkar MV, Steinman RM, Krasovsky J, et al. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 2001;193:233–8.
10. Jonuleit H, Schmitt E, Kakirman H, et al. Infectious tolerance: human CD25(+) regulatory T cells convey suppressor activity to conventional CD4(+) T helper cells. J Exp Med 2002;196:255–60.
Regulatory cells
1. Sakaguchi S, Sakaguchi N, Shimizu J, et al. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol 2001;182:18–32.
2. Shevach EM. Certified professionals: CD4(+)CD25(+) suppressor T cells. J Exp Med 2001;193:F41–6.
3. Van Maurik A, Herber M, Wood KJ, et al. Cutting edge: CD4+CD25+ alloantigen-specific immunoregulatory cells that can prevent CD8+ T cell-mediated graft rejection: implications for anti-CD154 immunotherapy. J Immunol 2002;169:5401–4.
4. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of the CD4+CD25+ regulatory T cells. Nat Immunol 2003;4:330–6.
5. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by transcription factor Foxp3. Science 2003;299:1507–61.
6. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Immunol Rev 2003;3:199–210.
Tolerance
1. Ildstad ST, Sachs DH. Reconstitution with syngeneic plus allogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature 984;307(5947):168–70.
2. Kawai T, Poncelet A, Sachs DH, et al. Long-term outcome and alloantibody production in a non-myeloablative regimen for induction of renal allograft tolerance. Transplantation 1999:68:1767–75.
3. Qin S, Cobbold SP, Pope H, et al. "Infectious" transplantation tolerance. Science 1993;259:974–7.
4. Rosengard BR, Ojikutu CA, Guzzetta PC, et al. Induction of specific tolerance to class I disparate renal allografts in miniature swine with cyclosporine. Transplantation 1992;54: 490–7.
5. Zheng XX, Sanchez-Fueyo A, Sho M, Domenig C, Sayegh MH, Strom TB. Favorably tipping the balance between cytopathic and regulatory T cells to create transplantation tolerance. Immunity 2003;19:503–14
6. Massicot-Fisher J, Noel P, Madsen JC. Recommendations of the national heart, lung and blood institute heart and lung tolerance working group. Transplantation 2001:72:1467–70.
T cells and acute rejection
1. Madsen JC, Superina RA, Wood KJ, et al. Immunological unresponsiveness induced by recipient cells transfected with donor MHC genes. Nature 1988;332:161–64.
2. Kreisel D, Krupnick AS, Gelman AE, et al. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an alternative mechanism of allorecognition. Nat Med 2002;8:233–39.
3. Lakkis FG, Arakelov A, Konieczny BT, et al. Immunologic ‘ignorance’ of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat Med 2000;6:686–88.
4. Li XC, Demirci G, Ferrari-Lacraz S, et al. IL-15 and IL-2: a matter of life and death for T cells in vivo. Nat Med 2001;7:114–18.
5. Auchincloss H, Lee RS, Shea S, et al. The role of "indirect" recognition in initiating rejection of skin grafts from major histocompatibility complex class II-deficient mice. Proc Natl Acad Sci USA 1993;90:3373–77.
Dendritic cells
1. Chang CC, Ciubotariu R, Manavalan JS, et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002;3:237–43.
2. Garrovillo M, Ali A, DePaz HA, et al. Induction of transplant tolerance with immunodominant allopeptide-pulsed host lymphoid and myeloid dendritic cells. Am J Transplant 2001;1:129–37.
Costimulation blockade
1. Larsen CP, Elwood ET, Alexander DZ, et al. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996;381:434–8.
2. Kirk AD, Burkly LC, Batty DS, et al. Treatment with humanized monoclonal antibody against CD154 prevents acute renal allograft rejection in nonhuman primates. Nat Med 1999;5:686–93.
3. Kirk AD, Harlan DM, Armstrong NN, et al. CTLA4-Ig and anti-CD40 ligand prevent renal allograft rejection in primates. Proc Natl Acad Sci 1997;94:8789–94.
4. Pierson RN III, Chang AC, Blum MG, et al. Prolongation of primate cardiac allograft survival by treatment with ANTI-CD40 ligand (CD154) antibody. Transplantation 1999;68:1800–5.
5. Ozkaynak E, Gao W, Shemmeri N, et al. Importance of ICOS-B7RP-1 costimulation in acute and chronic allograft rejection. Nat Immunol 2001;2:591–96.
Chronic rejection
1. Lee RS, Yamada K, Houser SL, et al. Indirect recognition of allopeptides promotes the development of cardiac allograft vasculopathy. Proc Natl Acad Sci USA 2001;98:3276–81.
2. Madsen JC, Yamada K, Allan JS, et al. Transplantation tolerance prevents cardiac allograft vasculopathy in major histocompatibility complex class I-disparate miniature swine. Transplantation 1998;65:304–13.
3. Russell PS, Chase CM, Winn HJ, et al. Coronary atherosclerosis in transplanted mouse hearts. II. Importance of humoral immunity. J Immunol 1994;152:5135–41.
4. Tellides G, Tereb DA, Kirkiles-Smith NC, et al. Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000;403:207–11.
5. Russell PS, Chase CM, Sykes M, et al. Tolerance, mixed chimerism, and chronic transplant arteriopathy. J Immunol 2001;167:5731–40.
Chemokines
1. Gao W, Topham PS, King JA, et al. Targeting of the chemokine receptor CCR1 suppresses development of acute and chronic cardiac allograft rejection. J Clin Invest 2000;105:35–44.
2. Belperio JA, Keane MP, Burdick MD, et al. Critical role for CXCR3 chemokine biology in the pathogenesis of bronchiolitis obliterans syndrome. J Immunol 2002;169:1037–49.
3. Yun JJ, Fischbein MP, Whiting D. The role of MIG/CXCL9 in cardiac allograft vasculopathy. Am J Pathol 2002;161:1307–13.
Xenotransplantation
1. Good AH, Cooper DKC, Malcolm AJ, et al. Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in man. Transplant Proc 1992;24:559–62.
2. Cozzi E, White DJG. The generation of transgenic pigs as potential organ donors for humans. Nat Med 1995;1:964–66.
3. Phelps CJ, Koike C, Vaught TD, et al. Production of 
1,3-galactosyltransferase-deficient pigs. Science 2003;299:411–14.
4. Pierson RN 3rd, Kasper-Konig W, Tew DN, et al. Hyperacute lung rejection in a pig-to-human transplant model: the role of anti-pig antibody and complement. Transplantation 1997;63:594–603.
5. Zhao Y, Swenson K, Sergio JJ, et al. Skin graft tolerance across a discordant xenogeneic barrier. Nat Med 1996;2:1211–6.
6. Cooper DK, Keogh AM, Brink J, et al. Report of the Xenotransplantation Advisory Committee of the International Society for Heart and Lung Transplantation: the present status of xenotransplantation and its potential role in the treatment of end-stage cardiac and pulmonary diseases. J Heart Lung Transplant. 2000;12:1125–65.
Acknowledgments
This work was supported in part by grants from the National Heart, Lung, and Blood Institute (R01 HL67110, R01 HL54211, RO1 HL71932, P01 HL18646), and the National Institute of Allergy and Infectious Disease (P01 AI50157) of the National Institutes of Health.
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