Graft

 

Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Click here to register today!

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Demetris, A. J.
Right arrow Articles by Delaney, C. P.
Right arrow Search for Related Content
Social Bookmarking
 Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?
Graft, Vol. 6, No. 1, 21-32 (2003)
DOI: 10.1177/1522162802239754
© 2003 SAGE Publications

Overlap between Alloimmunity and Autoimmunity in the Rat and Human: Evidence for Important Contributions for Dendritic and Regulatory Cells

Anthony J. Demetris, MD

Noriko Murase, MD

Pittsburgh Transplantation Institute and the University of Pittsburgh

Conor P. Delaney, MD, PhD

Cleveland Clinic Foundation

Alloimmunity and autoimmunity share a number of important afferent, effector, and regulatory immunological pathways. It is likely that they also share overlapping specificities that at least partially explain the ability of allograft rejection to trigger autoimmune responses, the increased susceptibility of patients with autoimmune diseases to allograft rejection, and a strikingly similar histopathologic appearance of acute and chronic rejection to some organ-specific autoimmune diseases. Clinical and experimental data are presented and reviewed, showing some overlapping specificities of effector and regulatory mechanisms during alloimmunity and autoimmunity. The speculation is made that tissue damage during acute rejection uncovers self-reactive T cell clones via the process of epitope spreading, perhaps mediated by heat-shock-protein-peptide complex-priming of recipient dendritic cells. Conversely, donor dendritic cells are suggested as a candidate for stimulating regulatory T cells that help maintain allograft acceptance in the periphery.

Key Words: autoimmunity • alloimmunity • immune regulation • dendritic cells

References

  • 1. Dubel L, Farges O, Johanet C, Sebagh M, Bismuth H. High incidence of antitissue antibodies in patients experiencing chronic liver allograft rejection . Transplantation 1998;65(8): 1072-5 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 2. Graze PR, Gale RP. Chronic graft versus host disease: a syndrome of disordered immunity . Am J Med 1979;66(4): 611-20 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 3. Harkis GD, Cave P, Brown DL, English TA. Anti-heart antibodies in cardiac allograft recipients . Int Arch Allergy Appl Immunol 1984;73(1): 18-22 .[Medline] [Order article via Infotrieve]OpenURL
  • 4. Quaranta S, Shulman H, Ahmed A, et al. Autoantibodies in human chronic graft-versus-host disease after hematopoietic cell transplantation . Clin Immunol 1999;91(1): 106-16 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 5. Duclos-Vallee JC, Johanet C, Bach JF, et al. Autoantibodies associated with acute rejection after liver transplantation for type-2 autoimmune hepatitis . J Hepatol 2000;33(1): 163-6 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 6. Varani S, Muratori L, De Ruvo N, et al. Autoantibody appearance in cytomegalovirus-infected liver transplant recipients: correlation with antigenemia . J Med Virol 2002;66(1): 56-62 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 7. Lytton SD, Berg U, Nemeth A, et al. Autoantibodies against cytochrome P450s in sera of children treated with immunosuppressive drugs . Clin Exp Immunol 2002;127(2): 293-302 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 8. Fedoseyeva EV, Kishimoto K, Rolls HK, et al. Modulation of tissue-specific immune response to cardiac myosin can prolong survival of allogeneic heart transplants . J Immunol 2002;169(3): 1168-74 .[Abstract/Free Full Text]
  • 9. Duquesnoy RJ, Liu K, Fu XF, et al. Evidence for heat shock protein immunity in a rat cardiac allograft model of chronic rejection . Transplantation 1999;67(1): 156-64 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 10. Fedoseyeva EV, Zhang F, Orr PL, et al. De novo autoimmunity to cardiac myosin after heart transplantation and its contribution to the rejection process . J Immunol 1999;162(11): 6836-42 .[Abstract/Free Full Text]
  • 11. Jaeger C, Brendel MD, Eckhard M, et al. Islet autoantibodies as potential markers for disease recurrence in clinical islet transplantation . Exp Clin Endocrinol Diabetes 2000;108(5): 328-33 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 12. Martin CA, Anthone S, Anthone R, et al. Antibodies to saline extractable tissue antigen in sera of patients with renal diseases . Proc Soc Exp Biol Med 1987;184(2): 211-7 .[Abstract]
  • 13. Jordan SC, Barkley SC, Lemire JM, et al. Spontaneous anti-tubular-basement-membrane antibody production by lymphocytes isolated from a rejected allograft . Transplantation 1986;41(2): 173-6 .[Medline] [Order article via Infotrieve]OpenURL
  • 14. Zelenika D, Adams E, Humm S, et al. The role of CD4+ T-cell subsets in determining transplantation rejection or tolerance . Immunol Rev 2001;182: 164-79 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 15. Delaney CP, Murase N, Chen-Woan M, et al. Allogeneic hematolymphoid microchimerism and prevention of autoimmune disease in the rat. A relationship between allo- and autoimmunity . J Clin Invest 1996;97(1): 217-25 .[Abstract/Free Full Text]
  • 16. Lymberi P, Hirsch F, Kuhn J, et al. Autoimmunity induced by HgCl2 in Brown-Norway rats. II. Monoclonal antibodies sharing specificities and idiotypes with mouse natural monoclonal antibodies . J Immunol 1986;136(9): 3277-81 .[Abstract]
  • 17. Hirsch F, Kuhn J, Ventura M, et al. Autoimmunity induced by HgCl2 in Brown-Norway rats. I. Production of monoclonal antibodies . J Immunol 1986;136(9): 3272-6 .[Abstract]
  • 18. Pelletier L, Pasquier R, Rossert J, et al. Autoreactive T cells in mercury-induced autoimmunity. Ability to induce the autoimmune disease . J Immunol 1988;140(3): 750-4 .[Abstract]
  • 19. Pelletier L, Pasquier R, Guettier C, et al. HgC12 induces T and B cells to proliferate and differentiate in BN rats . Clin Exp Immunol 1988;71(2): 336-42 .[Medline] [Order article via Infotrieve]OpenURL
  • 20. Pusey CD, Bowman C, Morgan A, et al. Kinetics and pathogenicity of autoantibodies induced by mercuric chloride in the brown Norway rat . Clin Exp Immunol 1990;81(1): 76-82 .[Medline] [Order article via Infotrieve]OpenURL
  • 21. Dubey C, Bellon B, Hirsch F, et al. Increased expression of class II major histocompatibility complex molecules on B cells in rats susceptible or resistant to HgCl2-induced autoimmunity . Clin Exp Immunol 1991;86(1): 118-23 .[Medline] [Order article via Infotrieve]OpenURL
  • 22. Mathieson PW, Stapleton KJ, Oliveira DB, et al. Immunoregulation of mercuric chloride-induced autoimmunity in Brown Norway rats: a role for CD8+ T cells revealed by in vivo depletion studies . Eur J Immunol 1991;21(9): 2105-9 .[Medline] [Order article via Infotrieve]OpenURL
  • 23. Pelletier L, Pasquier R, Guettier C, et al. HgCl2 induces T and B cells to proliferate and differentiate in BN rats . Clin Exp Immunol 1988;71: 336-42 .
  • 24. Demetris AJ, Murase N, Ye Q, et al. Analysis of chronic rejection and obliterative arteriopathy. Possible contributions of donor antigen-presenting cells and lymphatic disruption . Am J Pathol 1997;150(2): 563-78 .[Abstract]
  • 25. Demetris AJ, Murase N, Rao AS, et al. The role of passenger leukocytes in rejection and "tolerance" after solid organ transplantation: a potential explanation of a paradox. In: JL Touraine et al., editor. Rejection and tolerance. Dordrect (the Netherlands): Kluwer Academic; 1994. p. 325-92.
  • 26. Gillespie KM, Saoudi A, Kuhn J, et al. Th1/Th2 cytokine gene expression after mercuric chloride in susceptible and resistant rat strains . Eur J Immunol 1996;26(10): 2388-92 .[Medline] [Order article via Infotrieve]OpenURL
  • 27. Bridoux F, Badou A, Saoudi A, et al. Transforming growth factor beta (TGFbeta)-dependent inhibition of T helper cell 2 (Th2)-induced autoimmunity by self-major histocompatibility complex (MHC) class II-specific, regulatory CD4(+) T cell lines . J Exp Med 1997;185(10): 1769-75 .[Abstract/Free Full Text]
  • 28. Mathieson PW, Gillespie KM. Cloning of a partial cDNA for rat interleukin-12 (IL-12) and analysis of IL-12 expression in vivo . Scand J Immunol 1996;44(1): 11-4 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 29. Szeto C, Gillespie KM, Mathieson PW. Low-dose mercuric chloride induces resistance in brown Norway rats to further mercuric chloride by up-regulation of interferon-gamma . Scand J Immunol 1999;50(2): 195-201 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 30. Dubey D, Kuhn J, Vial MC, et al. Anti-interleukin-2 receptor monoclonal antibody therapy supports a role for Th1-like cells in HgCl2-induced autoimmunity in rats . Scand J Immunol 1993;37(4): 406-12 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 31. Matzinger P. The danger model: a renewed sense of self . Science 2002;296(5566): 301-5 .[Abstract/Free Full Text]
  • 32. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity . Nat Rev Immunol 2002;2(3): 185-94 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 33. Neuberger J, Portmann B, Calne R, et al. Recurrence of autoimmune chronic active hepatitis following orthotopic liver grafting . Transplantation 1984;37(4): 363-5 .[Medline] [Order article via Infotrieve]OpenURL
  • 34. Ahmed M, Mutimer D, Hathaway M, et al. Liver transplantation for autoimmune hepatitis: a 12-year experience . Transplant Proc 1997;29(1-2): 496 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 35. Kerkar N, Hadzic N, Davies ET, et al. De-novo autoimmune hepatitis after liver transplantation . Lancet 1998;351(9100): 409-13 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 36. Jaeckel E, Tillmann HL, Manns MP. Liver transplantation and autoimmunity . Acta Gastroenterol Belg 1999;62(3): 323-9 .[Medline] [Order article via Infotrieve]OpenURL
  • 37. Reich DJ, Fiel I, Guarrera JV, et al. Liver transplantation for autoimmune hepatitis . Hepatology 2000;32(4, Pt 1): 693-700 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 38. Salcedo M, Vaquero J, Banares R, et al. Response to steroids in de novo autoimmune hepatitis after liver transplantation . Hepatology 2002;35(2): 349-56 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 39. Neuberger J, Portmann B, Macdougall BR, et al. Recurrence of primary biliary cirrhosis after liver transplantation . N Engl J Med 1982;306(1): 1-4 .[Abstract]
  • 40. Polson RJ, Portmann B, Neuberger J, et al. Evidence for disease recurrence after liver transplantation for primary biliary cirrhosis. Clinical and histologic follow-up studies . Gastroenterology 1989;97(3): 715-25 .[Medline] [Order article via Infotrieve]OpenURL
  • 41. Neuberger J. Recurrent primary biliary cirrhosis . Liver Transpl 2001;7(7): 596-9 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 42. Hashimoto E, Shimada M, Noguchi S, et al. Disease recurrence after living liver transplantation for primary biliary cirrhosis: a clinical and histological follow-up study . Liver Transpl 2001;7(7): 588-95 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 43. Hariharan S, Adams MB, Brennan DC, et al. Recurrent and de novo glomerular disease after renal transplantation: a report from Renal Allograft Disease Registry (RADR) . Transplantation 1999;68(5): 635-41 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 44. Petruzzo P, Andreelli F, McGregor B, et al. Evidence of recurrent type I diabetes following HLA-mismatched pancreas transplantation . Diabetes Metab 2000;26(3): 215-8 .[Medline] [Order article via Infotrieve]OpenURL
  • 45. Okitsu T, Bartlett ST, Hadley GA, et al. Recurrent autoimmunity accelerates destruction of minor and major histoincompatible islet grafts in nonobese diabetic (NOD) mice . Am J Transplant 2001;1(2): 138-45 .[Medline] [Order article via Infotrieve]OpenURL
  • 46. Lohmann T, List C, Lamesch P, et al. Diabetes mellitus and islet cell specific autoimmunity as adverse effects of immunosuppressive therapy by FK506/tacrolimus . Exp Clin Endocrinol Diabetes 2000;108(5): 347-52 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 47. Oberholzer J, Triponez F, Mage R, et al. Human islet transplantation: lessons from 13 autologous and 13 allogeneic transplantations . Transplantation 2000;69(6): 1115-23 .[Medline] [Order article via Infotrieve]OpenURL
  • 48. Roep BO, Stobbe I, Duinkerken G, et al. Auto- and alloimmune reactivity to human islet allografts transplanted into type 1 diabetic patients . Diabetes 1999;48(3): 484-90 .[Abstract]
  • 49. Eisenbarth GS, Stegall M. Islet and pancreatic transplantation—autoimmunity and alloimmunity . N Engl J Med 1996;335(12): 888-90 .[Free Full Text]
  • 50. Braghi S, Bonifacio E, Secchi A, Di Carlo V, Pozza G, Bosi E. Modulation of humoral islet autoimmunity by pancreas allotransplantation influences allograft outcome in patients with type 1 diabetes . Diabetes 2000;49(2): 218-24 .[Abstract]
  • 51. Hernandez HM, Kovarik P, Whitington PF, et al. Autoimmune hepatitis as a late complication of liver transplantation . J Pediatr Gastroenterol Nutr 2001;32(2): 131-6 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 52. Gupta P, Hart J, Millis JM, et al. De novo hepatitis with autoimmune antibodies and atypical histology: a rare cause of late graft dysfunction after pediatric liver transplantation . Transplantation 2001;71(5): 664-8 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 53. Mieli-Vergani G, Vergani D. Immunological liver diseases in children . Semin Liver Dis 1998;18(3): 271-9 .[Medline] [Order article via Infotrieve]OpenURL
  • 54. Guttmann RD. Recurrent and de novo glomerulonephritis postrenal transplantation . Transplant Proc 1996;28(3): 1168-70 .[Medline] [Order article via Infotrieve]OpenURL
  • 55. Ashany D, Hines JJ, Gharavi AE, et al. MRL/lpr?severe combined immunodeficiency mouse allografts produce autoantibodies, acute graft-versushost disease or a wasting syndrome depending on the source of cells . Clin Exp Immunol 1992;90(3): 466-75 .[Medline] [Order article via Infotrieve]OpenURL
  • 56. Klassen J, Milgrom F. Autoimmune concomitants of renal allografts . Transplant Proc 1969;1(1): 605-8 .[Medline] [Order article via Infotrieve]OpenURL
  • 57. Krensky AM. T cells in autoimmunity and allograft rejection . Kidney Int Suppl 1994;44: S50-6 .[Medline] [Order article via Infotrieve]OpenURL
  • 58. McCarty GA, King LB, Sanfilippo F. Autoantibodies to nuclear, cytoplasmic, and cytoskeletal antigens in renal allograft rejection . Transplantation 1984;37(5): 446-51 .[Medline] [Order article via Infotrieve]OpenURL
  • 59. Ciubotariu R, Liu Z, Colovai AI, Ho E, Itescu S, Ravalli S, et al., Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts . J Clin Invest 1998;101(2): 398-405 .[Abstract/Free Full Text]
  • 60. Vanderlugt CL, Miller SD. Epitope spreading in immune-mediated diseases: implications for immunotherapy . Nat Rev Immunol 2002;2(2): 85-95 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 61. Zinkernagel RM, Ehl S, Aichele P, et al. Antigen localisation regulates immune responses in a dose- and time-dependent fashion: a geographical view of immune reactivity . Immunol Rev 1997;156: 199-209 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 62. Demetris AJ, Murase N, Starzl TE, et al. Pathology of chronic rejection: an overview of common findings and observations about pathogenic mechanisms and possible prevention . Graft 1998;1: 52-59 .
  • 63. Tori M, Ito T, Kitagawa-Sakakida S, et al. Importance of donor-derived lymphocytes in the protection of pancreaticoduodenal or islet grafts from recurrent autoimmunity: a role for RT6+NKR-P1+ T cells . Transplantation 2000;70(1): 32-8 .[Medline] [Order article via Infotrieve]OpenURL
  • 64. Bartlett ST, Schweitzer EJ, Kuo PC, et al. Prevention of autoimmune islet allograft destruction by engraftment of donor T cells . Transplantation 1997;63(2): 299-303 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 65. Qian S, Demetris AJ, Murase N, et al. Murine liver allograft transplantation: tolerance and donor cell chimerism . Hepatology 1994;19(4): 916-24 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 66. Starzl TE, Demetris AJ, Trucco M, et al. Cell migration and chimerism after whole-organ transplantation: the basis of graft acceptance . Hepatology 1993;17(6): 1127-52 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 67. Demetris AJ, Murase N, Starzl TE. Donor dendritic cells after liver and heart allotransplantation under short-term immunosuppression . Lancet 1992;339(8809): 1610 .OpenURL
  • 68. VanBuskirk AM, Burlingham WJ, Jankowska-Gan E, et al. Human allograft acceptance is associated with immune regulation . J Clin Invest 2000;106(1): 145-55 .[Abstract/Free Full Text]
  • 69. Carrodeguas L, Orosz CG, Waldman WJ, et al. Trans vivo analysis of human delayed-type hypersensitivity reactivity . Hum Immunol 1999;60(8): 640-51 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 70. Annacker O, Pimenta-Araujo R, Burlen-Defranoux O, et al. On the ontogeny and physiology of regulatory T cells . Immunol Rev 2001;182: 5-17 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 71. Salomon B, Bluestone JA. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation . Annu Rev Immunol 2001;19: 225-52 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 72. Munn DH, Sharma MD, Lee JR, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase . Science 2002;297(5588): 1867-70 .[Abstract/Free Full Text]
  • 73. Chatenoud L, Salomon B, Bluestone JA. Suppressor T cells—they’re back and critical for regulation of autoimmunity! Immunol Rev 2001;182: 149-63 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 74. Tung KS, Agersborg SS, Alard P, et al. Regulatory T-cell, endogenous antigen and neonatal environment in the prevention and induction of autoimmune disease . Immunol Rev 2001;182: 135-48 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 75. Coutinho A, Hori S, Carvalho T, et al. Regulatory T cells: the physiology of autoreactivity in dominant tolerance and "quality control" of immune responses . Immunol Rev 2001;182: 89-98 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 76. Mason D. Some quantitative aspects of T-cell repertoire selection: the requirement for regulatory T cells . Immunol Rev 2001;182: 80-8 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 77. Durkin HG, Waksman BH. Thymus and tolerance. Is regulation the major function of the thymus? Immunol Rev 2001;182: 33-57 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 78. 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 Rev 2001;182: 18-32 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 79. Seddon B, Mason D. Peripheral autoantigen induces regulatory T cells that prevent autoimmunity . J Exp Med 1999;189(5): 877-82 .[Abstract/Free Full Text]
  • 80. Ichikawa N, Demetris AJ, Starzl TE, et al. Donor and recipient leukocytes in organ allografts of recipients with variable donor-specific tolerance: with particular reference to chronic rejection . Liver Transpl 2000;6(6): 686-702 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 81. Okuda T, Ishikawa T, Azhipa O, et al. Early passenger leukocyte migration and acute immune reactions in the rat recipient spleen during liver engraftment: with particular emphasis on donor major histocompatibility complex class II+ cells . Transplantation 2002;74(1): 103-11 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 82. Young RA. Stress proteins and immunology . Ann Rev Immunol 1990;8: 401-20 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 83. Lamb JR, Bal V, Mendez-Samperio P, et al. Stress proteins may provide a link between the immune response to infection and autoimmunity . Intl Immunol 1989;1: 191-6 .[Abstract/Free Full Text]
  • 84. Moliterno R, Woan M, Bentlejewski C, et al. Heat shock protein-induced Tlymphocyte propagation from endomyocardial biopsies in heart transplantation . J Heart Lung Trans 1995;14(2): 329-37 .[Medline] [Order article via Infotrieve]OpenURL
  • 85. Birk OS, Gur SL, Elias D, et al. The 60-kDa heat shock protein modulates allograft rejection . Proc Natl Acad Sci U S A 1999;96(9): 5159-63 .[Abstract/Free Full Text]
  • 86. Manca F, Ferry B, Jaakkola M, et al. Frequency and functional characterization of specific T-helper cells infiltrating rat kidney allografts during acute rejection . Scand J Immunol 1987;25: 255-64 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 87. Medzhitov R, Janeway CA, Jr. Decoding the patterns of self and nonself by the innate immune system . Science 2002;296(5566): 298-300 .[Abstract/Free Full Text]
  • 88. Demetris AJ, Duquesnoy RJ, Fung JJ, et al. Pathophysiology of chronic allograft rejection. In: Medscape Transplantation. Retrieved March 29, 2000, from http://transplantation.medscape.com/Medscape/transplantation/ClinicalMgmt/CM.v02/public/index.CM.v02.html
  • 89. Rush DN, Nickerson P, Jeffery JR, et al. Protocol biopsies in renal transplantation: research tool or clinically useful? Curr Opin Nephrol Hypertens 1998;7(6): 691-4 .[Medline] [Order article via Infotrieve]OpenURL
  • 90. Rush DN, Karpinski ME, Nickerson P, et al. Does subclinical rejection contribute to chronic rejection in renal transplant patients? Clin Transplant 1999;13(6): 441-6 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 91. Li Y, Li XC, Zheng XX, et al. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance . Nat Med 1999;5(11): 1298-302 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL
  • 92. Wells AD, Li XC, Li Y, et al. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance . Nat Med 1999;5(11): 1303-7 .[CrossRef][Medline] [Order article via Infotrieve]OpenURL

Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Demetris, A. J.
Right arrow Articles by Delaney, C. P.
Right arrow Search for Related Content
Social Bookmarking
 Add to CiteULike   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?