Chronic allograft nephropathy: The mechanisms and strategies

Hong Kong Journal of Nephrology

Volumn 9, Issue 2, 2007, Pages 58-69

  Gong, Nianqiao ^a   Chen, Xilin ^a   Ding, Zhao ^a   Ming, Changsheng ^a   Chen, Xiaoping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Banff working classification; Chronic allograft nephropathy; Immunologic; Mechanism; Novel; Strategy

Indexed keywords

15 DEOXYSPERGUALIN; ABATACEPT; ANTISENSE OLIGODEOXYNUCLEOTIDE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCINEURIN INHIBITOR; CALCIUM CHANNEL BLOCKING AGENT; CD40 LIGAND MONOCLONAL ANTIBODY; CHEMOKINE; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CHEMOKINE RECEPTOR CXCR3 ANTAGONIST; CYCLOSPORIN; CYTOKINE; ENDOTHELIN RECEPTOR ANTAGONIST; EVEROLIMUS; GROWTH FACTOR; IMMUNOGLOBULIN; MATRIX METALLOPROTEINASE INHIBITOR; METHYLPREDNISOLONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD28; MONOCLONAL ANTIBODY ICOS; MYCOPHENOLIC ACID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; SCATTER FACTOR; TACROLIMUS; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACUTE GRAFT REJECTION; ANTIBODY DETECTION; ANTIGEN PRESENTATION; ANTISENSE THERAPY; BRAIN DEATH; BRAIN ISCHEMIA; CELL PROLIFERATION; CELLULAR IMMUNITY; CHRONIC ALLOGRAFT NEPHROPATHY; CHRONIC GRAFT REJECTION; COMBINATION CHEMOTHERAPY; DELAYED GRAFT FUNCTION; DRUG MECHANISM; DRUG MEGADOSE; DRUG SUBSTITUTION; DRUG WITHDRAWAL; FIBROGENESIS; GRAFT SURVIVAL; HLA MATCHING; HUMAN; HUMORAL IMMUNITY; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY FAILURE; KIDNEY GRAFT REJECTION; KIDNEY TRANSPLANTATION; MITOSIS INHIBITION; MONOTHERAPY; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PLASMAPHERESIS; PRIORITY JOURNAL; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; SPLENECTOMY; VASCULAR ENDOTHELIUM;

EID: 36648998734     PISSN: 15615413     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1561-5413(08)60002-2     Document Type: Review

References (123)

1. Solez K, Vincenti F, Filo RS. Histopathologic findings from 2-year protocol biopsies from a US multicenter kidney transplant trial comparing tacrolimus versus cyclosporine: a report of the FK506 Kidney Transplant Study Group. Transplantation 1998; 66:1736-40.
2. Kasiske BL, Andany MA, Danielson B. A thirty percent chronic decline in inverse serum creatinine is an excellent predictor of late renal allograft failure. Am J Kidney Dis 2002;39:762-8.
3. Solez K, Axelsen RA, Benediktsson H, Burdick JF, Cohen AH, Colvin RB, et al. International standardization of criteria for the histologic diagnosis of renal allograft rejection: the Banff working classification of kidney transplant pathology. Kidney Int 1993;44:411-22.
4. Racusen LC, Solez K, Colvin RB, Bonsib SM, Castro MC, Cavallo T, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int 1999;55:713-23.
5. Tullius SG, Hancock WW, Heemann U, Azuma H, Tilney NL. Reversibility of chronic renal allograft rejection. Critical effect of time after transplantation suggests both host immune dependent and independent phases of progressive injury. Transplantation 1994;58:93-9.
6. Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Allen RD, Chapman JR. The natural history of chronic allograft nephropathy. N Engl J Med 2003;349:2326-33.
7. Solez K, Colvin RB, Racusen LC, Sis B, Halloran PF, Birk PE, et al. Banff '05 Meeting Report: differential diagnosis of chronic allograft injury and elimination of chronic allograft nephropathy ('CAN'). Am J Transplant 2007;7:518-26.
8. Opelz G. New immunosuppressants and HLA matching. Transplant Proc 2001;33:467-8.
9. Sijpkens YW, Doxiadis II, Mallat MJ, de Fijter JW, Bruijn JA, Claas FH, Paul LC. Early versus late acute rejection episodes in renal transplantation. Transplantation 2003;75:204-8.
10. Sijpkens YW, Doxiadis II, De Fijter JW, Mallat MJ, van Es LA, De Lange P, et al. Sharing cross-reactive groups of MHC class I improves long-term graft survival. Kidney Int 1999;56:1920-7.
11. Hariharan S, Johnson CP, Bresnahan BA, Taranto SE, McIntosh MJ, Stablein D. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med 2000;342: 605-12.
12. Terasaki PI. Humoral theory of transplantation. Am J Transplant 2003;3:665-73.
13. Terasaki PI, Cai J. Humoral theory of transplantation: further evidence. Curr Opin Immunol 2005;17:541-5.
14. Sayegh MH. Why do we reject a graft? Role of indirect allorecognition in graft rejection. Kidney Int 1999;56:1967-79.
15. Womer KL, Stone JR, Murphy B, Chandraker A, Sayegh MH. Indirect allorecognition of donor class I and II major histocompatibility complex peptides promotes the development of transplant vasculopathy. J Am Soc Nephrol 2001;12: 2500-6.
16. 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;10:398-405.
17. Suciu-Foca N, Ciubotariu R, Colovai A, Foca-Rodi A, Ho E, Rose E, Cortesini R. Persistent allopeptide reactivity and epitope spreading in chronic rejection. Transplant Proc 1999;31:100-1.
18. Biedermann BC, Pober JS. Human endothelial cells induce and regulate cytolytic T cell differentiation. J Immunol 1998;161: 4679-87.
19. Biedermann BC, Pober JS. Human vascular endothelial cells favor clonal expansion of unusual alloreactive CTL. J Immunol 1999;162:7022-30.
20. Hasegawa S, Becker G, Nagano H, Libby P, Mitchell RN. Pattern of graft- and host-specific MHC class II expression in long-term murine cardiac allografts: origin of inflammatory and vascular wall cells. Am J Pathol 1998;153:69-79.
21. Gong N, Pleyer U, Yang J, Vogt K, Hill M, Anegon I, et al. Influence of local and systemic CTLA4Ig gene transfer on corneal allograft survival. J Gene Med 2006;8:459-67.
22. Linhart B, Bigenzahn S, Hartl A, Lupinek C, Thalhamer J, Valenta R, Wekerle T. Costimulation blockade inhibits allergic sensitization but does not affect established allergy in a murine model of grass pollen allergy. J Immunol 2007;178:3924-31.
23. Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999;397:263-6.
24. Yamashita K, Masunaga T, Yanagida N, Takehara M, Hashimoto T, Kobayashi T, et al. Long-term acceptance of rat cardiac allografts on the basis of adenovirus mediated CD40Ig plus CTLA4Ig gene therapies. Transplantation 2003;76:1089-96.
25. Guillonneau C, Aubry V, Renaudin K, Seveno C, Usal C, Tezuka K, Anegon I. Inhibition of chronic rejection and development of tolerogenic T cells after ICOS-ICOSL and CD40-CD40L co-stimulation blockade. Transplantation 2005;80:546-54.
26. Nurieva RI, Mai XM, Forbush K, Bevan MJ, Dong C. B7h is required for T cell activation, differentiation, and effector function. Proc Natl Acad Sci U S A 2003;100:14163-8.
27. Liang L, Sha WC. The right place at the right time: novel B7 family members regulate effector T cell responses. Curr Opin Immunol 2002;14:384-90.
28. Dong C, Nurieva RI. Regulation of immune and autoimmune responses by ICOS. J Autoimmun 2003;21:255-60.
29. Ozkaynak E, Gao W, Shemmeri N, Wang C, Gutierrez-Ramos JC, Amaral J, et al. Importance of ICOS-B7RP-1 costimulation in acute and chronic allograft rejection. Nat Immunol 2001;2: 573-4.
30. Niiro H, Clark EA. Regulation of B-cell fate by antigen-receptor signals. Nat Rev Immunol 2002;2:945-56.
31. Mak TW, Shahinian A, Yoshinaga SK, Wakeham A, Boucher LM, Pintilie M, et al. Costimulation through the inducible costimulator ligand is essential for both T helper and B cell functions in T cell-dependent B cell responses. Nat Immunol 2003;4:765-72.
32. Obata F, Yoshida K, Ohkubo M, Ikeda Y, Taoka Y, Takeuchi Y, et al. Contribution of CD4+ and CD8+ T cells and interferon-gamma to the progress of chronic rejection of kidney allografts: the Th1 response mediates both acute and chronic rejection. Transpl Immunol 2005;14:21-5.
33. Gong N, Du D, Dong C, Chen X, Xiao J, Zhang W, et al. The protective effects on allografts of AdHO-1 gene therapy against chronic rejection injury. Chin J Surg 2007;45:254-7. [In Chinese]
34. Mhoyan A, Wu GD, Kakoulidis TP, Que X, Yolcu ES, Cramer DV, Shirwan H. Predominant expression of the Th2 response in chronic cardiac allograft rejection. Transpl Int 2003;16: 464-73.
35. Koch M, Joosten SA, Mengel M, van Kooten C, Paul LC, Nashan B. Adoptive transfer of primed CD4+ T-lymphocytes induces pattern of chronic allograft nephropathy in a nude rat model. Transplantation 2005;79:753-61.
36. Kuo E, Maruyama T, Fernandez F, Mohanakumar T. Molecular mechanisms of chronic rejection following transplantation. Immunol Res 2005;32:179-85.
37. Libby P. Transplantation-associated arteriosclerosis: potential mechanisms. In: Tilney N, Strom T, Paul L, eds. Transplantation Biology: Cellular and Molecular Aspects. Philadelphia: Lippincott-Raven, 1996:577-86.
38. Mitchell RN. Allograft arteriopathy pathogenesis update. Cardiovasc Pathol 2004;13:33-40.
39. Robertson H, Ali S, McDonnell BJ, Burt AD, Kirby JA. Chronic renal allograft dysfunction: the role of T cell-mediated tubular epithelial to mesenchymal cell transition. J Am Soc Nephrol 2004; 15:390-7.
40. Demir Y, Chen Y, Metz C, Renz H, Heeger PS. Cardiac allograft rejection in the absence of macrophage migration inhibitory factor. Transplantation 2003;76:244-7.
41. Colvin RB. Antibody-mediated renal allograft rejection: diagnosis and pathogenesis. J Am Soc Nephrol 2007;18:1046-56.
42. Gong N, Xiao J, Ye Q. The deposit of C4d in the tissue from chronic allograft nephropathy. Chin J Modern Med 2005;15: 1003-4. [In Chinese]
43. Regele H, Hxner M, Watschinger B. Endothelial C4d deposition is associated with inferior kidney allograft outcome independently of cellular rejection. Nephrol Dial Transplant 2001;16:2058-66.
44. Regele H, Bohmig GA, Habicht A, Gollowitzer D, Schillinger M, Rockenschaub S, et al. Capillary deposition of complement split product C4d in renal allografts is associated with basement membrane injury in peritubular and glomerular capillaries: a contribution of humoral immunity to chronic allograft rejection. J Am Soc Nephrol 2002;13:2371-80.
45. Bohmig GA, Exner M, Habicht A, Schillinger M, Lang U, Kletzmayr J, et al. Capillary C4d deposition in kidney allografts: a specific marker of alloantibody-dependent graft injury. J Am Soc Nephrol 2002;13:1091-9.
46. Piazza A, Poggi E, Borrelli L, Servetti S, Monaco PI, Buonomo O, et al. Impact of donor-specific antibodies on chronic rejection occurrence and graft loss in renal transplantation: posttransplant analysis using flow cytometric techniques. Transplantation 2001; 71:1106-12.
47. Worthington JE, Martin S, Al-Husseini DM, Dyer PA, Johnson RW. Posttransplantation production of donor HLA-specific antibodies as a predictor of renal transplant outcome. Transplantation 2003;75:1034-40.
48. McKenna RM, Takemoto SK, Terasaki PI. Anti-HLA antibodies after solid organ transplantation. Transplantation 2000;69: 319-26.
49. Lee PC, Terasaki PI, Takemoto SK, Lee PH, Hung CJ, Chen YL, et al. All chronic rejection failures of kidney transplants were preceded by the development of HLA antibodies. Transplantation 2002;74:1192-4.
50. Joosten SA, van Kooten C, Paul LC. Pathogenesis of chronic allograft rejection. Transpl Int 2003;16:137-45.
51. Joosten SA, van Ham V, Borrias MC, van Kooten C, Paul LC. Antibodies against mesangial cells in a rat model of chronic renal allograft rejection. Nephrol Dial Transplant 2005;20:692-8.
52. Joosten SA, van Dixhoorn MG, Borrias MC, Benediktsson H, van Veelen PA, van Kooten C, Paul LC. Antibody response against perlecan and collagen types IV and VI in chronic renal allograft rejection in the rat. Am J Pathol 2002;160:1301-10.
53. Joosten SA, van Kooten C. Non-HLA humoral immunity and chronic kidney-graft loss. Lancet 2005;365:1522-3.
54. Le Bas-Bernardet S, Hourmant M, Coupel S, Bignon JD, Soulillou JP, Charreau B. Non-HLA-type endothelial cell reactive alloantibodies in pre-transplant sera of kidney recipients trigger apoptosis. Am J Transplant 2003;3:167-77.
55. Massy ZA, Guijarro C, Wiederkehr MR, Ma JZ, Kasiske BL. Chronic renal allograft rejection: immunologic and nonimmunologic risk factors. Kidney Int 1996;49:518-24.
56. Lindholm A, Ohlman S, Albrechtsen D, Tufveson G, Persson H, Persson NH. The impact of acute rejection episodes on long-term graft function and outcome in 1347 primary renal transplants treated by 3 cyclosporine regimens. Transplantation 1993;56: 307-15.
57. Lattmann T, Hein M, Horber S, Ortmann J, Teixeira MM, Souza DG, et al. Activation of pro-inflammatory and anti-inflammatory cytokines in host organs during chronic allograft rejection: role of endothelin receptor signaling. Am J Transplant 2005;5:1042-9.
58. Hayry P, Mennander A, Tiisala S, Halttunen J, Yilmaz S, Paavonen T. Rat aortic allografts: an experimental model for chronic transplant arteriosclerosis. Transplant Proc 1991;23: 611-2.
59. Hayry P, Yilmaz S. Role of growth factors in graft vessel disease. Transplant Proc 1995;27:2066-7.
60. Li J, Han X, Jiang J, Zhong R, Williams GM, Pickering JG, Chow LH. Vascular smooth muscle cells of recipient origin mediate intimal expansion after aortic allotransplantation in mice. Am J Pathol 2001;158:1943-7.
61. Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation 2002;106:1199-204.
62. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, et al. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation 2002;106:1834-9.
63. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res 2003;93:783-90.
64. Shimizu K, Sugiyama S, Aikawa M, Fukumoto Y, Rabkin E, Libby P, Mitchell RN. Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nat Med 2001;7:738-41.
65. Joosten SA, Sijpkens YW, van Kooten C, Paul LC. Chronic renal allograft rejection: pathophysiologic considerations. Kidney Int 2005;68:1-13.
66. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-84.
67. Gong N, Ming C, Guo H, Chen Z. The clinical pathological characteristics and immunosuppressant conversion treatment of chronic allograft nephropathy. Chin J Organ Transplant 2007; 28:in press. [In Chinese]
68. Slattery C, McMorrow T, Ryan MP. Overexpression of E2A proteins induces epithelial-mesenchymal transition in human renal proximal tubular epithelial cells suggesting a potential role in renal fibrosis. FEBS Lett 2006;580:4021-30.
69. Healy E, Leonard M, Madrigal-Estebas L, O'Farrelly C, Watson AJ, Ryan MP. Factors produced by activated leukocytes alter renal epithelial cell differentiation. Kidney Int 1999;56:1266-9.
70. Lee TK, Man K, Poon RT, Lo CM, Yuen AP, Ng IO, et al. Signal transducers and activators of transcription 5b activation enhances hepatocellular carcinoma aggressiveness through induction of epithelial-mesenchymal transition. Cancer Res 2006;66:9948-56.
71. Wu WS, Tsai RK, Chang CH, Wang S, Wu JR, Chang YX. Reactive oxygen species mediated sustained activation of protein kinase C alpha and extracellular signal-regulated kinase for migration of human hepatoma cell Hepg2. Mol Cancer Res 2006; 4:747-58.
72. Strutz F, Muller GA. Transdifferentiation comes of age. Nephrol Dial Transplant 2000;15:1729-31.
73. Sharma VK, Bologa RM, Xu GP, Li B, Mouradian J, Wang J, et al. Intragraft TGF-beta 1 mRNA: a correlate of interstitial fibrosis and chronic allograft nephropathy. Kidney Int 1996;49:1297-303.
74. Floege J, Hudkins KL, Davis CL, Schwartz SM, Alpers CE. Expression of PDGF alpha-receptor in renal arteriosclerosis and rejecting renal transplants. J Am Soc Nephrol 1998;9:211-23.
75. Gasser M, Waaga AM, Kist-Van Holthe JE, Lenhard SM, Laskowski I, Shaw GD, et al. Normalization of brain death-induced injury to rat renal allografts by recombinant soluble P-selectin glycoprotein ligand. J Am Soc Nephrol 2002;13: 1937-45.
76. Tullius SG, Nieminen-Kelha M, Buelow R, Reutzel-Selke A, Martins PN, Pratschke J, et al. Inhibition of ischemia/reperfusion injury and chronic graft deterioration by a single-donor treatment with cobalt-protoporphyrin for the induction of heme oxygenase-1. Transplantation 2002;74:591-8.
77. Boom H, Mallat MJ, de Fijter JW, Zwinderman AH, Paul LC. Delayed graft function influences renal function, but not survival. Kidney Int 2000;58:859-66.
78. Takemoto SK, Cho YW, Gjertson DW. Transplant risk. In: Terasaki PI, Cecka JM, eds. Clinical Transplants. Los Angeles: Tissue Typing Laboratory, 1999:325.
79. Ferlicot S, Durrbach A, Ba N, Desvaux D, Bedossa P, Paradis V. The role of replicative senescence in chronic allograft nephropathy. Hum Pathol 2003;34:924-8.
80. Chkhotua AB, Gabusi E, Altimari A, D'Errico A, Yakubovich M, Vienken J, et al. Increased expression of p16(INK4a) and p27(Kip1) cyclin-dependent kinase inhibitor genes in aging human kidney and chronic allograft nephropathy. Am J Kidney Dis 2003;41:1303-13.
81. Chkhotua AB, Altimari A, Gabusi E, D'Errico A, Stefoni S, Chieco P, et al. Increased expression of p21(WAF1/CIP1) cyclin-dependent kinase (CDK) inhibitor gene in chronic allograft nephropathy correlates with the number of acute rejection episodes. Transpl Int 2003;16:502-6.
82. Bestard O, Cruzado JM, Grinyo JM. Calcineurin-inhibitor-sparing immunosuppressive protocols. Transplant Proc 2005;37: 3729-32.
83. Stallone G, Infante B, Schena A, Battaglia M, Ditonno P, Loverre A, et al. Rapamycin for treatment of chronic allograft nephropathy in renal transplant patients. J Am Soc Nephrol 2005; 16:3755-62.
84. Gregory CR, Pratt RE, Huie P, Shorthouse R, Dzau VJ, Billingham ME, Morris RE. Effects of treatment with cyclosporine, FK 506, rapamycin, mycophenolic acid, or deoxyspergualin on vascular muscle proliferation in vitro and in vivo. Transplant Proc 1993;25:770-1.
85. Nashan B. Review of the proliferation inhibitor everolimus. Expert Opin Investig Drugs 2002;11:1845-57.
86. Eugui EM, Almquist SJ, Muller CD, Allison AC. Lymphocyte-selective cytostatic and immunosuppressive effects of mycophenolic acid in vitro: role of deoxyguanosine nucleotide depletion. Scand J Immunol 1991;33:161-73.
87. Quemeneur L, Flacher M, Gerland LM, Ffrench M, Revillard JP, Bonnefoy-Berard N. Mycophenolic acid inhibits IL-2-dependent T cell proliferation, but not IL-2-dependent survival and sensitization to apoptosis. J Immunol 2002;169:2747-55.
88. Eugui EM, Mirkovich A, Allison AC. Lymphocyte-selective antiproliferative and immunosuppressive effects of mycophenolic acid in mice. Scand J Immunol 1991;33:175-83.
89. Looney RJ, Anolik J, Sanz I. B cells as therapeutic targets for rheumatic diseases. Curr Opin Rheumatol 2004;16:180-5.
90. Lagaraine C, Hoarau C, Chabot V, Velge-Roussel F, Lebranchu Y. Mycophenolic acid-treated human dendritic cells have a mature migratory phenotype and inhibit allogeneic responses via direct and indirect pathways. Int Immunol 2005;17:351-63.
91. Heemann U, Azuma H, Hamar P, Schmid C, Tilney N, Philipp T. Mycophenolate mofetil inhibits lymphocyte binding and the upregulation of adhesion molecules in acute rejection of rat kidney allografts. Transpl Immunol 1996;4:64-7.
92. Senda M, DeLustro B, Eugui E, Natsumeda Y. Mycophenolic acid, an inhibitor of IMP dehydrogenase that is also an immunosuppressive agent, suppresses the cytokine-induced nitric oxide production in mouse and rat vascular endothelial cells. Transplantation 1995;60:1143-8.
93. Utimura R, Fujihara CK, Mattar AL, Malheiros DM, Noronha IL, Zatz R. Mycophenolate mofetil prevents the development of glomerular injury in experimental diabetes. Kidney Int 2003;63: 209-16.
94. Russell ME. Chronic cardiac rejection in the Lewis to F344 rat model: blockade of CD28-B7 costimulation by CTLA4Ig modulates T cell and macrophage activation and attenuates arteriosclerosis. J Clin Invest 1996;97:833-8.
95. Laskowsk IA, Pratschke J, Wilhelm MJ. Anti-CD28 monoclonal antibody therapy prevents chronic rejection of renal allografts in rats. J Am Soc Nephrol 2002;13:519-27.
96. Shirasugi N, Adams AB, Durham MM, Lukacher AE, Xu H, Rees P, et al. Prevention of chronic rejection in murine cardiac allografts: a comparison of chimerism- and nonchimerism-inducing costimulation blockade-based tolerance induction regimens. J Immunol 2002;169:2677-84.
97. Shimizu K, Schonbeck U, Mach F, Libby P, Mitchell RN. Host CD40 ligand deficiency induces long-term allograft survival and donor-specific tolerance in mouse cardiac transplantation but does not prevent graft arteriosclerosis. J Immunol 2000;165: 3506-18.
98. Guillot C, Guillonneau C, Mathieu P, Gerdes CA, Menoret S, Braudeau C, et al. Prolonged blockade of CD40-CD40 ligand interactions by gene transfer of CD40Ig results in long-term heart allograft survival and donor-specific hyporesponsiveness, but does not prevent chronic rejection. J Immunol 2002;168: 1600-9.
99. Larsen CP, Elwood ET, Alexander DZ, Ritchie SC, Hendrix R, Tucker-Burden C, et al. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996; 381:434-8.
100. Yamada And A, Sayegh MH. The CD154-CD40 costimulatory pathway in transplantation. Transplantation 2002;73(1 Suppl): S36-9.
101. Harada H, Salama AD, Sho M, Izawa A, Sandner SE, Ito T, et al. The role of the ICOS-B7h T cell costimulatory pathway in transplantation immunity. J Clin Invest 2003;112:234-43.
102. Neto JS, Nakao A, Toyokawa H, Nalesnik MA, Romanosky AJ, Kimizuka K, et al. Low-dose carbon monoxide inhalation prevents development of chronic allograft nephropathy. Am J Physiol Renal Physiol 2006; 290:F324-34.
103. Yang J, Reutzel-Selke A, Steier C, Jurisch A, Tullius SG, Sawitzki B, et al. Targeting of macrophage activity by adenovirus-mediated intragraft overexpression of TNFRp55-Ig, IL-12p40, and vIL-10 ameliorates adenovirus-mediated chronic graft injury, whereas stimulation of macrophages by overexpression of IFN-gamma accelerates chronic graft injury in a rat renal allograft model. J Am Soc Nephrol 2003;14:214-25.
104. Keane MP, Gomperts BN, Weigt S, Xue YY, Burdick MD, Nakamura H, et al. IL-13 is pivotal in the fibro-obliterative process of bronchiolitis obliterans syndrome. J Immunol 2007; 178:511-9.
105. Schnickel GT, Hsieh GR, Garcia C, Shefizadeh A, Fishbein MC, Ardehali A. Role of CXCR3 and CCR5 in allograft rejection. Transplant Proc 2006;38:3221-4.
106. Daniel S, Patel VI, Shrikhande GV, Scali ST, Ramsey HE, Csizmadia E, et al. The universal NF-kappaB inhibitor a20 protects from transplant vasculopathy by differentially affecting apoptosis in endothelial and smooth muscle cells. Transplant Proc 2006;38:3225-7.
107. Nykanen AI, Krebs R, Tikkanen JM, Raisky O, Sihvola R, Wood J, et al. Combined vascular endothelial growth factor and platelet-derived growth factor inhibition in rat cardiac allografts: beneficial effects on inflammation and smooth muscle cell proliferation. Transplantation 2005;79:182-9.
108. Herrero-Fresneda I, Torras J, Franquesa M, Vidal A, Cruzado JM, Lloberas N, et al. HGF gene therapy attenuates renal allograft scarring by preventing the profibrotic inflammatory-induced mechanisms. Kidney Int 2006;70:265-74.
109. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY. Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 2004;164: 1389-97.
110. Dong C, Gong N, Chen Z, Chen X, Xu Q, Guo H, et al. Antisense ERK1/2 oligodeoxynucleotide gene therapy attenuates graft arteriosclerosis of aortic transplant in a rat model. Transplant Proc 2006;38:3304-6.
111. Gong N, Dong C, Chen Z, Chen X, Guo H, Zeng Z, et al. Adenovirus-mediated antisense-ERK2 gene therapy attenuates chronic allograft nephropathy. Transplant Proc 2006;38: 3228-30.
112. Djamali A, Reese S, Yracheta J, Oberley T, Hullett D, Becker B. Epithelial-to-mesenchymal transition and oxidative stress in chronic allograft nephropathy. Am J Transplant 2005;5:500-9.
113. Djamali A, Sadowski EA, Muehrer RJ, Reese S, Smavatkul C, Vidyasagar A, et al. BOLD-MRI assessment of intrarenal oxygenation and oxidative stress in patients with chronic kidney allograft dysfunction. Am J Physiol Renal Physiol 2007;292: F513-22.
114. Inkinen KA, Soots AP, Krogerus LA, Lautenschlager IT, Ahonen JP. Fibrosis and matrix metalloproteinases in rat renal allografts. Transpl Int 2005;18:506-12.
115. Chang HR, Yang SF, Li ML, Lin CC, Hsieh YS, Lian JD. Relationships between circulating matrix metalloproteinase-2 and -9 and renal function in patients with chronic kidney disease. Clin Chim Acta 2006;366:243-8.
116. Blindt R, Vogt F, Lamby D, Zeiffer U, Krott N, Hilger-Eversheim K, et al. Characterization of differential gene expression in quiescent and invasive human arterial smooth muscle cells. J Vasc Res 2002;39:340-52.
117. Taki M, Verschueren K, Yokoyama K, Nagayama M, Kamata N. Involvement of Ets-1 transcription factor in inducing matrix metalloproteinase-2 expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Int J Oncol 2006; 28:487-96.
118. Tan XY, Zheng FL, Zhou QG, Duan L, Li Y. Effect of bone morphogenetic protein-7 on monocyte chemoattractant protein-1 induced epithelial-myofibroblast transition and TGF-beta1-Smad 3 signaling pathway of HKC cells. Zhonghua Yi Xue Za Zhi 2005; 85:2607-12. [In Chinese]
119. Segerer S, Bohmig GA, Exner M, Colin Y, Cartron JP, Kerjaschki D, et al. When renal allografts turn DARC. Transplantation 2003; 75:1030-4.
120. Salama AD, Delikouras A, Pusey CD, Cook HT, Bhangal G, Lechler RI, Dorling A. Transplant accommodation in highly sensitized patients: a potential role for Bcl-xL and alloantibody. Am J Transplant 2001;1:260-9.
121. Cornell L, Della Pelle P, Brousaides N. Endothelial response to rejection: enhanced expression of complement regulatory proteins decay accelerating factor (DAF, CD55) and protectin (CD59) in human renal allografts. Mod Pathol 2004;17: 285A.
122. Semiletova NV, Shen XD, Baibakov B, Feldman DM, Mukherjee K, Frank JM, et al. Inhibition of chronic rejection by antibody induced vascular accommodation in fully allogeneic heart allografts. Transplantation 2005;80:1535-40.
123. Artz MA, Hilbrands LB, Borm G, Assmann KJ, Wetzels JF. Blockade of the renin-angiotensin system increases graft survival in patients with chronic allograft nephropathy. Nephrol Dial Transplant 2004;19:2852-7.