Donor CD4 T cells contribute to cardiac allograft vasculopathy by providing help for autoantibody production

Circulation: Heart Failure

Volumn 2, Issue 4, 2009, Pages 361-369

  Win, Thet Su ^a   Rehakova, Sylvia ^a   Negus, Margaret C ^a   Parsy, Kourosh Saeb ^a   Goddard, Martin ^a   Conlon, Thomas M ^a   Bolton, Eleanor M ^a   Bradley, J Andrew ^a   Pettigrew, Gavin J ^a  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Allograft vasculopathy; Allorecognition; Antibodies; Autoantibody; Graft versus host disease; Rejection; Transplantation

Indexed keywords

ANTINUCLEAR ANTIBODY; AUTOANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BLOOD VESSEL OCCLUSION; CARDIAC ALLOGRAFT VASCULOPATHY; CONTROLLED STUDY; GRAFT RECIPIENT; GRAFT REJECTION; HEART TRANSPLANTATION; HUMORAL IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIBODIES, ANTINUCLEAR; AUTOANTIBODIES; CD4-POSITIVE T-LYMPHOCYTES; GRAFT REJECTION; HEART TRANSPLANTATION; MICE; MICE, INBRED C57BL; TRANSPLANTATION, HOMOLOGOUS;

EID: 77949886463     PISSN: 19413289     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.108.827139     Document Type: Article

References (50)

1. Libby P, Pober JS. Chronic rejection. Immunity. 2001;14:387-397.
2. Salama AD, Womer KL, Sayegh MH. Clinical transplantation tolerance: many rivers to cross. J Immunol. 2007;178:5419-5423.
3. Salomon RN, Hughes CC, Schoen FJ, Payne DD, Pober JS, Libby P. Human coronary transplantation-associated arteriosclerosis. Evidence for a chronic immune reaction to activated graft endothelial cells. Am J Pathol. 1991;138:791-798.
4. Schwarzacher SP, Uren NG, Ward MR, Schwarzkopf A, Giannetti N, Hunt S, Fitzgerald PJ, Oesterle SN, Yeung AC. Determinants of coronary remodeling in transplant coronary disease: a simultaneous intravascular ultrasound and Doppler flow study. Circulation. 2000;101:1384-1389.
5. Koh KP, Wang Y, Yi T, Shiao SL, Lorber MI, Sessa WC, Tellides G, Pober JS. T cell-mediated vascular dysfunction of human allografts results from IFN-gamma dysregulation of NO synthase. J Clin Invest. 2004;114:846-856.
6. Mitchell RN. Allograft arteriopathy: pathogenesis update. Cardiovasc Pathol. 2004;13:33-40.
7. Gould DS, Auchincloss H Jr. Direct and indirect recognition: the role of MHC antigens in graft rejection. Immunol Today. 1999;20:77-82.
8. Burlingham WJ, Jankowska-Gan E. Mouse strain and injection site are crucial for detecting linked suppression in transplant recipients by trans-vivo DTH assay. Am J Transplant. 2007;7:466-470.
9. Haque MA, Mizobuchi T, Yasufuku K, Fujisawa T, Brutkiewicz RR, Zheng Y, Woods K, Smith GN, Cummings OW, Heidler KM, Blum JS, Wilkes DS. Evidence for immune responses to a self-antigen in lung transplantation: role of type V collagen-specific T cells in the patho-genesis of lung allograft rejection. J Immunol. 2002;169:1542-1549.
10. Fedoseyeva EV, Zhang F, Orr PL, Levin D, Buncke HJ, Benichou G. De novo autoimmunity to cardiac myosin after heart transplantation and its contribution to the rejection process. J Immunol. 1999;162:6836-6842.
11. Fedoseyeva EV, Kishimoto K, Rolls HK, Illigens BM, Dong VM, Valu- jskikh A, Heeger PS, Sayegh MH, Benichou G. Modulation of tissue-specific immune response to cardiac myosin can prolong survival of allogeneic heart transplants. J Immunol. 2002;169:1168-1174.
12. Jindra PT, Hsueh A, Hong L, Gjertson D, Shen XD, Gao F, Dang J, Mischel PS, Baldwin WM III, Fishbein MC, Kupiec-Weglinski JW, Reed EF. Anti-MHC class I antibody activation of proliferation and survival signaling in murine cardiac allografts. J Immunol. 2008;180:2214-2224.
13. Goers TA, Ramachandran S, Aloush A, Trulock E, Patterson GA, Mohanakumar T. De novo production of K-alpha1 tubulin-specific anti- bodies: role in chronic lung allograft rejection. J Immunol. 2008;180: 4487-4494.
14. 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;160:1301-1310.
15. Jurcevic S, Ainsworth ME, Pomerance A, Smith JD, Robinson DR, Dunn MJ, Yacoub MH, Rose ML. Antivimentin antibodies are an independent predictor of transplant-associated coronary artery disease after cardiac transplantation. Transplantation. 2001;71:886-892.
16. Morgun A, Shulzhenko N, Unterkircher CS, Diniz RV, Pereira AB, Silva MS, Nishida SK, Almeida DR, Carvalho AC, Franco M, Souza MM, Gerbase-DeLima M. Pre- and post-transplant anti-myosin and anti-heat shock protein antibodies and cardiac transplant outcome. J Heart Lung Transplant. 2004;23:204-209.
17. Valujskikh A, Fedoseyeva E, Benichou G, Heeger PS. Development of autoimmunity after skin graft rejection via an indirect alloresponse. Transplantation. 2002;73:1130-1137.
18. Hirota K, Hashimoto M, Yoshitomi H, Tanaka S, Nomura T, Yamaguchi T, Iwakura Y, Sakaguchi N, Sakaguchi S. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J Exp Med. 2007;204:41-47.
19. Tanaka M, Zwierzchoniewska M, Mokhtari GK, Terry RD, Balsam LB, Robbins RC, Fedoseyeva EV. Progression of alloresponse and tissue-specific immunity during graft coronary artery disease. Am J Transplant. 2005;5:1286-1296. (Pubitemid 40839416)
20. Cosgrove D, Gray D, Dierich A, Kaufman J, Lemeur M, Benoist C, Mathis D. Mice lacking MHC class II molecules. Cell. 1991;66: 1051-1066.
21. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM, et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 1992;68:855-867.
22. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 1991;350:423-426.
23. Takeuchi K, Turley SJ, Tan EM, Pollard KM. Analysis of the autoan-tibody response to fibrillarin in human disease and murine models of autoimmunity. J Immunol. 1995;154:961-971.
24. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176:1693-1702.
25. Gigli I, Sorvillo J, Halbwachs-Mecarelli L. Regulation and deregulation ofthe fluid-phase classical pathway C3 convertase. JImmunol. 1985;135: 440-444.
26. Ardehali A, Fischbein MP, Yun J, Irie Y, Fishbein MC, Laks H. Indirect alloreactivity and chronic rejection. Transplantation. 2002;73: 1805-1807.
27. Nagano H, Mitchell RN, Taylor MK, Hasegawa S, Tilney NL, Libby P. Interferon-gamma deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts. J Clin Invest. 1997; 100:550-557.
28. Sayegh MH, Wu Z, Hancock WW, Langmuir PB, Mata M, Sandner S, Kishimoto K, Sho M, Palmer E, Mitchell RN, Turka LA. Allograft rejection in a new allospecific CD4+ TCR transgenic mouse. Am J Transplant. 2003;3:381-389.
29. Takemoto SK, Zeevi A, Feng S, Colvin RB, Jordan S, Kobashigawa J, Kupiec-Weglinski J, Matas A, Montgomery RA, Nickerson P, Platt JL, Rabb H, Thistlethwaite R, Tyan D, Delmonico FL. National conference to assess antibody-mediated rejection in solid organ transplantation. Am J Transplant. 2004;4:1033-1041.
30. Egner W. The use of laboratory tests in the diagnosis of SLE. J Clin Pathol. 2000;53:424-432.
31. Morris SC, Cheek RL, Cohen PL, Eisenberg RA. Autoantibodies in chronic graft versus host result from cognate T-B interactions. J Exp Med. 1990;171:503-517.
32. Azimzadeh AM, Pfeiffer S, Wu GS, Schroder C, Zhou H, Zorn GL III, Kehry M, Miller GG, Rose ML, Pierson RN III. Humoral immunity to vimentin is associated with cardiac allograft injury in nonhuman primates. Am J Transplant. 2005;5:2349-2359.
33. Kerkar N, Hadzic N, Davies ET, Portmann B, Donaldson PT, Rela M, Heaton ND, Vergani D, Mieli-Vergani G. De-novo autoimmune hepatitis after liver transplantation. Lancet. 1998;351:409-413.
34. Dragun D, Muller DN, Brasen JH, Fritsche L, Nieminen-Kelha M, Dechend R, Kintscher U, Rudolph B, Hoebeke J, Eckert D, Mazak I, Plehm R, Schonemann C, Unger T, Budde K, Neumayer HH, Luft FC, Wallukat G. Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N Engl J Med. 2005;352:558-569.
35. Russell PS, Chase CM, Colvin RB. Alloantibody- and T cell-mediated immunity in the pathogenesis of transplant arteriosclerosis: lack of progression to sclerotic lesions in B cell-deficient mice. Transplantation. 1997;64:1531-1536.
36. Hancock WW, Buelow R, Sayegh MH, Turka LA. Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes. Nat Med. 1998;4:1392-1396.
37. Michaels PJ, Espejo ML, Kobashigawa J, Alejos JC, Burch C, Takemoto S, Reed EF, Fishbein MC. Humoral rejection in cardiac transplantation: risk factors, hemodynamic consequences and relationship to transplant coronary artery disease. J Heart Lung Transplant. 2003;22:58-69.
38. Mahoney JA, Rosen A. Apoptosis and autoimmunity. Curr Opin Immunol. 2005;17:583-588.
39. Casciola-Rosen L, Andrade F, Ulanet D, Wong WB, Rosen A. Cleavage by granzyme B is strongly predictive of autoantigen status: implications for initiation of autoimmunity. J Exp Med. 1999;190:815-826.
40. Mahesh B, Leong HS, McCormack A, Sarathchandra P, Holder A, Rose ML. Autoantibodies to vimentin cause accelerated rejection of cardiac allografts. Am J Pathol. 2007;170:1415-1427.
41. Uehara S, Chase CM, Cornell LD, Madsen JC, Russell PS, Colvin RB. Chronic cardiac transplant arteriopathy in mice: relationship of alloan-tibody, C4d deposition and neointimal fibrosis. Am J Transplant. 2007; 7:57-65.
42. Fischbein MP, Yun J, Laks H, Irie Y, Fishbein MC, Espejo M, Bonavida B, Ardehali A. CD8 + lymphocytes augment chronic rejection in a MHC class II mismatched model. Transplantation. 2001;71:1146-1153.
43. Richards DM, Dalheimer SL, Ehst BD, Vanasek TL, Jenkins MK, Hertz MI, Mueller DL. Indirect minor histocompatibility antigen presentation by allograft recipient cells in the draining lymph node leads to the activation and clonal expansion of CD4+ T cells that cause obliterative airways disease. J Immunol. 2004;172:3469-3479.
44. Uehara S, Chase CM, Kitchens WH, Rose HS, Colvin RB, Russell PS, Madsen JC. NK cells can trigger allograft vasculopathy: the role of hybrid resistance in solid organ allografts. J Immunol. 2005;175:3424-3430.
45. Cose S. T-cell migration: a naive paradigm? Immunology. 2007;120:1-7.
46. Holzinger C, Zuckermann A, Reinwald C, Imhof M, Schollhammer A, Kramer G, Wolner E, Steiner G. Are T cells from healthy heart really only passengers? Characterization of cardiac tissue T cells. Immunol Lett. 1996;53:63-67.
47. Cose S, Brammer C, Khanna KM, Masopust D, Lefrancois L. Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur J Immunol. 2006;36:1423-1433.
48. Starzl TE, Demetris AJ, Murase N, Ildstad S, Ricordi C, Trucco M. Cell migration, chimerism, and graft acceptance. Lancet. 1992;339:1579-1582.
49. Metes D, Logar A, Rudert WA, Zeevi A, Woodward J, Demetris AJ, Abu-Elmagd K, Eghtesad B, Shapiro R, Fung JJ, Trucco M, Starzl TE, Murase N. Four-color flow cytometric analysis of peripheral blood donor cell chimerism. Hum Immunol. 2003;64:787-795.
50. Anderson CC, Matzinger P. Immunity or tolerance: opposite outcomes of microchimerism from skin grafts. Nat Med. 2001;7:80-87.