An important role for autoimmunity in the immunopathogenesis of chronic allograft rejection

International Journal of Immunogenetics

Volumn 39, Issue 5, 2012, Pages 373-380

  Tiriveedhi, V ^a   Sarma, N ^a   Mohanakumar, T ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 5; CYTOSKELETON PROTEIN; HISTOCOMPATIBILITY ANTIGEN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; LYMPHOKINE; MYOSIN; RAPAMYCIN; RITUXIMAB; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VIMENTIN;

ALLOIMMUNITY; ALLOTRANSPLANTATION; AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL INFILTRATION; CHRONIC GRAFT REJECTION; CORONARY ARTERY ATHEROSCLEROSIS; EPITHELIUM HYPERPLASIA; FIBROSIS; GRAFT FAILURE; GRAFT RECIPIENT; GRAFT SURVIVAL; HELPER CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; ISOGRAFT; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; MUCOSAL IMMUNITY; NONHUMAN; OCCLUSION; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; VIRUS INFECTION;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; CARDIAC MYOSINS; GRAFT REJECTION; HLA ANTIGENS; HUMANS; LYMPHOCYTE COUNT; ORGAN TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84865864040     PISSN: 17443121     EISSN: 1744313X     Source Type: Journal    
DOI: 10.1111/j.1744-313X.2012.01112.x     Document Type: Review

References (69)

1. Atz, M.E. & Reed, E.F. (2008) Role of anti-MHC class I antibody in facilitating transplant accommodation. Critical Reviews in Immunology, 28, 485.
2. Benichou, G. & Fedoseyeva, E.V. (1996) The contribution of peptides to T cell allorecognition and allograft rejection. International Reviews of Immunology, 13, 231.
3. Benichou, G., Valujskikh, A. & Heeger, P.S. (1999) Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J Immunol, 162, 352.
4. Bestard, O., Nickel, P., Cruzado, J.M., Schoenemann, C., Boenisch, O., Sefrin, A., Grinyo, J.M., Volk, H.D. & Reinke, P. (2008) Circulating alloreactive T cells correlate with graft function in longstanding renal transplant recipients. Journal of the American Society of Nephrology, 19, 1419.
5. Bharat, A., Fields, R.C., Steward, N., Trulock, E.P., Patterson, G.A. & Mohanakumar, T. (2006a) CD4+25+ regulatory T cells limit Th1-autoimmunity by inducing IL-10 producing T cells following human lung transplantation. American Journal of Transplantation, 6, 1799.
6. Bharat, A., Fields, R.C., Trulock, E.P., Patterson, G.A. & Mohanakumar, T. (2006b) Induction of IL-10 suppressors in lung transplant patients by CD4+25+ regulatory T cells through CTLA-4 signaling. Journal of immunology, 177, 5631.
7. Bharat, A., Kuo, E., Saini, D., Steward, N., Hachem, R., Trulock, E.P., Patterson, G.A., Meyers, B.F. & Mohanakumar, T. (2010) Respiratory virus-induced dysregulation of T-regulatory cells leads to chronic rejection. Annals of Thoracic Surgery, 90, 1637.
8. Bhorade, S., Ahya, V.N., Baz, M.A., Valentine, V.G., Arcasoy, S.M., Love, R.B. et al. (2011) Comparison of sirolimus with azathioprine in a tacrolimus-based immunosuppressive regimen in lung transplantation. American Journal of Respiratory and Critical Care Medicine, 183, 379.
9. Birnbaum, L.M., Lipman, M., Paraskevas, S., Chaudhury, P., Tchervenkov, J., Baran, D., Herrera-Gayol, A. & Cantarovich, M. (2009) Management of chronic allograft nephropathy: a systematic review. Clinical Journal of American Society of Nephrology, 4, 860.
10. Burke III, G.W., Vendrame, F., Pileggi, A., Ciancio, G., Reijonen, H. & Pugliese, A. (2011) Recurrence of autoimmunity following pancreas transplantation. Current Diabetes Reports, 11, 413.
11. Burlingham, W.J., Love, R.B., Jankowska-Gan, E., Haynes, L.D., Xu, Q., Bobadilla, J.L. et al. (2007) IL-17-dependent cellular immunity to collagen type V predisposes to obliterative bronchiolitis in human lung transplants. Journal of Clinical Investigation, 117, 3498.
12. Ciancio, G., Burke, G.W., Gaynor, J.J., Carreno, M.R., Cirocco, R.E., Mathew, J.M. et al. (2005) A randomized trial of three renal transplant induction antibodies: early comparison of tacrolimus, mycophenolate mofetil, and steroid dosing, and newer immune-monitoring. Transplantation, 80, 457.
13. Cypel, M., Liu, M., Rubacha, M., Yeung, J.C., Hirayama, S., Anraku, M. et al. (2009) Functional repair of human donor lungs by IL-10 gene therapy. Science Translational Medicine, 1, 4ra9.
14. El-Zoghby, Z.M., Stegall, M.D., Lager, D.J., Kremers, W.K., Amer, H., Gloor, J.M. & Cosio, F.G. (2009) Identifying specific causes of kidney allograft loss. American Journal of Transplantation, 9, 527.
15. Fishman, J.A. (2007) Infection in solid-organ transplant recipients. New England Journal of Medicine, 357, 2601.
16. Fotheringham, J., Angel, C.A. & McKane, W. (2009) Transplant glomerulopathy: morphology, associations and mechanism. Nephron Clinical Practice, 113, c1.
17. Fukami, N., Ramachandran, S., Saini, D., Walter, M., Chapman, W., Patterson, G.A. & Mohanakumar, T. (2009) Antibodies to MHC class I induce autoimmunity: role in the pathogenesis of chronic rejection. Journal of Immunology, 182, 309.
18. Game, D.S. & Lechler, R.I. (2002) Pathways of allorecognition: implications for transplantation tolerance. Transplant Immunology, 10, 101.
19. Girnita, A.L., McCurry, K.R. & Zeevi, A. (2007) Increased lung allograft failure in patients with HLA-specific antibody. Clinical Transplants, 23, 1.
20. Goers, T.A., Ramachandran, S., Aloush, A., Trulock, E., Patterson, G.A. & Mohanakumar, T. (2008) De novo production of K-alpha1 tubulin-specific antibodies: role in chronic lung allograft rejection. Journal of Immunology, 180, 4487.
21. Grossman, E.J. & Shilling, R.A. (2009) Bronchiolitis obliterans in lung transplantation: the good, the bad, and the future. Translational Research, 153, 153.
22. Hachem, R.R. (2009) Lung allograft rejection: diagnosis and management. Current Opinion in Organ Transplantation, 14, 477.
23. Hachem, R.R., Yusen, R.D., Meyers, B.F., Aloush, A.A., Mohanakumar, T., Patterson, G.A. & Trulock, E.P. (2010) Anti-human leukocyte antigen antibodies and preemptive antibody-directed therapy after lung transplantation. Journal of Heart and Lung Transplantation, 29, 973.
24. Haque, M.A., Mizobuchi, T., Yasufuku, K., Fujisawa, T., Brutkiewicz, R.R., Zheng, Y. et al. (2002) Evidence for immune responses to a self-antigen in lung transplantation: role of type V collagen-specific T cells in the pathogenesis of lung allograft rejection. Journal of Immunology, 169, 1542.
25. Hauptman, P.J. & O'Connor, K.J. (1997) Procurement and allocation of solid organs for transplantation. New England Journal of Medicine, 336, 422.
26. Heeger, P.S. (2003) T-cell allorecognition and transplant rejection: a summary and update. American Journal of Transplantation, 3, 525.
27. Hertig, A., Anglicheau, D., Verine, J., Pallet, N., Touzot, M., Ancel, P.Y. et al. (2008) Early epithelial phenotypic changes predict graft fibrosis. Journal of the American Society of Nephrology, 19, 1584.
28. Hornick, P. & Rose, M. (2006) Chronic rejection in the heart. Methods in Molecular Biology, 333, 131.
29. Iwata, T., Philipovskiy, A., Fisher, A.J., Presson Jr, R.G., Chiyo, M., Lee, J. et al. (2008) Anti-type V collagen humoral immunity in lung transplant primary graft dysfunction. Journal of Immunology, 181, 5738.
30. Jaramillo, A., Smith, M.A., Phelan, D., Sundaresan, S., Trulock, E.P., Lynch, J.P., Cooper, J.D., Patterson, G.A. & Mohanakumar, T. (1999) Development of ELISA-detected anti-HLA antibodies precedes the development of bronchiolitis obliterans syndrome and correlates with progressive decline in pulmonary function after lung transplantation. Transplantation, 67, 1155.
31. Jaramillo, A., Smith, C.R., Maruyama, T., Zhang, L., Patterson, G.A. & Mohanakumar, T. (2003) 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. Human immunology, 64, 521.
32. Jindra, P.T., Hsueh, A., Hong, L., Gjertson, D., Shen, X.D., Gao, F. et al. (2008) Anti-MHC class I antibody activation of proliferation and survival signaling in murine cardiac allografts. Journal of Immunology, 180, 2214.
33. Joosten, S.A., Sijpkens, Y.W., van Ham, V., Trouw, L.A., van der Vlag, J., van den Heuvel, B., van Kooten, C. & Paul, L.C. (2005) Antibody response against the glomerular basement membrane protein agrin in patients with transplant glomerulopathy. American Journal of Transplantation, 5, 383.
34. Kaczmarek, I., Deutsch, M.A., Kauke, T., Beiras-Fernandez, A., Schmoeckel, M., Vicol, C., Sodian, R., Reichart, B., Spannagl, M. & Ueberfuhr, P. (2008) Donor-specific HLA alloantibodies: long-term impact on cardiac allograft vasculopathy and mortality after heart transplant. Experimental and Clinical Transplantation, 6, 229.
35. Kalache, S., Dinavahi, R., Pinney, S., Mehrotra, A., Cunningham, M.W. & Heeger, P.S. (2011) Anticardiac myosin immunity and chronic allograft vasculopathy in heart transplant recipients. Journal of Immunology, 187, 1023.
36. Leong, H.S., Mahesh, B.M., Day, J.R., Smith, J.D., McCormack, A.D., Ghimire, G., Podor, T.J. & Rose, M.L. (2008) Vimentin autoantibodies induce platelet activation and formation of platelet-leukocyte conjugates via platelet-activating factor. Journal of Leukocyte Biology, 83, 263.
37. Li, C. & Yang, C.W. (2009) The pathogenesis and treatment of chronic allograft nephropathy. Nature reviews. Nephrology, 5, 513.
38. Lietz, K., John, R., Burke, E., Schuster, M., Rogers, T.B., Suciu-Foca, N., Mancini, D. & Itescu, S. (2005) Immunoglobulin M-to-immunoglobulin G anti-human leukocyte antigen class II antibody switching in cardiac transplant recipients is associated with an increased risk of cellular rejection and coronary artery disease. Circulation, 112, 2468.
39. Maruyama, T., Jaramillo, A., Narayanan, K., Higuchi, T. & Mohanakumar, T. (2005) Induction of obliterative airway disease by anti-HLA class I antibodies. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons, 5, 2126.
40. Meier-Kriesche, H.U., Schold, J.D., Srinivas, T.R. & Kaplan, B. (2004) Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons, 4, 378.
41. Mertens, V., Dupont, L. & Sifrim, D. (2010) Relevance of GERD in lung transplant patients. Current gastroenterology reports, 12, 160.
42. Millington, T.M. & Madsen, J.C. (2010) Innate immunity and cardiac allograft rejection. Kidney International. Supplement, 119, S18.
43. Mizobuchi, T., Yasufuku, K., Zheng, Y., Haque, M.A., Heidler, K.M., Woods, K. et al. (2003) Differential expression of Smad7 transcripts identifies the CD4+CD45RChigh regulatory T cells that mediate type V collagen-induced tolerance to lung allografts. Journal of Immunology, 171, 1140.
44. Morris, G.P., Phelan, D.L., Jendrisak, M.D. & Mohanakumar, T. (2010) Virtual crossmatch by identification of donor-specific anti-human leukocyte antigen antibodies by solid-phase immunoassay: a 30-month analysis in living donor kidney transplantation. Human Immunology, 71, 268.
45. Nakajima, J., Poindexter, N.J., Hillemeyer, P.B., Trulock, E.P., Cooper, J.D., Patterson, G.A., Mohanakumar, T. & Sundaresan, R.S. (1999) Cytotoxic T lymphocytes directed against donor HLA class I antigens on airway epithelial cells are present in bronchoalveolar lavage fluid from lung transplant recipients during acute rejection. Journal of Thoracic and Cardiovascular Surgery, 117, 565.
46. Nath, D.S., Ilias Basha, H., Tiriveedhi, V., Alur, C., Phelan, D., Ewald, G.A., Moazami, N. & Mohanakumar, T. (2010) 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, 29, 1277.
47. Nath, D.S., Tiriveedhi, V., Basha, H.I., Phelan, D., Moazami, N., Ewald, G.A. & Mohanakumar, T. (2011) A role for antibodies to human leukocyte antigens, collagen-V, and K-alpha1-Tubulin in antibody-mediated rejection and cardiac allograft vasculopathy. Transplantation, 91, 1036.
48. Ojo, A.O., Held, P.J., Port, F.K., Wolfe, R.A., Leichtman, A.B., Young, E.W., Arndorfer, J., Christensen, L. & Merion, R.M. (2003) Chronic renal failure after transplantation of a nonrenal organ. New England Journal of Medicine, 349, 931.
49. Palmer, S.M., Davis, R.D., Hadjiliadis, D., Hertz, M.I., Howell, D.N., Ward, F.E., Savik, K. & Reinsmoen, N.L. (2002) Development of an antibody specific to major histocompatibility antigens detectable by flow cytometry after lung transplant is associated with bronchiolitis obliterans syndrome. Transplantation, 74, 799.
50. Paraskeva, M., Bailey, M., Levvey, B.J., Griffiths, A.P., Kotsimbos, T.C., Williams, T.P., Snell, G. & Westall, G. (2011) Cytomegalovirus replication within the lung allograft is associated with bronchiolitis obliterans syndrome. American Journal of Transplantation, 11, 2190.
51. Paul, L.C., Muralidharan, J., Muzaffar, S.A., Manting, E.H., Valentin, J.F., de Heer, E. & Kashgarian, M. (1998) Antibodies against mesangial cells and their secretory products in chronic renal allograft rejection in the rat. American Journal of Pathology, 152, 1209.
52. Potena, L. & Valantine, H.A. (2007) Cytomegalovirus-associated allograft rejection in heart transplant patients. Current opinion in infectious diseases, 20, 425.
53. Reznik, S.I., Jaramillo, A., SivaSai, K.S., Womer, K.L., Sayegh, M.H., Trulock, E.P., Patterson, G.A. & Mohanakumar, T. (2001) Indirect allorecognition of mismatched donor HLA class II peptides in lung transplant recipients with bronchiolitis obliterans syndrome. American Journal of Transplantation, 1, 228.
54. Rizzo, M., Sundaresan, S., Lynch, J., Trulock, E.P., Cooper, J., Patterson, G.A. & Mohanakumar, T. (1997) Increased concentration of soluble human leukocyte antigen class I levels in the bronchoalveolar lavage of human pulmonary allografts. Journal of Heart and Lung Transplantation, 16, 1135.
55. Robertson, R.P. (2004) Islet transplantation as a treatment for diabetes - a work in progress. New England Journal of Medicine, 350, 694.
56. Rose, M.L. & Smith, J.D. (2009) Clinical relevance of complement-fixing antibodies in cardiac transplantation. Human Immunology, 70, 605.
57. Saini, D., Weber, J., Ramachandran, S., Phelan, D., Tiriveedhi, V., Liu, M. et al. (2011) Alloimmunity-induced autoimmunity as a potential mechanism in the pathogenesis of chronic rejection of human lung allografts. Journal of Heart and Lung Transplantation, 30, 624.
58. Sakaguchi, S. & Sakaguchi, N. (2005) Regulatory T cells in immunologic self-tolerance and autoimmune disease. International Reviews of Immunology, 24, 211.
59. Shilling, R.A. & Wilkes, D.S. (2009) Immunobiology of chronic lung allograft dysfunction: new insights from the bench and beyond. American Journal of Transplantation, 9, 1714.
60. Steele, D.J., Laufer, T.M., Smiley, S.T., Ando, Y., Grusby, M.J., Glimcher, L.H. & Auchincloss Jr, H. (1996) Two levels of help for B cell alloantibody production. Journal of Experimental Medicine, 183, 699.
61. Sumpter, T.L. & Wilkes, D.S. (2004) Role of autoimmunity in organ allograft rejection: a focus on immunity to type V collagen in the pathogenesis of lung transplant rejection. American Journal of Physiology. Lung Cellular and Molecular Physiology, 286, L1129.
62. Tiriveedhi, V., Weber, J., Seetharam, A. & Mohanakumar, T. (2010a) Cross-talk of alloimmune response and autoimmunity: role in pathogenesis of chronic rejection. Discovery Medicine, 9, 229.
63. Tiriveedhi, V., Angaswamy, N., Weber, J. & Mohanakumar, T. (2010b) Lipid raft facilitated ligation of K-alpha1-tubulin by specific antibodies on epithelial cells: role in pathogenesis of chronic rejection following human lung transplantation. Biochemical and Biophysical Research Communications, 399, 251.
64. Tiriveedhi, V., Angaswamy, N., Brand, D., Weber, J., Gelman, A.G., Hachem, R., Trulock, E.P., Meyers, B., Patterson, G. & Mohanakumar, T. (2012) A shift in the collagen V antigenic epitope leads to T helper phenotype switch and immune response to self-antigen leading to chronic lung allograft rejection. Clinical and Experimental Immunology, 167, 158.
65. Tiriveedhi, V., Gelman, A.E. & Mohanakumar, T. (2012) HIF-1α signaling by airway epithelial cell K-α1-tubulin: role in fibrosis and chronic rejection of human lung allografts. Cellular Immunology, 273, 59.
66. Yamakuchi, M., Kirkiles-Smith, N.C., Ferlito, M., Cameron, S.J., Bao, C., Fox-Talbot, K., Wasowska, B.A., Baldwin III, W.M., Pober, J.S. & Lowenstein, C.J. (2007) Antibody to human leukocyte antigen triggers endothelial exocytosis. Proceedings of the National Academy of Sciences of the United States of America, 104, 1301.
67. Yasui, H., Ogura, A., Asanuma, T., Matsuda, A., Kashiwakura, I., Kuwabara, M. & Inanami, O. (2008) Inhibition of HIF-1alpha by the anticancer drug TAS106 enhances X-ray-induced apoptosis in vitro and in vivo. British Journal of Cancer, 99, 1442.
68. Yeo, E.J., Chun, Y.S., Cho, Y.S., Kim, J., Lee, J.C., Kim, M.S. & Park, J.W. (2003) YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. Journal of the National Cancer Institute, 95, 516.
69. Yoshida, S., Haque, A., Mizobuchi, T., Iwata, T., Chiyo, M., Webb, T.J. et al. (2006) Anti-type V collagen lymphocytes that express IL-17 and IL-23 induce rejection pathology in fresh and well-healed lung transplants. American Journal of Transplantation, 6, 724.