Graft rejection mediated by CD4+ T cells via indirect recognition of alloantigen is associated with a dominant Th2 response

European Journal of Immunology

Volumn 35, Issue 3, 2005, Pages 843-851

  Csencsits, Keri ^a   Wood, Sherri Chan ^a   Lu, Guanyi ^a   Magee, John C ^a   Eichwald, Ernst J ^b   Chang, Cheong Hee ^c   Bishop, D Keith ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen recognition; T cells; Th1 Th2; Transplantation

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLOTRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTERY OCCLUSION; ARTICLE; CARDIAC GRAFT REJECTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GRAFT SURVIVAL; GRANULATION TISSUE; HEART MUSCLE NECROSIS; HEART TRANSPLANTATION; HISTOCOMPATIBILITY; HISTOLOGY; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; LYMPHOCYTIC INFILTRATION; MOUSE; MOUSE STRAIN; NONHUMAN; ORGAN DONOR; PRIORITY JOURNAL; RECIPIENT; T CELL DEPLETION; T LYMPHOCYTE; TH1 CELL; TH2 CELL; WILD TYPE;

ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; GRAFT REJECTION; HEART TRANSPLANTATION; IMMUNOGLOBULIN G; ISOANTIGENS; LYMPHOCYTE ACTIVATION; MICE; NUCLEAR PROTEINS; TH2 CELLS; TRANS-ACTIVATORS; TRANSPLANTATION, HETEROTOPIC;

EID: 15844395238     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425685     Document Type: Article

References (56)

1. Lechler, R. I. and Batchelor, J. R., Restoration of immunogenicity to passenger cell-depleted kidney allografts by the addition of donor strain dendritic cells. J. Exp. Med. 1982. 155: 31-41.
2. Braun, M. Y., McCormack, A., Webb, G. and Batchelor, J. R., Mediation of acute but not chronic rejection of MHC-incompatible rat kidney grafts by alloreactive CD4 T cells activated by the direct pathway of sensitization. Transplantation 1993. 55: 177-182.
3. Sherman, L. A. and Chattopadhyay, S., The molecular basis of allorecognition. Annu. Rev. Immunol. 1993. 11: 385-402.
4. Gould, D. S. and Auchincloss, H., Jr., Direct and indirect recognition: the role of MHC antigens in graft rejection. Immuno.l Today 1999. 20: 77-82.
5. Benichou, G., Takizawa, P. A., Olson, C. A., McMillan, M. and Sercarz, E. E., Donor major histocompatibility complex (MHC) peptides are presented by recipient MHC molecules during graft rejection. J. Exp. Med. 1992. 175: 305-308.
6. Shoskes, D. A. and Wood, K. J., Indirect presentation of MHC antigens in transplantation. Immunol. Today 1994. 15: 32-38.
7. Rogers, N. J. and Lechler, R. I., Allorecognition. Am. J. Transplant. 2001. 1: 97-102.
8. Liu, Z., Colovai, A. I., Tugulea, S., Reed, E. F., Fisher, P. E., Mancini, D., Rose, E. A., Cortesini, R., Michler, R. E. and Suciu-Foca, N., Indirect recognition of donor HLA-DR peptides in organ allograft rejection. J. Clin. Invest. 1996. 98: 1150-1157.
9. Benichou, G., Malloy, K. M., Tam, R. C., Heeger, P. S. and Fedoseyeva, E. V., The presentation of self and allogeneic MHC peptides to T lymphocytes. Hum. Immunol. 1998. 59: 540-548.
10. Vella, J. P., Spadafora-Ferreira, M., Murphy, B., Alexander, S. I., Harmon, W., Carpenter, C. B. and Sayegh, M. H., Indirect allorecognition of major histocompatibility complex allopeptides in human renal transplant recipients with chronic graft dysfunction. Transplantation 1997. 64: 795-800.
11. Ciubotariu, R., Liu, Z., Colovai, A. I., Ho, E., Itescu, S., Ravalli, S., Hardy, M. A., Cortesini, R., Rose, E. A. and Suciu-Foca, N., Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts. J. Clin. Invest. 1998. 101: 398-405.
12. Hornick, P. I., Mason, P. D., Yacoub, M. H., Rose, M. L., Batchelor, R. and Lechler, R. I., Assessment of the contribution that direct allorecognition makes to the progression of chronic cardiac transplant rejection in humans. Circulation 1998. 97: 1257-1263.
13. Ensminger, S. M., Spriewald, B. M., Witzke, O., Pajaro, O. E., Yacoub, M. H., Morris, P. J., Rose, M. L. and Wood, K. J., Indirect allorecognition can play an important role in the development of transplant arteriosclerosis. Transplantation 2002. 73: 279-286.
14. Shirwan, H., Chronic allograft rejection. Do the Th2 cells preferentially induced by indirect alloantigen recognition play a dominant role? Transplantation 1999. 68: 715-726.
15. Waaga, A. M., Chandraker, A., Spadafora-Ferreira, M., Iyengar, A. R., Khoury, S. J., Carpenter, C. B. and Sayegh, M. H., Mechanisms of indirect allorecognition: characterization of MHC class II allopeptide-specific T helper cell clones from animals undergoing acute allograft rejection. Transplantation 1998, 65: 876-883.
16. Benichou, G., Valujskikh, A. and Heeger, P. S., Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J. Immunol. 1999. 162: 352-358.
17. + T cell recognition of a single discordant HLA-A2-transgenic molecule through the indirect antigen presentation pathway induces acute rejection of murine cardiac allografts. Transplantation 2001. 71: 1640-1648.
18. DeVito-Haynes, L. D., Jankowska-Gan, E., Heisey, D., Jutte, N. H., Balk, A. H., Weimar, W., Claas, F. H., Warner, T. F., Mentzer, R. M., Love, R. B. and Burlingham, W. J., Donor-derived leukocyte antigen class I proteins in the serum of heart transplant recipients. J. Heart Lung Transplant. 1996. 15: 1012-1026.
19. Lee, R. S., Grusby, M. J., Glimcher, L. H., Winn, H. J. and Auchincloss, H.,Jr., Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo. J. Exp. Med. 1994. 179: 865-872.
20. Steele, D. J., Laufer, T. M., Smiley, S. T., Ando, Y., Grusby, M. J., Glimcher, L. H. and Auchincloss, H., Jr., Two levels of help for B cell alloantibody production. J. Exp. Med. 1996. 183: 699-703.
21. Pettigrew, G. J., Lovegrove, E., Bradley, J. A., Maclean, J. and Bolton, E. M., Indirect T cell allorecognition and alloantibody-mediated rejection of MHC class I-disparate heart grafts. J. Immunol. 1998. 161: 1292-1298.
22. Auchincloss, H., Jr., Lee, R., Shea, S., Markowitz, J. S., Grusby, M. J. and Glimcher, L. H., 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: 3373-3377.
23. Campos, L., Naji, A., Deli, B. C., Kern, J. H., Kim, J. I., Barker, C. F. and Markmann, J. F., Survival of MHC-deficient mouse heterotopic cardiac allografts. Transplantation 1995. 59: 187-191.
24. Pietra, B. A., Wiseman, A., Bolwerk, A., Rizeq, M. and Gill, R. G., CD4 T cell-mediated cardiac allograft rejection requires donor but not host MHC class II. J. Clin. Invest. 2000. 106: 1003-1010.
25. -/- mice show the importance of major histocompatibility complex-bound peptide in cardiac allograft rejection. J. Exp. Med. 2000. 192: 31-40.
26. June Brickey, W., Felix, N. J., Griffiths, R., Zhang, J., Wang, B., Piskurich, J. F., Itoh-Lindstrom, Y., Coffman, T. M. and Ting, J. P.-Y., Prolonged survival of class II transactivator-deficient cardiac allografts. Transplantation 2002. 74: 1341-1348.
27. Chang, C.-H., Guerder, S., Hong, S. C., van Ewijk, W. and Flavell, R. A., Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity 1996. 4: 167-178.
28. Williams, G. S., Malin, M., Vremec, D., Chang, C. H., Boyd, R., Benoist, C. and Mathis, D., Mice lacking the transcription factor CIITA-a second look. Int. Immunol. 1998. 10: 1957-1967.
29. -/- in second-set skin allograft rejection. J. Surg. Res. 2002. 102: 185-192.
30. Sims, T. N., Afrouzian, M., Urmson, J., Zhu, L. F. and Halloran, P. F., The role of the class II transactivator (CIITA) in MHC class I and II regulation and graft rejection in kidney. Am. J. Transplant. 2001. 1: 211-221.
31. Bishop, D. K., DeBruyne, L. A., Chan, S., Xu, S. and Eichwald, E. J., Dissociation of mouse cardiac transplant rejection and donor alloantigen-specific T cell responsiveness. Transplant. Immunol. 1995. 3: 222-228.
32. Piccotti, J. R., Chan, S. Y., Goodman, R. E., Magram, J., Eichwald, E. J. and Bishop, D. K., IL-12 antagonism induces T helper 2 responses, yet exacerbates cardiac allograft rejection. Evidence against a dominant protective role for T helper 2 cytokines in alloimmunity. J. Immunol. 1996. 157: 1951-1957.
33. Chan, S. Y., DeBruyne, L. A., Goodman, R. E., Eichwald, E. J. and Bishop, D. K., In vivo depletion of CD8+ T cells results in Th2 cytokine production and alternate mechanisms of allograft rejection. Transplantation 1995. 59: 1155-1161.
34. Le Moine, A., Flamand, V., Demoor, F.-X., Noel, J.-C., Surquin, M., Kiss, R., Nahori, M.-A., Pretolani, M., Goldman, M. and Abramowicz, D., Critical roles for IL-4, IL-5, and eosinophils in chronic skin allograft rejection. J. Clin. Invest. 1999. 103: 1659-1667:
35. + lymphocytes and IFN-γ. Eur. J. Immunol. 2000. 30: 1290-1296.
36. Goldman, M., Le Moine, A., Braun, M. Y., Flamand, V. and Abramowicz, D., A role for eosinophils in transplant rejection. Trends Immunol. 2001. 22: 247-251.
37. Bishop, D. K., Shelby, J. and Eichwald, E. J., Mobilization of T lymphocytes following cardiac transplantation. Evidence that CD4-positive cells are required for cytotoxic T lymphocyte activation, inflammatory endothelial development, graft infiltration, and acute allograft rejection. Transplantation 1992. 53: 849-857.
38. Piccotti, J. R., Li, K., Chan, S. Y., Ferrante, J., Magram, J., Eichwald, E. J. and Bishop, D. K., Alloantigen-reactive Th1 development in IL-12-deficient mice. J. Immunol. 1998. 160: 1132-1138.
39. Fischer K., Collins, H., Taniguchi, M., Kaufmann, S. H. E. and Schaible, U. E., IL-4 and T cells are required for generation of IgG1 isotype antibodies against cardiolipin. J. Immunol. 2002. 168: 2689-2694.
40. Snapper, C. M., Peschel, C. and Paul, W. E., IFN-γ stimulates IgG2a secretion by murine B cells stimulated with baterial lipopolysaccharide. J. Immunol. 1988. 140: 2121-2127.
41. Itoh-Lindstrom, Y., Piskurich, J. F., Felix, N. J., Wang, Y., Brickey, W. J., Platt, J. L., Koller, B. H. and Ting, J. P., Reduced IL-4-, lipopolysaccharide-, and IFN-γ-induced MHC class II expression in mice lacking class II transactivator due to targeted deletion of the GTP-binding domain. J. Immunol. 1999. 163: 2425-2431.
42. Foucras, G., Coudert, J. D., Coureau, C. and Guery, J.-C., Dendritic cells prime in vivo alloreactive CD4 T lymphocytes toward type 2 cytokine- and TGFβ-producing cells in the absence of CD8 T cell activation. J. Immunol. 2000. 165: 4994-5003.
43. + cells and CD40-CD40 ligand interactions. J. Immunol. 2001. 166: 3248-3255.
44. Koniecnzy, B. T., Dai, Z., Elwood, E. T., Saleem, S., Linsley, P. S., Baddoura, F. K., Larsen, C. P., Pearson, T. C. and Lakkis, F. G., IFN-γ is critical for long-term allograft survival induced by blocking the CD28 and CD40 ligand T cell costimulation pathways. J. Immunol. 1998. 160: 2059-2064.
45. Bishop, D. K., Chan, S., Li, W., Ensley, R. D., Xu, S. and Eichwald, E. J., CD4-positive helper T lymphocytes mediate mouse cardiac allograft rejection independent of donor alloantigen specific cytotoxic T lymphocytes. Transplantation 1993. 56: 892-897.
46. Mathis, D. J., Benoist, C., Williams, V. E., 2nd, Kanter, M. and McDevitt, H. O., Several mechanisms can account for defective E alpha gene expression in different mouse haplotypes. Proc. Natl. Acad. Sci. USA 1983. 80: 273-277.
47. Fremont, D. H., Hendrickson, W. A., Marrack, P. and Kappler, J., Structures of an MHC class II molecule with covalently bound single peptides. Science 1996. 272: 1001-1004.
48. Bradley, B. A., The role of HLA matching in transplantation. Immunol. Lett 1991. 29: 55-59.
49. Braun, M. Y., Grandjean, I., Feunou, P., Duban, L., Kiss, R., Goldman, M. and Lantz, O., Acute rejection in the absence of cognate recognition of allograft by T cells. J. Immunol. 2001. 166: 4879-4883.
50. Chen, Y., Demir, Y., Valujskikh, A. and Heeger, P. S., The male minor transplantation antigen preferentially activates recipient CD4+ T cells through the indirect presentation pathway in vivo. J. Immunol. 2003. 171: 6510-6518.
51. Sacks, D. and Noben-Trauth, N., The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002. 2: 845-858.
52. + T cells during a Th2 response in Leishmania major-infected mice. Eur. J. Immunol. 2000. 30: 2007-2014.
53. Laskay, T., Diefenbach, A., Rollinghoff, M. and Solbach, W., Early parasite containment is decisive for resistance to Leishmania major infection. Eur. J. Immunol. 1995. 25: 2220-2227.
54. Kane, M. M. and Mosser, D. M., The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 2001. 166: 1141-1147.
55. + T cells in vivo. J. Exp. Med. 1991. 173: 1463-1471.
56. Corry, R. J., Winn, H. J. and Russell, P. S., Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2 K, and non-H-2 antigens in rejection. Transplantation 1973. 16: 343-350.