Novel CD8 T cell alloreactivities in CCR5-deficient recipients of class II MHC disparate kidney grafts

Journal of Immunology

Volumn 193, Issue 7, 2014, Pages 3816-3824

  Ishii, Daisuke ^a,b   Rosenblum, Joshua M ^a,c   Nozaki, Taiji ^a   Schenk, Austin D ^a,c   Setoguchi, Kiyoshi ^a   Su, Charles A ^a,c   Gorbacheva, Victoria ^a   Baldwin, William M ^a,c   Valujskikh, Anna ^a,c   Fairchild, Robert L ^a,c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b KITASATO UNIVERSITY   (Japan)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; CYTOKINE; H2 ANTIGEN; HLA ANTIGEN CLASS 2;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; ENDOTHELIUM CELL; GRAFT SURVIVAL; KIDNEY GRAFT; KIDNEY GRAFT REJECTION; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; ALLOGRAFT; ANIMAL; GENETICS; GRAFT REJECTION; IMMUNOLOGY; KIDNEY TRANSPLANTATION; KNOCKOUT MOUSE; PATHOLOGY;

ALLOGRAFTS; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; GRAFT REJECTION; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS II; KIDNEY TRANSPLANTATION; MICE; MICE, KNOCKOUT; RECEPTORS, CCR5;

EID: 84907200991     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303256     Document Type: Article

References (37)

1. Rosenberg, A. S., and A. Singer. 1992. Cellular basis of skin allograft rejection: an in vivo model of immune-mediated tissue destruction. Annu. Rev. Immunol. 10: 333-358.
2. Sho, M., A. Yamada, N. Najafian, A. D. Salama, H. Harada, S. E. Sandner, A. Sanchez-Fueyo, X. X. Zheng, T. B. Strom, and M. H. Sayegh. 2002. Physiological mechanisms of regulating alloimmunity: cytokines, CTLA-4, CD25+ cells, and the alloreactive T cell clone size. J. Immunol. 169: 3744-3751.
3. Wood, K. J., and R. Goto. 2012. Mechanisms of rejection: current perspectives. Transplantation 93: 1-10.
4. Afzali, B., G. Lombardi, and R. I. Lechler. 2008. Pathways of ma jor histocompatibility complex allorecognition. Curr. Opin. Organ Transplant. 13: 438-444.
5. Benichou, G., A. Valujskikh, and P. S. Heeger. 1999. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J. Immunol. 162: 352-358.
6. Heeger, P. S. 2003. T-cell allorecognition and transplant rejection: a summary and update. Am. J. Transplant. 3: 525-533.
7. Zhang, Q., Y. Chen, R. L. Fairchild, P. S. Heeger, and A. Valujskikh. 2006. Lymphoid sequestration of alloreactive memory CD4 T cells promotes cardiac allograft survival. J. Immunol. 176: 770-777.
8. Lee, R. S., M. J. Grusby, L. H. Glimcher, H. J. Winn, and H. Auchincloss, Jr. 1994. Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo. J. Exp. Med. 179: 865-872.
9. Pettigrew, G. J., E. Lovegrove, J. A. Bradley, J. Maclean, and E. M. Bolton. 1998. Indirect T cell allorecognition and alloantibody-mediated rejection of MHC class I-disparate heart grafts. J. Immunol. 161: 1292-1298.
10. Steele, D. J., T. M. Laufer, S. T. Smiley, Y. Ando, M. J. Grusby, L. H. Glimcher, and H. Auchincloss, Jr. 1996. Two levels of help for B cell alloantibody production. J. Exp. Med. 183: 699-703.
11. Hansen, S. G., J. B. Sacha, C. M. Hughes, J. C. Ford, B. J. Burwitz, I. Scholz, R. M. Gilbride, M. S. Lewis, A. N. Gilliam, A. B. Ventura, et al. 2013. Cytomegalovirus vector violate CD8+ T cell epitope recognition paradigms. Science 340: 1237874.
12. Rist, M., C. Smith, M. J. Bell, S. R. Burrows, and R. Khanna. 2009. Crossrecognition of HLA DR4 alloantigen by virus-specific CD8+ T cells: a new paradigm for self-/nonself-recognition. Blood 114: 2244-2253.
13. McKenzie, I. F., G. M. Morgan, M. S. Sandrin, M. M. Michaelides, R. W. Melvold, and H. I. Kohn. 1979. B6.C-H-2bm12. A new H-2 mutation in the I region in the mouse. J. Exp. Med. 150: 1323-1338.
14. Mengle-Gaw, L., S. Conner, H. O. McDevitt, and C. G. Fathman. 1984. Gene conversion between murine class II major histocompatibility complex loci. Functional and molecular evidence from the bm 12 mutant. J. Exp. Med. 160: 1184-1194.
15. Schenk, S., D. D. Kish, C. He, T. El-Sawy, E. Chiffoleau, C. Chen, Z. Wu, S. Sandner, A. V. Gorbachev, K. Fukamachi, et al. 2005. Alloreactive T cell responses and acute rejection of single class II MHC-disparate heart allografts are under strict regulation by CD4+ CD25+ T cells. J. Immunol. 174: 3741-3748.
16. Yun, J. J., M. P. Fischbein, D. Whiting, Y. Irie, M. C. Fishbein, M. D. Burdick, J. Belperio, R. M. Strieter, H. Laks, J. A. Berliner, and A. Ardehali. 2002. The role of MIG/CXCL9 in cardiac allograft vasculopathy. Am. J. Pathol. 161: 1307-1313.
17. Nozaki, T., J. M. Rosenblum, A. D. Schenk, D. Ishii, and R. L. Fairchild. 2009. CCR5 is required for regulation of alloreactive T-cell responses to single class II MHC-mismatched murine cardiac grafts. Am. J. Transplant. 9: 2251-2261.
18. B ickerstaff, A. A., J. J. Wang, R. P. Pelletier, and C. G. Orosz. 2001. Murine renal allografts: spontaneous acceptance is associated with regulated T cellmediated immunity. J. Immunol. 167: 4821-4827.
19. Miyajima, M., C. M. Chase, A. Alessandrini, E. A. Farkash, P. Della Pelle, G. Benichou, J. A. Graham, J. C. Madsen, P. S. Russell, and R. B. Colvin. 2011. Early acceptance of renal allografts in mice is de pendent on Foxp3(+) cells. Am. J. Pathol. 178: 1635-1645 .
20. Russell P.S.,C.M. Chase,R.B. Colvin,J.M. Plate., 1978, Kidney transplants in mice. An analysis of the immune status of mice be aring long-term, H-2 incompatible transplants. J. Exp. Med., 147, 1449-1468.
21. Bickerstaff, A., T. Nozaki, J.-J. Wang, R. Pelletier, G. Hadley, G. Nadasdy, T. Nadasdy, and R. L. Fair child. 2008. Acute humoral rejection of renal allografts in CCR5(-/-) recipients. Am. J. Transplant. 8: 557-566.
22. Zhang, Z., C. Schlachta, J. Duff, C. Stiller, D. Grant, and R. Zhong. 1995. Improved techniques for kidney transplantation in mice. Microsurgery 16: 103-109.
23. Corry, R. J., H. J. Winn, and P. S. Russell. 1973. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16: 343-350.
24. Schenk, A. D., T. Nozaki, M. Rabant, A. Valujskikh, and R. L. Fairchild. 2008. Donor-reactive CD8 memor y T cells infiltrate cardiac allografts within 24-h posttransplant in naive recipients. Am. J. Transplant. 8: 1652-1661.
25. Afanasyeva, M., D. Georgakopoulos, D. F. Belardi, A. C. Ramsundar, J. G. Barin, D. A. Kass, and N. R. Rose. 2004. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: correlation with cardiac function. Am. J. Pathol. 164: 807-815.
26. S etoguchi, K., A. D. Schenk, D. Ishii, Y. Hattori, W. M. Baldwin, III, K. Tanabe, and R. L. Fairchild. 2011. LFA-1 antagonism inhibits early infiltration of endogenous memory CD8 T cells into cardiac allografts and donor-re active T cell priming. Am. J. Transplant. 11: 923-935.
27. Kreisel, D., A. S. Krupnick, W. Y. Szeto, S. H. Popma, D. Sankaran, A. M. Krasinskas, K. M. Amin, and B. R. Rosengard. 2001. A simple method for culturing mouse vascular endothelium. J. Immunol. Methods 254: 31-45.
28. Valujskikh, A., O. Lantz, S. Celli, P. Matzinger, and P. S. Heeger. 2002. Crossprimed CD8(+) T cells mediate graft rejection via a distinct effector pathway. Nat. Immunol. 3: 844-851.
29. Melino, M. R., S. L. Epstein, D. H. Sachs, and T. H. Hansen. 1983. Idiotypic and fluorometric analysis of the antibodies that distinguish the lesion of the I-A mutant B6.C-H-2bm12. J. Immunol. 131: 359-364.
30. Kreisel, D., A. S. Krupnick, A. E. Gelman, F. H. Engels, S. H. Popma, A. M. Krasinskas, K. R. Balsara, W. Y. Szeto, L. A. Turka, and B. R. Rosengard. 2002. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an a lternative mechanism of allorecognition. Nat. Med. 8: 233-239.
31. Schnickel, G. T., D. Whiting, G. R. Hsieh, J. J. Yun, M. P. Fischbein, M. C. Fishbein, W. Yao, A. Shfizadeh, and A. Ardeha li. 2004. CD8 lymphocytes are sufficient for the development of chronic rejection. Transplantation 78: 1634-1639.
32. Al-Lamki, R. S., J. R. Bradley, and J. S. Pober. 2008. Endothelial cells in allograft rejection. Transplantation 86: 1340-1348.
33. Skaro, A. I., R. S. Liwski, J. Zhou, E. L. Vessie, T. D. G. Lee, and G. M. Hirsch. 2005. CD8+ T cells mediate aortic allograft vasculopathy by direct killing and an interferon-g-dependent indirect pathway. Cardiovasc. Res. 65: 283-291.
34. Valujskikh, A., and P. S. Heeger. 2003. Emerging roles of endothelial cells in transplant rejection. Curr. Opin. Immunol. 15: 493-498.
35. Bickerstaff, A., R. Pelletier, J.-J. Wang, G. Nadasdy, N. DiPaola, C. Orosz, A. Satoskar, G. Hadley, and T. Nadasdy. 2008. An experiment al model of acute humoral rejection of renal allografts associated with concomitant cellular rejection. Am. J. Pathol. 173: 347-357.
36. Sun, Q., Z. H. Liu, Z. Cheng, J. Chen, S. Ji, C. Zeng, and L. S. Li. 2007. Treatment of early mixed cellular and humoral renal allograft rejection with tacrolimus and mycophenolate mofetil. Kidney Int. 71: 24-30.
37. Fischereder, M., B. Luckow, B. Hocher, R. P. Wuthrich, U. Rothenpieler, H. Schneeberger, U. Panzer, R. A. K. Stahl, I. A. Hauser, K. Budde, et al. 2001. CC chemokine receptor 5 and renal-transplant survival. Lancet 357: 1758-1761