Endogenous memory CD8 T cells are activated within cardiac allografts without mediating rejection

American Journal of Transplantation

Volumn 13, Issue 9, 2013, Pages 2293-2307

  Setoguchi, K ^a,b   Hattori, Y ^a,c   Iida, S ^a,b   Baldwin, W M ^a,d   Fairchild, R L ^a,d  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

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

Author keywords

Cardiac allograft; memory; T cell activation inactivation; T cell graft infiltration

Indexed keywords

GAMMA INTERFERON; MESSENGER RNA; ODULIMOMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC GRAFT REJECTION; CD8+ T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; GRAFT RECIPIENT; HEART TRANSPLANTATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; UPREGULATION;

CARDIAC ALLOGRAFT; MEMORY; T CELL ACTIVATION/INACTIVATION; T CELL GRAFT INFILTRATION;

ALLOGRAFTS; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; CD4-POSITIVE T-LYMPHOCYTES; CD40 LIGAND; CD8-POSITIVE T-LYMPHOCYTES; HEART TRANSPLANTATION; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; LYMPHOCYTE ACTIVATION; MICE; TRANSPLANTATION IMMUNOLOGY;

EID: 84883463377     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12372     Document Type: Article

References (52)

1. Augustine JJ, Siu DS, Clemente MJ, Schulak JA, Heeger PS, Hricik DE., Pre-transplant IFN-gamma ELISPOTs are associated with post-transplant renal function in African American renal transplant recipients. Am J Transplant 2005; 5: 1971-1975.
2. Cherkassky L, Lanning M, Lalli PN, et al. Evaluation of alloreactivity in kidney transplant recipients treated with antithymocyte globulin versus IL-2 receptor blockade. Am J Transplant 2011; 11: 1388-1396.
3. Heeger PS, Greenspan NS, Kuhlenschmidt S, et al. Pretransplant frequency of donor-specific, IFN-gamma-producing lymphcytes is a manifestation of immunologic memory and correlates with the risk of post-transplant rejection episodes. J Immunol 1999; 163: 2267-2275.
4. Poggio ED, Augustine JJ, Clemente M, et al. Pretransplant cellular alloimmunity as assessed by a panel of reactive T cells assay correlates with acute renal graft rejection. Transplantation 2007; 83: 847-852.
5. Krummey SM, Ford ML., Heterogeneity within T cell memory: Implications for transplant tolerance. Front Immunol 2012; 3: 1-15.
6. Valujskikh A, Lakkis FG., In remembrance of things past: Memory T cells and transplant rejection. Immunol Rev 2003; 196: 65-74.
7. Valujskikh A, Baldwin WM III, Fairchild RL., Recent progress and new perspectives in studying T cell responses to allografts. Am J Transplant 2010; 10: 1117-1125.
8. + T-cell cross-reactivity and heterologous immunity. Immunol Rev 2006; 211: 164-181.
9. Adams AB, Williams MR, Jones TR, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003; 111: 1887-1895.
10. Brehm MA, Markees TG, Daniels KA, Greiner DL, Rossini AA, Welsh RM., Direct visualization of cross-reactive effector and memory allo-specific CD8 T cells generated in response to viral infections. J Immunol 2003; 170: 4077-4086.
11. Kitchens WH, Haridas D, Wagener ME, Song M, Ford ML., Combined costimulatory and leukocyte functional antigen-1 blockade prevents transplant rejection mediated by heterologous memory alloresponses. Transplantation 2012; 93: 997-1005.
12. Welsh RM, markees TG, Woda BA, et al. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD154 antibody. J Virol 2000; 74: 2210-2218.
13. Nadazdin O, Boskovic S, Murakami T, et al. Phenotype, distribution and alloreactive properties of memory T cells from cynomolgus monkeys. Am J Transplant 2010; 10: 1375-1384.
14. Nadazdin O, Boskovic S, Murakami T, et al. Host alloreactive memory T cells influence tolerance to kidney allografts in nonhuman primates. Sci Transl Med 2011; 3: Online.
15. Schenk AD, Gorbacheva V, Rabant M, Fairchild RL, Valujskikh A., Effector functions of donor-reactive CD8 memory T cells are dependent on ICOS induced during division in cardiac grafts. Am J Transplant 2009; 9: 64-73.
16. Schenk AD, Nozaki T, Rabant M, Valujskikh A, Fairchild RL., Donor-reactive CD8 memory T cells infiltrate cardiac allografts within 24-h posttransplant in naive recipients. Am J Transplant 2008; 8: 1652-1661.
17. El-Sawy T, Miura M, Fairchild R., Early T cell response to allografts occurring prior to alloantigen priming up-regulates innate mediated inflammation and graft necrosis. Am J Pathol 2004; 165: 147-157.
18. Setoguchi K, Schenk AD, Ishii D, et al. LFA-1 antagonism inhibits early infiltration of endgenous memory CD8 T cells into cardiac allografts and donor-reactive T cell priming. Am J Transplant 2011; 11: 923-935.
19. Corry RJ, Winn HJ, Russell PS., Primarily vascularized allografts of hearts in mice. Transplantation 1973; 16: 343-350.
20. Afanasyeva M, Georgakopoulos D, Belardi DF, et al. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: Correlation with cardiac function. Am J Pathol 2004; 164: 807-815.
21. Mosser DM, Edwards JP., Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8: 958-969.
22. Adams AB, Pearson TC, Larsen CP., Heterologous immunity: An overlooked barrier to tolerance. Immunol Rev 2003; 196: 147-160.
23. Lakkis FG, Sayegh MH., Memory T cells: A hurdle to immunologic tolerance. J Am Soc Nephrol 2003; 14: 2402-2410.
24. Nikolich-Zugich J, Sifka MK, Messaoudi I., The many important facets of T-cell repertoire divesity. Nat Rev Immunol 2004; 4: 123-132.
25. Zheng Y, Zha Y, Driessens G, Locke F, Gajewski TF., Transcriptional regulator early growth response gene 2 (Egr2) is required for T cell anergy in vitro and in vivo. J Exp Med 2012; 209: 2157-2163.
26. + T cell exhaustion versus memory. Immunity 2012; 37: 1130-1144.
27. Crespo J, Sun H, Welling TH, Tian Z, Zou W., T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr Opin Immunol 2013; 25: 214-221.
28. Valujskikh A, Li XC., Memory T cells and their exhaustive differentiation in allograft tolerance and rejection. Curr Opin Organ Transplant 2012; 17: 15-19.
29. Belperio JA, Keane MP, Burdick MD, et al. CXCR2/CXCR2 ligand biology during lung transplant ischemia/reperfusion injury. J Immunol 2005; 175: 6931-6939.
30. De Greef KE, Ysebaert DK, Ghielli M, et al. Neutrophils and acute ischemia-reperfusion injury. J Nephrol 1998; 11: 110-122.
31. Hernandez LA, Grisham MB, Twohig B, Arfors KE, Harlan JM, Granger DN., The role of neutrophils in ischemia-reperfusion-induced microvascular injury. Am J Physiol 1987; 253: H699-H703.
32. Iwahori Y, Ishiguro N, Shimizu T, et al. Selective neutrophil depletion with monoclonal antibodies attenuates ischemia/reperfusion injury in skeletal muscle. J Reconstr Microsurg 1998; 14: 109-116.
33. Jaeschke H, Farhood A, Smith C., Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J 1990; 4: 3355-3364.
34. Kreisel D, Sugimoto S, Tietjens J, et al. Bcl3 prevents acute inflammtory lung injury in mice by restraining emergency granulopoiesis. J Clin Invest 2011; 121: 265-276.
35. Miura M, Fu X, Zhang Q-W, Remick DG, Fairchild RL., Neutralization of Groα and macrophage inflammatory protein-2 attenuates renal ischemia/reperfusion injury. Am J Pathol 2001; 159: 2137-2145.
36. Citro A, Cantarelli E, maffi P, et al. CXCR1/2 inhibition enhances pancreatic islet survival after transplantation. J Clin Invest 2012; 122: 3647-3651.
37. Denicola MM, Weigt SS, Belperio JA, Reed EF, Ross DJ, Wallace WD., Pathologic findings in lung allografts with anti-HLA antibodies. J Heart Lung Transplant 2013; 32: 326-332.
38. Devitt JJ, King CL, Lee TDG, Friesen CLH., Early innate immune events induced by prolonged cold ischemia exacerbate allograft vaasculopathy. J Cardiothorac Surg 2011; 6: 2-10.
39. El-Sawy T, Belperio JA, Strieter RM, Remick DG, Fairchild RL., Inhibition of polymorphonuclear leukocyte-mediated graft damage synergizes with short-term costimulatory blockade to prevent cardiac allograft rejection. Circulation 2005; 112: 320-331.
40. Healy DG, Watson RWG, O'Mahony U, Egan JJ, Wood AE., Neutrophil immunosurveillance for heart transplant rejection: A prospective study. Transplant Proc 2010; 42: 1788-1792.
41. Jaeger K, Rauschulte H, Heine J, et al. Neutrophil respiratory burst following liver transplantation: In vitro effects of granulocyte colony-stimulating factor. Transplant Intect Dis 1999; 1: 153-156.
42. Miura M, El-Sawy T, Fairchild RL., Neutrophils mediate parenchymal tissue necrosis and accelerate the rejection of complete major histocompatibility complex-disparate cardiac allografts in the absence of interferon-γ. Am J Pathol 2003; 162: 509-519.
43. Soo A, Maher B, McCarthy J, Nolke L, Wood A, Watson RWG., Pre-operative determination of an individual's neutrophil response: A potential predictor of early cardiac transplant cellular rejection. J Heart Lung Transplant 2009; 28: 1198-1205.
44. + myeloid cells infiltrate allografts and contribute to an imaging signature of organ rejection in mice. J Clin Invest 2010; 120: 2627-2634.
45. Biswas SK, Mantovani A., Macrophage plasicity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat Immunol 2010; 11: 889-896.
46. Mantovani A, Biswas SK, Faldiero MR, Sica A, Locati M., Macrophage plasticity and polarization in tissue repair and remodeling. J Pathol 2013; 229: 176-185.
47. Csencsits K, Wood SC, Lu G, et al. Transforming growth factor beta-induced connective tissue growth factor and chronic allograft rejection. Am J Transplant 2006; 6: 959-966.
48. Nathan MJ, Yin D, Eichwald EJ, Bishop DK., The immunobiology of inductive anti-CD40L therapy in transplantation: Allograft acceptance is not dependent upon the deletion of graft-reactive T cells. Am J Transplant 2002; 2: 323-332.
49. Piccotti JR, Li K, Cahn SY, Eichwald EJ, Bishop DK., Cytokine regulation of chronic cardiac allograft rejection: Evidence against a role for th1 in the disease process. Transplantation 1999; 67: 1548-1555.
50. Muller YD, Mai G, Morel P, et al. Anti-CD154 mAb and rapamycin induce T regulatory cell mediated tolerance in rat-to-mouse islet transplantation. PLoS ONE 2010; 5.
51. Rigby MR, Trexler AM, Pearson TC, Lasen CP., CD28/CD154 blockade prevents autoimmune dabetes by inducing nondeletional tolerance after effector T-cell inhibition and regulatory T-cell expansion. Diabetes 2008; 57: 2672-2683.
52. Yamazaki M, Pearson T, Brehm MA, et al. Different mechanisms control peripheral and central tolerance in hematopoietic chimeric mice. Am J Transplant 2007; 7: 1710-1721.