A novel pathway of chronic allograft rejection mediated by NK cells and alloantibody

American Journal of Transplantation

Volumn 12, Issue 2, 2012, Pages 313-321

  Hirohashi, T ^a   Chase, C M ^a   Della Pelle, P ^a   Sebastian, D ^a   Alessandrini, A ^a   Madsen, J C ^a   Russell, P S ^a   Colvin, R B ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Antibody mediated rejection; chronic allograft vasculopathy; Fc receptors; heart transplantation; NK cells

Indexed keywords

ALLOANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC ALLOGRAFT VASCULOPATHY; CELL SELECTION; CHRONIC GRAFT REJECTION; ENDOTHELIUM CELL; HEART TRANSPLANTATION; IN VIVO STUDY; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNITY, CELLULAR; IMMUNOHISTOCHEMISTRY; ISOANTIBODIES; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; TRANSPLANTATION, HOMOLOGOUS;

EID: 84856431851     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2011.03836.x     Document Type: Article

References (42)

1. Mehra MR,. Contemporary concepts in prevention and treatment of cardiac allograft vasculopathy. Am J Transplant 2006; 6: 1248-1256. (Pubitemid 44030306)
2. Taylor DO, Edwards LB, Boucek MM, et al,. Registry of the International Society for Heart and Lung Transplantation: Twenty-third official adult heart transplantation report-2006. J Heart Lung Transplant 2006; 25: 869-879. (Pubitemid 44143013)
3. Uehara S, Chase CM, Colvin RB, Madsen JC, Russell PS,. T-cell depletion eliminates the development of cardiac allograft vasculopathy in mice rendered tolerant by the induction of mixed chimerism. Transplant Proc 2006; 38: 3169-3171. (Pubitemid 44908523)
4. Uehara S, Chase CM, Cornell LD, Madsen JC, Russell PS, Colvin RB,. Chronic cardiac transplant arteriopathy in mice: Relationship of alloantibody, C4d deposition and neointimal fibrosis. Am J Transplant 2007; 7: 57-65. (Pubitemid 44952856)
5. Graham JA, Wilkinson RA, Hirohashi T, et al,. Viral infection induces de novo lesions of coronary allograft vasculopathy through a natural killer cell-dependent pathway. Am J Transplant 2009; 9: 2479-2484.
6. Uehara S, Chase CM, Kitchens WH, et al,. NK cells can trigger allograft vasculopathy: The role of hybrid resistance in solid organ allografts. J Immunol 2005; 175: 3424-3430. (Pubitemid 41170566)
7. Hirohashi T, Uehara S, Chase CM, et al,. Complement independent antibody-mediated endarteritis and transplant arteriopathy in mice. Am J Transplant 2010; 10: 510-517.
8. Russell PS, Chase CM, Winn HJ, Colvin RB,. Coronary atherosclerosis in transplanted mouse hearts. II. Importance of humoral immunity. J Immunol 1994; 152: 5135-5141. (Pubitemid 24139110)
9. Galvani S, Auge N, Calise D, et al,. HLA class I antibodies provoke graft arteriosclerosis in human arteries transplanted into SCID/beige mice. Am J Transplant 2009; 9: 2607-2614.
10. Rahimi S, Qian Z, Layton J, Fox-Talbot K, Baldwin WM III, Wasowska BA,. Non-complement- and complement-activating antibodies synergize to cause rejection of cardiac allografts. Am J Transplant 2004; 4: 326-334. (Pubitemid 38282287)
11. Wang H, Jiang J, Liu W, et al,. Prevention of acute vascular rejection by a functionally blocking anti-C5 monoclonal antibody combined with cyclosporine. Transplantation 2005; 79: 1121-1127. (Pubitemid 40664008)
12. Yin D, Zeng H, Ma L, et al,. Cutting Edge: NK cells mediate IgG1-dependent hyperacute rejection of xenografts. J Immunol 2004; 172: 7235-7238. (Pubitemid 38747581)
13. Lee CY, Lotfi-Emran S, Erdinc M, et al,. The involvement of FcR mechanisms in antibody-mediated rejection. Transplantation 2007; 84: 1324-1334. (Pubitemid 351339321)
14. Trotta R, Col JD, Yu J, et al,. TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J Immunol 2008; 181: 3784-3792.
15. Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, Carson WE III,. Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 2006; 177: 120-129. (Pubitemid 43939123)
16. Bian H, Harris PE, Reed EF,. Ligation of HLA class I molecules on smooth muscle cells with anti-HLA antibodies induces tyrosine phosphorylation, fibroblast growth factor receptor expression and cell proliferation. Int Immunol 1998; 10: 1315-1323. (Pubitemid 28414337)
17. Bian H, Reed EF,. Alloantibody-mediated class I signal transduction in endothelial cells and smooth muscle cells: Enhancement by IFN-gamma and TNF-alpha. J Immunol 1999; 163: 1010-1018. (Pubitemid 29328114)
18. Jin YP, Fishbein MC, Said JW, et al,. Anti-HLA class I antibody-mediated activation of the PI3K/Akt signaling pathway and induction of Bcl-2 and Bcl-xL expression in endothelial cells. Hum Immunol 2004; 65: 291-302. (Pubitemid 38543064)
19. Jin YP, Jindra PT, Gong KW, Lepin EJ, Reed EF,. Anti-HLA class I antibodies activate endothelial cells and promote chronic rejection. Transplantation 2005; 79: S19-S21. (Pubitemid 40293567)
20. Jin YP, Singh RP, Du ZY, Rajasekaran AK, Rozengurt E, Reed EF,. Ligation of HLA class I molecules on endothelial cells induces phosphorylation of Src, paxillin, and focal adhesion kinase in an actin-dependent manner. J Immunol 2002; 168: 5415-5423. (Pubitemid 34556118)
21. Narayanan K, Jaramillo A, Phelan DL, Mohanakumar T,. Pre-exposure to sub-saturating concentrations of HLA class I antibodies confers resistance to endothelial cells against antibody complement-mediated lysis by regulating Bad through the phosphatidylinositol 3-kinase/Akt pathway. Eur J Immunol 2004; 34: 2303-2312. (Pubitemid 39256112)
22. Corry RJ, Winn HJ, Russell PS,. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 1973; 16: 343-350.
23. Russell PS, Chase CM, Sykes M, Ito H, Shaffer J, Colvin RB,. Tolerance, mixed chimerism, and chronic transplant arteriopathy. J Immunol 2001; 167: 5731-5740. (Pubitemid 33062764)
24. Armstrong AT, Strauch AR, Starling RC, Sedmak DD, Orosz CG,. Morphometric analysis of neointimal formation in murine cardiac allografts. Transplantation 1997; 63: 941-947. (Pubitemid 27173014)
25. Arase N, Arase H, Hirano S, Yokosuka T, Sakurai D, Saito T,. IgE-mediated activation of NK cells through FcgRIII. J Immunol 2003; 170: 3054-3058. (Pubitemid 36302180)
26. Arase N, Arase H, Park SY, Ohno H, Ra C, Saito T,. Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1 +T cells. J Exp Med 1997; 186: 1957-1963. (Pubitemid 28013679)
27. Vosshenrich CA, Ranson T, Samson SI, et al,. Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J Immunol 2005; 174: 1213-1221.
28. Colvin RB,. Antibody-mediated renal allograft rejection: Diagnosis and pathogenesis. J Am Soc Nephrol 2007; 18: 1046-1056. (Pubitemid 46536891)
29. Sis B, Halloran PF,. Endothelial transcripts uncover a previously unknown phenotype: C4d-negative antibody-mediated rejection. Curr Opin Organ Transplant 2010; 15: 42-48.
30. Chen D, Weber M, Lechler R, Dorling A,. NK-cell-dependent acute xenograft rejection in the mouse heart-to-rat model. Xenotransplantation 2006; 13: 408-414. (Pubitemid 44265709)
31. Zhang X, Reed EF,. Effect of antibodies on endothelium. Am J Transplant 2009; 9: 2459-2465.
32. Harris PE, Bian H, Reed EF,. Induction of high affinity fibroblast growth factor receptor expression and proliferation in human endothelial cells by anti-HLA antibodies: A possible mechanism for transplant atherosclerosis. J Immunol 1997; 159: 5697-5704. (Pubitemid 127470101)
33. Jindra PT, Jin YP, Jacamo R, Rozengurt E, Reed EF,. MHC class I and integrin ligation induce ERK activation via an mTORC2-dependent pathway. Biochem Biophys Res Commun 2008; 369: 781-787.
34. Chadee DN, Kyriakis JM,. MLK3 is required for mitogen activation of B-Raf, ERK and cell proliferation. Nat Cell Biol 2004; 6: 770-776. (Pubitemid 39144483)
35. Zhou Q, Heinke J, Vargas A, et al,. ERK signaling is a central regulator for BMP-4 dependent capillary sprouting. Cardiovasc Res 2007; 76: 390-399. (Pubitemid 350007461)
36. Andreucci M, Michael A, Kramers C, et al,. Renal ischemia/reperfusion and ATP depletion/repletion in LLC-PK(1) cells result in phosphorylation of FKHR and FKHRL1. Kidney Int 2003; 64: 1189-1198. (Pubitemid 37153783)
37. Jindra PT, Hsueh A, Hong L, et al,. Anti-MHC class I antibody activation of proliferation and survival signaling in murine cardiac allografts. J Immunol 2008; 180: 2214-2224.
38. Reyes-Vargas E, Pavlov IY, Martins TB, Schwartz JJ, Hill HR, Delgado JC,. Binding of anti-HLA class I antibody to endothelial cells produce an inflammatory cytokine secretory pattern. J Clin Lab Anal 2009; 23: 157-160.
39. Gill RG,. NK cells: Elusive participants in transplantation immunity and tolerance. Curr Opin Immunol 2010; 22: 649-654.
40. Beilke JN, Gill RG,. Frontiers in nephrology: The varied faces of natural killer cells in transplantation-contributions to both allograft immunity and tolerance. J Am Soc Nephrol 2007; 18: 2262-2267. (Pubitemid 47208109)
41. Hidalgo LG, Sis B, Sellares J, et al,. NK cell transcripts and NK cells in kidney biopsies from patients with donor-specific antibodies: Evidence for NK cell involvement in antibody-mediated rejection. Am J Transplant 2010; 10: 1812-1822.
42. Fildes JE, Yonan N, Tunstall K, et al,. Natural killer cells in peripheral blood and lung tissue are associated with chronic rejection after lung transplantation. J Heart Lung Transplant 2008; 27: 203-207. (Pubitemid 351221052)