NK cells induce apoptosis in tubular epithelial cells and contribute to renal ischemia-reperfusion injury

Journal of Immunology

Volumn 181, Issue 11, 2009, Pages 7489-7498

  Zhang, Zhu Xu ^a,b,c   Wang, Shuang ^a,c   Huang, Xuyan ^a,c   Min, Wei Ping ^a,b,c   Sun, Hongtao ^a,c   Liu, Weihua ^a,c   Garcia, Bertha ^a,b,c   Jevnikar, Anthony M ^a,b,c  

^a LONDON HEALTH SCIENCES CENTRE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; FAS LIGAND; GAMMA INTERFERON; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; RAE PROTEIN; RAG2 PROTEIN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL KILLING; CELL LOSS; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY TUBULE EPITHELIUM; MALE; MOLECULAR MECHANICS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; T LYMPHOCYTE; WILD TYPE;

EID: 71849114521     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.11.7489     Document Type: Article

References (57)

1. Thadhani, R., M. Pascual, and J. V. Bonventre. 1996. Acute renal failure. N. Engl. J. Med. 334: 1448-1460.
2. Shoskes, D. A., and P. F. Halloran. 1996. Delayed graft function in renal transplantation: etiology, management, and long-term significance. J. Urol. 155:1831-1840. (Pubitemid 26144066)
3. Bonventre, J. V. 2003. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol. 14 (Suppl. 1): S55-S61. (Pubitemid 36687041)
4. Molitoris, B. A., and T. A. Sutton. 2004. Endothelial injury and dysfunction: role in the extension phase of acute renal failure. Kidney Int. 66: 496-499. (Pubitemid 38981985)
5. Boros, P., and J. S. Bromberg. 2006. New cellular and molecular immune pathways in ischemia/reperfusion injury. Am. J. Transplant. 6: 652-658. (Pubitemid 43345001)
6. Du, C., J. Jiang, Q. Guan, Z. Yin, M. Masterson, A. Parbtani, R. Zhong, and A. M. Jevnikar. 2004. Renal tubular epithelial cell self-injury through Fas/Fas ligand interaction promotes renal allograft injury. Am. J. Transplant. 4:1583-1594. (Pubitemid 39312292)
7. Du, C., S. Wang, H. Diao, Q. Guan, R. Zhong, and A. M. Jevnikar. 2006. Increasing resistance of tubular epithelial cells to apoptosis by shRNA therapy ameliorates renal ischemia-reperfusion injury. Am. J. Transplant. 6: 2256-2267. (Pubitemid 44359411)
8. Du, C., Q. Guan, Z. Yin, R. Zhong, and A. M. Jevnikar. 2005. IL-2-mediated apoptosis of kidney tubular epithelial cells is regulated by the caspase-8 inhibitor c-FLIP. Kidney Int. 67: 1397-1409. (Pubitemid 40463116)
9. Toledo-Pereyra, L. H., F. Lopez-Neblina, and A. H. Toledo. 2004. Reactive oxygen species and molecular biology of ischemia/reperfusion. Ann. Transplant. 9:81-83.
10. Millar, T. M., V. Phan, and L. A. Tibbles. 2007. ROS generation in endothelial hypoxia and reoxygenation stimulates MAP kinase signaling and kinase-dependent neutrophil recruitment. Free Radic. Biol. Med. 42: 1165-1177.
11. Cassie, S., M. F. Masterson, A. Polukoshko, M. M. Viskovic, and L. A. Tibbles. 2004. Ischemia/reperfusion induces the recruitment of leukocytes from whole blood under flow conditions. Free Radic. Biol. Med. 36: 1102-1111. (Pubitemid 38479864)
12. Bonventre, J. V., and A. Zuk. 2004. Ischemic acute renal failure: an inflammatory disease? Kidney Int. 66: 480-485. (Pubitemid 38981982)
13. Ysebaert, D. K., K. E. De Greef, S. R. Vercauteren, M. Ghielli, G. A. Verpooten, E. J. Eyskens, and M. E. De Broe. 2000. Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol. Dial. Transplant. 15:1562-1574.
14. De Greef, K. E., D. K. Ysebaert, M. Ghielli, S. Vercauteren, E. J. Nouwen, E. J. Eyskens, and M. E. De Broe. 1998. Neutrophils and acute ischemia-reperfusion injury. J. Nephrol. 11: 110-122.
15. Dragun, D., U. Hoff, J. K. Park, Y. Qun, W. Schneider, F. C. Luft, and H. Haller. 2000. Ischemia-reperfusion injury in renal transplantation is independent of the immunologic background. Kidney Int. 58: 2166-2177. (Pubitemid 30807946)
16. + T cell as a major pathogenic factor in ischemic acute renal failure. J. Clin. Invest. 108: 1283-1290.
17. De Greef, K. E., D. K. Ysebaert, S. Dauwe, V. Persy, S. R. Vercauteren, D. Mey, and M. E. De Broe. 2001. Anti-B7-1 blocks mononuclear cell adherence in vasa recta after ischemia. Kidney Int. 60: 1415-1427.
18. + T cells and IFN-γ. J. Immunol. 176: 3108-3114.
19. Ascon, D. B., S. Lopez-Briones, M. Liu, M. Ascon, V. Savransky, R. B. Colvin, M. J. Soloski, and H. Rabb. 2006. Phenotypic and functional characterization of kidney-infiltrating lymphocytes in renal ischemia reperfusion injury. J. Immunol. 177: 3380-3387.
20. Ysebaert, D. K., K. E. De Greef, S. R. Vercauteren, A. Verhulst, M. Kockx, G. A. Verpooten, and M. E. De Broe. 2003. Effect of immunosuppression on damage, leukocyte infiltration, and regeneration after severe warm ischemia/ reperfusion renal injury. Kidney Int. 64: 864-873.
21. Rabb, H., F. Daniels, M. O'Donnell, M. Haq, S. R. Saba, W. Keane, and W. W. Tang. 2000. Pathophysiological role of T lymphocytes in renal ischemiareperfusion injury in mice. Am. J. Physiol. 279: F525-F531.
22. Takada, M., A. Chandraker, K. C. Nadeau, M. H. Sayegh, and N. L. Tilney. 1997. The role of the B7 costimulatory pathway in experimental cold ischemia/reperfusion injury. J. Clin. Invest. 100: 1199-1203. (Pubitemid 27386305)
23. Azuma, H., K. Nadeau, M. Takada, H. S. Mackenzie, and N. L. Tilney. 1997. Cellular and molecular predictors of chronic renal dysfunction after initial ischemia/ reperfusion injury of a single kidney. Transplantation 64: 190-197. (Pubitemid 27332657)
24. Takada, M., K. C. Nadeau, G. D. Shaw, K. A. Marquette, and N. L. Tilney. 1997. The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J. Clin. Invest. 99: 2682-2690. (Pubitemid 27259815)
25. Yokota, N., F. Daniels, J. Crosson, and H. Rabb. 2002. Protective effect of T cell depletion in murine renal ischemia-reperfusion injury. Transplantation 74:759-763.
26. Friedewald, J. J., and H. Rabb. 2004. Inflammatory cells in ischemic acute renal failure. Kidney Int. 66: 486-491. (Pubitemid 38981983)
27. Lai, L. W., K. C. Yong, S. Igarashi, and Y. H. Lien. 2007. A sphingosine-1-phosphate type 1 receptor agonist inhibits the early T-cell transient following renal ischemia-reperfusion injury. Kidney Int. 71: 1223-1231.
28. Dong, X., S. Swaminathan, L. A. Bachman, A. J. Croatt, K. A. Nath, and M. D. Griffin. 2007. Resident dendritic cells are the predominant TNF-secreting cell in early renal ischemia-reperfusion injury. Kidney Int. 71: 619-628. (Pubitemid 46494569)
29. Li, L., L. Huang, S. S. Sung, P. I. Lobo, M. G. Brown, R. K. Gregg, V. H. Engelhard, and M. D. Okusa. 2007. NKT cell activation mediates neutrophil IFN-γ production and renal ischemia-reperfusion injury. J. Immunol. 178:5899-5911. (Pubitemid 46674387)
30. Burne-Taney, M. J., D. B. Ascon, F. Daniels, L. Racusen, W. Baldwin, and H. Rabb. 2003. B cell deficiency confers protection from renal ischemia reperfusion injury. J. Immunol. 171: 3210-3215. (Pubitemid 37093547)
31. Park, P., M. Haas, P. N. Cunningham, L. Bao, J. J. Alexander, and R. J. Quigg. 2002. Injury in renal ischemia-reperfusion is independent from immunoglobulins and T lymphocytes. Am. J. Physiol. 282: F352-F357. (Pubitemid 34654567)
32. Burne-Taney, M. J., N. Yokota-Ikeda, and H. Rabb. 2005. Effects of combined T- and B-cell deficiency on murine ischemia reperfusion injury. Am. J. Transplant.5: 1186-1193. (Pubitemid 40839406)
33. Feng, L., F. Cheng, Z. Ye, S. Li, Y. He, X. Yao, Q. Tang, and Y. Li. 2006. The effect of renal ischemia-reperfusion injury on expression of RAE-1 and H60 in mice kidney. Transplant. Proc. 38: 2195-2198.
34. Hoglund, P., J. Sundback, M. Y. Olsson-Alheim, M. Johansson, M. Salcedo, C. Ohlen, H. G. Ljunggren, C. L. Sentman, and K. Karre. 1997. Host MHC class I gene control of NK-cell specificity in the mouse. Immunol. Rev. 155: 11-28. (Pubitemid 27076055)
35. Kane, K. P., K. J. Lavender, and B. J. Ma. 2004. Ly-49 receptors and their functions. Crit. Rev. Immunol. 24: 321-348.
36. Brooks, A. G., P. E. Posch, C. J. Scorzelli, F. Borrego, and J. E. Coligan. 1997. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 185: 795-800.
37. b. J. Exp. Med. 188:1841-1848.
38. Snyder, M. R., C. M. Weyand, and J. J. Goronzy. 2004. The double life of NK receptors: stimulation or co-stimulation? Trends Immunol. 25: 25-32.
39. Raziuddin, A., D. L. Longo, M. Bennett, R. Winkler-Pickett, J. R. Ortaldo, and W. J. Murphy. 2002. Increased bone marrow allograft rejection by depletion of NK cells expressing inhibitory Ly49 NK receptors for donor class I antigens. Blood 100: 3026-3033.
40. Matzinger, P. 1991. The JAM test: a simple assay for DNA fragmentation and cell death. J. Immunol. Methods 145: 185-192.
41. Hoves, S., S. W. Krause, J. Scholmerich, and M. Fleck. 2003. The JAM-assay: optimized conditions to determine death-receptor-mediated apoptosis. Methods31: 127-134. (Pubitemid 37075897)
42. Ayres, F. M., M. Narita, M. Takahashi, L. Alldawi, A. Liu, Y. Osman, T. Abe, T. Yano, M. Sakaue, K. Toba, et al. 2003. A comparative study of the JAM test and 51Cr-release assay to assess the cytotoxicity of dendritic cells on hematopoietic tumor cells. Immunol. Invest. 32: 219-227.
43. Prlic, M., B. R. Blazar, M. A. Farrar, and S. C. Jameson. 2003. In vivo survival and homeostatic proliferation of natural killer cells. J. Exp. Med. 197: 967-976. (Pubitemid 36523194)
44. Pagtalunan, M. E., J. L. Olson, N. L. Tilney, and T. W. Meyer. 1999. Late consequences of acute ischemic injury to a solitary kidney. J. Am. Soc. Nephrol. 10: 366-373.
45. Nogae, S., M. Miyazaki, N. Kobayashi, T. Saito, K. Abe, H. Saito, P. K. Nakane, Y. Nakanishi, and T. Koji. 1998. Induction of apoptosis in ischemia-reperfusion model of mouse kidney: possible involvement of Fas. J. Am. Soc. Nephrol. 9:620-631. (Pubitemid 28186051)
46. Daemen, M. A., M. W. van de Ven, E. Heineman, and W. A. Buurman. 1999. Involvement of endogenous interleukin-10 and tumor necrosis factor-α in renal ischemia-reperfusion injury. Transplantation 67: 792-800.
47. Donnahoo, K. K., B. D. Shames, A. H. Harken, and D. R. Meldrum. 1999. Review article: the role of tumor necrosis factor in renal ischemia-reperfusion injury. J. Urol. 162: 196-203. (Pubitemid 29420927)
48. Zhang, X., X. Zheng, H. Sun, B. Feng, G. Chen, C. Vladau, M. Li, D. Chen, M. Suzuki, L. Min, et al. 2006. Prevention of renal ischemic injury by silencing the expression of renal caspase 3 and caspase 8. Transplantation 82: 1728-1732. (Pubitemid 46035659)
49. Zheng, X., X. Zhang, H. Sun, B. Feng, M. Li, G. Chen, C. Vladau, D. Chen, M. Suzuki, L. Min, et al. 2006. Protection of renal ischemia injury using combination gene silencing of complement 3 and caspase 3 genes. Transplantation 82: 1781-1786. (Pubitemid 46035667)
50. de Vries, B., J. Kohl, W. K. Leclercq, T. G. Wolfs, A. A. van Bijnen, P. Heeringa, and W. A. Buurman. 2003. Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils. J. Immunol. 170: 3883-3889.
51. Puri, T. S., and R. J. Quigg. 2007. The many effects of complement C3- and C5-binding proteins in renal injury. Semin. Nephrol. 27: 321-337.
52. Du, C., Q. Guan, H. Diao, Z. Yin, and A. M. Jevnikar. 2006. Nitric oxide induces apoptosis in renal tubular epithelial cells through activation of caspase-8. Am. J. Physiol. 290: F1044-F1054. (Pubitemid 43724903)
53. Glynne, P. A., and T. J. Evans. 1999. Inflammatory cytokines induce apoptotic and necrotic cell shedding from human proximal tubular epithelial cell monolayers. Kidney Int. 55: 2573-2597.
54. Bottinger, E. P. 2007. TGF-β in renal injury and disease. Semin. Nephrol. 27:309-320.
55. Lodoen, M. B., and L. L. Lanier. 2006. Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 18: 391-398. (Pubitemid 43947576)
56. Zingoni, A., T. Sornasse, B. G. Cocks, Y. Tanaka, A. Santoni, and L. L. Lanier.2005. NK cell regulation of T cell-mediated responses. Mol. Immunol. 42:451-454.
57. Vujanovic, N. L. 2001. Role of TNF family ligands in antitumor activity of natural killer cells. Int. Rev. Immunol. 20: 415-437.