Osteopontin expressed in tubular epithelial cells regulates NK cell-mediated kidney ischemia reperfusion injury

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 967-973

  Zhang, Zhu Xu ^a,b   Shek, Kelvin ^a   Wang, Shuang ^a,b   Huang, Xuyan ^a   Lau, Arthur ^a   Yin, Ziqin ^a,b   Sun, Hongtao ^a,b   Liu, Weihua ^a,b   Garcia, Bertha ^a,b   Rittling, Susan ^c   Jevnikar, Anthony M ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c FORSYTH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 7; MESSENGER RNA; OSTEOPONTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL MIGRATION; KIDNEY EPITHELIUM; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL PROTECTION; REPERFUSION INJURY; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL MOTION; CYTOLOGY; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; KIDNEY; KIDNEY TUBULE; MALE; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULARIZATION;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY TUBULES; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; OSTEOPONTIN; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77955493511     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903245     Document Type: Article

References (53)

1. 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.
2. Thadhani, R., M. Pascual, and J. V. Bonventre. 1996. Acute renal failure. N. Engl. J. Med. 334: 1448-1460.
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.
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.
5. Boros, P., and J. S. Bromberg. 2006. New cellular and molecular immune pathways in ischemia/reperfusion injury. Am. J. Transplant. 6: 652-658.
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.
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.
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.
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 kinasedependent neutrophil recruitment. Free Radic. Biol. Med. 42: 1165-1177.
11. Burne, M. J., F. Daniels, A. El Ghandour, S. Mauiyyedi, R. B. Colvin, M. P. O'Donnell, and H. Rabb. 2001. Identification of the CD4(+) T cell as a major pathogenic factor in ischemic acute renal failure. J. Clin. Invest. 108: 1283-1290.
12. 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.
13. Day, Y. J., L. Huang, H. Ye, L. Li, J. Linden, and M. D. Okusa. 2006. Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: the role of CD4+ T cells and IFN-gamma. J. Immunol. 176: 3108-3114.
14. 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.
15. 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.
16. 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 ischemia-reperfusion injury in mice. Am. J. Physiol. Renal Physiol. 279: F525-F531.
17. Friedewald, J. J., and H. Rabb. 2004. Inflammatory cells in ischemic acute renal failure. Kidney Int. 66: 486-491. (Pubitemid 38981983)
18. 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.
19. 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.
20. 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-gamma production and renal ischemia-reperfusion injury. J. Immunol. 178: 5899-5911.
21. 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)
22. 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. Renal Physiol. 282: F352-F357.
23. Burne-Taney, M. J., N. Yokota-Ikeda, and H. Rabb. 2005. Effects of combined Tand B-cell deficiency on murine ischemia reperfusion injury. Am. J. Transplant. 5: 1186-1193.
24. Zhang, Z. X., S. Wang, X. Huang, W. P. Min, H. Sun, W. Liu, B. Garcia, and A. M. Jevnikar. 2008. NK cells induce apoptosis in tubular epithelial cells and contribute to renal ischemia-reperfusion injury. J. Immunol. 181: 7489-7498.
25. Patarca, R., G. J. Freeman, R. P. Singh, F. Y. Wei, T. Durfee, F. Blattner, D. C. Regnier, C. A. Kozak, B. A. Mock, H. C. Morse, III, et al. 1989. Structural and functional studies of the early T lymphocyte activation 1 (Eta-1) gene. Definition of a novel T cell-dependent response associated with genetic resistance to bacterial infection. J. Exp. Med. 170: 145-161.
26. Pollack, S. B., P. A. Linnemeyer, and S. Gill. 1994. Induction of osteopontinmRNA expression during activation of murine NK cells. J. Leukoc. Biol. 55: 398-400.
27. O'Regan, A. W., J. M. Hayden, and J. S. Berman. 2000. Osteopontin augments CD3-mediated interferon-gamma and CD40 ligand expression by T cells, which results in IL-12 production from peripheral blood mononuclear cells. J. Leukoc. Biol. 68: 495-502.
28. Ashkar, S., G. F. Weber, V. Panoutsakopoulou, M. E. Sanchirico, M. Jansson, S. Zawaideh, S. R. Rittling, D. T. Denhardt, M. J. Glimcher, and H. Cantor. 2000. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287: 860-864. (Pubitemid 30084330)
29. O'Regan, A. W., G. J. Nau, G. L. Chupp, and J. S. Berman. 2000. Osteopontin (Eta-1) in cell-mediated immunity: teaching an old dog new tricks. Immunol. Today 21: 475-478.
30. Chabas, D., S. E. Baranzini, D. Mitchell, C. C. Bernard, S. R. Rittling, D. T. Denhardt, R. A. Sobel, C. Lock, M. Karpuj, R. Pedotti, et al. 2001. The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294: 1731-1735.
31. Jansson, M., V. Panoutsakopoulou, J. Baker, L. Klein, and H. Cantor. 2002. Cutting edge: Attenuated experimental autoimmune encephalomyelitis in eta-1/osteopontin-deficient mice. J. Immunol. 168: 2096-2099. (Pubitemid 34171807)
32. Xie, Y., M. Sakatsume, S. Nishi, I. Narita, M. Arakawa, and F. Gejyo. 2001. Expression, roles, receptors, and regulation of osteopontin in the kidney. Kidney Int. 60: 1645-1657. (Pubitemid 32999968)
33. Persy, V. P., A. Verhulst, D. K. Ysebaert, K. E. De Greef, and M. E. De Broe. 2003. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int. 63: 543-553.
34. Noiri, E., K. Dickman, F. Miller, G. Romanov, V. I. Romanov, R. Shaw, A. F. Chambers, S. R. Rittling, D. T. Denhardt, and M. S. Goligorsky. 1999. Reduced tolerance to acute renal ischemia in mice with a targeted disruption of the osteopontin gene. Kidney Int. 56: 74-82.
35. Rittling, S. R., H. N. Matsumoto, M. D. McKee, A. Nanci, X. R. An, K. E. Novick, A. J. Kowalski, M. Noda, and D. T. Denhardt. 1998. Mice lacking osteopontin show normal development and bone structure but display altered osteoclast formation in vitro. J. Bone Miner. Res. 13: 1101-1111.
36. Jang, H. R., and H. Rabb. 2009. The innate immune response in ischemic acute kidney injury. Clin. Immunol. 130: 41-50.
37. Giachelli, C. M., R. Pichler, D. Lombardi, D. T. Denhardt, C. E. Alpers, S. M. Schwartz, and R. J. Johnson. 1994. Osteopontin expression in angiotensin II-induced tubulointerstitial nephritis. Kidney Int. 45: 515-524.
38. Wüthrich, R. P., X. Fan, T. Ritthaler, V. Sibalic, D. J. Yu, J. Loffing, and B. Kaissling. 1998. Enhanced osteopontin expression and macrophage in- filtration in MRL-Fas(lpr) mice with lupus nephritis. Autoimmunity 28: 139-150.
39. Ophascharoensuk, V., C. M. Giachelli, K. Gordon, J. Hughes, R. Pichler, P. Brown, L. Liaw, R. Schmidt, S. J. Shankland, C. E. Alpers, et al. 1999. Obstructive uropathy in the mouse: role of osteopontin in interstitial fibrosis and apoptosis. Kidney Int. 56: 571-580. (Pubitemid 29353155)
40. Yu, X. Q., L. L. Wu, X. R. Huang, N. Yang, R. E. Gilbert, M. E. Cooper, R. J. Johnson, K. N. Lai, and H. Y. Lan. 2000. Osteopontin expression in progressive renal injury in remnant kidney: role of angiotensin II. Kidney Int. 58: 1469-1480.
41. Yu, X. Q., J. M. Fan, D. J. Nikolic-Paterson, N. Yang, W. Mu, R. Pichler, R. J. Johnson, R. C. Atkins, and H. Y. Lan. 1999. IL-1 up-regulates osteopontin expression in experimental crescentic glomerulonephritis in the rat. Am. J. Pathol. 154: 833-841.
42. Kiefer, F. W., M. Zeyda, J. Todoric, J. Huber, R. Geyeregger, T. Weichhart, O. Aszmann, B. Ludvik, G. R. Silberhumer, G. Prager, and T. M. Stulnig. 2008. Osteopontin expression in human and murine obesity: extensive local upregulation in adipose tissue but minimal systemic alterations. Endocrinology 149: 1350-1357.
43. Diao, H., S. Kon, K. Iwabuchi, C. Kimura, J. Morimoto, D. Ito, T. Segawa, M. Maeda, J. Hamuro, T. Nakayama, et al. 2004. Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 21: 539-550.
44. Koh, A., A. P. da Silva, A. K. Bansal, M. Bansal, C. Sun, H. Lee, M. Glogauer, J. Sodek, and R. Zohar. 2007. Role of osteopontin in neutrophil function. Immunology 122: 466-475.
45. Banerjee, A., U. M. Apte, R. Smith, and S. K. Ramaiah. 2006. Higher neutrophil infiltration mediated by osteopontin is a likely contributing factor to the increased susceptibility of females to alcoholic liver disease. J. Pathol. 208: 473-485.
46. Chung, J. W., M. S. Kim, Z. H. Piao, M. Jeong, S. R. Yoon, N. Shin, S. Y. Kim, E. S. Hwang, Y. Yang, Y. H. Lee, et al. 2008. Osteopontin promotes the development of natural killer cells from hematopoietic stem cells. Stem Cells 26: 2114-2123.
47. Padanilam, B. J., D. R. Martin, and M. R. Hammerman. 1996. Insulin-like growth factor I-enhanced renal expression of osteopontin after acute ischemic injury in rats. Endocrinology 137: 2133-2140.
48. Kleinman, J. G., E. M. Worcester, A. M. Beshensky, A. M. Sheridan, J. V. Bonventre, and D. Brown. 1995. Upregulation of osteopontin expression by ischemia in rat kidney. Ann. N. Y. Acad. Sci. 760: 321-323.
49. Persy, V. P., W. A. Verstrepen, D. K. Ysebaert, K. E. De Greef, and M. E. De Broe. 1999. Differences in osteopontin up-regulation between proximal and distal tubules after renal ischemia/reperfusion. Kidney Int. 56: 601-611.
50. Hwang, S. M., P. D. Wilson, J. D. Laskin, and D. T. Denhardt. 1994. Age and development-related changes in osteopontin and nitric oxide synthase mRNA levels in human kidney proximal tubule epithelial cells: contrasting responses to hypoxia and reoxygenation. J. Cell. Physiol. 160: 61-68.
51. Scatena, M., M. Almeida, M. L. Chaisson, N. Fausto, R. F. Nicosia, and C. M. Giachelli. 1998. NF-kappaB mediates alphavbeta3 integrin-induced endothelial cell survival. J. Cell Biol. 141: 1083-1093.
52. Lewington, A. J., B. J. Padanilam, D. R. Martin, and M. R. Hammerman. 2000. Expression of CD44 in kidney after acute ischemic injury in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278: R247-R254.
53. Burne, M. J., M. Haq, H. Matsuse, S. Mohapatra, and H. Rabb. 2000. Genetic susceptibility to renal ischemia reperfusion injury revealed in a murine model. Transplantation 69: 1023-1025.