JAK2/Y343/STAT5 signaling axis is required for erythropoietin-mediated protection against ischemic injury in primary renal tubular epithelial cells

American Journal of Physiology - Renal Physiology

Volumn 295, Issue 6, 2008, Pages

  Breggia, A C ^a   Wojchowski, D M ^a   Himmelfarb, J ^b  

^a Maine Medical Center Research Institute   (United States)

^b MAINE MEDICAL CENTER   (United States)

Author keywords

Hypoxia; Ischemic preconditioning

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; JANUS KINASE 2; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; EPITHELIUM CELL; IN VITRO STUDY; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY TUBULE EPITHELIUM; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RENAL PROTECTION; SIGNAL TRANSDUCTION;

EID: 57349143796     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90333.2008     Document Type: Article

References (38)

1. Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int J Biochem Cell Biol 37: 726-730, 2005.
2. Bernhardt WM, Campean V, Kany S, Jurgensen JS, Weidemann A, Warnecke C, Arend M, Klaus S, Gunzler V, Amann K, Willam C, Wiesener MS, Eckardt KU. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 17: 1970-1978, 2006.
3. Bonegio R, Lieberthal W. Role of apoptosis in the pathogenesis of acute renal failure. Curr Opin Nephrol Hypertens 11: 301-308, 2002.
4. Bonventre JV. Kidney ischemic preconditioning. Curr Opin Nephrol Hypertens 11: 43-48, 2002.
5. Breggia AC, Himmelfard J. Primary mouse renal tubular epithelial cells have variable injury tolerance to ishemic and chemical mediators of oxidative stress. Oxidative Med Cell Longevity 1: 1-6, 2008.
6. Cai Z, Manalo DJ, Wei G, Rodriguez ER, Fox-Talbot K, Lu H, Zweier JL, Semenza GL. Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation 108: 79-85, 2003.
7. Cai Z, Semenza GL. Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/reperfusion injury. Circulation 109: 2050-2053, 2004.
8. Chong ZZ, Kang JQ, Maiese K. Apaf-1, Bcl-xL, cytochrome c, and caspase-9 form the critical elements for cerebral vascular protection by erythropoietin. J Cereb Blood Flow Metab 23: 320-330, 2003.
9. Dagher PC. Apoptosis in ischemic renal injury: roles of GTP depletion and p53. Kidney Int 66: 506-509, 2004.
10. Digicaylioglu M, Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412: 641-647, 2001.
11. Hattori R, Maulik N, Otani H, Zhu L, Cordis G, Engelman RM, Siddiqui MA, Das DK. Role of STAT3 in ischemic preconditioning. J Mol Cell Cardiol 33: 1929-1936, 2001.
12. Johnson DW, Pat B, Vesey DA, Guan Z, Endre Z, Gobe GC. Delayed administration of darbepoetin or erythropoietin protects against ischemic acute renal injury and failure. Kidney Int 69: 1806-1813, 2006.
13. Junk AK, Mammis A, Savitz SI, Singh M, Roth S, Malhotra S, Rosenbaum PS, Cerami A, Brines M, Rosenbaum DM. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci USA 99: 10659-10664, 2002.
14. Kaushal GP, Basnakian AG, Shah SV. Apoptotic pathways in ischemic acute renal failure. Kidney Int 66: 500-506, 2004.
15. Kirken RA, Erwin-Cohen R, Behbod F, Wang M, Stepkowski SM, Kahan BD. Tyrphostin AG490 selectively inhibits activation of the JAK3/STAT5/MAPK pathway and rejection of rat heart allografts. Transplant Proc 33: 95, 2001.
16. Kirken RA, Erwin RA, Taub D, Murphy WJ, Behbod F, Wang L, Pericle F, Farrar WL. Tyrphostin AG-490 inhibits cytokine-mediated JAK3/STAT5a/b signal transduction and cellular proliferation of antigen-activated human T cells. J Leukoc Biol 65: 891-899, 1999.
17. Kumral A, Tugyan K, Gonenc S, Genc K, Genc S, Sonmez U, Yilmaz O, Duman N, Uysal N, Ozkan H. Protective effects of erythropoietin against ethanol-induced apoptotic neurodegenaration and oxidative stress in the developing C57BL/6 mouse brain. Brain Res Dev Brain Res 160: 146-156, 2005.
18. Menon MP, Fang J, Wojchowski DM. Core erythropoietin receptor signals for late erythroblast development. Blood 107: 2662-2672, 2006.
19. Menon MP, Karur V, Bogacheva O, Bogachev O, Cuetara B, Wojchowski DM. Signals for stress erythropoiesis are integrated via an erythropoietin receptor phosphotyrosine-343-Stat5 axis. J Clin Invest 116: 683- 694, 2006.
20. Meydan N, Grunberger T, Dadi H, Shahar M, Arpaia E, Lapidot Z, Leeder JS, Freedman M, Cohen A, Gazit A, Levitzki A, Roifman CM. Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379: 645-648, 1996.
21. Pardanani A. JAK2 inhibitor therapy in myeloproliferative disorders: rationale, preclinical studies and ongoing clinical trials. Leukemia 22: 23-30, 2008.
22. Parsa CJ, Matsumoto A, Kim J, Riel RU, Pascal LS, Walton GB, Thompson RB, Petrofski JA, Annex BH, Stamler JS, Koch WJ. A novel protective effect of erythropoietin in the infarcted heart. J Clin Invest 112: 999-1007, 2003.
23. Patel NS, Sharples EJ, Cuzzocrea S, Chatterjee PK, Britti D, Yaqoob MM, Thiemermann C. Pretreatment with EPO reduces the injury and dysfunction caused by ischemia/reperfusion in the mouse kidney in vivo. Kidney Int 66: 983-989, 2004.
24. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
25. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, Priller J, Dirnagl U, Meisel A. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22: 10291-10301, 2002.
26. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, Glass T, Ardizzone T, Bernaudin M. Hypoxic preconditioning protects against ischemic brain injury. NeuroRx 1: 26-35, 2004.
27. Sharples EJ, Patel N, Brown P, Stewart K, Mota-Philipe H, Sheaff M, Kieswich J, Allen D, Harwood S, Raftery M, Thiemermann C, Yaqoob MM. Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion. J Am Soc Nephrol 15: 2115-2124, 2004.
28. Sheridan AM, Schwartz JH, Kroshian VM, Tercyak AM, Laraia J, Masino S, Lieberthal W. Renal mouse proximal tubular cells are more susceptible than MDCK cells to chemical anoxia. Am J Physiol Renal Fluid Electrolyte Physiol 265: F342-F350, 1993.
29. Shimamura H, Terada Y, Okado T, Tanaka H, Inoshita S, Sasaki S. The PI3-kinase-Akt pathway promotes mesangial cell survival and inhibits apoptosis in vitro via NF-κB and Bad. J Am Soc Nephrol 14: 1427-1434, 2003.
30. Socolovsky M, Nam H, Fleming MD, Haase VH, Brugnara C, Lodish HF. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood 98: 3261-3273, 2001.
31. Vesey DA, Cheung C, Pat B, Endre Z, Gobe G, Johnson DW. Erythropoietin protects against ischaemic acute renal injury. Nephrol Dial Transplant 19: 348-355, 2004.
32. Wang LH, Kirken RA, Erwin RA, Yu CR, Farrar WL. JAK3, STAT, and MAPK signaling pathways as novel molecular targets for the tyrphostin AG-490 regulation of IL-2-mediated T cell response. J Immunol 162: 3897-3904, 1999.
33. Wojchowski DM, Gregory RC, Miller CP, Pandit AK, Pircher TJ. Signal transduction in the erythropoietin receptor system. Exp Cell Res 253: 143-156, 1999.
34. Xiong H, Zhang ZG, Tian XQ, Sun DF, Liang QC, Zhang YJ, Lu R, Chen YX, Fang JY. Inhibition of JAK1,2/STAT3 signaling induces apoptosis, cell cycle arrest, and reduces tumor cell invasion in colorectal cancer cells. Neoplasia 10: 287-297, 2008.
35. Yamaura G, Turoczi T, Yamamoto F, Siddqui MA, Maulik N, Das DK. STAT signaling in ischemic heart: a role of STAT5A in ischemic preconditioning. Am J Physiol Heart Circ Physiol 285: H476-H482, 2003.
36. Yang N, Luo M, Li R, Huang Y, Zhang R, Wu Q, Wang F, Li Y, Yu X. Blockage of JAK/STAT signalling attenuates renal ischaemia-reperfusion injury in rat. Nephrol Dial Transplant 23: 91-100, 2008.
37. Yoshimura A, Misawa H. Physiology and function of the erythropoietin receptor. Curr Opin Hematol 5: 171-176, 1998.
38. Zang H, Sato K, Nakajima H, McKay C, Ney PA, Ihle JN. The distal region and receptor tyrosines of the Epo receptor are nonessential for in vivo erythropoiesis. EMBO J 20: 3156-3166, 2001.