Sestrin-2 and BNIP3 regulate autophagy and mitophagy in renal tubular cells in acute kidney injury

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 4, 2013, Pages

  Ishihara, Masayuki ^a   Urushido, Madoka ^a   Hamada, Kazu ^a   Matsumoto, Tatsuki ^a   Shimamura, Yoshiko ^a   Ogata, Koji ^a   Inoue, Kosuke ^a   Taniguchi, Yoshinori ^a   Horino, Taro ^a   Fujieda, Mikiya ^a   Fujimoto, Shimpei ^a   Terada, Yoshio ^a  

^a KOCHI MEDICAL SCHOOL   (Japan)

Author keywords

Acute kidney injury; Autophagy; Bcl 2 adenovirus E1B 19 kDa interacting protein 3; Mitophagy; Sestrin 2

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEIN; PROTEIN BNIP3; PROTEIN P53; SESTRIN 2; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY TUBULE CELL; MALE; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RENAL PROTECTION; REPERFUSION INJURY; WESTERN BLOTTING;

EID: 84881619807     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00642.2012     Document Type: Article

References (49)

1. Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 14: S55-S61, 2003.
2. Budanov AV, Karin M. p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134: 451-460, 2008.
3. Budanov AV, Shoshani T, Faerman A, Zelin E, Kamer I, Kalinski H, Gorodin S, Fishman A, Chajut A, Einat P, Skaliter R, Gudkov AV, Chumakov PM, Feinstein E. Identification of a novel stress-responsive gene Hi95 involved in regulation of cell viability. Oncogene 21: 6017-6031, 2002.
4. Byun YJ, Kim SK, Kim YM, Chae GT, Jeong SW, Lee SB. Hydrogen peroxide induces autophagic cell death in C6 glioma cells via BNIP3- mediated suppression of the mTOR pathway. Neurosci Lett 461: 131-135, 2009.
5. Castedo M, Ferri KF, Kroemer G. Mammalian target of rapamycin (mTOR): pro-and anti-apoptotic. Cell Death Differ 9: 99-100, 2002.
6. Chen G, Ray R, Dubik D, Shi L, Cizeau J, Bleackley RC, Saxena S, Gietz RD, Greenberg AH. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 186: 1975-1983, 1997.
7. Chien CT, Shyue SK, Lai MK. Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy. Transplantation 84: 1183-1190, 2007.
8. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126: 121-134, 2006.
9. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 17: 1503-1520, 2006.
10. Diwan A, Koesters AG, Odley AM, Pushkaran S, Baines CP, Spike BT, Daria D, Jegga AG, Geiger H, Aronow BJ, Molkentin JD, Macleod KF, Kalfa TA, Dorn 2nd G. Unrestrained erythroblast development in Nix-/- mice reveals a mechanism for apoptotic modulation of erythropoiesis. Proc Natl Acad Sci USA 104: 6794-6799, 2007.
11. Diwan A, Krenz M, Syed FM, Wansapura J, Ren X, Koesters AG, Li H, Kirshenbaum LA, Hahn HS, Robbins J, Jones WK, Dorn GW. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J Clin Invest 117: 2825-2833, 2007.
12. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E. Contribution of impaired mitochondrial autophagy to cardiac aging mechanisms and therapeutic opportunities. Circ Res 110: 1125-1138, 2012.
13. Elmore SP, Qian T, Grissom SF, Lemasters JJ. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15: 2286-2287, 2001.
14. Essler S, Dehne N, Brüne B. Role of sestrin2 in peroxide signaling in macrophages. FEBS Lett 583: 3531-3535, 2009.
15. Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 102: 8204-8209, 2005.
16. Fischer F, Hamann A, Osiewacz HD. Mitochondrial quality control: an integrated network of pathways. Trends Biochem Sci 37: 284-292, 2012.
17. Gottlieb RA, Carreira RS. Autophagy in health and disease. Mytophagy as a way of life. Am J Physiol Cell Physiol 299: C203-C210, 2010.
18. Gu L, Zhou C, Liu H, Gao J, Li Q, Mu D, Ma Z. Rapamycin sensitizes T-ALL cells to dexamethasone-induced apoptosis. J Exp Clin Cancer Res 29: 150, 2010.
19. Huber TB, Edelstein CL, Hartleben B, Inoki K, Jiang M, Koya D, Kume S, Lieberthal W, Pallet N, Quiroga A, Ravichandran K, Susztak K, Yoshida S, Dong Z. Emerging role of autophagy in kidney function, diseases and aging. Autophagy 8: 1-12, 2012.
20. Inoue K, Kuwana H, Shimamura Y, Ogata K, Taniguchi Y, Kagawa T, Horino T, Takao T, Morita T, Sasaki S, Mizushima N, Terada Y. Cisplatin-induced macroautophagy occurs prior to apoptosis in proximal tubules in vivo. Clin Exp Nephrol 14: 112-122, 2010.
21. Jiang M, Liu K, Luo J, Dong Z. Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am J Pathol 176: 1181-1192, 2010.
22. Kimura T, Takabatake Y, Takahashi A, Kaimori J, Matsui I, Namba T, Kitamura H, Niimura F, Matsusaka T, Soga T, Rakugi H, Isaka Y. Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J Am Soc Nephrol 22: 902-913, 2011.
23. Kobayashi T, Terada Y, Kuwana H, Tanaka H, Okado T, Kuwahara M, Tohda S, Sakano S, Sasaki S. Expression and function of the Delta-1/Notch-2/Hes-1 pathway during experimental acute kidney injury. Kidney Int 73: 1240-1250, 2008.
24. Kubli DA, Quinsay MN, Huang C, Lee Y, Gustafsson AB. Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 295: H2025-H2031, 2008.
25. Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441: 523-540, 2012.
26. Maiuri MC, Malik SA, Morselli E, Kepp O, Criollo A, Mouchel PL, Carnuccio R, Kroemer G. Stimulation of autophagy by the p53 target gene sestrin2. Cell Cycle 8: 1571-1576, 2009.
27. Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nature Cell Biol 12: 823-830, 2010.
28. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 140: 313-326, 2010.
29. Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A, Rogov V, Löhr F, Popovic D, Occhipinti A, Reichert AS, Terzic J, Dötsch V, Ney PA, Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 11: 45-51, 2009.
30. Periyasamy-Thandavan S, Jiang M, Wei Q, Smith R, Yin XM, Dong Z. Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells. Kidney Int 74: 631-640, 2008.
31. Regula KM, Ens K, Kirshenbaum LA. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 91: 226-231, 2002.
32. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, Chumakov PM. The antioxidant function of the p53 tumor suppressor. Nat Med 11: 1306-1313, 2005.
33. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 454: 232-235, 2008.
34. Sanli T, Linher-Melville K, Tsakiridis T, Singh G. Sestrin2 modulates AMPK subunit expression and its response to ionizing radiation in breast cancer cells. PloS One 7: e32035, 2012.
35. Sansanwal P, Yen B, Gahl WA, Ma Y, Ying L, Wong LJ, Sarwal MM. Mitochondrial autophagy promotes cellular injury in nephropathic cystinosis. J Am Soc Nephrol 21: 272-283, 2010.
36. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, Ney PA. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 104: 19500-19505, 2007.
37. Suzuki C, Isaka Y, Takabatake Y, Tanaka H, Koike M, Shibata M, Uchiyama Y, Takahara S, Imai E. Participation of autophagy in renal ischemia/reperfusion injury. Biochem Biophys Res Commun 368: 100-106, 2008.
38. Tanaka H, Terada Y, Kobayashi T, Okado T, Inoshita S, Kuwahara M, Seth A, Sato Y, Sasaki S. Expression and function of Ets-1 during experimental acute renal failure in rats. J Am Soc Nephrol 15: 3083-3092, 2004.
39. Terada Y, Inoshita S, Hanada S, Shimamura H, Kuwahara M, Ogawa W, Kasuga M, Sasaki S, Marumo F. Hyperosmolality activates Akt and regulates apoptosis in renal tubular cells. Kidney Int 60: 553-567, 2001.
40. Terada Y, Tanaka H, Okado T, Shimamura H, Inoshita S, Kuwahara M, Sasaki S. Expression and function of the developmental gene Wnt-4 during experimental acute renal failure in rats. J Am Soc Nephrol 14: 1223-1233, 2003.
41. Terada Y, Tomita K, Homma MK, Nonoguchi H, Yang T, Yamada T, Yuasa Y, Krebs EG, Sasaki S, Marumo F. Sequential activation of Raf-1 kinase, mitogen-activated protein (MAP) kinase kinase, MAP kinase, and S6 kinase by hyperosmolality in renal cells. J Biol Chem 269: 31296-31301, 1994.
42. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27: 433-446, 2008.
43. Wallin A, Zhang G, Jones TW, Jaken S, Stevens JL. Mechanism of the nephrogenic repair response. Studies on proliferation and vimentin expression after 35S-1,2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Invest 66: 474-484, 1992.
44. Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 7: 297-300, 2011.
45. Wu HH, Hsiao TY, Chien CT, Lai MK. Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced apoptosis and autophagy in the rat. J Biomed Sci 16: 19-22, 2009.
46. Xi H, Kurtoglu M, Liu H, Wangpaichitr M, You M, Liu X, Savaraj N, Lampidis TJ. 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion. Cancer Chemother Pharmacol 67: 899-910, 2011.
47. Yang C, Kaushal V, Shah SV, Kaushal GP. Autophagy is associated with apoptosis in cisplatin injury to renal tubular epithelial cells. Am J Physiol Renal Physiol 294: F777-F787, 2008.
48. Yasuda M, Theodorakis P, Subramanian T, Chinnadurai G. Adenovirus E1B-19K/BCL-2 interacting protein BNIP3 contains a BH3 domain and a mitochondrial targeting sequence. J Biol Chem 273: 12415-12421, 1998.
49. Zhang S, Zhang Z, Sandhu G, Ma X, Yang X, Geiger J, Kong J. Evidence of oxidative stress-induced BNIP3 expression in amyloid beta neurotoxicity. Brain Res 1138: 221-230, 2007.