zVAD-fmk prevents cisplatin-induced cleavage of autophagy proteins but impairs autophagic flux and worsens renal function

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 8, 2012, Pages

  Kaushal, Gur P ^a,b   Herzog, Christian ^a   Yang, Cheng ^a   Holmes, Alexandrea ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

Author keywords

Acute kidney injury; Atg5; Beclin 1; LC3; P62

Indexed keywords

AUTOPHAGY PROTEIN 5; BECLIN 1; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALPAIN; CATHEPSIN B; CHLOROQUINE; CISPLATIN; MEMBRANE PROTEIN; MEMBRANE PROTEIN ATG12; MEMBRANE PROTEIN LC3 II; PROTEIN P62; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME INHIBITION; HISTOPATHOLOGY; KIDNEY; KIDNEY DYSFUNCTION; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY TUBULE CELL; LYSOSOME; MOUSE; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RENAL PROTECTION; WESTERN BLOTTING;

EID: 84867731370     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00659.2011     Document Type: Article

References (68)

1. Arany I, Safirstein RL. Cisplatin nephrotoxicity. Semin Nephrol 23: 460-464, 2003.
2. Bizat N, Galas MC, Jacquard C, Boyer F, Hermel JM, Schiffmann SN, Hantraye P, Blum D, Brouillet E. Neuroprotective effect of zVAD against the neurotoxin 3-nitropropionic acid involves inhibition of calpain. Neuropharmacology 49: 695-702, 2005.
3. Bjorkoy G, Lamark T, Pankiv S, Overvatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 452: 181-197, 2009.
4. Bolisetty S, Traylor AM, Kim J, Joseph R, Ricart K, Landar A, Agarwal A. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 21: 1702-1712, 2010.
5. Cho DH, Jo YK, Hwang JJ, Lee YM, Roh SA, Kim JC. Caspase-mediated cleavage of ATG6/Beclin-1 links apoptosis to autophagy in HeLa cells. Cancer Lett 274: 95-100, 2009.
6. Cummings BS, Schnellmann RG. Cisplatin-induced renal cell apoptosis: caspase 3-dependent and -independent pathways. J Pharmacol Exp Ther 302: 8-17, 2002.
7. Daemen MA, van't Veer C, Denecker G, Heemskerk VH, Wolfs TG, Clauss M, Vandenabeele P, Buurman WA. Inhibition of apoptosis induced by ischemia-reperfusion prevents inflammation. J Clin Invest 104: 541-549, 1999.
8. de Duve C, de Barsy T, Poole B, Trouet A, Tulkens P, Van Hoof F. Commentary. Lysosomotropic agents. Biochem Pharmacol 23: 2495- 2531, 1974.
9. Demarchi F, Bertoli C, Copetti T, Eskelinen EL, Schneider C. Calpain as a novel regulator of autophagosome formation. Autophagy 3: 235-237, 2007.
10. Demarchi F, Bertoli C, Copetti T, Tanida I, Brancolini C, Eskelinen EL, Schneider C. Calpain is required for macroautophagy in mammalian cells. J Cell Biol 175: 595-605, 2006.
11. Dursun B, He Z, Somerset H, Oh DJ, Faubel S, Edelstein CL. Caspases and calpain are independent mediators of cisplatin-induced endothelial cell necrosis. Am J Physiol Renal Physiol 291: F578-F587, 2006.
12. Faubel S, Ljubanovic D, Reznikov L, Somerset H, Dinarello CA, Edelstein CL. Caspase-1-deficient mice are protected against cisplatin-induced apoptosis and acute tubular necrosis. Kidney Int 66: 2202-2213, 2004.
13. Funderburk SF, Wang QJ, Yue Z. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol 20: 355-362, 2010.
14. Guo R, Wang Y, Minto AW, Quigg RJ, Cunningham PN. Acute renal failure in endotoxemia is dependent on caspase activation. J Am Soc Nephrol 15: 3093-3102, 2004.
15. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroau-tophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 281: 29776-29787, 2006.
16. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43: 67-93, 2009.
17. 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.
18. Isaka Y, Kimura T, Takabatake Y. The protective role of autophagy against aging and acute ischemic injury in kidney proximal tubular cells. Autophagy 7: 1085-1087, 2011.
19. Ishida Y, Yamamoto A, Kitamura A, Lamande SR, Yoshimori T, Bateman JF, Kubota H, Nagata K. Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection. Mol Biol Cell 20: 2744-2754, 2009.
20. 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.
21. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728, 2000.
22. Kaminskyy V, Zhivotovsky B. Proteases in autophagy. Biochim Biophys Acta 1824: 44-50, 2012.
23. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 18: 571-580, 2011.
24. Kaushal GP, Kaushal V, Hong X, Shah SV. Role and regulation of activation of caspases in cisplatin-induced injury to renal tubular epithelial cells. Kidney Int 60: 1726-1736, 2001.
25. Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell 34: 259-269, 2009.
26. Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931-937, 2007.
27. Komatsu M, Ichimura Y. Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 584: 1374-1378, 2010.
28. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 40: 280-293, 2010.
29. Lau AH. Apoptosis induced by cisplatin nephrotoxic injury. Kidney Int 56: 1295-1298, 1999.
30. Levine B, Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest 115: 2679-2688, 2005.
31. Ling H, Vamvakas S, Busch G, Dammrich J, Schramm L, Lang F, Heidland A. Suppressing role of transforming growth factor-p1 on cathepsin activity in cultured kidney tubule cells. Am J Physiol Renal Fluid Electrolyte Physiol 269: F911-F917, 1995.
32. Linkermann A, Brasen JH, Himmerkus N, Liu S, Huber TB, Kun-zendorf U, Krautwald S. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Kidney Int 81: 751-761, 2012.
33. Liu H, Baliga R. Endoplasmic reticulum stress-associated caspase 12 mediates cisplatin-induced LLC-PK1 cell apoptosis. J Am Soc Nephrol 16: 1985-1992, 2005.
34. Madden DT, Egger L, Bredesen DE. A calpain-like protease inhibits autophagic cell death. Autophagy 3: 519-522, 2007.
35. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 140: 313-326, 2010.
36. Monick MM, Powers LS, Walters K, Lovan N, Zhang M, Gerke A, Hansdottir S, Hunninghake GW. Identification of an autophagy defect in smokers' alveolar macrophages. J Immunol 185: 5425-5435, 2010.
37. Nascimento-Ferreira I, Santos-Ferreira T, Sousa-Ferreira L, Auregan G, Onofre I, Alves S, Dufour N, Colomer Gould VF, Koeppen A, Deglon N, Pereira de Almeida L. Overexpression of the autophagic beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease. Brain 134: 1400-1415, 2011.
38. Ng S, Wu YT, Chen B, Zhou J, Shen HM. Impaired autophagy due to constitutive mTOR activation sensitizes TSC2-null cells to cell death under stress. Autophagy 7: 1173-1186, 2011.
39. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2: 211-216, 2001.
40. Pabla N, Dong Z. Cisplatin nephrotoxicity: mechanisms and renoprotec-tive strategies. Kidney Int 73: 994-1007, 2008.
41. Pallet N, Bouvier N, Legendre C, Gilleron J, Codogno P, Beaune P, Thervet E, Anglicheau D. Autophagy protects renal tubular cells against cyclosporine toxicity. Autophagy 4: 783-791, 2008.
42. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145, 2007.
43. Park MS, De Leon M, Devarajan P. Cisplatin induces apoptosis in LLC-PK1 cells via activation of mitochondrial pathways. J Am Soc Nephrol 13: 858-865, 2002.
44. 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.
45. Rozman-Pungercar J, Kopitar-Jerala N, Bogyo M, Turk D, Vasiljeva O, Stefe I, Vandenabeele P, Bromme D, Puizdar V, Fonovic M, Trstenjak-Prebanda M, Dolenc I, Turk V, Turk B. Inhibition of papain-like cysteine proteases and legumain by caspase-specific inhibitors: when reaction mechanism is more important than specificity. Cell Death Differ 10: 881-888, 2003.
46. Scaringi L, Cornacchione P, Ayroldi E, Corazzi L, Capodicasa E, Rossi R, Marconi P. Omeprazole induces apoptosis in jurkat cells. Int J Immunopathol Pharmacol 17: 331-342, 2004.
47. Schotte P, Declercq W, Van Huffel S, Vandenabeele P, Beyaert R. Nonspecific effects of methyl ketone peptide inhibitors of caspases. FEBS Lett 442: 117-121, 1999.
48. Sheikh-Hamad D, Cacini W, Buckley AR, Isaac J, Truong LD, Tsao CC, Kishore BK. Cellular and molecular studies on cisplatin-induced apoptotic cell death in rat kidney. Arch Toxicol 78: 147-155, 2004.
49. Su H, Li F, Ranek MJ, Wei N, Wang X. COP9 signalosome regulates autophagosome maturation. Circulation 124: 2117-2128, 2011.
50. 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.
51. Takahashi A, Kimura T, Takabatake Y, Namba T, Kaimori J, Kita-mura H, Matsui I, Niimura F, Matsusaka T, Fujita N, Yoshimori T, Isaka Y, Rakugi H. Autophagy guards against cisplatin-induced acute kidney injury. Am J Pathol 180: 517-525, 2012.
52. Tasdemir E, Galluzzi L, Maiuri MC, Criollo A, Vitale I, Hangen E, Modjtahedi N, Kroemer G. Methods for assessing autophagy and au-tophagic cell death. Methods Mol Biol 445: 29-76, 2008.
53. Tooze SA, Jefferies HB, Kalie E, Longatti A, McAlpine FE, McKnight NC, Orsi A, Polson HE, Razi M, Robinson DJ, Webber JL. Trafficking and signaling in mammalian autophagy. IUBMB Life 62: 503-508, 2010.
54. Tsuruya K, Ninomiya T, Tokumoto M, Hirakawa M, Masutani K, Taniguchi M, Fukuda K, Kanai H, Kishihara K, Hirakata H, Iida M. Direct involvement of the receptor-mediated apoptotic pathways in cis-platin-induced renal tubular cell death. Kidney Int 63: 72-82, 2003.
55. Turk B, Turk D, Salvesen GS. Regulating cysteine protease activity: essential role of protease inhibitors as guardians and regulators. Curr Pharm Des 8: 1623-1637, 2002.
56. Uchiyama Y. Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol 64: 233-246, 2001.
57. Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 80: 125-156, 2011.
58. White E. Autophagic cell death unraveled: pharmacological inhibition of apoptosis and autophagy enables necrosis. Autophagy 4: 399-401, 2008.
59. Wirawan E, Vande Walle L, Kersse K, Cornelis S, Claerhout S, Vanoverberghe I, Roelandt R, De Rycke R, Verspurten J, Declercq W, Agostinis P, Vanden Berghe T, Lippens S, Vandenabeele P. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced au-tophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria. Cell Death Dis 1: e18, 2010.
60. Wu HH, Hsiao TY, Chien CT, Lai MK. Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced ap-optosis and autophagy in the rat. J Biomed Sci 16: 19, 2009.
61. Wu YT, Tan HL, Huang Q, Kim YS, Pan N, Ong WY, Liu ZG, Ong CN, Shen HM. Autophagy plays a protective role during zVAD-induced necrotic cell death. Autophagy 4: 457-466, 2008.
62. Xia HG, Zhang L, Chen G, Zhang T, Liu J, Jin M, Ma X, Ma D, Yuan J. Control of basal autophagy by calpain1 mediated cleavage of ATG5. Autophagy 6: 61-66, 2009.
63. 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.
64. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 12: 814-822, 2010.
65. Yang Z, Klionsky DJ. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 22: 124-131, 2009.
66. Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T, Simon HU. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 8: 1124-1132, 2006.
67. Zhan Y, van de Water B, Wang Y, Stevens JL. The roles of caspase-3 and bcl-2 in chemically induced apoptosis but not necrosis of renal epithelial cells. Oncogene 18: 6505-6512, 1999.
68. Zhu Y, Zhao L, Liu L, Gao P, Tian W, Wang X, Jin H, Xu H, Chen Q. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis. Protein Cell 1: 468-477, 2010.