NQO1 Deficiency Leads Enhanced Autophagy in Cisplatin-Induced Acute Kidney Injury Through the AMPK/TSC2/mTOR Signaling Pathway

Antioxidants and Redox Signaling

Volumn 24, Issue 15, 2016, Pages 867-883

  Kim, Tae Won ^a   Kim, Young Jung ^a   Kim, Hyun Tae ^a   Park, Se Ra ^a   Lee, Mee Young ^b   Park, Yong Deok ^c   Lee, Chul Ho ^d   Jung, Ju Young ^a  

^a Chungnam National University   (South Korea)

^b Korea Institute of Oriental Medicine (KIOM)   (South Korea)

^c Youngdong University   (South Korea)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN P62; RAPAMYCIN; RAS PROTEIN; RAS RELATED PROTEIN 7; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); TUBERIN; UNCLASSIFIED DRUG; ADENYLATE KINASE; ANTINEOPLASTIC AGENT; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; MTOR PROTEIN, MOUSE; NQO1 PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE; TUMOR SUPPRESSOR PROTEIN;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KIDNEY TUBULE DAMAGE; LYSOSOME; MALE; MOUSE; NEPHROTOXICITY; NONHUMAN; NQO1 GENE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KIDNEY; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ACUTE KIDNEY INJURY; ADENYLATE KINASE; ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL LINE, TUMOR; CISPLATIN; HUMANS; KIDNEY; MALE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NAD(P)H DEHYDROGENASE (QUINONE); REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84971277813     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6386     Document Type: Article

References (49)

1. Alexander A, Cai SL, Kim J, Naneza A, Sahinc M, MacLeand KH, Inokie K, Guanf KL, Shena J, Persong MD, Kusewitt D, Millsh GB, Kastand MB, and Walker CL. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA 107: 4153-4158, 2010.
2. Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, and Johansen T. Monitoring autophagic degradation of p62/ SQSTM1. Methods Enzymol 452: 181-197, 2009.
3. Bolisetty S, Traylor AM, Kim J, Joseph R, Ricart K, Landar A, and Agarwal A. Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 21: 1702-1712, 2010.
4. Chen Y, Azad MB, and Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 16: 1040-1052, 2009.
5. Chen Y, McMillan-Ward E, Kong J, Israels SJ, and Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 15: 171-182, 2007.
6. Codogno P and Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12: 1509-1518, 2005.
7. Cummings BS and Schnellmann RG. Cisplatin-induced renal cell apoptosis: caspase 3-dependent and-independent pathways. J Pharm Exp Ther 302: 8-17, 2002.
8. Dinkova-Kostova AT and Talalay P. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch Biochem Biophys 501: 116-123, 2010.
9. Eskelinen EL, Schmidt CK, Neu S, Willenborg M, Fuertes G, Salvador N, Tanaka Y, Lullmann-Rauch R, Hartmann D, Heeren J, von Figura K, Knecht E, and Saftig P. Disturbed cholesterol traffic but normal proteolytic function in LAMP-1/LAMP-2 double-deficient fibroblasts. Mol Biol Cell 15: 3132-3145, 2004.
10. Fang B and Xiao H. Rapamycin alleviates cisplatin-induced ototoxicity in vivo. Biochem Biophys Res Commun 448: 443-447, 2014.
11. Fleury C, Mignotte B, and Vayssière JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84: 131-141, 2002.
12. Gaikwad A, Long DJ, Stringer JL, and Jaiswal AK. In vivo role of NAD (P) H: quinone oxidoreductase 1 (NQO1) in the regulation of intracellular redox state and accumulation of abdominal adipose tissue.JBiolChem276: 22559-22564, 2001.
13. Gang GT, Kim YH, Noh JR, Kim KS, Jung JY, Shong M, Hwang JH, and Lee CH. Protective role of NAD (P) H: quinone oxidoreductase 1 (NQO1) in cisplatin-induced nephrotoxicity. Toxicol Lett 221: 165-175, 2013.
14. Ganley IG, Wong PM, Gammoh N, and Jiang X. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42: 731-743, 2011.
15. Hariharan N, Zhai P, and Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Sign 14: 2179-2190, 2011.
16. Hasegawa K, Wakino S, Yoshioka K, Tatematsu S, Hara Y, Minakuchi H, Sueyasu K, Washida N, Tokuyama H, Tzukerman M, Skorecki K, Hayashi K, and Itoh H. Kidneyspecific overexpression of Sirt1 protects against acute kidney injury by retaining peroxisome function. J Bio Chem 285: 13045-13056, 2010.
17. Himmelfarb J, McMonagle E, Freedman S, Klenzak J, McMenamin E, Le P, Pupim LB, Ikizler TA, and The PICARD Group. Oxidative stress is increased in critically ill patientswith acute renal failure. J Am Soc Nephrol 15: 2449-2456, 2004.
18. Howell GM, Gomez H, Collage RD, Loughran P, Zhang X, Escobar DA, Billiar TR, Zuckerbraun BS, and Rosengart MR. Augmenting autophagy to treat acute kidney injury during endotoxemia in mice. PloS One 8: e69520, 2013.
19. Inoki K, Zhu T, and Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590, 2003.
20. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, and Yamamoto M. Transcription factor NRF2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Bio Chem 275: 16023-16029, 2000.
21. Iskander K, Barrios RJ, and Jaiswal AK. Disruption of NAD (P) H: quinone oxidoreductase 1 gene in mice leads to radiation-induced myeloproliferative disease. Cancer Res 68: 7915-7922, 2008.
22. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, and Eskelinen EL. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117: 4837-4848, 2004.
23. Jiang M, Wei Q, Dong G, Komatsu M, Su Y, and Dong Z. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 82: 1271-1283, 2012.
24. Juhász G, Erdi B, Sass M, and Neufeld TP. Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes Dev 21: 3061-3066, 2007.
25. Jung YJ, Lee JE, Lee AS, Kang KP, Lee S, Park SK, Lee SY, Han MK, Kim DH, and Kim W. SIRT1 overexpression decreases cisplatin-induced acetylation of NF-jB p65 subunit and cytotoxicity in renal proximal tubule cells. Biochem Biophys Res Commun 419: 206-210, 2012.
26. Kimura S, Fujita N, Noda T, and Yoshimori T. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 452: 1-12, 2009.
27. Larosche I, Letteron P, Berson A, Fromenty B, Huang TT, Moreau R, Pessayre D, and Mansouri A. Hepatic mitochondrial DNA depletion after an alcohol binge in mice: probable role of peroxynitrite and modulation by manganese superoxide dismutase. J Pharmacol Exp Ther 332: 886-897, 2010.
28. Long DJ, Waikel RL, Wang XJ, Roop DR, and Jaiswal AK. NAD (P) H: quinone oxidoreductase 1 deficiency and increased susceptibility to 7, 12-dimethylbenz [a]-anthracene-induced carcinogenesis in mouse skin. J Natl Cancer Inst 93: 1166-1170, 2001.
29. Lee JS, Giordano S, and Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J 441: 523-540, 2012.
30. Lu C. β-Lapachone ameliorates murine cisplatin nephrotoxicity: NAD+, NQO1, and SIRT1 at the crossroads of metabolism, injury, and inflammation. Kidney Int 85: 496-498, 2014.
31. Marullo R, Werner E, Degtyareva N, Moore B, Altavilla G, Ramalingam SS, and Doetsch, PW. Cisplatin induces a mitochondrial-ros response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PloS One 8: e81162. 2013.
32. Mizushima N. Autophagy: process and function. Genes Dev 21: 2861-2873, 2007.
33. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1-13, 2009.
34. Nioi P and Hayes JD. Contribution of NAD (P) H: quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the NRF2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loophelix transcription factors. Mutat Res 555: 149-171, 2004.
35. Oh GS, Kim HJ, Choi JH, Shen A, Choe SK, Karna A, Lee SH, Jo HJ, Yang SH, Kwak TH, Lee CH, Park R, and So HS. Pharmacological activation of NQO1 increases NAD+; levels and attenuates cisplatin-mediated acute kidney injury in mice. Kidney Int 85: 547-560, 2014.
36. Periyasamy-Thandavan S, Jiang M, Wei Q, Smith R, Yin XM, and Dong Z. Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells. Kidney Int 74: 631-640, 2008.
37. Pflueger A, Abramowitz D, and Calvin AD. Role of oxidative stress in contrast-induced acute kidney injury in diabetes mellitus. Med Sci Monit 15: RA125-RA136, 2009.
38. Rao VA, Klein SR, Bonar SJ, Zielonka J, Mizuno N, Dickey JS, Keller PW, Joseph J, Kalyanaraman B, and Shacter E. The antioxidant transcription factor NRF2 negatively regulates autophagy and growth arrest induced by the anticancer redox agent mitoquinone. J Bio Chem 285: 34447-34459, 2010.
39. Reef S, Zalckvar E, Shifman O, Bialik S, Sabanay H, Oren M, and Kimchi A. A short mitochondrial form of p19 ARF induces autophagy and caspase-independent cell death. Mol Cell 22: 463-475, 2006.
40. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, and Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290-303, 2010.
41. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, and Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760, 2007.
42. Siegel D, Gustafson DL, Dehn DL, Han JY, Boonchoong P, Berliner LJ, and Ross D. NAD (P) H: quinone oxidoreductase 1: role as a superoxide scavenger. Mol Pharmacol 65: 1238-1247, 2004.
43. Takahashi A, Kimura T, Takabatake Y, Namba T, Kaimori J, Kitamura H, Matsui I, Niimura F, Matsusaka T, Fujita N, Yoshimori T, Isaka Y, and Rakugi H. Autophagy guards against cisplatin-induced acute kidney injury. Am J Pathol 180: 517-525, 2012.
44. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lullmann-Rauch R, Janssen PM, Blanz J, von Figura K, and Saftig P. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406: 902-906, 2000.
45. Tian Z, Wang C, Hu C, Tian Y, Liu J, and Wang X. Autophagic-lysosomal inhibition compromises ubiquitinproteasome system performance in a p62 dependent manner in cardiomyocytes. PloS One 9: e100715, 2014.
46. Vasiliou V, Ross D, and Nebert DW. Update of the NAD(P)H:quinone oxidoreductase (NQO) gene family. Hum Genomics 2: 329-335, 2006.
47. Watanabe R, Wei L, and Huang J. mTOR signaling, function, novel inhibitors, and therapeutic targets. J Nucl Med 52: 497-500, 2011.
48. Yang Z, Schumaker LM, Egorin MJ, Zuhowski EG, Guo Z, and Cullen KJ. Cisplatin preferentially binds mitochondrial DNA and voltage-dependent anion channel protein in the mitochondrial membrane of head and neck squamous cell carcinoma: possible role in apoptosis. Clin Cancer Res 12: 5817-5825, 2006.
49. Yorimitsu T and Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ 12: 1542-1552, 2005.