Autophagy induction promotes aristolochic acid-I-induced renal injury in vivo and in vitro

Toxicology

Volumn 312, Issue 1, 2013, Pages 63-73

  Yang, Ching Chin ^a   Wu, Cheng Tien ^a   Chen, Li Ping ^b   Hung, Kuan Yu ^a   Liu, Shing Hwa ^a,c   Chiang, Chih Kang ^a,d  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Apoptosis; Aristolochic acid; Atg5; Autophagy; Nephropathy

Indexed keywords

ARISTOLOCHIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; FRAGMENTATION REACTION; KIDNEY INJURY; KIDNEY TUBULE CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN POLYMERIZATION;

3-MA; 3-METHYL ADENINE; AA; APOPTOSIS; ARISTOLOCHIC ACID; ATG; ATG5; AUTOPHAGY; AUTOPHAGY-RELATED GENE; LC3; LD50; MEDIAN LETHAL DOSE; MICROTUBULE-ASSOCIATED PROTEIN LIGHT CHAIN 3; NEPHROPATHY; NORMAL RAT RENAL PROXIMAL TUBULAR EPITHELIAL CELLS; NRK52E; PARP; POLY (ADP-RIBOSE) POLYMERASE;

ANIMALS; APOPTOSIS; ARISTOLOCHIC ACIDS; AUTOPHAGY; KIDNEY; MALE; PROTEINS; RATS; RATS, WISTAR;

EID: 84883263888     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.07.017     Document Type: Article

References (39)

1. Chen Y., Klionsky D.J. The regulation of autophagy - unanswered questions. J. Cell Sci. 2011, 124:161-170.
2. Chiang C.K., Hsu S.P., Wu C.T., Huang J.W., Cheng H.T., Chang Y.W., Hung K.Y., Wu K.D., Liu S.H. Endoplasmic reticulum stress implicated in the development of renal fibrosis. Mol. Med. 2011, 17:1295-1305.
3. Chiang C.K., Sheu M.L., Lin Y.W., Wu C.T., Yang C.C., Chen M.W., Hung K.Y., Wu K.D., Liu S.H. Honokiol ameliorates renal fibrosis by inhibiting extracellular matrix and pro-inflammatory factors in vivo and in vitro. Br. J. Pharmacol. 2011, 163:586-597.
4. Chiang C.K., Tanaka T., Inagi R., Fujita T., Nangaku M. Indoxyl sulfate, a representative uremic toxin, suppresses erythropoietin production in a HIF-dependent manner. Lab. Invest. 2011, 91:1564-1571.
5. Fass E., Amar N., Elazar Z. Identification of essential residues for the C-terminal cleavage of the mammalian LC3: a lesson from yeast Atg8. Autophagy 2007, 3:48-50.
6. Filippi-Chiela E.C., Villodre E.S., Zamin L.L., Lenz G. Autophagy interplay with apoptosis and cell cycle regulation in the growth inhibiting effect of resveratrol in glioma cells. PLoS ONE 2011, 6:e20849.
7. Funk J.A., Schnellmann R.G. Persistent disruption of mitochondrial homeostasis after acute kidney injury. Am. J. Physiol. Renal Physiol. 2012, 302:F853-F864.
8. Glick D., Barth S., Macleod K.F. Autophagy: cellular and molecular mechanisms. J. Pathol. 2010, 221:3-12.
9. Hammond E.M., Brunet C.L., Johnson G.D., Parkhill J., Milner A.E., Brady G., Gregory C.D., Grand R.J. Homology between a human apoptosis specific protein and the product of APG5, a gene involved in autophagy in yeast. FEBS Lett. 1998, 425:391-395.
10. Hsin Y.H., Cheng C.H., Tzen J.T., Wu M.J., Shu K.H., Chen H.C. Effect of aristolochic acid on intracellular calcium concentration and its links with apoptosis in renal tubular cells. Apoptosis 2006, 11:2167-2177.
11. Kimura T., Takabatake Y., Takahashi A., Kaimori J.Y., 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. 2011, 22:902-913.
12. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007, 8:741-752.
13. Mitra S., Gera R., Siddiqui W.A., Khandelwal S. Tributyltin induces oxidative damage, inflammation and apoptosis via disturbance in blood-brain barrier and metal homeostasis in cerebral cortex of rat brain: an in vivo and in vitro study. Toxicology 2013, 310C:39-52.
14. Mizushima N., Sugita H., Yoshimori T., Ohsumi Y. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem. 1998, 273:33889-33892.
15. 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 2008, 4:783-791.
16. Park M.A., Walker T., Martin A.P., Allegood J., Vozhilla N., Emdad L., Sarkar D., Rahmani M., Graf M., Yacoub A., Koumenis C., Spiegel S., Curiel D.T., Voelkel-Johnson C., Grant S., Fisher P.B., Dent P. MDA-7/IL-24-induced cell killing in malignant renal carcinoma cells occurs by a ceramide/CD95/PERK-dependent mechanism. Mol. Cancer Ther. 2009, 8:1280-1291.
17. Periyasamy-Thandavan S., Jiang M., Wei Q., Smith R., Yin X.M., Dong Z. Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells. Kidney Int. 2008, 74:631-640.
18. Pozdzik A.A., Salmon I.J., Debelle F.D., Decaestecker C., Van den Branden C., Verbeelen D., Deschodt-Lanckman M.M., Vanherweghem J.L., Nortier J.L. Aristolochic acid induces proximal tubule apoptosis and epithelial to mesenchymal transformation. Kidney Int. 2008, 73:595-607.
19. Program N.T. Final report on carcinogens background document for aristolochic acids. Rep. Carcinog. Backgr. Doc. 2008, I-XXV:1-246.
20. Pyo J.O., Jang M.H., Kwon Y.K., Lee H.J., Jun J.I., Woo H.N., Cho D.H., Choi B., Lee H., Kim J.H., Mizushima N., Oshumi Y., Jung Y.K. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J. Biol. Chem. 2005, 280:20722-20729.
21. Rovetta F., Stacchiotti A., Consiglio A., Cadei M., Grigolato P.G., Lavazza A., Rezzani R., Aleo M.F. ER signaling regulation drives the switch between autophagy and apoptosis in NRK-52E cells exposed to cisplatin. Exp. Cell Res. 2012, 318:238-250.
22. Sansanwal P., Yen B., Gahl W.A., Ma Y., Ying L., Wong L.J., Sarwal M.M. Mitochondrial autophagy promotes cellular injury in nephropathic cystinosis. J. Am. Soc. Nephrol. 2010, 21:272-283.
23. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 2004, 6:1221-1228.
24. Sou Y.S., Tanida I., Komatsu M., Ueno T., Kominami E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J. Biol. Chem. 2006, 281:3017-3024.
25. Sun Y., Liu J.H., Jin L., Lin S.M., Yang Y., Sui Y.X., Shi H. Over-expression of the Beclin1 gene upregulates chemosensitivity to anti-cancer drugs by enhancing therapy-induced apoptosis in cervix squamous carcinoma CaSki cells. Cancer Lett. 2010, 294:204-210.
26. Tra T., Gong L., Kao L.P., Li X.L., Grandela C., Devenish R.J., Wolvetang E., Prescott M. Autophagy in human embryonic stem cells. PLoS ONE 2011, 6:e27485.
27. Tsujimoto Y., Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ. 2005, 12(Suppl 2):1528-1534.
28. Varma H., Gangadhar N.M., Letso R.R., Wolpaw A.J., Sriramaratnam R., Stockwell B.R. Identification of a small molecule that induces ATG5-and-cathepsin-l-dependent cell death and modulates polyglutamine toxicity. Exp. Cell Res. 2013, 319:1759-1773.
29. Wang Y., Han R., Liang Z.Q., Wu J.C., Zhang X.D., Gu Z.L., Qin Z.H. An autophagic mechanism is involved in apoptotic death of rat striatal neurons induced by the non-N-methyl-d-aspartate receptor agonist kainic acid. Autophagy 2008, 4:214-226.
30. Wu C.T., Sheu M.L., Tsai K.S., Weng T.I., Chiang C.K., Liu S.H. The role of endoplasmic reticulum stress-related unfolded protein response in the radiocontrast medium-induced renal tubular cell injury. Toxicol. Sci. 2010, 114:295-301.
31. Wu K.M., Farrelly J.G., Upton R., Chen J. Complexities of the herbal nomenclature system in traditional Chinese medicine (TCM): lessons learned from the misuse of aristolochia-related species and the importance of the pharmaceutical name during botanical drug product development. Phytomedicine 2007, 14:273-279.
32. Yang L., Su T., Li X.M., Wang X., Cai S.Q., Meng L.Q., Zou W.Z., Wang H.Y. Aristolochic acid nephropathy: variation in presentation and prognosis. Nephrol. Dial. Transplant. 2012, 27:292-298.
33. Young M.M., Takahashi Y., Khan O., Park S., Hori T., Yun J., Sharma A.K., Amin S., Hu C.D., Zhang J., Kester M., Wang H.G. Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis. J. Biol. Chem. 2012, 287:12455-12468.
34. Yousefi S., Perozzo R., Schmid I., Ziemiecki A., Schaffner T., Scapozza L., Brunner T., Simon H.U. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat. Cell Biol. 2006, 8:1124-1132.
35. Zeng Y., Yang X., Wang J., Fan J., Kong Q., Yu X. Aristolochic acid I induced autophagy extenuates cell apoptosis via ERK 1/2 pathway in renal tubular epithelial cells. PLoS ONE 2012, 7:e30312.
36. Zhang C., Wang X., Shang M., Yu J., Xu Y., Li Z., Lei L., Li X., Cai S., Namba T. Simultaneous determination of five aristolochic acids and two aristololactams in Aristolochia plants by high-performance liquid chromatography. Biomed. Chromatogr. 2006, 20:309-318.
37. Zhang Y., Calderwood S.K. Autophagy, protein aggregation and hyperthermia: a mini-review. Int. J. Hyperthermia 2011, 27:409-414.
38. Zhou F., Yang Y., Xing D. Bcl-2 and Bcl-xL play important roles in the crosstalk between autophagy and apoptosis. FEBS J. 2011, 278:403-413.
39. Zhu S., Wang Y., Jin J., Guan C., Li M., Xi C., Ouyang Z., Chen M., Qiu Y., Huang M., Huang Z. Endoplasmic reticulum stress mediates aristolochic acid I-induced apoptosis in human renal proximal tubular epithelial cells. Toxicol. In Vitro 2012, 26:663-671.