Ursolic acid induces autophagy in U87MG cells via ROS-dependent endoplasmic reticulum stress

Chemico-Biological Interactions

Volumn 218, Issue , 2014, Pages 28-41

  Shen, Shuying ^a   Zhang, Yi ^a   Zhang, Rui ^b   Tu, Xintao ^a   Gong, Xingguo ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; Calcium; ER stress; Ursolic acid

Indexed keywords

ADENYLATE KINASE; BECLIN 1; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CELL ENZYME; CELL PROTEIN; EUKARYOTIC TRANSLATION INITIATION FACTOR 2ALPHA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2; IRE1ALPHA PROTEIN; JANUS KINASE; LC3 II PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PKR LIKE ENDOPLASMIC RETICULUM KINASE; PROTEIN BCL 2; PROTEIN IRE1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; URSOLIC ACID;

ARTICLE; AUTOPHAGY; BIOACCUMULATION; CALCIUM CELL LEVEL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

AUTOPHAGY; CALCIUM; ER STRESS; URSOLIC ACID;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; AUTOPHAGY; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; ENDOPLASMIC RETICULUM STRESS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR STRUCTURE; REACTIVE OXYGEN SPECIES; TRITERPENES;

EID: 84901062374     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2014.04.017     Document Type: Article

References (60)

1. A. Gorostizaga, M.M. Mori Sequeiros García, A. Acquier, N.V. Gomez, P.M. Malobert, C.F. Mendez, and C. Paz Modulation of albumin-induced endoplasmic reticulum stress in renal proximal tubule cells by upregulation of mapk phosphatase-1 Chem. Biol. Interact. 206 1 2013 47 54
2. X. Li, K. Zhang, and Z. Li Unfolded protein response in cancer: the physician's perspective J. Hematol. Oncol. 4 2011 8
3. S. Srinivasan, M. Ohsugi, Z. Liu, S. Fatrai, E. Bernal-Mizrachi, and M.A. Permutt Endoplasmic reticulum stress-induced apoptosis is partly mediated by reduced insulin signaling through phosphatidylinositol 3-kinase/Akt and increased glycogen synthase kinase-3beta in mouse insulinoma cells Diabetes 54 4 2005 968 975
4. A. Lugea, D. Tischler, J. Nguyen, J. Gong, I. Gukovsky, S.W. French, F.S. Gorelick, and S.J. Pandol Adaptive unfolded protein response attenuates alcohol-induced pancreatic damage Gastroenterology 140 3 2011 987 997
5. C. Bincoletto, A. Bechara, G.J. Pereira, C.P. Santos, F. Antunes, J. Peixoto da-Silva, M. Muler, R.D. Gigli, P.T. Monteforte, H. Hirata, A. Jurkiewicz, and S.S. Smaili Interplay between apoptosis and autophagy, a challenging puzzle: new perspectives on antitumor chemotherapies Chem. Biol. Interact. 206 2 2013 279 288
6. J. Li, L. Zhang, Z. Jiang, B. Shu, F. Li, Q. Bao, and L. Zhang Toxicities of aristolochic acid I and aristololactam I in cultured renal epithelial cells Toxicol. In Vitro 24 4 2010 1092 1097
7. S. Periyasamy-Thandavan, M. Jiang, P. Schoenlein, and Z. Dong Autophagy: molecular machinery, regulation, and implications for renal pathophysiology Am. J. Physiol. Renal Physiol. 297 2 2009 F244 F256
8. M. Djavaheri-Mergny, M. Amelotti, J. Mathieu, F. Besancon, C. Bauvy, and P. Codogno Regulation of autophagy by NFkappaB transcription factor and reactive oxygen species Autophagy 3 4 2007 390 392
9. I. Tanida Autophagosome formation and molecular mechanism of autophagy Antioxid. Redox Signal. 14 11 2011 2201 2214
10. P. Codogno, S. Pattingre, and C. Bauvy Amino acids interfere with the ERK1/2-dependent control of macroautophagy by control-ling the activation of Raf-1 in human colon cancer HT-29 cells J. Biol. Chem. 278 19 2003 16667 16674
11. T. Opriessnig, M.J. Meng, and P.G. Halbur Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies J. Vet. Diagn. Invest. 19 6 2007 591 615
12. A. Alexander, S.L. Cai, J. Kim, A. Nanez, M. Sahin, K.H. MacLean, K. Inoki, K.L. Guan, J. Shen, M.D. Person, D. Kusewitt, G.B. Mils, M.B. Kastan, and C.L. Walker ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS Proc. Natl. Acad. Sci. U.S.A. 107 9 2010 4153 4158
13. T. Okazaki, T. Kageji, K. Kuwayama, K.T. Kitazato, H. Mure, K. Hara, R. Morigaki, Y. Mizobuchi, K. Matsuzaki, and S. Nagahiro Upregulation of endogenous PML induced by a combination of interferon-beta and temozolomide enhances p73/YAP-mediated apoptosis in glioblastoma Cancer Lett. 323 2 2012 199 207
14. M. Niikawa, H. Hayashi, T. Sato, H. Nagase, and H. Kito Isolation of substances from glossy privet (Ligustrum lucidum Ait) inhibiting the mutagenicity of benzo[a] pyrene in bacteria Mutat. Res. 319 1 1993 1 9
15. A.K. Pathak, M. Bhutani, A.S. Nair, K.S. Ahn, A. Chakraborty, H. Kadara, S. Guha, G. Sethi, and B.B. Aggarwal Ursolic acid inhibits STAT3 activation pathway leading to suppression of proliferation and chemosensitization of human multiple myeloma cells Mol. Cancer Res. 5 9 2007 943 955
16. S. Shishodia, S. Majumdar, S. Banerjee, and B.B. Aggarwal Ursolic acid inhibits nuclear factor-kappaB activation induced by carcinogenic agents through suppression of IkappaBalpha kinase and p65 phosphorylation: correlation with down-regulation of cyclooxygenase 2, matrix metalloproteinase 9, and cyclin D1 Cancer Res. 63 15 2003 4375 4383
17. Y. Zhang, C. Kong, Y. Zeng, L. Wang, Z. Li, H. Wang, C. Xu, and Y. Sun Ursolic acid induces PC-3 cell apoptosis via activation of JNK and inhibition of Akt pathways in vitro Mol. Carcinog. 49 4 2010 374 385
18. Y.L. Hsu, P.L. Kuo, and C.C. Lin Proliferative inhibition, cell-cycle dysregulation, and induction of apoptosis by ursolic acid in human non-small cell lung cancer A549 cells Life Sci. 75 19 2004 2303 2316
19. K. Sato, K. Tsuchihara, S. Fujii, M. Sugiyama, T. Goya, Y. Atomi, T. Ueno, A. Ochiai, and H. Esumi Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation Cancer Res. 67 20 2007 9677 9684
20. A. Gruzman, G. Babai, and S. Ssasson Adenosine monophosphate-activated protein kinase (AMPK) as a new target for antidiabetic drugs: a review on metabolic, pharmacological and chemical considerations Rev. Diabetic Stud. 6 1 2009 13 36
21. H.J. Chung, H.K. Rhee, S.K. Lee, and H.Y. Park Choo Antitumor effects of a novel benzonaphthofurandione derivative (8e) on the human colon cancer cells in vitro and in vivo through cell cycle arrest accompanied with the modulation of EGFR and mTOR signaling Chem. Biol. Interact. 193 1 2011 43 49
22. V.K. Wong, T. Li, B.Y. Law, E.D. Ma, C.N. Yip, F. Michelangeli, C.K. Law, M.M. Zhang, K.Y. Lam, P.L. Chan, and L. Liu Saikosaponin-d, a novel SERCA inhibitor, induces autophagic cell death in apoptosis-defective cells Cell Death Dis. 4 2013 e720
23. Y.L. Hsu, L.Y. Wu, and P.L. Kuo Dehydrocostuslactone a medicinal plant-derived sesquiterpene lactone, induces apoptosis coupled to endoplasmic reticulum stress in liver cancer cells J. Pharmacol. Exp. Ther. 329 2 2009 808 819
24. J. Li, and A.S. Lee Stress induction of GRP78/BiP and its role in cancer Curr. Mol. Med. 6 1 2006 45 54
25. H.P. Harding, Y. Zhang, and D. Ron Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase Nature 397 6716 1999 271 274
26. S. Lépine, J.C. Allegood, M. Park, P. Dent, S. Milstien, and S. Spiegel Sphingosine-1-phosphate phosphohydrolase-1 regulates ER stress-induced autophagy Cell Death Differ. 18 2 2011 350 361
27. C.W. Younce, and P.E. Kolattukudy MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP Biochemistry 426 1 2010 43 53
28. T. Rzymski, M. Milani, L. Pike, F. Buffa, H.R. Mellor, L. Winchester, I. Pires, E. Hammond, I. Ragoussis, and A.L. Harris Regulation of autophagy by ATF4 in response to severe hypoxia Oncogene 29 31 2010 4424 4435
29. M. Ogata, S. Hino, A. Saito, K. Morikawa, S. Kondo, S. Kanemoto, T. Murakami, M. Taniguchi, I. Tanii, K. Yoshinaga, S. Shiosaka, J.A. Hammarback, F. Urano, and K. Imaizumi Autophagy is activated for cell survival after endoplasmic reticulum stress Mol. Cell. Biol. 26 24 2006 9220 9231
30. D. Rodriguez, D. Rojas-Rivera, and C. Hetz Integrating stress signals at the endoplasmic reticulum: the BCL-2 protein family rheostat Biochim. Biophys. Acta 1813 4 2011 564 574
31. R.T. Marquez, and L. Xu Bcl-2:Beclin 1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch Am. J. Cancer Res. 2 2 2012 214 221
32. D. Lu, J. Liu, J. Jiao, B. Long, Q. Li, W. Tan, and P. Li Transcription factor Foxo3a prevents apoptosis by regulating calcium through the apoptosis repressor with caspase recruitment domain J. Biol. Chem. 288 12 2013 8491 8504
33. R.M. Kluck, C.A. McDougall, B.V. Harmon, and J.W. Halliday Calcium chelators induce apoptosis-evidence that raised intracellular ionised calcium is not essential for apoptosis Biochim. Biophys. Acta 1223 2 1994 247 254
34. J.D. Malhotra, and R.J. Kaufman Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9 12 2007 2277 2293
35. L. Yang, X. Liu, Z. Lu, J. Yuet-Wa Chan, L. Zhou, KP. Fung, P. Wu, and S. Wu Ursolic acid induces doxorubicin-resistant HepG2 cell death via the release of apoptosis-inducing factor Cancer Lett. 298 1 2010 128 138
36. E.K. Yim, K.H. Lee, S.E. Namkoong, S.J. Um, and J.S. Park Proteomic analysis of ursolic acid-induced apoptosis in cervical carcinoma cells Cancer Lett. 235 2 2006 209 220
37. S. Prasad, V.R. Yadav, R. Kannappan, and B.B. Aggarwal Ursolic acid, a pentacyclin triterpene, potentiates TRAIL induced apoptosis through p53-independent upregulation of death receptors: evidence for the role of reactive oxygen species and JNK J. Biol. Chem. 286 7 2011 5546 5557
38. S. Leng, Y. Hao, D. Du, S. Xie, L. Hong, H. Gu, X. Zhu, J. Zhang, D. Fan, and H. Kung Ursolic acid promotes cancer cell death by inducing Atg5-dependent autophagy Int. J. Cancer 133 12 2013 2781 2790
39. E. Buytaert, G. Callewaert, N. Hendrickx, L. Scorrano, D. Hartmann, L. Missiaen, J.R. Vandenheede, I. Heirman, J. Grooten, and P. Agostinis Role of endoplasmic reticulum depletion and multidomain proapoptotic Bax and Bak proteins in shaping cell death after hypericin-mediated photodynamic therapy FASEB J. 20 6 2006 756 758
40. M. Hoyer-Hansen, L. Bastholm, P. Szyniarowski, M. Campanella, G. Szabadkai, T. Farkas, K. Bianchi, N. Fehrenbacher, F. Elling, R. Rizzuto, I.S. Mathiasen, and M. Jäättelä Control of macroautophagy by calcium, calmodulindependent kinase kinase-b, and Bcl-2 Mol. Cell 25 2 2007 193 205
41. D.V. Gordienko, and T.B. Bolton Crosstalk between ryanodine receptors and IP(3) receptors as a factor shaping spontaneous Ca(2+)-release events in rabbit portal vein myocytes J. Physiol. 542 Pt 3 2002 743 762
42. A. Criollo, M.C. Maiuri, E. Tasdemir, I. Vitale, A.A. Fiebig, D. Andrews, J. Molgó, J. Díaz, S. Lavandero, F. Harper, G. Pierron, D. di Stefano, R. Rizzuto, G. Szabadkai, and G. Kroemer Regulation of autophagy by the inositol trisphosphate receptor Cell Death Differ. 14 5 2007 1029 1039
43. T. Verfaillie, M. Salazar, G. Velasco, and P. Agostinis Linking ER stress to autophagy: potential implications for cancer therapy Int. J. Cell Biol. 2010 2010 930509
44. K. Inoki, T. Zhu, and K.L. Guan TSC2 mediates cellular energy response to control cell growth and survival Cell 115 5 2003 577 590
45. L. Ma, N. Niknejad, I. Gorn-Hondermann, K. Dayekh, and J. Dimitroulakos Lovastatin induces multiple stress pathways including LKB1/AMPK activation that regulate its cytotoxic effects in squamous cell carcinoma cells PLoS One 7 9 2012 e46055
46. J. Merlin, B.A. Evans, R.I. Csikasz, T. Bengtsson, R.J. Summers, and D.S. Hutchinson The M3-muscarinic acetylcholine receptor stimulates glucose uptake in L6 skeletal muscle cells by a CaMKK-AMPK-dependent mechanism Cell Signal. 22 7 2010 1104 1113
47. M. Høyer-Hansen, and M. Jäättelä AMP-activated protein kinase: a universal regulator of autophagy? Autophagy 3 4 2007 381 383
48. X. Tong, K.A. Smith, and J.C. Pelling Apigenin, a chemopreventive bioflavonoid, induces AMP-activated protein kinase activation in human keratinocytes Mol. Carcinog. 51 3 2012 268 279
49. C.W. Park, S.M. Hong, E.S. Kim, J.H. Kwon, K.T. Kim, H.G. Nam, and K.Y. Choi 25BNIP3 is degraded by ULK1-dependent autophagy via MTORC1 and AMPK Autophagy 9 3 2013 345 360
50. A. Grotemeier, S. Alers, S.G. Pfisterer, F. Paasch, M. Daubrawa, A. Dieterle, B. Viollet, S. Wesselborg, T. Proikas-Cezanne, and B. Stork AMPK-independent induction of autophagy by cytosolic Ca2+ increase Cell Signal. 22 6 2010 914 925
51. Z. Tallóczy, W.X. Jiang, H.W. Virgin, D.A. Leib, D. Scheuner, R.J. Kaufman, E.L. Eskelinen, and B. Levine Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway Proc. Natl. Acad. Sci. U.S.A. 99 1 2002 190 195
52. M.A. Garcia, E.F. Meurs, and M. Esteban The dsRNA protein kinase PKR: virus and cell control Biochimie 89 6-7 2007 799 811
53. Y. Kouroku, E. Fujita, I. Tanida, T. Ueno, A. Isoai, H. Kumagai, S. Ogawa, R.J. Kaufman, E. Kominami, and T. Momoi ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation Cell Death Diff. 14 2 2007 230 239
54. K.M. Rouschop, T. van den Beucken, L. Dubois, H. Niessen, J. Bussink, K. Savelkouls, T. Keulers, H. Mujcic, W. Landuyt, J.W. Voncken, P. Lambin, A.J. van der Kogel, M. Koritzinsky, and B.G. Wouters The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5 J. Clin. Invest. 120 1 2010 127 141
55. M. Ito, H. Nakagawa, T. Okada, S. Miyazaki, and S. Matsuo ER-stress caused by accumulated intracistanal granules activates autophagy through a different signal pathway from unfolded protein response in exocrine pancreas cells of rats exposed to fluoride Arch. Toxicol. 83 2 2009 151 159
56. J.F. Raven, D. Baltzis, S. Wang, Z. Mounir, A.I. Papadakis, H.Q. Gao, and A.E. Koromilas PKR and PKR-like endoplasmic reticulum kinase induce the proteasome-dependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation J. Biol. Chem. 283 6 2008 3097 3108
57. S.R. Stockwell, G. Platt, S.E. Barrie, G. Zoumpoulidou, R.H. Te Poele, G.W. Aherne, S.C. Wilson, P. Sheldrake, E. McDonald, M. Venet, C. Soudy, F. Elustondo, L. Rigoreau, J. Blagg, P. Workman, M.D. Garrett, and S. Mittnacht Mechanism-based screen for G1/S checkpoint activators identifies a selective activator of EIF2AK3/PERK signalling PLoS One 7 1 2012 e28568
58. C. Hetz, and L.H. Glimcher Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome Mol. Cell 35 5 2009 551 561
59. T. Shintani, and D.J. Klionsky Autophagy in health and disease: a double-edged sword Science 306 5698 2004 990 995
60. J.H. Lee, E.J. Kwon, and H. Kim do Calumenin has a role in the alleviation of ER stress in neonatal rat cardiomyocytes Biochem. Biophys. Res. Commun. 439 3 2013 327 332