Withaferin A induced impaired autophagy and unfolded protein response in human breast cancer cell-lines MCF-7 and MDA-MB-231

Toxicology in Vitro

Volumn 44, Issue , 2017, Pages 330-338

  Ghosh, Kamalini ^a   De, Soumasree ^a   Mukherjee, Srimoyee ^a   Das, Sayantani ^a   Ghosh, Amar Nath ^b  

^a Bandyopadhyay)   (India)

^b NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

Author keywords

Breast cancer; ER stress; Incomplete autophagy; Ubiquitine proteasome system; Unfolded protein response

Indexed keywords

AUTOPHAGY RELATED PROTEIN 12; AUTOPHAGY RELATED PROTEIN 5; BECLIN 1; CASPASE 4; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 2 LIGHT CHAIN 3; SEQUESTOSOME 1; TUBULIN; UNCLASSIFIED DRUG; WITHAFERIN A; WORTMANNIN; X BOX BINDING PROTEIN 1; DDIT3 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; LIGHT CHAIN 3, HUMAN; MAP1LC3A PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; MOLECULAR CHAPERONE GRP78; WITHANOLIDE; XBP1 PROTEIN, HUMAN;

ACIDIC VESICULAR ORGANELLE; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL ORGANELLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; MCF-7 CELL LINE; MDA-MB-231 CELL LINE; MICROTUBULE; MICROTUBULE ASSEMBLY; PROTEIN ACETYLATION; PROTEIN DEGRADATION; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; BREAST TUMOR; DRUG EFFECT; LYSOSOME; METABOLISM; TUMOR CELL LINE;

AUTOPHAGY; BREAST NEOPLASMS; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM STRESS; HEAT-SHOCK PROTEINS; HUMANS; LYSOSOMES; MICROTUBULE-ASSOCIATED PROTEINS; TRANSCRIPTION FACTOR CHOP; UNFOLDED PROTEIN RESPONSE; WITHANOLIDES; X-BOX BINDING PROTEIN 1;

EID: 85026892123     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2017.07.025     Document Type: Article

References (50)

1. 4Cl. Exp. Cell Res. 126 (1980), 167–174.
2. Amenta, J.S., Hlivko, T.J., Mcbee, A.G., Shinozuka, H., Brocher, S., Specific inhibition by NH4Cl of autophagy-associated proteolysis in cultured fibroblasts. Exp. Cell Res. 115 (1978), 357–366.
3. Antony, M.L., Lee, J., Hahm, E.R., Kim, S.H., et al., Growth arrest by the antitumor steroidal lactone Withaferin A in human breast cancer cells is associated with down-regulation and covalent binding at cysteine 303 of β-tubulin. J. Biol. Chem. 289 (2013), 1852–1865.
4. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Øvervatn, A., Stenmark, H., Johansen, T., p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171 (2005), 603–614.
5. Bonet-Ponce, L., Saez-Atienzar, S., Casa da, C., Sancho-Pelluz, J., et al., Rotenone induces the formation of 4-Hydroxynonenal aggresomes. Role of ROS-mediated tubulin hyperactylation and autophagic flux disruption. Mol. Neurobiol., 2015.
6. Castoldi, M., Popov, A.V., Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr. Purif. 32 (2003), 83–88.
7. Choi, M.J., Park, E.J., Min, K.J., Park, J.W., Kwon, T.K., Endoplasmic reticulum stress mediates Withaferin A-induced apoptosis in human renal carcinoma cells. Toxicol. in Vitro 25 (2013), 692–698.
8. Ciechanover, A., Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Bioorg. Med. Chem. 21 (2013), 3400–3410.
9. Ciechanover, A., Orian, A., Schwartz, A.L., Ubiquitin-mediated proteolysis: biological regulation via destruction. BioEssays 22 (2000), 442–451.
10. Codogno, P., Mehrpour, M., Proikas-Cezanne, T., Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat. Rev. Mol. Cell Biol. 13 (2011), 7–12.
11. Das, G., Shravage, B.V., Baehrecke, E.H., Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb. Perspect. Biol., 4, 2012 (pii: a008813).
12. Dasgupta, P., Bandyopadhyay, S.S., Role of di-allyl disulfide, a garlic component in NF-κB mediated transient G2-M phase arrest and apoptosis in human leukemic cell-lines. Nutr. Cancer 65 (2013), 611–622.
13. Gao, Z., Gammoh, N., Wong, P.M., Erdjument-Bromage, H., Tempst, P., Jiang, X., Processing of autophagic protein LC3 by the 20S proteasome. Autophagy 6 (2010), 126–137.
14. Ghosh, K., De, S., Das, S., Mukherjee, S., Sengupta, Bandyopadhyay S., Withaferin A induces ROS-mediated paraptosis in human breast cancer cell-lines MCF-7 and MDA-MB-231. PLoS One, 11e0168488, 2016.
15. Grover, A., Shandilya, A., Bisaria, V.S., Sundar, D., Probing the anticancer mechanism of prospective herbal drug Withaferin A on mammals: a case study on human and bovine proteasomes. BMC Genomics, 11, 2010.
16. Hahm, E.R., Singh, S.V., Autophagy fails to alter Withaferin A-mediated lethality in human breast cancer cell lines. Curr. Cancer Drug Targets 13 (2013), 640–650.
17. Hoyer-Hansen, M., Jaattela, M., Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14 (2007), 1576–1582.
18. Igney, F.H., Krammer, P.H., Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2 (2002), 277–288.
19. Jordan, M.A., Thrower, D., Wilson, L., Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis. J. Cell Sci. 102 (1992), 401–416.
20. Katayama, H., Yamamoto, A., Mizushima, N., Yoshimori, T., Miyawaki, A., GFP-like proteins stably accumulate in lysosomes. Cell Struct. Funct. 33 (2008), 1–12.
21. Kaur, J., Debnath, J., Autophagy at the crossroads of catabolism and anabolism. Nat. Rev. Mol. Cell Biol. 16 (2015), 461–472.
22. Khan, S., Rammeloo, A.W., Heikkila, J.J., Withaferin A induces proteasome inhibition, endoplasmic reticulum stress, the heat shock response and acquisition of thermotolerance. PLoS One, 7, 2007, e50547.
23. Kirkin, V., McEwan, D.G., Novak, I., Dikic, I., A role for ubiquitin in selective autophagy. Mol. Cell 34 (2009), 259–269.
24. Klionsky et al, Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 8 (2012), 445–544.
25. Kochl, R., Hu, X.W., Chan, E.Y., Tooze, S.A., Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 7 (2006), 129–145.
26. Korolchuk, V.I., Mansilla, A., Menzies, F.M., Rubinsztein, D.C., Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol. Cell 33 (2009), 517–527.
27. Korolchuk, V.I., Menzies, F.M., Rubinsztein, D.C., Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 584 (2010), 1393–1398.
28. Liu, B., Wen, X., Cheng, Y., Survival or death: disequilibrating the oncogenic and tumor suppressive autophagy in cancer. Cell Death Dis., 4, 2013, e892.
29. Liu, D., Gao, M., Yang, Y., Qi, Y., Wu, K., Zhao, S., Inhibition of autophagy promotes cell apoptosis induced by proteasome inhibitor MG-132 in human esophageal squamous cell carcinoma EC9706 cells. Oncol. Lett. 9 (2015), 2278–2282.
30. Livesey, K.M., Tang, D., Zeh, H.J., Lotze, M.T., Autophagy inhibition in combination cancer treatment. Curr. Opin. Investig. Drugs 10 (2009), 1269–1279.
31. Logue, S.E., Cleary, P., Saveljeva, S., Samali, A., New directions in ER stress-induced cell death. Apoptosis 18 (2013), 537–546.
32. Low, P., Varga, A., Pircs, K., Nagy, P., et al., Impaired proteasomal degradation enhances autophagy via hypoxia signalling in drosophila. BMC Cell Biol., 14, 2013, 29.
33. Martens, S., Bachmair, A., How cells coordinate waste removal through their major proteolytic pathways. Nat. Cell Biol. 17 (2015), 841–842.
34. Mizushima, N., Yoshimorim, T., Levine, B., Methods in mammalian autophagy research. Cell 140 (2010), 313–326.
35. Noh, H.J., Lee, S.J., Sung, E.G., Song, I.H., Kim, J.Y., Woo, C.H., Kwon, T.K., Lee, T.J., CHOP down-regulates cFLIP(L) expression by promoting ubiquitin/proteasome-mediated cFLIP(L) degradation. J. Cell. Biochem. 113 (2012), 3692–3700.
36. Rastogi, N., Mishra, D.P., Therapeutic targeting of cancer cell cycle using proteasome inhibitors. Cell Div 7 (2012), 26–35.
37. Rippe, R.A., Brenner, D.A., Leffert, H.L., DNA-mediated gene transfer into adult rat hepatocytes in primary culture. Mol. Cell. Biol. 10 (1990), 689–695.
38. Saha, S., Chakraborty, A., Bandyopadhyay, S.S., Stabilization of Oncostatin-M mRNA by binding of nucleolin to a GC-rich element in its 3′UTR. J. Cell. Biochem. 117 (2016), 988–999.
39. Shen, M., Schmitt, S., Buac, D., Dou, Q.P., Targeting the ubiquitin-proteasome system for cancer therapy. Expert Opin. Ther. Targets 17 (2013), 1091–1108.
40. Sui, X., Chen, R., Wang, Z., Huang, Z., et al., Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis., 4, 2013, e838.
41. Tu, Y., Chen, C., Pan, J., Xu, J., Zhou, Z.G., Wang, C.Y., The ubiquitin proteasome pathway (UPP) in the regulation of cell cycle control and DNA damage repair and its implication in tumorigenesis. Int. J. Clin. Exp. Pathol. 5 (2012), 726–738.
42. VandenBerghe, W., Sabbe, L., Kaileh, M., Haegeman, G., Heyninck, K., Molecular insight in the multifunctional activities of WithaferinA. Biochem. Pharmacol. 84 (2012), 1282–1291.
43. Vyas, A.R., Singh, S.V., Molecular targets and mechanisms of cancer prevention and treatment by withaferina, a naturally occurring steroidal lactone. AAPS J. 16 (2014), 1–10.
44. Wang, C., Wang, X., The interplay between autophagy and the ubiquitin-proteasome system in cardiac proteotoxicity. Biochim. Biophys. Acta 1852 (2015), 188–194.
45. Weihl, C.C., Monitoring autophagy in the treatment of protein aggregate diseases: steps toward identifying autophagic biomarkers. Neurotherapeutics 10 (2013), 383–390.
46. White, E., The role for autophagy in cancer. J. Clin. Invest. 125 (2015), 42–46.
47. Yamamoto, K., Sato, T., Matsui, T., Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 13 (2007), 365–376.
48. Yang, H., Shi, G., Dou, Q.P., Thetumor proteasome is a primary target for the natural anticancer compound Withaferin a isolated from “Indian winter cherry”. Mol. Pharmacol. 7 (2007), 426–437.
49. Yang, H., Wang, Y., Cheryan, V.T., Wu, W., Withaferin A inhibits the proteasome activity in mesothelioma in vitro and in vivo. PLoS One, 7, 2012, e41214.
50. Zhang, Y., Xu, M., Xia, M., Li, X., et al., Defective autophagosome trafficking contributes to impaired autophagic flux in coronary arterial myocytes lacking CD38gene. Cardiovasc. Res. 102 (2014), 68–78.