Regulation of HA14-1 mediated oxidative stress, toxic response, and autophagy by curcumin to enhance apoptotic activity in human embryonic kidney cells

BioFactors

Volumn 40, Issue 1, 2014, Pages 157-169

  Ranjan, Kishu ^a   Sharma, Anupama ^a   Surolia, Avadhesha ^b   Pathak, Chandramani ^a  

^a Koba Institutional Area   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Apoptosis; Autophagy; Curcumin; Cytotoxicity; HA14 1; Oxidative stress; ROS

Indexed keywords

APOPTOSIS; AUTOPHAGY; CURCUMIN; CYTOTOXICITY; HA14-1; OXIDATIVE STRESS; ROS;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BENZOPYRANS; CASPASE 3; CATALASE; CELL PROLIFERATION; CELL SURVIVAL; CURCUMIN; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HEK293 CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NITRILES; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR RELA;

EID: 84894065670     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1098     Document Type: Article

References (42)

1. Tsuruo, T., Naito, M., Tomida, A., Fujita, N., Mashima, T., et al. (2003) Molecular targeting therapy of cancer: drug resistance, apoptosis and survival signal. Cancer Sci. 94, 15-21.
2. Dai, Y., Rahmani, M., Corey, S. J., Dent, P., and Grant, S. (2004) A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571) resistance is associated with altered expression of Bcl-2. J. Biol. Chem. 279, 34227-34239.
3. Lickliter, J. D., Wood, N. J., Johnson, L., McHugh, G., Tan, J., et al. (2003) HA14-1 selectively induces apoptosis in Bcl-2-overexpressing leukemia/lymphoma cells, and enhances cytarabine-induced cell death. Leukemia 17, 2074-2080.
4. Pei, X. Y., Dai, Y., and Grant, S. (2003) The proteasome inhibitor bortezomib promotes mitochondrial injury and apoptosis induced by the small molecule Bcl-2 inhibitor HA14-1 in multiple myeloma cells. Leukemia 17, 2036-2045.
5. Skommer, J., Wlodkowic, D., Matto, M., Eray, M., and Pelkonen, J. (2006) HA14-1, a small molecule Bcl-2 antagonist, induces apoptosis and modulates action of selected anticancer drugs in follicular lymphoma B cells. Leukemia Res. 30, 322-331.
6. An, J., Chen, Y., and Huang, Z. (2004) Critical upstream signals of cytochrome C release induced by a novel Bcl-2 inhibitor. J. Biol. Chem. 279, 19133-19140.
7. Manero, F., Gautier, F., Gallenne, T., Cauquil, N., Gree, D., et al. (2006) The small organic compound HA14-1 prevents Bcl-2 interaction with Bax to sensitize malignant glioma cells to induction of cell death. Cancer Res. 66, 2757-2764.
8. Milanesi, E., Costantini, P., Gambalunga, A., Colonna, R., Petronilli, V., et al. (2006) The mitochondrial effects of small organic ligands of BCL-2: sensitization of BCL-2-overexpressing cells to apoptosis by a pyrimidine-2, 4, 6-trione derivative. J. Biol. Chem. 281, 10066-10072.
9. Zhou, Y., Hileman, E. O., Plunkett, W., Keating, M.J., and Huang, P. (2003) Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents. Blood 101, 4098-4104.
10. Doshi, J. M., Tian, D., and Xing, C. (2007) Ethyl-2-amino-6-bromo-4-(1-cyano-2-ethoxy-2-oxoethyl)-4H- chromene-3-carboxylate (HA 14-1), a prototype small-molecule antagonist against antiapoptotic Bcl-2 proteins, decomposes to generate reactive oxygen species that induce apoptosis. Mol. Pharm. 4, 919-928.
11. Halliwell, B. (1997) Ascorbic acid: hype, hoax, or healer? Am J. Clin. Nutr. 65, 1891-1892.
12. Nakano, H., Nakajima, A., Sakon-Komazawa, S., Piao, J. H., Xue, X., et al. (2006) Reactive oxygen species mediate crosstalk between NF-kappaB and JNK. Cell Death Differ. 13, 730-737.
13. Ozben, T. (2007) Oxidative stress and apoptosis: impact on cancer therapy. J. Pharm. Sci. 96, 2181-2196.
14. Rushworth, S. A., Ogborne, R. M., Charalambos, C. A., and O'Connell, M. A. (2006) Role of protein kinase C delta in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochem. Biophys. Res. Commun. 341, 1007-1016.
15. Zhang, H. G., Kim, H., Liu, C., Yu, S., Wang, J., et al. (2007) Curcumin reverses breast tumor exosomes mediated immune suppression of NK cell tumor cytotoxicity. Biochim. Biophys. 1773, 1116-1123.
16. Ak, T. and Gulcin, I. (2008) Antioxidant and radical scavenging properties of curcumin. Chem. Biol. Interact. 174, 27-37.
17. Balasubramanyam, M., Koteswari, A. A., Kumar, R. S., Monickaraj, S. F., Maheswari, J. U., et al. (2003) Curcumin-induced inhibition of cellular reactive oxygen species generation: novel therapeutic implications. J. Biosci. 28, 715-721.
18. Daniel, S., Limson, J. L., Dairam, A., Watkins, G. M., and Daya, S. (2004) Through metal binding, curcumin protects against lead- and cadmium-induced lipid peroxidation in rat brain homogenates and against lead-induced tissue damage in rat brain. J. Inorg. Biochem. 98, 266-275.
19. Reddy, A. C. and Lokesh, B. R. (1996) Effect of curcumin and eugenol on iron-induced hepatic toxicity in rats. Toxicology 107, 39-45.
20. Chen, X., Zhong, Z., Xu, Z., Chen, L., and Wang, Y. (2011) No protective effect of curcumin on hydrogen peroxide-induced cytotoxicity in HepG2 cells. Pharmacol. Rep. 63, 724-732.
21. Barzegar, A. and Moosavi-Movahedi, A. A. (2011) Intracellular ROS protection efficiency and free radical-scavenging activity of curcumin. PloS One 6, e26012.
22. Beers, R. F., Jr. and Sizer, I. W. (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195, 133-140.
23. Marklund, S. and Marklund, G. (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47, 469-474.
24. Tian, D., Das, S. G., Doshi, J. M., Peng, J., Lin, J., et al. (2008) sHA 14-1, a stable and ROS-free antagonist against anti-apoptotic Bcl-2 proteins, bypasses drug resistances and synergizes cancer therapies in human leukemia cell. Cancer Lett. 259, 198-208.
25. Iqbal, M., Sharma, S. D., Okazaki, Y., Fujisawa, M., and Okada, S. (2003) Dietary supplementation of curcumin enhances antioxidant and phase II metabolizing enzymes in ddY male mice: possible role in protection against chemical carcinogenesis and toxicity. Pharmacol. Toxicol. 92, 33-38.
26. Reed, J. C. (1999) Mechanisms of apoptosis avoidance in cancer. Curr. Opin. Oncol. 11, 68-75.
27. Wang, J. L., Liu, D., Zhang, Z. J., Shan, S., Han, X., et al. (2000) Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc. Natl. Acad. Sci. USA 97, 7124-7129.
28. Reed, J. C. (1997) Bcl-2 family proteins: strategies for overcoming chemoresistance in cancer. Adv. Pharmacol. 41, 501-532.
29. Kessel, D., Castelli, M., and Reiners, J. J., Jr. (2002) Apoptotic response to photodynamic therapy versus the Bcl-2 antagonist HA14-1. Photochem. Photobiol. 76, 314-319.
30. Kessel, D. and Reiners, J.J., Jr. (2007) Initiation of apoptosis and autophagy by the Bcl-2 antagonist HA14-1. Cancer Lett. 249, 294-299.
31. Jia, Y. L., Li, J., Qin, Z. H., and Liang, Z. Q. (2009) Autophagic and apoptotic mechanisms of curcumin-induced death in K562 cells. J. Asian Nat. Prod. Res. 11, 918-928.
32. Juin, P., Geneste, O., Raimbaud, E., and Hickman, J. A. (2004) Shooting at survivors: Bcl-2 family members as drug targets for cancer. Biochim. Biophys. 1644, 251-260.
33. Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681.
34. Kunwar, A., Sandur, S. K., Krishna, M., and Priyadarsini, K. I. (2009) Curcumin mediates time and concentration dependent regulation of redox homeostasis leading to cytotoxicity in macrophage cells. Eur. J. Pharmacol. 611, 8-16.
35. Gao, X., Deeb, D., Jiang, H., Liu, Y. B., Dulchavsky, S. A., et al. (2005) Curcumin differentially sensitizes malignant glioma cells to TRAIL/Apo2L-mediated apoptosis through activation of procaspases and release of cytochrome c from mitochondria. J. Exp. Therapeut. Oncol. 5, 39-48.
36. Azmi, A. S., Wang, Z., Philip, P. A., Mohammad, R. M., and Sarkar, F. H. (2011) Emerging Bcl-2 inhibitors for the treatment of cancer. Exp. Opin. Emerg. Drugs 16, 59-70.
37. Muppidi, J. R., Tschopp, J., Siegel, R. M. (2004) Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 21, 461-465.
38. Reddy, N. and Czuczman, M. S. (2010) Enhancing activity and overcoming chemoresistance in hematologic malignancies with bortezomib: preclinical mechanistic studies. Ann. Oncol. 21, 1756-1764.
39. Chen, H. W., Yu, S. L., Chen, J. J., Li, H. N., Lin, Y. C., et al. (2004) Anti-invasive gene expression profile of curcumin in lung adenocarcinoma based on a high throughput microarray analysis. Mol. Pharmacol. 65, 99-110.
40. Green, D. R. and Kroemer, G. (2004) The pathophysiology of mitochondrial cell death. Science 305, 626-629.
41. Notte, A., Leclere, L., and Michiels, C. (2011) Autophagy as a mediator of chemotherapy-induced cell death in cancer. Biochem. Pharmacol. 82, 427-434.
42. Nyhan, M. J., O'Donovan, T. R., Elzinga, B., Crowley, L. C., O'Sullivan, G. C., et al (2012) The BH3 mimetic HA14-1 enhances 5-fluorouracil-induced autophagy and type II cell death in oesophageal cancer cells. Br. J. Cancer 106, 711-718.