Role of lipid peroxidation in cellular responses to d, l -sulforaphane, a promising cancer chemopreventive agent

Biochemistry

Volumn 49, Issue 14, 2010, Pages 3191-3202

  Sharma, Rajendra ^a   Sharma, Abha ^a   Chaudhary, Pankaj ^a   Pearce, Virginia ^b   Vatsyayan, Rit ^a   Singh, Shivendra V ^a   Awasthi, Sanjay ^a   Awasthi, Yogesh C ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-HYDROXY-NONENAL; ACQUIRED RESISTANCE; APOPTOSIS; APOPTOSIS INDUCTION; CANCER DEVELOPMENT; CELL-CYCLE ARREST; CELLULAR RESPONSE; CHEMOPREVENTIVE AGENTS; CYTOCHROME C; CYTOSOLS; ECTOPIC EXPRESSIONS; GROWTH ARREST; HUMAN CANCER CELLS; HUMAN LEUKEMIC CELLS; LIPID PEROXIDATION; NUCLEAR ACCUMULATION; NUCLEAR TRANSLOCATIONS; REACTIVE OXYGEN SPECIES; REGULATORY PROTEIN; SULFORAPHANE; SYNTHETIC ANALOGUES; TRANSGENIC MICE; UP-REGULATION;

CELL CULTURE; MAMMALS; OXIDATION; OXIDATIVE STRESS; OXYGEN; PLANTS (BOTANY); SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

CELL DEATH;

4 HYDROXYNONENAL; CYTOCHROME C; DAXX PROTEIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE TRANSFERASE A1; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; HUMAN GLUTATHIONE TRANSFERASE A1; PROTEIN BAX; PROTEIN BCL XL; REGULATOR PROTEIN; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL STRAIN HL 60; CELL STRAIN K 562; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; ENZYME RELEASE; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIPID PEROXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTICARCINOGENIC AGENTS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; CELL CYCLE; CELL NUCLEUS; CYTOSOL; DNA-BINDING PROTEINS; GLUTATHIONE TRANSFERASE; HL-60 CELLS; HUMANS; K562 CELLS; LIPID PEROXIDATION; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; PROTEIN TRANSPORT; THIOCYANATES; TRANSCRIPTION FACTORS; TRANSFECTION;

BRASSICA OLERACEA VAR. ITALICA; MUS MUSCULUS; RODENTIA;

EID: 77950633812     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100104e     Document Type: Article

References (53)

1. Juge, N., Mithen, R. F., and Traka, M. (2007) Molecular basis for chemoprevention by sulforaphane: A comprehensive review Cell. Mol. Life Sci. 64, 1105 - 1127 (Pubitemid 46684547)
2. Payrastre, G. L., Li, P., Lumeau, S., Cassar, G., Dupont, M. A., Chevolleau, S., Gasc, N., Tulliez, J., and Tercé, F. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells Cancer Res. 60, 1426 - 1433 (Pubitemid 30152017)
3. Singh, S. V., Herman-Antosiewicz, A., Singh., A. V., Lew, K. L., Srivastava, S. K., Kamath, R., Brown, K. D., Zhang, L., and Baskaran, R. (2004) Sulforaphane-induced G2/M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C J. Biol. Chem. 279, 25813 - 25822 (Pubitemid 38756846)
4. Singh, S. V., Srivastava, S. K., Choi, S., Lew, K. L., Antosiewicz, J., Xiao, D., Zeng, Y., Watkins, S. C., Johnson, C. S., Trump, D. L., Lee, Y. J., Xiao, H., and Herman-Antosiewicz, A. (2005) Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species J. Biol. Chem. 280, 19911 - 19924 (Pubitemid 41379520)
5. Xiao, D., Srivastava, S. K., Lew, K. L., Zeng, Y., Hershberger, P., Johnson, C. S., Trump, D. L., and Singh, S. V. (2003) Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits proliferation of human prostate cancer cells by causing G2/M arrest and inducing apoptosis Carcinogenesis 24, 891 - 897 (Pubitemid 36748905)
6. McWalter, G. K., Higgins, L. G., McLellan, L. I., Henderson, C. J., Song, L., Thornalley, P. J., Itoh, K., Yamamoto, M., and Hayes, J. D. (2004) Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates J. Nutr. 134, 3499S - 3506S (Pubitemid 39587596)
7. Zhang, Y. (2004) Cancer-preventive isothiocyanates: Measurement of human exposure and mechanism of action Mutat. Res. 555, 173 - 190 (Pubitemid 39345403)
8. Thimmulappa, R. K., Mai, K. H., Srisuma, S., Kensler, T. W., Yamamoto, M., and Biswal, S. (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray Cancer Res. 62, 5196 - 5203 (Pubitemid 35033454)
9. Yang, Y., Sharma, R., Sharma, A., Awasthi, S., and Awasthi, Y. C. (2003) Lipid peroxidation and cell cycle signaling: 4-Hydroxynonenal, a key molecule in stress mediated signaling Acta Biochim. Pol. 50, 319 - 336 (Pubitemid 37034689)
10. Cheng, J. Z., Singhal, S. S., Sharma, A., Saini, M., Yang, Y., Awasthi, S., Zimniak, P., and Awasthi, Y. C. (2001) Transfection of mGSTA4 in HL-60 cells protects against 4-hydroxynonenal-induced apoptosis by inhibiting JNK-mediated signaling Arch. Biochem. Biophys. 392, 197 - 207 (Pubitemid 32757030)
11. Cheng, J. Z., Singhal, S. S., Saini, M., Singhal, J., Piper, J. T., Van Kuijk, F. J., Zimniak, P., Awasthi, Y. C., and Awasthi, S. (1999) Effects of mGST A4 transfection on 4-hydroxynonenal-mediated apoptosis and differentiation of K562 human erythroleukemia cells Arch. Biochem. Biophys. 372, 29 - 36
12. Sharma, R., Brown, D., Awasthi, S., Yang, Y., Sharma, A., Patrick, B., Saini, M. K., Singh, S. P., Zimniak, P., Singh, S. V., and Awasthi, Y. C. (2004) Transfection with 4-hydroxynonenal-metabolizing glutathione S-transferase isozymes leads to phenotypic transformation and immortalization of adherent cells Eur. J. Biochem. 271, 1690 - 1701 (Pubitemid 38586301)
13. Awasthi, Y. C., Sharma, R., Sharma, A., Yadav, S., Singhal, S. S., Chaudhary, P., and Awasthi, S. (2008) Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death Free Radical Biol. Med. 45, 111 - 118
14. Yang, Y., Sharma, R., Cheng, J. Z., Saini, M. K., Ansari, N. H., Andley, U. P., Awasthi, S., and Awasthi, Y. C. (2002) Protection of HLE B-3 cells against hydrogen peroxide- and naphthalene-induced lipid peroxidation and apoptosis by transfection with hGSTA1 and hGSTA2 Invest. Ophthalmol. Visual Sci. 43, 434 - 445 (Pubitemid 34113226)
15. Yang, Y., Cheng, J. Z., Singhal, S. S., Saini, M., Pandya, U., Awasthi, S., and Awasthi, Y. C. (2001) Role of glutathione S-transferases in protection against lipid peroxidation: Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide induced apoptosis and inhibits JNK and caspase 3 activation J. Biol. Chem. 276, 19220 - 19230 (Pubitemid 37411254)
16. Yang, Y., Sharma, A., Sharma, R., Patrick, B., Singhal, S. S., Zimniak, P., Awasthi, S., and Awasthi, Y. C. (2003) Cells preconditioned with mild, transient UVA irradiation acquire resistance to oxidative stress and UVA-induced apoptosis: Role of 4-hydroxynonenal in UVA-mediated signaling for apoptosis J. Biol. Chem. 278, 41380 - 41388 (Pubitemid 37280967)
17. Sharma, A., Patrick, B., Li, J., Sharma, R., Jeyabal, P. V. S., Reddy, P. M. R. V., Awasthi, S., and Awasthi, Y. C. (2006) Glutathione S-transferases as antioxidant enzymes: Small cell lung cancer (H69) cells transfected with hGSTA1 resist doxorubicin-induced apoptosis Arch. Biochem. Biophys. 452, 165 - 173 (Pubitemid 44175345)
18. Li, J., Sharma, R., Patrick, B., Sharma, A., Jeyabal, P. V., Reddy, P. M., Saini, M. K., Dwivedi, S., Dhanani, S., Ansari, N. H., Zimniak, P., Awasthi, S., and Awasthi, Y. C. (2006) Regulation of CD95 (Fas) expression and Fas-mediated apoptotic signaling in HLE B-3 cells by 4-hydroxynonenal Biochemistry 45, 12253 - 12264 (Pubitemid 44527548)
19. Sharma, R., Sharma, A., Dwivedi, S., Zimniak, P., Awasthi, S., and Awasthi, Y. C. (2008) 4-Hydroxynonenal self-limits Fas-mediated DISC-independent apoptosis by promoting export of Daxx from the nucleus to the cytosol and its binding to Fas Biochemistry 47, 143 - 156
20. Chen, Z. H., Saito, Y., Yoshida, Y., Sekine, A., Noguchi, N., and Niki, E. (2005) 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2 J. Biol. Chem. 280, 41921 - 41927 (Pubitemid 43023161)
21. Jacobs, A. T. and Marnett, L. J. (2009) HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins J. Biol. Chem. 284, 9176 - 9183
22. Jacobs, A. T. and Marnett, L. J. (2007) Heat shock factor 1 attenuates 4-hydroxynonenal-mediated apoptosis: Critical role for heat shock protein 70 induction and stabilization of Bcl-xL J. Biol. Chem. 282, 33412 - 33420
23. Zhao, T., Singhal, S. S., Piper, J. T., Cheng, J., Pandya, U., Clark-Wronski, J., Awasthi, S., and Awasthi, Y. C. (1999) The role of human glutathione S-transferases hGSTA1-1 and hGSTA2-2 in protection against oxidative stress Arch. Biochem. Biophys. 367, 216 - 224 (Pubitemid 29394168)
24. Koeffler, H. P. and Golde, D. W. (1980) Human myeloid leukemic cell lines: A review Blood 56, 344 - 350 (Pubitemid 11251010)
25. Singhal, S. S., Saxena, M., Ahmad, H., Awasthi, S., Haque, A. K., and Awasthi, Y. C. (1992) Glutathione S-transferases of human lung: Characterization and evaluation of the protective role of the α-class isozymes against lipid peroxidation Arch. Biochem. Biophys. 299, 232 - 241 (Pubitemid 23029025)
26. Habig, W. H., Pabst, M. J., and Jakoby, W. B. (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation J. Biol. Chem. 249, 7130 - 7139
27. Kolm, R. H., Danielson, U. H., Zhang, Y., Talalay, P., and Mannervik, B. (1995) Isothiocyanates as substrates for human glutathione transferases: Structure-activity studies Biochem. J. 311, 453 - 459
28. Awasthi, Y. C., Beutler, E., and Srivastava, S. K. (1975) Purification and properties of human erythrocyte glutathione peroxidase J. Biol. Chem. 250, 5144 - 5149
29. Carlberg, I. and Mannervik, B. (1985) Glutathione reductase Methods Enzymol. 113, 484 - 490 (Pubitemid 16195819)
30. Seelig, G. F. and Meister, A. (1984) γ-Glutamylcysteine synthetase. Interactions of an essential sulfhydryl group J. Biol. Chem. 259, 3534 - 3538 (Pubitemid 14170081)
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248 - 254
32. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227, 680 - 685
33. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications Proc. Natl. Acad. Sci. U.S.A. 76, 4350 - 4354 (Pubitemid 9256559)
34. Englander, E. W., Hu, Z., Sharma, A., Lee, H. M., Wu, Z. H., and Greeley, G. H. (2002) Rat MYH, a glycosylase for repair of oxidatively damaged DNA, has brain-specific isoforms that localize to neuronal mitochondria J. Neurochem. 83, 1471 - 1480 (Pubitemid 35477486)
35. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays J. Immunol. Methods 65, 55 - 63 (Pubitemid 14203433)
36. Beutler, E. (1984) Red Cell Metabolism. In A Manual of Biochemical Methods, Grune and Stratton, Orlando, FL.
37. Takizawa, C. G. and Morgan, D. O. (2000) Control of mitosis by changes in the subcellular location of cyclin-B1-Cdk1 and Cdc25C Curr. Opin. Cell Biol. 12, 658 - 665
38. Snchez, I. and Dynlacht, B. D. (2005) New insights into cyclins, CDKs, and cell cycle control Semin. Cell Dev. Biol. 16, 311 - 321 (Pubitemid 40504220)
39. Kaufmann, T., Schinzel, A., and Borner, C. (2004) Bcl-w(edding) with mitochondria Trends Cell Biol. 14, 8 - 12 (Pubitemid 38076855)
40. Ganju, N. and Eastman, A. (2002) Bcl-X(L) and calyculin A prevent translocation of Bax to mitochondria during apoptosis Biochem. Biophys. Res. Commun. 291, 1258 - 1264 (Pubitemid 34694325)
41. Candé, C., Cohen, I., Daugas, E., Ravagnan, L., Larochette, N., Zamzami, N., and Kroemer, G. (2002) Apoptosis-inducing factor (AIF): A novel caspase-independent death effector released from mitochondria Biochimie 84, 215 - 222
42. Lorenzo, H. K., Susin, S. A., Penninger, J., and Kroemer, G. (1999) Apoptosis inducing factor (AIF): A phylogenetically old, caspase-independent effector of cell death Cell Death Differ. 6, 516 - 524 (Pubitemid 29292107)
43. Kwak, M. K., Itoh, K., Yamamoto, M., Sutter, T. R., and Kensler, T. W. (2001) Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1,2-dimethiole-3-thione Mol. Med. 7, 135 - 145 (Pubitemid 33702029)
44. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proc. Natl. Acad. Sci. U.S.A. 99, 11908 - 11913 (Pubitemid 34994497)
45. Dai, C., Whitesell, L., Rogers, A. B., and Lindquist, S. (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis Cell 130, 1005 - 1118 (Pubitemid 47410269)
46. Nollen, E. A. and Morimoto, R. I. (2002) Chaperoning signaling pathways: Molecular chaperones as stress-sensing 'heat shock' proteins J. Cell Sci. 115, 2809 - 2816
47. Salomoni, P. and Khelifi, A. F. (2006) Daxx: Death or survival protein? Trends Cell Biol. 16, 97 - 104 (Pubitemid 43247405)
48. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radical Biol. Med. 11, 81 - 128 (Pubitemid 121003917)
49. Barrera, G., Pizzimenti, S., Muraca, R., Barbiero, G., Bonelli, G., Baccino, F. M., Fazio, V. M., and Dianzani, M. U. (1996) Effect of 4-hydroxynonenal on cell cycle progression and expression of differentiation-associated antigens in HL-60 cells Free Radical Biol. Med. 20, 455 - 462 (Pubitemid 26077869)
50. Awasthi, Y. C., Sharma, R., Cheng, J. Z., Yang, Y., Sharma, A., Singhal, S. S., and Awasthi, S. (2003) Role of 4-hydroxynonenal in stress-mediated apoptosis signaling Mol. Aspects Med. 24, 219 - 230 (Pubitemid 36945022)
51. Jackson, S. J. T. and Singletary, K. W. (2004) Sulforaphane inhibits human MCF-7 mammary cancer cell mitotic progression and tubulin polymerization J. Nutr. 134, 2229 - 2236
52. Dashwood, R. H. and Ho, E. (2007) Dietary histone deacetylase inhibitors: From cells to mice to man Semin. Cancer Biol. 17, 363 - 369 (Pubitemid 47369168)
53. Joza, N., Susin, S. A., Daugas, E., Stanford, W. L., Cho, S. K., Li, C. Y., Sasaki, T., Elia, A. J., Cheng, H. Y., Ravagnan, L., Ferri, K. F., Zamzami, N., Wakeham, A., Hakem, R., Yoshida, H., Kong, Y. Y., Mak, T. W., Ziga-Pflücker, J. C., Kroemer, G., and Penninger, J. M. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death Nature 410, 549 - 554 (Pubitemid 32267191)