Benzyl isothiocyanate causes FoxO1-mediated autophagic death in human breast cancer cells

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Xiao, Dong ^a   Bommareddy, Ajay ^b   Kim, Su Hyeong ^a   Sehrawat, Anuradha ^a   Hahm, Eun Ryeong ^a   Singh, Shivendra V ^a,c  

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

^b WILKES UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLADENINE; ACRIDINE ORANGE; BAFILOMYCIN A1; BENZYL ISOTHIOCYANATE; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MANGANESE SUPEROXIDE DISMUTASE; MICROTUBULE ASSOCIATED PROTEIN 1; ONCOPROTEIN; PROTEIN P62; RHEB PROTEIN; S6 KINASE; SEQUESTOSOME 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; ISOTHIOCYANIC ACID DERIVATIVE; MTOR PROTEIN, HUMAN; SUPEROXIDE DISMUTASE; TARGET OF RAPAMYCIN KINASE;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CANCER INHIBITION; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; LIGHT CHAIN; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; STABLE EXPRESSION; TRANSIENT EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; ANIMAL; BREAST TUMOR; CELL LINE; DRUG EFFECT; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

MUS;

ACETYLATION; ANIMALS; AUTOPHAGY; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; ISOTHIOCYANATES; MICE; SUPEROXIDE DISMUTASE; TOR SERINE-THREONINE KINASES; TRANSPLANTATION, HETEROLOGOUS;

EID: 84863360319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032597     Document Type: Article

References (39)

1. Jemal A, Siegel R, Xu J, Ward E, (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
2. Kelsey JL, Gammon MD, John EM, (1993) Reproductive factors and breast cancer. Epidemiol Rev 15: 36-47.
3. Hulka BS, Stark AT, (1995) Breast cancer: cause and prevention. Lancet 346: 883-887.
4. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, et al. (1998) Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 90: 1371-1388.
5. Obiorah I, Jordan VC, (2011) Progress in endocrine approaches to the treatment and prevention of breast cancer. Maturitas 70: 315-321.
6. Wattenberg LW, (1977) Inhibition of carcinogenic effects of polycyclic hydrocarbons by benzyl isothiocyanate and related compounds. J Natl Cancer Inst 58: 395-398.
7. Zhang Y, Tang L, Gonzalez V, (2003) Selected isothiocyanates rapidly induce growth inhibition of cancer cells. Mol Cancer Ther 2: 1045-1052.
8. Tseng E, Scott-Ramsay EA, Morris ME, (2004) Dietary organic isothiocyanates are cytotoxic in human breast cancer MCF-7 and mammary epithelial MCF-12A cell lines. Exp Biol Med 229: 835-842.
9. Xiao D, Vogel V, Singh SV, (2006) Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol Cancer Ther 5: 2931-2945.
10. Warin R, Xiao D, Arlotti JA, Bommareddy A, Singh SV, (2010) Inhibition of human breast cancer xenograft growth by cruciferous vegetable constituent benzyl isothiocyanate. Mol Carcinog 49: 500-507.
11. Warin R, Chambers WH, Potter DM, Singh SV, (2009) Prevention of mammary carcinogenesis in MMTV-neu mice by cruciferous vegetable constituent benzyl isothiocyanate. Cancer Res 69: 9473-9480.
12. Fowke JH, Chung FL, Jin F, Qi D, Cai Q, et al. (2003) Urinary isothiocyanate levels, brassica, and human breast cancer. Cancer Res 63: 3980-3986.
13. Ambrosone CB, McCann SE, Freudenheim JL, Marshall JR, Zhang Y, et al. (2004) Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 134: 1134-1138.
14. Xiao D, Powolny AA, Singh SV, (2008) Benzyl isothiocyanate targets mitochondrial respiratory chain to trigger reactive oxygen species-dependent apoptosis in human breast cancer cells. J Biol Chem 283: 30151-30163.
15. Kim SH, Singh SV, (2010) p53-Independent apoptosis by benzyl isothiocyanate in human breast cancer cells is mediated by suppression of XIAP expression. Cancer Prev Res 3: 718-726.
16. Kim SH, Nagalingam A, Saxena NK, Singh SV, Sharma D, (2011) Benzyl isothiocyanate inhibits oncogenic actions of leptin in human breast cancer cells by suppressing activation of signal transducer and activator of transcription 3. Carcinogenesis 32: 359-367.
17. Gibson SB, (2010) A matter of balance between life and death: targeting reactive oxygen species (ROS)-induced autophagy for cancer therapy. Autophagy 6: 835-837.
18. Chen N, Karantza V, (2011) Autophagy as a therapeutic target in cancer. Cancer Biol Ther 11: 157-168.
19. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4: 151-175.
20. Iwamaru A, Kondo Y, Iwado E, Aoki H, Fujiwara K, et al. (2007) Silencing mammalian target of rapamycin signaling by small interfering RNA enhances rapamycin-induced autophagy in malignant glioma cells. Oncogene 26: 1840-1851.
21. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
22. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, et al. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171: 603-614.
23. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
24. Bai X, Ma D, Liu A, Shen X, Wang QJ, et al. (2007) Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318: 977-980.
25. Zhao Y, Yang J, Liao W, Liu X, Zhang H, et al. (2010) Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 12: 665-675.
26. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, et al. (2008) Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 10: 676-687.
27. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, et al. (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117: 326-336.
28. Herman-Antosiewicz A, Johnson DE, Singh SV, (2006) Sulforaphane causes autophagy to inhibit release of cytochrome c and apoptosis in human prostate cancer cells. Cancer Res 66: 5828-5835.
29. Kanzawa T, Kondo Y, Ito H, Kondo S, Germano I, (2003) Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res 63: 2103-2108.
30. Demasters G, Di X, Newsham I, Shiu R, Gewirtz DA, (2006) Potentiation of radiation sensitivity in breast tumor cells by the vitamin D3 analogue, EB 1089, through promotion of autophagy and interference with proliferative recovery. Mol Cancer Ther 5: 2786-2797.
31. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB, (2008) Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 15: 171-182.
32. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB, (2007) Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci 120: 4155-4166.
33. Scherz-Shouval R, Shvets E, Elazar Z, (2007) Oxidation as a post-translational modification that regulates autophagy. Autophagy 3: 371-373.
34. Sarbassov DD, Ali SM, Sabatini DM, (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603.
35. Chiang GG, Abraham RT, (2007) Targeting the mTOR signaling network in cancer. Trends Mol Med 13: 433-442.
36. Arden KC, (2007) FOXOs in tumor suppression and stem cell maintenance. Cell 128: 235-237.
37. Xiao D, Choi S, Johnson DE, Vogel VG, Johnson CS, et al. (2004) Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene 23: 5594-5606.
38. Xiao D, Srivastava SK, Lew KL, Zeng Y, Hershberger P, et al. (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.
39. Singh SV, Powolny AA, Stan SD, Xiao D, Arlotti JA, et al, (2008) Garlic constituent diallyl trisulfide prevents development of poorly differentiated prostate cancer and pulmonary metastasis multiplicity in TRAMP mice. Cancer Res 68: 9503-9511.