Dietary chemopreventative benzyl isothiocyanate inhibits breast cancer stem cells in vitro and in vivo

Cancer Prevention Research

Volumn 6, Issue 8, 2013, Pages 782-790

  Kim, Su Hyeong ^a   Sehrawat, Anuradha ^a   Singh, Shivendra V ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; BENZYL ISOTHIOCYANATE; BIOLOGICAL MARKER; CARCINOGEN; CD24 ANTIGEN; EPITHELIAL SPECIFIC ANTIGEN 1; HERMES ANTIGEN; MACROPHAGE STIMULATING PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN; RNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER INHIBITION; CANCER PREVENTION; CANCER STEM CELL; CELL LYSATE; CELL STRAIN MCF 7; CONTROLLED STUDY; DIETARY INTAKE; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEPIDIUM SATIVUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUMOR CELL; TUMOR XENOGRAFT; VEGETABLE; WESTERN BLOTTING;

EID: 84883828864     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-13-0100     Document Type: Article

References (44)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
2. Higgins MJ, Baselga J. Breast cancer in 2010: novel targets and therapies for a personalized approach. Nat Rev Clin Oncol 2011;8:65-6.
3. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel project P-1 Study. J Natl Cancer Inst 1998;90:1371-88. (Pubitemid 28439961)
4. Cauley JA, Norton L, Lippman ME, Eckert S, Krueger KA, Purdie DW, et al. Continued breast cancer risk reduction in postmenopausal women treated with raloxifene: 4-year results from the MORE trial: multiple outcomes of raloxifene evaluation. Breast Cancer Res Treat 2001;65:125-34. (Pubitemid 32193616)
5. Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, et al. Exemestane for breast-cancer prevention in postmenopausal women. N Eng J Med 2011;364:2381-91.
6. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003;3:768-80.
7. Stan SD, Kar S, Stoner GD, Singh SV. Bioactive food components and cancer risk reduction. J Cell Biochem 2008;104:339-56.
8. Wattenberg LW. Inhibition of carcinogenic effects of polycyclic hydrocarbons by benzyl isothiocyanate and related compounds. J Natl Cancer Inst 1977;58:395-8. (Pubitemid 8042532)
9. Warin R, Chambers WH, Potter DM, Singh SV. Prevention of mammary carcinogenesis in MMTV-neu mice by cruciferous vegetable constituent benzyl isothiocyanate. Cancer Res 2009;69:9473-80.
10. Warin R, Xiao D, Arlotti JA, Bommareddy A, Singh SV. Inhibition of human breast cancer xenograft growth by cruciferous vegetable constituent benzyl isothiocyanate. Mol Carcinogenesis 2010;49:500-7.
11. Xiao D, Vogel V, Singh SV. Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol Cancer Ther 2006;5:2931-45. (Pubitemid 44849021)
12. Xiao D, Powolny AA, Singh SV. Benzyl isothiocyanate targets mitochondrial respiratory chain to trigger reactive oxygen species-dependent apoptosis in human breast cancer cells. J Biol Chem 2008;283:30151-63.
13. Xiao D, Bommareddy A, Kim SH, Sehrawat A, Hahm ER, Singh SV. Benzyl isothiocyanate causes FoxO1-mediated autophagic death in human breast cancer cells. PLoS One 2012;7:e32597.
14. Antony ML, Kim SH, Singh SV. Critical role of p53 upregulated modulator of apoptosis in benzyl isothiocyanate-induced apoptotic cell death. PLoS One 2012;7:e32267.
15. Oliveira LR, Jeffrey SS, Rebeiro-Silva A. Stem cells in human breast cancer. Histol Histopathol 2010;25:371-85.
16. Velasco-Velázquez MA, Homsi N, De La Fuente M, Pestell RG. Breast cancer stem cells. Int J Biochem Cell Biol 2012;44:573-7.
17. O'Brien CS, Farnie G, Howell SJ, Clarke RB. Breast cancer stem cells and their role in resistance to endocrine therapy. Horm Cancer 2011;2:91-103.
18. Raimondi C, Gradilone A, Naso G, Vincenzi B, Petracca A, Nicolazzo C, et al. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat 2011;130:449-55.
19. Dave B, Mittal V, Tan NM, Chang JC. Epithelial-mesenchymal transition, cancer stem cells, and treatment resistance. Breast Cancer Res 2012;14:202.
20. Velasco-Velázquez MA, Popov VM, Lisanti MP, Pestell RG. The role of breast cancer stem cells in metastasis and therapeutic implications. Am J Pathol 2011;179:2-11.
21. Sehrawat A, Singh SV. Benzyl isothiocyanate inhibits epithelial- mesenchymal transition in cultured and xenografted human breast cancer cells. Cancer Prev Res 2011;4:1107-17.
22. Sehrawat A, Kim SH, Vogt A, Singh SV. Suppression of FOXQ1 in benzyl isothiocyanate-mediated inhibition of epithelial-mesenchymal transition in human breast cancer cells. Carcinogenesis 2013;34:864-73.
23. Jo M, Eastman BM, Webb DL, Stoletov K, Klemke R, Gonias SL. Cell signaling by urokinase-type plasminogen activator receptor induces stem cell-like properties in breast cancer cells. Cancer Res 2010;70:8948-58.
24. Liu X, Zhao L, Derose YS, Lin YC, Bieniasz M, Eyob H, et al. Short-form Ron promotes spontaneous breast cancer metastasis through interaction with phosphoinositide 3-kinase. Genes Cancer 2011;2:753-62.
25. Li Y, Zhang T, Korkaya H, Liu S, Lee HF, Newman B, et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 2010;16:2580-90.
26. Liao MJ, Zhang CC, Zhou B, Zimonjic DB, Mani SA, Kaba M, et al. Enrichment of a population of mammary gland cells that form mammosphere and have in vivo repopulating activity. Cancer Res 2007;67:8131-8. (Pubitemid 47395148)
27. Xiao D, Srivastava SK, Lew KL, Zeng Y, Hershberger P, Johnson CS, et al. Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits proliferation of human prostate cancer cells by causing G2/M arrest and inducing apoptosis. Carcinogenesis 2003;24:891-7. (Pubitemid 36748905)
28. Powolny AA, Bommareddy A, Hahm ER, Normolle DP, Beumer JH, Nelson JB, et al. Chemopreventative potential of the cruciferous vegetable constituent phenethyl isothiocyanate in a mouse model of prostate cancer. J Natl Cancer Inst 2011;103:571-84.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔT method. Methods 2001;25:402-8. (Pubitemid 34164012)
30. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009;138:1083-95.
31. Lester RD, Jo M, Montel V, Takimoto S, Gonias SL. uPAR induces epithelial-mesenchymal transition in hypoxic breast cancer cells. J Cell Biol 2007;178:425-36. (Pubitemid 47196151)
32. Bardella C, Costa B, Maggiora P, Patane' S, Olivero M, Ranzani GN, et al. Truncated RON tyrosine kinase drives tumor cell progression and abrogates cell-cell adhesion through E-cadherin transcriptional repression. Cancer Res 2004;64:5154-61. (Pubitemid 39006533)
33. Kretschmann KL, Eyob H, Buys SS, Welm AL. The macrophage stimulating protein/Ron pathway as a potential therapeutic target to impede multiple mechanisms involved in breast cancer progression. Curr Drug Targets 2010;11:1157-68.
34. Zinser GM, Leonis MA, Toney K, Pathrose P, Thobe M, Kader SA, et al. Mammary-specific Ron receptor overexpression induces highly metastatic mammary tumors associated with beta-catenin activation. Cancer Res 2006;66:11967-74. (Pubitemid 46094210)
35. Boreddy SR, Pramanik KC, Srivastava SK. Pancreatic tumor suppression by benzyl isothiocyanate is associated with inhibition of PI3K/AKT/FOXO pathway. Clin Cancer Res 2011;17:1784-95.
36. Hildenbrand R, Allgayer H, Marx A, Stroebel P. Modulators of the urokinase-type plasminogen activation system for cancer. Expert Opin Investig Drugs 2010;19:641-52.
37. Jo M, Thomas KS, O'Donnell DM, Gonias SL. Epidermal growth factor receptor-dependent and -independent cell-signaling pathways originating fromthe urokinase receptor. J Biol Chem 2003;278:1642-6. (Pubitemid 36801395)
38. Kwaan HC, McMahon B. The role of plasminogen-plasmin system in cancer. Cancer Treat Res 2009;148:43-66.
39. Lai KC, Huang AC, Hsu SC, Kuo CL, Yang JS, Wu SH, et al. Benzyl isothiocyanate (BITC) inhibits migration and invasion of human colon cancer HT29 cells by inhibiting matrix metalloproteinase-2/-9 and urokinase plasminogen (uPA) through PKC and MAPK signaling pathway. J Agric Food Chem 2010;58:2935-42.
40. Kim EJ, Eom SJ, Hong JE, Lee JY, Choi MS, Park JH. Benzyl isothiocyanate inhibits basal and hepatocyte growth factor-stimulated migration of breast cancer cells. Mol Cell Biochem 2012;359:431-40.
41. Maggiora P, Marchio S, Stella MC, Giai M, Belfiore A, De Bortoli M, et al. Overexpression of the RON gene in human breast carcinoma. Oncogene 1998;16:2927-33. (Pubitemid 28383277)
42. Lee WY, Chen HH, Chow NH, Su WC, Lin PW, Guo HR. Prognostic signi ficance of co-expression of RON and MET receptors in nodenegative breast cancer patients. Clin Cancer Res 2005;11:2222-8. (Pubitemid 40490180)
43. Feres KJ, Ischenko I, Hayman MJ. The RON receptor tyrosine kinase promotes MSP-independent cell spreading and survival in breast epithelial cells. Oncogene 2009;28:279-88.
44. McClaine RJ, Marshall AM, Wagh PK, Waltz SE. Ron receptor tyrosine kinase activation confers resistance to tamoxifen in breast cancer cell lines. Neoplasia 2010;12:650-8.