Notch2 activation by benzyl isothiocyanate impedes its inhibitory effect on breast cancer cell migration

Breast Cancer Research and Treatment

Volumn 134, Issue 3, 2012, Pages 1067-1079

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

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Benzyl isothiocyanate; Breast cancer; Cell migration; Notch2

Indexed keywords

BENZYL ISOTHIOCYANATE; GAMMA SECRETASE INHIBITOR; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; LUCIFERASE; NICASTRIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH4 RECEPTOR; PRESENILIN 1; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL MIGRATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; DRUG MECHANISM; ENZYME ASSAY; GENE REPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; ISOTHIOCYANATES; MICE; MICE, NUDE; PROTEOLYSIS; RECEPTOR, NOTCH1; RECEPTOR, NOTCH2; RECEPTORS, NOTCH; RNA INTERFERENCE; TRANSCRIPTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84868204922     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-012-2043-3     Document Type: Article

References (43)

1. Fowke JH, Chung FL, Jin F, Qi D, Cai Q, Conaway C, Cheng JR, Shu XO, Gao YT, Zheng W (2003) Urinary isothiocyanate levels, brassica, and human breast cancer. Cancer Res 63:3980-3986
2. Ambrosone CB, McCann SE, Freudenheim JL, Marshall JR, Zhang Y, Shields PG (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
3. Zhao H, Lin J, Grossman HB, Hernandez LM, Dinney CP, Wu X (2007) Dietary isothiocyanates, GSTM1, GSTT1, NAT2 polymorphisms and bladder cancer risk. Int J Cancer 120:2208-2213
4. Moy KA, Yuan JM, Chung FL, Van Den Berg D, Wang R, Gao YT, Yu MC (2008) Urinary total isothiocyanates and colorectal cancer: a prospective study of men in Shanghai, China. Cancer Epidemiol Biomarkers Prev 17:1354-1359
5. Hecht SS (2000) Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev 32:395-411
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. 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
8. 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 Carcinogenesis 49:500-507
9. Kim EJ, Hong JE, Eom SJ, Lee JY, Park J H Y (2011) Oral administration of benzyl-isothiocyanate inhibits solid tumor growth and lung metastasis of 4T1 murine mammary carcinoma cells in BALB/c mice. Breast Cancer Res Treat 130:61-71
10. Xiao D, Vogel V, Singh SV (2006) Benzyl isothiocyanateinduced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol Cancer Ther 5:2931-2945
11. Zhang Y, Tang L, Gonzalez V (2003) Selected isothiocyanates rapidly induce growth inhibition of cancer cells. Mol Cancer Ther 2:1045-1052
12. 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
13. 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
14. Kang L, Ding L, Wang ZY (2009) Isothiocyanates repress estrogen receptor alpha expression in breast cancer cells. Oncol Rep 21:185-192
15. 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
16. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J, Daly M, Wieand S, Tan-Chiu E, Ford L, Wolmark N (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
17. Sehrawat A, Singh SV (2011) Benzyl isothiocyanate inhibits epithelial-mesenchymal transition in cultured and xenografted human breast cancer cells. Cancer Prev Res 4:1107-1117
18. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442-454
19. Tomaskovic-Crook E, Thompson EW, Thiery JP (2009) Epithelial to mesenchymal transition and breast cancer. Breast Cancer Res 11:213
20. Hollier BG, Evans K, Mani SA (2009) The epithelial-tomesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mammary Gland Biol Neoplasia 14:29-43
21. Chen J, Imanaka N, Chen J, Griffin JD (2010) Hypoxia potentiates Notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion. Br J Cancer 102:351-360
22. Borggrefe T, Oswald F (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66:1631-1646
23. Leong KG, Karsan A (2006) Recent insights into the role of Notch signaling in tumorigenesis. Blood 107:2223-2233
24. Mumm JS, Kopan R (2000) Notch signaling: from the outside in. Dev Biol 228:151-165
25. Hu C, Dievart A, Lupien M, Calvo E, Tremblay G, Jolicoeur P (2006) Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. Am J Pathol 168:973-990
26. Reedijk M, Odorcic S, Chang L, Zhang H, Miller N, McCready DR, Lockwood G, Egan SE (2005) High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res 65:8530-8537
27. Dickson BC, Mulligan AM, Zhang H, Lockwood G, O'Malley FP, Egan SE, Reedijk M (2007) High-level JAG1 mRNA and protein predict poor outcome in breast cancer. Mod Pathol 20:685-693
28. Reedijk M, Pinnaduwage D, Dickson BC, Mulligan AM, Zhang H, Bull SB, O'Malley FP, Egan SE, Andrulis IL (2008) JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Res Treat 111:439-448
29. Xiao D, Srivastava SK, Lew KL, Zeng Y, Hershberger P, Johnson CS, Trump DL, Singh SV (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
30. Powolny AA, Bommareddy A, Hahm ER, Normolle DP, Beumer JH, Nelson JB, Singh SV (2011) Chemopreventative potential of the cruciferous vegetable constituent phenethyl isothiocyanate in a mouse model of prostate cancer. J Natl Cancer Inst 103:571-584
31. Curry CL, Reed LL, Nickoloff BJ, Miele L, Foreman KE (2006) Notch-independent regulation of Hes-1 expression by c-Jun. N-terminal kinase signaling in human endothelial cells. Lab Invest 86:842-852
32. Wang J, Fu L, Gu F, Ma Y (2011) Notch1 is involved in migration and invasion of human breast cancer cells. Oncol Rep 26:1295-1303
33. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, Bundred NJ, Clarke RB (2010) Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 70:709-718
34. Lindsay J, Jiao X, Sakamaki T, Casimiro MC, Shirley LA, Tran TH, Ju X, Liu M, Li Z, Wang C, Katiyar S, Rao M, Allen KG, Glazer RI, Ge C, Stanley P, Lisanti MP, Rui H, Pestell RG (2008) ErbB2 induces Notch1 activity and function in breast cancer cells. Clin Transl Sci 1:107-115
35. Rizzo P, Miao H, D'Souza G, Osipo C, Song LL, Yun J, Zhao H, Mascarenhas J, Wyatt D, Antico G, Hao L, Yao K, Rajan P, Hicks C, Siziopikou K, Selvaggi S, Bashir A, Bhandari D, Marchese A, Lendahl U, Qin JZ, Tonetti DA, Albain K, Nickoloff BJ, Miele L (2008) Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Res 68:5226-5235
36. Leong KG, Niessen K, Kulic I, Raouf A, Eaves C, Pollet I, Karsan A (2007) Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J Exp Med 204:2935-2948
37. Srivastava SK, Singh SV (2004) Cell cycle arrest, apoptosis induction and inhibition of nuclear factor kappa B activation in anti-proliferative activity of benzyl isothiocyanate against human pancreatic cancer cells. Carcinogenesis 25:1701-1709
38. Boreddy SR, Pramanik KC, Srivastava SK (2011) Pancreatic tumor suppression by benzyl isothiocyanate is associated with inhibition of PI3K/AKT/FOXO pathway. Clin Cancer Res 17:1784-1795
39. Chen X, Stoeck A, Lee SJ, Shih IM, Wang MM, Wang TL (2010) Jagged1 expression regulated by Notch3 and Wnt/β-catenin signaling pathways in ovarian cancer. Oncotarget 1:210-218
40. Schlange T, Matsuda Y, Lienhard S, Huber A, Hynes NE (2007) Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivation. Breast Cancer Res 9:R63
41. Shimizu M, Cohen B, Goldvasser P, Berman H, Virtanen C, Reedijk M (2011) Plasminogen activator uPA is a direct transcriptional target of the JAG1-Notch receptor signaling pathway in breast cancer. Cancer Res 71:277-286
42. Annecke K, Schmitt M, Euler U, Zerm M, Paepke D, Paepke S, Von Minckwitz G, Thomssen C, Harbeck N (2008) uPA and PAI-1 in breast cancer: review of their clinical utility and current validation in the prospective NNBC-3 trial. Adv Clin Chem 45:31-45
43. Lai KC, Huang AC, Hsu SC, Kuo CL, Yang JS, Wu SH, Chung JG (2010) 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 58:2935-2942