Sulforaphane increases drug-mediated cytotoxicity toward cancer stem-like cells of pancreas and prostate

Molecular Therapy

Volumn 19, Issue 1, 2011, Pages 188-195

  Kallifatidis, Georgios ^a   Labsch, Sabrina ^a   Rausch, Vanessa ^a   Mattern, Juergen ^a   Gladkich, Jury ^a   Moldenhauer, Gerhard ^b   Büchler, Markus W ^a   Salnikov, Alexei V ^a,b   Herr, Ingrid ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CISPLATIN; DOXORUBICIN; FLUOROURACIL; GEMCITABINE; NOTCH1 RECEPTOR; PACLITAXEL; SULFORAPHANE; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER STEM CELL; CELL CLONING; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SAFETY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PROSTATE CANCER; PROTEIN EXPRESSION; TARGET CELL DESTRUCTION;

BRASSICA OLERACEA VAR. ITALICA; MUS;

EID: 78650901935     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.216     Document Type: Article

References (42)

1. Jemal, A, Siegel, R, Ward, E, Hao, Y, Xu, J, Murray, T et al. (2008). Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
2. Reya, T, Morrison, SJ, Clarke, MF and Weissman, IL (2001). Stem cells, cancer, and cancer stem cells. Nature 414: 105-111.
3. Ribacka, C, Pesonen, S and Hemminki, A (2008). Cancer, stem cells, and oncolytic viruses. Ann Med 40: 496-505.
4. Li, C, Heidt, DG, Dalerba, P, Burant, CF, Zhang, L, Adsay, V et al. (2007). Identifcation of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
5. Hermann, PC, Huber, SL, Herrler, T, Aicher, A, Ellwart, JW, Guba, M et al. (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323.
6. Kallifatidis, G, Rausch, V, Baumann, B, Apel, A, Beckermann, BM, Groth, A et al. (2009). Sulforaphane targets pancreatic tumour-initiating cells by NF-kappaB-induced antiapoptotic signalling. Gut 58: 949-963.
7. Mueller, MT, Hermann, PC, Witthauer, J, Rubio-Viqueira, B, Leicht, SF, Huber, S et al. (2009). Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 137: 1102-1113.
8. + cell population is enriched in tumor-initiating cells. Cancer Res 67: 6796-6805.
9. Pham, NA, Jacobberger, JW, Schimmer, AD, Cao, P, Gronda, M and Hedley, DW (2004). The dietary isothiocyanate sulforaphane targets pathways of apoptosis, cell cycle arrest, and oxidative stress in human pancreatic cancer cells and inhibits tumor growth in severe combined immunodefcient mice. Mol Cancer Ther 3: 1239-1248.
10. Rausch, V, Liu, L, Kallifatidis, G, Baumann, B, Mattern, J, Gladkich, J et al. (2010). Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res 70: 5004-5013.
11. Zhang, C, Mattern, J, Haferkamp, A, Pftzenmaier, J, Hohenfellner, M, Rittgen, W et al. (2006). Corticosteroid-induced chemotherapy resistance in urological cancers. Cancer Biol Ther 5: 59-64.
12. + CD24- prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer 98: 756-765.
13. Yao, J, Cai, HH, Wei, JS, An, Y, Ji, ZL, Lu, ZP et al. (2010). Side population in the pancreatic cancer cell lines SW1990 and CFPAC-1 is enriched with cancer stem-like cells. Oncol Rep 23: 1375-1382.
14. Pfeiffer, MJ and Schalken, JA (2010). Stem cell characteristics in prostate cancer cell lines. Eur Urol 57: 246-254.
15. Mochizuki, H, Matsubara, A, Teishima, J, Mutaguchi, K, Yasumoto, H, Dahiya, R et al. (2004). Interaction of ligand-receptor system between stromal-cell-derived factor-1 and CXC chemokine receptor 4 in human prostate cancer: a possible predictor of metastasis. Biochem Biophys Res Commun 320: 656-663.
16. Klarmann, GJ, Hurt, EM, Mathews, LA, Zhang, X, Duhagon, MA, Mistree, T et al. (2009). Invasive prostate cancer cells are tumor initiating cells that have a stem celllike genomic signature. Clin Exp Metastasis 26: 433-446.
17. Zhou, W, Kallifatidis, G, Baumann, B, Rausch, V, Mattern, J, Gladkich, J et al. (2010). Dietary polyphenol quercetin targets pancreatic cancer stem cells. Int J Oncol 37: 551-561.
18. Wei, C, Guomin, W, Yujun, L and Ruizhe, Q (2007). Cancer stem-like cells in human prostate carcinoma cells DU145: the seeds of the cell line? Cancer Biol Ther 6: 763-768.
19. Dontu, G, Jackson, KW, McNicholas, E, Kawamura, MJ, Abdallah, WM and Wicha, MS (2004). Role of Notch signaling in cell-fate determination of human mammary stem/ progenitor cells. Breast Cancer Res 6: R605-R615.
20. Osipo, C, Golde, TE, Osborne, BA and Miele, LA (2008). Off the beaten pathway: the complex cross talk between Notch and NF-kappaB. Lab Invest 88: 11-17.
21. Ginestier, C, Hur, MH, Charafe-Jauffret, E, Monville, F, Dutcher, J, Brown, M et al. (2007). ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
22. Shankar, S, Ganapathy, S and Srivastava, RK (2008). Sulforaphane enhances the therapeutic potential of TRAIL in prostate cancer orthotopic model through regulation of apoptosis, metastasis, and angiogenesis. Clin Cancer Res 14: 6855-6866.
23. Juge, N, Mithen, RF and Traka, M (2007). Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci 64: 1105-1127.
24. Myzak, MC and Dashwood, RH (2006). Chemoprotection by sulforaphane: keep one eye beyond Keap1. Cancer Lett 233: 208-218.
25. Myzak, MC, Tong, P, Dashwood, WM, Dashwood, RH and Ho, E (2007). Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Exp Biol Med (Maywood) 232: 227-234.
26. Singh, AV, Xiao, D, Lew, KL, Dhir, R and Singh, SV (2004). Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 25: 83-90.
27. Choi, S, Lew, KL, Xiao, H, Herman-Antosiewicz, A, Xiao, D, Brown, CK et al. (2007). D,L-Sulforaphane-induced cell death in human prostate cancer cells is regulated by inhibitor of apoptosis family proteins and Apaf-1. Carcinogenesis 28: 151-162.
28. Pledgie-Tracy, A, Sobolewski, MD and Davidson, NE (2007). Sulforaphane induces cell type-specifc apoptosis in human breast cancer cell lines. Mol Cancer Ther 6: 1013-1021.
29. Jackson, SJ and Singletary, KW (2004). Sulforaphane: a naturally occurring mammary carcinoma mitotic inhibitor, which disrupts tubulin polymerization. Carcinogenesis 25: 219-227.
30. Shen, G, Xu, C, Chen, C, Hebbar, V and Kong, AN (2006). p53-independent G1 cell cycle arrest of human colon carcinoma cells HT-29 by sulforaphane is associated with induction of p21CIP1 and inhibition of expression of cyclin D1. Cancer Chemother Pharmacol 57: 317-327.
31. Yu, D, Sekine-Suzuki, E, Xue, L, Fujimori, A, Kubota, N and Okayasu, R (2009). Chemopreventive agent sulforaphane enhances radiosensitivity in human tumor cells. Int J Cancer 125: 1205-1211.
32. Wang, Z, Desmoulin, S, Banerjee, S, Kong, D, Li, Y, Deraniyagala, RL et al. (2008). Synergistic effects of multiple natural products in pancreatic cancer cells. Life Sci 83: 293-300.
33. Fimognari, C and Hrelia, P (2007). Sulforaphane as a promising molecule for fghting cancer. Mutat Res 635: 90-104.
34. Wang, Z, Banerjee, S, Li, Y, Rahman, KM, Zhang, Y and Sarkar, FH (2006). Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 66: 2778-2784.
35. Jimeno, A, Feldmann, G, Suárez-Gauthier, A, Rasheed, Z, Solomon, A, Zou, GM et al. (2009). A direct pancreatic cancer xenograft model as a platform for cancer stem cell therapeutic development. Mol Cancer Ther 8: 310-314.
36. Tanei, T, Morimoto, K, Shimazu, K, Kim, SJ, Tanji, Y, Taguchi, T et al. (2009). Association of breast cancer stem cells identifed by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 15: 4234-4241.
37. Dave, B and Chang, J (2009). Treatment resistance in stem cells and breast cancer. J Mammary Gland Biol Neoplasia 14: 79-82.
38. Sell, S (2006). Cancer stem cells and differentiation therapy. Tumour Biol 27: 59-70.
39. Fimognari, C, Lenzi, M, Cantelli-Forti, G and Hrelia, P (2008). Induction of differentiation in human promyelocytic cells by the isothiocyanate sulforaphane. In Vivo 22: 317-320.
40. Hunakova, L, Sedlakova, O, Cholujova, D, Gronesova, P, Duraj, J and Sedlak, J (2009). Modulation of markers associated with aggressive phenotype in MDA-MB-231 breast carcinoma cells by sulforaphane. Neoplasma 56: 548-556.
41. Kakarala, M, Brenner, DE, Korkaya, H, Cheng, C, Tazi, K, Ginestier, C et al. (2010). Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res Treat 122: 777-785.
42. Koziol, JA, Maxwell, DA, Fukushima, M, Colmerauer, ME, and Pilch, YH (1981). A distribution-free test for tumor growth curve analyses with application to an animal tumor immunotherapy experiment. Biometrics 37: 383-390.