Targeting cancer stem cells with sulforaphane, a dietary component from broccoli and broccoli sprouts

Future Oncology

Volumn 9, Issue 8, 2013, Pages 1097-1103

  Li, Yanyan ^a   Zhang, Tao ^b  

^a MONTCLAIR STATE UNIVERSITY   (United States)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

broccoli sprout; cancer; cancer stem cell; self renewal; sulforaphane

Indexed keywords

SULFORAPHANE;

ARTICLE; BREAST CANCER; BROCCOLI; CANCER STEM CELL; DRUG BIOAVAILABILITY; DRUG EFFECT; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; LIVER CELL CARCINOMA; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER;

ANTICARCINOGENIC AGENTS; BRASSICA; EPITHELIAL-MESENCHYMAL TRANSITION; HEDGEHOG PROTEINS; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; NF-KAPPA B; THIOCYANATES;

EID: 84881309783     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.13.108     Document Type: Article

References (66)

1. Clarke JD, Dashwood RH, Ho E. Multi-targeted prevention of cancer by sulforaphane. Cancer Lett. 269 (2), 291-304 (2008).
2. Fahey JW, Zalcmann AT, Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56 (1), 5-51 (2001).
3. Matusheski NV, Swarup R, Juvik JA, Mithen R, Bennett M, Jeffery EH. Epithiospecifier protein from broccoli (Brassica oleracea L. ssp. italica) inhibits formation of the anticancer agent sulforaphane. J. Agric. Food Chem. 54 (6), 2069-2076 (2006).
4. Fahey JW, Wehage SL, Holtzclaw WD et al. Protection of humans by plant glucosinolates: Efficiency of conversion of glucosinolates to isothiocyanates by the gastrointestinal microflora. Cancer Prev. Res. (Phila.) 5 (4), 603-611 (2012).
5. Egner PA, Chen JG, Wang JB et al. Bioavailability of sulforaphane from two broccoli sprout beverages: Results of a short-term, cross-over clinical trial in Qidong, China. Cancer Prev. Res. (Phila.) 4 (3), 384-395 (2011).
6. Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: An exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc. Natl Acad. Sci. USA 94 (19), 10367-10372 (1997).
7. Xu C, Huang MT, Shen G et al. Inhibition of 7,12-dimethylbenz (a)anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Res. 66 (16), 8293-8296 (2006).
8. Singh AV, Xiao D, Lew KL, Dhir R, Singh SV. Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 25 (1), 83-90 (2004).
9. Adams JM, Strasser A. Is tumor growth sustained by rare cancer stem cells or dominant clones? Cancer Res. 68 (11), 4018-4021 (2008).
10. Campbell LL, Polyak K. Breast tumor heterogeneity: Cancer stem cells or clonal evolution? Cell Cycle 6 (19), 2332-2338 (2007).
11. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3 (7), 730-737 (1997).
12. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100 (7), 3983-3988 (2003).
13. Singh SK, Clarke ID, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63 (18), 5821-5828 (2003).
14. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 (7123), 106-110 (2007).
15. Li C, Heidt DG, Dalerba P et al. Identification of pancreatic cancer stem cells. Cancer Res. 67 (3), 1030-1037 (2007).
16. Schatton T, Murphy GF, Frank NY et al. Identification of cells initiating human melanomas. Nature 451 (7176), 345-349 (2008).
17. Yang ZF, Ho DW, Ng MN et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13 (2), 153-166 (2008).
18. Liu S, Dontu G, Wicha MS. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res. 7 (3), 86-95 (2005).
19. Korkaya H, Paulson A, Charafe-Jauffret E et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/b-catenin signaling. PLoS Biol. 7 (6), e1000121 (2009).
20. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 414 (6859), 105-111 (2001).
21. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: Challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 8 (10), 806-823 (2009).
22. Shafee N, Smith CR, Wei S et al. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Res. 68 (9), 3243-3250 (2008).
23. Hambardzumyan D, Squatrito M, Holland EC. Radiation resistance and stem-like cells in brain tumors. Cancer Cell 10 (6), 454-456 (2006).
24. Visvader JE, Lindeman GJ. Cancer stem cells: Current status and evolving complexities. Cell Stem Cell 10 (6), 717-728 (2012).
25. Schweizer L, Varmus H. Wnt/Wingless signaling through b-catenin requires the function of both LRP/Arrow and frizzled classes of receptors. BMC Cell Biol. 4, 4 (2003).
26. He TC, Sparks AB, Rago C et al. Identification of c-MYC as a target of the APC pathway. Science 281 (5382), 1509-1512 (1998).
27. Tetsu O, McCormick F. b-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398 (6726), 422-426 (1999).
28. Liu C, Li Y, Semenov M et al. Control of b-catenin phosphorylation/ degradation by a dual-kinase mechanism. Cell 108 (6), 837-847 (2002).
29. Liu S, Dontu G, Mantle ID et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66 (12), 6063-6071 (2006).
30. Cohen MM Jr. The hedgehog signaling network. Am. J. Med. Genet. A 123A (1), 5-28 (2003).
31. Wang Z, Li Y, Banerjee S, Sarkar FH. Emerging role of Notch in stem cells and cancer. Cancer Lett. 279 (1), 8-12 (2009).
32. Mumm JS, Kopan R. Notch signaling: From the outside in. Dev. Biol. 228 (2), 151-165 (2000).
33. Borggrefe T, Oswald F. The Notch signaling pathway: Transcriptional regulation at Notch target genes. Cell. Mol. Life Sci. 66 (10), 1631-1646 (2009).
34. Palomero T, Lim WK, Odom DT et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc. Natl Acad. Sci. USA 103 (48), 18261-18266 (2006).
35. Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kB. J. Clin. Invest. 107 (3), 241-246 (2001).
36. Xu C, Shen G, Chen C, Gelinas C, Kong AN. Suppression of NF-kB and NF-kB-regulated gene expression by sulforaphane and PEITC through IkBa, IKK pathway in human prostate cancer PC-3 cells. Oncogene 24 (28), 4486-4495 (2005).
37. Jeong WS, Kim IW, Hu R, Kong AN. Modulatory properties of various natural chemopreventive agents on the activation of NF-kB signaling pathway. Pharm. Res. 21 (4), 661-670 (2004).
38. Kallifatidis G, Rausch V, Baumann B et al. Sulforaphane targets pancreatic tumour-initiating cells by NF-kB-induced antiapoptotic signalling. Gut 58 (7), 949-963 (2009).
39. Zhou W, Kallifatidis G, Baumann B et al. Dietary polyphenol quercetin targets pancreatic cancer stem cells. Int. J. Oncol. 37 (3), 551-561 (2010).
40. Rausch V, Liu L, Kallifatidis G et al. Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res. 70 (12), 5004-5013 (2010).
41. Karin M, Greten FR. NF-kB: Linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5 (10), 749-759 (2005).
42. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 140 (6), 883-899 (2010).
43. Schwitalla S, Fingerle AA, Cammareri P et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152 (1-2), 25-38 (2013).
44. Nakashima H, Nakamura M, Yamaguchi H et al. Nuclear factor-kB contributes to hedgehog signaling pathway activation through sonic hedgehog induction in pancreatic cancer. Cancer Res. 66 (14), 7041-7049 (2006).
45. Kasperczyk H, Baumann B, Debatin KM, Fulda S. Characterization of sonic hedgehog as a novel NF-kB target gene that promotes NF-kB-mediated apoptosis resistance and tumor growth in vivo. FASEB J. 23 (1), 21-33 (2009).
46. Rodova M, Fu J, Watkins DN, Srivastava RK, Shankar S. Sonic hedgehog signaling inhibition provides opportunities for targeted therapy by sulforaphane in regulating pancreatic cancer stem cell self-renewal. PLoS One 7 (9), e46083 (2012).
47. Li SH, Fu J, Watkins DN, Srivastava RK, Shankar S. Sulforaphane regulates self-renewal of pancreatic cancer stem cells through the modulation of Sonic hedgehog-GLI pathway. Mol. Cell. Biochem. 373 (1-2), 217-227 (2012).
48. Iwatsuki M, Mimori K, Yokobori T et al. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci. 101 (2), 293-299 (2010).
49. Srivastava RK, Tang SN, Zhu W, Meeker D, Shankar S. Sulforaphane synergizes with quercetin to inhibit self-renewal capacity of pancreatic cancer stem cells. Front. Biosci. (Elite Ed.) 3, 515-528 (2011).
50. Shan Y, Zhang L, Bao Y et al. Epithelial-mesenchymal transition, a novel target of sulforaphane via COX-2/MMP2, 9/Snail, ZEB1 and miR-200c/ZEB1 pathways in human bladder cancer cells. J. Nutr. Biochem. 24 (6), 1062-1069 (2013).
51. Park SY, Kim GY, Bae SJ, Yoo YH, Choi YH. Induction of apoptosis by isothiocyanate sulforaphane in human cervical carcinoma HeLa and hepatocarcinoma HepG2 cells through activation of caspase-3. Oncol. Rep. 18 (1), 181-187 (2007).
52. Li Y, Zhang T, Korkaya H et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin. Cancer Res. 16 (9), 2580-2590 (2010).
53. Cornblatt BS, Ye L, Dinkova-Kostova AT et al. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis 28 (7), 1485-1490 (2007).
54. Clarke JD, Hsu A, Riedl K et al. Bioavailability and inter-conversion of sulforaphane and erucin in human subjects consuming broccoli sprouts or broccoli supplement in a cross-over study design. Pharmacol. Res. 64 (5), 456-463 (2011).
55. Ye L, Dinkova-Kostova AT, Wade KL, Zhang Y, Shapiro TA, Talalay P. Quantitative determination of dithiocarbamates in human plasma, serum, erythrocytes and urine: Pharmacokinetics of broccoli sprout isothiocyanates in humans. Clin. Chim. Acta 316 (1-2), 43-53 (2002).
56. Shen G, Khor TO, Hu R et al. Chemoprevention of familial adenomatous polyposis by natural dietary compounds sulforaphane and dibenzoylmethane alone and in combination in ApcMin/+ mouse. Cancer Res. 67 (20), 9937-9944 (2007).
57. Chaudhuri D, Orsulic S, Ashok BT. Antiproliferative activity of sulforaphane in Akt-overexpressing ovarian cancer cells. Mol. Cancer Ther. 6 (1), 334-345 (2007).
58. Roy SK, Srivastava RK, Shankar S. Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J. Mol. Signal. 5, 10 (2010).
59. Pap M, Cooper GM. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273 (32), 19929-19932 (1998).
60. Cohen P, Frame S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2 (10), 769-776 (2001).
61. Kallifatidis G, Labsch S, Rausch V et al. Sulforaphane increases drug-mediated cytotoxicity toward cancer stem-like cells of pancreas and prostate. Mol. Ther. 19 (1), 188-195 (2011).
62. Lin LC, Yeh CT, Kuo CC et al. Sulforaphane potentiates the efficacy of imatinib against chronic leukemia cancer stem cells through enhanced abrogation of Wnt/b-catenin function. J. Agric. Food Chem. 60 (28), 7031-7039 (2012).
63. Shapiro TA, Fahey JW, Dinkova-Kostova AT et al. Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: A clinical Phase I study. Nutr. Cancer 55 (1), 53-62 (2006).
64. Kensler TW, Chen JG, Egner PA et al. Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China. Cancer Epidemiol. Biomarkers Prev. 14 (11 Pt 1), 2605-2613 (2005).
65. Kensler TW, Ng D, Carmella SG et al. Modulation of the metabolism of airborne pollutants by glucoraphanin-rich and sulforaphane-rich broccoli sprout beverages in Qidong, China. Carcinogenesis 33 (1), 101-107 (2012).
66. Qian GS, Ross RK, Yu MC et al. A follow-up study of urinary markers of aflatoxin exposure and liver cancer risk in Shanghai, People's Republic of China. Cancer Epidemiol. Biomarkers Prev. 3 (1), 3-10 (1994).