Sulforaphane, a cruciferous vegetable-derived isothiocyanate, inhibits protein synthesis in human prostate cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 8, 2012, Pages 1295-1305

  Wiczk, Aleksandra ^a   Hofman, Dagmara ^a   Konopa, Grazyna ^a   Herman Antosiewicz, Anna ^a  

^a UNIVERSITY OF GDA SK   (Poland)

Author keywords

MTOR; Prostate cancer; Protein synthesis; S6K1; Sulforaphane; Survivin

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; REACTIVE OXYGEN METABOLITE; SULFORAPHANE; SURVIVIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; GLYCOLYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BRASSICACEAE; CELL LINE, TUMOR; CELL SURVIVAL; ENERGY METABOLISM; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MALE; MITOCHONDRIA; PHOSPHORYLATION; PLANT EXTRACTS; PROSTATIC NEOPLASMS; PROTEIN BIOSYNTHESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SYNTHESIS INHIBITORS; REACTIVE OXYGEN SPECIES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SIROLIMUS; THIOCYANATES; TOR SERINE-THREONINE KINASES;

ANIMALIA;

EID: 84862272583     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.05.020     Document Type: Article

References (54)

1. Lin H.J., Probst-Hensch N.M., Louie A.D., Kau I.H., Witte J.S., Ingles S.A., Frankl H.D., Lee E.R., Haile R.W. Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal adenomas. Cancer Epidemiol. Biomarkers Prev. 1998, 7:647-652.
2. Joseph M.A., Moysich K.B., Freudenheim J.L., Shields P.G., Bowman E.D., Zhang Y., Marshall J.R., Ambrosone C.B. Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutr. Cancer 2004, 50:206-213.
3. Carpenter C.L., Yu M.C., London S.J. Dietary isothiocyanates, glutathione S-transferase M1 (GSTM1), and lung cancer risk in African Americans and Caucasians from Los Angeles County, California. Nutr. Cancer 2009, 61:492-499.
4. Kirsh V.A., Peters U., Mayne S.T., Subar A.F., Chatterjee N., Johnson C.C., Hayes R.B. Prospective study of fruit and vegetable intake and risk of prostate cancer. J. Natl. Cancer Inst. 2007, 99:1200-1209.
5. Giovannucci E., Rimm E.B., Liu Y., Stampfer M.J., Willett W.C. A prospective study of cruciferous vegetables and prostate cancer. Cancer Epidemiol. Biomarkers Prev. 2003, 12:1403-1409.
6. Zhang Y., Talalay P., Cho C.G., Posner G.H. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:2399-2403.
7. Barcelo S., Gardiner J.M., Gescher A., Chipman J.K. CYP2E1-mediated mechanism of anti-genotoxicity of the broccoli constituent sulforaphane. Carcinogenesis 1996, 17:277-282.
8. Gamet-Payrastre L. Signaling pathways and intracellular targets of sulforaphane mediating cell cycle arrest and apoptosis. Curr. Cancer Drug Targets 2006, 6:135-145.
9. Clarke J.D., Dashwood R.H., Ho E. Multi-targeted prevention of cancer by sulforaphane. Cancer Lett. 2008, 269:291-304.
10. Xiao D., Powolny A.A., Antosiewicz J., Hahm E.R., Bommareddy A., Zeng Y., Desai D., Amin S., Herman-Antosiewicz A., Singh S.V. Cellular responses to cancer chemopreventive agent D,L-sulforaphane in human prostate cancer cells are initiated by mitochondrial reactive oxygen species. Pharm. Res. 2009, 26:1729-1738.
11. Choi W.Y., Choi B.T., Lee W.H., Choi Y.H. Sulforaphane generates reactive oxygen species leading to mitochondrial perturbation for apoptosis in human leukemia U937 cells. Biomed. Pharmacother. 2008, 62:637-644.
12. Singh S.V., Srivastava S.K., Choi S., Lew K.L., Antosiewicz J., Xiao D., Zeng Y., Watkins S.C., Johnson C.S., Trump D.L., Lee Y.J., Xiao H., Herman-Antosiewicz A. Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J. Biol. Chem. 2005, 280:19911-19924.
13. Singh S.V., Herman-Antosiewicz A., Singh A.V., Lew K.L., Srivastava S.K., Kamath R., Brown K.D., Zhang L., Baskaran R. Sulforaphane-induced G2/M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C. J. Biol. Chem. 2004, 279:25813-25822.
14. Myzak M.C., Hardin K., Wang R., Dashwood R.H., Ho E. Sulforaphane inhibits histone deacetylase activity in BPH-1, LnCaP and PC-3 prostate epithelial cells. Carcinogenesis 2006, 27:811-819.
15. Pledgie-Tracy A., Sobolewski M.D., Davidson N.E. Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol. Cancer Ther. 2007, 6:1013-1021.
16. Mi L., Gan N., Cheema A., Dakshanamurthy S., Wang X., Yang D.C., Chung F.L. Cancer preventive isothiocyanates induce selective degradation of cellular alpha- and beta-tubulins by proteasomes. J. Biol. Chem. 2009, 284:17039-17051.
17. Yeh C.T., Yen G.C. Effect of sulforaphane on metallothionein expression and induction of apoptosis in human hepatoma HepG2 cells. Carcinogenesis 2005, 26:2138-2148.
18. Singh A.V., Xiao D., Lew K.L., Dhir R., Singh S.V. Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 2004, 25:83-90.
19. Singh S.V., Warin R., Xiao D., Powolny A.A., Stan S.D., Arlotti J.A., Zeng Y., Hahm E.R., Marynowski S.W., Bommareddy A., Desai D., Amin S., Parise R.A., Beumer J.H., Chambers W.H. Sulforaphane inhibits prostate carcinogenesis and pulmonary metastasis in TRAMP mice in association with increased cytotoxicity of natural killer cells. Cancer Res. 2009, 69:2117-2125.
20. Bilanges B., Stokoe D. Mechanisms of translational deregulation in human tumors and therapeutic intervention strategies. Oncogene 2007, 26:5973-5990.
21. Altomare D.A., Testa J.R. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005, 24:7455-7464.
22. Mamane Y., Petroulakis E., LeBacquer O., Sonenberg N. mTOR, translation initiation and cancer. Oncogene 2006, 25:6416-6422.
23. Holz M.K., Ballif B.A., Gygi S.P., Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 2005, 123:569-580.
24. Wang X., Li W., Williams M., Terada N., Alessi D.R., Proud C.G. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 2001, 20:4370-4379.
25. Raught B., Peiretti F., Gingras A.C., Livingstone M., Shahbazian D., Mayeur G.L., Polakiewicz R.D., Sonenberg N., Hershey J.W. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J. 2004, 23:1761-1769.
26. King M.P., Attardi G. Isolation of human cell lines lacking mitochondrial DNA. Methods Enzymol. 1996, 264:304-313.
27. Herman-Antosiewicz A., Johnson D.E., Singh S.V. Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res. 2006, 66:5828-5835.
28. Pearson R.B., Dennis P.B., Han J.W., Williamson N.A., Kozma S.C., Wettenhall R.E., Thomas G. The principal target of rapamycin-induced p70s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain. EMBO J. 1995, 14:5279-5287.
29. Burnett P.E., Barrow R.K., Cohen N.A., Snyder S.H., Sabatini D.M. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1432-1437.
30. Peterson R.T., Desai B.N., Hardwick J.S., Schreiber S.L. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin associated protein. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4438-4442.
31. Tang H., Hornstein E., Stolovich M., Levy G., Livingstone M., Templeton D., Avruch J., Meyuhas O. Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol. Cell. Biol. 2001, 21:8671-8683.
32. Barth-Baus D., Stratton C.A., Parrott L., Myerson H., Meyuhas O., Templeton D.J., Landreth G.E., Hensold J.O. S6 phosphorylation-independent pathways regulate translation of 5'-terminal oligopyrimidine tract-containing mRNAs in differentiating hematopoietic cells. Nucleic Acids Res. 2002, 30:1919-1928.
33. Pende M., Um S.H., Mieulet V., Sticker M., Goss V.L., Mestan J., Mueller M., Fumagalli S., Kozma S.C., Thomas G. S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 2004, 24:3112-3124.
34. Gilkerson R.W., Margineantu D.H., Capaldi R.A., Selker J.M. Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett. 2000, 474:1-4.
35. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
36. Ma X.M., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 2009, 10:307-318.
37. Schmid T., Jansen A.P., Baker A.R., Hegamyer G., Hagan J.P., Colburn N.H. Translation inhibitor Pdcd4 is targeted for degradation during tumor promotion. Cancer Res. 2008, 68:1254-1260.
38. Yang H.S., Jansen A.P., Komar A.A., Zheng X., Merrick W.C., Costes S., Lockett S.J., Sonenberg N., Colburn N.H. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol. Cell. Biol. 2003, 23:26-37.
39. Sarbassov D.D., Sabatini D.M. Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J. Biol. Chem. 2005, 280:39505-39509.
40. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 2001, 294:1102-1105.
41. Choo A.Y., Kim S.G., Vander Heiden M.G., Mahoney S.J., Vu H., Yoon S.O., Cantley L.C., Blenis J. Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with supply. Mol. Cell 2010, 38:487-499.
42. Gebauer F., Hentze M.W. Molecular mechanisms of translational control. Nat. Rev. Mol. Cell Biol. 2004, 5:827-835.
43. Zhao J., Tenev T., Martins L.M., Downward J., Lemoine N.R. The ubiquitin-proteasome pathway regulates survivin degradation in a cell cycle-dependent manner. J. Cell. Sci. 2000, 113:4363-4371.
44. Ambrosini G., Adida C., Altieri D.C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 1997, 3:917-921.
45. Kishi H., Igawa M., Kikuno N., Yoshino T., Urakami S., Shiina H. Expression of the survivin gene in prostate cancer: correlation with clinicopathological characteristics, proliferative activity and apoptosis. J. Urol. 2004, 171:1855-1860.
46. Zaffaroni N., Daidone M.G. Survivin expression and resistance to anticancer treatments: perspectives for new therapeutic interventions. Drug Resist. Updat. 2002, 5:65-72.
47. Altieri D.C. Survivin, cancer networks and pathway-directed drug discovery. Nat. Rev. Cancer 2008, 8:61-70.
48. Vaira V., Lee C.W., Goel H.L., Bosari S., Languino L.R., Altieri D.C. Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene 2007, 26:2678-2684.
49. Roca H., Varsos Z.S., Mizutani K., Pienta K.J. CCL2, survivin and autophagy: new links with implications in human cancer. Autophagy 2008, 4:969-971.
50. Roca H., Varsos Z.S., Pienta K.J. CCL2 is a negative regulator of AMP-activated protein kinase to sustain mTOR complex-1 activation, survivin expression, and cell survival in human prostate cancer PC3 cells. Neoplasia 2009, 11:1309-1317.
51. Altieri D.C. Targeted therapy by disabling crossroad signaling networks: the survivin paradigm. Mol. Cancer Ther. 2006, 5:478-482.
52. Hahm E.R., Singh S.V. Sulforaphane inhibits constitutive and interleukin-6-induced activation of signal transducer and activator of transcription 3 in prostate cancer cells. Cancer Prev. Res. (Phila) 2010, 3:484-494.
53. Kwak M.K., Cho J.M., Huang B., Shin S., Kensler T.W. Role of increased expression of the proteasome in the protective effects of sulforaphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells. Free Radic. Biol. Chem. 2007, 43:809-817.
54. Gan N., Wu Y.C., Brunet M., Garrido C., Chung F.L., Dai C., Mi L. Sulforaphane activates heat shock response and enhances proteasome activity through up-regulation of Hsp27. J. Biol. Chem. 2010, 285:35528-35536.