Simvastatin rises reactive oxygen species levels and induces senescence in human melanoma cells by activation of p53/p21 pathway

Experimental Cell Research

Volumn 319, Issue 19, 2013, Pages 2977-2988

  Guterres, Fernanda Augusta de Lima Barbosa ^a   Martinez, Glaucia Regina ^a   Rocha, Maria Eliane Merlin ^a   Winnischofer, Sheila Maria Brochado ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

Melanoma cells; ROS; Senescence; Simvastatin

Indexed keywords

BETA GALACTOSIDASE; PROTEIN P21; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SIMVASTATIN;

ARTICLE; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MELANOMA CELL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENESCENCE; UPREGULATION;

EID: 84886597050     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.07.026     Document Type: Article

References (47)

1. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell. Res. 1961, 25:585-621.
2. Stewart S.A., Weinberg R.A. Telomeres: cancer to human aging. Annu. Rev. Cell. Dev. Biol. 2006, 22:531-557.
3. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 2005, 6:611-622.
4. Muller M. Cellular senescence: molecular mechanisms, in vivo significance, and redox considerations. Antioxid. Redox Sign. 2009, 11:59-98.
5. Mooi W.J., Peeper D.S. Oncogene-induced cell senescence - halting on the road to cancer. N. Engl. J. Med. 2006, 355:1037-1046.
6. Campisi J., di Fagagna F.D. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell. Bio. 2007, 8:729-740.
7. Elmore L.W., Rehder C.W., Di X., McChesney P.A., Jackson-Cook C.K., Gewirtz D.A., Holt S.E. Adriamycin-induced senescence in breast tumor cells involves functional p53 and telomere dysfunction. J. Biol. Chem. 2002, 277:35509-35515.
8. Chang B.D., Broude E.V., Dokmanovic M., Zhu H.M., Ruth A., Xuan Y.Z., Kandel E.S., Lausch E., Christov K., Roninson I.B. A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Res. 1999, 59:3761-3767.
9. Dabrowska M., Mosieniak G., Skierski J., Sikora E., Rode W. Methotrexate-induced senescence in human adenocarcinoma cells is accompanied by induction of p21(waf1/cip1) expression and lack of polyploidy. Cancer Lett. 2009, 284:95-101.
10. Zhang Y., Yang J.M. The impact of cellular senescence in cancer therapy: is it true or not?. Acta Pharmacol. Sin. 2011, 32:1199-1207.
11. Takeda I., Maruya S., Shirasaki T., Mizukami H., Takahata T., Myers J.N., Kakehata S., Yagihashi S., Shinkawa H. Simvastatin inactivates beta1-integrin and extracellular signal-related kinase signaling and inhibits cell proliferation in head and neck squamous cell carcinoma cells. Cancer Sci. 2007, 98:890-899.
12. Agarwal B., Halmos B., Feoktistov A.S., Protiva P., Ramey W.G., Chen M., Pothoulakis C., Lamont J.T., Holt P.R. Mechanism of lovastatin-induced apoptosis in intestinal epithelial cells. Carcinogenesis 2002, 23:521-528.
13. Denoyelle C., Albanese P., Uzan G., Hong L., Vannier J.P., Soria J., Soria C. Molecular mechanism of the anti-cancer activity of cerivastatin, an inhibitor of HMG-CoA reductase, on aggressive human breast cancer cells. Cell Signal 2003, 15:327-338.
14. Koyuturk M., Ersoz M., Altiok N. Simvastatin induces apoptosis in human breast cancer cells: p53 and estrogen receptor independent pathway requiring signalling through JNK. Cancer Lett. 2007, 250:220-228.
15. Koomen E.R., Joosse A., Herings R.M., Casparie M.K., Bergman W., Nijsten T., Guchelaar H.J. Is statin use associated with a reduced incidence, a reduced Breslow thickness or delayed metastasis of melanoma of the skin?. Eur. J. Cancer 2007, 43:2580-2589.
16. Kaminsky Y.G., Kosenko E.A. Molecular mechanisms of toxicity of simvastatin, widely used cholesterol-lowering drug. A review. Cent. Eur. J. Med. 2010, 5:269-279.
17. Saito A., Saito N., Mol W., Furukawa H., Tsutsumida A., Oyama A., Sekido M., Sasaki S., Yamamoto Y. Simvastatin inhibits growth via apoptosis and the induction of cell cycle arrest in human melanoma cells. Melanoma Res. 2008, 18:85-94.
18. Glynn S.A., O'Sullivan D., Eustace A.J., Clynes M., O'Donovan N. The 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors, simvastatin, lovastatin and mevastatin inhibit proliferation and invasion of melanoma cells. BMC Cancer 2008, 8:9.
19. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (RESEARCH0034).
20. Schachter M. Chemical, pharmacokinetic and pharmacodynamic properties of statins: an update. Fundam. Clin. Pharmacol. 2005, 19:117-125.
21. Lennernas H., Fager G. Pharmacodynamics and pharmacokinetics of the HMG-CoA reductase inhibitors. Similarities and differences. Clin. Pharmacokinet. 1997, 32:403-425.
22. Demierre M.F., Sondak V.K. Cutaneous melanoma: pathogenesis and rationale for chemoprevention. Crit. Rev. Oncol. Hematol. 2005, 53:225-239.
23. Breslow A. Thickness, cross-sectional areas and depth of invasion in the prognosis of cutaneous melanoma. Ann. Surg. 1970, 172:902-908.
24. Denoyelle C., Vasse M., Korner M., Mishal Z., Ganne F., Vannier J.P., Soria J., Soria C. Cerivastatin, an inhibitor of HMG-CoA reductase, inhibits the signaling pathways involved in the invasiveness and metastatic properties of highly invasive breast cancer cell lines: an in vitro study. Carcinogenesis 2001, 22:1139-1148.
25. Shellman Y.G., Ribble D., Miller L., Gendall J., Vanbuskirk K., Kelly D., Norris D.A., Dellavalle R.P. Lovastatin-induced apoptosis in human melanoma cell lines. Melanoma Res. 2005, 15:83-89.
26. Collisson E.A., Kleer C., Wu M., De A., Gambhir S.S., Merajver S.D., Kolodney M.S. Atorvastatin prevents RhoC isoprenylation, invasion, and metastasis in human melanoma cells. Mol. Cancer Ther. 2003, 2:941-948.
27. Cafforio P., Dammacco F., Gernone A., Silvestris F. Statins activate the mitochondrial pathway of apoptosis in human lymphoblasts and myeloma cells. Carcinogenesis 2005, 26:883-891.
28. Hoque A., Chen H., Xu X.C. Statin induces apoptosis and cell growth arrest in prostate cancer cells. Cancer Epidemiol. Biomarkers Prev. 2008, 17:88-94.
29. Relja B., Meder F., Wilhelm K., Henrich D., Marzi I., Lehnert M. Simvastatin inhibits cell growth and induces apoptosis and G0/G1 cell cycle arrest in hepatic cancer cells. Int. J. Mol. Med. 2010, 26:735-741.
30. Yang Y.C., Xiao D.W., Liu H., Chuan L.M., Zeng Y.L., Zhou D.A., Liu W., Xu G.Q., Huang W.F. Mechanism of simvastatin-induced K562 cell apoptosis. Pharmacology 2009, 84:191-195.
31. Giuliano S., Ohanna M., Ballotti R., Bertolotto C. Advances in melanoma senescence and potential clinical application. Pigm. Cell Melanoma Res. 2011, 24:295-308.
32. Lee J., Lee I., Park C., Kang W.K. Lovastatin-induced RhoA modulation and its effect on senescence in prostate cancer cells. Biochem. Biophys. Res. Commun. 2006, 339:748-754.
33. Murtola T.J., Syvala H., Pennanen P., Blauer M., Solakivi T., Ylikomi T., Tammela T.L.J. Comparative effects of high and low-dose simvastatin on prostate epithelial cells: The role of LDL. Eur. J. Pharmacol. 2011, 673:96-100.
34. Romagosa C., Simonetti S., Lopez-Vicente L., Mazo A., Lleonart M.E., Castellvi J., Ramon y Cajal S. p16(Ink4a) overexpression in cancer: a tumor suppressor gene associated with senescence and high-grade tumors. Oncogene 2011, 30:2087-2097.
35. Ha L.N., Merlino G., Sviderskaya E.V. Melanomagenesis - overcoming the barrier of melanocyte senescence. Cell Cycle 2008, 7:1944-1948.
36. England N.L., Cuthbert A.P., Trott D.A., Jezzard S., Nobori T., Carson D.A., Newbold R.F. Identification of human tumour suppressor genes by monochromosome transfer: rapid growth-arrest response mapped to 9p21 is mediated solely by the cyclin-D-dependent kinase inhibitor gene, CDKN2A (p16(INK4A)). Carcinogenesis 1996, 17:1567-1575.
37. Kim W.Y., Sharpless N.E. The regulation of INK4/ARF in cancer and aging. Cell 2006, 127:265-275.
38. Zhu Y., Xu L., Zhang J., Hu X., Liu Y., Yin H., Lv T., Zhang H., Liu L., An H., Liu H., Xu J., Lin Z. Sunitinib induces cellular senescence via p53/Dec1 activation in renal cell carcinoma cells. Cancer Sci. 2013.
39. Mhaidat N.M., Zhang X.D., Allen J., Avery-Kiejda K.A., Scott R.J., Hersey P. Temozolomide induces senescence but not apoptosis in human melanoma cells. Br. J. Cancer 2007, 97:1225-1233.
40. Tavintharan S., Ong C.N., Jeyaseelan K., Sivakumar M., Lim S.C., Sum C.F. Reduced mitochondrial coenzyme Q10 levels in HepG2 cells treated with high-dose simvastatin: a possible role in statin-induced hepatotoxicity?. Toxicol. Appl. Pharmacol. 2007, 223:173-179.
41. Sanchez C.A., Rodriguez E., Varela E., Zapata E., Paez A., Masso F.A., Montano L.F., Loopez-Marure R. Statin-induced inhibition of MCF-7 breast cancer cell proliferation is related to cell cycle arrest and apoptotic and necrotic cell death mediated by an enhanced oxidative stress. Cancer Invest. 2008, 26:698-707.
42. Qi X.F., Kim D.H., Yoon Y.S., Kim S.K., Cai D.Q., Teng Y.C., Shim K.Y., Lee K.J. Involvement of oxidative stress in simvastatin-induced apoptosis of murine CT26 colon carcinoma cells. Toxicol. Lett. 2010, 199:277-287.
43. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
44. Wittgen H.G., van Kempen L.C. Reactive oxygen species in melanoma and its therapeutic implications. Melanoma Res. 2007, 17:400-409.
45. Sander C.S., Chang H., Hamm F., Elsner P., Thiele J.J. Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis. Int. J. Dermatol. 2004, 43:326-335.
46. Miao L., Clair D.K. Regulation of superoxide dismutase genes: implications in disease. Free Radical Biol. Med. 2009, 47:344-356.
47. Gechev T., Gadjev I., Van Breusegem F., Inze D., Dukiandjiev S., Toneva V., Minkov I. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell. Mol. Life. Sci. 2002, 59:708-714.