Effects of lovastatin on breast cancer cells: A proteo-metabonomic study

Breast Cancer Research

Volumn 12, Issue 2, 2010, Pages

  Klawitter, Jelena ^a   Shokati, Touraj ^a   Moll, Vanessa ^a   Christians, Uwe ^a   Klawitter, Jost ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Eurofins Medinet Inc   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; DJ 1 PROTEIN; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 2; GUANOSINE TRIPHOSPHATASE; LACTONE; MEVINOLIN; MINICHROMOSOME MAINTENANCE PROTEIN 7; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROHIBITIN; PROTEIN CDC42; PROTEIN KINASE B; PROTEIN MSH2; RETINOBLASTOMA PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PROTEOME;

ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE; CELL PROLIFERATION; DRUG EFFECT; HUMAN; HUMAN CELL; METABOLOMICS; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; BREAST TUMOR; CELL SURVIVAL; CITRIC ACID CYCLE; CLASSIFICATION; ENERGY METABOLISM; FEMALE; GLYCOLYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATIVE STRESS; PATHOLOGY; TUMOR CELL LINE; TWO DIMENSIONAL GEL ELECTROPHORESIS; WESTERN BLOTTING;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHROMATOGRAPHY, LIQUID; CITRIC ACID CYCLE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENERGY METABOLISM; FEMALE; GLYCOLYSIS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LOVASTATIN; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; METABOLOMICS; OXIDATIVE STRESS; PROTEOME; PROTEOMICS;

EID: 77956628140     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2485     Document Type: Article

References (67)

1. Kumar AS, Benz CC, Shim V, Minami CA, Moore DH, Esserman LJ. Estrogen receptor-negative breast cancer is less likely to arise among lipophilic statin users. Cancer Epidemiol Biomarkers Prev 2008, 17:1028-1033. 10.1158/1055-9965.EPI-07-0726, 18463402.
2. Kwan ML, Habel LA, Flick ED, Quesenberry CP, Caan B. Post-diagnosis statin use and breast cancer recurrence in a prospective cohort study of early stage breast cancer survivors. Breast Cancer Res Treat 2008, 109:573-579. 10.1007/s10549-007-9683-8, 17674197.
3. Cauley JA, Zmuda JM, Lui LY, Hillier TA, Ness RB, Stone KL, Cummings SR, Bauer DC. Lipid-lowering drug use and breast cancer in older women: a prospective study. J Womens Health (Larchmt) 2003, 12:749-756. 10.1089/154099903322447710, 14588125.
4. Boudreau DM, Gardner JS, Malone KE, Heckbert SR, Blough DK, Daling JR. The association between 3-hydroxy-3-methylglutaryl conenzyme A inhibitor use and breast carcinoma risk among postmenopausal women: a case-control study. Cancer 2004, 100:2308-2316. 10.1002/cncr.20271, 15160333.
5. Larner J, Jane J, Laws E, Packer R, Myers C, Shaffrey M. A phase I-II trial of lovastatin for anaplastic astrocytoma and glioblastoma multiforme. Am J Clin Oncol 1998, 21:579-583. 10.1097/00000421-199812000-00010, 9856659.
6. Katz MS, Minsky BD, Saltz LB, Riedel E, Chessin DB, Guillem JG. Association of statin use with a pathologic complete response to neoadjuvant chemoradiation for rectal cancer. Int J Radiat Oncol Biol Phys 2005, 62:1363-1370.
7. Sassano A, Platanias LC. Statins in tumor suppression. Cancer Lett 2008, 260:11-19. 10.1016/j.canlet.2007.11.036, 18180097.
8. Goldstein JL, Brown MS. Regulation of the mevalonate pathway. Nature 1990, 343:425-430. 10.1038/343425a0, 1967820.
9. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635. 10.1038/nature01148, 12478284.
10. 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. 10.1093/carcin/bgi036, 15705602.
11. Graaf MR, Richel DJ, van Noorden CJ, Guchelaar HJ. Effects of statins and farnesyltransferase inhibitors on the development and progression of cancer. Cancer Treat Rev 2004, 30:609-641. 10.1016/j.ctrv.2004.06.010, 15531395.
12. Campbell MJ, Esserman LJ, Zhou Y, Shoemaker M, Lobo M, Borman E, Baehner F, Kumar AS, Adduci K, Marx C, Petricoin EF, Liotta LA, Winters M, Benz S, Benz CC. Breast cancer growth prevention by statins. Cancer Res 2006, 66:8707-8714. 10.1158/0008-5472.CAN-05-4061, 16951186.
13. Kuhajda FP, Jenner K, Wood FD, Hennigar RA, Jacobs LB, Dick JD, Pasternack GR. Fatty acid synthesis: a potential selective target for antineoplastic therapy. Proc Natl Acad Sci USA 1994, 91:6379-6383. 10.1073/pnas.91.14.6379, 44205, 8022791.
14. Kotamraju S, Williams CL, Kalyanaraman B. Statin-induced breast cancer cell death: role of inducible nitric oxide and arginase-dependent pathways. Cancer Res 2007, 67:7386-7394. 10.1158/0008-5472.CAN-07-0993, 17671209.
15. Takeda I, Maruya S, Shirasaki T, Mizukami H, Takahata T, Myers JN, 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. 10.1111/j.1349-7006.2007.00471.x, 17428261.
16. Hirai A, Nakamura S, Noguchi Y, Yasuda T, Kitagawa M, Tatsuno I, Oeda T, Tahara K, Terano T, Narumiya S, Kohn LD, Saito Y. Geranylgeranylated rho small GTPase(s) are essential for the degradation of p27Kip1 and facilitate the progression from G1 to S phase in growth-stimulated rat FRTL-5 cells. J Biol Chem 1997, 272:13-16. 10.1074/jbc.272.1.13, 8995216.
17. Seillier-Moiseiwitsch F. The Proteomics Protocols Handbook. 2005, 239-258.
18. Biosciences A. Melanie: The 2D gel analysis software User Manual. 2004, Amersham Biosciences and Geneva Bioinformatics SA.
19. Laudi S, Steudel W, Jonscher K, Schoning W, Schniedewind B, Kaisers U, Christians U, Trump S. Comparison of lung proteome profiles in two rodent models of pulmonary arterial hypertension. Proteomics 2007, 7:2469-2478. 10.1002/pmic.200600848, 17623304.
20. Havlis J, Thomas H, Sebela M, Shevchenko A. Fast-response proteomics by accelerated in-gel digestion of proteins. Anal Chem 2003, 75:1300-1306. 10.1021/ac026136s, 12659189.
21. Serkova N, Brand A, Christians U, Leibfritz D. Evaluation of the effects of immunosuppressants on neuronal and glial cells in vitro by multinuclear magnetic resonance spectroscopy. Biochim Biophys Acta 1996, 1314:93-104. 10.1016/S0167-4889(96)00081-X, 8972722.
22. Klawitter J, Kominsky DJ, Brown JL, Klawitter J, Christians U, Leibfritz D, Melo JV, Eckhardt SG, Serkova NJ. Metabolic characteristics of imatinib resistance in chronic myeloid leukaemia cells. Br J Pharmacol 2009, 158:588-600. 10.1111/j.1476-5381.2009.00345.x, 19663881.
23. Kominsky DJ, Klawitter J, Brown JL, Boros LG, Melo JV, Eckhardt SG, Serkova NJ. Abnormalities in glucose uptake and metabolism in imatinib-resistant human BCR-ABL-positive cells. Clin Cancer Res 2009, 15:3442-3450. 10.1158/1078-0432.CCR-08-3291, 19401345.
24. Klawitter J, Anderson N, Klawitter J, Christians U, Leibfritz D, Eckhardt SG, Serkova NJ. Time-dependent effects of imatinib in human leukaemia cells: a kinetic NMR-profiling study. Br J Cancer 2009, 100:923-931. 10.1038/sj.bjc.6604946, 2661771, 19259085.
25. Zwingmann C, Leibfritz D, Hazell AS. Energy metabolism in astrocytes and neurons treated with manganese: relation among cell-specific energy failure, glucose metabolism, and intercellular trafficking using multinuclear NMR-spectroscopic analysis. J Cereb Blood Flow Metab 2003, 23:756-771. 10.1097/01.WCB.0000056062.25434.4D, 12796724.
26. Zwingmann C, Chatauret N, Leibfritz D, Butterworth RF. Selective increase of brain lactate synthesis in experimental acute liver failure: results of a [H-C] nuclear magnetic resonance study. Hepatology 2003, 37:420-428. 10.1053/jhep.2003.50052, 12540793.
27. Konstantinopoulos PA, Karamouzis MV, Papavassiliou AG. Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets. Nat Rev Drug Discov 2007, 6:541-555. 10.1038/nrd2221, 17585331.
28. Swanson KM, Hohl RJ. Anti-cancer therapy: targeting the mevalonate pathway. Curr Cancer Drug Targets 2006, 6:15-37. 10.2174/156800906775471743, 16475974.
29. Lei M. The MCM complex: its role in DNA replication and implications for cancer therapy. Curr Cancer Drug Targets 2005, 5:365-380. 10.2174/1568009054629654, 16101384.
30. Istvan ES, Deisenhofer J. Structural mechanism for statin inhibition of HMG-CoA reductase. Science 2001, 292:1160-1164. 10.1126/science.1059344, 11349148.
31. Liao JK. Isoprenoids as mediators of the biological effects of statins. J Clin Invest 2002, 110:285-288. 151100, 12163444.
32. Dimitroulakos J, Ye LY, Benzaquen M, Moore MJ, Kamel-Reid S, Freedman MH, Yeger H, Penn LZ. Differential sensitivity of various pediatric cancers and squamous cell carcinomas to lovastatin-induced apoptosis: therapeutic implications. Clin Cancer Res 2001, 7:158-167.
33. Hancock JF, Magee AI, Childs JE, Marshall CJ. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 1989, 57:1167-1177. 10.1016/0092-8674(89)90054-8, 2661017.
34. Mackay DJ, Hall A. Rho GTPases. J Biol Chem 1998, 273:20685-20688. 10.1074/jbc.273.33.20685, 9694808.
35. Casey PJ, Thissen JA, Moomaw JF. Enzymatic modification of proteins with a geranylgeranyl isoprenoid. Proc Natl Acad Sci USA 1991, 88:8631-8635. 10.1073/pnas.88.19.8631, 52563, 1924324.
36. Zhong WB, Wang CY, Chang TC, Lee WS. Lovastatin induces apoptosis of anaplastic thyroid cancer cells via inhibition of protein geranylgeranylation and de novo protein synthesis. Endocrinology 2003, 144:3852-3859. 10.1210/en.2003-0098, 12933658.
37. Javanmoghadam-Kamrani S, Keyomarsi K. Synchronization of the cell cycle using lovastatin. Cell Cycle 2008, 7:2434-2440.
38. Wong WW, Clendening JW, Martirosyan A, Boutros PC, Bros C, Khosravi F, Jurisica I, Stewart AK, Bergsagel PL, Penn LZ. Determinants of sensitivity to lovastatin-induced apoptosis in multiple myeloma. Mol Cancer Ther 2007, 6:1886-1897. 10.1158/1535-7163.MCT-06-0745, 17575117.
39. Xia Z, Tan MM, Wong WW, Dimitroulakos J, Minden MD, Penn LZ. Blocking protein geranylgeranylation is essential for lovastatin-induced apoptosis of human acute myeloid leukemia cells. Leukemia 2001, 15:1398-1407. 10.1038/sj.leu.2402196, 11516100.
40. Coleman ML, Olson MF. Rho GTPase signalling pathways in the morphological changes associated with apoptosis. Cell Death Differ 2002, 9:493-504. 10.1038/sj.cdd.4400987, 11973608.
41. Fritz G, Just I, Kaina B. Rho GTPases are over-expressed in human tumors. Int J Cancer 1999, 81:682-687. 10.1002/(SICI)1097-0215(19990531)81:5<682::AID-IJC2>3.0.CO;2-B, 10328216.
42. Etienne-Manneville S. Cdc42--the centre of polarity. J Cell Sci 2004, 117:1291-1300. 10.1242/jcs.01115, 15020669.
43. Tocque B, Delumeau I, Parker F, Maurier F, Multon MC, Schweighoffer F. Ras-GTPase activating protein (GAP): a putative effector for Ras. Cell Signal 1997, 9:153-158. 10.1016/S0898-6568(96)00135-0, 9113414.
44. Wang W, Eddy R, Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 2007, 7:429-440. 10.1038/nrc2148, 17522712.
45. Fernandez-Hernando C, Suarez Y, Lasuncion MA. Lovastatin-induced PC-12 cell differentiation is associated with RhoA/RhoA kinase pathway inactivation. Mol Cell Neurosci 2005, 29:591-602. 10.1016/j.mcn.2005.04.012, 15951198.
46. Luo Y, Hurwitz J, Massague J. Cell-cycle inhibition by independent CDK and PCNA binding domains in p21Cip1. Nature 1995, 375:159-161. 10.1038/375159a0, 7753174.
47. Gehen SC, Vitiello PF, Bambara RA, Keng PC, O'Reilly MA. Downregulation of PCNA potentiates p21-mediated growth inhibition in response to hyperoxia. Am J Physiol Lung Cell Mol Physiol 2007, 292:L716-724. 10.1152/ajplung.00135.2006, 17085526.
48. Sanchez CA, Rodriguez E, Varela E, Zapata E, Paez A, Masso FA, Montano LF, Lopez-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, 1.
49. Sanchez CA, Rodriguez E, Varela E, Zapata E, Paez A, Masso FA, Montano LF, 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. 10.1080/07357900701874658, 18608208.
50. Sivaprasad U, Abbas T, Dutta A. Differential efficacy of 3-hydroxy-3-methylglutaryl CoA reductase inhibitors on the cell cycle of prostate cancer cells. Mol Cancer Ther 2006, 5:2310-2316. 10.1158/1535-7163.MCT-06-0175, 16985065.
51. Cortez D, Glick G, Elledge SJ. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci USA 2004, 101:10078-10083. 10.1073/pnas.0403410101, 454167, 15210935.
52. Chang IY, Jin M, Yoon SP, Youn CK, Yoon Y, Moon SP, Hyun JW, Jun JY, You HJ. Senescence-dependent MutS alpha dysfunction attenuates mismatch repair. Mol Cancer Res 2008, 6:978-989. 10.1158/1541-7786.MCR-07-0380, 18567801.
53. Montesano Gesualdi N, Chirico G, Pirozzi G, Costantino E, Landriscina M, Esposito F. Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress 2007, 10:342-350. 10.1080/10253890701314863, 17853063.
54. Song JY, Lim JW, Kim H, Morio T, Kim KH. Oxidative stress induces nuclear loss of DNA repair proteins Ku70 and Ku80 and apoptosis in pancreatic acinar AR42J cells. J Biol Chem 2003, 278:36676-36687. 10.1074/jbc.M303692200, 12867423.
55. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314. 10.1126/science.123.3191.309, 13298683.
56. Plas DR, Thompson CB. Akt-dependent transformation: there is more to growth than just surviving. Oncogene 2005, 24:7435-7442. 10.1038/sj.onc.1209097, 16288290.
57. Li X, Lin G, Wu B, Zhou X, Zhou K. Overexpression of PTEN induces cell growth arrest and apoptosis in human breast cancer ZR-75-1 cells. Acta Biochim Biophys Sin (Shanghai) 2007, 39:745-750. 10.1111/j.1745-7270.2007.00337.x, 17928923.
58. Cantley LC, Neel BG. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci USA 1999, 96:4240-4245. 10.1073/pnas.96.8.4240, 33561, 10200246.
59. Mensah K, Mocanu MM, Yellon DM. Failure to protect the myocardium against ischemia/reperfusion injury after chronic atorvastatin treatment is recaptured by acute atorvastatin treatment: a potential role for phosphatase and tensin homolog deleted on chromosome ten?. J Am Coll Cardiol 2005, 45:1287-1291. 10.1016/j.jacc.2005.01.021, 15837263.
60. Teresi RE, Shaiu CW, Chen CS, Chatterjee VK, Waite KA, Eng C. Increased PTEN expression due to transcriptional activation of PPARgamma by Lovastatin and Rosiglitazone. Int J Cancer 2006, 118:2390-2398. 10.1002/ijc.21799, 16425225.
61. Teresi RE, Planchon SM, Waite KA, Eng C. Regulation of the PTEN promoter by statins and SREBP. Hum Mol Genet 2008, 17:919-928. 10.1093/hmg/ddm364, 18065496.
62. Kim RH, Peters M, Jang Y, Shi W, Pintilie M, Fletcher GC, DeLuca C, Liepa J, Zhou L, Snow B, Binari RC, Manoukian AS, Bray MR, Liu FF, Tsao MS, Mak TW. DJ-1, a novel regulator of the tumor suppressor PTEN. Cancer Cell 2005, 7:263-273. 10.1016/j.ccr.2005.02.010, 15766664.
63. Davidson B, Hadar R, Schlossberg A, Sternlicht T, Slipicevic A, Skrede M, Risberg B, Florenes VA, Kopolovic J, Reich R. Expression and clinical role of DJ-1, a negative regulator of PTEN, in ovarian carcinoma. Hum Pathol 2008, 39:87-95. 10.1016/j.humpath.2007.05.014, 17949781.
64. Nagakubo D, Taira T, Kitaura H, Ikeda M, Tamai K, Iguchi-Ariga SM, Ariga H. DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. Biochem Biophys Res Commun 1997, 231:509-513. 10.1006/bbrc.1997.6132, 9070310.
65. Bandyopadhyay S, Pai SK, Hirota S, Hosobe S, Tsukada T, Miura K, Takano Y, Saito K, Commes T, Piquemal D, Watabe M, Gross S, Wang Y, Huggenvik J, Watabe K. PTEN up-regulates the tumor metastasis suppressor gene Drg-1 in prostate and breast cancer. Cancer Res 2004, 64:7655-7660. 10.1158/0008-5472.CAN-04-1623, 15520163.
66. Baum CL, Reschly EJ, Gayen AK, Groh ME, Schadick K. Sterol carrier protein-2 overexpression enhances sterol cycling and inhibits cholesterol ester synthesis and high density lipoprotein cholesterol secretion. J Biol Chem 1997, 272:6490-6498. 10.1074/jbc.272.10.6490, 9045674.
67. Frolov A, Miller K, Billheimer JT, Cho TH, Schroeder F. Lipid specificity and location of the sterol carrier protein-2 fatty acid-binding site: a fluorescence displacement and energy transfer study. Lipids 1997, 32:1201-1209. 10.1007/s11745-997-0154-5, 9397406.