Inhibition of farnesyl protein transferase sensitizes human MCF-7 breast cancer cells to roscovitine-mediated cell cycle arrest

Journal of Cellular Biochemistry

Volumn 102, Issue 3, 2007, Pages 736-747

  Wȩsierska Ga̧dek, Józefa ^a   Maurer, Margarita ^a   Schmid, Gerald ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

CDK inhibitors; G2 cell cycle arrest; p53 activation; Signal transduction

Indexed keywords

2 [[2 [[2 [(2 AMINO 3 MERCAPTOPROPYL)AMINO] 3 METHYLPENTYL]OXY] 1 OXO 3 PHENYLPROPYL]AMINO] 4 (METHYLSULFONYL)BUTANOIC ACID ISOPROPYL ESTER; CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN FARNESYLTRANSFERASE; PROTEIN FARNESYLTRANSFERASE INHIBITOR; PROTEIN P53; ROSCOVITINE;

APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; ONCOGENE C H RAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

CELL CYCLE; CELL LINE, TUMOR; CELL SEPARATION; FARNESYLTRANSTRANSFERASE; FLOW CYTOMETRY; G2 PHASE; GENES, P53; HUMANS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS P21(RAS); PURINES; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 35048874800     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21325     Document Type: Article

References (53)

1. Bargonetti J, Manfredi JJ. 2002. Multiple roles of the tumor suppressor p53. Curr Opin Oncol 14:86-91.
2. Blagosklonny MV. 2002. P53: An ubiquitous target of anticancer drugs. Int J Cancer 98:161-166.
3. Cantley LC. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
4. Chong H, Vikis HG, Guan KL. 2003. Mechanisms of regulating the Raf kinase family. Cell Signal 15:463-469.
5. Cohen-Jonathan E, Evans SM, Koch CJ, Muschel RJ, McKenna WG, Wu J, Bernhard EJ. 2001. The farnesyltransferase inhibitor L744,832 reduces hypoxia in tumors expressing activated H-ras. Cancer Res 61:2289-2293.
6. David-Pfeuty T. 1999. Potent inhibitors of cyclin-dependent kinase 2 induce nuclear accumulation of wild-type p53 and nucleolar fragmentation in human untransformed and tumor-derived cells. Oncogene 18:7409-7422.
7. De Azevedo WF, Leclerc S, Meijer L, Havlicek L, Strnad M, Kim SH. 1997. Inhibition of cyclin-dependent kinases by purine analogues: Crystal structure of human cdk2 complexed with roscovitine. Eur J Biochem 243:518-526.
8. de la Motte S, Gianella-Borradori A. 2004. Pharmacokinetic model of R-roscovitine and its metabolite in healthy male subjects. Int J Clin Pharmacol Ther 42:232-239.
9. Delmas C, Heliez C, Cohen-Jonathan E, End D, Bonnet J, Favre G, Toulas C. 2002. Farnesyltransferase inhibitor, R115777, reverses the resistance of human glioma cell lines to ionizing radiation. Int J Cancer 100:43-48.
10. Eckert LB, Repasky GA, Ulku AS, McFall A, Zhou H, Sartor CI, Der CJ. 2004. Involvement of Ras activation in human breast cancer cell signaling, invasion, and anoikis. Cancer Res 64:4585-4592.
11. Edamatsu H, Gau CL, Nemoto T, Guo L, Tamanoi F. 2000. Cdk inhibitors, roscovitine and olomoucine, synergize with farnesyltransferase inhibitor (FTI) to induce efficient apoptosis of human cancer cell lines. Oncogene 19:3059-3068.
12. Fischer PM, Gianella-Borradori A. 2005. Recent progress in the discovery and development of cyclin-dependent kinase inhibitors. Expert Opin Invest Drugs 14:457-477.
13. Fokstuen T, Rabo YB, Zhou JN, Karlson J, Platz A, Shoshan MC, Hansson J, Linder S. 1997. The Ras farnesylation inhibitor BZA-5B increases the resistance to cisplatin in a human melanoma cell line. Anticancer Res 17:2347-2352.
14. Gibbs JB, Oliff A, Kohl NE. 1994. Farnesyltransferase inhibitors: Ras research yields a potential cancer therapeutic. Cell 77:175-178.
15. Gray N, Detivaud L, Doerig C, Meijer L. 1999. ATP-site directed inhibitors of cyclin-dependent kinases. Curr Med Chem 6:859-875.
16. Jacks T, Weinberg RA. 1998. The expanding role of cell cycle regulators. Science 280:1035-1036.
17. Janicke RU, Sprengart ML, Wati MR, Porter AG. 1998. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273:9357-9360.
18. Khwaja A, Dockrell ME, Hendry BM, Sharpe CC. 2006. Prenylation is not necessary for endogenous Ras activation in non-malignant cells. J Cell Biochem 97:412-422.
19. Koch S, Mayer F, Honecker F, Schittenhelm M, Bokemeyer C. 2003. Efficacy of cytotoxic agents used in the treatment of testicular germ cell tumours under normoxic and hypoxic conditions in vitro. Br J Cancer 89:2133-2139.
20. Kotala V, Uldrijan S, Horky M, Trbusek M, Strnad M, Vojtesek B. 2001. Potent induction of wild-type p53-dependent transcription in tumour cells by a synthetic inhibitor of cyclin-dependent kinases. Cell Mol Life Sci 58:1333-1339.
21. Ljungman M, Paulsen MT. 2001. The cyclin-dependent kinase inhibitor roscovitine inhibits RNA synthesis and triggers nuclear accumulation of p53 that is unmodified at Ser15 and Lys382. Mol Pharmacol 60:785-789.
22. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243:527-536.
23. Moasser MM, Sepp-Lorenzino L, Kohl NE, Oliff A, Balog A, Su DS, Danishefsky SJ, Rosen N. 1998. Farnesyl transferase inhibitors cause enhanced mitotic sensitivity to taxol and epothilones. Proc Natl Acad Sci U S A 95:1369-1374.
24. Motokura T, Arnold A. 1993. Cyclins and oncogenesis. Biochim Biophys Acta 1155:63-78.
25. Nakade K, Zheng H, Ganguli G, Buchwalter G, Gross C, Wasylyk B. 2004. The tumor suppressor p53 inhibits Net, an effector of Ras/extracellular signal-regulated kinase signaling. Mol Cell Biol 24:1132-1142.
26. North S, Pluquet O, Maurici D, El-Ghissassi F, Hainaut P. 2002. Restoration of wild-type conformation and activity of a temperature-sensitive mutant of p53 (p53(V272M)) by the cytoprotective aminothiol WR1065 in the esophageal cancer cell line TE-1. Mol Carcinog 33:181-188.
27. Nurse P. 1997. Reductionism. The ends of understanding. Nature 387:657.
28. Nurse P. 2002. Cyclin dependent kinases and cell cycle control (nobel lecture). Chembiochem 3:596-603.
29. Prendergast GC. 2000. Farnesyltransferase inhibitors: Antineoplastic mechanism and clinical prospects. Curr Opin Cell Biol 12:166-173.
30. Prives C, Hall PA. 1999. The p53 pathway. J Pathol 187: 112-126.
31. Rodriguez-Puebla ML, Robles AI, Conti CJ. 1999. ras activity and cyclin D1 expression: An essential mechanism of mouse skin tumor development. Mol Carcinog 24:1-6.
32. Senderowicz AM. 2003. Small-molecule cyclin-dependent kinase modulators. Oncogene 22:6609-6620.
33. Sherr CJ, Roberts JM. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512.
34. Sizemore N, Cox AD, Barnard JA, Oldham SM, Reynolds ER, Der CJ, Coffey RJ. 1999. Pharmacological inhibition of Ras-transformed epithelial cell growth is linked to down-regulation of epidermal growth factor-related peptides. Gastroenterology 117:567-576.
35. Smalley KS, Eisen TG. 2003. Farnesyl transferase inhibitor SCH66336 is cytostatic, pro-apoptotic and enhances chemosensitivity to cisplatin in melanoma cells. Int J Cancer 105:165-175.
36. Song X, Liu X, Chi W, Liu Y, Wei L, Wang X, Yu J. 2006. Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1alpha gene. Cancer Chemother Pharmacol 58:776-784.
37. Toledo F, Wahl GM. 2006. Regulating the p53 pathway: In vitro hypotheses, in vivo veritas. Nat Rev Cancer 6:909-923.
38. van den Heuvel S, Harlow E. 1993. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 262:2050-2054.
39. Vindelov LL, Christensen IJ, Nissen NI. 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3:323-327.
40. Vogelstein B, Kinzler KW. 2004. Cancer genes and the pathways they control. Nat Med 10:789-799.
41. Weinberg RA. 1996. The molecular basis of carcinogenesis: Understanding the cell cycle clock. Cytokines Mol Ther 2:105-110.
42. Wesierska-Gadek J. 2005. Major contribution of the multidrug transporter P-glycoprotein to reduced susceptibility of poly(ADP-ribose) polymerase-1 knock-out cells to doxorubicin action. J Cell Biochem 95:1012-1028.
43. Wesierska-Gadek J, Schmid G. 2000. Overexpressed poly-(ADP-ribose) polymerase delays the release of rat cells from p53-mediated G(1) checkpoint. J Cell Biochem 80:85-103.
44. Wesierska-Gadek J, Hohenauer H, Hitchman E, Penner E. 1995. Autoantibodies from patients with primary biliary cirrhosis preferentially react with the amino-terminal domain of nuclear pore complex glycoprotein gp210. J Exp Med 182:1159-1162.
45. Wesierska-Gadek J, Bugajska-Schretter A, Cerni C. 1996. ADP-ribosylation of p53 tumor suppressor protein: Mutant but not wild-type p53 is modified. J Cell Biochem 62:90-101.
46. Wesierska-Gadek J, Schloffer D, Kotala V, Horky M. 2002. Escape of p53 protein from E6-mediated degradation in HeLa cells after cisplatin therapy. Int J Cancer 101:128-136.
47. Wesierska-Gadek J, Gueorguieva M, Horky M. 2003. Dual action of cyclin-dependent kinase inhibitors: Induction of cell cycle arrest and apoptosis. A comparison of the effects exerted by roscovitine and cisplatin. Pol J Pharmacol 55:895-902.
48. Wesierska-Gadek J, Gueorguieva M, Horky M. 2005a. Roscovitine-induced up-regulation of p53AIP1 protein precedes the onset of apoptosis in human MCF-7 breast cancer cells. Mol Cancer Ther 4:113-124.
49. Wesierska-Gadek J, Gueorguieva M, Ranftler C, Zerza-Schnitzhofer G. 2005b. A new multiplex assay allowing simultaneous detection of the inhibition of cell proliferation and induction of cell death. J Cell Biochem 96:1-7.
50. Wesierska-Gadek J, Kramer M, Schmid G. 2006a. Prevention of farnesylation of c-Ha-Ras protein enhances synergistically the cytotoxic action of doxorubicin in cycling but not in quiescent cells. J Cell Biochem 99:1664-1676.
51. Wesierska-Gadek J, Schreiner T, Gueorguieva M, Ranftler C. 2006b. Phenol red reduces ROSC mediated cell cycle arrest and apoptosis in human MCF-7 cells. J Cell Biochem 98:1367-1379.
52. Wesierska-Gadek J, Schmitz C-L, Ranftler C. 2007. Roscovitine-activated HIP2 kinase induces phosphorylation of wt p53 at Ser-46 in human MCF-7 breast cancer cells. J Cell Biochem in press
53. Wojciechowski J, Horky M, Gueorguieva M, Wesierska-Gadek J. 2003. Rapid onset of nucleolar disintegration preceding cell cycle arrest in roscovitine-induced apoptosis of human MCF-7 breast cancer cells. Int J Cancer 106:486-495.