The inhibition of Ras farnesylation leads to an increase in p27Kip1 and G1 cell cycle arrest

European Journal of Biochemistry

Volumn 270, Issue 13, 2003, Pages 2759-2772

  Reuveni, Hadas ^a,b   Klein, Shoshana ^a   Levitzki, Alexander ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b AKEBIA THERAPEUTICS   (United States)

Author keywords

Cell cycle; Farnesyl transferase inhibitor (FTI); p27Kip1; Ras

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN E; CYSTEINE N METHYLVALINE N CYCLOHEXYLGLYCINE METHIONINE METHYL ESTER; HR 12; PROTEIN FARNESYLTRANSFERASE INHIBITOR; PROTEIN KIP 1; PROTEIN P27; RAS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; FARNESYLATION; FIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; RAT;

ANIMALS; CDC2-CDC28 KINASES; CELL ADHESION; CELL CYCLE PROTEINS; CELL DIVISION; CELL LINE; CYCLIN D1; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYCLINS; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLASTS; G1 PHASE; HUMANS; OLIGOPEPTIDES; PHOSPHORYLATION; PROTEIN ISOPRENYLATION; PROTEIN-SERINE-THREONINE KINASES; RAS PROTEINS; RATS; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0038052955     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03647.x     Document Type: Article

References (63)

1. Zhang, F.L. & Casey, P.J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65, 241-269.
2. Hancock, J.F., Magee, A.I., Childs, J.E. & Marshall, C.J. (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57, 1167-1177.
3. Jackson, J.H., Cochrane, C.G., Bourne, J.R., Solski, P.A., Der Buss, J.E., Cox, A.D., Hisaka, M.M., Graham, S.M., Der Buss, J.E.&., C.J. (1992) Isoprenoid addition to Ras protein is the critical modification for its membrane association and transforming activity. Proc. Natl Acad. Sci. USA 89, 6403-6407.
4. Kato, K., Cox, A.D., Hisaka, M.M., Graham, S.M., Buss, J.E. and Der, C.J. (1992) Isoprenoid addition to Ras protein is the critical modification for its membrane association and transforming activity. Proc. Natl Acad. Sci. USA, 89, 6403-6407.
5. Reuveni, H., Gitler, A., Poradosu, E., Gilon, C. & Levitzki, A. (1997) Synthesis and biological activity of semipeptoid farnesyltransferase inhibitors. Bioorg. Med. Chem. 5, 85-92.
6. Reuveni, H., Geiger, T., Geiger, B. & Levitzki, A. (2000) Reversal of the ras-induced transformed phenotype by HR12, a novel ras farnesylation inhibitor, is mediated by the Mek/Erk pathway. J. Cell Biol. 151, 1179-1192.
7. Frixen, U.H., Behrens, J., Sachs, M., Eberle, G., Voss, B., Warda, A., Lochner, D. & Birchmeier, W. (1991) E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J. Cell Biol. 113, 173-185.
8. Vleminckx, K., Vakaet, L. Jr, Mareel, M., Fiers, W. & van Roy, F. (1991) Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66, 107-119.
9. Perl, A.K., Wilgenbus, P., Dahl, U., Semb, H. & Christofori, G. (1998) A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392, 190-193.
10. Birchmeier, W. & Behrens, J. (1994) Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta 1198, 11-26.
11. Levenberg, S., Yarden, A., Kam, Z. & Geiger, B. (1999) p27 is involved in N-cadherin-mediated contact inhibition of cell growth and S-phase entry. Oncogene 18, 869-876.
12. St. Croix, B., Sheehan, C., Rak, J.W., Florenes, V.A., Slingerland, J.M. & Kerbel, R.S. (1998) E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27 (KIP1). J. Cell Biol. 142, 557-571.
13. Sherr, C.J. (1993) Mammalian G1 cyclins. Cell 73, 1059-1065.
14. Draetta, G.F. (1994) Mammalian G1 cyclins. Curr. Opin. Cell Biol. 6, 842-846.
15. Sherr, C.J. & Roberts, J.M. (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9, 1149-1163.
16. Massague, J. & Roberts, J.M. (1995) Cell cycle 1995: constructing cell physiology with molecular building blocks. Curr. Opin. Cell Biol. 7, 769-772.
17. Guan, K.L., Jenkins, C.W., Li, Y., Nichols, M.A., Wu, X., O'Keefe, C.L., Matera, A.G. & Xiong, Y. (1994) Growth suppression by p18, a p16INK4/MTS1- and p14INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev. 8, 2939-2952.
18. Coats, S., Flanagan, W.M., Nourse, J. & Roberts, J.M. (1996) Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272, 877-880.
19. Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K. & Elledge, S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816.
20. Polyak, K., Lee, M.H., Erdjument-Bromage, H., Koff, A., Roberts, J.M., Tempst, P. & Massague, J. (1994) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78, 59-66.
21. Rivard, N., L'Allemain, G., Bartek, J. & Pouyssegur, J. (1996) Abrogation of p27Kip1 by cDNA antisense suppresses quiescence (G0 state) in fibroblasts. J. Biol. Chem. 271, 18337-18341.
22. Cai, H., Szeberenyi, J. & Cooper, G.M. (1990) Effect of a dominant inhibitory Ha-ras mutation on mitogenic signal transduction in NIH 3T3 cells. Mol. Cell Biol. 10, 5314-5323.
23. Feig, L.A. & Cooper, G.M. (1988) Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell Biol. 8, 3235-3243.
24. Mulcahy, L.S., Smith, M.R. & Stacey, D.W. (1985) Requirement for ras proto-oncogene function during serum-stimulated growth of NIH 3T3 cells. Nature 313, 241-243.
25. Aktas, H., Cai, H. & Cooper, G.M. (1997) Ras links growth factor signaling to the cell cycle machinery via regulation of cyclin D1 and the Cdk inhibitor p27KIP1. Mol. Cell Biol. 17, 3850-3857.
26. Takuwa, N. & Takuwa, Y. (1997) Ras activity late in G1 phase required for p27kip1 downregulation, passage through the restriction point, and entry into S phase in growth factor-stimulated NIH 3T3 fibroblasts. Mol. Cell Biol. 17, 5348-5358.
27. Weber, J.D., Hu, W., Jefcoat, S.C. Jr, Raben, D.M. & Baldassare, J.J. (1997) Ras-stimulated extracellular signal-related kinase I and RhoA activities coordinate platelet-derived growth factor-induced G1 progression through the independent regulation of cyclin D1 and p27. J. Biol. Chem. 272, 32966-32971.
28. Kawada, M., Yamagoe, S., Murakami, Y., Suzuki, K., Mizuno, S. & Uehara, Y. (1997) Induction of p27Kip1 degradation and anchorage independence by Ras through the MAP kinase signaling pathway. Oncogene 15, 629-637.
29. Rivard, N., Boucher, M.J., Asselin, C. & L'Allemain, G. (1999) MAP kinase cascade is required for p27 downregulation and S phase entry in fibroblasts and epithelial cells. Am. J. Physiol. 277, C652-C664.
30. Slingerland, J. & Pagano, M. (2000) Regulation of the cdk inhibitor p27 and its deregulation in cancer. J. Cell Physiol. 183, 10-17.
31. Sgambato, A., Cittadini, A., Faraglia, B. & Weinstein, I.B. (2000) Multiple functions of p27 (Kip1) and its alterations in tumor cells: a review. J. Cell Physiol. 183, 18-27.
32. Du, W., Lebowitz, P.F. & Prendergast, G.C. (1999) Cell growth inhibition by farnesyltransferase inhibitors is mediated by gain of geranylgeranylated RhoB. Mol. Cell Biol. 19, 1831-1840.
33. Ashar, H., James, L., Gray, K., Carr, D., McGuirk, M., Maxwell, E., Black, S., Armstrong, L., Doll, R., Taveras, A., Bishop, W. & Kirschmeier, P. (2001) The farnesyl transferase inhibitor SCH 66336 induces a G (2) → M or G (1) pause in sensitive human tumor cell lines. Exp. Cell Res. 262, 17-27.
34. Lebowitz, P. & Prendergast, G. (1998) Non-Ras targets of farnesyltransferase inhibitors: focus on Rho. Oncogene 17, 1439-1445.
35. Prendergast, G. & Oliff, A. (2000) Farnesyltransferase inhibitors: antineoplastic properties, mechanisms of action, and clinical prospects. Cancer Biol. 10, 443-452.
36. Haklai, R., Weisz, M.G., Elad, G., Paz, A., Marciano, D., Egozi, Y., Ben-Baruch, G. & Kloog, Y. (1998) Dislodgment and accelerated degradation of Ras. Biochemistry 37, 1306-1314.
37. Horowitz, D. & King, A.G. (2000) Colorimetric determination of inhibition of hematopoietic progenitor cells in soft agar. J. Immunol. Methods 244, 49-58.
38. Resnitzky, D., Hengst, L. & Reed, S.I. (1995) Cyclin A-associated kinase activity is rate limiting for entrance into S phase and is negatively regulated in G1 by p27Kip1. Mol. Cell Biol. 15, 4347-4352.
39. Agrawal, D., Hauser, P., McPherson, F., Dong, F., Garcia, A. & Pledger, W.J. (1996) Repression of p27kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol. Cell Biol. 16, 4327-4336.
40. Pagano, M., Tam, S.W., Theodoras, A.M., Beer-Romero, P., Del Sal, G., Chau, V., Yew, P.R., Draetta, G.F. & Rolfe, M. (1995) Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269, 682-685.
41. Medema, R.H., Kops, G.J., Bos, J.L. & Burgering, B.M. (2000) AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404, 782-787.
42. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. & Goldberg, A.L. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761-771.
43. Palombella, V.J., Rando, O.J., Goldberg, A.L. & Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78, 773-785.
44. Prendergast, G.C. (2000) Farnesyltransferase inhibitors: antineoplastic mechanism and clinical prospects. Curr. Opin. Cell Biol. 12, 166-173.
45. Prendergast, G.C., Davide, J.P., deSolms, S.J., Giuliani, E.A., Graham, S.L., Gibbs, J.B., Oliff, A. & Kohl, N.E. (1994) Farnesyltransferase inhibition causes morphological reversion of ras-transformed cells by a complex mechanism that involves regulation of the actin cytoskeleton. Mol. Cell Biol. 14, 4193-4202.
46. Zhang, H., Hannon, G.J. & Beach, D. (1994) p21-containing cyclin kinases exist in both active and inactive states. Genes Dev 8, 1750-1758.
47. LaBaer, J., Garrett, M.D., Stevenson, L.F., Slingerland, J.M., Sandhu, C., Chou, H.S., Fattaey, A. & Harlow, E. (1997) New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11, 847-862.
48. Cheng, M., Olivier, P., Diehl, J.A., Fero, M., Roussel, M.F., Roberts, J.M. & Sherr, C.J. (1999) The p21 (Cip1) and p27 (Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18, 1571-1583.
49. Du, W. & Prendergast, G. (1999) Geranylgeranylated RhoB mediates suppression of human tumor cell growth by farnesyl-transferase inhibitors. Cancer Res. 59, 5492-5496.
50. Hengst, L. & Reed, S.I. (1996) Translational control of p27Kip1 accumulation during the cell cycle. Science 271, 1861-1864.
51. Hirai, A., Nakamura, S., Noguchi, Y., Yasuda, T., Kitagawa, M., Tatsuno, I., Oeda, T., Tahara, K., Terano, T., Narumiya, S., Kohn, L.D. & Saito, Y. (1997) 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. 272, 13-16.
52. Vidal, A., Millard, S.S., Miller, J.P. & Koff, A. (2002) Rho activity can alter the translation of p27 mRNA and is important for RasV12-induced transformation in a manner dependent on p27 status. J. Biol. Chem. 277, 16433-16440.
53. Zohn, I.M., Campbell, S.L., Khosravi-Far, R., Der Rossman, K.L.&.,.Bellone, C.J. & Baldassare, J.J. (1999) RhoA stimulates p27 (Kip) degradation through its regulation of cyclin E/CDK2 activity. J. Biol. Chem. 274, 3396-3401.
54. Hu, W., Bellone, C.J. & Baldassare, J.J. (1999) RhoA stimulates p27(Kip) degradation through its regulation of cyclin E/CDK2 activity. J. Biol. Chem. 274, 3396-3401.
55. Sheaff, R.J., Groudine, M., Gordon, M., Roberts, J.M. & Clurman, B.E. (1997) Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11, 1464-1478.
56. Vlach, J., Hennecke, S. & Amati, B. (1997) Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16, 5334-5344.
57. Potempa, S. & Ridley, A.J. (1998) Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol. Biol. Cell 9, 2185-2200.
58. Muise-Helmericks, R.C., Grimes, H.L., Bellacosa, A., Malstrom, S.E., Tsichlis, P.N. & Rosen, N. (1998) Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J. Biol. Chem. 273, 29864-29872.
59. Diehl, J.A., Cheng, M., Roussel, M.F. & Sherr, C.J. (1998) Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12, 3499-3511.
60. Diehl, J.A., Zindy, F. & Sherr, C.J. (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11, 957-972.
61. Frame, S. & Balmain, A. (2000) Integration of positive and negative growth signals during ras pathway activation in vivo. Curr. Opin. Genet. Dev. 10, 106-113.
62. Chen, D., Walsh, K. & Wang, J. (2000) Regulation of cdk2 activity in endothelial cells that are inhibited from growth by cell contact. Arterioscler. Thromb. Vasc. Biol. 20, 629-635.
63. Sahai, E., Olson, M.F. & Marshall, C.J. (2001) Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility. EMBO J. 20, 755-766.