Arrest of mammalian fibroblasts in G1 in response to actin inhibition is dependent on retinoblastoma pocket proteins but not on p53

Journal of Cell Biology

Volumn 161, Issue 1, 2003, Pages 67-77

  Lohez, Olivier D ^a   Reynaud, Caroline ^a   Borel, Franck ^a   Andreassen, Paul R ^a,b   Margolis, Robert L ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Aneuploidy; Cell cycle; Cytoskeleton; Dihydrocytochalasin B; Tetraploidy

Indexed keywords

ACTIN; ANTINEOPLASTIC AGENT; CYTOCHALASIN D; DIHYDROCYTOCHALASIN B; HYDROXYUREA; LATRUNCULIN A; MERLIN; NOCODAZOLE; PROTEIN INHIBITOR; PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS LARGE T ANTIGEN;

ANEUPLOIDY; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ADHESION; CELL CYCLE G1 PHASE; CELL DEATH; CELL DIVISION; CELL SURFACE; CELL TRANSFORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; EMBRYO; EMBRYO CELL; FIBROBLAST; GROWTH REGULATION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; RAT; REGULATORY MECHANISM; TETRAPLOIDY;

ACTINS; ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL ADHESION; CELL CYCLE PROTEINS; CELL DEATH; CELL MEMBRANE; CELL SIZE; CYTOCHALASIN B; DOSE-RESPONSE RELATIONSHIP, DRUG; FETUS; FIBROBLASTS; G1 PHASE; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; NEUROFIBROMIN 2; PROTEIN SYNTHESIS INHIBITORS; REACTION TIME; RETINOBLASTOMA PROTEIN; THIAZOLES; THIAZOLIDINES; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; FALCO COLUMBARIUS; MAMMALIA;

EID: 0037437151     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200208140     Document Type: Article

References (67)

1. Andreassen, P.R., and R.L. Margolis. 1994. Microtubule dependency of p34cdc2 inactivation and mitotic exit in mammalian cells. J. Cell Biol. 127:789-802.
2. Andreassen, P.R., F.B. Lacroix, O.D. Lohez, and R.L. Margolis. 2001a. Neither p21WAFI nor 14-3-3σ prevents G2 progression to mitotic catastrophe in human colon carcinoma cells after DNA damage, but p21WAF1 induces stable G1 arrest in resulting tetraploid cells. Cancer Res. 61:7660-7668.
3. Andreassen, P.R., O.D. Lohez, F.B. Lacroix, and R.L. Margolis. 2001b. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell. 12:1315-1328.
4. Aplin, A.E., S.M. Short, and R.L. Juliano. 1999. Anchorage-dependent regulation of the mitogen-activated protein kinase cascade by growth factors is supported by a variety ofintegrin α chains. J. Biol. Chem. 274:31223-31228.
5. Assoian, R.K. 1997. Anchorage-dependent cell cycle progression. J. Cell Biol. 136:1-4.
6. Assoian, R.K., and M.A. Schwartz. 2001. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11:48-53.
7. Assoian, R.K., and X. Zhu. 1997. Cell anchorage and the cytoskeleton as partners in growth factor dependent cell cycle progression. Curr. Opin. Cell Biol. 9:93-98.
8. Aubin, J.E., M. Osborn, and K. Weber. 1981. Inhibition of cytokinesis and altered contractile ring morphology induced by cytochalasins in synchronized PtK2 cells. Exp. Cell Res. 136:63-79.
9. Bargonetti, J., I. Reynisdottir, P.N. Friedman, and C. Prives. 1992. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 6:1886-1898.
10. Bashour, A.M., J.J. Meng, W. Ip, M. MacCollin, and N. Ratner. 2002. The neurofibromatosis type 2 gene product, merlin, reverses the F-actin cytoskeletal defects in primary human Schwannoma cells. Mol. Cell. Biol. 22:1150-1157.
11. Blajeski, A.L., T.J. Kottke, and S.H. Kaufmann. 2001. A multistep model for paclitaxel-induced apoptosis in human breast cancer cell lines. Exp. Cell Res. 270:277-288.
12. Bohmer, R.M., E. Scharf, and R.K. Assoian. 1996. Cytoskeletal integrity is required throughout the mitogen stimulation phase of the cell cycle and mediates the anchorage-dependent expression of cyclin D1. Mol. Biol. Cell. 7:101-111.
13. Borel, F., F.B. Lacroix, and R.L. Margolis. 2002a. Prolonged arrest of mammalian cells at the G1/S boundary results in permanent S phase stasis. J. Cell Sci. 115:2829-2838.
14. Borel, F., O.D. Lohez, F.B. Lacroix, and R.L. Margolis. 2002b. Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc. Natl. Acad. Sci. USA. 99:9819-9824.
15. Brenot-Bosc, F., S. Gupta, R.L. Margolis, and R. Fotedar. 1995. Changes in the subcellular localization of replication initiation proteins and cell cycle proteins during G1- to S-phase transition in mammalian cells. Chromosoma. 103:517-527.
16. Cross, S.M., C.A. Sanchez, C.A. Morgan, M.K. Schimke, S. Ramel, R.L Idzerda, W.H. Raskind, and B.J. Reid. 1995. A p53-dependent mouse spindle checkpoint. Science. 267:1353-1356.
17. Dannenberg, J.H., A. van Rossum, L. Schuijff, and H. te Riele. 2000. Ablation of the retinoblastoma gene family deregulates G(1) control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev. 14:3051-3064.
18. Delmas, C., S. Manenti, A. Boudjelal, C. Peyssonnaux, A. Eychene, and J.M. Darbon. 2001. The p42/p44 mitogen-activated protein kinase activation triggers p27Kipl degradation independently of CDK2/cyclin E in NIH 3T3 cells. J. Biol. Chem. 276:34958-34965.
19. Di Leonardo, A., S.P. Linke, K. Clarkin, and G.M. Wahl. 1994. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cipl in normal human fibroblasts. Genes Dev. 8:2540-2551.
20. Di Leonardo, A., S.H. Khan, S.P. Linke, V. Greco, G. Seidita, and G.M. Wahl. 1997. DNA rereplication in the presence of mitotic spindle inhibitors in human and mouse fibroblasts lacking either p53 or pRb function, Cancer Res. 57:1013-1019.
21. Dulic, V., W.K. Kaufmann, S.J. Wilson, T.D. Tlsty, E. Lees, J.W. Harper, S.J. Elledge, and S.I. Reed. 1994. p53-dependent inhibition ofcyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell. 76:1013-1023.
22. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
23. el-Deiry, W.S., T. Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D. Lin, W.E. Mercer, K.W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell. 75:817-825.
24. Gautreau, A., D. Louvard, and M. Arpin. 2002. ERM proteins and NF2 tumor suppressor: the Yin and Yang of cortical actin organization and cell growth signaling. Curr. Opin. Cell Biol. 14:104-109.
25. Hanahan, D., and R.A. Weinberg. 2000. The hallmarks of cancer. Cell. 100:57-70.
26. Howe, A., A.E. Aplin, S.K. Alahari, and R.L. Juliano. 1998. Integrin signaling and cell growth control. Curr. Opin. Cell Biol. 10:220-231.
27. Huang, S., C.S. Chen, and D.E. Ingber. 1998. Control of cyclin D1, p27(Kipl), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol. Biol. Cell. 9:3179-3193.
28. Iliakis, G. 1991. The role of DNA double strand breaks in ionizing radiation-induced killing of eukaryotic cells. Bioessays. 13:641-648.
29. Iwig, M., E. Czeslick, A. Muller, M. Gruner, M. Spindler, and D. Glaesser. 1995. Growth regulation by cell shape alteration and organization of the cytoskeleton. Eur. J. Cell Biol. 67:145-157.
30. Jordan, M.A., and L. Wilson. 1998. Microtubules and actin filaments: dynamic targets for cancer chemotherapy. Curr. Opin. Cell Biol. 10:123-130.
31. Jordan, M.A., D. Thrower, and L. Wilson. 1992. Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis. J. Cell Sci. 102:401-416.
32. Kastan, M.B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R.W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
33. Lanni, J.S., and T. Jacks. 1998. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18:1055-1064.
34. Lavoie, J.N., G. L'Allemain, A. Brunet, R. Muller, and J. Pouyssegur. 1996. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem. 271:20608-20616.
35. Le Gall, M., D. Grall, J.C. Chambard, J. Pouyssegur, and E. Van Obberghen-Schilling. 1998. An anchorage-dependent signal distinct from p42/44 MAP kinase activation is required for cell cycle progression. Oncogene. 17:1271-1277.
36. Levine, A.J. 1997. p53, the cellular gatekeeper for growth and division. Cell. 88:323-331.
37. Lin, T.H., Q: Chen, A. Howe, and R.L. Juliano. 1997. Cell anchorage permits efficient signal transduction between ras and its downstream kinases. J. Biol. Chem. 272:8849-8852.
38. Linke, S.P., K.C. Clarkin, A. Di Leonardo, A. Tsou, and G.M. Wahl. 1996. A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:934-947.
39. Maness, P.F., and R.C. Walsh, Jr. 1982. Dihydrocytochalasin B disorganizes actin cytoarchitecture and inhibits initiation of DNA synthesis in 3T3 cells. Cell. 30:253-262.
40. Martineau, S.N., P.R. Andreassen, and R.L. Margolis. 1995. Delay of HeLa cell cleavage into interphase using dihydrocytochalasin B: retention of a postmitotic spindle and telophase disc correlates with synchronous cleavage recovery. J. Cell Biol. 131:191-205.
41. Minn, A.J., L.H. Boise, and C.B. Thompson. 1996. Expression of Bcl-xL and loss of p53 an cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage. Genes Dev. 10:2621-2631
42. Mittnacht, S. 1998. Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8:21-27.
43. Morrison, H., L.S. Sherman, J. Legg, F. Banine, C. Isacke, C.A. Haipek, D.H. Gutmann, H. Ponta, and P. Herrlich. 2001. The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev. 15:968-980.
44. Mulligan, G., and T. Jacks. 1998. The retinoblastoma gene family: cousins with overlapping interests. Trends Genet. 14:223-229.
45. Perry, M.E., M. Commane, and G.R. Stark. 1992. Simian virus 40 large tumor antigen alone or two cooperating oncogenes convert REF52 cells to a state permissive for gene amplification. Proc. Natl. Acad. Sci. USA., 89:8112-8116.
46. Polyak, K., J.Y. Kato, M.J. Solomon, C.J. Sherr, J. Massague, J.M. Roberts, and A. Koff. 1994a. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
47. Polyak, K., M.H. Lee, H. Erdjument-Bromage, A. Koff, J.M. Roberts, P. Tempst, and J. Massague. 1994b. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:59-66.
48. Renshaw, M.W., X.D. Ren, and M.A. Schwartz. 1997. Growth factor activation of MAP kinase requires cell adhesion. EMBOJ. 16:5592-5599.
49. Reshemikova, G., R. Barkan, B. Popov, N. Nikolsky, and L.S. Chang. 2000. Disruption of the actin cytoskeleton leads to inhibition of mitogen-induced cyclin E expression, Cdk2 phosphorylation, and nuclear accumulation of the retinoblastoma protein-related p107 protein. Exp. CellRes. 259:35-53.
50. Rivard, N., M.J. Bouchet, C. Asselin, and G. L'Allemain. 1999. MAP kinase cascade is required for p27 downregulation and S phase entry in fibroblasts and epithelial cells. Am. J. Physiol. 277:C652-C664.
51. Sage, J., G.J. Mulligan, L.D. Attardi, A. Miller, S. Chen, B. Williams, E. Theodorou, and T. Jacks. 2000. Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev. 14:3037-3050.
52. Shaulian, E., A. Zauberman, D. Ginsberg, and M. Oren. 1992. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol. Cell. Biol. 12:5581-5592.
53. Shaw, R.J., A.I. McClatchey, and T. Jacks. 1998. Regulation of the neurofibromatosis type 2 tumor suppressor protein, merlin, by adhesion and growth arrest stimuli. J. Biol. Chem. 273:7757-7764.
54. Sherr, C.J. 1996. Cancer cell cycles. Science. 274:1672-1677.
55. Sherr, C.J., and J.M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
56. Sherr, C.J., and J.M. Roberts. 1999. CDK inhibitors: positive and negative regulators of Gl-phase progression. Genes Dev. 13:1501-1512.
57. Sherr, C.J., and J.D. Weber. 2000. The ARF/p53 pathway. Curr. Opin. Genet. Dev. 10:94-99.
58. Spector, I., N.R. Shochet, D. Blasberger, and Y. Kashman. 1989. Latrunculins-novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil. Cytoskeleton. 13:127-144.
59. Stoker, M., C. O'Neill, S. Berryman, and V., Waxman. 1968. Anchorage and growth regulation in normal and virus-transformed cells. Int. J. Cancer. 3:683-693.
60. Trielli, M.O., P.R. Andreassen, F.B. Lacroix, and R.L. Margolis. 1996. Differential Taxol-dependent arrest of transformed and nontransformed cells in the G1 phase of the cell cycle, and specific-related mortality of transformed cells. Cell Biol. 135:689-700.
61. Vogelstein, B., D. Lane, and A.J. Levine. 2000. Surfing the p53 network. Nature. 408:307-310.
62. Wahl, A.F., K.L. Donaldson, C. Fairchild, F.Y. Lee, S.A. Foster, G.W. Demers, and D.A, Galloway. 1996. Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat. Med. 2:72-79.
63. Weber, J.D., D.M. Raben, P.J. Phillips, and J.J. Baldassare. 1997, Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem. J. 326:61-68.
64. Weinberg, R.A, 1995. The retinoblastoma protein and cell cycle control. Cell. 81:323-330.
65. Zalvide, J., H. Stubdal, and J.A. DeCaprio. 1998. The J domain of simian virus 40 large T antigen is required to functionally inactivate RB family proteins. Mol. Cell. Biol. 18:1408-1415.
66. Zhang, H.S., A.A. Postigo, and D.C. Dean. 1999. Active transcriptional repression by the Rb-E2F complex mediates G1 arrest triggered by pl6INK4a, TGFβ, and contact inhibition. Cell. 97:53-61.
67. Zhu, J., P.W. Rice, L. Gorsch, M. Abate, and C.N. Cole. 1992. Transformation of a continuous rat embryo fibroblast cell line requires three separate domains of simian virus 40 large T antigen. J. Virol. 66:2780-2791.