Adhesion-dependent cell cycle progression linked to the expression of cyclin D1, activation of cyclin E-cdk2, and phosphorylation of the retinoblastoma protein

Journal of Cell Biology

Volumn 133, Issue 2, 1996, Pages 391-403

  Zhu, Xiaoyun ^a   Ohtsubo, Motoaki ^b   Böhmer, Ralph M ^a   Roberts, James M ^b   Assoian, Richard K ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN E; CYCLINE; ENZYME INHIBITOR; GROWTH FACTOR; PROTEIN P21; PROTEIN P27; RETINOBLASTOMA PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

3T3 CELLS; ANIMALS; CDC2-CDC28 KINASES; CELL ADHESION; CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN D1; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; CYCLINS; CYCLOHEXIMIDE; ENZYME INHIBITORS; FIBROBLASTS; GENE EXPRESSION; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOGENS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RETINOBLASTOMA PROTEIN; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS;

EID: 0029876639     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.133.2.391     Document Type: Article

References (82)

1. Albelda, S.M., and C.A. Buck 1990. Integrins and other cell adhesion molecules. FASEB (Fed. Am Soc. Exp. Biol) J. 4:2868-2880.
2. Benecke, B.-J., A. Ben-Ze'ev, and S. Penman 1978. The control of mRNA production, translation and turnover in suspended and reattached anchorage-dependent fibroblasts. Cell. 14:931-939.
3. Böhmer, 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.
4. mk4. Mol Cell. Biol. 15:2682-2688.
5. Chen, Q., M S. Kinch, T.S. Lin, K. Burridge, and R.L. Juliano 1994. Integrinmediated cell adhesion activates mitogen-activated protein kineses. J Biol. Chem. 269:26602-26605.
6. Chong, L D., A. Traynor-Kaplan, G.M. Bokoch, and M.A. Schwartz 1994. The small GTP-binding protein rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell. 79 507-513.
7. Daksis, J.I., L.M. Facchini, W W. Marhin, and L.J. Penn, 1994. Myc induces cyclin D1 expression in the absence of de novo protein synthesis and links mitogen-stimulated signal transduction to the cell cycle. Oncogene. 9:3635-3645.
8. Dowdy, S F , P.W. Hinds, K. Louie, S.I. Reed, A. Arnold, and R.A. Weinberg, 1993. Physical interaction of the retinoblastoma protein with human D cyclins. Cell. 73:499-511.
9. Dulic, V , E. Lees, and S.I. Reed 1992. Association of human cyclin E with a periodic G1-S phase protein kinase. Science (Wash. DC) 257:1958-1961.
10. Dunaief, J.L., B.E. Strober, S. Guha, P.A. Khavari, K. Alin, J. Luban, M. Begemann, G.R Crabtree, and S.P. Goff, 1994 The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest Cell. 79: 119-130.
11. El-Deiry, W.S , T Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D Lin, W.E Mercer, W.K. Kinzler, and B. Vogelstein, 1993. WAF1, a potential mediator of p53 tumor suppression. Cell. 75:817-825.
12. Ewen, M.E., H.K Sluss, C J. Sherr, H. Matsushirne, J.-Y. Kato, and D.M Livingston, 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell. 73:487-497
13. Fang, F., G. Orend, N Watanabe, T. Hunter, and E Ruoslahti, 1996. Dependence of cyclin E-cdk2 kinase activity on cell anchorage Science (Wash DC). 271:499-502.
14. Fesquet, D., J -C. Labbe, J. Derancourt, J.-P. Capony, S. Galas, F. Girard, T. Lorca, J. Shuttleworth, M. Doree, and J.-C. Cavadore, 1993. The MO15 gene encodes the catalytic subunit of a protein kinase that activates cdc2 and other cyclin-dependent kinases (CDKs) through phosphorylation of Thr161 and its homologues. EMBO (Eur Mol. Biol. Organ.) J. 12:3111-3121.
15. Fisher, R.P., and D O. Morgan, 1994. A novel cyclin associates with MO15/ CDK7 to form the CDK-activating kinase. Cell. 78:713-724.
16. Girard, F , U. Strausfeld, A. Fernandez, and N.J.C. Lamb 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell. 67: 1169-1179.
17. Gu, W., J.W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal-Ginard, 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 72:309-324.
18. Guadagno, T.M., and R.K. Assoian, 1991. G1/S control of anchorage-independent growth in the fibroblast cell cycle J. Cell Biol 115:1419-1425.
19. Guadagno, T.M , M. Ohtsubo, J.M. Roberts, and R K. Assoian, 1993. A link between cyclin A expression and adhesion-dependent cell cycle progression. Science (Wash. DC). 262:1572-1575
20. INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes & Dev 8:2939-2952.
21. Han, E.K., T.M. Guadagno, S.L. Dalton, and R K. Assoian, 1993. A cell cycle and mutational analysis of anchorage-independent growth: cell adhesion and TGF-β1 control G1/S transit specifically. J. Cell Biol. 122:461-471.
22. INK4B is a potential effector of TGF-β-induced cell cycle arrest. Nature (Lond) 371:257-261.
23. Harper, J.W., G.R. Adami, N Wei, K. Keyomarsi, and S.J. Elledge, 1993. The p21 cdk-interacting protein Cip-1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 75:805-816.
24. Harper, J.W., S.J. Elledge, K. Keyomarsi, B. Dynlacht, L.-H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, E Swindell et al. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6:387-400.
25. Hatakeyama, M , J.A. Bril, G.R. Fink, and R.A. Weinberg, 1994. Collaboration of G1 cyclins m the functional mactivation of the retinoblastoma protein. Genes & Dev. 8:1759-1771.
26. Heichman, K.A , and J M Roberts, 1994. Rules to replicate by. Cell. 79:557-562.
27. Henglein, B., X. Chenivesse, J. Wang, D. Eick, and C. Bréchot, 1994. Structure and cell cycle-regulated transcription of the human cyclin A gene. Proc. Natl. Acad. Sci. USA. 91:5490-5494.
28. Hemler, M. 1990. VLA proteins in the integrin family. Annu. Rev. Immunol. 8: 365-400.
29. Hinds, P.W., S. Mittnacht, V. Dulic, A. Arnold, S.I. Reed, and R.A. Weinberg, 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell. 70:993-1006.
30. Hirai, H , M.F. Roussel, J.-Y. Kato, R.A. Ashmun, and C.J. Sherr, 1995. Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol Cell. Biol. 15:2672-2681.
31. Hunter, T , and J. Pines 1994. Cyclins and cancer II cyclin D and CDK inhibitors come of age. Cell. 79:573-582.
32. Hynes, R.O. 1987. Integrins: a family of cell surface receptors. Cell. 48:549-554.
33. Hynes, R.O. 1992. Integrins: versatility, modulation and signaling in cell adhesion. Cell. 69:11-25.
34. Johnson, D.G., J.K. Schwarz, W.D. Cress, and J.R. Nevins, 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature (Lond.) 365:349-352.
35. Kato, J -Y., H. Matsushime, S.W. Hiebert, M.E. Ewen, and C.J. Sherr 1993. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes & Dev. 7: 331-342.
36. kip1) of cyclin-dependent kinase 4 activation. Cell. 79:487-496.
37. Kato, J.-Y., M Matsuoka, O.K. Strom, and C.J. Sherr, 1994b Regulation of cyclin D-dependent kinase 4 (cdk4) by cdk4-activating kinase. Mol. Cell. Biol 14:2713-2721
38. Kim, S -J , U.S. Onwuta, Y.I. Lee, R. Li, M.R. Bolchan, and P.D Robbins, 1992. The retinoblastoma gene product regulates Sp-1 mediated transcription. Mol. Cell. Biol. 12:2455-2463.
39. Koff, A., A. Giordano, D. Desai, K. Yamashita, J.W. Harper, S. Elledge, T. Nishmioto, D.O. Morgan, R. Franza, and J.M. Roberts, 1992. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science (Wash. DC). 257:1689-1694.
40. KIP2. a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes & Dev. 9.639-649.
41. Lew, D.J., D. Vjekoslav, and S.I. Reed, 1991. Isolation of three novel human cyclins by rescue of G1 cyclin (Cln) function in yeast. Cell. 66:1597-1206.
42. Lewis, J M., and M.A. Schwanz, 1995. Mapping in vivo associations of cytoplasmic proteins with integrin β1 cytoplasmic domain mutants. Mol. Biol. Cell 6: 151-160.
43. Lin, T.-A., X. Kong, T.A.J. Haystead, A. Pause, G. Belsham, N. Sonenberg, and J.C. Lawrence, Jr. 1994. PHAS-1 as a link between mitogen-activated protein kinase and translation initiation Science (Wash. DC). 266:653-656.
44. Makela, T.P., J -P. Tassan, E.A. Nigg, S. Frutiger, G J. Hughes, and R.A. Weinberg 1994. A cyclin associated with the CDK-activating kinase MOIS. Nature (Lond.). 371:254-257.
45. Massague, J , B. Kelly, and C. Mottola, 1985. Stimulation by insulin-like growth factors is required for cellular transformation by type β transforming growth factor. J. Biol. Chem. 260:4551-4554.
46. Matsuoka, M., J.-Y. Kato, R.P. Fisher, D O. Morgan, and C. Sherr 1994. Activation of cyclin-dependent kinase 4 (cdk4) by mouse MO15-associated kinase. Mol Cell Biol 14 7265-7275.
47. CIP1 cdk inhibitor family, is a candidate tumor suppressor gene. Genes & Dev. 9.650-662.
48. Matsushime, H., M.F. Roussel, R.A. Ashmun, and C.J. Sherr, 1991 Colonystimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65:701-713.
49. PSK-J3/cdk4) for mammalian D type G1 cyclins Cell 71 323-334.
50. Matsushime, H., D.E. Quelle, S.A. Shurtleff, M. Shibuya, C J. Sherr, and J.-Y, Kato, 1994. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol. 14:2066-2076.
51. McNamee, H.P., D.E Ingber, and M.A. Schwartz, 1993. Adhesion to tibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J Cell Biol 121:673-678.
52. Meyerson, M., and E. Harlow 1994. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell Biol. 14.2077-2086.
53. Miyamoto, S., H. Teramoto, O.A. Coso, S Gutkind, P D. Burbelo, S.K Akiyama, and K.M. Yamada, 1995. Intcgrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell Biol. 131:791-505.
54. erk-2. J. Biol. Chem. 270:269-273
55. Nevins, J.R. 1992 E2F: a link between the Rb tumor suppressor protein and viral oncoproteins Science (Wash. DC). 258.424-429.
56. Ohtsubo, M., and J.M Roberts, 1993. Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science (Wash. DC) 259:1908-1912.
57. kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature (Lond.). 372:570-573.
58. Pagano, M., R Pepperkok, F. Verde, W. Ansorge, and G. Draetta, 1992 Cyclin A is required at two points in the human cell cycle. EMBO (Eur. Mol. Biol. Organ.) J. 11:961-971
59. Pardee, A.B 1989. G1 events and regulation of cell proliferation Science (Wash DC) 246:603-608.
60. kip1, a cyclin-cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes & Dev 8.9-22.
61. kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
62. Poon, R., K Yamashita, J. Adamczewski, T Hunt, and J. Shuttleworth, 1993. The cdc2-related protein p40MO15 is the catalytic subunit of a protein kinase that can activate p33cdk2 EMBO (Eur. Mol Biol Organ.) J. 12:3123-3132.
63. Quelle, D.E., R.A. Ashmun, S.A Shurtleff, J -Y. Kato, D. Bar-Sagi, M.F. Roussel, and C.J Sherr 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes & Dev. 7:1559-1571.
64. Reynisdóttir, I., K. Polyak, A. Iavorone, and J. Massagué 1995. Kip/Cip and Ink4 cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes & Dev. 9:1831-1845.
65. Rosenwald, I.B., A. Lazaris-Karatzas, N. Sonenberg, and E.V. Schmidt, 1993. Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E Mol Cell. Biol. 13.7358-7363.
66. Schlaepfer, D.D., S.K. Hanks, T Hunter, and P. Van der Geer, 1994 Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature (Lond.). 372.786-790.
67. Schulze, A., K. Zerfass, D. Spitkovsky, S Middendorp, J Berges, K. Helin, P. Jansen-Durr, and B. Henglein, 1995 Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc Natl. Acad. Sci. USA. 92 11264-11268.
68. Serrano, M., G.J. Hannon, and D. Beach, 1993 A new regulatory motif in cellcycle control causing specific inhibition of cyclin D/CDK4 Nature (Lond.) 366:704-707.
69. Sherr, C.J. 1994 G1 phase progression: cycling on cue. Cell. 79:551-555.
70. Shin, S., V.H. Freedman, R. Risser, and R Pollack, 1975. Tumorigenicity of virus-transformed cells in nude mice is correlated specifically with anchorage-independent growth in vitro. Proc. Natl. Acad Sci. USA. 72:4435-4439.
71. Solomon, M.J., J. Harper, and J. Shuttleworth, 1993 CAT, the p34cdc2 activating kinase. contains a protein identical or closely related to p40MO15. EMBO (Eur. Mol Biol. Organ.) J. 12:3133-3142
72. Toyoshima, H , and T. Hunter, 1994. p27, a novel inhibitor of G1 cyclin-cdk protein kinase activity, is related to p21 Cell 78:67-74.
73. Vuori, K., and E. Ruoslahti, 1993. Activation of protein kinase C precedes α5β1 integrin-mediated cell spreading on fibronectin J. Biol Chem. 268:21459-21462.
74. Vuori, K , and E Ruoslahti, 1994. Association of insulin receptor substrate-1 with integrins. Science (Wash DC) 266:1576-1578.
75. Welch, P.J., and J.Y.J. Wang 1993. A C-terminal protein binding domain in the retinobiastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell. 75:779-790.
76. Welch, P.J., and J.Y.J. Wang, 1995 Disruption of retinoblastoma protein function by coexpression of its C pocket fragment. Genes & Dev 9:31-46.
77. Woods, A. and J.R. Couchman, 1992. Protein kinase C involvement in focal adhesion formation. J. Cell Sci 101:277-290.
78. Woods, A., and J.R. Couchman, 1994. Syndccan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell. 5:183-192.
79. Xiong, Y., G J. Hannon, H. Zhang, D. Casso, R. Kobayasoi, and D. Beach, 1993. p21 is a universal inhibitor of cyclin kinases. Nature (Lond.). 366:701-704.
80. Xu G., D M. Livingston, and W. Krek, 1995. Multiple members of the E2F transcription factor family are the products of oncogenes. Proc. Natl. Acad. Sci. USA 92:1357-1361.
81. Zhang, H., G. Hannon, and D Beach, 1994. p21-containing cyclin kinases exist in both active and inactive states Genes & Dev. 8:1750-1758.
82. Zhu, X., and R.K. Assoian, 1995 Integrin-dependent activation of MAP kinase: a link to shape-dependent cell proliferation. Mol Biol Cell. 6.273-282.