ΔRaf-1:ER* Bypasses the Cyclic AMP Block of Extracellular Signal-Regulated Kinase 1 and 2 Activation but Not CDK2 Activation or Cell Cycle Reentry

Molecular and Cellular Biology

Volumn 23, Issue 24, 2003, Pages 9303-9317

  Balmanno, Kathryn ^a   Millar, Tracy ^a   McMahon, Martin ^b   Cook, Simon J ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CYCLIC AMP; CYCLIN A; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; ENZYME ACTIVATOR; GROWTH FACTOR; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN CDC25A; PROTEIN P21; PROTEIN P27; RAF PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL GROWTH; CELL LEVEL; CELL STIMULATION; CELL STRAIN; CELL TYPE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA SYNTHESIS INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; FIBROBLAST CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; SERUM;

ANIMALIA; BOVINAE;

EID: 0345060033     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.24.9303-9317.2003     Document Type: Article

References (82)

1. Allan, L. A., T. Dohig, M. Read, and M. Fried. 2000. The p21(WAF1/CIP1) promoter is methylated in Rat-1 cells: stable restoration of p53-dependent p21(WAF1/CIP1) expression after transfection of a genomic clone containing the p21(WAF1/CIP1) gene. Mol. Cell. Biol. 20:1291-1298.
2. Ally, S., T. Clair, D. Katsaros, G. Tortora, H. Yokozaki, R. A. Finch, T. L. Avery, and Y. S. Cho-Chung. 1989. Inhibition of growth and modulation of gene expression in human lung carcinoma in athymic mice by site-selective 8-CI-cyclic adenosine monophosphate. Cancer Res. 49:5650-5655.
3. Ariga, M., T. Nedachi, M. Akahori, H. Sakamoto, Y. Ito, F. Hakuno, and S. Takahashi. 2000. Signalling pathways of insulin-like growth factor-I that are augmented by cAMP in FRTL-5 cells. Biochem. J. 348:409-416.
4. CIP1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 18:3085-3097.
5. Baptist, M., F. Lamy, J. Gannon, T. Hunt, J. E. Dumont, and P. P. Roger. 1996. Expression and subcellular localization of CDK2 and cdc2 kinases and their common partner cyclin A in thyroid epithelial cells: comparison of cyclic AMP-dependent and -independent cell cycles. J. Cell Physiol. 166:256-273.
6. Barlat, I., B. Henglein, A. Plet, N. Lamb, A. Fernandez, F. R. McKenzie, J. Pouyssegur, A. Vie, and J. M. Blanchard. 1995. TGF-β1 and cAMP attenuate cyclin A gene transcription via a cAMP responsive element through independent pathways. Oncogene 11:1309-1318.
7. 1/S transition and leads to premature activation of cyclin E- and cyclin A-dependent kinases. Mol. Cell. Biol. 19:6183-6194.
8. Bortner, D. M., and M. P. Rosenberg. 1995. Overexpression of cyclin A in the mammary glands of transgenic mice results in the induction of nuclear abnormalities and increased apoptosis. Cell Growth Differ. 6:1579-1589.
9. Burgering, B. M., G. J. Pronk, P. C. van Weeren, P. Chardin, and J. L. Bos. 1993. cAMP antagonizes p21ras-directed activation of extracellular signal-regulated kinase 2 and phosphorylation of mSos nucleotide exchange factor. EMBO J. 12:4211-4220.
10. Calleja, V., P. R. Enriquez, C. Filloux, P. Peraldi, V. Baron, and E. Van Obberghen. 1997. The effect of cyclic adenosine monophosphate on the mitogen-activated protein kinase pathway depends on both the cell type and the type of tyrosine kinase-receptor. Endocrinology 138:1111-1120.
11. Coats, S., W. M. Flanagan, J. Nourse, and J. M. Roberts. 1996. Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 272:877-880.
12. Connell-Crowley, L., J. W. Harper, and D. W. Goodrich. 1997. Cyclin D1/Cdk4 regulates retinoblastoma protein-mediated cell cycle arrest by site-specific phosphorylation. Mol. Biol. Cell 8:287-301.
13. Cook, S. J., and F. McCormick. 1993. Inhibition by cAMP of Ras-dependent activation of Raf. Science 262:1069-1072.
14. 2+-dependent signal pathways in Rat-1 cells. J. Biol. Chem. 272:13309-13319.
15. 1 phase of the cell cycle is determined by the duration of mitogen-activated protein kinase activation. Mol. Cell. Biol. 19:330-341.
16. Cospedal, R., M. Lobo, and I. Zachary. 1999. Differential regulation of extracellular signal-regulated protein kinases (ERKs) 1 and 2 by cAMP and dissociation of ERK inhibition from anti-mitogenic effects in rabbit vascular smooth muscle cells. Biochem. J. 342:407-414.
17. Davies, H., G. R. Bignell, C. Cox, P. Stephens, S. Edkins, S. Clegg, J. Teague, H. Woffendin, M. J. Garnett, W. Bottomley, N. Davis, E. Dicks, R. Ewing, Y. Floyd, K. Gray, S. Hall, R. Hawes, J. Hughes, V. Kosmidou, A. Menzies, C. Mould, A. Parker, C. Stevens, S. Watt, S. Hooper, R. Wilson, H. Jayatilake, B. A. Gusterson, C. Cooper, J. Shipley, D. Hargrave, K. Pritchard-Jones, N. Maitland, G. Chenevix-Trench, G. J. Riggins, D. D. Bigner, G. Palmieri, A. Cossu, A. Flanagan, A. Nicholson, J. W. Ho, S. Y. Leung, S. T. Yuen, B. L. Weber, H. F. Seigler, T. L. Darrow, H. Paterson, R. Marais, C. J. Marshall, R. Wooster, M. R. Stratton, and P. A. Futreal. 2002. Mutations of the BRAF gene in human cancer. Nature 417:949-954.
18. DeGregori, J., G. Leone, K. Ohtani, A. Miron, and J. R. Nevins. 1995. E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity. Genes Dev. 9:2873-2887.
19. Dhillon, A. S., C. Pollock, H. Steen, P. E. Shaw, H. Mischak, and W. Kolch. 2002. Cyclic AMP-dependent kinase regulates Raf-1 kinase mainly by phosphorylation of serine 259. Mol. Cell. Biol. 22:3237-3246.
20. Dumaz, N., Y. Light, and R. Marais. 2002. Cyclic AMP blocks cell growth through Raf-1-dependent and Raf-1-independent mechanisms. Mol. Cell. Biol. 22:3717-3728.
21. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
22. Enserink, J. M., A. E. Christensen, J. de Rooij, M. van Triest, F. Schwede, H. G. Genieser, S. O. Doskeland, J. L. Blank, and J. L. Bos. 2002. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 4:901-906.
23. Erhardt, P., J. Troppmair, U. R. Rapp, and G. M. Cooper. 1995. Differential regulation of Raf-1 and B-Raf and Ras-dependent activation of mitogen-activated protein kinase by cyclic AMP in PC12 cells. Mol. Cell. Biol. 15: 5524-5530.
24. Faure, M., and H. R. Bourne. 1995. Differential effects on cAMP on the MAP kinase cascade: evidence for a cAMP-insensitive step that can bypass Raf-1. Mol. Biol. Cell 6:1025-1035.
25. Gagelin, C., D. Toru-Delbauffe, J. M. Gavaret, and M. Pierre. 1999. Effects of cyclic AMP on components of the cell cycle machinery regulating DNA synthesis in cultured astrocytes. J. Neurochem. 73:1799-1805.
26. Galaktionov, K., X. Chen, and D. Beach. 1996. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382:511-517.
27. 2 checkpoint. Oncogene 21:8089-8104.
28. Gartel, A. L., E. Goufman, S. G. Tevosian, H. Shih, A. S. Yee, and A. L. Tyner. 1998. Activation and repression of p21(WAF1/CIP1) transcription by RB binding proteins. Oncogene 17:3463-3469.
29. Geng, Y., W. Whoriskey, M. Y. Park, R. T. Bronson, R. H. Medema, T. Li, R. A. Weinberg, and P. Sicinski. 1999. Rescue of cyclin D1 deficiency by knockin cyclin E. Cell 97:767-777.
30. Graves, L. M., K. E. Bornfeldt, E. W. Raines, B. C. Potts, S. G. Macdonald, R. Ross, and E. G. Krebs. 1993. Protein kinase A antagonizes platelet-derived growth factor-induced signalling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc. Natl. Acad. Sci. USA 90:10300-10304.
31. Gu, Y., J. Rosenblatt, and D. O. Morgan. 1992. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11:3995-4005.
32. Hafner, S., H. S. Adler, H. Mischak, P. Janosch, G. Heidecker, A. Wolfman, S. Pippig, M. Lohse, M. Ueffing, and W. Kolch. 1994. Mechanism of inhibition of Raf-1 by protein kinase A. Mol. Cell. Biol. 14:6696-6703.
33. Hoang, A. T., K. J. Cohen, J. F. Barrett, D. A. Bergstrom, and C. V. Dang. 1994. Participation of cyclin A in Myc-induced apoptosis. Proc. Natl. Acad. Sci. USA 91:6875-6879.
34. ras-mitogen-activated protein kinase pathway in fibroblasts. J. Biol. Chem. 269:3534-3538.
35. Houslay, M. D., and W. Kolch. 2000. Cell-type specific integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling. Mol. Pharmacol. 58:659-668.
36. Jinno, S., K. Suto, A. Nagata, M. Igarashi, Y. Kanaoka, H. Nojima, and H. Okayama. 1994. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J. 13:1549-1556.
37. Kato, J. Y., M. Matsuoka, K. Polyak, J. Massague, and C. J. Sherr. 1994. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 79:487-496.
38. Kerkhoff, E., and U. R. Rapp. 1998. Cell cycle targets of Ras/Raf signalling. Oncogene 17:1457-1462.
39. Kikukawa, M., Y. Okamoto, H. Fukui, and H. Nakano. 1997. Effect of dibutyryl cyclic AMP on the cyclin-dependent kinase inhibitor p27Kip1 in the human hepatoma cells PLC/PRF/5. Anticancer Res. 17:3287-3291.
40. Kim, T. Y., W. I. Kim, R. E. Smith, and E. D. Kay. 2001. Role of p27(Kip1) in cAMP- and TGF-beta2-mediated antiproliferation in rabbit corneal endothelial cells. Investig. Ophthalmol. Vis. Sci. 42:3142-3149.
41. Kolch, W. 2000. Meaningful relationships: the regulation of the Ras/Raf/ MEK/ERK pathway by protein interactions. Biochem. J. 351:289-305.
42. LaBaer, J., M. D. Garrett, L. F. Stevenson, J. M. Slingerland, C. Sandhu, H. S. Chou, A. Fattaey, and E. Harlow. 1997. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 11:847-862.
43. L'Allemain, G., J. N. Lavoie, N. Rivard, V. Baldin, and J. Pouyssegur. 1997. Cyclin D1 expression is a major target of the cAMP-induced inhibition of cell cycle re-entry in fibroblasts Oncogene 14:1981-1990.
44. Lee, T. H., L. Y. Chuang, and W. C. Hung. 2000. Induction of p21WAF1 expression via Spl-binding sites by tamoxifen in estrogen receptor-negative lung cancer cells. Oncogene 19:3766-3773.
45. Lee, Y. H., J. S. Park, C. H. Park, and S. K. Lee. 1998. Synergistic effect of cyclic AMP and insulin on the expression of cyclin A gene in Swiss 3T3 cells. Biochem. Biophys. Res. Commun. 244:843-848.
46. Lerner, A., D. H. Kim, and R. Lee. 2000. The cAMP signaling pathway as a therapeutic target in lymphoid malignancies. Leuk. Lymphoma 37:39-51.
47. Lewis, T. S., P. S. Shapiro, and N. G. Ahn. 1998. Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74:49-139.
48. Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evan. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686-1690.
49. Lomazzi, M., M. C. Moroni, M. R. Jensen, E. Frittoli, and K. Helin. 2002. Suppression of the p53- or pRB-mediated G1 checkpoint is required for E2F-induced S-phase entry. Nat. Genet. 31:190-194.
50. Magnaldo, I., J. Pouyssegur, and S. Paris. 1989. Cyclic AMP inhibits mitogen-induced DNA synthesis in hamster fibroblasts, regardless of the signalling pathway involved. FEBS Lett. 245:65-69.
51. Marshall, C. J. 1999. How do small GTPase signal transduction pathways regulate cell cycle entry? Curr. Opin. Cell Biol. 11:732-736.
52. McKenzie, F. R., and J. Pouyssegur. 1996. cAMP-mediated growth inhibition in fibroblasts is not mediated via mitogen-activated protein (MAP) kinase (ERK) inhibition. cAMP-dependent protein kinase induces a temporal shift in growth factor-stimulated MAP kinases. J. Biol. Chem. 271:13476-13483.
53. Mischak, H., T. Seitz, P. Janosch, M. Eulitz, H. Steen, M. Schellerer, A. Philipp, and W. Kolch. 1996. Negative regulation of Raf-1 by phosphorylation of serine 621. Mol. Cell. Biol. 16:5409-5418.
54. Morrison, D. K., G. Heidecker, U. R. Rapp, and T. D. Copeland. 1993. Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268:17309-17316.
55. Nilsson, I., and I. Hoffmann. 2000. Cell cycle regulation by the Cdc25 phosphatase family. Prog. Cell Cycle Res. 4:107-114.
56. Palmero, I., and G. Peters. 1996. Perturbation of cell cycle regulators in human cancer. Cancer Surv. 27:351-367.
57. Pastan, I. H., G. S. Johnson, and W. B. Anderson. 1975. Role of cyclic nucleotides in growth control. Annu. Rev. Biochem. 44:491-522.
58. Rao, S., J. Gray-Bablin, T. W. Herliczek, and K. Keyomarsi. 1999. The biphasic induction of p21 and p27 in breast cancer cells by modulators of cAMP is posttranscriptionally regulated and independent of the PKA pathway. Exp. Cell Res. 252:211-223.
59. Robinson, M. J., and M. H. Cobb. 1997. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9:180-186.
60. Roger, P. P., D. Christophe, J. E. Dumont, and I. Pirson. 1997. The dog thyroid primary culture system: a model of the regulation of function, growth and differentiation expression by cAMP and other well-defined signaling cascades. Eur. J. Endocrinol. 137:579-598.
61. Samuels, M. L., M. J. Weber, J. M. Bishop, and M. McMahon. 1993. Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human raf-1 protein kinase. Mol. Cell. Biol. 13:6241-6252.
62. Santoni-Rugiu, E., J. Falck, N. Mailand, J. Bartek, and J. Lukas. 2000. Involvement of Myc activity in a G(1)/S-promoting mechanism parallel to the pRb/E2F pathway. Mol. Cell. Biol. 20:3497-3509.
63. Sewing, A., C. Burger, S. Brusselbach, C. Schalk, F. C. Lucibello, and R. Muller. 1993. Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP. J. Cell Sci. 104:545-555.
64. Schmitt, J. M., and P. J. S. Stork. 2001. Cyclic AMP-mediated inhibition of cell growth requires the small G protein Rapl. Mol., Cell. Biol. 21:3671-3683.
65. Shaulian, E., and M. Karin. 2002. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4:E131-E136.
66. Sidovar, M. F., P. Kozlowski, J. W. Lee, M. A. Collins, Y. He, and L. M. Graves. 2000. Phosphorylation of serine 43 is not required for inhibition of c-Raf kinase by the cAMP-dependent protein kinase. J. Biol. Chem. 275: 28688-28694.
67. Solomon, M. J., M. Glotzer, T. H. Lee, M. Philippe, and M. W. Kirschner. 1990. Cyclin activation of p34cdc2. Cell 63:1013-1024.
68. Squires, M. S., P. M. Nixon, and S. J. Cook. 2002. Cell cycle arrest by PD184352 requires inhibition of the extracellular signal-regulated kinases (ERK) 1/2 but not ERK5/BMK1. Biochem. J. 366:673-680.
69. Stork, P. J. S., and J. M. Schmitt. 2002. Crosstalk between cAMP and MAP kinase signalling in the regulation of cell proliferation. Trends Cell Biol. 12:258-266.
70. Tortora, G., F. Ciardiello, S. Ally, T. Clair, D. S. Salomon, and Y. S. Cho-Chung. 1989. Site-selective 8-chloroadenosine 3′,5′-cyclic monophosphate inhibits transformation and transforming growth factor alpha production in Ki-ras-transformed rat fibroblasts. FEBS Lett. 242:363-367.
71. Treinies, I., H. F. Paterson, S. Hooper, R. Wilson, and C. J. Marshall. 1999. Activated MEK stimulates expression of AP-1 components independently of phosphatidylinositol 3-kinase (PI3-kinase) but requires a PI3-kinase signal to stimulate DNA synthesis. Mol. Cell. Biol. 19:321-329.
72. Vadiveloo, P. K., E. L. Filonzi, H. R. Stanton, and J. A. Hamilton. 1997. G1 phase arrest of human smooth muscle cells by heparin, IL-4 and cAMP is linked to repression of cyclin D1 and cdk2. Atherosclerosis 133:61-69.
73. Van Keymeulen, A., J. Bartek, J. E. Dumont, and P. P. Roger. 1999. Cyclin D3 accumulation and activity integrate and rank the comitogenic pathways of thyrotropin and insulin in thyrocytes in primary culture. Oncogene 18: 7351-7359.
74. Vigo, E., H. Muller, E. Prosperini, G. Hateboer, P. Cartwright, M. C. Moroni, and K. Helin. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol. Cell. Biol. 19:6379-6395.
75. Vossler, M. R., H. Yao, R. D. York, M. G. Pan, C. S. Rim, and P. J. Stork. 1997. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82.
76. Weston, C. R., K. Balmanno, C. Chalmers, K. Hadfield, S. A Molton, R. Ley, E. F. Wagner, and S. J. Cook. 2003. Activation of ERK1/2 by ΔRaf-1:ER* represses Bim expression independently of the JNK or PI3K pathways. Oncogene 22:1281-1293.
77. Whitehurst, C. E., O. Hakime, J. T. Bruder, U. R. Rapp, and T. D. Geppert. 1995. The MEK kinase activity of the catalytic domain of RAF-1 is regulated independently of Ras binding in T cells. J. Biol. Chem. 270:5594-5599.
78. Whitmarsh, A. J., and R. J. Davis. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. 74:589-607.
79. Williamson, E. A., G. S. Burgess, P. Eder, S. Litz-Jackson, and H. S. Boswell. 1997. Cyclic AMP negatively controls c-myc transcription and G1 cell cycle progression in p210 BCR-ABL transformed cells: inhibitory activity exerted through cyclin D1 and cdk4. Leukemia 11:73-85.
80. Woods, D., D. Parry, H. Cherwinski, E. Bosch, E. Lees, and M. McMahon. 1997. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol. Cell. Biol. 17:5598-5611.
81. Wu, J., P. Dent, T. Jelinek, A. Wolfman, M. J. Weber, and T. W. Sturgill. 1993. Inhibition of the EGF-stimulated MAP kinase signalling pathway by adenosine 3′,5′-monophosphate. Science 262:1065-1069.
82. 1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101:79-89.