Control of Cyclin G2 mRNA Expression by Forkhead Transcription Factors: Novel Mechanism for Cell Cycle Control by Phosphoinositide 3-Kinase and Forkhead

Molecular and Cellular Biology

Volumn 24, Issue 5, 2004, Pages 2181-2189

  Martínez Gac, Lorena ^a   Marqués, Miriam ^a   García, Zaira ^a   Campanero, Miguel R ^b   Carrera, Ana C ^a,c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; CYCLINE G2; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL STRAIN 3T3; FOXO GENE; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BASE SEQUENCE; CELL CYCLE; CYCLINS; DNA-BINDING PROTEINS; DOWN-REGULATION; FIBROBLASTS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 2342653278     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.5.2181-2189.2004     Document Type: Article

References (63)

1. Alvarez, B., E. Garrido, J. A. Garcia-Sanz, and A. C. Carrera. 2003. Phosphoinositide 3-kinase activation regulates cell division time by coordinated control of cell mass and cell cycle progression rate. J. Biol. Chem. 27:26466-26473.
2. Alvarez, B., C. Martinez-A., B. M. T. Burgering, and A. C. Carrera. 2001. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413:744-747.
3. Bennin, D. A., A. S. Don, T. Brake, J. L. McKenzie, H. Rosenbaum, L. Ortiz, A. A. DePaoli-Roach, and M. C. Horne. 2002. Cyclin G2 associates with protein phosphatase 2A catalytic and regulatory B′ subunits in active complexes and induces nuclear aberrations and a G1/S phase cell cycle arrest. J. Biol. Chem. 277:27449-27467.
4. Biggs, W. H. I., J. Meisenhelder, T. Hunter, W. K., Cavenee, and K. C. Arden. 1999. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA 96:7421-7426.
5. Boyd, K. E., J. Wells, J. Gutman, S. M. Bartley, and P. J. Farnham. 1998. c-Myc target gene specificity is determined by a post-DNA binding mechanism. Proc. Natl. Acad. Sci. USA 95:13887-13892.
6. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
7. Burgering, B. M., and G. J. Kops. 2002. Cell cycle and death control: long live Forkheads. Trends Biochem. Sci. 7:352-360.
8. Campanero, M. R., M. Armstrong, and E. Flemington. 1999. Distinct cellular factors regulate the c-myb promoter through its E2F element. Mol. Cell. Biol. 19:8442-8450.
9. Cogswell, J. P., M. M. Godlevski, M. Bonham, J. Bisi, and L. Babiss. 1995. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter. Mol. Cell. Biol. 15:2782-2790.
10. Cooper, S. 2003. Reappraisal of serum starvation, the restriction point, G0, and G1 phase arrest points. FASEB J. 17:333-340.
11. del Peso, L., V. M. Gonzalez, R. Hernandez, F. G. Barr, and G. Nunez. 1999. Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene 18:7328-7333.
12. De Ruiter, N. D., B. M. T. Burgering, and J. L. Bos. 2001. Regulation of the Forkhead transcription factor AFX by Ral-dependent phosphorylation of threonines 447 and 451. Mol. Cell. Biol. 21:8225-8235.
13. Diehl, J. A., M. Cheng, M. F. Roussel, and C. J. Sherr. 1998. Glycogen synthase kinase-3 beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12:3499-3511.
14. Dijkers, P. F., R. H. Medema, J. W. Lammers, L. Koenderman, and P. J. Coffer. 2000. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription FKHR-L1. Curr. Biol. 10:1201-1204.
15. Dynlacht, B. D. 1997. Regulation of transcription by proteins that control the cell cycle. Nature 389:149-152.
16. Fang, Y., M. Vilella-Bach, R. Bachmann, A. Flanigan, and J. Chen. 2001. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294:1942-1945.
17. Fruman, D. A., R. E. Meyers, and L. A. Cantley. 1998. Phosphoinositide kinases. Annu. Rev. Biochem. 67:481-507.
18. Furuyama, T., T. Nakazawa, I. Nakano, and N. Mori. 2000. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem. J. 349:629-634.
19. Guo, S., G. Rena, S. Cichy, X. He, P. Cohen, and T. Unterman. 1999. Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274:17184-17192.
20. Horne, M. C., K. L. Donaldson, G. L. Goolsby, D. Tran, M. Mulheisen, J. W. Hell, and A. F. Wahl. 1997. Cyclin G2 is up-regulated during growth inhibition and B cell antigen receptor-mediated cell cycle arrest. J. Biol. Chem. 272:12650-12661.
21. Horne, M. C., G. L. Goolsby, K. L. Donaldson, D. Tran, M. Neubauer, and A. F. Wahl. 1996. Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression. J. Biol. Chem. 271:6050-6061.
22. Hunt, T. 1991. Cyclins and their partners: from a simple idea to complicated reality. Semin. Cell Biol. 2:213-222.
23. Jensen, M. R., T. Audolfsson, C. L. Keck, D. B. Zimonjic, and S. S. Thorgeirsson. 1999. Gene structure and chromosomal localization of mouse cyclin G2 (Ccng2). Gene (Amsterdam) 230:171-180.
24. Jensen, M. R., V. M. Factor, and S. S. Thorgeirsson. 1998. Regulation of cyclin G1 during murine hepatic regeneration following Dipin-induced DNA damage. Hepatology 28:537-546.
25. Jimenez, C., D. R. Jones, P. Rodriguez-Viciana, A. Gonzalez-Garcia, E. Leonardo, S. Wennstrom, C. von Kobbe, J. L. Toran, L.-R. Borlado, V. Calvo, S. G. Copin, J. P. Albar, M. L. Gaspar, E. Diez, M. A. Marcos, J. Downward, C. Martinez-A., I. Merida, and A. C. Carrera. 1998. Identification and characterization of a new oncogene derived from the regulatory subunit of phosphoinositide 3-kinase. EMBO J. 17:743-753.
26. Jimenez, C., R. A. Portela, M. Mellado, J. M. Rodriguez-Frade, J. Collard, A. Serrano, C. Martinez-A., J. Avila, and A. C. Carrera. 2000. Role of the PI3K regulatory subunit in the control of actin organization and cell migration. J. Cell Biol. 151:249-262.
27. Kaestner, K. H., W. Knochel, and D. E. Martinez. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14:142-146.
28. Klippel, A., M.-A. Escobedo, M. S. Wachowicz, G. Apell, T. W. Brown, M. A. Giedlin, W. M. Kavanaugh, and L. T. Williams. 1998. Activation of phosphatidylinositol 3-kinase is sufficient for cell cycle entry and promotes cellular changes characteristic of oncogenic transformation. Mol. Cell. Biol. 18:5699-5711.
29. Kops, G. J., and B. M. Burgering. 2000. Forkhead transcription factors are targets of signalling by the proto-oncogene PKB (C-AKT). J. Anat. 197(part 4):571-574.
30. Kops, G. J., N. D. de Ruiter, A. M. De Vries-Smits, D. R. Powell, J. L. Bos, and B. M. Burgering. 1999. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398:630-634.
31. Kops, G. J. P. L., R. H. Medema, J. Glassford, M. A. G. Essers, P. F. Dijkers, P. J. Coffer, E. W.-F. Lam, and B. M. T. Burgering. 2002. Control of cell cycle exit and entry by protein kinase B-regulated Forkhead transcription factors. Mol. Cell. Biol. 22, 2025-2036.
32. Lew, J., and J. H. Wang. 1995. Neuronal cdc2-like kinase. Trends Biochem. Sci. 20:33-37.
33. MacLachlan, T. K., N. Sang, and A. Giordano. 1995. Cyclins, cyclin-dependent kinases and cdk inhibitors: implications in cell cycle control and cancer. Crit. Rev. Eukaryot. Gene Expr. 5:127-156.
34. Medema, R. H., G. J. Kops, J. L. Bos, and B. M. Burgering. 2000. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404:782-787.
35. Morgan, D. O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13:261-291.
36. Müllner, E. W., and J. A. Garcia-Sanz. 1997. Analysis of RNA expression by Northern blotting, p. 401-424. In I. Lefkovits (ed.), Immunology methods manual, vol. 1. Academic Press, London, United Kingdom.
37. Nakamura, T., R. Sanokawa, Y. F. Sasaki, D. Ayusawa, M. Oishi, and N. Mori. 1995. Cyclin I: a new cyclin encoded by a gene isolated from human brain. Exp. Cell Res. 221:534-542.
38. Noble, M. E., J. A. Endicott, N. R. Brown, and L. N. Johnson. 1997. The cyclin box fold: protein recognition in cell cycle and transcription control. Trends Biochem. Sci. 22:482-487.
39. Nugent, J. H., C. E. Alfa, T. Young, and J. S. Hyams. 1991. Conserved structural motifs in cyclins identified by sequence analysis. J. Cell Sci. 99:669-674.
40. Ohshima, T., J. M. Ward, C. G. Huh, G. Longenecker, Veeranna, H. C. Pants, R. O. Brady, L. J. Martin, and A. B. Kulkarni. 1996. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. USA 93:11173-11178.
41. Okamoto, K., C. Kamibayashi, M. Serrano, C. Prives, M. C. Mumby, and D. Beach. 1996. p53-dependent association between cyclin G and the B′ subunit of protein phosphatase 2A. Mol. Cell. Biol. 16:6593-6602.
42. Pardee, A. B. 1989. G1 events and regulation of cell proliferation. Science 246:603-608.
43. Pines, J. 1995. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 308:697-711.
44. Pines, J. 1995. Cyclins and cyclin-dependent kinases: theme and variations. Adv. Cancer Res. 66:181-212.
45. Polyak, K., M. H. Lee, H. Erdjument-Bromage, A. Koff, J. M. Roberts, P. Tempst, and J. Massague. 1994. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
46. Polymenis, M., and E. V. Schmidt. 1999. Coordination of cell growth with cell division. Curr. Opin. Genet. Dev. 9:76-80.
47. Rena, G., S. Guo, S. Cichy, T. G. Unterman, and P. Cohen. 1999. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274:17179-17183.
48. Ridley, A. J., and A. Hall. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:389-399.
49. Saucedo, L. J., and B. A. Edgar. 2002. Why size matters: altering cell size. Curr. Opin. Genet. Dev. 12:565-571.
50. Schmidt, M., S. Fernandez de Mattos, A. van der Horst, R. Klompmaker, G. J. P. L. Kops, E. W.-F. Lam, B. M. T. Burgering, and R. H. Medema. 2002. Cell cycle inhibition by FoxO Forkhead transcription factors involves down-regulation of cyclin D. Mol. Cell. Biol. 22:7842-7852.
51. Sherr, C. J. 1995. D-type cyclins. Trends Biochem. Sci. 20:187-190.
52. Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512.
53. Shimizu, A., J. Nishida, Y. Ueoka, K. Kato, T. Hachiya, Y. Kuriaki, and N. Wake. 1998. Cyclin G contributes to G2/M arrest of cells in response to DNA damage. Biochem. Biophys. Res. Commun. 242:529-533.
54. 1 cell state. Mol. Cell. Biol. 16:6965-6976.
55. Stephens, L. R., T. R. Jackson, and P. T. Hawkins. 1993. Agonist-stimulated synthesis of phosphatidylinositol(3, 4, 5)-trisphosphate: a new intracellular signalling system? Biochim. Biophys. Acta 1179:27-75.
56. Takeshita, T., T. Arita, M. Higuchi, H. Asao, K. Endo, H. Kuroda, N. Tanaka, K. Murata, N. Ishii, and K. Sugamura. 1997. STAM, signal transducing adaptor molecule, is associated with Janus kinases and involved in signaling for cell growth and c-myc induction. Immunity 6:449-457.
57. Tamura, K., Y. Kanaoka, S. Jinno, A. Nagata, Y. Ogiso, K. Shimizu, T. Hayakawa, H. Nojima, and H. Okayama. 1993. Cyclin G: a new mammalian cyclin with homology to fission yeast Cig1. Oncogene 8:2113-2118.
58. Tapon, N., K. H. Moberg, and I. K. Hariharan. 2001. The coupling of cell growth to the cell cycle. Curr. Opin. Cell Biol. 13:731-737.
59. Vanhaesebroeck, B., and M. D. Waterfield. 1999. Signaling by distinct classes of phosphoinositide 3-kinases. Exp. Cell Res. 253:239-254.
60. Zetterberg, A., and O. Larsson. 1985. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc. Natl. Acad. Sci. USA 82:5365-5369.
61. Zhang, X., L. Gan, H. Pan, S. Guo, X. He, S. T. Olson, A. Mesecar, S. Adam, and T. G. Unterman. 2002. Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J. Biol. Chem. 277:45276-45284.
62. Zhu, G., P. T. Spellman, T. Volpe, P. O. Brown, D. Botstein, T. N. Davis, and B. Futcher. 2000. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406:90-94.
63. Zvelebil, M. J., L. MacDougall, S. Leevers, S. Volinia, B. Vanhaesebroeck, I. Gout, G. Panayotou, J. Domin, R. Stein, F. Pages, H. Koga, K. Salim, J. Linacre, P. Das, C. Panaretou, R. Wetzler, and M. D. Waterfield. 1996. Structural and functional diversity of phosphoinositide 3-kinases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351:217-223.