Fos Family Members Induce Cell Cycle Entry by Activating Cyclin D1

ABSTRACT Expression of the fos family of transcription factors is stimulated by growth factors that induce quiescent cells to reenter the cell cycle, but the cellular targets of the Fos family that regulate cell cycle reentry have not been identified. To address this issue, mice that lack two members of the fos family, c-fos and fosB, were derived. ThefosB−/− c-fos−/−mice are similar in phenotype to c-fos−/−mice but are 30% smaller. This decrease in size is consistent with an abnormality in cell proliferation. Fibroblasts derived fromfosB−/− c-fos−/−mice were found to have a defect in proliferation that results at least in part from a failure to induce cyclin D1 following serum-stimulated cell cycle reentry. Although definitive evidence that c-Fos and FosB directly induce cyclin D1 transcription will require further analysis, these findings raise the possibility that c-Fos and FosB are either direct or indirect transcriptional regulators of the cyclin D1 gene and may function as a critical link between serum stimulation and cell cycle progression.

[1]  G. Cooper,et al.  Ras links growth factor signaling to the cell cycle machinery via regulation of cyclin D1 and the Cdk inhibitor p27KIP1 , 1997, Molecular and cellular biology.

[2]  L. Zon,et al.  Induction of cyclin D1 by simian virus 40 small tumor antigen. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Richard J. Lee,et al.  Angiotensin II Activation of Cyclin D1-dependent Kinase Activity* , 1996, The Journal of Biological Chemistry.

[4]  Michael E Greenberg,et al.  A Defect in Nurturing in Mice Lacking the Immediate Early Gene fosB , 1996, Cell.

[5]  S K Durham,et al.  Expression of FosB during mouse development: normal development of FosB knockout mice. , 1996, Oncogene.

[6]  C. Albanese,et al.  Transforming p21ras Mutants and c-Ets-2 Activate the Cyclin D1 Promoter through Distinguishable Regions (*) , 1995, The Journal of Biological Chemistry.

[7]  G. Stamp,et al.  Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. , 1995, Genes & development.

[8]  S. Elledge,et al.  Cyclin D1 provides a link between development and oncogenesis in the retina and breast , 1995, Cell.

[9]  C. Sherr,et al.  D-type cyclins. , 1995, Trends in biochemical sciences.

[10]  J. Bartek,et al.  Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity , 1995, Molecular and cellular biology.

[11]  L. Matrisian,et al.  A Novel Nerve Growth Factor-responsive Element in the Stromelysin-1 (Transin) Gene That Is Necessary and Sufficient for Gene Expression in PC12 Cells (*) , 1995, The Journal of Biological Chemistry.

[12]  David O. Morgan,et al.  Principles of CDK regulation , 1995, Nature.

[13]  F. C. Lucibello,et al.  Cell proliferation and cell cycle progression are not impaired in fibroblasts and ES cells lacking c-Fos. , 1995, Oncogene.

[14]  C. Albanese,et al.  c-Jun represses transcription of the human chorionic gonadotropin alpha and beta genes through distinct types of CREs. , 1994, The Journal of biological chemistry.

[15]  C. Sherr.  G1 phase progression: Cycling on cue , 1994, Cell.

[16]  R. Sutherland,et al.  Cyclin D1 induction in breast cancer cells shortens G1 and is sufficient for cells arrested in G1 to complete the cell cycle. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[17]  E. Hu,et al.  Targeted disruption of the c‐fos gene demonstrates c‐fos‐dependent and ‐independent pathways for gene expression stimulated by growth factors or oncogenes. , 1994, The EMBO journal.

[18]  T. Curran,et al.  Cell transformation by c-fos requires an extended period of expression and is independent of the cell cycle , 1994, Molecular and cellular biology.

[19]  M. Beato,et al.  Inducible regulatory elements in the human cyclin D1 promoter. , 1994, Oncogene.

[20]  M. Gossen,et al.  Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. , 1994, Molecular and cellular biology.

[21]  M. Rudnicki,et al.  MyoD or Myf-5 is required for the formation of skeletal muscle , 1993, Cell.

[22]  Pengcheng Zhou,et al.  Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. , 1993, Oncogene.

[23]  S. Shurtleff,et al.  Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. , 1993, Genes & development.

[24]  M. Hadman,et al.  In vivo viral and cellular Jun complexes exhibit differential interaction with a number of in vitro generated 'AP-1- and CREB-like' target sequences. , 1993, Oncogene.

[25]  James M. Roberts,et al.  Cyclin-dependent regulation of G1 in mammalian fibroblasts. , 1993, Science.

[26]  B. Spiegelman,et al.  Pleiotropic effects of a null mutation in the c-fos proto-oncogene , 1992, Cell.

[27]  Y. Xiong,et al.  Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[28]  B. Spiegelman,et al.  Growth and differentiation of embryonic stem cells that lack an intact c-fos gene. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Mattei,et al.  Structure and mapping of the fosB gene. FosB downregulates the activity of the fosB promoter. , 1992, Nucleic acids research.

[30]  R. Bravo,et al.  The jun and fos protein families are both required for cell cycle progression in fibroblasts , 1991, Molecular and cellular biology.

[31]  I. Verma,et al.  An alternative spliced form of FosB is a negative regulator of transcriptional activation and transformation by Fos proteins. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Tsonwin Hai,et al.  Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  I. Verma,et al.  Phosphorylation of the C terminus of Fos protein is required for transcriptional transrepression of the c-fos promoter , 1990, Nature.

[34]  T. Curran,et al.  Transcriptional activation and repression by Fos are independent functions: the C terminus represses immediate-early gene expression via CArG elements , 1990, Molecular and cellular biology.

[35]  J. Cherrington,et al.  Human cytomegalovirus ie1 transactivates the alpha promoter-enhancer via an 18-base-pair repeat element , 1989, Journal of virology.

[36]  M. Sheng,et al.  Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences , 1988, Molecular and cellular biology.

[37]  E. Wagner,et al.  c-fos expression interferes with thymus development in transgenic mice , 1988, Cell.

[38]  K. Riabowol,et al.  Microinjection of fos-specific antibodies blocks DNA synthesis in fibroblast cells , 1988, Molecular and cellular biology.

[39]  K. Nishikura,et al.  Antisense RNA of proto-oncogene c-fos blocks renewed growth of quiescent 3T3 cells. , 1987, Molecular and cellular biology.

[40]  A. Nienhuis,et al.  Inducible production of c-fos antisense RNA inhibits 3T3 cell proliferation. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[41]  L. Matrisian,et al.  The role of C-Fos in growth factor regulation of stromelysin/transin gene expression. , 1992, Matrix (Stuttgart, Germany). Supplement.

[42]  H. Herschman.  Primary response genes induced by growth factors and tumor promoters. , 1991, Annual review of biochemistry.

[43]  P. Sassone-Corsi,et al.  Dimers, leucine zippers and DNA-binding domains. , 1990, Trends in genetics : TIG.

[44]  E. Robertson.  Teratocarcinomas and embryonic stem cells : a practical approach , 1987 .

[45]  T. Curran,et al.  Isolation and characterization of the c-fos(rat) cDNA and analysis of post-translational modification in vitro. , 1987, Oncogene.