Cyclin E and c-Myc promote cell proliferation in the presence of p16INK4a and of hypophosphorylated retinoblastoma family proteins

EMBO J. 1997 Sep 1;16(17):5322-33. doi: 10.1093/emboj/16.17.5322.

Abstract

Retroviral expression of the cyclin-dependent kinase (CDK) inhibitor p16(INK4a) in rodent fibroblasts induces dephosphorylation of pRb, p107 and p130 and leads to G1 arrest. Prior expression of cyclin E allows S-phase entry and long-term proliferation in the presence of p16. Cyclin E prevents neither the dephosphorylation of pRb family proteins, nor their association with E2F proteins in response to p16. Thus, cyclin E can bypass the p16/pRb growth-inhibitory pathway downstream of pRb activation. Retroviruses expressing E2F-1, -2 or -3 also prevent p16-induced growth arrest but are ineffective against the cyclin E-CDK2 inhibitor p27(Kip1), suggesting that E2F cannot substitute for cyclin E activity. Thus, cyclin E possesses an E2F-independent function required to enter S-phase. However, cyclin E may not simply bypass E2F function in the presence of p16, since it restores expression of E2F-regulated genes such as cyclin A or CDC2. Finally, c-Myc bypasses the p16/pRb pathway with effects indistinguishable from those of cyclin E. We suggest that this effect of Myc is mediated by its action upstream of cyclin E-CDK2, and occurs via the neutralization of p27(Kip1) family proteins, rather than induction of Cdc25A. Our data imply that oncogenic activation of c-Myc, and possibly also of cyclin E, mimics loss of the p16/pRb pathway during oncogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Carrier Proteins*
  • Cell Cycle Proteins*
  • Cell Division / physiology*
  • Cyclin E / metabolism*
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism*
  • DNA-Binding Proteins*
  • E2F Transcription Factors
  • E2F1 Transcription Factor
  • Mice
  • Nuclear Proteins / metabolism
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Proteins*
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Rats
  • Recombinant Proteins / metabolism
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / metabolism*
  • Retinoblastoma-Binding Protein 1
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Retroviridae / genetics
  • Transcription Factor DP1
  • Transcription Factors / metabolism

Substances

  • Arid4a protein, mouse
  • Carrier Proteins
  • Cell Cycle Proteins
  • Cyclin E
  • Cyclin-Dependent Kinase Inhibitor p16
  • DNA-Binding Proteins
  • E2F Transcription Factors
  • E2F1 Transcription Factor
  • E2f1 protein, mouse
  • E2f1 protein, rat
  • Nuclear Proteins
  • Phosphoproteins
  • Proteins
  • Proto-Oncogene Proteins c-myc
  • Rbl1 protein, mouse
  • Rbl2 protein, mouse
  • Rbl2 protein, rat
  • Recombinant Proteins
  • Retinoblastoma Protein
  • Retinoblastoma-Binding Protein 1
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Transcription Factor DP1
  • Transcription Factors