c-Myc regulates cyclin D-Cdk4 and -Cdk6 activity but affects cell cycle progression at multiple independent points

Mol Cell Biol. 1999 Jul;19(7):4672-83. doi: 10.1128/MCB.19.7.4672.

Abstract

c-myc is a cellular proto-oncogene associated with a variety of human cancers and is strongly implicated in the control of cellular proliferation, programmed cell death, and differentiation. We have previously reported the first isolation of a c-myc-null cell line. Loss of c-Myc causes a profound growth defect manifested by the lengthening of both the G1 and G2 phases of the cell cycle. To gain a clearer understanding of the role of c-Myc in cellular proliferation, we have performed a comprehensive analysis of the components that regulate cell cycle progression. The largest defect observed in c-myc-/- cells is a 12-fold reduction in the activity of cyclin D1-Cdk4 and -Cdk6 complexes during the G0-to-S transition. Downstream events, such as activation of cyclin E-Cdk2 and cyclin A-Cdk2 complexes, are delayed and reduced in magnitude. However, it is clear that c-Myc affects the cell cycle at multiple independent points, because restoration of the Cdk4 and -6 defect does not significantly increase growth rate. In exponentially cycling cells the absence of c-Myc reduces coordinately the activities of all cyclin-cyclin-dependent kinase complexes. An analysis of cyclin-dependent kinase complex regulators revealed increased expression of p27(KIP1) and decreased expression of Cdk7 in c-myc-/- cells. We propose that c-Myc functions as a crucial link in the coordinate adjustment of growth rate to environmental conditions.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • CDC2-CDC28 Kinases*
  • Calcium-Calmodulin-Dependent Protein Kinases / biosynthesis
  • Carrier Proteins*
  • Cell Cycle / physiology*
  • Cell Cycle Proteins*
  • Cell Division
  • Cell Line
  • Cyclin A / biosynthesis
  • Cyclin D
  • Cyclin E / biosynthesis
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Cyclin-Dependent Kinase Inhibitor p27
  • Cyclin-Dependent Kinases / biosynthesis
  • Cyclin-Dependent Kinases / metabolism*
  • Cyclins / metabolism*
  • DNA-Binding Proteins*
  • E2F Transcription Factors
  • Enzyme Activation
  • Humans
  • Microtubule-Associated Proteins / genetics
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases*
  • Nuclear Proteins / metabolism
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Protein Serine-Threonine Kinases / biosynthesis
  • Protein Serine-Threonine Kinases / metabolism*
  • Proteins*
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-fos / biosynthesis
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / physiology*
  • Proto-Oncogene Proteins*
  • Rats
  • Retinoblastoma Protein / metabolism
  • Retinoblastoma-Binding Protein 1
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Transcription Factor DP1
  • Transcription Factors / biosynthesis
  • Tumor Suppressor Proteins*

Substances

  • Carrier Proteins
  • Cdkn1b protein, rat
  • Cell Cycle Proteins
  • Cyclin A
  • Cyclin D
  • Cyclin E
  • Cyclins
  • DNA-Binding Proteins
  • E2F Transcription Factors
  • MAS1 protein, human
  • Microtubule-Associated Proteins
  • Nuclear Proteins
  • Phosphoproteins
  • Proteins
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-fos
  • Proto-Oncogene Proteins c-myc
  • RBL2 protein, human
  • Rbl2 protein, rat
  • Retinoblastoma Protein
  • Retinoblastoma-Binding Protein 1
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Transcription Factor DP1
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Cyclin-Dependent Kinase Inhibitor p27
  • Protein Serine-Threonine Kinases
  • Calcium-Calmodulin-Dependent Protein Kinases
  • CDC2-CDC28 Kinases
  • CDK2 protein, human
  • CDK4 protein, human
  • CDK6 protein, human
  • Cdk2 protein, rat
  • Cdk4 protein, rat
  • Cdk6 protein, rat
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • Cyclin-Dependent Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases