Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins

Mol Cell Biol. 1996 Jun;16(6):2570-8. doi: 10.1128/MCB.16.6.2570.

Abstract

Cells which are highly proliferative typically lack expression of differentiated, lineage-specific characteristics. Id2, a member of the helix-loop-helix (HLH) protein family known to inhibit cell differentiation, binds to the retinoblastoma protein (pRb) and abolishes its growth-suppressing activity. We found that Id2 but not Id1 or Id3 was able to bind in vitro not only pRb but also the related proteins p107 and p130. Also, an association between Id2 and p107 or p130 was observed in vivo in transiently transfected Saos-2 cells. In agreement with these results, expression of Id1 or Id3 did not affect the block of cell cycle progression mediated by pRb. Conversely, expression of Id2 specifically reversed the cell cycle arrest induced by each of the three members of the pRb family. Furthermore, the growth-suppressive activities of cyclin-dependent kinase inhibitors p16 and p21 were efficiently antagonized by high levels of Id2 but not by Id1 Id3. Consistent with the role of p16 as a selective inhibitor of pRb and pRb-related protein kinase activity, p16-imposed cell cycle arrest was completely abolished by Id2. Only a partial reversal of p21-induced growth suppression was observed, which correlated with the presence of a functional pRb. We also documented decreased levels of cyclin D1 protein and mRNA and the loss of cyclin D1-cdk4 complexes in cells constitutively expressing Id2. These data provide evidence for important Id2-mediated alterations in cell cycle components normally involved in the regulatory events of cell cycle progression, and they highlight a specific role for Id2 as an antagonist of multiple tumor suppressor proteins.

Publication types

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

MeSH terms

  • Cell Cycle / physiology*
  • Cyclin D1
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinases / genetics
  • Cyclin-Dependent Kinases / physiology
  • Cyclins / genetics
  • Cyclins / physiology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Helix-Loop-Helix Motifs
  • Humans
  • Inhibitor of Differentiation Protein 1
  • Inhibitor of Differentiation Protein 2
  • Inhibitor of Differentiation Proteins
  • Neoplasm Proteins*
  • Nuclear Proteins / antagonists & inhibitors
  • Nuclear Proteins / physiology
  • Oncogene Proteins / genetics
  • Oncogene Proteins / physiology
  • Phosphoproteins / antagonists & inhibitors
  • Phosphoproteins / physiology
  • Protein Binding
  • Proteins*
  • Proto-Oncogene Proteins*
  • Repressor Proteins*
  • Retinoblastoma Protein / antagonists & inhibitors
  • Retinoblastoma Protein / physiology*
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Transcription Factors / genetics
  • Transcription Factors / physiology
  • Transfection
  • Tumor Cells, Cultured

Substances

  • Cyclins
  • DNA-Binding Proteins
  • ID1 protein, human
  • ID2 protein, human
  • Inhibitor of Differentiation Protein 1
  • Inhibitor of Differentiation Protein 2
  • Inhibitor of Differentiation Proteins
  • Neoplasm Proteins
  • Nuclear Proteins
  • Oncogene Proteins
  • Phosphoproteins
  • Proteins
  • Proto-Oncogene Proteins
  • RBL1 protein, human
  • RBL2 protein, human
  • Repressor Proteins
  • Retinoblastoma Protein
  • Retinoblastoma-Like Protein p107
  • Retinoblastoma-Like Protein p130
  • Transcription Factors
  • Cyclin D1
  • ID3 protein, human
  • CDK4 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinases