DNA damage uncouples the mitogenic response to IGF-I in MCF-7 malignant breast cancer cells by switching the roles of PI3 kinase and p21WAF1/Cip1

Int J Cancer. 2005 Sep 10;116(4):506-13. doi: 10.1002/ijc.21029.

Abstract

In addition to its mitogenic and survival actions, recent evidence indicates that IGF-I can enhance DNA repair, implying IGF activity may limit the efficacy of many therapeutic strategies that rely on induction of DNA damage. Although the individual pathways by which DNA damage and IGF-I act are well understood, the cross-talk between these signaling events is not well defined. We examined the effects of DNA damage on the IGF-I response of MCF-7 breast cancer cells. Cells were exposed to the UV mimetic, 4-NQO, or the gamma-irradiation mimetic and chemotherapeutic drug, bleomycin; cellular proliferation was assessed by cell counting, tritiated thymidine incorporation and FACS cell cycle analysis. Although IGF-I acutely suppressed the p53 response to both agents, it subsequently enhanced the chronic increase in p53 and p21(WAF1/Cip1), resulting in cell cycle arrest; however, no apoptosis was observed. Use of specific inhibitors demonstrated that PI3 kinase was utilized with p38 MAPK to induce the p53 response to DNA damage, but was also utilized by IGF-I to diminish the acute p53 response. In addition, p21WAF1/Cip1 was increased by IGF-I, which has previously been shown to contribute to the mitogenic response. Here we demonstrate that with DNA damage IGF-I can also enhance the chronic p53-dependent increase in p21WAF1/Cip1, culminating in growth arrest. Overall, we have shown that PI3 kinase and p21WAF1/Cip1 play dual roles in mediating the mitogenic response to IGF-I, but these are both switched by cellular DNA damage to mediate a growth arrest.

MeSH terms

  • Breast Neoplasms / genetics*
  • Breast Neoplasms / pathology*
  • Cell Cycle
  • Cell Cycle Proteins / biosynthesis*
  • Cell Cycle Proteins / physiology*
  • Cyclin-Dependent Kinase Inhibitor p21
  • DNA Damage*
  • DNA Repair
  • Female
  • Humans
  • Insulin-Like Growth Factor I / physiology*
  • Mitogens
  • Phosphatidylinositol 3-Kinases / biosynthesis*
  • Phosphatidylinositol 3-Kinases / physiology*
  • Signal Transduction
  • Tumor Cells, Cultured
  • Tumor Suppressor Protein p53 / physiology*

Substances

  • CDKN1A protein, human
  • Cell Cycle Proteins
  • Cyclin-Dependent Kinase Inhibitor p21
  • Mitogens
  • Tumor Suppressor Protein p53
  • Insulin-Like Growth Factor I
  • Phosphatidylinositol 3-Kinases