Abrogation of the retinoblastoma tumor suppressor checkpoint during keratinocyte immortalization is not sufficient for induction of centrosome-mediated genomic instability

Cancer Res. 2003 Jan 15;63(2):476-83.

Abstract

Deregulation of the retinoblastoma (pRB) tumor suppressor pathway and telomerase activation have been identified as rate-limiting steps for immortalization of primary human epithelial cells. However, additional molecular aberrations including p53 inactivation, ras activation, and deregulation of protein phosphatase 2A activity are necessary for full transformation of immortalized epithelial cells. Genomic instability is observed in most human tumors and constitutes an important mechanism to allow emerging tumor cells to acquire additional mutations to efficiently overcome selection barriers during carcinogenic progression. In an attempt to model oral cancer in a human cell-based system, we analyzed normal oral epithelial keratinocytes with the pRB pathway dysregulated by loss of expression of the cyclin-dependent kinase (cdk) 4/cdk6 inhibitor p16(INK4A) and/or ectopic expression of cdk4 or expression of the human papillomavirus (HPV) type 16 E7 oncoprotein. Ectopic expression of cdk4 and HPV-16 E7 was equally efficient in extending the life span of normal oral keratinocytes, and each was able to cooperate with telomerase (hTERT) to immortalize these cells. HPV-16 E7/hTERT-immortalized normal oral keratinocytes showed centrosome abnormalities, whereas populations of cdk4/hTERT-immortalized cells or hTERT-immortalized cells that had lost expression of p16INK4A showed no such abnormalities. These results demonstrate that disruption of the p16INK4A/pRB checkpoint of epithelial cell immortalization does not necessarily lead to centrosome-associated genomic instability.

Publication types

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

MeSH terms

  • Cell Transformation, Neoplastic / genetics*
  • Cell Transformation, Neoplastic / metabolism
  • Centrosome / physiology*
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase Inhibitor p16 / antagonists & inhibitors
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • Cyclin-Dependent Kinase Inhibitor p16 / physiology
  • Cyclin-Dependent Kinases / biosynthesis
  • DNA-Binding Proteins
  • Gingiva / cytology
  • Humans
  • Keratinocytes / cytology
  • Keratinocytes / metabolism
  • Keratinocytes / physiology*
  • Keratinocytes / virology
  • Oncogene Proteins, Viral / biosynthesis
  • Papillomavirus E7 Proteins
  • Proto-Oncogene Proteins*
  • Retinoblastoma Protein / antagonists & inhibitors*
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / physiology
  • Telomerase / biosynthesis
  • Tumor Suppressor Protein p53 / antagonists & inhibitors
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / physiology

Substances

  • Cyclin-Dependent Kinase Inhibitor p16
  • DNA-Binding Proteins
  • Oncogene Proteins, Viral
  • Papillomavirus E7 Proteins
  • Proto-Oncogene Proteins
  • Retinoblastoma Protein
  • Tumor Suppressor Protein p53
  • oncogene protein E7, Human papillomavirus type 16
  • CDK4 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinases
  • Telomerase