Cyclin K regulates prereplicative complex assembly to promote mammalian cell proliferation

Nat Commun. 2018 May 14;9(1):1876. doi: 10.1038/s41467-018-04258-w.

Abstract

The assembly of prereplicative complex (pre-RC) during G1 phase must be tightly controlled to sustain cell proliferation and maintain genomic stability. Mechanisms to prevent pre-RC formation in G2/M and S phases are well appreciated, whereas how cells ensure efficient pre-RC assembly during G1 is less clear. Here we report that cyclin K regulates pre-RC formation. We find that cyclin K expression positively correlates with cell proliferation, and knockdown of cyclin K or its cognate kinase CDK12 prevents the assembly of pre-RC in G1 phase. Mechanistically we uncover that cyclin K promotes pre-RC assembly by restricting cyclin E1 activity in G1. We identify a cyclin K-dependent, novel phosphorylation site in cyclin E1 that disrupts its interaction with CDK2. Importantly, this antagonistic relationship is largely recapitulated in cyclin E1-overexpressing tumors. We discuss the implications of our findings in light of recent reports linking cyclin K and CDK12 to human tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Carcinogenesis / genetics*
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Proliferation
  • Cyclin E / genetics
  • Cyclin E / metabolism
  • Cyclin-Dependent Kinase 2 / genetics
  • Cyclin-Dependent Kinase 2 / metabolism
  • Cyclin-Dependent Kinases / genetics*
  • Cyclin-Dependent Kinases / metabolism
  • Cyclins / antagonists & inhibitors
  • Cyclins / genetics*
  • Cyclins / metabolism
  • Female
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • G1 Phase Cell Cycle Checkpoints / genetics*
  • G2 Phase Cell Cycle Checkpoints / genetics
  • Genomic Instability
  • HCT116 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • NIH 3T3 Cells
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism
  • Primary Cell Culture
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • S Phase Cell Cycle Checkpoints / genetics

Substances

  • CCNE1 protein, human
  • CCNK protein, human
  • Cyclin E
  • Cyclins
  • Oncogene Proteins
  • RNA, Small Interfering
  • CDK12 protein, human
  • CDK2 protein, human
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinases