14-3-3γ Prevents Centrosome Amplification and Neoplastic Progression

Sci Rep. 2016 Jun 2:6:26580. doi: 10.1038/srep26580.

Abstract

More than 80% of malignant tumors show centrosome amplification and clustering. Centrosome amplification results from aberrations in the centrosome duplication cycle, which is strictly coordinated with DNA-replication-cycle. However, the relationship between cell-cycle regulators and centrosome duplicating factors is not well understood. This report demonstrates that 14-3-3γ localizes to the centrosome and 14-3-3γ loss leads to centrosome amplification. Loss of 14-3-3γ results in the phosphorylation of NPM1 at Thr-199, causing early centriole disjunction and centrosome hyper-duplication. The centrosome amplification led to aneuploidy and increased tumor formation in mice. Importantly, an increase in passage of the 14-3-3γ-knockdown cells led to an increase in the number of cells containing clustered centrosomes leading to the generation of pseudo-bipolar spindles. The increase in pseudo-bipolar spindles was reversed and an increase in the number of multi-polar spindles was observed upon expression of a constitutively active 14-3-3-binding-defective-mutant of cdc25C (S216A) in the 14-3-3γ knockdown cells. The increase in multi-polar spindle formation was associated with decreased cell viability and a decrease in tumor growth. Our findings uncover the molecular basis of regulation of centrosome duplication by 14-3-3γ and inhibition of tumor growth by premature activation of the mitotic program and the disruption of centrosome clustering.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / genetics
  • 14-3-3 Proteins / metabolism*
  • Aneuploidy
  • Animals
  • Cell Cycle
  • Cell Line, Tumor
  • Centrosome / metabolism*
  • Centrosome / pathology
  • Chromosomal Instability*
  • Gene Deletion
  • HCT116 Cells
  • Humans
  • Mice
  • Neoplasm Transplantation
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / pathology*
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / metabolism
  • Nucleophosmin
  • Phosphorylation
  • Threonine / chemistry
  • cdc25 Phosphatases / metabolism

Substances

  • 14-3-3 Proteins
  • NPM1 protein, human
  • Npm1 protein, mouse
  • Nuclear Proteins
  • Nucleophosmin
  • Threonine
  • Cdc25c protein, mouse
  • cdc25 Phosphatases