Loss of Par3 promotes prostatic tumorigenesis by enhancing cell growth and changing cell division modes

Oncogene. 2019 Mar;38(12):2192-2205. doi: 10.1038/s41388-018-0580-x. Epub 2018 Nov 22.

Abstract

Although cell polarity plays an important role in epithelial tumorigenesis, the consequence of polarity protein loss in prostatic tumorigenesis and the underlying mechanisms remain unclear. Using conditional knockout mouse models, we found in the current study that loss of polarity protein Par3 increases prostatic epithelial cell growth, elevates symmetrical cell divisions in basal cells, and randomizes spindle orientation in luminal cells, causing the development of high-grade prostatic intraepithelial neoplasia (PIN). Mechanistically, loss of Par3 dissociates the Par3/merlin/Lats1 complex, consequently inhibiting phosphorylation of Lats1 to attenuate the Hippo pathway. Furthermore, attenuated Hippo pathway enhances nuclear translocation of Yes-associated protein (YAP), which promotes cell proliferation and symmetrical cell divisions through transcriptional activation of Ki-67 and Sox2. In addition, Lats1 dephosphorylation impairs its interaction with G protein signaling modulator 2 (GPSM2, which is also known as LGN) that causes randomization of spindle orientation in luminal cells. Interestingly, co-deletion of Par3 and Lats1 for complete blockade of the Hippo pathway in mice results in prostate tumor initiation, whereas co-deletion of Par3 and YAP for disrupting YAP nuclear translocation reverses the phenotypes to a relatively normal state. Therefore, our findings highlight combination of Par3 loss and blockade of the Hippo pathway as a novel mechanism for prostatic tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Carcinogenesis / genetics*
  • Cell Adhesion Molecules / deficiency*
  • Cell Adhesion Molecules / genetics*
  • Cell Cycle Proteins
  • Cell Division*
  • Cell Membrane / metabolism
  • Cell Nucleus / metabolism
  • Cell Proliferation
  • Epithelial Cells / pathology
  • Gene Knockout Techniques*
  • Hippo Signaling Pathway
  • Hippocalcin / metabolism
  • Male
  • Mice
  • Neoplasm Grading
  • Phenotype
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Prostatic Neoplasms / pathology*
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • Cell Adhesion Molecules
  • Cell Cycle Proteins
  • Pard3 protein, mouse
  • Phosphoproteins
  • YAP-Signaling Proteins
  • Yap1 protein, mouse
  • Hippocalcin
  • Lats1 protein, mouse
  • Stk4 protein, mouse
  • Protein Serine-Threonine Kinases