Nuclear pore protein NUP210 depletion suppresses metastasis through heterochromatin-mediated disruption of tumor cell mechanical response

Nat Commun. 2021 Dec 13;12(1):7216. doi: 10.1038/s41467-021-27451-w.

Abstract

Mechanical signals from the extracellular microenvironment have been implicated in tumor and metastatic progression. Here, we identify nucleoporin NUP210 as a metastasis susceptibility gene for human estrogen receptor positive (ER+) breast cancer and a cellular mechanosensor. Nup210 depletion suppresses lung metastasis in mouse models of breast cancer. Mechanistically, NUP210 interacts with LINC complex protein SUN2 which connects the nucleus to the cytoskeleton. In addition, the NUP210/SUN2 complex interacts with chromatin via the short isoform of BRD4 and histone H3.1/H3.2 at the nuclear periphery. In Nup210 knockout cells, mechanosensitive genes accumulate H3K27me3 heterochromatin modification, mediated by the polycomb repressive complex 2 and differentially reposition within the nucleus. Transcriptional repression in Nup210 knockout cells results in defective mechanotransduction and focal adhesion necessary for their metastatic capacity. Our study provides an important role of nuclear pore protein in cellular mechanosensation and metastasis.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology*
  • CCCTC-Binding Factor / metabolism
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Cytoskeleton / metabolism
  • Enhancer of Zeste Homolog 2 Protein / metabolism
  • Focal Adhesions / genetics
  • Gene Expression Regulation, Neoplastic
  • Heterochromatin / metabolism*
  • Histones / metabolism
  • Humans
  • Mechanotransduction, Cellular / genetics*
  • Methyltransferases / metabolism
  • Mice
  • Neoplasm Metastasis
  • Neoplastic Cells, Circulating / metabolism
  • Nuclear Envelope / metabolism
  • Nuclear Pore Complex Proteins / genetics
  • Nuclear Pore Complex Proteins / metabolism*
  • Nuclear Proteins / metabolism
  • Polymorphism, Genetic
  • Prognosis
  • Promoter Regions, Genetic
  • Protein Binding
  • Repressor Proteins / metabolism
  • Transcription Factors / metabolism
  • Tumor Microenvironment

Substances

  • Brd4 protein, mouse
  • CCCTC-Binding Factor
  • Ctcf protein, mouse
  • Heterochromatin
  • Histones
  • Nuclear Pore Complex Proteins
  • Nuclear Proteins
  • Nup210 protein, mouse
  • Repressor Proteins
  • Transcription Factors
  • Suv39h1 protein, mouse
  • Methyltransferases
  • Enhancer of Zeste Homolog 2 Protein
  • Ezh2 protein, mouse