Inner nuclear protein Matrin-3 coordinates cell differentiation by stabilizing chromatin architecture

Nat Commun. 2021 Oct 29;12(1):6241. doi: 10.1038/s41467-021-26574-4.

Abstract

Precise control of gene expression during differentiation relies on the interplay of chromatin and nuclear structure. Despite an established contribution of nuclear membrane proteins to developmental gene regulation, little is known regarding the role of inner nuclear proteins. Here we demonstrate that loss of the nuclear scaffolding protein Matrin-3 (Matr3) in erythroid cells leads to morphological and gene expression changes characteristic of accelerated maturation, as well as broad alterations in chromatin organization similar to those accompanying differentiation. Matr3 protein interacts with CTCF and the cohesin complex, and its loss perturbs their occupancy at a subset of sites. Destabilization of CTCF and cohesin binding correlates with altered transcription and accelerated differentiation. This association is conserved in embryonic stem cells. Our findings indicate Matr3 negatively affects cell fate transitions and demonstrate that a critical inner nuclear protein impacts occupancy of architectural factors, culminating in broad effects on chromatin organization and cell differentiation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CCCTC-Binding Factor
  • Cell Cycle Proteins / metabolism
  • Cell Differentiation / physiology
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Cell Nucleus / ultrastructure
  • Chromatin / chemistry*
  • Chromatin / metabolism
  • Chromosomal Proteins, Non-Histone / metabolism
  • Cohesins
  • Embryonic Stem Cells / physiology
  • Erythroid Cells / pathology
  • Leukemia, Erythroblastic, Acute / metabolism
  • Leukemia, Erythroblastic, Acute / pathology*
  • Mice
  • Mice, Knockout
  • Nuclear Matrix-Associated Proteins / genetics
  • Nuclear Matrix-Associated Proteins / metabolism*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*

Substances

  • CCCTC-Binding Factor
  • Cell Cycle Proteins
  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • Ctcf protein, mouse
  • Nuclear Matrix-Associated Proteins
  • RNA-Binding Proteins
  • matrin-3 protein, mouse