Zmat3 Is a Key Splicing Regulator in the p53 Tumor Suppression Program

Mol Cell. 2020 Nov 5;80(3):452-469.e9. doi: 10.1016/j.molcel.2020.10.022.

Abstract

Although TP53 is the most commonly mutated gene in human cancers, the p53-dependent transcriptional programs mediating tumor suppression remain incompletely understood. Here, to uncover critical components downstream of p53 in tumor suppression, we perform unbiased RNAi and CRISPR-Cas9-based genetic screens in vivo. These screens converge upon the p53-inducible gene Zmat3, encoding an RNA-binding protein, and we demonstrate that ZMAT3 is an important tumor suppressor downstream of p53 in mouse KrasG12D-driven lung and liver cancers and human carcinomas. Integrative analysis of the ZMAT3 RNA-binding landscape and transcriptomic profiling reveals that ZMAT3 directly modulates exon inclusion in transcripts encoding proteins of diverse functions, including the p53 inhibitors MDM4 and MDM2, splicing regulators, and components of varied cellular processes. Interestingly, these exons are enriched in NMD signals, and, accordingly, ZMAT3 broadly affects target transcript stability. Collectively, these studies reveal ZMAT3 as a novel RNA-splicing and homeostasis regulator and a key component of p53-mediated tumor suppression.

Keywords: CRISPR screen; Mdm4; RBP; RNAi screen; Zmat3; alternative splicing; hepatocellular carcinoma; lung adenocarcinoma; p53; tumor suppression.

Publication types

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

MeSH terms

  • Adenocarcinoma / genetics
  • Alternative Splicing
  • Animals
  • Cell Cycle Proteins / metabolism
  • Exons
  • Gene Expression Profiling / methods
  • Genes, Tumor Suppressor
  • Humans
  • Liver Neoplasms / genetics
  • Male
  • Mice
  • Mice, Inbred ICR
  • Mice, SCID
  • RNA Interference
  • RNA Splicing
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • Tumor Suppressor Protein p53 / genetics*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Cell Cycle Proteins
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • ZMAT3 protein, human