Oncogenic ZMYND11-MBTD1 fusion protein anchors the NuA4/TIP60 histone acetyltransferase complex to the coding region of active genes

Cell Rep. 2022 Jun 14;39(11):110947. doi: 10.1016/j.celrep.2022.110947.

Abstract

A recurrent chromosomal translocation found in acute myeloid leukemia leads to an in-frame fusion of the transcription repressor ZMYND11 to MBTD1, a subunit of the NuA4/TIP60 histone acetyltransferase complex. To understand the abnormal molecular events that ZMYND11-MBTD1 expression can create, we perform a biochemical and functional characterization comparison to each individual fusion partner. ZMYND11-MBTD1 is stably incorporated into the endogenous NuA4/TIP60 complex, leading to its mislocalization on the body of genes normally bound by ZMYND11. This can be correlated to increased chromatin acetylation and altered gene transcription, most notably on the MYC oncogene, and alternative splicing. Importantly, ZMYND11-MBTD1 expression favors Myc-driven pluripotency during embryonic stem cell differentiation and self-renewal of hematopoietic stem/progenitor cells. Altogether, these results indicate that the ZMYND11-MBTD1 fusion functions primarily by mistargeting the NuA4/TIP60 complex to the body of genes, altering normal transcription of specific genes, likely driving oncogenesis in part through the Myc regulatory network.

Keywords: AML; CP: Molecular biology; MBTD1; MYC; NuA4; TIP60; ZMYND11; acetylation; chromatin; mRNA processing; protein fusion; transcription; translocation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Cell Cycle Proteins / metabolism
  • Chromatin*
  • Chromosomal Proteins, Non-Histone / metabolism
  • Co-Repressor Proteins / metabolism
  • DNA-Binding Proteins / metabolism
  • Histone Acetyltransferases* / genetics
  • Histone Acetyltransferases* / metabolism
  • Humans
  • Lysine Acetyltransferase 5 / genetics
  • Lysine Acetyltransferase 5 / metabolism
  • Oncogene Proteins, Fusion* / genetics
  • Oncogene Proteins, Fusion* / metabolism
  • Open Reading Frames* / genetics
  • Translocation, Genetic

Substances

  • Cell Cycle Proteins
  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • Co-Repressor Proteins
  • DNA-Binding Proteins
  • MBTD1 protein, human
  • Oncogene Proteins, Fusion
  • ZMYND11 protein, human
  • Histone Acetyltransferases
  • Lysine Acetyltransferase 5