Jak2V617F and Dnmt3a loss cooperate to induce myelofibrosis through activated enhancer-driven inflammation

Blood. 2018 Dec 27;132(26):2707-2721. doi: 10.1182/blood-2018-04-846220. Epub 2018 Oct 26.

Abstract

Myeloproliferative neoplasms (MPNs) are a group of blood cancers that arise following the sequential acquisition of genetic lesions in hematopoietic stem and progenitor cells (HSPCs). We identify mutational cooperation between Jak2V617F expression and Dnmt3a loss that drives progression from early-stage polycythemia vera to advanced myelofibrosis. Using in vivo, clustered regularly interspaced short palindromic repeats (CRISPR) with CRISPR-associated protein 9 (Cas9) disruption of Dnmt3a in Jak2V617F knockin HSPC, we show that Dnmt3a loss blocks the accumulation of erythroid elements and causes fibrotic infiltration within the bone marrow and spleen. Transcriptional analysis and integration with human data sets identified a core DNMT3A-driven gene-expression program shared across multiple models and contexts of Dnmt3a loss. Aberrant self-renewal and inflammatory signaling were seen in Dnmt3a-/- Jak2V617F HSPC, driven by increased chromatin accessibility at enhancer elements. These findings identify oncogenic cooperativity between Jak2V617F-driven MPN and Dnmt3a loss, leading to activation of HSPC enhancer-driven inflammatory signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution*
  • Animals
  • DNA (Cytosine-5-)-Methyltransferases* / genetics
  • DNA (Cytosine-5-)-Methyltransferases* / metabolism
  • DNA Methyltransferase 3A
  • Hematologic Neoplasms* / enzymology
  • Hematologic Neoplasms* / genetics
  • Hematologic Neoplasms* / pathology
  • Hematopoietic Stem Cells* / enzymology
  • Hematopoietic Stem Cells* / pathology
  • Humans
  • Janus Kinase 2 / genetics
  • Janus Kinase 2 / metabolism
  • Mice
  • Mice, Mutant Strains
  • Mutation, Missense*
  • Primary Myelofibrosis* / enzymology
  • Primary Myelofibrosis* / genetics
  • Primary Myelofibrosis* / pathology
  • Signal Transduction / genetics*

Substances

  • DNMT3A protein, human
  • Dnmt3a protein, mouse
  • DNA (Cytosine-5-)-Methyltransferases
  • DNA Methyltransferase 3A
  • Jak2 protein, mouse
  • Janus Kinase 2