Effect of the unfolded protein response and oxidative stress on mutagenesis in CSF3R: a model for evolution of severe congenital neutropenia to myelodysplastic syndrome/acute myeloid leukemia

Mutagenesis. 2020 Dec 1;35(5):381-389. doi: 10.1093/mutage/geaa027.

Abstract

Severe congenital neutropenia (SCN) is a rare blood disorder characterised by abnormally low levels of circulating neutrophils. The most common recurrent mutations that cause SCN involve neutrophil elastase (ELANE). The treatment of choice for SCN is the administration of granulocyte-colony stimulating factor (G-CSF), which increases the neutrophil number and improves the survival and quality of life. Long-term survival is however linked to the development of myelodysplastic syndrome/acute myeloid leukemia (MDS/AML). About 70% of MDS/AML patients acquire nonsense mutations affecting the cytoplasmic domain of CSF3R (the G-CSF receptor). About 70% of SCN patients with AML harbour additional mutations in RUNX1. We hypothesised that this coding region of CSF3R constitutes a hotspot vulnerable to mutations resulting from excessive oxidative stress or endoplasmic reticulum (ER) stress. We used the murine Ba/F3 cell line to measure the effect of induced oxidative or ER stress on the mutation rate in our hypothesised hotspot of the exogenous human CSF3R, the corresponding region in the endogenous Csf3r, and Runx1. Ba/F3 cells transduced with the cDNA for partial C-terminal of CSF3R fused in-frame with a green fluorescent protein (GFP) tag were subjected to stress-inducing treatment for 30 days (~51 doubling times). The amplicon-based targeted deep sequencing data for days 15 and 30 samples show that although there was increased mutagenesis observed in all the three genes of interest (partial CSF3R, Csf3r and Runx1), there were more mutations in the GFP region compared with the partial CSF3R region. Our findings also indicate that there is no correlation between the stress-inducing chemical treatments and mutagenesis in Ba/F3 cells. Our data suggest that oxidative or ER stress induction does not promote genomic instability, affecting partial C-terminal of the transduced CSF3R, the endogenous Csf3R and the endogenous Runx1 in Ba/F3 cells that could account for these targets to being mutational hotspots. We conclude that other mechanisms to acquire mutations of CSF3R that help drive the evolution of SCN to MDS/AML.

Publication types

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

MeSH terms

  • Animals
  • Congenital Bone Marrow Failure Syndromes / complications
  • Congenital Bone Marrow Failure Syndromes / drug therapy
  • Congenital Bone Marrow Failure Syndromes / genetics
  • Congenital Bone Marrow Failure Syndromes / pathology
  • Core Binding Factor Alpha 2 Subunit / drug effects
  • Core Binding Factor Alpha 2 Subunit / genetics*
  • Endoplasmic Reticulum Stress / drug effects
  • GATA2 Deficiency / complications
  • GATA2 Deficiency / drug therapy*
  • GATA2 Deficiency / genetics
  • GATA2 Deficiency / pathology
  • Gene Expression Regulation, Leukemic / drug effects
  • Granulocyte Colony-Stimulating Factor / pharmacology
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Mice
  • Mutagenesis / drug effects
  • Mutagenesis / genetics
  • Mutation / drug effects
  • Mutation Rate
  • Neutropenia / complications
  • Neutropenia / congenital
  • Neutropenia / drug therapy
  • Neutropenia / genetics
  • Neutropenia / pathology
  • Neutrophils / drug effects
  • Oxidative Stress / drug effects
  • Receptors, Colony-Stimulating Factor / administration & dosage
  • Receptors, Colony-Stimulating Factor / genetics*
  • Signal Transduction
  • Unfolded Protein Response / drug effects

Substances

  • CSF3R protein, human
  • Core Binding Factor Alpha 2 Subunit
  • Csf3r protein, mouse
  • Receptors, Colony-Stimulating Factor
  • Runx1 protein, mouse
  • Granulocyte Colony-Stimulating Factor

Supplementary concepts

  • Neutropenia, Severe Congenital, Autosomal Recessive 3