Malignant Transformation Involving <i>CXXC4</i> Mutations Identified in a Leukemic Progression Model of Severe Congenital Neutropenia.

Olofsen, Patricia A; Fatrai, Szabolcs; van Strien, Paulina M H; Obenauer, Julia C; de Looper, Hans W J; Hoogenboezem, Remco M; Erpelinck-Verschueren, Claudia A J; Vermeulen, Michael P W M et al. · Cell Rep Med · 2020

basic_science · Level V

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Abstract

Severe congenital neutropenia (SCN) patients treated with CSF3/G-CSF to alleviate neutropenia frequently develop acute myeloid leukemia (AML). A common pattern of leukemic transformation involves the appearance of hematopoietic clones with CSF3 receptor (<i>CSF3R</i>) mutations in the neutropenic phase, followed by mutations in <i>RUNX1</i> before AML becomes overt. To investigate how the combination of CSF3 therapy and <i>CSF3R</i> and <i>RUNX1</i> mutations contributes to AML development, we make use of mouse models, SCN-derived induced pluripotent stem cells (iPSCs), and SCN and SCN-AML patient samples. CSF3 provokes a hyper-proliferative state in <i>CSF3R</i>/<i>RUNX1</i> mutant hematopoietic progenitors but does not cause overt AML. Intriguingly, an additional acquired driver mutation in <i>Cxxc4</i> causes elevated CXXC4 and reduced TET2 protein levels in murine AML samples. Expression of multiple pro-inflammatory pathways is elevated in mouse AML and human SCN-AML, suggesting that inflammation driven by downregulation of TET2 activity is a critical step in the malignant transformation of SCN.

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