Genetic and epigenetic evolution as a contributor to WT1-mutant leukemogenesis

Blood. 2018 Sep 20;132(12):1265-1278. doi: 10.1182/blood-2018-03-837468. Epub 2018 Jul 31.

Abstract

Genetic studies have identified recurrent somatic mutations in acute myeloid leukemia (AML) patients, including in the Wilms' tumor 1 (WT1) gene. The molecular mechanisms by which WT1 mutations contribute to leukemogenesis have not yet been fully elucidated. We investigated the role of Wt1 gene dosage in steady-state and pathologic hematopoiesis. Wt1 heterozygous loss enhanced stem cell self-renewal in an age-dependent manner, which increased stem cell function over time and resulted in age-dependent leukemic transformation. Wt1-haploinsufficient leukemias were characterized by progressive genetic and epigenetic alterations, including those in known leukemia-associated alleles, demonstrating a requirement for additional events to promote hematopoietic transformation. Consistent with this observation, we found that Wt1 depletion cooperates with Flt3-ITD mutation to induce fully penetrant AML. Our studies provide insight into mechanisms of Wt1-loss leukemogenesis and into the evolutionary events required to induce transformation of Wt1-haploinsufficient stem/progenitor cells.

Publication types

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

MeSH terms

  • Animals
  • Carcinogenesis / genetics
  • Carcinogenesis / pathology
  • Cell Self Renewal
  • Epigenesis, Genetic*
  • Gene Deletion
  • Gene Expression Regulation, Leukemic*
  • Hematopoietic Stem Cells / metabolism
  • Hematopoietic Stem Cells / pathology
  • Leukemia, Myeloid, Acute / genetics*
  • Leukemia, Myeloid, Acute / pathology
  • Leukopoiesis
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation*
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Repressor Proteins / genetics*
  • WT1 Proteins
  • fms-Like Tyrosine Kinase 3 / genetics

Substances

  • Repressor Proteins
  • WT1 Proteins
  • WT1 protein, mouse
  • Flt3 protein, mouse
  • fms-Like Tyrosine Kinase 3