Myeloproliferative neoplasms can be initiated from a single hematopoietic stem cell expressing JAK2-V617F

J Exp Med. 2014 Oct 20;211(11):2213-30. doi: 10.1084/jem.20131371. Epub 2014 Oct 6.

Abstract

The majority of patients with myeloproliferative neoplasms (MPNs) carry a somatic JAK2-V617F mutation. Because additional mutations can precede JAK2-V617F, it is questioned whether JAK2-V617F alone can initiate MPN. Several mouse models have demonstrated that JAK2-V617F can cause MPN; however, in all these models disease was polyclonal. Conversely, cancer initiates at the single cell level, but attempts to recapitulate single-cell disease initiation in mice have thus far failed. We demonstrate by limiting dilution and single-cell transplantations that MPN disease, manifesting either as erythrocytosis or thrombocytosis, can be initiated clonally from a single cell carrying JAK2-V617F. However, only a subset of mice reconstituted from single hematopoietic stem cells (HSCs) displayed MPN phenotype. Expression of JAK2-V617F in HSCs promoted cell division and increased DNA damage. Higher JAK2-V617F expression correlated with a short-term HSC signature and increased myeloid bias in single-cell gene expression analyses. Lower JAK2-V617F expression in progenitor and stem cells was associated with the capacity to stably engraft in secondary recipients. Furthermore, long-term repopulating capacity was also present in a compartment with intermediate expression levels of lineage markers. Our studies demonstrate that MPN can be initiated from a single HSC and illustrate that JAK2-V617F has complex effects on HSC biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • Antigens, Ly / metabolism
  • Antigens, Surface / metabolism
  • Biomarkers / metabolism
  • Bone Marrow Transplantation
  • Cell Cycle / genetics
  • Cell Lineage / genetics
  • Cell Transformation, Neoplastic / genetics*
  • Cluster Analysis
  • DNA Damage
  • Female
  • Gene Expression
  • Gene Expression Profiling
  • Hematopoietic Stem Cells / metabolism*
  • Hematopoietic Stem Cells / pathology
  • Immunophenotyping
  • Janus Kinase 2 / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Mutation*
  • Myeloproliferative Disorders / genetics*
  • Phenotype
  • Proto-Oncogene Proteins c-kit / metabolism
  • Transplantation Chimera

Substances

  • Antigens, Ly
  • Antigens, Surface
  • Biomarkers
  • Ly6a protein, mouse
  • Membrane Proteins
  • Proto-Oncogene Proteins c-kit
  • Janus Kinase 2