Identification of oncostatin M as a JAK2 V617F-dependent amplifier of cytokine production and bone marrow remodeling in myeloproliferative neoplasms

FASEB J. 2012 Feb;26(2):894-906. doi: 10.1096/fj.11-193078. Epub 2011 Nov 3.

Abstract

The JAK2 mutation V617F is detectable in a majority of patients with Philadelphia chromosome-negative myeloproliferative neoplasms (MPNs). Enforced expression of JAK2 V617F in mice induces myeloproliferation and bone marrow (BM) fibrosis, suggesting a causal role for the JAK2 mutant in the pathogenesis of MPNs. However, little is known about mechanisms and effector molecules contributing to JAK2 V617F-induced myeloproliferation and fibrosis. We show that JAK2 V617F promotes expression of oncostatin M (OSM) in neoplastic myeloid cells. Correspondingly, OSM mRNA levels were increased in the BM of patients with MPNs (median 287% of ABL, range 22-1450%) compared to control patients (median 59% of ABL, range 12-264%; P < 0.0001). OSM secreted by JAK2 V617F+ cells stimulated growth of fibroblasts and microvascular endothelial cells and induced the production of angiogenic and profibrogenic cytokines (HGF, VEGF, and SDF-1) in BM fibroblasts. All effects of MPN cell-derived OSM were blocked by a neutralizing anti-OSM antibody, whereas the production of OSM in MPN cells was suppressed by a pharmacologic JAK2 inhibitor or RNAi-mediated knockdown of JAK2. In summary, JAK2 V617F-mediated up-regulation of OSM may contribute to fibrosis, neoangiogenesis, and the cytokine storm observed in MPNs, suggesting that OSM might serve as a novel therapeutic target molecule in these neoplasms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Base Sequence
  • Bone Marrow / metabolism
  • Bone Marrow / pathology
  • Case-Control Studies
  • Cell Line
  • Cytokines / biosynthesis
  • Gene Knockdown Techniques
  • Humans
  • Janus Kinase 2 / antagonists & inhibitors
  • Janus Kinase 2 / genetics*
  • Janus Kinase 2 / metabolism*
  • Mice
  • Mutant Proteins / genetics*
  • Mutant Proteins / metabolism*
  • Mutation, Missense
  • Myeloproliferative Disorders / genetics*
  • Myeloproliferative Disorders / metabolism*
  • Myeloproliferative Disorders / pathology
  • Neovascularization, Pathologic
  • Oncostatin M / blood
  • Oncostatin M / genetics
  • Oncostatin M / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Polycythemia Vera / genetics
  • Polycythemia Vera / metabolism
  • Polycythemia Vera / pathology
  • Primary Myelofibrosis / genetics
  • Primary Myelofibrosis / metabolism
  • Primary Myelofibrosis / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • STAT5 Transcription Factor / metabolism
  • Thrombocythemia, Essential / genetics
  • Thrombocythemia, Essential / metabolism
  • Thrombocythemia, Essential / pathology

Substances

  • Cytokines
  • Mutant Proteins
  • OSM protein, human
  • RNA, Messenger
  • STAT5 Transcription Factor
  • Oncostatin M
  • Phosphatidylinositol 3-Kinases
  • JAK2 protein, human
  • Janus Kinase 2