JAK2V617F but not CALR mutations confer increased molecular responses to interferon-α via JAK1/STAT1 activation

Leukemia. 2019 Apr;33(4):995-1010. doi: 10.1038/s41375-018-0295-6. Epub 2018 Nov 23.

Abstract

Pegylated interferon-α (peg-IFNa) treatment induces molecular responses (MR) in patients with myeloproliferative neoplasms (MPNs), including partial MR (PMR) in 30-40% of patients. Here, we compared the efficacy of IFNa treatment in JAK2V617F- vs. calreticulin (CALR)-mutated cells and investigated the mechanisms of differential response. Retrospective analysis of MPN patients treated with peg-IFNa demonstrated that patients harboring the JAK2V617F mutation were more likely to achieve PMR than those with mutated CALR (p = 0.004), while there was no significant difference in hematological response. In vitro experiments confirmed an upregulation of IFN-stimulated genes in JAK2V617F-positive 32D cells as well as patient samples (peripheral blood mononuclear cells and CD34+ hematopoietic stem cells) compared to their CALR-mutated counterparts, and higher IFNa doses were needed to achieve the same IFNa response in CALR- as in JAK2V617F-mutant 32D cells. Additionally, Janus-activated kinase-1 (JAK1) and signal transducers and activators of transcription 1 (STAT1) showed constitutive phosphorylation in JAK2V617F-mutated but not CALR-mutated cells, indicating priming towards an IFNa response. Moreover, IFN-induced growth arrest was counteracted by selective JAK1 inhibition but enhanced by JAK2 inhibition. In conclusion, our data suggest that, clinically, higher doses of IFNa are needed in CALR-mutated vs. JAK2V617F-positive patients and we suggest a model of JAK2V617F-JAK1/STAT1 crosstalk leading to a priming of JAK2V617F-positive cells to IFNa resulting in differential sensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antiviral Agents / pharmacology
  • Apoptosis
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Calreticulin / genetics*
  • Cell Proliferation
  • Female
  • Follow-Up Studies
  • Humans
  • Interferon-alpha / pharmacology*
  • Janus Kinase 1 / genetics
  • Janus Kinase 1 / metabolism*
  • Janus Kinase 2 / genetics*
  • Male
  • Mice
  • Middle Aged
  • Mutation*
  • Myeloproliferative Disorders / drug therapy*
  • Myeloproliferative Disorders / genetics
  • Myeloproliferative Disorders / metabolism
  • Myeloproliferative Disorders / pathology
  • Prognosis
  • Retrospective Studies
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / metabolism*
  • Tumor Cells, Cultured

Substances

  • Antiviral Agents
  • Biomarkers, Tumor
  • CALR protein, human
  • Calreticulin
  • Interferon-alpha
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • JAK1 protein, human
  • JAK2 protein, human
  • Janus Kinase 1
  • Janus Kinase 2