Chromosome 9p trisomy increases stem cells clonogenic potential and fosters T-cell exhaustion in JAK2-mutant myeloproliferative neoplasms

Leukemia. 2024 Oct;38(10):2171-2182. doi: 10.1038/s41375-024-02373-w. Epub 2024 Aug 23.

Abstract

JAK2V617F is the most recurrent genetic mutation in Philadelphia-negative chronic Myeloproliferative Neoplasms (MPNs). Since the JAK2 locus is located on Chromosome 9, we hypothesized that Chromosome 9 copy number abnormalities may be a disease modifier in JAK2V617F-mutant MPN patients. In this study, we identified a subset of MPN patients with partial or complete Chromosome 9 trisomy (+9p patients), who differ from JAK2V617F-homozygous MPN patients as they carry three JAK2 alleles as well as three copies of all neighboring gene loci, including CD274, encoding immunosuppressive Programmed death-ligand 1 (PD-L1) protein. Investigation of the clonal hierarchy revealed that the JAK2V617F occurs first, followed by +9p. Functionally, CD34+ cells from +9p MPN patients demonstrated increased clonogenicity, generating a greater number of primitive colonies, due to high OCT4 and NANOG expression, with knock-down of these genes leading to a genotype-specific decrease in colony numbers. Moreover, our analysis revealed increased PD-L1 surface expression in malignant monocytes from +9p patients, while analysis of the T cell compartment unveiled elevated levels of exhausted cytotoxic T cells. Overall, here we identify a distinct novel subgroup of MPN patients, who feature a synergistic interplay between +9p and JAK2V617F that shapes immune escape characteristics and increased stemness in CD34+ cells.

MeSH terms

  • Adult
  • Aged
  • Chromosomes, Human, Pair 9* / genetics
  • Female
  • Humans
  • Janus Kinase 2* / genetics
  • Male
  • Middle Aged
  • Mutation*
  • Myeloproliferative Disorders* / genetics
  • Myeloproliferative Disorders* / pathology
  • T-Cell Exhaustion
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Trisomy* / genetics

Substances

  • Janus Kinase 2
  • JAK2 protein, human