Differential modulation of mutant CALR and JAK2 V617F-driven oncogenesis by HLA genotype in myeloproliferative neoplasms

Front Immunol. 2024 Sep 16:15:1427810. doi: 10.3389/fimmu.2024.1427810. eCollection 2024.

Abstract

It has been demonstrated previously that human leukocyte antigen class I (HLA-I) and class II (HLA-II) alleles may modulate JAK2 V617F and CALR mutation (CALRmut)-associated oncogenesis in myeloproliferative neoplasms (MPNs). However, the role of immunogenetic factors in MPNs remains underexplored. We aimed to investigate the potential involvement of HLA genes in CALRmut+ MPNs. High-resolution genotyping of HLA-I and -II loci was conducted in 42 CALRmut+ and 158 JAK2 V617F+ MPN patients and 1,083 healthy controls. A global analysis of the diversity of HLA-I genotypes revealed no significant differences between CALRmut+ patients and controls. However, one HLA-I allele (C*06:02) showed an inverse correlation with presence of CALR mutation. A meta-analysis across independent cohorts and healthy individuals from the 1000 Genomes Project confirmed an inverse correlation between the presentation capabilities of the HLA-I loci for JAK2 V617F and CALRmut-derived peptides in both patients and healthy individuals. scRNA-Seq analysis revealed low expression of TAP1 and CIITA genes in CALRmut+ hematopoietic stem and progenitor cells. In conclusion, the HLA-I genotype differentially restricts JAK2 V617F and CALRmut-driven oncogenesis potentially explaining the mutual exclusivity of the two mutations and differences in their presentation latency. These findings have practical implications for the development of neoantigen-based vaccines in MPNs.

Keywords: CALR; HLA; JAK2 V617F; MPN; immunoediting; mutation; neoantigen.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Alleles
  • Calreticulin* / genetics
  • Carcinogenesis / genetics
  • Female
  • Genotype*
  • Histocompatibility Antigens Class I / genetics
  • Humans
  • Janus Kinase 2* / genetics
  • Male
  • Middle Aged
  • Mutation*
  • Myeloproliferative Disorders* / genetics
  • Myeloproliferative Disorders* / immunology

Substances

  • Janus Kinase 2
  • Calreticulin
  • JAK2 protein, human
  • CALR protein, human
  • Histocompatibility Antigens Class I

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was partly supported by grant NSF (Bulgaria) project KP-06-PN-41/4 (contract KP-06-H41/2, 30.11.2020).