Epstein-Barr virus and immune status imprint the immunogenomics of non-Hodgkin lymphomas occurring in immune-suppressed environments

Haematologica. 2024 Nov 1;109(11):3615-3630. doi: 10.3324/haematol.2023.284332.

Abstract

Non-Hodgkin lymphomas (NHL) commonly occur in immunodeficient patients, both those infected by human immunodeficiency virus (HIV) and those who have been transplanted, and are often driven by Epstein-Barr virus (EBV) with cerebral localization, raising the question of tumor immunogenicity, a critical issue for treatment responses. We investigated the immunogenomics of 68 lymphoproliferative disorders from 51 immunodeficient (34 post-transplant, 17 HIV+) and 17 immunocompetent patients. Overall, 72% were large B-cell lymphoma and 25% were primary central nervous system lymphoma, while 40% were EBV+. Tumor whole-exome and RNA sequencing, along with a bioinformatics pipeline allowed analysis of tumor mutational burden, tumor landscape and tumor microenvironment and prediction of tumor neoepitopes. Both tumor mutational burden (2.2 vs. 3.4/Mb, P=0.001) and numbers of neoepitopes (40 vs. 200, P=0.00019) were lower in EBV+ than in EBV- NHL, regardless of the immune status. In contrast both EBV and the immune status influenced the tumor mutational profile, with HNRNPF and STAT3 mutations observed exclusively in EBV+ and immunodeficient NHL, respectively. Peripheral blood T-cell responses against tumor neoepitopes were detected in all EBV- cases but in only half of the EBV+ ones, including responses against IgH-derived MHC-class-II restricted neoepitopes. The tumor microenvironment analysis showed higher CD8 T-cell infiltrates in EBV+ versus EBV- NHL, together with a more tolerogenic profile composed of regulatory T cells, type-M2 macrophages and an increased expression of negative immune-regulators. Our results highlight that the immunogenomics of NHL in patients with immunodeficiency primarily relies on the tumor EBV status, while T-cell recognition of tumor- and IgH-specific neoepitopes is conserved in EBV- patients, offering potential opportunities for future T-cell-based immune therapies.

MeSH terms

  • Adult
  • Aged
  • Epstein-Barr Virus Infections* / complications
  • Epstein-Barr Virus Infections* / genetics
  • Epstein-Barr Virus Infections* / immunology
  • Epstein-Barr Virus Infections* / virology
  • Female
  • Herpesvirus 4, Human* / genetics
  • Herpesvirus 4, Human* / immunology
  • Humans
  • Immunocompromised Host
  • Immunogenetics
  • Lymphoma, Non-Hodgkin* / genetics
  • Lymphoma, Non-Hodgkin* / immunology
  • Lymphoma, Non-Hodgkin* / virology
  • Male
  • Middle Aged
  • Mutation*
  • Tumor Microenvironment* / immunology
  • Young Adult

Grants and funding

Funding: The IDeaTIon project is financially supported by the MSDAvenir endowment fund (grant number DS-2017-0018). This work was in part supported by the grant INCa-DGOS-Inserm_12560 of the SiRIC CURAMUS (Cancer United Research Associating Medicine, University and Society integrated cancer research program), and by the Fondation pour la Recherche Médicale, grant number FDT202106013113 to MB.