Peculiar transcriptional reprogramming with functional impairment of dendritic cells upon exposure to transformed HTLV-1-infected cells

PLoS Pathog. 2024 Sep 16;20(9):e1012555. doi: 10.1371/journal.ppat.1012555. eCollection 2024 Sep.

Abstract

Manipulation of immune cell functions, independently of direct infection of these cells, emerges as a key process in viral pathophysiology. Chronic infection by Human T-cell Leukemia Virus type 1 (HTLV-1) is associated with immune dysfunctions, including misdirected responses of dendritic cells (DCs). Here, we interrogate the ability of transformed HTLV-1-infected T cells to manipulate human DC functions. We show that exposure to transformed HTLV-1-infected T cells induces a biased and peculiar transcriptional signature in monocyte-derived DCs, associated with an inefficient maturation and a poor responsiveness to subsequent stimulation by a TLR4 agonist. This poor responsiveness is also associated with a unique transcriptional landscape characterized by a set of genes whose expression is either conferred, impaired or abolished by HTLV-1 pre-exposure. Induction of this functional impairment requires several hours of coculture with transformed HTLV-1-infected cells, and associated mechanisms driven by viral capture, cell-cell contacts, and soluble mediators. Altogether, this cross-talk between infected T cells and DCs illustrate how HTLV-1 might co-opt communications between cells to induce a unique local tolerogenic immune microenvironment suitable for its own persistence.

MeSH terms

  • Cellular Reprogramming
  • Dendritic Cells* / immunology
  • Dendritic Cells* / metabolism
  • Dendritic Cells* / virology
  • HTLV-I Infections* / genetics
  • HTLV-I Infections* / immunology
  • HTLV-I Infections* / virology
  • Human T-lymphotropic virus 1* / immunology
  • Humans
  • T-Lymphocytes / immunology
  • T-Lymphocytes / virology

Grants and funding

This study was supported by the Fondation pour la Recherche Médicale, DEQ. 20180339200, and by the Agence Nationale de la Recherche (ANR) to HD, ANR-22-CE15-0044. AC and CJ are employees of ENS de Lyon. CM is employee of CNRS. HD, FM and SA are employees of INSERM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.