γδ T cell-mediated activation of cDC1 orchestrates CD4+ Th1 cell priming in malaria

Front Immunol. 2024 Aug 15:15:1426316. doi: 10.3389/fimmu.2024.1426316. eCollection 2024.

Abstract

γδ T cells facilitate the CD4+ T helper 1 (Th1) cell response against Plasmodium infection by activating conventional dendritic cells (cDCs), although the underlying mechanism remains elusive. Our study revealed that γδ T cells promote the complete maturation and production of interleukin-12 and CXCR3-ligands specifically in type 1 cDCs (cDC1), with minimal impact on cDC2 and monocyte derived DCs (Mo-DCs). During the initial infection phase, γδ T cell activation and temporal accumulation in the splenic white pulp, alongside cDC1, occur via CCR7-signaling. Furthermore, cDC1/γδ T cell interactions in the white pulp are amplified through CXCR3 signaling in γδ T cells, optimizing Th1 cell priming by cDC1. We also demonstrated how transitional Th1 cells arise in the white pulp before establishing their presence in the red pulp as fully differentiated Th1 cells. Additionally, we elucidate the reciprocal activation between γδ T cells and cDC1s. These findings suggest that Th1 cell priming is orchestrated by this reciprocal activation in the splenic white pulp during the early phase of blood-stage Plasmodium infection.

Keywords: Plasmodium; Th1 cell response; blood-stage infection; cDC1; malaria; spleen; γδ T cells.

MeSH terms

  • Animals
  • Cell Differentiation / immunology
  • Dendritic Cells* / immunology
  • Dendritic Cells* / metabolism
  • Female
  • Lymphocyte Activation* / immunology
  • Malaria* / immunology
  • Malaria* / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Antigen, T-Cell, gamma-delta / immunology
  • Receptors, Antigen, T-Cell, gamma-delta / metabolism
  • Receptors, CCR7 / immunology
  • Receptors, CCR7 / metabolism
  • Receptors, CXCR3 / metabolism
  • Signal Transduction
  • Spleen / immunology
  • Th1 Cells* / immunology

Substances

  • Receptors, CXCR3
  • Receptors, Antigen, T-Cell, gamma-delta
  • Receptors, CCR7
  • Cxcr3 protein, mouse
  • Ccr7 protein, mouse

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. S-II was supported by funding from the Heiwa Nakajima Foundation, Takeda Science Foundation, Bilateral Joint Research Projects of JSPS (JPJSBP1-120197730), and JSPS KAKENHI (Grant-in-Aid for Scientific Research (C): 22K07042 and 18K07094).