Active dissemination of cellular antigens by DCs facilitates CD8+ T-cell priming in lymph nodes

Eur J Immunol. 2017 Oct;47(10):1802-1818. doi: 10.1002/eji.201747042.

Abstract

Antigen (Ag) specific activation of naïve T cells by migrating dendritic cells (DCs) is a highly efficient process, although the chances for their colocalization in lymph nodes (LNs) appear low. Ag presentation may be delegated from Ag-donor DCs to the abundant resident DCs, but the routes of Ag transfer and how it facilitates T-cell activation remain unclear. We visualized CD8+ T cell-DC interactions to study the sites, routes, and cells mediating Ag transfer in mice. In vitro, Ag transfer from isolated ovalbumin (OVA)+ bone marrow (BM) DCs triggered widespread arrest, Ca2+ flux, and CD69 upregulation in OT-I T cells contacting recipient DCs. Intravital two-photon imaging revealed that survival of Ag-donor DCs in LNs was required for Ag dissemination among resident CD11c+ DCs. Upon interaction with recipient DCs, CD8+ T cells clustered, upregulated CD69, proliferated and differentiated into effectors. Few DCs sufficed for activation, and for efficient Ag dissemination lymphocyte function associated antigen 1 (LFA-1) expression on recipient DCs was essential. Similar findings characterized DCs infected with a replication-deficient OVA-expressing Vaccinia virus known to downregulate MHC-I. Overall, active Ag dissemination from live incoming DCs helped activate CD8+ T cells by increasing the number of effective presenting cells and salvaged T-cell priming when Ag-donor DCs could not present Ag.

Keywords: Antigen presentation; CD8+ T cells; Cell migration; Dendritic cells; In vivo imaging; T-cell activation; Vaccinia virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigen Presentation
  • Antigens / immunology
  • Antigens / metabolism*
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • Antigens, Differentiation, T-Lymphocyte / genetics
  • Antigens, Differentiation, T-Lymphocyte / immunology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Movement
  • Cross-Priming*
  • Dendritic Cells / chemistry
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Intravital Microscopy
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology
  • Lymph Nodes / cytology
  • Lymph Nodes / immunology*
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Ovalbumin / genetics
  • Ovalbumin / immunology
  • Vaccinia virus / genetics
  • Vaccinia virus / physiology

Substances

  • Antigens
  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD69 antigen
  • Lectins, C-Type
  • Ovalbumin