Cross-presentation by dendritic cells (DC) is a
process in which extracellular antigen is shunted into the MHC I presentation
pathway and presented to CD8+ T cells. Due to the lack of an
appropriate lineage marker, murine cross-presenting DC were to date defined by
the expression of the co-receptor CD8 in the spleen and the integrin CD103 in
the periphery. In humans, the scarcity of DC and in
particular the very low frequency of CD141+ (BDCA-3) DC in the peripheral
blood, impeded their functional characterization and complicated their comparison
to primary murine DC subsets.
Using
a newly generated monoclonal antibody specific for the chemokine receptor XCR1,
we determined that 80% of CD8+ DC and 5% of CD8- DC in
the spleen uniquely express XCR1 on their surface. These XCR1+ DC
efficiently take up cellular material and excel in antigen cross-presentation,
independent of their CD8 expression. In lymph nodes and peripheral tissues,
XCR1+ DC largely, but not fully, correspond to CD103+ DC.
Furthermore, we demonstrate that XCR1+ DC in the spleen, lymph
nodes, and peripheral tissues are dependent on the growth factor Flt3 ligand
and are selectively absent in animals deficient for the transcription factors Batf3 and Irf-8. Therefore, XCR1 emerges as the first highly specific surface
marker of cross-presenting Batf3- and
Irf-8-dependent
DC in the mouse. Crucial for the translation of mouse models to the human, we additionally
demonstrate that XCR1 is specifically expressed on human primary CD141+
DC. This DC subset, similar to murine XCR1+ DC, excels in cross-presentation
of soluble and cell-associated antigens. Hence, the expression of XCR1 demarcates
a subset of human and mouse DC that are functional homologues. At the same
time, XCR1 emerges as a highly attractive structure for targeting of antigen and
induction of CD8 T cell cytotoxic
immunity in prophylactic or therapeutic vaccines.