Contact dependent and cytokine mediated signals from CD1c+(BDCA1+) mDC are central to the appropriate activation of naive CD4 and CD8 T cells during infection. In acute falciparum and vivax malaria, CD1c+mDC decline, but it remains to be determined whether CD1c+mDC that remain circulating in the peripheral blood are functional.
We investigated CD1c+mDC absolute counts, maturation and cytokine production in a first experimental P. falciparum infection in healthy volunteers and in adult patients with acute uncomplicated P. falciparum or P. knowlesi malaria from Sabah, Malaysia. CD1c+mDC decreased from day 7 post experimental infection and were significantly reduced in acute malaria compared to ethnicity matched healthy controls. In patients with acute P. knowlesi malaria, CD1c+mDC DC counts remained significantly reduced 7 days after anti-malarial treatment and recovered only 2-4 weeks following treatment. CD1c+mDC loss was partially explained by apoptosis, determined by intracellular staining of cleaved caspase 3. In experimental P. falciparum infection, only a minority of CD1c+mDC were activated, with only 13% (IQR: 9.4-13.3%) expressing the co-stimulatory molecule CD86, and the majority having downregulated HLA-DR expression, suggesting reduced ability to present antigen. This was paralleled by reduced uptake of particulate antigen. In acute malaria, neither HLA-DR or CD86 were up-regulated. In experimental infection, intracellular cytokine staining of CD1c+mDC in whole blood showed increased TNF secretion but no increase in IL-12 secretion.
Our data demonstrate impaired antigen-uptake and presentation ability of circulating CD1c+mDC. These cells appear functionally compromised in acute falciparum and knowlesi malaria. The increased production of TNF by CD1c+mDC in experimental infection indicates these cells can directly contribute to Plasmodium pro-inflammatory immune responses. Overall, we conclude that CD1c+mDC are functionally and numerically compromised in malaria with impairment persisting at least one week after parasite clearance.