The role of primary subsets of DCs in Mycobacterium tuberculosis infection in humans is incompletely understood. In this study, we identified a CD1c DC subset with phenotype of CD1c⁺CD11c⁺CD19⁻CD11b⁺ that was significantly increased in tuberculous pleural effusions and in peripheral blood from patients with TB compared with that from healthy controls (p < 0.0001). Sputum smear/culture-positive patients with tuberculosis had significantly higher frequency of CD1c⁺CD11b⁺ DC subset than sputum smear/culture-negative patients (p < 0.0001). After effective anti-TB chemotherapy, the frequency of CD1c⁺CD11b⁺ DC subset in peripheral blood and tuberculous pleural effusions was decreased. CD1c⁺CD11b⁺ DC subset from tuberculous pleural effusions expressed higher levels of TLR2, TLR4, CD172a, CD206 and FcεRⅠ, but lower levels of CD80, CD83 and CD86 compared with CD1c⁺CD11b⁻ DC subset. Expression of IL-1β, IL-6, IL-8, IL-23, TNF-α, IFN-γ and TGF-β mRNA in CD1c⁺CD11b⁺ DCs was higher than in CD1c⁺CD11b⁻ DC subset. Co-culture of autologous naive CD4⁺ T cells with sorted CD1c⁺CD11b⁺ DCs expressed significantly increased levels of IL-17A and RORγt transcripts as compared with those co-cultured with CD11b⁻ subset. In conclusion, a CD1c⁺CD11b⁺ DC subset with elevated frequency in patients with tuberculosis was identified and it promoted Th17 cell differentiation.