Enterococcus faecalis (E. faecalis), long implicated in serious systemic infections and failure of root canal treatment, is a persistent inhabitant of oral periapical lesions. Dendritic cells (DCs) and other innate immune cells patrol the oral mucosa for infecting microbes. Dendritic cells are efficient at capturing microbes when immature, whereupon they can transform into potent antigen-presenting cells upon full maturation. Autophagy, a sophisticated intracellular process first described for elimination of damaged organelles, regulates DC maturation and other important immune functions of DCs. The present study examined how E. faecalis influences differentiation of murine bone marrow-derived stem cells (BMSCs) into functional DCs in the presence of the cytokines GM-CSF/IL4. Although the viability and differentiation of DCs were not affected by E. faecalis, expression of the autophagy-related proteins ATG7, Beclin1, and LC3bI/II were significantly suppressed in an mTOR-dependent manner. Ultrastructurally, E. faecalis were identified in single-membrane vacuoles, some of were in the process of binary fission. Bacteria-containing autophagosomes were absent within the cytoplasm. Accessory molecules (MHCII, CD80, CD86) and anti-inflammatory cytokine (TGFβ1) were suppressed in E. faecalis-induced DCs, while IL1β, TNFα and IL12 levels were upregulated. When pulsed with OVA, the E. faecalis-induced DCs showed reduction in CD4+ OVA-specific OTII T cells proliferation. It is concluded that E. faecalis promotes differentiation of bone marrow stem cells into CD11c-positive DCs with aberrant-immune functions while retaining the capability of pro-inflammatory cytokine induction.