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Loss of immune control over opportunistic infections can occur at different stages of HIV-1 (HIV) disease, among which mucosal candidiasis caused by the fungal pathogen  Candida albicans (C .  albicans)  is one of the early and common manifestations in HIV-infected human subjects. The underlying immunological basis is not well defined. We have previously shown that compared to cytomegalovirus (CMV)-specific CD4 cells,  C .  albicans-specific  CD4 T cells are highly permissive to HIV  in vitro . Here, based on an antiretroviral treatment (ART) naïve HIV infection cohort (RV21), we investigated longitudinally the impact of HIV on  C .  albicans - and CMV-specific CD4 T-cell immunity  in vivo . We found a sequential dysfunction and preferential depletion for  C .  albicans- specific CD4 T cell response during progressive HIV infection. Compared to Th1 (IFN-γ, MIP-1β) functional subsets, the Th17 functional subsets (IL-17, IL-22) of  C .  albicans- specific CD4 T cells were more permissive to HIV  in vitro  and impaired earlier in HIV-infected subjects. Infection history analysis showed that  C .  albicans- specific CD4 T cells were more susceptible to HIV  in vivo , harboring modestly but significantly higher levels of HIV DNA, than CMV-specific CD4 T cells. Longitudinal analysis of HIV-infected individuals with ongoing CD4 depletion demonstrated that  C .  albicans- specific CD4 T-cell response was preferentially and progressively depleted. Taken together, these data suggest a potential mechanism for earlier loss of immune control over mucosal candidiasis in HIV-infected patients and provide new insights into pathogen-specific immune failure in AIDS pathogenesis.

Sequential Dysfunction and Progressive Depletion of Candida albicans-Specific CD4 T Cell Response in HIV-1 Infection