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Targeting inflammation for the prevention of human immunodeficiency virus (HIV) transmission and disease progression
Dissertation   Open access

Targeting inflammation for the prevention of human immunodeficiency virus (HIV) transmission and disease progression

Joseph A. Fraietta
Doctor of Philosophy (Ph.D.), Drexel University
Feb 2012
DOI:
https://doi.org/10.17918/00000727
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Abstract

Microbiology
In HIV-1 infections, innate immune signaling results in the generation of pro-inflammatory cytokines that play an important role in determining the course of disease. However, aberrant cytokine production mediates pathological effects by increasing virus dissemination and facilitating the dysfunction/death of T lymphocytes. We have undertaken investigations to examine the effects of inhibiting immunoinflammatory signaling in the context of HIV-1 transmission and chronic disease. Initially, we determined whether suppressing inflammation and simultaneously inhibiting viral infectivity would mediate protection against HIV-1 infection. This led to the development of PDB oligomers as dual-acting microbicides that inhibit HIV-1 infection and also dampen inflammation. PDB compounds were potent anti-inflammatory agents through their TLR7/9-specific antagonistic properties. In addition, as anti-HIV inhibitors, PDBs prevented reverse transcription. Importantly, intravaginal application of PDB delayed mucosal acquisition of SHIV in rhesus macaques. These data suggest that PDB-based compounds may be promising microbicide candidates for clinical development. A pro-inflammatory cytokine environment during chronic HIV-1 infection favors a hyperimmune activation state that leads to T cell exhaustion and depletion. Because type I IFN production distinguishes pathogenic and non-pathogenic AIDS virus infections, we examined how IFN[alpha]/[beta] can prime T cells in HIV-1 infection to undergo apoptosis. The mitochondrial death mediator Bak was increased in patients and correlated positively with sensitivity to CD95/Fas-mediated T cell apoptosis and negatively with CD4+ T cell counts. Importantly, IFN[alpha]/[beta] increased Bak expression and CD95/Fas-induced apoptosis in T cells from healthy donors. IFN[alpha]/[beta] further primed T cells, including HIV-specific CD8+ T cells from patients to CD95/Fas-mediated death. HIV-1 exposure sensitized T cells to CD95/Fas-induced apoptosis, which was IFN[alpha]/[beta]-dependent. In HIV-1-infected patients, an IFN[alpha]-stimulated gene signature correlated positively with ex vivo Bak levels and CD95/Fas-mediated apoptosis, but negatively with CD4+ T cell counts. Plasma IFN[alpha] was also inversely correlated with CD4+ T cell counts in chronic SIV infection. Finally, in SIV-infected rhesus macaques, plasma IFN[alpha] and viral loads correlated negatively during acute infection suggesting an antiviral effect, but positively during chronic infection indicating that virus may drive type I IFN. Therefore, type I IFN generated during chronic HIV-1 infection may contribute to the loss of T cells and disease progression.

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