Abstract
A majority of individuals infected with human immunodeficiency virus (HIV) have inadequate access to antiretroviral therapy and ultimately develop debilitating oral infections that often correlate with disease progression. Due to the impracticalities of conducting host-microbe systems-based studies in HIV infected patients, we have evaluated the potential of simian immunodeficiency virus (SIV) infected rhesus macaques to serve as a non-human primate model for oral manifestations of HIV disease. We present the first description of the rhesus macaque oral microbiota and show that a mixture of human commensal bacteria and “macaque versions” of human commensals colonize the tongue dorsum and dental plaque. Our findings indicate that SIV infection results in chronic activation of antiviral and inflammatory responses in the tongue mucosa that may collectively lead to repression of epithelial development and impact the microbiome. In addition, we show that dysbiosis of the lingual microbiome in SIV infection is characterized by outgrowth of Gemella morbillorum that may result from impaired macrophage function. Finally, we provide evidence that the increased capacity of opportunistic pathogens (e.g. E. coli) to colonize the microbiome is associated with reduced production of antimicrobial peptides.
Highlights
A majority of human immunodeficiency virus (HIV)-infected individuals world-wide do not have adequate access to antiretroviral therapy and experience opportunistic oral infections [1,2,3,4] that are linked to deterioration of immune function [5,6] and severely impact nutritional health [7,8]
Characterization of the rhesus macaque oral microbiota In implementing a systems biology approach to investigate the relationship between simian immunodeficiency virus (SIV) associated oral pathogenesis and hostmicrobe dysbiosis, we first sought to characterize the types of bacterial species that colonize the rhesus macaque oral microbiome
Multiple studies indicate that commensal oral bacteria can escape from their normal niches and cause infective endocarditis, bacteremia, and septicemia [41,42], and may do so at a higher frequency in HIV infected patients compared to healthy subjects
Summary
A majority of HIV-infected individuals world-wide do not have adequate access to antiretroviral therapy and experience opportunistic oral infections [1,2,3,4] that are linked to deterioration of immune function [5,6] and severely impact nutritional health [7,8]. The various types of oral manifestation of HIV disease are likely to be connected to profound yet potentially unrelated perturbations (dysbiosis) of distinct, extremely complex and delicately balanced host-microbe ecosystems. Rhesus macaques infected with simian immunodeficiency virus (SIV) have the potential to circumvent such restrictions, and are already well-established as an animal model for the immunopathologies of HIV disease; displaying CD4+ T cell depletion kinetics [20,21] and mucosal pathologies [22,23] strikingly similar to humans. SIV infected macaques are likely to provide a valuable, yet untapped, resource for investigating mechanisms of oral mucosal immunopathology, host-microbe dysbiosis, and manifestation of secondary infections
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