Abstract
Understanding factors that affect heterosexual transmission of HIV in women is of great importance. Lactobacilli in the lower genital tract of women utilize glycogen in vaginal epithelial cells as an energy source and produce lactic acid. The resultant vaginal acidity is believed to provide protection against HIV infection. Conversely, bacterial vaginosis (BV) is characterized by less lactic acid and a higher pH, and is associated with increased susceptibility to HIV infection. Because vaginal infection of macaques with simian immunodeficiency virus (SIV) or simian-human immunodeficiency virus (SHIV) is used as a model to study HIV sexual transmission, and because previous studies have shown a paucity of lactobacilli in rhesus macaques' lower genital tract, we compared lactic acid and glycogen levels in the genital fluid of rhesus and pigtail macaques with levels found in humans. The levels of lactic acid were lower in both rhesus (median=1.2 mol lactate/mg protein) and pigtail macaques (median=0.7 mol/mg) compared to women with healthy genital microbiota (median=4.2 mol/mg). Glycogen levels were significantly lower in both rhesus (median=0.004 μg glycogen/μg protein) and pigtail macaques (median=0 μg/μg) than in women (median=0.2 μg/μg). No significant differences in glycogen or lactate levels were observed comparing longitudinally collected samples from cycling pigtail macaques. These data show that the previously reported scarcity of lactobacilli in macaques correlates with low glycogen and lactic acid levels. These findings have important implications for studies of vaginal infection of macaques with SIV or SHIV and further our understanding of how the bacterial microbiota influences HIV infection.
Highlights
Bacterial vaginosis (BV), a common condition in women in which the lower genital tract bacterial microbiota is altered, is associated with increased susceptibility to infection with herpes simplex virus (HSV)-1, HSV-2, human papillomavirus (HPV), and HIV when compared to women with microbiota dominated by lactobacilli.[1,2,3,4]
While the explanation for this increased susceptibility to infection in BV is not well understood, it is widely believed that the acidic environment of the vagina in women colonized by lactobacilli contributes to the protection against infection by pathogens, including HIV
As previously reported,[10] only 2 out of the 11 rhesus monkeys, housed at the Tulane facility and whose microbiota were analyzed by pyrosequencing, were colonized with lactobacilli. These two monkeys had increased levels of lactate:protein; one had 11% lactobacilli and a lactate:protein of 2.7 mol/mg, while the other had 39% lactobacilli and a lactate:protein of 2.3 mol/mg, compared to their cohort’s median of 1.2 mol/mg. These data show that the reported scarcity of lactobacilli observed in the macaques[10] is associated with relatively low levels of lactic acid when compared to women without BV
Summary
Bacterial vaginosis (BV), a common condition in women in which the lower genital tract bacterial microbiota is altered, is associated with increased susceptibility to infection with herpes simplex virus (HSV)-1, HSV-2, human papillomavirus (HPV), and HIV when compared to women with microbiota dominated by lactobacilli.[1,2,3,4] While the explanation for this increased susceptibility to infection in BV is not well understood, it is widely believed that the acidic environment of the vagina in women colonized by lactobacilli contributes to the protection against infection by pathogens, including HIV. While a healthy vagina is characterized as having a pH of less than 4.5, BV is marked by its relatively high pH (pH > 4.5).[5,6,7,8] Lactobacilli contribute primarily to vaginal acidity by producing high levels of lactic acid.[7,8] Glycogen, produced by vaginal epithelial cells, is used by vaginal bacteria, such as lactobacilli, as an energy source during anaerobic metabolism.[6,7,8,9] The synthesis of this large branched glucose polymer is influenced by the menstrual cycle in women, and is believed to be made and deposited in vaginal epithelia during times when estrogen levels are the highest.[6,7,8]
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