Impact of bacterial vaginosis, as assessed by nugent criteria and hormonal status on glycosidases and lectin binding in cervicovaginal lavage samples.

Bernard J Moncla,Lara K Mahal,Catherine A Chappell,Brian M Debo,Sharon L Hillier,Leslie A Meyn,David N Fredricks

doi:10.1371/journal.pone.0127091

Abstract

The objective of this study was to evaluate the impact of hormonal status and bacterial vaginosis (BV) on the glycosidases present and glycosylation changes as assessed by lectin binding to cervicovaginal lavage constituents. Frozen cervicovaginal lavage samples from a completed study examining the impact of reproductive hormones on the physicochemical properties of vaginal fluid were utilized for the present study. In the parent study, 165 women were characterized as having BV, intermediate or normal microflora using the Nugent criteria. The presence of glycosidases in the samples was determined using quantitative 4-methyl-umbelliferone based assays, and glycosylation was assessed using enzyme linked lectin assays (ELLA). Women with BV had elevated sialidase, α-galactosidase, β-galactosidase and α-glucosidase activities compared to intermediate or normal women (P<0.001, 0.003, 0.006 and 0.042 respectively). The amount of sialic acid (Sambucus nigra, P = 0.003) and high mannose (griffithsin, P<0.001) were reduced, as evaluated by lectin binding, in women with BV. When the data were stratified according to hormonal status, α-glucosidase and griffithsin binding were decreased among postmenopausal women (P<0.02) when compared to premenopausal groups. These data suggest that both hormonal status and BV impact the glycosidases and lectin binding sites present in vaginal fluid. The sialidases present at increased levels in women with BV likely reduce the number of sialic acid binding sites. Other enzymes likely reduce griffithsin binding. The alterations in the glycosidase content, high mannose and sialic acid binding sites in the cervicovaginal fluid associated with bacterial vaginosis may impact susceptibility to viruses, such as HIV, that utilize glycans as a portal of entry.

Highlights

Secreted cervical mucus coats the vaginal and cervical epithelium forming a protective biochemical and physical barrier to infection
Microorganisms recovered from the vagina of women having Bacterial vaginosis (BV) produce a range of glycosidases, including sialidase, and the presence of these microorganisms is associated with decreased vaginal fluid viscosity and increased symptoms of vaginal discharge [11, 12]; to date, no one has quantified the glycosidases in cervicovaginal lavage (CVL) components and concurrently evaluated changes in lectin binding
We demonstrate that in women with BV, there is an increase in four glycosidases, suggesting that these are correlated with a change in the bacterial flora

Summary

Introduction

Secreted cervical mucus coats the vaginal and cervical epithelium forming a protective biochemical and physical barrier to infection. The mucus is composed of mucins, glycoproteins and other secreted proteins, including antibodies, antibacterial proteins and peptides. Bacterial vaginosis (BV) is a common vaginal syndrome in which lactobacilli are replaced by a diverse community of anaerobic and facultative microorganisms [8,9,10]. Microorganisms recovered from the vagina of women having BV produce a range of glycosidases, including sialidase, and the presence of these microorganisms is associated with decreased vaginal fluid viscosity and increased symptoms of vaginal discharge [11, 12]; to date, no one has quantified the glycosidases in cervicovaginal lavage (CVL) components and concurrently evaluated changes in lectin binding

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