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A Streptococcus aquaporin acts as peroxiporin for efflux of cellular hydrogen peroxide and alleviation of oxidative stress.

ABSTRACT: Aquaporins (AQPs) are transmembrane proteins widely distributed in various organisms, and they facilitate bidirectional diffusion of water and uncharged solutes. The catalase-negative bacterium Streptococcus oligofermentans produces the highest H₂O₂ levels reported to date, which has to be exported to avoid oxidative stress. Here, we report that a S. oligofermentans aquaporin functions as a peroxiporin facilitating bidirectional transmembrane H₂O₂ transport. Knockout of this aquaporin homolog, So-AqpA, reduced H₂O₂ export by ?50% and increased endogenous H₂O₂ retention, as indicated by the cellular H₂O₂ reporter HyPer. Heterologous expression of So-aqpA accelerated exogenous H₂O₂ influx into Saccharomyces cerevisiae and Escherichia coli cells, indicating that So-AqpA acts as an H₂O₂-transferring aquaporin. Alanine substitution revealed Phe-40 as a key residue for So-AqpA-mediated H₂O₂ transport. Northern blotting, qPCR, and luciferase reporter assays disclosed that H₂O₂ induces a >10-fold expression of So-aqpA Super-resolution imaging showed that H₂O₂ treatment increases So-AqpA protein molecules per cell by 1.6- to 3-fold. Inactivation of two redox-regulatory transcriptional repressors, PerR and MntR, reduced H₂O₂-induced So-aqpA expression to 1.8- and 4-fold, respectively. Electrophoretic mobility shift assays determined that MntR, but not PerR, binds to the So-aqpA promoter, indicating that MntR directly regulates H₂O₂-induced So-aqpA expression. Importantly, So-aqpA deletion decreased oxic growth and intraspecies competition and diminished the competitive advantages of S. oligofermentans over the caries pathogen Streptococcus mutans Of note, So-aqpA orthologs with the functionally important Phe-40 are present in all streptococci. Our work has uncovered an intrinsic, H₂O₂-inducible bacterial peroxiporin that has a key physiological role in H₂O₂ detoxification in S. oligofermentans.

SUBMITTER: Tong H

PROVIDER: S-EPMC6433050 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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A Streptococcus aquaporin acts as peroxiporin for efflux of cellular hydrogen peroxide and alleviation of oxidative stress.

Tong Huichun H Wang Xinhui X Dong Yuzhu Y Hu Qingqing Q Zhao Ziyi Z Zhu Yun Y Dong Linxuan L Bai Fan F Dong Xiuzhu X

The Journal of biological chemistry 20190131 12

Aquaporins (AQPs) are transmembrane proteins widely distributed in various organisms, and they facilitate bidirectional diffusion of water and uncharged solutes. The catalase-negative bacterium Streptococcus oligofermentans produces the highest H2O2 levels reported to date, which has to be exported to avoid oxidative stress. Here, we report that a S. oligofermentans aquaporin functions as a peroxiporin facilitating bidirectional transmembrane H2O<su ...[more]

PMID: 30705089

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Project description:Aquaporin-8 (AQP8), a member of the aquaporin family, is strongly expressed in follicular granulosa cells, which could affect the hormone secretion level in females. AQP8, as a membrane protein, could mediate H2O2 into cells, thereby triggering various biological events. The deficiency of Aqp8 increases female fertility, resulting from the decrease in follicular atresia. The low cell death rate is related to the apoptosis of granulosa cells. However, the mechanism by which AQP8 regulates the autophagy of granulosa cells remains unclear. Thus, this study aimed to explore the effect of AQP8 on autophagy in follicular atresia. We found that the expression of the autophagy marker light-chain protein 3 was significantly downregulated in the granulosa cells of Aqp8-knockout (Aqp8 -/- ) mice, compared with wild-type (Aqp8 +/+ ) mice. Immunofluorescence staining and transmission electron microscopic examination indicated that the number of autophagosomes in the granulosa cells of Aqp8 -/- mice decreased. Using a follicular granulosa cell autophagy model, namely a follicular atresia model, we verified that the concentration of H2O2 significantly increased during the autophagy of granulosa cells, consistent with the Aqp8 mRNA level. Intracellular H2O2 accumulation was modulated by endogenous AQP8 expression level, indicating that AQP8-mediated H2O2 was involved in the autophagy of granulosa cells. AQP8 deficiency impaired the elevation of H2O2 concentration through phosphorylated tyrosine activation. In addition, we carried out the analysis of transcriptome sequencing datasets in the ovary and found there were obvious differences in principal components, differentially expressed genes (DEGs) and KEGG pathways, which might be involved in AQP8-regulated follicular atresia. Taken together, these findings indicated that AQP8-mediated H2O2 transport could mediate the autophagy of granulosa cells. AQP8 might be a potential target for diseases related to ovarian insufficiency.

Dataset Information

A Streptococcus aquaporin acts as peroxiporin for efflux of cellular hydrogen peroxide and alleviation of oxidative stress.

Publications

A <i>Streptococcu</i>s aquaporin acts as peroxiporin for efflux of cellular hydrogen peroxide and alleviation of oxidative stress.

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