Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity

Reactive sulfur species (RSS) like hydrogen sulfide (H<sub>2</sub>S) and cysteine persulfide (Cys-SSH) emerged as key signaling molecules with diverse physiological roles in the body, depending on their concentration and the cellular environment. While it is known that H<sub>2</...

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Main Authors: Jun Ye, Talal Salti, Eva Zanditenas, Meirav Trebicz-Geffen, Moran Benhar, Serge Ankri
Format: Article
Language:English
Published: MDPI AG 2024-02-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/13/2/245
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author Jun Ye
Talal Salti
Eva Zanditenas
Meirav Trebicz-Geffen
Moran Benhar
Serge Ankri
author_facet Jun Ye
Talal Salti
Eva Zanditenas
Meirav Trebicz-Geffen
Moran Benhar
Serge Ankri
author_sort Jun Ye
collection DOAJ
description Reactive sulfur species (RSS) like hydrogen sulfide (H<sub>2</sub>S) and cysteine persulfide (Cys-SSH) emerged as key signaling molecules with diverse physiological roles in the body, depending on their concentration and the cellular environment. While it is known that H<sub>2</sub>S and Cys-SSH are produced by both colonocytes and by the gut microbiota through sulfur metabolism, it remains unknown how these RSS affect amebiasis caused by <i>Entamoeba histolytica</i>, a parasitic protozoan that can be present in the human gastrointestinal tract. This study investigates H<sub>2</sub>S and Cys-SSH’s impact on <i>E. histolytica</i> physiology and explores potential therapeutic implications. Exposing trophozoites to the H<sub>2</sub>S donor, sodium sulfide (Na<sub>2</sub>S), or to Cys-SSH led to rapid cytotoxicity. A proteomic analysis of Cys-SSH-challenged trophozoites resulted in the identification of >500 S-sulfurated proteins, which are involved in diverse cellular processes. Functional assessments revealed inhibited protein synthesis, altered cytoskeletal dynamics, and reduced motility in trophozoites treated with Cys-SSH. Notably, cysteine proteases (CPs) were significantly inhibited by S-sulfuration, affecting their bacterial biofilm degradation capacity. Immunofluorescence microscopy confirmed alterations in actin dynamics, corroborating the proteomic findings. Thus, our study reveals how RSS perturbs critical cellular functions in <i>E. histolytica</i>, potentially influencing its pathogenicity and interactions within the gut microbiota. Understanding these molecular mechanisms offers novel insights into amebiasis pathogenesis and unveils potential therapeutic avenues targeting RSS-mediated modifications in parasitic infections.
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spelling doaj.art-e0f1e4ca6c574ed499e7d821807598de2024-02-23T15:05:36ZengMDPI AGAntioxidants2076-39212024-02-0113224510.3390/antiox13020245Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation CapacityJun Ye0Talal Salti1Eva Zanditenas2Meirav Trebicz-Geffen3Moran Benhar4Serge Ankri5Department of Molecular Microbiology, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelDepartment of Biochemistry, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelDepartment of Molecular Microbiology, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelDepartment of Molecular Microbiology, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelDepartment of Biochemistry, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelDepartment of Molecular Microbiology, Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 3525433, IsraelReactive sulfur species (RSS) like hydrogen sulfide (H<sub>2</sub>S) and cysteine persulfide (Cys-SSH) emerged as key signaling molecules with diverse physiological roles in the body, depending on their concentration and the cellular environment. While it is known that H<sub>2</sub>S and Cys-SSH are produced by both colonocytes and by the gut microbiota through sulfur metabolism, it remains unknown how these RSS affect amebiasis caused by <i>Entamoeba histolytica</i>, a parasitic protozoan that can be present in the human gastrointestinal tract. This study investigates H<sub>2</sub>S and Cys-SSH’s impact on <i>E. histolytica</i> physiology and explores potential therapeutic implications. Exposing trophozoites to the H<sub>2</sub>S donor, sodium sulfide (Na<sub>2</sub>S), or to Cys-SSH led to rapid cytotoxicity. A proteomic analysis of Cys-SSH-challenged trophozoites resulted in the identification of >500 S-sulfurated proteins, which are involved in diverse cellular processes. Functional assessments revealed inhibited protein synthesis, altered cytoskeletal dynamics, and reduced motility in trophozoites treated with Cys-SSH. Notably, cysteine proteases (CPs) were significantly inhibited by S-sulfuration, affecting their bacterial biofilm degradation capacity. Immunofluorescence microscopy confirmed alterations in actin dynamics, corroborating the proteomic findings. Thus, our study reveals how RSS perturbs critical cellular functions in <i>E. histolytica</i>, potentially influencing its pathogenicity and interactions within the gut microbiota. Understanding these molecular mechanisms offers novel insights into amebiasis pathogenesis and unveils potential therapeutic avenues targeting RSS-mediated modifications in parasitic infections.https://www.mdpi.com/2076-3921/13/2/245reactive sulfur specieshydrogen sulfidecysteine persulfideS-sulfuration<i>Entamoeba histolytica</i>
spellingShingle Jun Ye
Talal Salti
Eva Zanditenas
Meirav Trebicz-Geffen
Moran Benhar
Serge Ankri
Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
Antioxidants
reactive sulfur species
hydrogen sulfide
cysteine persulfide
S-sulfuration
<i>Entamoeba histolytica</i>
title Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
title_full Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
title_fullStr Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
title_full_unstemmed Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
title_short Impact of Reactive Sulfur Species on <i>Entamoeba histolytica</i>: Modulating Viability, Motility, and Biofilm Degradation Capacity
title_sort impact of reactive sulfur species on i entamoeba histolytica i modulating viability motility and biofilm degradation capacity
topic reactive sulfur species
hydrogen sulfide
cysteine persulfide
S-sulfuration
<i>Entamoeba histolytica</i>
url https://www.mdpi.com/2076-3921/13/2/245
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