Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells

ABSTRACT Vibrio parahaemolyticus is a Gram-negative halophilic pathogen that frequently causes acute gastroenteritis and occasional wound infection. V. parahaemolyticus contains several virulence factors, including type III secretion systems (T3SSs) and thermostable direct hemolysin (TDH). In partic...

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Autores principales:	Anh Quoc Nguyen, Takaaki Shimohata, Sho Hatayama, Aya Tentaku, Junko Kido, Thi Mai Huong Bui, Takashi Uebanso, Kazuaki Mawatari, Akira Takahashi
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	metabolomics host-pathogen interaction Vibrio parahaemolyticus T3SS effector Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/efd1521897b842b8b4a63f35bdd33339
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spelling	oai:doaj.org-article:efd1521897b842b8b4a63f35bdd333392021-11-15T15:29:17ZType III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells10.1128/mSphere.00960-192379-5042https://doaj.org/article/efd1521897b842b8b4a63f35bdd333392020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00960-19https://doaj.org/toc/2379-5042ABSTRACT Vibrio parahaemolyticus is a Gram-negative halophilic pathogen that frequently causes acute gastroenteritis and occasional wound infection. V. parahaemolyticus contains several virulence factors, including type III secretion systems (T3SSs) and thermostable direct hemolysin (TDH). In particular, T3SS1 is a potent cytotoxic inducer, and T3SS2 is essential for causing acute gastroenteritis. Although much is known about manipulation of host signaling transductions by the V. parahaemolyticus effector, little is known about the host metabolomic changes modulated by V. parahaemolyticus. To address this knowledge gap, we performed a metabolomic analysis of the epithelial cells during V. parahaemolyticus infection using capillary electrophoresis-time of flight mass spectrometry (CE-TOF/MS). Our results revealed significant metabolomic perturbations upon V. parahaemolyticus infection. Moreover, we identified that T3SS1’s VopQ effector was responsible for inducing the significant metabolic changes in the infected cells. The VopQ effector dramatically altered the host cell’s glycolytic, tricarboxylic acid cycle (TCA), and amino acid metabolisms. VopQ effector disrupted host cell redox homeostasis by depleting cellular glutathione and subsequently increasing the level of reactive oxygen species (ROS) production. IMPORTANCE The metabolic response of host cells upon infection is pathogen specific, and infection-induced host metabolic reprogramming may have beneficial effects on the proliferation of pathogens. V. parahaemolyticus contains a range of virulence factors to manipulate host signaling pathways and metabolic processes. In this study, we identified that the T3SS1 VopQ effector rewrites host metabolism in conjunction with the inflammation and cell death processes. Understanding how VopQ reprograms host cell metabolism during the infection could help us to identify novel therapeutic strategies to enhance the survival of host cells during V. parahaemolyticus infection.Anh Quoc NguyenTakaaki ShimohataSho HatayamaAya TentakuJunko KidoThi Mai Huong BuiTakashi UebansoKazuaki MawatariAkira TakahashiAmerican Society for Microbiologyarticlemetabolomicshost-pathogen interactionVibrio parahaemolyticusT3SS effectorMicrobiologyQR1-502ENmSphere, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	metabolomics host-pathogen interaction Vibrio parahaemolyticus T3SS effector Microbiology QR1-502
spellingShingle	metabolomics host-pathogen interaction Vibrio parahaemolyticus T3SS effector Microbiology QR1-502 Anh Quoc Nguyen Takaaki Shimohata Sho Hatayama Aya Tentaku Junko Kido Thi Mai Huong Bui Takashi Uebanso Kazuaki Mawatari Akira Takahashi Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
description	ABSTRACT Vibrio parahaemolyticus is a Gram-negative halophilic pathogen that frequently causes acute gastroenteritis and occasional wound infection. V. parahaemolyticus contains several virulence factors, including type III secretion systems (T3SSs) and thermostable direct hemolysin (TDH). In particular, T3SS1 is a potent cytotoxic inducer, and T3SS2 is essential for causing acute gastroenteritis. Although much is known about manipulation of host signaling transductions by the V. parahaemolyticus effector, little is known about the host metabolomic changes modulated by V. parahaemolyticus. To address this knowledge gap, we performed a metabolomic analysis of the epithelial cells during V. parahaemolyticus infection using capillary electrophoresis-time of flight mass spectrometry (CE-TOF/MS). Our results revealed significant metabolomic perturbations upon V. parahaemolyticus infection. Moreover, we identified that T3SS1’s VopQ effector was responsible for inducing the significant metabolic changes in the infected cells. The VopQ effector dramatically altered the host cell’s glycolytic, tricarboxylic acid cycle (TCA), and amino acid metabolisms. VopQ effector disrupted host cell redox homeostasis by depleting cellular glutathione and subsequently increasing the level of reactive oxygen species (ROS) production. IMPORTANCE The metabolic response of host cells upon infection is pathogen specific, and infection-induced host metabolic reprogramming may have beneficial effects on the proliferation of pathogens. V. parahaemolyticus contains a range of virulence factors to manipulate host signaling pathways and metabolic processes. In this study, we identified that the T3SS1 VopQ effector rewrites host metabolism in conjunction with the inflammation and cell death processes. Understanding how VopQ reprograms host cell metabolism during the infection could help us to identify novel therapeutic strategies to enhance the survival of host cells during V. parahaemolyticus infection.
format	article
author	Anh Quoc Nguyen Takaaki Shimohata Sho Hatayama Aya Tentaku Junko Kido Thi Mai Huong Bui Takashi Uebanso Kazuaki Mawatari Akira Takahashi
author_facet	Anh Quoc Nguyen Takaaki Shimohata Sho Hatayama Aya Tentaku Junko Kido Thi Mai Huong Bui Takashi Uebanso Kazuaki Mawatari Akira Takahashi
author_sort	Anh Quoc Nguyen
title	Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
title_short	Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
title_full	Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
title_fullStr	Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
title_full_unstemmed	Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells
title_sort	type iii secretion effector vopq of <named-content content-type="genus-species">vibrio parahaemolyticus</named-content> modulates central carbon metabolism in epithelial cells
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/efd1521897b842b8b4a63f35bdd33339
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Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial Cells

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