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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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-04-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00960-19 |
| _version_ | 1818754503325777920 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T05:24:17Z |
| format | Article |
| id | doaj.art-efd1521897b842b8b4a63f35bdd33339 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-18T05:24:17Z |
| publishDate | 2020-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-efd1521897b842b8b4a63f35bdd333392022-12-21T21:19:34ZengAmerican Society for MicrobiologymSphere2379-50422020-04-015210.1128/mSphere.00960-19Type III Secretion Effector VopQ of <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Modulates Central Carbon Metabolism in Epithelial CellsAnh Quoc Nguyen0Takaaki Shimohata1Sho Hatayama2Aya Tentaku3Junko Kido4Thi Mai Huong Bui5Takashi Uebanso6Kazuaki Mawatari7Akira Takahashi8Department of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Food Microbiology and Molecular Biology, National Institute of Nutrition, Hanoi, VietnamDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanDepartment of Preventive Environment and Nutrition, Institute of Biomedical Sciences, Tokushima University Graduate School, Tokushima, JapanABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00960-19metabolomicshost-pathogen interactionVibrio parahaemolyticusT3SS effector |
| spellingShingle | 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 mSphere metabolomics host-pathogen interaction Vibrio parahaemolyticus T3SS effector |
| 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_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_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_sort | type iii secretion effector vopq of named content content type genus species vibrio parahaemolyticus named content modulates central carbon metabolism in epithelial cells |
| topic | metabolomics host-pathogen interaction Vibrio parahaemolyticus T3SS effector |
| url | https://journals.asm.org/doi/10.1128/mSphere.00960-19 |
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