Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics

Salmonella enterica serovar Typhimurium (S. Typhimurium) is a food-borne bacterium that causes acute gastroenteritis in humans and typhoid fever in mice. Salmonella pathogenicity island II (SPI-2) is an important virulence gene cluster responsible for Salmonella survival and replication within host...

Full description

Saved in:
Bibliographic Details
Main Authors: Yuanyuan Wang, Chunmei Wu, Jiacong Gao, Xudong Du, Xiangyun Chen, Mei Zhang
Format: Article
Language:English
Published: Taylor & Francis Group 2021-01-01
Series:Emerging Microbes and Infections
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2021.1974316
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849322547412205568
author Yuanyuan Wang
Chunmei Wu
Jiacong Gao
Xudong Du
Xiangyun Chen
Mei Zhang
author_facet Yuanyuan Wang
Chunmei Wu
Jiacong Gao
Xudong Du
Xiangyun Chen
Mei Zhang
author_sort Yuanyuan Wang
collection DOAJ
description Salmonella enterica serovar Typhimurium (S. Typhimurium) is a food-borne bacterium that causes acute gastroenteritis in humans and typhoid fever in mice. Salmonella pathogenicity island II (SPI-2) is an important virulence gene cluster responsible for Salmonella survival and replication within host cells, leading to systemic infection. Previous studies have suggested that SPI-2 function to modulate host vesicle trafficking and immune response to promote systemic infection. However, the molecular mechanism and the host responses triggered by SPI-2 remain largely unknown. To assess the roles of SPI-2, we used a differential proteomic approach to analyse host proteins levels during systemic infections in mice. Our results showed that infection by WT S. Typhimurium triggered the reprogramming of host cell metabolism and inflammatory response. Salmonella systemic infection induces an up-regulation of glycolytic process and a repression of the tricarboxylic acid (TCA) cycle. WT-infected tissues prefer to produce adenosine 5′-triphosphate (ATP) through aerobic glycolysis rather than relying on oxidative phosphorylation to generate energy. Moreover, our data also revealed that infected macrophages may undergo both M1 and M2 polarization. In addition, our results further suggest that SPI-2 is involved in altering actin cytoskeleton to facilitate the Salmonella-containing vacuole (SCV) biogenesis and perhaps even the release of bacteria later in the infection process. Results from our study provide valuable insights into the roles of SPI-2 during systemic Salmonella infection and will guide future studies to dissect the molecular mechanisms of how SPI-2 functions in vivo.
format Article
id doaj-art-c46db9c065fc47fea18d06f77d25e3f6
institution Kabale University
issn 2222-1751
language English
publishDate 2021-01-01
publisher Taylor & Francis Group
record_format Article
series Emerging Microbes and Infections
spelling doaj-art-c46db9c065fc47fea18d06f77d25e3f62025-08-20T03:49:21ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512021-01-011011849186110.1080/22221751.2021.1974316Host metabolic shift during systemic Salmonella infection revealed by comparative proteomicsYuanyuan Wang0Chunmei Wu1Jiacong Gao2Xudong Du3Xiangyun Chen4Mei Zhang5TEDA School of Biological Sciences and Biotechnology, Nankai University, Tianjin, People’s Republic of ChinaSchool of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing, People’s Republic of ChinaTEDA School of Biological Sciences and Biotechnology, Nankai University, Tianjin, People’s Republic of ChinaTEDA School of Biological Sciences and Biotechnology, Nankai University, Tianjin, People’s Republic of ChinaTEDA School of Biological Sciences and Biotechnology, Nankai University, Tianjin, People’s Republic of ChinaSchool of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing, People’s Republic of ChinaSalmonella enterica serovar Typhimurium (S. Typhimurium) is a food-borne bacterium that causes acute gastroenteritis in humans and typhoid fever in mice. Salmonella pathogenicity island II (SPI-2) is an important virulence gene cluster responsible for Salmonella survival and replication within host cells, leading to systemic infection. Previous studies have suggested that SPI-2 function to modulate host vesicle trafficking and immune response to promote systemic infection. However, the molecular mechanism and the host responses triggered by SPI-2 remain largely unknown. To assess the roles of SPI-2, we used a differential proteomic approach to analyse host proteins levels during systemic infections in mice. Our results showed that infection by WT S. Typhimurium triggered the reprogramming of host cell metabolism and inflammatory response. Salmonella systemic infection induces an up-regulation of glycolytic process and a repression of the tricarboxylic acid (TCA) cycle. WT-infected tissues prefer to produce adenosine 5′-triphosphate (ATP) through aerobic glycolysis rather than relying on oxidative phosphorylation to generate energy. Moreover, our data also revealed that infected macrophages may undergo both M1 and M2 polarization. In addition, our results further suggest that SPI-2 is involved in altering actin cytoskeleton to facilitate the Salmonella-containing vacuole (SCV) biogenesis and perhaps even the release of bacteria later in the infection process. Results from our study provide valuable insights into the roles of SPI-2 during systemic Salmonella infection and will guide future studies to dissect the molecular mechanisms of how SPI-2 functions in vivo.https://www.tandfonline.com/doi/10.1080/22221751.2021.1974316Salmonella Typhimuriummouse infection modelsystemic infectionSPI-2comparative proteomics
spellingShingle Yuanyuan Wang
Chunmei Wu
Jiacong Gao
Xudong Du
Xiangyun Chen
Mei Zhang
Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
Emerging Microbes and Infections
Salmonella Typhimurium
mouse infection model
systemic infection
SPI-2
comparative proteomics
title Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
title_full Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
title_fullStr Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
title_full_unstemmed Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
title_short Host metabolic shift during systemic Salmonella infection revealed by comparative proteomics
title_sort host metabolic shift during systemic salmonella infection revealed by comparative proteomics
topic Salmonella Typhimurium
mouse infection model
systemic infection
SPI-2
comparative proteomics
url https://www.tandfonline.com/doi/10.1080/22221751.2021.1974316
work_keys_str_mv AT yuanyuanwang hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics
AT chunmeiwu hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics
AT jiaconggao hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics
AT xudongdu hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics
AT xiangyunchen hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics
AT meizhang hostmetabolicshiftduringsystemicsalmonellainfectionrevealedbycomparativeproteomics