Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro

Background: Nontyphoidal Salmonella (NTS) outbreaks of invasive diseases are increasing. Whether the genetic diversity of invasive NTS correlates with the clinical characteristics and bacteremia development in NTS infections remains unclear. In this study, we compared the global transcriptomes betwe...

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Main Authors: Buyandelger Batsaikhan, Pei-Chun Lin, Katsumi Shigemura, Yu-Wei Wu, Reo Onishi, Pei-Ru Chang, Hung-Yen Cheng, Shiuh-Bin Fang
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Journal of Microbiology, Immunology and Infection
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Online Access:http://www.sciencedirect.com/science/article/pii/S1684118224001750
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author Buyandelger Batsaikhan
Pei-Chun Lin
Katsumi Shigemura
Yu-Wei Wu
Reo Onishi
Pei-Ru Chang
Hung-Yen Cheng
Shiuh-Bin Fang
author_facet Buyandelger Batsaikhan
Pei-Chun Lin
Katsumi Shigemura
Yu-Wei Wu
Reo Onishi
Pei-Ru Chang
Hung-Yen Cheng
Shiuh-Bin Fang
author_sort Buyandelger Batsaikhan
collection DOAJ
description Background: Nontyphoidal Salmonella (NTS) outbreaks of invasive diseases are increasing. Whether the genetic diversity of invasive NTS correlates with the clinical characteristics and bacteremia development in NTS infections remains unclear. In this study, we compared the global transcriptomes between bacteremic and nonbacteremic NTS strains after their interaction with human intestinal epithelial cells in vitro. Methods: We selected clinical isolates obtained from stool and blood samples of patients with or without bacteremia and patients with high and low C-reactive protein (CRP) levels. The bacterial RNA samples were isolated after coculturing with Caco-2 cells for RNA sequencing and subsequent analyses. Results: CRP is an unreliable predictive maker for NTS bacteremia with a median CRP level of 1.6 mg/dL. Certain Salmonella Pathogenicity Island (SPI)-1 genes (sipC, sipA, sicA, sipD, and sipB), SPI-2 genes (ssaP, ssrA, and ssaS), and six SPI-4 genes (siiA, siiB, siiC, siiD, siiE, and siiF) remained upregulated in the bacteremic blood-derived strains but significantly downregulated in the nonbacteremic strains after their interaction with Caco-2 cells. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways analysis identified that arginine biosynthesis, ascorbate and aldarate metabolism, and phosphotransferase system pathways were activated in bacteremic NTS strains after Caco-2 cell priming. Conclusion: CRP levels were not correlated with bacteremia development. Significant regulation of certain SPI genes in bacteremic NTS strains after Caco-2 cell priming; bacteremia development might be influenced by the host immune response and the extent to which specific metabolism pathways in NTS strains can be prevented from invading the bloodstream.
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spelling doaj-art-0b0689a7d36c4c428019bd1a810d65882025-02-06T05:11:18ZengElsevierJournal of Microbiology, Immunology and Infection1684-11822025-02-015813847Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitroBuyandelger Batsaikhan0Pei-Chun Lin1Katsumi Shigemura2Yu-Wei Wu3Reo Onishi4Pei-Ru Chang5Hung-Yen Cheng6Shiuh-Bin Fang7Division of Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan; Department of Pediatrics, School of Medicine, College of Medicine, Taipei Medical University, Taipei City, TaiwanDivision of Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan; Department of Emergency Medicine, Shuang Ho Hospital, Taipei Medical University, New Taipei City, TaiwanDepartment of Public Health, Division of Infectious Diseases, Kobe University Graduate School of Health Sciences, Kobe, Japan; Department of Urology, Teikyo University School of Medicine, Tokyo, JapanGraduate Institute of Biomedical Informatics, College of Medical Science and Technology, Taipei Medical University, New Taipei City, TaiwanDepartment of Public Health, Division of Infectious Diseases, Kobe University Graduate School of Health Sciences, Kobe, JapanDivision of Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan; Department of Pediatrics, School of Medicine, College of Medicine, Taipei Medical University, Taipei City, TaiwanDivision of Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Shuang Ho Hospital, Taipei Medical University, New Taipei City, TaiwanDivision of Gastroenterology, Hepatology, and Nutrition, Department of Pediatrics, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan; Department of Pediatrics, School of Medicine, College of Medicine, Taipei Medical University, Taipei City, Taiwan; Master Program in Clinical Pharmacogenomics and Pharmacoproteomics, College of Pharmacy, Taipei Medical University, Taipei City, Taiwan; Research Center for Digestive Medicine, Taipei Medical University, Taipei City, Taiwan; Corresponding author. 291, Jhong Jheng Road, Jhong Ho District, New Taipei City, 23561, Taiwan.Background: Nontyphoidal Salmonella (NTS) outbreaks of invasive diseases are increasing. Whether the genetic diversity of invasive NTS correlates with the clinical characteristics and bacteremia development in NTS infections remains unclear. In this study, we compared the global transcriptomes between bacteremic and nonbacteremic NTS strains after their interaction with human intestinal epithelial cells in vitro. Methods: We selected clinical isolates obtained from stool and blood samples of patients with or without bacteremia and patients with high and low C-reactive protein (CRP) levels. The bacterial RNA samples were isolated after coculturing with Caco-2 cells for RNA sequencing and subsequent analyses. Results: CRP is an unreliable predictive maker for NTS bacteremia with a median CRP level of 1.6 mg/dL. Certain Salmonella Pathogenicity Island (SPI)-1 genes (sipC, sipA, sicA, sipD, and sipB), SPI-2 genes (ssaP, ssrA, and ssaS), and six SPI-4 genes (siiA, siiB, siiC, siiD, siiE, and siiF) remained upregulated in the bacteremic blood-derived strains but significantly downregulated in the nonbacteremic strains after their interaction with Caco-2 cells. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways analysis identified that arginine biosynthesis, ascorbate and aldarate metabolism, and phosphotransferase system pathways were activated in bacteremic NTS strains after Caco-2 cell priming. Conclusion: CRP levels were not correlated with bacteremia development. Significant regulation of certain SPI genes in bacteremic NTS strains after Caco-2 cell priming; bacteremia development might be influenced by the host immune response and the extent to which specific metabolism pathways in NTS strains can be prevented from invading the bloodstream.http://www.sciencedirect.com/science/article/pii/S1684118224001750RNA sequencingGlobal transcriptomeNontyphoidal SalmonellaBacteremiaC-reactive protein
spellingShingle Buyandelger Batsaikhan
Pei-Chun Lin
Katsumi Shigemura
Yu-Wei Wu
Reo Onishi
Pei-Ru Chang
Hung-Yen Cheng
Shiuh-Bin Fang
Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
Journal of Microbiology, Immunology and Infection
RNA sequencing
Global transcriptome
Nontyphoidal Salmonella
Bacteremia
C-reactive protein
title Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
title_full Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
title_fullStr Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
title_full_unstemmed Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
title_short Comparison of global transcriptomes for nontyphoidal Salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
title_sort comparison of global transcriptomes for nontyphoidal salmonella clinical isolates from pediatric patients with and without bacteremia after their interaction with human intestinal epithelial cells in vitro
topic RNA sequencing
Global transcriptome
Nontyphoidal Salmonella
Bacteremia
C-reactive protein
url http://www.sciencedirect.com/science/article/pii/S1684118224001750
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