Salmonella Infection Induces a Hypersecretory Phenotype in Human Intestinal Xenografts by Inducing Cyclooxygenase 2

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Published inInfection and Immunity Vol. 71; no. 4; pp. 2102 - 2109
Main Authors BERTELSEN, Lone S, PAESOLD, Guenther, ECKMANN, Lars, BARRETT, Kim E
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.04.2003
Subjects
Animals
Biological and medical sciences
Calcium - metabolism
Carbachol - metabolism
Cyclooxygenase 2
Dinoprostone - metabolism
Epithelial Cells - microbiology
Fundamental and applied biological sciences. Psychology
Host Response and Inflammation
Humans
Indomethacin - pharmacology
Intestines - cytology
Intestines - embryology
Intestines - microbiology
Intestines - transplantation
Ion Transport
Isoenzymes - antagonists & inhibitors
Isoenzymes - metabolism
Membrane Proteins
Mice
Mice, SCID
Microbiology
Prostaglandin-Endoperoxide Synthases - metabolism
Salmonella Infections - microbiology
Salmonella Infections - physiopathology
Salmonella typhimurium - enzymology
Salmonella typhimurium - pathogenicity
Transplantation, Heterologous
Up-Regulation
Microbiology
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AbstractList Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since species differences limit the utility of animal tissues and cell lines lack relevant cell-cell interactions, we have used a human model of fetal intestine grown as xenografts in SCID mice. We investigated here the effects of Salmonella enterica serovar Typhimurium SL1344 on xenograft ion transport. Harvested xenografts were stripped of seromuscular layers by blunt dissection, infected with Salmonella, and mounted in Ussing chambers. Salmonella infection for 1 h increased baseline ion transport without altering tissue conductance or morphology. The increased transport was blocked by the cyclooxygenase inhibitor, indomethacin, or the specific Cox-2 inhibitor, NS-398. Further, xenografts infected for 2 h showed increased secretory responses to the calcium-dependent agonist, carbachol, and the cyclic AMP- dependent agonists prostaglandin E sub(2) (PGE sub(2)) and forskolin, which were blocked by indomethacin. Western blot experiments revealed that infection was accompanied by increased cyclooxygenase 2 (Cox-2) expression, with no change in Cox-1 levels. Immunoassay demonstrated basolateral PGE sub(2) release, which was inhibited by indomethacin. Histological examination of infected xenografts illustrated that upregulated Cox-2 expression was restricted to the epithelium and that little or no invasion of the tissue by Salmonella occurred for up to 2 h. In summary, Salmonella infection rapidly increases Cox-2 expression in human intestinal tissue, accounting for increased epithelial ion transport characteristic of infectious diarrhea.
ABSTRACT Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since species differences limit the utility of animal tissues and cell lines lack relevant cell-cell interactions, we have used a human model of fetal intestine grown as xenografts in SCID mice. We investigated here the effects of Salmonella enterica serovar Typhimurium SL1344 on xenograft ion transport. Harvested xenografts were stripped of seromuscular layers by blunt dissection, infected with Salmonella , and mounted in Ussing chambers. Salmonella infection for 1 h increased baseline ion transport without altering tissue conductance or morphology. The increased transport was blocked by the cyclooxygenase inhibitor, indomethacin, or the specific Cox-2 inhibitor, NS-398. Further, xenografts infected for 2 h showed increased secretory responses to the calcium-dependent agonist, carbachol, and the cyclic AMP-dependent agonists prostaglandin E 2 (PGE 2 ) and forskolin, which were blocked by indomethacin. Western blot experiments revealed that infection was accompanied by increased cyclooxygenase 2 (Cox-2) expression, with no change in Cox-1 levels. Immunoassay demonstrated basolateral PGE 2 release, which was inhibited by indomethacin. Histological examination of infected xenografts illustrated that upregulated Cox-2 expression was restricted to the epithelium and that little or no invasion of the tissue by Salmonella occurred for up to 2 h. In summary, Salmonella infection rapidly increases Cox-2 expression in human intestinal tissue, accounting for increased epithelial ion transport characteristic of infectious diarrhea.
Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since species differences limit the utility of animal tissues and cell lines lack relevant cell-cell interactions, we have used a human model of fetal intestine grown as xenografts in SCID mice. We investigated here the effects of Salmonella enterica serovar Typhimurium SL1344 on xenograft ion transport. Harvested xenografts were stripped of seromuscular layers by blunt dissection, infected with Salmonella , and mounted in Ussing chambers. Salmonella infection for 1 h increased baseline ion transport without altering tissue conductance or morphology. The increased transport was blocked by the cyclooxygenase inhibitor, indomethacin, or the specific Cox-2 inhibitor, NS-398. Further, xenografts infected for 2 h showed increased secretory responses to the calcium-dependent agonist, carbachol, and the cyclic AMP-dependent agonists prostaglandin E 2 (PGE 2 ) and forskolin, which were blocked by indomethacin. Western blot experiments revealed that infection was accompanied by increased cyclooxygenase 2 (Cox-2) expression, with no change in Cox-1 levels. Immunoassay demonstrated basolateral PGE 2 release, which was inhibited by indomethacin. Histological examination of infected xenografts illustrated that upregulated Cox-2 expression was restricted to the epithelium and that little or no invasion of the tissue by Salmonella occurred for up to 2 h. In summary, Salmonella infection rapidly increases Cox-2 expression in human intestinal tissue, accounting for increased epithelial ion transport characteristic of infectious diarrhea.
Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since species differences limit the utility of animal tissues and cell lines lack relevant cell-cell interactions, we have used a human model of fetal intestine grown as xenografts in SCID mice. We investigated here the effects of Salmonella enterica serovar Typhimurium SL1344 on xenograft ion transport. Harvested xenografts were stripped of seromuscular layers by blunt dissection, infected with Salmonella, and mounted in Ussing chambers. Salmonella infection for 1 h increased baseline ion transport without altering tissue conductance or morphology. The increased transport was blocked by the cyclooxygenase inhibitor, indomethacin, or the specific Cox-2 inhibitor, NS-398. Further, xenografts infected for 2 h showed increased secretory responses to the calcium-dependent agonist, carbachol, and the cyclic AMP-dependent agonists prostaglandin E(2) (PGE(2)) and forskolin, which were blocked by indomethacin. Western blot experiments revealed that infection was accompanied by increased cyclooxygenase 2 (Cox-2) expression, with no change in Cox-1 levels. Immunoassay demonstrated basolateral PGE(2) release, which was inhibited by indomethacin. Histological examination of infected xenografts illustrated that upregulated Cox-2 expression was restricted to the epithelium and that little or no invasion of the tissue by Salmonella occurred for up to 2 h. In summary, Salmonella infection rapidly increases Cox-2 expression in human intestinal tissue, accounting for increased epithelial ion transport characteristic of infectious diarrhea.
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Author Kim E. Barrett
Lone S. Bertelsen
Lars Eckmann
Guenther Paesold
AuthorAffiliation Division of Gastroenterology, Department of Medicine, UCSD School of Medicine, San Diego, California 92103-8414
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Corresponding author. Mailing address: Division of Gastroenterology, UCSD Medical Center, 8414, 200 W. Arbor Dr., San Diego, CA 92103-8414. Phone: (619) 543-3726. Fax: (619) 543-6969. E-mail: kbarrett@ucsd.edu.
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Snippet Classifications Services IAI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit...
Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since...
ABSTRACT Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial...
Enteric Salmonella infection is accompanied by inflammation and diarrhea, and yet little is known about its effects on intestinal epithelial physiology. Since...
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StartPage 2102
SubjectTerms Animals
Biological and medical sciences
Calcium - metabolism
Carbachol - metabolism
Cyclooxygenase 2
Dinoprostone - metabolism
Epithelial Cells - microbiology
Fundamental and applied biological sciences. Psychology
Host Response and Inflammation
Humans
Indomethacin - pharmacology
Intestines - cytology
Intestines - embryology
Intestines - microbiology
Intestines - transplantation
Ion Transport
Isoenzymes - antagonists & inhibitors
Isoenzymes - metabolism
Membrane Proteins
Mice
Mice, SCID
Microbiology
Prostaglandin-Endoperoxide Synthases - metabolism
Salmonella Infections - microbiology
Salmonella Infections - physiopathology
Salmonella typhimurium - enzymology
Salmonella typhimurium - pathogenicity
Transplantation, Heterologous
Up-Regulation
Title Salmonella Infection Induces a Hypersecretory Phenotype in Human Intestinal Xenografts by Inducing Cyclooxygenase 2
URI http://iai.asm.org/content/71/4/2102.abstract
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