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PMID: 16391141 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression.

Applied and environmental microbiology ·Vol. 72 ·No. 1 ·2006-01-00 ·Pages 946-9

Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Hinton JC, Van Immerseel F

Abstract

Invasion of intestinal epithelial cells by Salmonella enterica is decreased after exposure to butyric acid. To understand the molecular mechanisms of this phenomenon, a comparative transcriptomic analysis of Salmonella enterica serovar Enteritidis and Salmonella enterica serovar Typhimurium grown in medium supplemented with butyrate was performed. We found that butyrate down-regulated the expression of 19 genes common to both serovars by a factor of twofold or more, and 17 of these genes localized to the Salmonella pathogenicity island 1 (SPI1). These included the SPI1 regulatory genes hilD and invF. Of the remaining two genes, ampH has 91% homology to an Escherichia coli penicillin-binding protein and sopE2 encodes a type III-secreted effector protein associated with invasion but located at a separate site on the chromosome from SPI1.

MeSH Terms
Animals Bacterial Proteins/genetics,metabolism Butyrates/pharmacology Culture Media Down-Regulation Gene Expression Regulation, Bacterial HeLa Cells Humans Oligonucleotide Array Sequence Analysis Salmonella enteritidis/genetics,growth & development,metabolism Salmonella typhimurium/genetics,growth & development,metabolism
Chemicals
Bacterial Proteins Butyrates Culture Media Spi1 protein, Salmonella
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Gantois I
Department of Pathology, Bacteriology and Avian Diseases, Research Group Veterinary Public Health and Zoonoses, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B-9820 Merelbeke, Belgium. inne.gantois@UGent.be
Ducatelle R
Pasmans F
Haesebrouck F
Hautefort I
Thompson A
Hinton J C
Van Immerseel F
References (35)
35 references, click to expand
  1. The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes.
    Mol Microbiol. 2000 Feb;35(4):949-60 PMID: 10692170
  2. Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP).
    Cell Death Differ. 1999 Aug;6(8):729-35 PMID: 10467346
  3. Identification and characterization of mutants with increased expression of hilA, the invasion gene transcriptional activator of Salmonella typhimurium.
    FEMS Immunol Med Microbiol. 2000 May;28(1):25-35 PMID: 10767604
  4. The cis requirements for transcriptional activation by HilA, a virulence determinant encoded on SPI-1.
    Mol Microbiol. 2000 Jul;37(2):300-15 PMID: 10931326
  5. Roles of hilC and hilD in regulation of hilA expression in Salmonella enterica serovar Typhimurium.
    J Bacteriol. 2001 May;183(9):2733-45 PMID: 11292791
  6. AraC/XylS family members, HilC and HilD, directly bind and derepress the Salmonella typhimurium hilA promoter.
    Mol Microbiol. 2001 Jun;40(6):1289-99 PMID: 11442828
  7. The HilA box and sequences outside it determine the magnitude of HilA-dependent activation of P(prgH) from Salmonella pathogenicity island 1.
    J Bacteriol. 2001 Aug;183(16):4876-85 PMID: 11466291
  8. Hha is a negative modulator of transcription of hilA, the Salmonella enterica serovar Typhimurium invasion gene transcriptional activator.
    J Bacteriol. 2001 Nov;183(22):6620-9 PMID: 11673432
  9. Salmonella entry into host cells: the work in concert of type III secreted effector proteins.
    Microbes Infect. 2001 Nov-Dec;3(14-15):1293-8 PMID: 11755417
  10. Design issues for cDNA microarray experiments.
    Nat Rev Genet. 2002 Aug;3(8):579-88 PMID: 12154381
  11. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA.
    Mol Microbiol. 2002 Dec;46(5):1451-64 PMID: 12453229
  12. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica.
    Mol Microbiol. 2003 Jan;47(1):103-18 PMID: 12492857
  13. The small nucleoid-binding proteins H-NS, HU, and Fis affect hilA expression in Salmonella enterica serovar Typhimurium.
    Infect Immun. 2003 Sep;71(9):5432-5 PMID: 12933899
  14. Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells.
    Appl Environ Microbiol. 2003 Dec;69(12):7480-91 PMID: 14660401
  15. Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella enteritidis in young chickens.
    Poult Sci. 2004 Jan;83(1):69-74 PMID: 14761086
  16. Medium-chain fatty acids decrease colonization and invasion through hilA suppression shortly after infection of chickens with Salmonella enterica serovar Enteritidis.
    Appl Environ Microbiol. 2004 Jun;70(6):3582-7 PMID: 15184160
  17. Interactions of butyric acid- and acetic acid-treated Salmonella with chicken primary cecal epithelial cells in vitro.
    Avian Dis. 2004 Apr-Jun;48(2):384-91 PMID: 15283426
  18. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines.
    Nature. 1981 May 21;291(5812):238-9 PMID: 7015147
  19. Short chain fatty acids in human large intestine, portal, hepatic and venous blood.
    Gut. 1987 Oct;28(10):1221-7 PMID: 3678950
  20. A review of human salmonellosis: III. Magnitude of Salmonella infection in the United States.
    Rev Infect Dis. 1988 Jan-Feb;10(1):111-24 PMID: 2832925
  21. Treatment of diversion colitis with short-chain-fatty acid irrigation.
    N Engl J Med. 1989 Jan 5;320(1):23-8 PMID: 2909876
  22. Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling.
    Infect Immun. 1990 Jun;58(6):1879-85 PMID: 2160435
  23. Butyrate increases colonocyte protein synthesis in ulcerative colitis.
    J Surg Res. 1994 Jul;57(1):210-4 PMID: 8041140
  24. The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins.
    Mol Microbiol. 1994 Aug;13(4):555-68 PMID: 7997169
  25. Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium.
    Infect Immun. 1996 Sep;64(9):3524-31 PMID: 8751894
  26. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes.
    Mol Microbiol. 1995 Nov;18(4):715-27 PMID: 8817493
  27. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression.
    Mol Microbiol. 1996 Nov;22(4):703-14 PMID: 8951817
  28. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches.
    Mol Microbiol. 1997 May;24(4):697-709 PMID: 9194698
  29. Pathogenesis of Salmonella enteritidis phage type four after experimental infection of young chickens.
    Vet Microbiol. 1997 May;56(1-2):99-109 PMID: 9228686
  30. A HilA-independent pathway to Salmonella typhimurium invasion gene transcription.
    J Bacteriol. 1999 May;181(10):3096-104 PMID: 10322010
  31. Two AraC/XylS family members can independently counteract the effect of repressing sequences upstream of the hilA promoter.
    Mol Microbiol. 1999 May;32(3):629-42 PMID: 10320584
  32. Characterization of SprA, an AraC-like transcriptional regulator encoded within the Salmonella typhimurium pathogenicity island 1.
    Mol Microbiol. 1999 Jul;33(1):139-52 PMID: 10411731
  33. Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and hilA.
    Infect Immun. 1999 Aug;67(8):4099-105 PMID: 10417179
  34. InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in Salmonella typhimurium.
    J Bacteriol. 1999 Aug;181(16):4949-54 PMID: 10438766
  35. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar typhimurium.
    J Bacteriol. 2000 Apr;182(7):1872-82 PMID: 10714991
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
DOI
10.1128/AEM.72.1.946-949.2006
Email
inne.gantois@ugent.be
Published
2006-01-00
Pages
946-9
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC1352287
Subset
IM
External Links
PubMed source DOI: 10.1128/AEM.72.1.946-949.2006 PMC Full Text View journal details
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