Regulation of monocarboxylate transporter 1 (MCT1) promoter by butyrate in human intestinal epithelial cells: involvement of NF-kappaB pathway

J Cell Biochem. 2008 Apr 1;103(5):1452-63. doi: 10.1002/jcb.21532.

Abstract

Butyrate, a short chain fatty acid (SCFA) produced by bacterial fermentation of undigested carbohydrates in the colon, constitutes the major fuel for colonocytes. We have earlier shown the role of apically localized monocarboxylate transporter isoform 1 (MCT1) in transport of butyrate into human colonic Caco-2 cells. In an effort to study the regulation of MCT1 gene, we and others have cloned the promoter region of the MCT1 gene and identified cis elements for key transcription factors. A previous study has shown up-regulation of MCT1 expression, and activity by butyrate in AA/C1 human colonic epithelial cells, however, the detailed mechanisms of this up-regulation are not known. In this study, we demonstrate that butyrate, a substrate for MCT1, stimulates MCT1 promoter activity in Caco-2 cells. This effect was dose dependent and specific to butyrate as other predominant SCFAs, acetate, and propionate, were ineffective. Utilizing progressive deletion constructs of the MCT1 promoter, we showed that the putative butyrate responsive elements are in the -229/+91 region of the promoter. Butyrate stimulation of the MCT1 promoter was found to be independent of PKC, PKA, and tyrosine kinases. However, specific inhibitors of the NF-kappaB pathway, lactacystein (LC), and caffeic acid phenyl ester (CAPE) significantly reduced the MCT1 promoter stimulation by butyrate. Also, butyrate directly stimulated NF-kappaB-dependent luciferase reporter activity. Histone deacetylase (HDAC) inhibitor trichostatin A (TSA) also stimulated MCT1 promoter activity, however, unlike butyrate, this stimulation was unaltered by the NF-kappaB inhibitors. Further, the combined effect of butyrate, and TSA on MCT1 promoter activity was additive, indicating that their mechanisms of action were independent. Our results demonstrate the involvement of NF-kappaB pathway in the regulation of MCT1 promoter activity by butyrate.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Butyrates / metabolism*
  • Butyrates / pharmacology
  • Caco-2 Cells
  • Caffeic Acids / pharmacology
  • Carrier Proteins / biosynthesis*
  • Carrier Proteins / genetics
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Humans
  • Intestinal Mucosa / metabolism*
  • Monocarboxylic Acid Transporters / biosynthesis*
  • Monocarboxylic Acid Transporters / genetics
  • NF-kappa B / genetics
  • NF-kappa B / metabolism*
  • Phenylethyl Alcohol / analogs & derivatives
  • Protein Kinase C / metabolism
  • Response Elements / physiology*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Substrate Specificity / physiology
  • Symporters / biosynthesis*
  • Symporters / genetics

Substances

  • Butyrates
  • Caffeic Acids
  • Carrier Proteins
  • Monocarboxylic Acid Transporters
  • NF-kappa B
  • Symporters
  • monocarboxylate transport protein 1
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C
  • caffeic acid phenethyl ester
  • Phenylethyl Alcohol