Sodium-coupled transport of the short chain fatty acid butyrate by SLC5A8 and its relevance to colon cancer

J Gastrointest Surg. 2008 Oct;12(10):1773-81; discussion 1781-2. doi: 10.1007/s11605-008-0573-0. Epub 2008 Jul 26.

Abstract

Introduction: SLC5A8, expressed predominantly in the colon, is a Na(+)-coupled transporter for short-chain fatty acids. In this paper, we report on the characterization of butyrate transport by SLC5A8 and the relevance of SLC5A8-mediated butyrate transport to colon cancer.

Results: SLC5A8 transports butyrate via a Na(+)-dependent electrogenic process. Na(+) activation of the transport process exhibits sigmoidal kinetics, indicating involvement of more than one Na(+) in the activation process. SLC5A8 is silenced in colon cancer in humans, in a mouse model of intestinal/colon cancer, and in colon cancer cell lines. The tumor-associated silencing of SLC5A8 involves DNA methylation by DNA methyltransferase 1. Reexpression of SLC5A8 in colon cancer cells leads to apoptosis but only in the presence of butyrate. SLC5A8-mediated entry of butyrate into cancer cells is associated with inhibition of histone deacetylation. The changes in gene expression in SLC5A8/butyrate-induced apoptosis include upregulation of pro-apoptotic genes and downregulation of anti-apoptotic genes. In addition, the expression of phosphatidylinositol-3-kinase subunits is affected differentially, with downregulation of p85alpha and upregulation of p55alpha and p50alpha.

Conclusion: These studies show that SLC5A8 mediates the tumor-suppressive effects of the bacterial fermentation product butyrate in the colon.

MeSH terms

  • Animals
  • Biological Transport, Active
  • Butyrates / metabolism*
  • Cation Transport Proteins / genetics*
  • Cell Line, Tumor
  • Cells, Cultured
  • Colonic Neoplasms / genetics*
  • Humans
  • Mice
  • Monocarboxylic Acid Transporters
  • Sodium / metabolism

Substances

  • Butyrates
  • Cation Transport Proteins
  • Monocarboxylic Acid Transporters
  • SLC5A8 protein, human
  • Sodium