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Experimental physiology2014; 99(10); 1335-1347; doi: 10.1113/expphysiol.2014.077982

Characterization of butyrate transport across the luminal membranes of equine large intestine.

Abstract: The diet of the horse, pasture forage (grass), is fermented by the equine colonic microbiota to short-chain fatty acids, notably acetate, propionate and butyrate. Short-chain fatty acids provide a major source of energy for the horse and contribute to many vital physiological processes. We aimed to determine both the mechanism of butyrate uptake across the luminal membrane of equine colon and the nature of the protein involved. To this end, we isolated equine colonic luminal membrane vesicles. The abundance and activity of cysteine-sensitive alkaline phosphatase and villin, intestinal luminal membrane markers, were significantly enriched in membrane vesicles compared with the original homogenates. In contrast, the abundance of GLUT2 protein and the activity of Na(+)-K(+)-ATPase, known markers of the intestinal basolateral membrane, were hardly detectable. We demonstrated, by immunohistochemistry, that monocarboxylate transporter 1 (MCT1) protein is expressed on the luminal membrane of equine colonocytes. We showed that butyrate transport into luminal membrane vesicles is energized by a pH gradient (out < in) and is not Na(+) dependent. Moreover, butyrate uptake is time and concentration dependent, with a Michaelis-Menten constant of 5.6 ± 0.45 mm and maximal velocity of 614 ± 55 pmol s(-1) (mg protein)(-1). Butyrate transport is significantly inhibited by p-chloromercuribenzoate, phloretin and α-cyano-4-hydroxycinnamic acid, all potent inhibitors of MCT1. Moreover, acetate and propionate, as well as the monocarboxylates pyruvate and lactate, also inhibit butyrate uptake. Data presented here support the conclusion that transport of butyrate across the equine colonic luminal membrane is predominantly accomplished by MCT1.
© 2014 The Authors. Experimental Physiology © 2014 The Physiological Society.
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Publication Date: 2014-08-28 PubMed ID: 25172888DOI: 10.1113/expphysiol.2014.077982Google Scholar: Lookup
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  • Journal Article
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  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The researchers isolated membranes from horse colon cells to understand how butyrate, a short-chain fatty acid produced by gut bacteria during the fermentation of grass, is transported into the cells. They have identified that the protein monocarboxylate transporter 1 (MCT1) predominantly facilitates butyrate transport across the cellular membrane.

Background

  • The study was motivated by the importance of the dietary intake of horses, primarily grass, which is fermented by the microbes in horse’s large intestine to produce short-chain fatty acids. These fatty acids, particularly butyrate, not only provide a major energy source for horses, but also participate in many crucial physiological processes.
  • In this context, understanding the mechanism and transport of butyrate into the cells across the luminal membrane (the inner layer of the intestine exposed to the gut contents) is of significant interest.

Experimental Approach

  • They began by isolating luminal membrane vesicles from horse colonic cells. These vesicles are essentially ‘bladders’ of cell membrane that allow testing of transport processes in isolation.
  • The researchers then analysed these vesicles for different proteins including intestinal luminal membrane markers (Cysteine-sensitive alkaline phosphatase and villin), a glucose transporter (GLUT2) and a pump protein (Na(+)-K(+)-ATPase). These investigations confirmed that the vesicles represent the luminal membrane.
  • Furthermore, the researchers used immunohistochemistry to show that the MCT1 protein is present on the luminal membrane of the cells in the horse colon (colonocytes).

Results and Interpretation

  • The research team showed that butyrate transport is driven by a pH gradient and is not dependent on sodium (Na+). It is also time and concentration dependent, with specific kinetics that are indicative of a particular transport mechanism.
  • Butyrate transport into the vesicles was significantly blocked by p-chloromercuribenzoate, phloretin and α-cyano-4-hydroxycinnamic acid – all known inhibitors of MCT1. This suggests that MCT1 facilitates the transport of butyrate.
  • Transport was also inhibited by other short-chain fatty acids and monocarboxylates (compounds with one carboxylate group), further supporting the involvement of MCT1, known to transport these substances.
  • All these findings strongly suggest that butyrate is mainly transported across the equine colonic luminal membrane via the MCT1 protein.

Cite This Article

APA
Nedjadi T, Moran AW, Al-Rammahi MA, Shirazi-Beechey SP. (2014). Characterization of butyrate transport across the luminal membranes of equine large intestine. Exp Physiol, 99(10), 1335-1347. https://doi.org/10.1113/expphysiol.2014.077982

Publication

Experimental physiology
ISSN: 1469-445X
NlmUniqueID: 9002940
Country: England
Language: English
Volume: 99
Issue: 10
Pages: 1335-1347

Researcher Affiliations

Nedjadi, Taoufik
  • Epithelial Function and Development Group, Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK.
Moran, Andrew W
  • Epithelial Function and Development Group, Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK.
Al-Rammahi, Miran A
  • Epithelial Function and Development Group, Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK.
Shirazi-Beechey, Soraya P
  • Epithelial Function and Development Group, Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK spsb@liverpool.ac.uk.

MeSH Terms

  • Animals
  • Biological Transport
  • Butyrates / pharmacokinetics
  • Cell Membrane / metabolism
  • Colon / drug effects
  • Colon / metabolism
  • Glucose Transporter Type 2 / metabolism
  • Horses
  • Humans
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / metabolism
  • Intestine, Large / drug effects
  • Intestine, Large / metabolism
  • Monocarboxylic Acid Transporters / metabolism
  • Symporters / metabolism

Citations

This article has been cited 18 times.
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