Acute interactions between intestinal sugar and calcium transport in vitro

Am J Physiol Gastrointest Liver Physiol. 2014 Jan 1;306(1):G1-12. doi: 10.1152/ajpgi.00263.2013. Epub 2013 Oct 31.

Abstract

Fructose consumption by Americans has increased markedly, whereas Ca(2+) intake has decreased below recommended levels. Because fructose metabolism decreases enterocyte ATP concentrations, we tested the hypothesis that luminal fructose acutely reduces active, diet-inducible Ca(2+) transport in the small intestine. We confirmed that the decrease in ATP concentrations was indeed greater in fructose- compared with glucose-incubated mucosal homogenates from wild-type and was prevented in fructose-incubated homogenates from ketohexokinase (KHK)(-/-) mice. We then induced active Ca(2+) transport by chronically feeding wild-type, fructose transporter glucose transporter 5 (GLUT5)(-/-), as well as KHK(-/-) mice a low Ca(2+) diet and measured transepithelial Ca(2+) transport in everted duodenal sacs incubated in solutions containing glucose, fructose, or their nonmetabolizable analogs. The diet-induced increase in active Ca(2+) transport was proportional to dramatic increases in expression of the Ca(2+)-selective channel transient receptor potential vanilloid family calcium channel 6 as well as of the Ca(2+)-binding protein 9k (CaBP9k) but not that of the voltage-dependent L-type channel Ca(v)1.3. Crypt-villus distribution of CaBP9k seems heterogeneous, but low Ca(2+) diets induce expression in more cells. In contrast, KHK distribution is homogeneous, suggesting that fructose metabolism can occur in all enterocytes. Diet-induced Ca(2+) transport was not enhanced by addition of the enterocyte fuel glutamine and was always greater in sacs of wild-type, GLUT5(-/-), and KHK(-/-) mice incubated with fructose or nonmetabolizable sugars than those incubated with glucose. Thus duodenal Ca(2+) transport is not affected by fructose and enterocyte ATP concentrations but instead may decrease with glucose metabolism, as Ca(2+) transport remains high with 3-O-methylglucose that is also transported by sodium-glucose cotransporter 1 but cannot be metabolized.

Keywords: calbindin; fructose; glucose; glucose transporter 5; metabolism; nutrition.

Publication types

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

MeSH terms

  • Animals
  • Biological Transport, Active / physiology*
  • Calcium / metabolism*
  • Calcium Channels, L-Type / metabolism
  • Calcium-Binding Proteins / metabolism
  • Enterocytes / metabolism*
  • Fructokinases / metabolism
  • Fructose / metabolism*
  • Gene Expression Profiling
  • Glucose Transporter Type 5 / metabolism
  • Intestine, Small / metabolism
  • Ion Transport / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Models, Animal
  • Nutritional Physiological Phenomena
  • Sodium-Glucose Transporter 1 / metabolism

Substances

  • Calcium Channels, L-Type
  • Calcium-Binding Proteins
  • Glucose Transporter Type 5
  • Sodium-Glucose Transporter 1
  • Fructose
  • Fructokinases
  • Calcium