Mucosal adaptation to enteral nutrients is dependent on the physiologic actions of glucagon-like peptide-2 in mice

Gastroenterology. 2005 May;128(5):1340-53. doi: 10.1053/j.gastro.2005.02.033.

Abstract

Background & aims: Our understanding of the intestinotropic actions of glucagon-like peptide-2 (GLP-2)(1-33) is based on pharmacologic studies involving exogenous administration. However, the physiologic role of GLP-2 in mucosal growth and adaptation to nutritional stimulation remains poorly understood.

Methods: The properties of GLP-2(3-33), a GLP-2(1-33) metabolite, were determined in baby-hamster kidney cells transfected with the mouse GLP-2 receptor complementary DNA and in isolated murine intestinal muscle strips. To investigate the role of endogenous GLP-2(1-33) in gut adaptation, GLP-2(3-33) was administered to mice that were re-fed for 24 hours after 24 hours of fasting, and the small intestine was analyzed. GLP-2(3-33) also was injected into rats for analysis of circulating GLP-2(1-33) levels.

Results: GLP-2(3-33) antagonized the actions of GLP-2(1-33) in vitro and ex vivo. Fasting mice exhibited small intestinal atrophy (37% +/- 1% decrease in small intestinal weight, 19% +/- 2% decrease in crypt-villus height, and 99% +/- 35% increase in villus apoptosis, P < .05-.01). Adaptive growth in re-fed mice restored all these parameters, as well as crypt-cell proliferation, to normal control levels (P < .05 vs. fasting); these adaptive changes were prevented partially or completely by co-administration of GLP-2(3-33) to refeeding mice (by 32% +/- 19% to 103% +/- 15%, P < .05-.01 vs re-fed mice). Exogenous GLP-2(3-33) did not affect endogenous GLP-2(1-33) levels.

Conclusions: These data show that endogenous GLP-2 regulates the intestinotropic response in re-fed mice through modulation of crypt-cell proliferation and villus apoptosis. GLP-2 is therefore a physiologic regulator of the dynamic adaptation of the gut mucosal epithelium in response to luminal nutrients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / drug effects
  • Adaptation, Physiological / physiology*
  • Amino Acid Sequence
  • Animals
  • Apoptosis / physiology
  • Body Weight
  • Cell Division / physiology
  • Cloning, Molecular
  • Drinking / physiology
  • Eating / physiology*
  • Female
  • Gene Expression
  • Glucagon / genetics
  • Glucagon-Like Peptide 2
  • Glucagon-Like Peptide-1 Receptor
  • Glucagon-Like Peptides
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / enzymology
  • Intestinal Mucosa / physiology*
  • Intestine, Small / cytology
  • Intestine, Small / enzymology
  • Intestine, Small / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Organ Size
  • Peptide Fragments / blood
  • Peptide Fragments / pharmacology
  • Peptide Fragments / physiology*
  • Proglucagon
  • Protein Precursors / genetics
  • Rats
  • Rats, Wistar
  • Receptors, Glucagon / genetics
  • Receptors, Glucagon / metabolism

Substances

  • Glp1r protein, mouse
  • Glp1r protein, rat
  • Glucagon-Like Peptide 2
  • Glucagon-Like Peptide-1 Receptor
  • Peptide Fragments
  • Protein Precursors
  • Receptors, Glucagon
  • glucagon-like peptide-2 (3-33)
  • Proglucagon
  • Glucagon-Like Peptides
  • Glucagon