Glucose sensing by gut endocrine cells and activation of the vagal afferent pathway is impaired in a rodent model of type 2 diabetes mellitus

Am J Physiol Regul Integr Comp Physiol. 2012 Mar 15;302(6):R657-66. doi: 10.1152/ajpregu.00345.2011. Epub 2011 Dec 7.

Abstract

Glucose in the gut lumen activates gut endocrine cells to release 5-HT, glucagon-like peptide 1/2 (GLP-1/2), and glucose-dependent insulinotropic polypeptide (GIP), which act to change gastrointestinal function and regulate postprandial plasma glucose. There is evidence that both release and action of incretin hormones is reduced in type 2 diabetes (T2D). We measured cellular activation of enteroendocrine and enterochromaffin cells, enteric neurons, and vagal afferent neurons in response to intestinal glucose in a model of type 2 diabetes mellitus, the UCD-T2DM rat. Prediabetic (PD), recent-diabetic (RD, 2 wk postonset), and 3-mo diabetic (3MD) fasted UCD-T2DM rats were given an orogastric gavage of vehicle (water, 0.5 ml /100 g body wt) or glucose (330 μmol/100 g body wt); after 6 min tissue was removed and cellular activation was determined by immunohistochemistry for phosphorylated calcium calmodulin-dependent kinase II (pCaMKII). In PD rats, pCaMKII immunoreactivity was increased in duodenal 5-HT (P < 0.001), K (P < 0.01) and L (P < 0.01) cells in response to glucose; glucose-induced activation of all three cell types was significantly reduced in RD and 3MD compared with PD rats. Immunoreactivity for GLP-1, but not GIP, was significantly reduced in RD and 3MD compared with PD rats (P < 0.01). Administration of glucose significantly increased pCaMKII in enteric and vagal afferent neurons in PD rats; glucose-induced pCaMKII immunoreactivity was attenuated in enteric and vagal afferent neurons (P < 0.01, P < 0.001, respectively) in RD and 3MD. These data suggest that glucose sensing in enteroendocrine and enterochromaffin cells and activation of neural pathways is markedly impaired in UCD-T2DM rats.

Publication types

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

MeSH terms

  • Afferent Pathways / physiopathology*
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetes Mellitus, Type 2 / pathology
  • Diabetes Mellitus, Type 2 / physiopathology*
  • Disease Models, Animal
  • Enterochromaffin Cells / metabolism
  • Enterochromaffin Cells / pathology
  • Enteroendocrine Cells / metabolism*
  • Enteroendocrine Cells / pathology
  • Gastric Inhibitory Polypeptide / metabolism
  • Glucagon-Like Peptides / metabolism
  • Glucose / metabolism*
  • Insulin Resistance / physiology
  • Obesity / metabolism
  • Obesity / physiopathology
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Zucker
  • Serotonin / metabolism
  • Vagus Nerve / physiopathology*

Substances

  • Serotonin
  • Gastric Inhibitory Polypeptide
  • Glucagon-Like Peptides
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Glucose