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Orexins control intestinal glucose transport by distinct neuronal, endocrine, and direct epithelial pathways
Robert Ducroc1, Thierry Voisin, Aadil El Firar
1Institut National de la Santé et de la Recherche Médicale U773, Centre de Recherche Biomédicale Bichat-Beaujon, 16 rue Henri Huchard, BP16, 75870 Paris cedex 18, France. ducroc@bichat.inserm.fr
Objective:
Orexins are neuropeptides involved in energy homeostasis. We investigated the effect of orexin A (OxA) and orexin B (OxB) on intestinal glucose transport in the rat.
Research Design And Methods And Results:
Injection of orexins led to a decrease in the blood glucose level in oral glucose tolerance tests (OGTTs). Effects of orexins on glucose entry were analyzed in Ussing chambers using the Na(+)-dependent increase in short-circuit current (Isc) to quantify jejunal glucose transport. The rapid and marked increase in Isc induced by luminal glucose was inhibited by 10 nmol/l OxA or OxB (53 and 59%, respectively). Response curves to OxA and OxB were not significantly different with half-maximal inhibitory concentrations at 0.9 and 0.4 nmol/l, respectively. On the one hand, OxA-induced inhibition of Isc was reduced by the neuronal blocker tetrodotoxin (TTX) and by a cholecystokinin (CCK) 2R antagonist, indicating involvement of neuronal and endocrine CCK-releasing cells. The OX(1)R antagonist SB334867 had no effect on OxA-induced inhibition, which is likely to occur via a neuronal and/or endocrine OX(2)R. On the other hand, SB334867 induced a significant right shift of the concentration-effect curve for OxB. This OxB-preferring OX(1)R pathway was not sensitive to TTX or to CCKR antagonists, suggesting that OxB may act directly on enterocytic OX(1)R. These distinct effects of OxA and OxB are consistent with the expression of OX(1)R and OX(2)R mRNA in the epithelial and nonepithelial tissues, respectively.
Conclusions:
Our data delineate a new function for orexins as inhibitors of intestinal glucose absorption and provide a new basis for orexin-induced short-term control of energy homeostasis.
Insights
Orexin A (OxA) and orexin B (OxB) inhibit intestinal glucose absorption in rats, decreasing blood glucose levels. This suggests a new role for orexins in regulating energy homeostasis.
Area of Science:
- Neuroendocrinology
- Gastroenterology
- Metabolic Regulation
Background:
- Orexins are neuropeptides crucial for energy homeostasis.
- Intestinal glucose absorption plays a key role in regulating blood glucose levels and overall energy balance.
Purpose of the Study:
- To investigate the effects of orexin A (OxA) and orexin B (OxB) on intestinal glucose transport in rats.
- To elucidate the mechanisms underlying orexin-mediated regulation of glucose absorption.
Main Methods:
- Oral glucose tolerance tests (OGTTs) were performed in rats following orexin administration.
- Jejunal glucose transport was quantified in Ussing chambers by measuring the Na(+)-dependent increase in short-circuit current (Isc).
- The involvement of neuronal and endocrine pathways was assessed using tetrodotoxin (TTX), cholecystokinin (CCK) 2R antagonists, and OX(1)R antagonist SB334867.
Main Results:
- Both OxA and OxB significantly decreased blood glucose levels during OGTTs.
- OxA and OxB inhibited glucose-induced Isc in the jejunum, indicating reduced glucose transport.
- OxA's inhibitory effect involved neuronal and CCK-releasing cells via OX(2)R, while OxB acted directly on enterocytic OX(1)R.
Conclusions:
- Orexins function as inhibitors of intestinal glucose absorption.
- These findings establish a novel role for orexins in the short-term control of energy homeostasis.
- Distinct orexin receptor pathways mediate the differential effects of OxA and OxB on glucose transport.
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