Gut-derived signaling molecules and vagal afferents in the control of glucose and energy homeostasis

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 7, Issue 4, 2004, Pages 471-478

  Thorens, Bernard ^a,c   Larsen, Philip Just ^b  

^a Department of Physiology ^*  (Switzerland)

^b Rheoscience A/S   (Denmark)

^c University of Lausanne Departement de Pharmacologie et de Toxicologie   (Switzerland)

Author keywords

Autonomous nervous system; Food intake; Glucose homeostasis; Glucose sensing; Gut brain axis

Indexed keywords

ADENYLATE KINASE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 2; GLUCOSE; GLUTAMIC ACID; PEPTIDE YY; NEUROPEPTIDE;

ARCUATE NUCLEUS; BIOSENSOR; BLOOD BRAIN BARRIER; BRAIN STEM; DNA MODIFICATION; FOOD COMPOSITION; GASTROINTESTINAL TRACT; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; GLUCOSE UTILIZATION; HORMONE RELEASE; HYPOTHALAMUS NUCLEUS; INTESTINE; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; STOMACH EMPTYING; ANIMAL; DIGESTIVE FUNCTION; DIGESTIVE SYSTEM; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; FOOD INTAKE; HUMAN; INNERVATION; METABOLISM; PHYSIOLOGY; SENSORY NERVE; VAGUS NERVE;

ANIMALIA;

AFFERENT PATHWAYS; ANIMALS; APPETITE REGULATION; DIGESTIVE PHYSIOLOGY; DIGESTIVE SYSTEM; EATING; ENERGY METABOLISM; FEEDING BEHAVIOR; GLUCOSE; HUMANS; NEUROPEPTIDES; SIGNAL TRANSDUCTION; VAGUS NERVE;

EID: 12244305762     PISSN: 13631950     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.mco.0000134368.91900.84     Document Type: Review

References (58)

1. Banks WA, Tschop M, Robinson SM, Heiman ML. Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 2002; 302:822-827.
2. 3-36 acts in the brain.
3. Horvath TL, Diano S, Tschop M. Ghrelin in hypothalamic regulation of energy balance. Curr Top Med Chem 2003; 3:921-927.
4. Schwanz GJ, Moran TH. CCK elicits and modulates vagal afferent activity arising from gastric and duodenal sites. Ann NY Acad Sci 1994; 713:121-128.
5. Nishizawa M, Nabakayashi H, Uchida K, et al. The hepatic vagal nerve is receptor to incretin hormone glucagon-like peptide-1, but to glucose-dependent insulinotropic polypeptide, in the portal vein. J Autonom Nerv Syst 1996; 61:149-154.
6. Phillips RJ, Baronowsky EA, Powley TL. Long-term regeneration of abdominal vagus: efferents fail while afferents succeed. J Comp Neurol 2003; 455:222-237. A thorough study combining an anatomical description of vagal innervation of the gut together with a functional characterization of selective fibre types.
7. Berthoud HR, Lynn PA, Blackshaw LA. Vagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields. Am J Physiol Regul Integr Comp Physiol 2001; 280:R1371-R1381.
8. Fox EA, Phillips RJ, Baronowsky EA, et al. Neurotrophin-4 deficient mice have a loss of vagal intraganglionic mechanoreceptors from the small intestine and a disruption of short-term satiety. J Neurosci 2001; 21:8602-8615.
9. Chi MM, Powley TL. c-Kit mutant mouse behavioral phenotype: altered meal patterns and CCK sensitivity but normal daily food intake and body weight. Am J Physiol Regul Integr Comp Physiol 2003; 285:R1170-R1183. A very elegant and thorough description of the functional implications of a life without mechanosensory IMAs.
10. Vrang N, Phifer CB, Corkern MM, Berthoud HR. Gastric distension induces c-Fos in medullary GLP-1/2-containing neurons. Am J Physiol Regul Integr Comp Physiol 2003, 285:R470-R478. A provocative functional anatomical study showing that gastric filling and the accompanying gastrointestinal mechanostimulation activates brain GLP-1/GLP-2 neurons, which are proposed to mediate postprandial satiety and perhaps premature meal termination.
11. Ward SM, Bayguinov J, Won KJ, et al. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol 2003; 465:121-135.
12. Schwarte GJ. The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition 2000; 16:866-573.
13. Corp ES, McQuade J, Moran TH, Smith GP. Characterization of type A and type B CCK receptor binding sites in rat vagus nerve. Brain Res 1993; 623:161-166.
14. Zhang X, Shi T, Holmberg K, et al. Expression and regulation of the neuropeptide Y Y2 receptor in sensory and autonomic ganglia. Proc Natl Acad Sci U S A 1997; 94:729-734.
15. Rinaman L. Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J Neurosci 2003; 23:10084-10092. A beautiful study employing site-directed neurotoxic lesioning of catecholaminergic brainstem neurons to confirm their importance as mediators of gastric viscerosensory information involved in meal termination.
16. Hay-Schmidt A, Helboe L, Larsen PJ. Leptin receptor immunoreactivity is present in ascending serotonergic and catecholaminergic neurons of the rat. Neuroendocrinology 2001; 73:215-226.
17. Lin L, Thomas SR, Kilroy G, et al. Enterostatin inhibition of dietary fat intake is dependent on CCK-A receptors. Am J Physiol Regul Integr Comp Physiol 2003; 285:R321-R328. A nice and clearly presented study demonstrating that enterostatin mediates its action via a neuronal pathway addressing peripherally accessible cholecystokinin-A receptors as a downstream target.
18. Gribble FM, Williams L, Simpson AK, Reimann F. A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line. Diabetes 2003; 52:1147-1154.
19. Hevener AL, Bergman RN, Donovan CM. Novel glucosensor for hypoglycemic detection localized to the portal vein. Diabetes 1997; 46:1521-1525.
20. Russek M. Participation of hepatic glucoreceptors in the control of intake of food. Nature 1963; 197:79-80.
21. Russek M. Demonstration of the influence of an hepatic glucosensitive mechanism on food-intake. Physiol Behav 1970; 5:1207-1209.
22. Gardemann A, Strulik H, Jungermann K. A portal-arterial glucose concentration gradient as a signal for an insulin-dependent net glucose uptake in perfused rat liver. FEBS Lett 1986; 202:255-259.
23. Cardin S, Emshwiller M, Jackson PA, et al. Portal glucose infusion increases hepatic glycogen deposition in conscious unrestrained rats. J Appl Physiol 1999; 87:1470-1475.
24. Burcelin R, Dolci W, Thorens B. Portal glucose infusion in the mouse induces hypoglycemia. Evidence that the hepatoportal glucose sensor stimulates glucose utilization. Diabetes 2000; 49:1635-1642.
25. Adachi A. Electrophysiological study of hepatic vagal projection to the medulla. Neurosci Lett 1981; 24:19-23.
26. Adachi A, Shimizu N, Oomura Y, Kobashi M. Convergence of hepatoportal glucose-sensitive afferents signal to glucose sensitive units within the nucleus of the solitary tract. Neurosci Lett 1984; 46:215-218.
27. Shimizu N, Oomura Y, Novin D, et al. Functional correlations between lateral hypothalamic glucose-sensitive neurons and hepatic portal glucose-sensitive units in rat. Brain Res 1983; 265:49-54.
28. Burcelin R, Dolci W, Thorens B. Glucose sensing by the hepatoportal sensor is GLUT2-dependent. In vivo analysis in GLUT2-null mice. Diabetes 2000; 49:1643-1648.
29. Nishizawa M, Moore MC, Shiota M, et al. Effect of intraportal glucagon-like peptide-1 on glucose metabolism in conscious dogs. Am J Physiol Endocrinol Metab 2003; 284:E1027-E1036.
30. Nishizawa M, Nakabayashi H, Kawai K, et al. The hepatic vagal reception of intraportal GLP-1 is via receptor different from the pancreatic GLP-1 receptor. J Autonom Nerv Syst 2000; 80:14-21.
31. Burcelin R, DaCosta A, Drucker D, Thorens B. Glucose competence of the hepatoporal vein sensor requires the presence of an activated GLP-1 receptor. Diabetes 2001; 50:1720-1728.
32. Nakagawa A, Satake H, Nakabayashi H, et al. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Autonom Neurosci 2004; 110:36-43.
33. Burcelin R, Crivelli V, Perrin C, et al. GLUT4, AMP kinase, but not the insulin receptor, are required for hepatoportal glucose sensor-stimulated muscle glucose utilization. J Clin Invest 2003; 111:1555-1562. A study in which mice with muscle-specific genetic modifications were used functionally to determine the role of the insulin receptors, GLUT4 and adenosine monophosphate kinase, in portal signal-induced glucose utilization.
34. Balkan B, Li X. Portal GLP-1 administration in rats augments the insulin response to glucose via neuronal mechanisms. Am J Physiol 2000; 279:R1449-R1454.
35. Preitner F, Ibberson M, Franklin I, et al. Gluco-incretin control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J Clin Invest 2004; 113:635-645. This study presents evidence that the hepatoportal sensor plays a critical role in triggering, in vivo, the first phase of insulin secretion.
36. Ahren B. Sensory nerves contribute to insulin secretion by glucagon-like peptide-1 in mice. Am J Physiol Regul lntegr Comp Physiol 2004; 286:R269-R272. The destruction of sensory nerves by capsaicin is shown to suppress the stimulation of insulin secretion by low doses of GLP-1, indicating that these nerves are an important site of action of this gastrointestinal hormone.
37. Berthoud H-R, Kressel M, Neuhuber WL. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anatom Embryol 1992; 186:431-442.
38. Berthoud H-R, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Autonom Neurosci: Basic Clin 2000; 85:1-17.
39. Pardal R, Lopez-Barneo J. Low glucose-sensing cells in the carotid body. Nat Neurosci 2002; 5:197-198.
40. Diez-Sampedro A, Hirayama BA, Osswald C, et al. A glucose sensor hiding in a family of transporters. Proc Natl Acad Sci U S A 2003; 100:11753-11758. This study provides evidence that the sodium ion/glucose symporter isoform SGLT3 does not transport glucose but is a glucose sensor, present in intestinal mucosa nerve terminals.
41. Batterham RL, Cowley MA, Small CJ, et al. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 2002; 418:650-654.
42. Batterham RL, Cohen MA, Ellis SM, et al. Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 2003; 349:941-948.
43. Naslund E, Gryback P, Hellstrom PM, et al. Gastrointestinal hormones and gastric emptying 20 years after jejunoileal bypass for massive obesity. Int J Obes Relat Metab Disord 1997; 21:387-392.
44. Gomez R, Navarro M, Ferrer B, et al. A peripheral mechanism for CB1 cannabinoid receptor-dependent modulation of feeding. J Neurosci 2002; 22:9612-9617.
45. Rodriguez de Fonseca F, Navarro M, Gomez R, et al. An anorexic lipid mediator regulated by feeding. Nature 2001; 414:209-212.
46. Izzo AA, Capasso F, Costagliola A, et al. An endogenous cannabinoid tone attenuates cholera toxin-induced fluid accumulation in mice. Gastroenterology 2003; 125:765-774.
47. Fu J, Gaetani S, Oveisi F, et al. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 2003; 425:90-93. A very interesting study showing that endocannabinoids synthesized in the gut can regulate food intake through their interaction with hepatocyte nuclear receptors.
48. Larsen PJ, Jensen PB, Sorensen RV, et al. Differential influences of peroxisome proliferator-activated receptors gamma and -alpha on food intake and energy homeostasis. Diabetes 2003; 52:2249-2259.
49. Prado CL, Pugh-Bernard AE, Elghazi L, et al. Ghrelin cells replace insulin-producing {beta} cells in two mouse models of pancreas development. Proc Natl Acad Sci U S A 2004; 101:2924-2929.
50. Wierup N, Yang S, McEvilly RJ, et al. Ghrelin is expressed in a novel endocrine cell type in developing rat islets and inhibits insulin secretion from INS-1 (832/13) cells. J Histochem Cytochem 2004; 52:301-310.
51. Wierup N, Svensson H, Mulder H, Sundler F. The ghrelin cell: a novel developmentally regulated islet cell in the human pancreas. Regul Pept 2002; 107:63-69.
52. Ruter J, Kobelt P, Tebbe JJ, et al. Intraperitoneal injection of ghrelin induces Fos expression in the paraventricular nucleus of the hypothalamus in rats. Brain Res 2003; 991:26-33.
53. Seoane LM, Lopez M, Tovar S, et al. Agouti-related peptide, neuropeptide Y, and somatostatin-producing neurons are targets for ghrelin actions in the rat hypothalamus. Endocrinology 2003; 144:544-551.
54. Kohno D, Gao HZ, Muroya S, et al. Ghrelin directly interacts with neuropeptide-Y-containing neurons in the rat arcuate nucleus: Ca2+ signaling via protein kinase A and N-type channel-dependent mechanisms and cross-talk with leptin and orexin. Diabetes 2003; 52:948-956. A nice study on the direct effect of ghrelin on isolated hypothalamic neuropeptide Y neurons.
55. Cowley MA, Smith RG, Diano S, et al. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 2003; 37:649-661. A detailed study of hypothalamic ghrelin expressing neurons and their local synaptic connections.
56. Toshinai K, Date Y, Murakami N, et al. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology 2003; 144:1506-1512.
57. Yamanaka A, Beuckmann CT, Willie JT, et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 2003; 38:701-713.
58. Sun Y, Ahmed S, Smith RG. Deletion of ghrelin impairs neither growth nor appetite. Mol Cell Biol 2003; 23:7973-7981.