Plasticity in vagal afferent neurones during feeding and fasting: Mechanisms and significance

Acta Physiologica

Volumn 201, Issue 3, 2011, Pages 313-321

  Dockray, G J ^a   Burdyga, G ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

CB1 receptors; Cholecystokinin; Cocaine and amphetamine regulated transcript; Ghrelin; Melanin concentrating hormone; Y2 receptors

Indexed keywords

CANNABINOID 1 RECEPTOR; CHOLECYSTOKININ; CHOLECYSTOKININ A RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; GHRELIN; LEPTIN; MELANIN CONCENTRATING HORMONE RECEPTOR 1; NEUROPEPTIDE Y2 RECEPTOR;

ANIMAL EXPERIMENT; CALORIC INTAKE; DIET RESTRICTION; ENZYME ACTIVATION; FEEDING; FOOD INTAKE; HORMONE RELEASE; MAJOR HISTOCOMPATIBILITY COMPLEX; NERVE CELL PLASTICITY; NEUROCHEMISTRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REVIEW; VAGUS NERVE; VAGUS NERVE STIMULATION;

AFFERENT PATHWAYS; ANIMALS; APPETITE REGULATION; FASTING; FEEDING BEHAVIOR; HUMANS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; RATS; SENSORY RECEPTOR CELLS; VAGUS NERVE;

EID: 79251634224     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2010.02219.x     Document Type: Review

References (74)

1. Arnold, M., Mura, A., Langhans, W. & Geary, N. 2006. Gut vagal afferents are not necessary for the eating-stimulatory effect of intraperitoneally injected ghrelin in the rat. J Neurosci 26, 11052-11060.
2. Beckmann, A.M. & Wilce, P.A. 1997. Egr transcription factors in the nervous system. Neurochem Int 31, 477-510.
3. Berthoud, H.R. 2008. The vagus nerve, food intake and obesity. Regul Pept 149, 15-25.
4. Broberger, C., Holmberg, K., Kuhar, M.J. & Hokfelt, T. 1999. Cocaine- and amphetamine-regulated transcript in the rat vagus nerve: a putative mediator of cholecystokinin-induced satiety. Proc Natl Acad Sci USA 96, 13506-13511.
5. Broberger, C., Holmberg, K., Shi, T.J., Dockray, G. & Hokfelt, T. 2001. Expression and regulation of cholecystokinin and cholecystokinin receptors in rat nodose and dorsal root ganglia. Brain Res 903, 128-140.
6. Browning, K.N. 2003. Excitability of nodose ganglion cells and their role in vago-vagal reflex control of gastrointestinal function. Curr Opin Pharmacol 3, 613-617.
7. Bucinskaite, V., Kurosawa, M., Miyasaka, K., Funakoshi, A. & Lundeberg, T. 1997. Interleukin-1beta sensitizes the response of the gastric vagal afferent to cholecystokinin in rat. Neurosci Lett 229, 33-36.
8. Burdyga, G., Spiller, D., Morris, R., Lal, S., Thompson, D.G., Saeed, S., Dimaline, R., Varro, A. & Dockray, G.J. 2002. Expression of the leptin receptor in rat and human nodose ganglion neurones. Neuroscience 109, 339-347.
9. Burdyga, G., Lal, S., Spiller, D., Jiang, W., Thompson, D.G., Attwood, S., Saeed, S., Grundy, D., Varro, A., Dimaline, R. & Dockray, G.J. 2003. Localization of orexin-1 receptors to vagal afferent neurons in the rat and humans. Gastroenterology 124, 129-139.
10. Burdyga, G., Lal, S., Varro, A., Dimaline, R., Thompson, D.G. & Dockray, G.J. 2004. Expression of cannabinoid CB1 receptors by vagal afferent neurons is inhibited by cholecystokinin. J Neurosci 24, 2708-2715.
11. Burdyga, G., Varro, A., Dimaline, R., Thompson, D.G. & Dockray, G.J. 2006a. Feeding-dependent depression of melanin-concentrating hormone and melanin-concentrating hormone receptor-1 expression in vagal afferent neurones. Neuroscience 137, 1405-1415.
12. Burdyga, G., Varro, A., Dimaline, R., Thompson, D.G. & Dockray, G.J. 2006b. Ghrelin receptors in rat and human nodose ganglia: putative role in regulating CB-1 and MCH receptor abundance. Am J Physiol Gastrointest Liver Physiol 290, G1289-G1297.
13. Burdyga, G., de Lartigue, G., Raybould, H.E., Morris, R., Dimaline, R., Varro, A., Thompson, D.G. & Dockray, G.J. 2008. Cholecystokinin regulates expression of Y2 receptors in vagal afferent neurons serving the stomach. J Neurosci 28, 11583-11592.
14. Burdyga, G., Varro, A., Dimaline, R., Thompson, D.G. & Dockray, G.J. 2010. Expression of cannabinoid CB1 receptors by vagal afferent neurons: kinetics, and role in influencing neurochemical phenotype. Am J Physiol Gastrointest Liver Physiol 299, 1514-1524.
15. Buyse, M., Ovesjo, M.L., Goiot, H., Guilmeau, S., Peranzi, G., Moizo, L., Walker, F., Lewin, M.J., Meister, B. & Bado, A. 2001. Expression and regulation of leptin receptor proteins in afferent and efferent neurons of the vagus nerve. Eur J Neurosci 14, 64-72.
16. Date, Y., Murakami, N., Toshinai, K., Matsukura, S., Niijima, A., Matsuo, H., Kangawa, K. & Nakazato, M. 2002. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 123, 1120-1128.
17. Date, Y., Toshinai, K., Koda, S., Miyazato, M., Shimbara, T., Tsuruta, T., Niijima, A., Kangawa, K. & Nakazato, M. 2005. Peripheral interaction of ghrelin with cholecystokinin on feeding regulation. Endocrinology 146, 3518-3525.
18. Dockray, G.J. 2009a. The brain-gut axis. In: Yamada, T. (ed.) Textbook of Gastroenterology, 5th edn, pp. 86-102. Chichester, WestSussex: Wiley-Blackwell.
19. Dockray, G.J. 2009b. The versatility of the vagus. Physiol Behav 97, 531-536.
20. Ellis, J., Pediani, J.D., Canals, M., Milasta, S. & Milligan, G. 2006. Orexin-1 receptor-cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and -independent coordinated alterations of receptor localization and function. J Biol Chem 281, 38812-38824.
21. Forster, E.R., Green, T., Elliot, M., Bremner, A. & Dockray, G.J. 1990. Gastric emptying in rats: role of afferent neurons and cholecystokinin. Am J Physiol 258, G552-G556.
22. Fraser, K.A. & Davison, J.S. 1992. Cholecystokinin-induced c-fos expression in the rat brain stem is influenced by vagal nerve integrity. Exp Physiol 77, 225-228.
23. Gaige, S., Abysique, A. & Bouvier, M. 2002. Effects of leptin on cat intestinal vagal mechanoreceptors. J Physiol 543, 679-689.
24. Gaige, S., Abou, E., Abysique, A. & Bouvier, M. 2004. Effects of interactions between interleukin-1 beta and leptin on cat intestinal vagal mechanoreceptors. J Physiol 555, 297-310.
25. Gautron, L., Lee, C., Funahashi, H., Friedman, J., Lee, S. & Elmquist, J. 2010. Melanocortin-4 receptor expression in a vago-vagal circuitry involved in postprandial functions. J Comp Neurol 518, 6-24.
26. Glatzle, J., Darcel, N., Rechs, A.J., Kalogeris, T.J., Tso, P. & Raybould, H.E. 2004. Apolipoprotein A-IV stimulates duodenal vagal afferent activity to inhibit gastric motility via a CCK1 pathway. Am J Physiol Regul Integr Comp Physiol 287, R354-R359.
27. Gomez, R., Navarro, M., Ferrer, B., Trigo, J.M., Bilbao, A., Del Arco, I., Cippitelli, A., Nava, F., Piomelli, D. & Rodriguez, D.F. 2002. A peripheral mechanism for CB1 cannabinoid receptor-dependent modulation of feeding. J Neurosci 22, 9612-9617.
28. Green, T. & Dockray, G.J. 1988. Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig. Neuroscience 25, 181-193.
29. Hayes, M.R., Skibicka, K.P., Leichner, T.M., Guarnieri, D.J., DiLeone, R.J., Bence, K.K. & Grill, H.J. 2010. Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation. Cell Metab 11, 77-83.
30. Hertz, A.F. 1911. The Sensibility of the Alimentary Tract. Hodder & Stoughton, London.
31. Hilairet, S., Bouaboula, M., Carriere, D., Le Fur, G. & Casellas, P. 2003. Hypersensitization of the Orexin 1 receptor by the CB1 receptor: evidence for cross-talk blocked by the specific CB1 antagonist, SR141716. J Biol Chem 278, 23731-23737.
32. Hondoh, A., Ishida, Y., Ugawa, S., Ueda, T., Shibata, Y., Yamada, T., Shikano, M., Murakami, S. & Shimada, S. 2010. Distinct expression of cold receptors (TRPM8 and TRPA1) in the rat nodose-petrosal ganglion complex. Brain Res 1319, 60-69.
33. Iggo, A. 1955. Tension receptors in the stomach and the urinary bladder. J Physiol 128, 593-607.
34. Izzo, A.A., Piscitelli, F., Capasso, R., Aviello, G., Romano, B., Borrelli, F., Petrosino, S. & Di, M.V. 2009. Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding. Br J Pharmacol 158, 451-461.
35. Kurosawa, M., Uvnas-Moberg, K., Miyasaka, K. & Lundeberg, T. 1997. Interleukin-1 increases activity of the gastric vagal afferent nerve partly via stimulation of type A CCK receptor in anesthetized rats. J Auton Nerv Syst 62, 72-78.
36. de Lartigue, G., Dimaline, R., Varro, A. & Dockray, G.J. 2007. Cocaine- and amphetamine-regulated transcript: stimulation of expression in rat vagal afferent neurons by cholecystokinin and suppression by ghrelin. J Neurosci 27, 2876-2882.
37. de Lartigue, G., Dimaline, R., Varro, A., Raybould, H., de la Serre, C.B. & Dockray, G.J. 2010a. Cocaine and amphetamine regulated transcript mediates the actions of cholecystokinin on rat vagal afferent neurons. Gastroenterology 138, 1479-1490.
38. de Lartigue, G., Lur, G., Dimaline, R., Varro, A., Raybould, H. & Dockray, G.J. 2010b. EGR1 is a target for cooperative interactions between cholecystokinin and leptin, and inhibition by ghrelin, in vagal afferent neurons. Endocrinology 151, 3589-3599.
39. Lassman, D.J., McKie, S., Gregory, L.J., Lal, S., D'Amato, M., Steele, I., Varro, A., Dockray, G.J., Williams, S.C. & Thompson, D.G. 2010. Defining the role of cholecystokinin in the lipid-induced human brain activation matrix. Gastroenterology 138, 1514-1524.
40. Li, Y. 2007. Sensory signal transduction in the vagal primary afferent neurons. Curr Med Chem 14, 2554-2563.
41. Luckman, S.M. 1992. Fos-like immunoreactivity in the brainstem of the rat following peripheral administration of cholecystokinin. J Neuroendocrinol 4, 149-151.
42. Luyer, M.D., Greve, J.W., Hadfoune, M., Jacobs, J.A., Dejong, C.H. & Buurman, W.A. 2005. Nutritional stimulation of cholecystokinin receptors inhibits inflammation via the vagus nerve. J Exp Med 202, 1023-1029.
43. McDermott, J.R., Leslie, F.C., D'Amato, M., Thompson, D.G., Grencis, R.K. & McLaughlin, J.T. 2006. Immune control of food intake: enteroendocrine cells are regulated by CD4+ T lymphocytes during small intestinal inflammation. Gut 55, 492-497.
44. Moran, T.H., Smith, G.P., Hostetler, A.M. & McHugh, P.R. 1987. Transport of cholecystokinin (CCK) binding sites in subdiaphragmatic vagal branches. Brain Res 415, 149-152.
45. Moriarty, P., Dimaline, R., Thompson, D.G. & Dockray, G.J. 1997. Characterization of cholecystokininA and cholecystokininB receptors expressed by vagal afferent neurons. Neuroscience 79, 905-913.
46. Morton, G.J., Blevins, J.E., Williams, D.L., Niswender, K.D., Gelling, R.W., Rhodes, C.J., Baskin, D.G. & Schwartz, M.W. 2005. Leptin action in the forebrain regulates the hindbrain response to satiety signals. J Clin Invest 115, 703-710.
47. Nakagawa, A., Satake, H., Nakabayashi, H., Nishizawa, M., Furuya, K., Nakano, S., Kigoshi, T., Nakayama, K. & Uchida, K. 2004. Receptor gene expression of glucagon-like peptide-1, but not glucose-dependent insulinotropic polypeptide, in rat nodose ganglion cells. Auton Neurosci 110, 36-43.
48. Nefti, W., Chaumontet, C., Fromentin, G., Tome, D. & Darcel, N. 2009. A high-fat diet attenuates the central response to within-meal satiation signals and modifies the receptor expression of vagal afferents in mice. Am J Physiol Regul Integr Comp Physiol 296, R1681-R1686.
49. Page, A.J., Young, R.L., Martin, C.M., Umaerus, M., O'Donnell, T.A., Cooper, N.J., Coldwell, J.R., Hulander, M., Mattsson, J.P., Lehmann, A. & Blackshaw, L.A. 2005. Metabotropic glutamate receptors inhibit mechanosensitivity in vagal sensory neurons. Gastroenterology 128, 402-410.
50. Paintal, A.S. 1973. Vagal sensory receptors and their reflex effects. Physiol Rev 53, 159-227.
51. Paulino, G., Barbier de la, S.C., Knotts, T.A., Oort, P.J., Newman, J.W., Adams, S.H. & Raybould, H.E. 2009. Increased expression of receptors for orexigenic factors in nodose ganglion of diet-induced obese rats. Am J Physiol Endocrinol Metab 296, E898-E903.
52. Peiser, C., Springer, J., Groneberg, D.A., McGregor, G.P., Fischer, A. & Lang, R.E. 2002. Leptin receptor expression in nodose ganglion cells projecting to the rat gastric fundus. Neurosci Lett 320, 41-44.
53. Peters, J.H., Karpiel, A.B., Ritter, R.C. & Simasko, S.M. 2004. Cooperative activation of cultured vagal afferent neurons by leptin and cholecystokinin. Endocrinology 145, 3652-3657.
54. Peters, J.H., Simasko, S.M. & Ritter, R.C. 2006. Modulation of vagal afferent excitation and reduction of food intake by leptin and cholecystokinin. Physiol Behav 89, 477-485.
55. Raybould, H.E. & Tache, Y. 1988. Cholecystokinin inhibits gastric motility and emptying via a capsaicin-sensitive vagal pathway in rats. Am J Physiol 255, G242-G246.
56. Raybould, H.E., Gayton, R.J. & Dockray, G.J. 1988. Mechanisms of action of peripherally administered cholecystokinin octapeptide on brain stem neurons in the rat. J Neurosci 8, 3018-3024.
57. Rogers, R.C. & Hermann, G.E. 2008. Mechanisms of action of CCK to activate central vagal afferent terminals. Peptides 29, 1716-1725.
58. Rogge, G., Jones, D., Hubert, G.W., Lin, Y. & Kuhar, M.J. 2008. CART peptides: regulators of body weight, reward and other functions. Nat Rev Neurosci 9, 747-758.
59. Schwartz, G.J., McHugh, P.R. & Moran, T.H. 1993. Gastric loads and cholecystokinin synergistically stimulate rat gastric vagal afferents. Am J Physiol 265, R872-R876.
60. Schwartz, G.J., Moran, T.H., White, W.O. & Ladenheim, E.E. 1997. Relationships between gastric motility and gastric vagal afferent responses to CCK and GRP in rats differ. Am J Physiol 272, R1726-R1733.
61. Schwartz, M.W., Woods, S.C., Porte, D. Jr, Seeley, R.J. & Baskin, D.G. 2000. Central nervous system control of food intake. Nature 404, 661-671.
62. Sharkey, K.A., Williams, R.G. & Dockray, G.J. 1984. Sensory substance P innervation of the stomach and pancreas. Demonstration of capsaicin-sensitive sensory neurons in the rat by combined immunohistochemistry and retrograde tracing. Gastroenterology 87, 914-921.
63. Smid, S.D., Young, R.L., Cooper, N.J. & Blackshaw, L.A. 2001. GABA(B)R expressed on vagal afferent neurones inhibit gastric mechanosensitivity in ferret proximal stomach. Am J Physiol Gastrointest Liver Physiol 281, G1494-G1501.
64. Smith, G.P., Jerome, C., Cushin, B.J., Eterno, R. & Simansky, K.J. 1981. Abdominal vagotomy blocks the satiety effect of cholecystokinin in the rat. Science 213, 1036-1037.
65. Smith, G.P., Jerome, C. & Norgren, R. 1985. Afferent axons in abdominal vagus mediate satiety effect of cholecystokinin in rats. Am J Physiol 249, R638-R641.
66. South, E.H. & Ritter, R.C. 1988. Capsaicin application to central or peripheral vagal fibers attenuates CCK satiety. Peptides 9, 601-612.
67. Wang, Y.H., Tache, Y., Sheibel, A.B., Go, V.L. & Wei, J.Y. 1997. Two types of leptin-responsive gastric vagal afferent terminals: an in vitro single-unit study in rats. Am J Physiol 273, R833-R837.
68. Wang, P.Y., Caspi, L., Lam, C.K., Chari, M., Li, X., Light, P.E., Gutierrez-Juarez, R., Ang, M., Schwartz, G.J. & Lam, T.K. 2008. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 452, 1012-1016.
69. Williams, D.L., Baskin, D.G. & Schwartz, M.W. 2009. Hindbrain leptin receptor stimulation enhances the anorexic response to cholecystokinin. Am J Physiol Regul Integr Comp Physiol 297, R1238-R1246.
70. Zeeni, N., Chaumontet, C., Moyse, E., Fromentin, G., Tardivel, C., Tome, D., Jean, A. & Darcel, N. 2009. A positive change in energy balance modulates TrkB expression in the hypothalamus and nodose ganglia of rats. Brain Res 1289, 49-55.
71. Zhang, X., Ji, R.R., Arvidsson, J., Lundberg, J.M., Bartfai, T., Bedecs, K. & Hokfelt, T. 1996. Expression of peptides, nitric oxide synthase and NPY receptor in trigeminal and nodose ganglia after nerve lesions. Exp Brain Res 111, 393-404.
72. Zhang, X., Shi, T., Holmberg, K., Landry, M., Huang, W., Xiao, H., Ju, G. & Hokfelt, T. 1997. Expression and regulation of the neuropeptide Y Y2 receptor in sensory and autonomic ganglia. Proc Natl Acad Sci USA 94, 729-734.
73. Zhao, H., Sprunger, L.K. & Simasko, S.M. 2010. Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat. Am J Physiol Gastrointest Liver Physiol 298, G212-G221.
74. Zhuo, H., Ichikawa, H. & Helke, C.J. 1997. Neurochemistry of the nodose ganglion. Prog Neurobiol 52, 79-107.