Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse

Journal of Physiology

Volumn 589, Issue 11, 2011, Pages 2857-2870

  Daly, Donna M ^a   Park, Sung Jin ^a   Valinsky, William C ^a   Beyak, Michael J ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CHOLECYSTOKININ; GLUCOSE; SEROTONIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEEDING; GLUCOSE BLOOD LEVEL; INTESTINE AFFERENT NERVE; INTRAABDOMINAL FAT; JEJUNUM; LIPID DIET; MALE; MOUSE; NERVE CELL; NERVE EXCITABILITY; NODOSE GANGLION; NONHUMAN; OBESITY; PATCH CLAMP; PRIORITY JOURNAL; SATIETY; SENSORY NERVE; VAGAL AFFERENT; WEIGHT GAIN;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CALCIUM SIGNALING; CHOLECYSTOKININ; DIETARY FATS; ELECTRIC IMPEDANCE; INTESTINES; INTRA-ABDOMINAL FAT; JEJUNUM; MALE; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; NEURONS; NODOSE GANGLION; OBESITY; PATCH-CLAMP TECHNIQUES; SATIETY RESPONSE; SEROTONIN; VAGUS NERVE;

EID: 79957859217     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.204594     Document Type: Article

References (53)

1. Abbott CR, Monteiro M, Small CJ, Sajedi A, Smith KL, Parkinson JR, Ghatei MA & Bloom SR (2005). The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Res 1044, 127-131.
2. Avenell A, Sattar N & Lean M (2006). ABC of obesity. Management: Part I - behaviour change, diet, and activity. BMJ 333, 740-743.
3. Berthoud HR (2008). Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterol Motil 20(Suppl 1), 64-72.
4. Beyak MJ, Bulmer DC, Sellers D & Grundy D (2009). Impairment of rectal afferent mechanosensitivity in experimental diabetes in the rat. Neurogastroenterol Motil 21, 678-681.
5. + currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 287, G845-G855.
6. Booth CE, Shaw J, Hicks GA, Kirkup AJ, Winchester W & Grundy D (2008). Influence of the pattern of jejunal distension on mesenteric afferent sensitivity in the anaesthetized rat. Neurogastroenterol Motil 20, 149-158.
7. Brierley SM (2010). Molecular basis of mechanosensitivity. Auton Neurosci 153, 58-68.
8. Bucinskaite V, Tolessa T, Pedersen J, Rydqvist B, Zerihun L, Holst JJ & Hellstrom PM (2009). Receptor-mediated activation of gastric vagal afferents by glucagon-like peptide-1 in the rat. Neurogastroenterol Motil 21, 978-e78.
9. Burdyga G, Varro A, Dimaline R, Thompson DG & Dockray GJ (2010). Expression of cannabinoid CB1 receptors by vagal afferent neurons: kinetics and role in influencing neurochemical phenotype. Am J Physiol Gastrointest Liver Physiol 299, G63-G69.
10. Canadian Community Health Survey (2005). xxxx. Statistics Canada.
11. Camilleri M (2009). Peripheral mechanisms in the control of appetite and related experimental therapies in obesity. Regul Pept 156, 24-27.
12. Carr MJ (2005). Chemical transduction in vagal afferent endings. In Advances in Vagal Afferent Neurobiology, ed. Unden B & Weinreich D, pp. 167-189. CRC Press, Boca Raton .
13. Cheung GW, Kokorovic A, Lam CK, Chari M & Lam TK (2009). Intestinal cholecystokinin controls glucose production through a neuronal network. Cell Metab 10, 99-109.
14. Collins S, Martin TL, Surwit RS & Robidoux J (2004). Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol Behav 81, 243-248.
15. Covasa M, Grahn J & Ritter RC (2000a). High fat maintenance diet attenuates hindbrain neuronal response to CCK. Regul Pept 86, 83-88.
16. Covasa M, Grahn J & Ritter RC (2000b). Reduced hindbrain and enteric neuronal response to intestinal oleate in rats maintained on high-fat diet. Auton Neurosci 84, 8-18.
17. Covasa M & Ritter RC (1998). Rats maintained on high-fat diets exhibit reduced satiety in response to CCK and bombesin. Peptides 19, 1407-1415.
18. Covasa M & Ritter RC (1999). Reduced sensitivity to the satiation effect of intestinal oleate in rats adapted to high-fat diet. Am J Physiol Regul Integr Comp Physiol 277, R279-R285.
19. Cummings DE & Overduin J (2007). Gastrointestinal regulation of food intake. J Clin Invest 117, 13-23.
20. De Lartigue G, Dimaline R, Varro A, Raybould H, De la Serre CB & Dockray GJ (2010a). Cocaine- and amphetamine-regulated transcript mediates the actions of cholecystokinin on rat vagal afferent neurons. Gastroenterology 138, 1479-1490.
21. De Lartigue G, Lur G, Dimaline R, Varro A, Raybould H & Dockray GJ (2010b). EGR1 is a target for cooperative interactions between cholecystokinin and leptin, and inhibition by ghrelin, in vagal afferent neurons. Endocrinology 151, 3589-3599.
22. Dockray GJ (2009). The versatility of the vagus. Physiol Behav 97, 531-536.
23. Dockray GJ & Burdyga G (2011). Plasticity in vagal afferent neurones during feeding and fasting: mechanisms and significance. Acta Physiol (Oxf) 201, 313-321.
24. Donovan MJ, Paulino G & Raybould HE (2009). Activation of hindbrain neurons in response to gastrointestinal lipid is attenuated by high fat, high energy diets in mice prone to diet-induced obesity. Brain Res 1248, 136-140.
25. Fox EA, Phillips RJ, Baronowsky EA, Byerly MS, Jones S & Powley TL (2001). Neurotrophin-4 deficient mice have a loss of vagal intraganglionic mechanoreceptors from the small intestine and a disruption of short-term satiety. J Neurosci 21, 8602-8615.
26. Fox EA, Phillips RJ, Byerly MS, Baronowsky EA, Chi MM & Powley TL (2002). Selective loss of vagal intramuscular mechanoreceptors in mice mutant for steel factor, the c-Kit receptor ligand. Anat Embryol (Berl) 205, 325-342.
27. Gallou-Kabani C, Vige A, Gross MS, Boileau C, Rabes JP, Fruchart-Najib J, Jais JP & Junien C (2007). Resistance to high-fat diet in the female progeny of obese mice fed a control diet during the periconceptual, gestation, and lactation periods. Am J Physiol Endocrinol Metab 292, E1095-E1100.
28. Grundy D, Hillsley K, Kirkup AJ & Richards W (1998). Mesenteric afferent sensitivity to cholecystokinin and 5-hydroxytryptamine. Dtsch Tierarztl Wochenschr 105, 466-468.
29. Hayes MR & Covasa M (2005). CCK and 5-HT act synergistically to suppress food intake through simultaneous activation of CCK-1 and 5-HT3 receptors. Peptides 26, 2322-2330.
30. Hillsley K & Grundy D (1998). Serotonin and cholecystokinin activate different populations of rat mesenteric vagal afferents. Neurosci Lett 255, 63-66.
31. Hillsley K, Kirkup AJ & Grundy D (1998). Direct and indirect actions of 5-hydroxytryptamine on the discharge of mesenteric afferent fibres innervating the rat jejunum. J Physiol 506, 551-561.
32. Lal S, Kirkup AJ, Brunsden AM, Thompson DG & Grundy D (2001). Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol 281, G907-G915.
33. 2+ signal transduction in vagal nodose ganglia. Am J Physiol Gastrointest Liver Physiol 282, G1002-G1008.
34. Lean M & Finer N (2006). ABC of obesity. Management: part II - drugs. BMJ 333, 794-797.
35. Lin S, Storlien LH & Huang XF (2000a). Leptin receptor, NPY, POMC mRNA expression in the diet-induced obese mouse brain. Brain Res 875, 89-95.
36. Lin S, Thomas TC, Storlien LH & Huang XF (2000b). Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes Relat Metab Disord 24, 639-646.
37. Moran TH, Baldessarini AR, Salorio CF, Lowery T & Schwartz GJ (1997). Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am J Physiol Regul Integr Comp Physiol 272, R1245-R1251.
38. 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.
39. Obrosova IG, Ilnytska O, Lyzogubov VV, Pavlov IA, Mashtalir N, Nadler JL & Drel VR (2007). High-fat diet induced neuropathy of pre-diabetes and obesity: effects of "healthy" diet and aldose reductase inhibition. Diabetes 56, 2598-2608.
40. Paulino G, Barbier de la Serre C, Knotts TA, Oort PJ, Newman JW, Adams SH & Raybould HE (2009). Increased expression of receptors for orexigenic factors in nodose ganglion of diet-induced obese rats. Am J Physiol Endocrinol Metab 296, E898-E903.
41. Petro AE, Cotter J, Cooper DA, Peters JC, Surwit SJ & Surwit RS (2004). Fat, carbohydrate, and calories in the development of diabetes and obesity in the C57BL/6J mouse. Metabolism 53, 454-457.
42. Richards W, Hillsley K, Eastwood C & Grundy D (1996). Sensitivity of vagal mucosal afferents to cholecystokinin and its role in afferent signal transduction in the rat. J Physiol 497, 473-481.
43. Rong W, Hillsley K, Davis JB, Hicks G, Winchester WJ & Grundy D (2004). Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J Physiol 560, 867-881.
44. Savastano DM, Carelle M & Covasa M (2005). Serotonin-type 3 receptors mediate intestinal Polycose- and glucose-induced suppression of intake. Am J Physiol Regul Integr Comp Physiol 288, R1499-R1508.
45. Schwartz GJ, Berkow G, McHugh PR & Moran TH (1993). Gastric branch vagotomy blocks nutrient and cholecystokinin-induced suppression of gastric emptying. Am J Physiol Regul Integr Comp Physiol 264, R630-R637.
46. Shields M & Tjepkema M (2006). Trends in Adult Obesity. Health Reports 17, 53-59.
47. Stewart T, Beyak MJ & Vanner S (2003). Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol 552, 797-807.
48. Surwit RS, Feinglos MN, Rodin J, Sutherland A, Petro AE, Opara EC, Kuhn CM & Rebuffe-Scrive M (1995). Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metabolism 44, 645-651.
49. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA & Feinglos MN (1988). Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37, 1163-1167.
50. Talsania T, Anini Y, Siu S, Drucker DJ & Brubaker PL (2005). Peripheral exendin-4 and peptide YY(3-36) synergistically reduce food intake through different mechanisms in mice. Endocrinology 146, 3748-3756.
51. Vahl TP, Tauchi M, Durler TS, Elfers EE, Fernandes TM, Bitner RD, Ellis KS, Woods SC, Seeley RJ, Herman JP & D'Alessio DA (2007). Glucagon-like peptide-1 (GLP-1) receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats. Endocrinology 148, 4965-4973.
52. Wang PY, Caspi L, Lam CK, Chari M, Li X, Light PE, Gutierrez-Juarez R, Ang M, Schwartz GJ & Lam TK (2008). Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 452, 1012-1016.
53. Zhu JX, Zhu XY, Owyang C & Li Y (2001). Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J Physiol 530, 431-442.