Gastric vagal afferent modulation by leptin is influenced by food intake status

Journal of Physiology

Volumn 591, Issue 7, 2013, Pages 1921-1934

  Kentish, Stephen J ^b   O'Donnell, Tracey A ^a   Isaacs, Nicole J ^b   Young, Richard L ^a,b,c   Li, Hui ^b   Harrington, Andrea M ^a,b   Brierley, Stuart M ^a,b,c   Wittert, Gary A ^b   Blackshaw, L Ashley ^b,d   Page, Amanda J ^a,b,c  

^a ROYAL ADELAIDE HOSPITAL   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LEPTIN; LEPTIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; TRANSIENT RECEPTOR POTENTIAL CHANNEL C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; FEMALE; FOOD INTAKE; GASTRIC VAGAL AFFERENT; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NERVE CONDUCTION; NERVE ENDING; NEUROMODULATION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STOMACH INNERVATION; TACTILE STIMULATION;

ANIMALS; DIET, HIGH-FAT; EATING; FEMALE; GASTRIC MUCOSA; LEPTIN; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH; NODOSE GANGLION; OBESITY; RECEPTORS, LEPTIN; VAGUS NERVE;

EID: 84875638215     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.247577     Document Type: Article

References (51)

1. Bado A, Levasseur S, Attoub S, Kermorgant S, Laigneau J, Bortoluzzi MI, Moizo L, Lehy T, Guerre-Millo M, Le Marchand-Brustel Y & Lewin MJM (1998). The stomach is a source of leptin. Nature 394, 790-793.
2. Barrachina MD, Martinez V, Wang L, Wei JY & Tache Y (1997). Synergistic interaction between leptin and cholecystokinin to reduce short-term food intake in lean mice. Proc Natl Acad Sci U S A 94, 10455-10460.
3. Becker JM & Kelly KA (1983). Antral control of canine gastric emptying of solids. Am J Physiol Gastrointest Liver Physiol 8, 334-338.
4. Blackshaw LA, Grundy D & Scratcherd T (1987). Vagal afferent discharge from gastric mechanoreceptors during contraction and relaxation of the ferret corpus. J Auton Nerv Syst 18, 19-24.
5. Burdyga G, Spiller D, Morris R, Lal S, Thompson DG, Saeed S, Dimaline R, Varro A & Dockray GJ (2002). Expression of the leptin receptor in rat and human nodose ganglion neurones. Neuroscience 109, 339-357.
6. Buyse M, Ovesjö M-L, Goïot H, Guilmeau S, Péranzi G, Moizo L, Walker F, Lewin MJM, 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.
7. Campbell MD, Subramaniam S, Kotlikoff MI, Williamson JR & Fluharty SJ (1990). Cyclic AMP inhibits inositol polyphosphate production and calcium mobilization in neuroblastoma x glioma NG1 08-15 cells. Mol Pharmacol 38, 282-288.
8. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, et al (1996). Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334, 292-295.
9. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD & Low MJ (2001). Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411, 480-484.
10. Daly DM, Park SJ, Valinsky WC & Beyak MJ (2011). Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol 589, 2857-2870.
11. de Lartigue G, Barbier de la Serre C, Espero E, Lee J & Raybould HE (2011a). Diet-induced obesity leads to the development of leptin resistance in vagal afferent neurons. Am J Physiol Endocrinol Metab 301, E187-E195.
12. de Lartigue G, Barbier de la Serre C, Espero E, Lee J & Raybould HE (2012). Leptin resistance in vagal afferent neurons inhibits cholecystokinin signaling and satiation in diet induced obese rats. PLoS One 7, e32967.
13. de Lartigue G, de La Serre CB & Raybould HE (2011b). Vagal afferent neurons in high fat diet-induced obesity; intestinal microflora, gut inflammation and cholecystokinin. Phyiol Behav 105, 100-105.
14. de Lartigue G, Lur G, Dimaline R, Varro A, Raybould H & Dockray GJ (2010). EGR1 is a target for cooperative interactions between cholecystokinin and leptin, and inhibition by ghrelin, in vagal afferent neurons. Endocrinology 151, 3589-3599.
15. Dietrich A, Kalwa H, Storch U, Schnitzler MM, Salanova B, Pinkenburg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L & Gudermann T (2007). Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 455, 465-477.
16. Farley C, Cook JA, Spar BD, Austin TM & Kowalski TJ (2003). Meal pattern analysis of diet-induced obesity in susceptible and resistant rats. Obesity 11, 845-851.
17. Frederich RC, Hamann A, Anderson S, Löllmann B, Lowell BB & Flier JS (1995). Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med 1, 1311-1314.
18. Harvey J, McKenna F, Herson PS, Spanswick D & Ashford ML (1997). Leptin activates ATP-sensitive potassium channels in the rat insulin-secreting cell line, CRI-G1. J Physiol 504, 527-535.
19. Hill JW, Williams KW, Ye C, Luo J, Balthasar N, Coppari R, Cowley MA, Cantley LC, Lowell BB & Elmquist JK (2008). Acute effects of leptin require PI3K signaling in hypothalamic proopiomelanocortin neurons in mice. J Clin Invest 118, 1796-1805.
20. Hughes PA, Brierley SM, Young RL & Blackshaw LA (2007). Localization and comparative analysis of acid-sensing ion channel (ASIC1, 2, and 3) mRNA expression in mouse colonic sensory neurons within thoracolumbar dorsal root ganglia. J Comp Neurol 500, 863-875.
21. Jiang L, Li Z & Rui L (2008). Leptin stimulates both JAK2-dependent and JAK2-independent signaling pathways. J Biol Chem 283, 28066-28073.
22. Kentish S, Li H, Philp LK, O'Donnell TA, Isaacs NJ, Young RL, Wittert GA, Blackshaw LA & Page AJ (2012). Diet-induced adaptation of vagal afferent function. J Physiol 590, 209-221.
23. Kressel M (1998). Tyramide amplification allows anterograde tracing by horseradish peroxidase-conjugated lectins in conjunction with simultaneous immunohistochemistry. J Histochem Cytochem 46, 527-533.
24. Lievremont JP, Bird GS & Putney JW Jr (2005). Mechanism of inhibition of TRPC cation channels by 2- aminoethoxydiphenylborane. Molec Pharmacol 68, 758-762.
25. Liu Z, Qiu YH, Li B, Ma SH & Peng YP (2011). Neuroprotection of interleukin-6 against NMDA-induced apoptosis and its signal-transduction mechanisms. Neurotox Res 19, 484-495.
26. Mix H, Widjaja A, Jandl O, Cornberg M, Kaul A, Göke M, Beil W, Kuske M, Brabant G, Manns MP & Wagner S (2000). Expression of leptin and leptin receptor isoforms in the human stomach. Gut 47, 481-486.
27. Morrison CD, Morton GJ, Niswender KD, Gelling RW & Schwartz MW (2005). Leptin inhibits hypothalamic Npy and Agrp gene expression via a mechanism that requires phosphatidylinositol 3-OH-kinase signaling. Am J Physiol Endocrinol Metab 289, 1051-1057.
28. Owyang C & Heldsinger A (2011). Vagal control of satiety and hormonal regulation of appetite. J Neurogastroenterol Motil 17, 338-348.
29. Page AJ, Martin CM & Blackshaw LA (2002). Vagal mechanoreceptors and chemoreceptors in mouse stomach and esophagus. J Neurophysiol 87, 2095-2103.
30. Page AJ, O'Donnell T, Cooper NJ, Young RL & Blackshaw LA (2009). Nitric oxide as an endogenous peripheral modulator of visceral sensory neuronal function. J Neurosci 29, 7246-7255.
31. Peiser C, Springer J, Groneberg DA, McGregor GP, Fischer A & Lang RE (2002). Leptin receptor expression in nodose ganglion cells projecting to the rat gastric fundus. Neurosci Lett 320, 41-44.
32. Peters JH, Karpiel AB, Ritter RC & Simasko SM (2004). Cooperative activation of cultured vagal afferent neurons by leptin and cholecystokinin. Endocrinology 145, 3652-3657.
33. Peters JH, McKay BM, Simasko SM & Ritter RC (2005). Leptin- induced satiation mediated by abdominal vagal afferents. Am J Physiol Regul Integr Comp Physiol 288, 879-884.
34. Peters JH, Ritter RC & Simasko SM (2006). Leptin and CCK selectively activate vagal afferent neurons innervating the stomach and duodenum. Am J Physiol Regul Integr Comp Physiol 290, 1544-1549.
35. Pfaffl MW, Horgan GW & Dempfle L (2002). Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, e36.
36. Powley TL & Phillips RJ (2004). Gastric satiation is volumetric, intestinal satiation is nutritive. Physiol Behav 82, 69-74.
37. Qiu J, Fang Y, Rønnekleiv OK & Kelly MJ (2010). Leptin excites proopiomelanocortin neurons via activation of TRPC channels. J Neurosci 30, 1560-1565.
38. Raybould HE & Tache Y (1988). Cholecystokinin inhibits gastric motility and emptying via a capsaicin-sensitive vagal pathway in rats. Am J Physiol Gastrointest Liver Physiol 255, G242-G246.
39. Rogers RC & Hermann GE (2008). Mechanisms of action of CCK to activate central vagal afferent terminals. Peptides 29, 1716-1725.
40. + channels. Nat Neurosci 5, 299-300.
41. Shyu KG, Wang BW, Chen WJ, Kuan P & Hung CR (2010). Mechanism of the inhibitory effect of atorvastatin on endoglin expression induced by transforming growth factor-beta1 in cultured cardiac fibroblasts. Eur J Heart Failure 12, 219-226.
42. Speakman JR, Levitsky DA, Allison DB, Bray MS, de Castro JM, Clegg DJ, Clapham JC, Dulloo AG, Gruer L, Haw S, Hebebrand J, Hetherington MM, Higgs S, Jebb SA, Loos RJ, Luckman S, Luke A, Mohammed-Ali V, O'Rahilly S, Pereira M, Perusse L, Robinson TN, Rolls B, Symonds ME & Westerterp-Plantenga MS (2011). Set points, settling points and some alternative models: theoretical options to understand how genes and environments combine to regulate body adiposity. Dis Mod Mech 4, 733-745.
43. Wang G, Tomasi D, Backus W, Wang R, Telang F, Geliebter A, Korner J, Bauman A, Fowler JS, Thanos PK & Volkow ND (2008a). Gastric distention activates satiety circuitry in the human brain. Neuroimage 39, 1824-1831.
44. Wang GJ, Tomasi D, Backus W, Wang R, Telang F, Geliebter A, Korner J, Bauman A, Fowler JS, Thanos PK & Volkow ND (2008b). Gastric distention activates satiety circuitry in the human brain. NeuroImage 39, 1824-1831.
45. Williams JL Jr & Malik KU (1990). Forskolin stimulates prostaglandin synthesis in rabbit heart by a mechanism that requires calcium and is independent of cyclic AMP. Circ Res 67, 1247-1256.
46. Williams KW, Zsombok A & Smith BN (2007). Rapid inhibition of neurons in the dorsal motor nucleus of the vagus by leptin. Endocrinology 148, 1868-1881.
47. + channels in cerebellar Purkinje neurons. Eur J Neurosci 16, 1214-1222.
48. Yada Y, Nagao S, Okano Y & Nozawa Y (1989). Inhibition by cyclic AMP of guanine nucleotide-induced activation of phosphoinositide-specific phospholipase C in human platelets. FEBS Lett 242, 368-372.
49. Yannakoulia M, Yiannakouris N, Bluher S, Matalas AL, Klimis-Zacas D & Mantzoros CS (2003). Body fat mass and macronutrient intake in relation to circulating soluble leptin receptor, free leptin index, adiponectin, and resistin concentrations in healthy humans. J Clin Endocrinol Metab 88, 1730-1736.
50. Zhoa AZ, Huan J, Gupta S, Pal R & Sahu A (2002). A phosphatidylinositol 3-kinase-phosphodiesterase 3B-cyclic AMP pathway in hypothalamic action of leptin on feeding. Nat Neurosci 5, 727-728.
51. Zhoa H, Sprunger LK & Simasko SM (2009). 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.