Ghrelin prevents levodopa-induced inhibition of gastric emptying and increases circulating levodopa in fasted rats

Neurogastroenterology and Motility

Volumn 24, Issue 5, 2012, Pages

  Wang, L ^a   Murphy, N P ^b   Stengel, A ^a   Goebel Stengel, M ^a   St Pierre, D H ^c   Maidment, N T ^b   Tache Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Dopamine; Gastric emptying; Ghrelin; Levodopa; Rats

Indexed keywords

DOPAMINE; GHRELIN; LEVODOPA; METHYLCELLULOSE; PHENOLSULFONPHTHALEIN; PROTEIN FOS; RECOMBINANT GHRELIN; RECOMBINANT HORMONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; DRUG BLOOD LEVEL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIOIMMUNOASSAY; RAT; STOMACH EMPTYING;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; CATHETERIZATION; DOPAMINE; DOPAMINE AGENTS; FASTING; GASTRIC EMPTYING; GENE EXPRESSION; GENES, FOS; GHRELIN; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; INTUBATION, GASTROINTESTINAL; LEVODOPA; MALE; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84862809496     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2012.01904.x     Document Type: Article

References (72)

1. Poewe W, Antonini A, Zijlmans JC, Burkhard PR, Vingerhoets F. Levodopa in the treatment of Parkinson's disease: an old drug still going strong. Clin Interv Aging 2010; 5: 229-38.
2. Gottwald MD, Aminoff MJ. Therapies for dopaminergic-induced dyskinesias in parkinson disease. Ann Neurol 2011; 69: 919-27.
3. Robertson DR, Renwick AG, Macklin B et al. The influence of levodopa on gastric emptying in healthy elderly volunteers. Eur J Clin Pharmacol 1992; 42: 409-12.
4. Waller DG, Roseveare C, Renwick AG, Macklin B, George CF. Gastric emptying in healthy volunteers after multiple doses of levodopa. Br J Clin Pharmacol 1991; 32: 691-5.
5. Tazawa S, Masuda N, Koizumi T, Kitazawa M, Nakane T, Miyata H. KDR-5169, a new gastrointestinal prokinetic agent, enhances gastric contractile and emptying activities in dogs and rats. Eur J Pharmacol 2002; 434: 169-76.
6. Hardoff R, Sula M, Tamir A et al. Gastric emptying time and gastric motility in patients with Parkinson's disease. Mov Disord 2001; 16: 1041-7.
7. Nyholm D, Lennernas H. Irregular gastrointestinal drug absorption in Parkinson's disease. Expert Opin Drug Metab Toxicol 2008; 4: 193-203.
8. Muller T, Erdmann C, Bremen D et al. Impact of gastric emptying on levodopa pharmacokinetics in Parkinson disease patients. Clin Neuropharmacol 2006; 29: 61-7.
9. Djaldetti R, Baron J, Ziv I, Melamed E. Gastric emptying in Parkinson's disease: patients with and without response fluctuations. Neurology 1996; 46: 1051-4.
10. Asai H, Udaka F, Hirano M et al. Increased gastric motility during 5-HT4 agonist therapy reduces response fluctuations in Parkinson's disease. Parkinsonism Relat Disord 2005; 11: 499-502.
11. Quigley EM. Cisapride: what can we learn from the rise and fall of a prokinetic? J Dig Dis 2011; 12: 147-56.
12. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999; 402: 656-60.
13. Stengel A, Goebel M, Wang L, Tache Y. Ghrelin, des-acyl ghrelin and nesfatin-1 in gastric X/A-like cells: role as regulators of food intake and body weight. Peptides 2010; 31: 357-69.
14. Masuda Y, Tanaka T, Inomata N et al. Ghrelin stimulates gastric acid secretion and motility in rats. Biochem Biophys Res Commun 2000; 276: 905-8.
15. Kitazawa T, De Smet B, Verbeke K, Depoortere I, Peeters TL. Gastric motor effects of peptide and non-peptide ghrelin agonists in mice in vivo and in vitro. Gut 2005; 54: 1078-84.
16. Zheng J, Ariga H, Taniguchi H, Ludwig K, Takahashi T. Ghrelin regulates gastric phase III-like contractions in freely moving conscious mice. Neurogastroenterol Motil 2009; 21: 78-84.
17. Nakamura T, Onaga T, Kitazawa T. Ghrelin stimulates gastric motility of the guinea pig through activation of a capsaicin-sensitive neural pathway: in vivo and in vitro functional studies. Neurogastroenterol Motil 2010; 22: 446-52.
18. Tack J, Depoortere I, Bisschops R et al. Influence of ghrelin on interdigestive gastrointestinal motility in humans. Gut 2006; 55: 327-33.
19. Levin F, Edholm T, Schmidt PT et al. Ghrelin stimulates gastric emptying and hunger in normal-weight humans. J Clin Endocrinol Metab 2006; 91: 3296-302.
20. Murray CD, Martin NM, Patterson M et al. Ghrelin enhances gastric emptying in diabetic gastroparesis: a double blind, placebo controlled, crossover study. Gut 2005; 54: 1693-8.
21. Trudel L, Tomasetto C, Rio MC et al. Ghrelin/motilin-related peptide is a potent prokinetic to reverse gastric postoperative ileus in rat. Am J Physiol Gastrointest Liver Physiol 2002; 282: G948-52.
22. Trudel L, Bouin M, Tomasetto C et al. Two new peptides to improve post-operative gastric ileus in dog. Peptides 2003; 24: 531-4.
23. Stengel A, Tache Y. Ghrelin: new insight to mechanisms and treatment of postoperative gastric ileus. Curr Pharm Des 2011; 17: 1587-93.
24. Sallam HS, Oliveira HM, Liu S, Chen JD. Mechanisms of burn-induced impairment in gastric slow waves and emptying in rats. Am J Physiol Regul Integr Comp Physiol 2010; 299: R298-305.
25. De SB, Thijs T, Moechars D et al. Endogenous and exogenous ghrelin enhance the colonic and gastric manifestations of dextran sodium sulphate-induced colitis in mice. Neurogastroenterol Motil 2009; 21: 59-70.
26. Wang L, Basa NR, Shaikh A et al. LPS inhibits fasted plasma ghrelin levels in rats: role of IL-1 and PGs and functional implications. Am J Physiol Gastrointest Liver Physiol 2006; 291: G611-20.
27. Gourcerol G, Wang L, Million M, Adelson DW, Tanaka T, Tache Y. Peripheral urocortin 2 blocks the gastric motility activation induced by ghrelin. Gastroenterology 2008;134:A-90 (Abstract).
28. Stengel A, Keire D, Goebel M et al. The RAPID method for blood processing yields new insight in plasma concentrations and molecular forms of circulating gut peptides. Endocrinology 2009; 150: 5113-8.
29. Stengel A, Goebel M, Luckey A, Yuan PQ, Wang L, Tache Y. Cold ambient temperature reverses abdominal surgery-induced delayed gastric emptying and decreased plasma ghrelin levels in rats. Peptides 2010; 31: 2229-35.
30. Stengel A, Goebel-Stengel M, Wang L et al. Central administration of pan-somatostatin agonist ODT8-SST prevents abdominal surgery-induced inhibition of circulating ghrelin, food intake and gastric emptying in rats. Neurogastroenterol Motil 2011; 23: e294-308.
31. Ebihara K, Ishida Y, Takeda R et al. Differential expression of FosB, c-Fos, and Zif268 in forebrain regions after acute or chronic L-DOPA treatment in a rat model of Parkinson's disease. Neurosci Lett 2011; 496: 90-4.
32. Shimamura M, Shimizu M, Yagami T et al. L-3, 4-dihydroxyphenylalanine-induced c-Fos expression in the CNS under inhibition of central aromatic L-amino acid decarboxylase. Neuropharmacology 2006; 50: 909-16.
33. Martinez V, Rivier J, Wang L, Tache Y. Central injection of a new corticotropin-releasing factor (CRF) antagonist, astressin, blocks CRF- and stress-related alterations of gastric and colonic motor function. J Pharmacol Exp Ther 1997; 280: 754-60.
34. Paxinos G, Watson C. The Rat Brain In Stereotaxic Coordinates, 6th edn. Orlando: Academic Press, 2007.
35. Wang L, Martinez V, Larauche M, Tache Y. Proximal colon distension induces Fos expression in oxytocin-, vasopressin-, CRF- and catecholamines-containing neurons in rat brain. Brain Res 2009; 1247: 79-91.
36. Bredberg E, Lennernas H, Paalzow L. Pharmacokinetics of levodopa and carbidopa in rats following different routes of administration. Pharm Res 1994; 11: 549-55.
37. Kaenmaki M, Tammimaki A, Garcia-Horsman JA et al. Importance of membrane-bound catechol-O-methyltransferase in L-DOPA metabolism: a pharmacokinetic study in two types of Comt gene modified mice. Br J Pharmacol 2009; 158: 1884-94.
38. Djaldetti R, Ziv I, Melamed E. Impaired absorption of oral levodopa: a major cause for response fluctuations in Parkinson's disease. Isr J Med Sci 1996; 32: 1224-7.
39. Fernandez N, Garcia JJ, Diez MJ et al. Effects of slowed gastrointestinal motility on levodopa pharmacokinetics. Auton Neurosci 2010; 156: 67-72.
40. Kashyap P, Micci MA, Pasricha S, Pasricha PJ. The D2/D3 agonist PD128907 (R-(+)-trans-3, 4a, 10b-tetrahydro-4-propyl-2H, 5H-[1]benzopyrano[4, 3-b]-1, 4-oxazin- 9-ol) inhibits stimulated pyloric relaxation and spontaneous gastric emptying. Dig Dis Sci 2009; 54: 57-62.
41. Yoshikawa T, Yoshida N. The possible involvement of dopamine D3 receptors in the regulation of gastric emptying in rats. Life Sci 2010; 87: 638-42.
42. Kusunoki M, Taniyama K, Tanaka C. Dopamine regulation of [3H]acetylcholine release from guinea-pig stomach. J Pharmacol Exp Ther 1985; 234: 713-9.
43. Tonini M, Cipollina L, Poluzzi E, Crema F, Corazza GR, De PF. Review article: clinical implications of enteric and central D2 receptor blockade by antidopaminergic gastrointestinal prokinetics. Aliment Pharmacol Ther 2004; 19: 379-90.
44. de la Cour CD, Norlen P, Hakanson R. Secretion of ghrelin from rat stomach ghrelin cells in response to local microinfusion of candidate messenger compounds: a microdialysis study. Regul Pept 2007; 143: 118-26.
45. Iwakura H, Ariyasu H, Hosoda H et al. Oxytocin and dopamine stimulate ghrelin secretion by the ghrelin-producing cell line, MGN3-1 in vitro. Endocrinology 2011; 152: 2619-25.
46. Dhasmana KM, Villalon CM, Zhu YN, Parmar SS. The role of dopamine (D2), alpha and beta-adrenoceptor receptors in the decrease in gastrointestinal transit induced by dopamine and dopamine-related drugs in the rat. Pharmacol Res 1993; 27: 335-47.
47. Tumer C, Oflazoglu HD, Obay BD, Kelle M, Tasdemir E. Effect of ghrelin on gastric myoelectric activity and gastric emptying in rats. Regul Pept 2008; 146: 26-32.
48. Depoortere I, De Winter B, Thijs T, De Man J, Pelckmans P, Peeters T. Comparison of the gastroprokinetic effects of ghrelin, GHRP-6 and motilin in rats in vivo and in vitro. Eur J Pharmacol 2005; 515: 160-8.
49. Fujino K, Inui A, Asakawa A, Kihara N, Fujimura M, Fujimiya M. Ghrelin induces fasted motor activity of the gastrointestinal tract in conscious fed rats. J Physiol 2003; 550: 227-40.
50. Akamizu T, Takaya K, Irako T et al. Pharmacokinetics, safety, and endocrine and appetite effects of ghrelin administration in young healthy subjects. Eur J Endocrinol 2004; 150: 447-55.
51. Wang L, Saint-Pierre DH, Tache Y. Peripheral ghrelin selectively increases Fos expression in neuropeptide Y - synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett 2002; 325: 47-51.
52. Camilleri M, Papathanasopoulos A, Odunsi ST. Actions and therapeutic pathways of ghrelin for gastrointestinal disorders. Nat Rev Gastroenterol Hepatol 2009; 6: 343-52.
53. De SB, Mitselos A, Depoortere I. Motilin and ghrelin as prokinetic drug targets. Pharmacol Ther 2009; 123: 207-23.
54. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 2006; 494: 528-48.
55. Dass NB, Munonyara M, Bassil AK et al. Growth hormone secretagogue receptors in rat and human gastrointestinal tract and the effects of ghrelin. Neuroscience 2003; 120: 443-53.
56. Jiang H, Li LJ, Wang J, Xie JX. Ghrelin antagonizes MPTP-induced neurotoxicity to the dopaminergic neurons in mouse substantia nigra. Exp Neurol 2008; 212: 532-7.
57. Moon M, Kim HG, Hwang L et al. Neuroprotective effect of ghrelin in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease by blocking microglial activation. Neurotox Res 2009; 15: 332-47.
58. Bassil AK, Dass NB, Sanger GJ. The prokinetic-like activity of ghrelin in rat isolated stomach is mediated via cholinergic and tachykininergic motor neurones. Eur J Pharmacol 2006; 544: 146-52.
59. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 1989; 283: 248-68.
60. Herbert H, Moga MM, Saper CB. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 1990; 293: 540-80.
61. Sawchenko PE, Swanson LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 1982; 257: 275-325.
62. Schwaber JS, Kapp BS, Higgins GA, Rapp PR. Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 1982; 2: 1424-38.
63. Herman MA, Alayan A, Sahibzada N, et al. micro-Opioid receptor stimulation in the medial subnucleus of the tractus solitarius inhibits gastric tone and motility by reducing local GABA activity. Am J Physiol Gastrointest Liver Physiol 2010; 299:G494-506.
64. Sakaguchi T, Sandoh N, Aono T. Glucose signal in the nucleus of the vagus nerve modulates the cyclicity of gastric motility in rats. Brain Res 1994; 641: 163-6.
65. Price CJ, Hoyda TD, Ferguson AV. The area postrema: a brain monitor and integrator of systemic autonomic state. Neuroscientist 2008; 14: 182-94.
66. Date Y, Murakami N, Toshinai K et al. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 2002; 123: 1120-8.
67. 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.
68. Li Y, Wu X, Zhao Y, Chen S, Owyang C. Ghrelin acts on the dorsal vagal complex to stimulate pancreatic protein secretion. Am J Physiol Gastrointest Liver Physiol 2006; 290: G1350-8.
69. Egecioglu E, Jerlhag E, Salome N et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol 2010; 15: 304-11.
70. Jiang H, Betancourt L, Smith RG. Ghrelin amplifies dopamine signaling by cross talk involving formation of growth hormone secretagogue receptor/dopamine receptor subtype 1 heterodimers. Mol Endocrinol 2006; 20: 1772-85.
71. Fukuda H, Mizuta Y, Isomoto H et al. Ghrelin enhances gastric motility through direct stimulation of intrinsic neural pathways and capsaicin-sensitive afferent neurones in rats. Scand J Gastroenterol 2004; 39: 1209-14.
72. Takahashi T, Kurosawa S, Wiley JW, Owyang C. Mechanism for the gastrokinetic action of domperidone in vitro studies in guinea pigs. Gastroenterology 1991; 101: 703-10.