Central administration of pan-somatostatin agonist ODT8-SST prevents abdominal surgery-induced inhibition of circulating ghrelin, food intake and gastric emptying in rats

Neurogastroenterology and Motility

Volumn 23, Issue 7, 2011, Pages

  Stengel, A ^a   Goebel Stengel, M ^a   Wang, L ^a   Luckey, A ^a   Hu, E ^a   Rivier, J ^b   Tache Y ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Acyl ghrelin; Food intake; Gastric emptying; Postoperative gastric ileus; Somatostatin agonist; Somatostatin 28

Indexed keywords

DEXTRO PHENYLALANYLPHENYLALANYLPHENYLALANYL DEXTRO TRYPTOPHYLLYSYLTHREONYLPHENYLALANYLTHREONINAMIDE; GHRELIN; ODT8 SST; S 315 297; S 346 011; S 406 062; SOMATOSTATIN 28; SOMATOSTATIN DERIVATIVE; SOMATOSTATIN RECEPTOR 1; SOMATOSTATIN RECEPTOR 2; SOMATOSTATIN RECEPTOR 4; UNCLASSIFIED DRUG;

ABDOMINAL SURGERY; ANIMAL EXPERIMENT; ARTICLE; BRAIN; FOOD INTAKE; LAPAROTOMY; MALE; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SIGNAL TRANSDUCTION; STOMACH EMPTYING;

ABDOMEN; ANIMALS; BRAIN; CORTICOTROPIN-RELEASING HORMONE; EATING; GASTRIC EMPTYING; GHRELIN; INJECTIONS, INTRAVENTRICULAR; MALE; MODELS, ANIMAL; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SOMATOSTATIN; SOMATOSTATIN-28; STRESS, PSYCHOLOGICAL;

EID: 79959324854     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2011.01721.x     Document Type: Article

References (75)

1. Zeinali F, Stulberg JJ, Delaney CP. Pharmacological management of postoperative ileus. Can J Surg 2009; 52: 153-7.
2. Zittel TT, De Giorgio R, Brecha NC, Sternini C, Raybould HE. Abdominal surgery induces c-fos expression in the nucleus of the solitary tract in the rat. Neurosci Lett 1993; 159: 79-82.
3. Bonaz B, Plourde V, Taché Y. Abdominal surgery induces Fos immunoreactivity in the rat brain. J Comp Neurol 1994; 349: 212-22.
4. Barquist E, Bonaz B, Martinez V, Rivier J, Zinner MJ, Taché Y. Neuronal pathways involved in abdominal surgery-induced gastric ileus in rats. Am J Physiol 1996; 270: R888-94.
5. Bonaz B, Taché Y. Corticotropin-releasing factor and systemic capsaicin-sensitive afferents are involved in abdominal surgery-induced Fos expression in the paraventricular nucleus of the hypothalamus. Brain Res 1997; 748: 12-20.
6. Stengel A, Goebel M, Wang L, Taché Y. Abdominal surgery activates nesfatin-1 immunoreactive brain nuclei in rats. Peptides 2010; 31: 263-70.
7. Luckey A, Livingston E, Taché Y. Mechanisms and treatment of postoperative ileus. Arch Surg 2003; 138: 206-14.
8. Holzer P, Lippe IT, Amann R. Participation of capsaicin-sensitive afferent neurons in gastric motor inhibition caused by laparotomy and intraperitoneal acid. Neuroscience 1992; 48: 715-22.
9. Boeckxstaens GE, Hirsch DP, Kodde A et al. Activation of an adrenergic and vagally-mediated NANC pathway in surgery-induced fundic relaxation in the rat. Neurogastroenterol Motil 1999; 11: 467-74.
10. Naito Y, Fukata J, Tamai S et al. Biphasic changes in hypothalamo-pituitary-adrenal function during the early recovery period after major abdominal surgery. J Clin Endocrinol Metab 1991; 73: 111-7.
11. Gourcerol G, Gallas S, Mounien L et al. Gastric electrical stimulation modulates hypothalamic corticotropin-releasing factor-producing neurons during post-operative ileus in rat. Neuroscience 2007; 148: 775-81.
12. Irwin M, Hauger R, Brown M. Central corticotropin-releasing hormone activates the sympathetic nervous system and reduces immune function: increased responsivity of the aged rat. Endocrinology 1992; 131: 1047-53.
13. Wiersma A, Bohus B, Koolhaas JM. Corticotropin-releasing hormone microinfusion in the central amygdala diminishes a cardiac parasympathetic outflow under stress-free conditions. Brain Res 1993; 625: 219-27.
14. Wang L, Cardin S, Martinez V, Taché Y. Intracerebroventricular CRF inhibits cold restraint-induced c-fos expression in the dorsal motor nucleus of the vagus and gastric erosions in rats. Brain Res 1996; 736: 44-53.
15. Kosoyan HP, Wei JY, Taché Y. Intracisternal sauvagine is more potent than corticotropin-releasing factor to decrease gastric vagal efferent activity in rats. Peptides 1999; 20: 851-8.
16. Usui D, Yamaguchi-Shima N, Okada S, Shimizu T, Wakiguchi H, Yokotani K. Selective activation of the sympathetic ganglia by centrally administered corticotropin-releasing factor in rats. Auton Neurosci 2009; 146: 111-4.
17. Martinez V, Rivier J, Wang L, Taché 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.
18. Luckey A, Wang L, Jamieson PM et al. Corticotropin-releasing factor receptor 1-deficient mice do not develop postoperative gastric ileus. Gastroenterology 2003; 125: 654-9.
19. Taché Y, Yang H, Miampamba M, Martinez V, Yuan PQ. Role of brainstem TRH/TRH-R1 receptors in the vagal gastric cholinergic response to various stimuli including sham-feeding. Auton Neurosci 2006; 125: 42-52.
20. Stengel A, Goebel M, Luckey A, Yuan PQ, Wang L, Taché Y. Cold ambient temperature reverses abdominal surgery-induced delayed gastric emptying and decreased plasma ghrelin levels in rats. Peptides 2010; 31: 2229-35.
21. Brown MR, Fisher LA. Brain peptide regulation of adrenal epinephrine secretion. Am J Physiol 1984; 247: E41-6.
22. Barnes AJ, Long RG, Adrian TE et al. Effect of a long-acting octapeptide analogue of somatostatin on growth hormone and pancreatic and gastrointestinal hormones in man. Clin Sci (Lond) 1981; 61: 653-6.
23. Erchegyi J, Grace CR, Samant M et al. Ring size of somatostatin analogues (ODT-8) modulates receptor selectivity and binding affinity. J Med Chem 2008; 51: 2668-75.
24. Brown MR, Rivier C, Vale W. Central nervous system regulation of adrenocorticotropin secretion: role of somatostatins. Endocrinology 1984; 114: 1546-9.
25. Fisher DA, Brown MR. Somatostatin analog: plasma catecholamine suppression mediated by the central nervous system. Endocrinology 1980; 107: 714-8.
26. Brown MR, Fisher LA, Spiess J, Rivier C, Rivier J, Vale W. Corticotropin-releasing factor: actions on the sympathetic nervous system and metabolism. Endocrinology 1982; 111: 928-31.
27. Martinez V, Rivier J, Coy D, Taché Y. Intracisternal injection of somatostatin receptor 5-preferring agonists induces a vagal cholinergic stimulation of gastric emptying in rats. J Pharmacol Exp Ther 2000; 293: 1099-105.
28. Stengel A, Coskun T, Goebel M et al. Central injection of the stable somatostatin analog, ODT8-SST induces a somatostatin2 receptor mediated orexigenic effect: role of neuropeptide Y and opioid signaling pathways in rats. Endocrinology 2010; 151: 4224-35.
29. Boeckxstaens GE, de Jonge WJ. Neuroimmune mechanisms in postoperative ileus. Gut 2009; 58: 1300-11.
30. Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol 1999; 20: 157-98.
31. Patel YC, Srikant CB. Subtype selectivity of peptide analogs for all five cloned human somatostatin receptors (hsstr 1-5). Endocrinology 1994; 135: 2814-7.
32. Brown M, Rivier J, Vale W. Somatostatin-28: selective action on the pancreatic beta-cell and brain. Endocrinology 1981; 108: 2391-6.
33. O'Carroll AM, Raynor K, Lolait SJ, Reisine T. Characterization of cloned human somatostatin receptor SSTR5. Mol Pharmacol 1994; 46: 291-8.
34. Erchegyi J, Cescato R, Grace CR et al. Novel, potent, and radio-iodinatable somatostatin receptor 1 (sst1) selective analogues. J Med Chem 2009; 52: 2733-46.
35. Grace CR, Erchegyi J, Koerber SC, Reubi JC, Rivier J, Riek R. Novel sst2-selective somatostatin agonists. Three-dimensional consensus structure by NMR. J Med Chem 2006; 49: 4487-96.
36. Erchegyi J, Waser B, Schaer JC et al. Novel sst(4)-selective somatostatin (SRIF) agonists. 3. Analogues amenable to radiolabeling. J Med Chem 2003; 46: 5597-605.
37. Poitras P, Polvino WJ, Rocheleau B. Gastrokinetic effect of ghrelin analog RC-1139 in the rat. Effect on post-operative and on morphine induced ileus. Peptides 2005; 26: 1598-601.
38. 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.
39. Venkova K, Fraser G, Hoveyda HR, Greenwood-Van Meerveld B. Prokinetic effects of a new ghrelin receptor agonist TZP-101 in a rat model of postoperative ileus. Dig Dis Sci 2007; 52: 2241-8.
40. Tschöp M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 2000; 407: 908-13.
41. Davenport AP, Bonner TI, Foord SM et al. International Union of Pharmacology. LVI. Ghrelin receptor nomenclature, distribution, and function. Pharmacol Rev 2005; 57: 541-6.
42. Ariga H, Tsukamoto K, Chen C, Mantyh C, Pappas TN, Takahashi T. Endogenous acyl ghrelin is involved in mediating spontaneous phase III-like contractions of the rat stomach. Neurogastroenterol Motil 2007; 19: 675-80.
43. Stengel A, Goebel M, Wang L et al. Selective central activation of somatostatin2 receptor increases food intake, grooming behavior and rectal temperature in rats. J Physiol Pharmacol 2010; 61: 399-407.
44. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press, 2007.
45. Barquist E, Zinner M, Rivier J, Taché Y. Abdominal surgery-induced delayed gastric emptying in rats: role of CRF and sensory neurons. Am J Physiol 1992; 262: G616-20.
46. 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.
47. 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.
48. Liao Z, Li ZS, Lu Y, Wang WZ. Microinjection of exogenous somatostatin in the dorsal vagal complex inhibits pancreatic secretion via somatostatin receptor-2 in rats. Am J Physiol Gastrointest Liver Physiol 2007; 292: G746-52.
49. Viollet C, Lepousez G, Loudes C, Videau C, Simon A, Epelbaum J. Somatostatinergic systems in brain: networks and functions. Mol Cell Endocrinol 2008; 286: 75-87.
50. Gastambide F, Viollet C, Lepousez G, Epelbaum J, Guillou JL. Hippocampal SSTR4 somatostatin receptors control the selection of memory strategies. Psychopharmacology (Berl) 2009; 202: 153-63.
51. Fehlmann D, Langenegger D, Schuepbach E, Siehler S, Feuerbach D, Hoyer D. Distribution and characterisation of somatostatin receptor mRNA and binding sites in the brain and periphery. J Physiol Paris 2000; 94: 265-81.
52. Viollet C, Vaillend C, Videau C et al. Involvement of sst2 somatostatin receptor in locomotor, exploratory activity and emotional reactivity in mice. Eur J Neurosci 2000; 12: 3761-70.
53. Allen JP, Hathway GJ, Clarke NJ et al. Somatostatin receptor 2 knockout/lacZ knockin mice show impaired motor coordination and reveal sites of somatostatin action within the striatum. Eur J Neurosci 2003; 17: 1881-95.
54. Singh V, Grotzinger C, Nowak KW et al. Somatostatin receptor subtype-2-deficient mice with diet-induced obesity have hyperglycemia, nonfasting hyperglucagonemia, and decreased hepatic glycogen deposition. Endocrinology 2007; 148: 3887-99.
55. Rocheville M, Lange DC, Kumar U, Sasi R, Patel RC, Patel YC. Subtypes of the somatostatin receptor assemble as functional homo- and heterodimers. J Biol Chem 2000; 275: 7862-9.
56. Lubbers T, Buurman W, Luyer M. Controlling postoperative ileus by vagal activation. World J Gastroenterol 2010; 16: 1683-7.
57. Thoss VS, Perez J, Duc D, Hoyer D. Embryonic and postnatal mRNA distribution of five somatostatin receptor subtypes in the rat brain. Neuropharmacology 1995; 34: 1673-88.
58. Miampamba M, Million M, Taché Y. Brain-gut interactions between central vagal activation and abdominal surgery to influence gastric myenteric ganglia Fos expression in rats. Peptides 2011; 32: 1078-82.
59. Satou M, Nishi Y, Yoh J, Hattori Y, Sugimoto H. Identification and characterization of acyl-protein thioesterase 1/lysophospholipase I as a ghrelin deacylation/lysophospholipid hydrolyzing enzyme in fetal bovine serum and conditioned medium. Endocrinology 2010; 151: 4765-75.
60. Fraser GL, Venkova K, Hoveyda HR, Thomas H, Greenwood-Van Meerveld B. Effect of the ghrelin receptor agonist TZP-101 on colonic transit in a rat model of postoperative ileus. Eur J Pharmacol 2009; 604: 132-7.
61. Venkova K, Mann W, Nelson R, Greenwood-Van Meerveld B. Efficacy of ipamorelin, a novel ghrelin mimetic, in a rodent model of postoperative ileus. J Pharmacol Exp Ther 2009; 329: 1110-6.
62. 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.
63. Tack J, Depoortere I, Bisschops R, Verbeke K, Janssens J, Peeters T. Influence of ghrelin on gastric emptying and meal-related symptoms in idiopathic gastroparesis. Aliment Pharmacol Ther 2005; 22: 847-53.
64. Binn M, Albert C, Gougeon A et al. Ghrelin gastrokinetic action in patients with neurogenic gastroparesis. Peptides 2006; 27: 1603-6.
65. Popescu I, Fleshner PR, Pezzullo JC, Charlton PA, Kosutic G, Senagore AJ. The Ghrelin agonist TZP-101 for management of postoperative ileus after partial colectomy: a randomized, dose-ranging, placebo-controlled clinical trial. Dis Colon Rectum 2010; 53: 126-34.
66. Cremonini F, Camilleri M, Vazquez Roque M et al. Obesity does not increase effects of synthetic ghrelin on human gastric motor functions. Gastroenterology 2006; 131: 1431-9.
67. Stengel A, Goebel M, Wang L et al. Activation of brain somatostatin(2) receptors stimulates feeding in mice: analysis of food intake microstructure. Physiol Behav 2010; 101: 614-22.
68. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 2000; 404: 661-71.
69. Goebel M, Stengel A, Wang L, Coskun T, Rivier J, Taché Y. Pattern of Fos expression in the brain induced by selective activation of somatostatin receptor 2 in rats. Brain Res 2010; 1351: 150-64.
70. Stroh T, Kreienkamp HJ, Beaudet A. Immunohistochemical distribution of the somatostatin receptor subtype 5 in the adult rat brain: predominant expression in the basal forebrain. J Comp Neurol 1999; 412: 69-82.
71. Kumar U. Colocalization of somatostatin receptor subtypes (SSTR1-5) with somatostatin, NADPH-diaphorase (NADPH-d), and tyrosine hydroxylase in the rat hypothalamus. J Comp Neurol 2007; 504: 185-205.
72. Silva AP, Bethmann K, Raulf F, Schmid HA. Regulation of ghrelin secretion by somatostatin analogs in rats. Eur J Endocrinol 2005; 152: 887-94.
73. Barkan AL, Dimaraki EV, Jessup SK, Symons KV, Ermolenko M, Jaffe CA. Ghrelin secretion in humans is sexually dimorphic, suppressed by somatostatin, and not affected by the ambient growth hormone levels. J Clin Endocrinol Metab 2003; 88: 2180-4.
74. Wang Y, Dong L, Cheng Y, Zhao P. Effects of ghrelin on feeding regulation and interdigestive migrating complex in rats. Scand J Gastroenterol 2007; 42: 447-53.
75. Viollet C, Prevost G, Maubert E et al. Molecular pharmacology of somatostatin receptors. Fundam Clin Pharmacol 1995; 9: 107-13.