Abdominal surgery inhibits circulating acyl ghrelin and ghrelin-O-acyltransferase levels in rats: Role of the somatostatin receptor subtype 2

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 2, 2011, Pages

  Stengel, Andreas ^a   Goebel Stengel, Miriam ^a   Wang, Lixin ^a   Shaikh, Almaas ^a   Lambrecht, Nils W G ^b   Rivier, Jean ^c   Taché, Yvette ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA LONG BEACH HEALTHCARE SYSTEM   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Gastric emptying; Somatostatin receptor 2 agonist; Somatostatin receptor 2 antagonist; X A like cell

Indexed keywords

ACYL GHRELIN; ACYLTRANSFERASE; DESACYL GHRELIN; GASTROINTESTINAL HORMONE; GHRELIN; GHRELIN O ACYLTRANSFERASE; HORMONE RECEPTOR BLOCKING AGENT; HORMONE RECEPTOR STIMULATING AGENT; S 346011; S 406028; SOMATOSTATIN RECEPTOR; SOMATOSTATIN RECEPTOR 2; SOMATOSTATIN RECEPTOR 2 ALPHA; UNCLASSIFIED DRUG;

ABDOMINAL SURGERY; ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CIRCULATION; CONTROLLED STUDY; DIET RESTRICTION; ENZYME INHIBITION; INJECTION; LAPAROTOMY; MALE; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SHAM PROCEDURE; SIGNAL TRANSDUCTION; STOMACH EMPTYING; STOMACH MUCOSA;

ABDOMEN; ACYLTRANSFERASES; ANALYSIS OF VARIANCE; ANIMALS; GASTRIC EMPTYING; GASTRIC MUCOSA; GHRELIN; ILEUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SOMATOSTATIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; STOMACH; STOMACH DISEASES; TIME FACTORS;

EID: 79960005949     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00018.2011     Document Type: Article

References (75)

1. Antal A, Nemeth J, Szolcsanyi J, Pozsgai G, Pinter E. Abdominal surgery performed under general anesthesia increases somatostatin-like immunoreactivity in human serum. Neuroimmunomodulation 15: 153-156, 2008.
2. 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 19: 675-680, 2007.
3. Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Shirakami G, Usui T, Shimatsu A, Doi K, Hosoda H, Kojima M, Kangawa K, Nakao K. Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab 86: 4753-4758, 2001.
4. Asakawa A, Inui A, Ueno N, Fujimiya M, Fujino MA, Kasuga M. Mouse pancreatic polypeptide modulates food intake, while not influencing anxiety in mice. Peptides 20: 1445-1448, 1999.
5. 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 88: 2180-2184, 2003.
6. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418: 650-654, 2002.
7. Bednarek MA, Feighner SD, Pong SS, McKee KK, Hreniuk DL, Silva MV, Warren VA, Howard AD, Van Der Ploeg LH, Heck JV. Structurefunction studies on the new growth hormone-releasing peptide, ghrelin: minimal sequence of ghrelin necessary for activation of growth hormone secretagogue receptor 1a. J Med Chem 43: 4370-4376, 2000.
8. Bunnett NW, Helton WS, Debas HT, Ensinck JW. CGRP stimulates the release of pro-somatostatin-derived peptides from the gastric fundus. Am J Physiol Gastrointest Liver Physiol 258: G316-G319, 1990.
9. Camilleri M, Papathanasopoulos A, Odunsi ST. Actions and therapeutic pathways of ghrelin for gastrointestinal disorders. Nat Rev Gastroenterol Hepatol 6: 343-352, 2009.
10. Caminos JE, Bravo SB, Gonzalez CR, Garces MF, Cepeda LA, Gonzalez AC, Cordido F, Lopez M, Dieguez C. Food-intake-regulatingneuropeptides are expressed and regulated through pregnancy and following food restriction in rat placenta. Reprod Biol Endocrinol 6: 14, 2008.
11. Cescato R, Erchegyi J, Waser B, Piccand V, Maecke HR, Rivier JE, Reubi JC. Design and in vitro characterization of highly sst2-selective somatostatin antagonists suitable for radiotargeting. J Med Chem 51: 4030-4037, 2008.
12. Chelikani PK, Haver AC, Reidelberger RD. Comparison of the inhibitoryeffects of PYY(3-36) and PYY(1-36) on gastric emptying in rats. Am J Physiol Regul Integr Comp Physiol 287: R1064-R1070, 2004.
13. Cremonini F, Camilleri M, Vazquez Roque M, McKinzie S, Burton D, Baxter K, Zinsmeister AR. Obesity does not increase effects of synthetic ghrelin on human gastric motor functions. Gastroenterology 131: 1431-1439, 2006.
14. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50: 1714-1719, 2001.
15. Czimmer J, Million M, Tacheacute Y. Urocortin 2 acts centrally to delay gastric emptying through sympathetic pathways while CRF and urocortin 1 inhibitory actions are vagal dependent in rats. Am J Physiol Gastrointest Liver Physiol 290: G511-G518, 2006.
16. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, Matsukura S, Kangawa K, Nakazato M. Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141: 4255-4261, 2000.
17. Davenport AP, Bonner TI, Foord SM, Harmar AJ, Neubig RR, Pin JP, Spedding M, Kojima M, Kangawa K. International Union of Pharmacology. LVI. Ghrelin receptor nomenclature, distribution, and function. Pharmacol Rev 57: 541-546, 2005.
18. 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 143: 118-126, 2007.
19. De Vriese C, Gregoire F, Lema-Kisoka R, Waelbroeck M, RobberechtP, Delporte C. Ghrelin degradation by serum and tissue homogenates: identification of the cleavage sites. Endocrinology 145: 4997-5005, 2004.
20. Fischer T, Doll C, Jacobs S, Kolodziej A, Stumm R, Schulz S. Reassessment of sst2 somatostatin receptor expression in human normal and neoplastic tissues using the novel rabbit monoclonal antibody UMB-1. J Clin Endocrinol Metab 93: 4519-4524, 2008.
21. 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 550: 227-240, 2003.
22. Fukuhara S, Suzuki H, Masaoka T, Arakawa M, Hosoda H, Minegishi Y, Kangawa K, Ishii H, Kitajima M, Hibi T. Enhanced ghrelin secretion in rats with cysteamine-induced duodenal ulcers. Am J Physiol Gastrointest Liver Physiol 289: G138-G145, 2005.
23. Gahete MD, Cordoba-Chacon J, Salvatori R, Castano JP, Kineman RD, Luque RM. Metabolic regulation of ghrelin O-acyl transferase (GOAT) expression in the mouse hypothalamus, pituitary, and stomach. Mol Cell Endocrinol 317: 154-160, 2010.
24. Gallas S, Sinno MH, Boukhettala N, Coeffier M, Dourmap N, Gourcerol G, Ducrotte P, Dechelotte P, Leroi AM, Fetissov SO. Gastric electrical stimulation increases ghrelin production and inhibits catecholaminergic brainstem neurons in rats. Eur J Neurosci 33: 276-284, 2011.
25. Garner AL, Janda KD. cat-ELCCA: A robust method to monitor the fatty acid acyltransferase activity of ghrelin O-acyltransferase (GOAT). Angew Chem Int Ed Engl 49: 9630-9634, 2010.
26. 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 49: 4487-4496, 2006.
27. Gutierrez JA, Solenberg PJ, Perkins DR, Willency JA, Knierman MD, Jin Z, Witcher DR, Luo S, Onyia JE, Hale JE. Ghrelin octanoylation mediated by an orphan lipid transferase. Proc Natl Acad Sci USA 105: 6320-6325, 2008.
28. Hirayama H, Shiina T, Shima T, Kuramoto H, Takewaki T, JBF, Shimizu Y. Contrasting effects of ghrelin and des-acyl ghrelin on thelumbo-sacral defecation center and regulation of colorectal motility in rats.Neurogastroenterol Motil 22: 1124-1131, 2011.
29. Holzer P, Lippe IT, Holzer-Petsche U. Inhibition of gastrointestinal transit due to surgical trauma or peritoneal irritation is reduced in capsaicin- treated rats. Gastroenterology 91: 360-363, 1986.
30. Hosoda H, Kojima M, Matsuo H, Kangawa K. Ghrelin and des-acyl ghrelin: two major forms of rat ghrelin peptide in gastrointestinal tissue. Biochem Biophys Res Commun 279: 909-913, 2000.
31. Hosoda H, Kojima M, Matsuo H, Kangawa K. Purification and characterization of rat des-Gln14-Ghrelin, a second endogenous ligand for the growth hormone secretagogue receptor. J Biol Chem 275: 21995-22000, 2000.
32. Inhoff T, Modiennikes H, Noetzel S, Stengel A, Goebel M, Dinh QT, Riedl A, Bannert N, Wisser AS, Wiedenmann B, Klapp BF, Tacheacute Y, Kobelt P. Desacyl ghrelin inhibits the orexigenic effect of peripherally injected ghrelin in rats. Peptides 29: 2159-2168, 2008.
33. Inhoff T, Wiedenmann B, Klapp BF, Modiennikes H, Kobelt P. Is desacyl ghrelin a modulator of food intake Peptides 30: 991-994, 2009.
34. Inui T, Kinoshita Y, Yamaguchi A, Yamatani T, Chiba T. Linkage between capsaicin-stimulated calcitonin gene-related peptide and somatostatin release in rat stomach. Am J Physiol Gastrointest Liver Physiol 261: G770-G774, 1991.
35. Kawakubo K, Coy DH, Walsh JH, Tacheacute Y. Urethane-induced somatostatin mediated inhibition of gastric acid: reversal by the somatostatin 2 receptor antagonist PRL-2903. Life Sci 65: PL115-PL120, 1999.
36. Kumar R, Salehi A, Rehfeld JF, Hoglund P, Lindstrom E, Hakanson R. Proghrelin peptides: desacyl ghrelin is a powerful inhibitor of acylatedghrelin, likely to impair physiological effects of acyl ghrelin but not of obestatin A study of pancreatic polypeptide secretion from mouse islets. Regul Pept 164: 65-70, 2010.
37. Kumar U, Grant M. Somatostatin and somatostatin receptors. Results Probl Cell Differ 50: 137-184, 2010.
38. Lehto-Axtelius D, Chen D, Surve VV, Hakanson R. Post-gastrectomy osteopenia in the rat: bone structure is preserved by retaining 10%-30% of the oxyntic gland area. Scand J Gastroenterol 37: 437-443, 2002.
39. Lippl F, Kircher F, Erdmann J, Allescher HD, Schusdziarra V. Effect of GIP, GLP-1, insulin and gastrin on ghrelin release in the isolated rat stomach. Regul Pept 119: 93-98, 2004.
40. Livingston EH, Passaro EP J Postoperative ileus. Dig Dis Sci 35: 121-132, 1990.
41. Luckey A, Livingston E, Tacheacute Y. Mechanisms and treatment of postoperative ileus. Arch Surg 138: 206-214, 2003.
42. Luque RM, Gahete MD, Hochgeschwender U, Kineman RD. Evidence that endogenous SST inhibits ACTH and ghrelin expression by independent pathways. Am J Physiol Endocrinol Metab 291: E395-E403, 2006.
43. Mizutani M, Atsuchi K, Asakawa A, Matsuda N, Fujimura M, Inui A, Kato I, Fujimiya M. Localization of acyl ghrelin- and des-acyl ghrelinimmunoreactive cells in the rat stomach and their responses to intragastric pH. Am J Physiol Gastrointest Liver Physiol 297: G974-G980, 2009.
44. Murray CD, Martin NM, Patterson M, Taylor SA, Ghatei MA, Kamm MA, Johnston C, Bloom SR, Emmanuel AV. Ghrelin enhances gastric emptying in diabetic gastroparesis: a double blind, placebo controlled, crossover study. Gut 54: 1693-1698, 2005.
45. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
46. Plourde V, Wong HC, Walsh JH, Raybould HE, Tacheacute Y. CGRP antagonists and capsaicin on celiac ganglia partly prevent postoperative gastric ileus. Peptides 14: 1225-1229, 1993.
47. 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, placebocontrolled clinical trial. Dis Colon Rectum 53: 126-134, 2010.
48. Ren J, Young RL, Lassiter DC, Harty RF. Calcitonin gene-related peptide mediates capsaicin-induced neuroendocrine responses in rat antrum. Gastroenterology 104: 485-491, 1993.
49. Romero A, Kirchner H, Heppner K, Pfluger P, Tschoep M, Nogueiras R. GOAT-the master switch for the ghrelin system Eur J Endocrinol 163: 1-8, 2010.
50. Rossowski WJ, Cheng BL, Taylor JE, Datta R, Coy DH. Human urotensin II-induced aorta ring contractions are mediated by protein kinase C, tyrosine kinases and Rho-kinase: inhibition by somatostatin receptor antagonists. Eur J Pharmacol 438: 159-170, 2002.
51. Ruttimann EB, Arnold M, Hillebrand JJ, Geary N, Langhans W. Intrameal hepatic portal and intraperitoneal infusions of glucagon-like peptide-1 reduce spontaneous meal size in the rat via different mechanisms. Endocrinology 150: 1174-1181, 2009.
52. Sachs G, Zeng N, Prinz C. Physiology of isolated gastric endocrine cells. Annu Rev Physiol 59: 243-256, 1997.
53. Schindler M, Humphrey PP. Differential distribution of somatostatin sst2 receptor splice variants in rat gastric mucosa. Cell Tissue Res 297: 163-168, 1999.
54. Seoane LM, Al-Massadi O, Barreiro F, Dieguez C. Casanueva FF. Growth hormone and somatostatin directly inhibit gastric ghrelin secretion. An in vitro organ culture system. J Endocrinol Invest 30: 22-25, 2007.
55. Shimada M, Date Y, Mondal MS, Toshinai K, Shimbara T, Fukunaga K, Murakami N, Miyazato M, Kangawa K, Yoshimatsu H, Matsuo H, Nakazato M. Somatostatin suppresses ghrelin secretion from the rat stomach. Biochem Biophys Res Commun 302: 520-525, 2003.
56. Shulkes A. Somatostatin: physiology and clinical applications. Baillieres Clin Endocrinol Metab 8: 215-236, 1994.
57. Silva AP, Bethmann K, Raulf F, Schmid HA. Regulation of ghrelin secretion by somatostatin analogs in rats. Eur J Endocrinol 152: 887-894, 2005.
58. Stengel A, Goebel M, Luckey A, Yuan PQ, Wang L, Tacheacute Y. Cold ambient temperature reverses abdominal surgery-induced delayed gastric emptying and decreased plasma ghrelin levels in rats. Peptides 31: 2229- 2235, 2010.
59. Stengel A, Goebel M, Wang L, Reeve JR, Tacheacute Y, Lambrecht NW. Lipopolysaccharide differentially decreases plasma acyl and desacyl ghrelin levels in rats: potential role of the circulating ghrelin-acylating enzyme GOAT. Peptides 31: 1689-1696, 2010.
60. Stengel A, Goebel M, Wang L, Tacheacute Y. Ghrelin, des-acyl ghrelin and nesfatin-1 in gastric X/A-like cells: role as regulators of food intake and body weight. Peptides 31: 357-369, 2010.
61. Stengel A, Goebel M, Wang L, Tacheacute Y. Abdominal surgery activates nesfatin-1 immunoreactive brain nuclei in rats. Peptides 31: 263-270, 2010.
62. Stengel A, Goebel M, Wang L, Tacheacute Y, Sachs G, Lambrecht NW. Differential distribution of ghrelin-O-acyltransferase (GOAT) immunoreactive cells in the mouse and rat gastric oxyntic mucosa. Biochem Biophys Res Commun 392: 67-71, 2010.
63. Stengel A, Goebel M, Yakubov I, Wang L, Witcher D, Coskun T, Tacheacute Y, Sachs G, Lambrecht NW. Identification and characterization of nesfatin-1 immunoreactivity in endocrine cell types of the rat gastric oxyntic mucosa. Endocrinology 150: 232-238, 2009.
64. Stengel A, Keire D, Goebel M, Evilevitch L, Wiggins B, Tacheacute Y, Reeve JR Jr. The RAPID method for blood processing yields new insight in plasma concentrations and molecular forms of circulating gut peptides. Endocrinology 150: 5113-5118, 2009.
65. Sternini C, Wong H, Wu SV, de Giorgio R, Yang M, Reeve J, Brecha NC, Walsh JH. Somatostatin 2A receptor is expressed by enteric neurons, and by interstitial cells of Cajal and enterochromaffin-like cells of the gastrointestinal tract. J Comp Neurol 386: 396-408, 1997.
66. Tacheacute Y, Barquist E, Stephens RL, Rivier J. Abdominal surgery- and trephination-induced delay in gastric emptying is prevented by intracisternal injection of CRF antagonist in the rat. J Gastrointest Motil 3: 19-25, 1991.
67. 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 22: 847-853, 2005.
68. Tolessa T, Gutniak M, Holst JJ, Efendic S, Hellstrom PM. Glucagonlike peptide-1 retards gastric emptying and small bowel transit in the rat: effect mediated through central or enteric nervous mechanisms. Dig Dis Sci 43: 2284-2290, 1998.
69. Venkova K, Greenwood-Van Meerveld B. Application of ghrelin to gastrointestinal diseases. Curr Opin Investig Drugs 9: 1103-1107, 2008.
70. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA, Bloom SR. Ghrelin causes hyperphagia and obesity in rats. Diabetes 50: 2540-2547, 2001.
71. Yang H, Wong H, Wu V, Walsh JH, Tacheacute Y. Somatostatin monoclonal antibody immunoneutralization increases gastrin and gastric acid secretion in urethane-anesthetized rats. Gastroenterology 99: 659-665, 1990.
72. Yang J, Brown MS, Liang G, Grishin NV, Goldstein JL. Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 132: 387-396, 2008.
73. Young AA, Gedulin BR, Rink TJ. Dose-responses for the slowing of gastric emptying in a rodent model by glucagon-like peptide (7-36) NH2, amylin, cholecystokinin, and other possible regulators of nutrient uptake. Metabolism 45: 1-3, 1996.
74. Zeinali F, Stulberg JJ, Delaney CP. Pharmacological management of postoperative ileus. Can J Surg 52: 153-157, 2009.
75. Zittel TT, Reddy SN, Plourde V, Raybould HE. Role of spinal afferents and calcitonin gene-related peptide in the postoperative gastric ileus in anesthetized rats. Ann Surg 219: 79-87, 1994.