Ghrelin accelerates the healing of oral ulcers in non-sialoadenectomized and sialoadenectomized rats

Journal of Physiology and Pharmacology

Volumn 64, Issue 5, 2013, Pages 657-668

  Warzecha, Z ^a   Kownacki, P ^a   Ceranowicz, P ^a   Dembinski, M ^a   Cieszkowski, J ^a   Dembinski, A ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Ghrelin; Gingival mucosa; Healing; Interleukin 1beta; Lingual mucosal blood flow; Oral ulcers; Sialoadenectomy

Indexed keywords

GHRELIN; INTERLEUKIN 1BETA; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; GINGIVA ULCER; MALE; MOUTH MUCOSA; MOUTH ULCER; NONHUMAN; RAT; SALIVARY GLAND; SALIVATION; TISSUE BLOOD FLOW; TISSUE LEVEL; TONGUE ULCER; ULCER HEALING;

ANIMALS; CELL PROLIFERATION; DNA; GHRELIN; INTERLEUKIN-1BETA; MALE; MOUTH MUCOSA; ORAL ULCER; RATS; RATS, WISTAR; REGIONAL BLOOD FLOW; SALIVARY GLANDS;

EID: 84888265553     PISSN: 08675910     EISSN: 18991505     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Nauntofte B, Jensen JL. Salivary secretion. In: Textbook of Gastroenterology. Yamada T, Alpers D, Laine L, Owang C, Powell DW (eds), Philadelphia, Lippincott, Wiliams & Wilkins Publishers, 1999, pp. 263-278.
2. Leitch GJ. Role of the salivary glands in protecting the stomach against ethanol. Alcohol Alcohol 1985; 20: 305-311.
3. Konturek SJ, Brzozowski T, Konturek PK, Majka J, Dembinski A. Role of salivary glands and epidermal growth factor (EGF) in gastric secretion and mucosal integrity in rats exposed to stress. Regul Pept 1991; 32: 203-215.
4. Noguchi S, Ohba Y, Oka T. Effect of salivary epidermal growth factor on wound healing of tongue in mice. Am J Physiol 1991; 260: E620-E625.
5. Bodner L, Dayan D, Pinto Y, Hammel I. Characteristics of palatal wound healing in desalivated rats. Arch Oral Biol 1993; 38: 17-21.
6. Konturek SJ, Dembinski A, Warzecha Z, Brzozowski T, Gregory H. Role of epidermal growth factor in healing of chronic gastroduodenal ulcers in rats. Gastroenterology 1988; 94: 1300-1307.
7. Lambotte L, Saliez A, Triest S, et al. Effect of sialoadenectomy and epidermal growth factor administration on liver regeneration after partial hepatectomy. Hepatology 1997; 25: 607-612.
8. Oudhoff MJ, Bolscher J G, Nazmi K, et al. Histatins are the major wound-closure stimulating factors in human saliva as identified in a cell culture assay. FASEBJ 2008; 22: 3805-3812.
9. Bowen WH, Pearson SK, Young DA. The effect of desalivation on coronal and root surface caries in rats. J Dent Res 1988; 67: 21-23.
10. Kaplan I, Zuk-Paz L, Wolff A. Association between salivary flow rates, oral symptoms, and oral mucosal status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 106: 235-241.
11. Caplan DJ, Hunt RJ. Salivary flow and risk of tooh loss in an elderly population. Community Dent Oral Epidemiol 1996; 24: 68-71.
12. Bodner L, Dayan D, Pinto Y, Hammel I. Characteristics of palatal wound healing in desalivated rats. Arch Oral Biol 1993; 38: 17-21.
13. Bodner L, Kaffe I, Cohen Z, Dayan D. Long-term effect of desalivation on extraction wound healing: a densitometric study in rats. Dentomaxillofac Radiol 1993; 22: 195-198.
14. Warzecha Z, Dembinski A. Protective and therapeutic effects of ghrelin in the gut. Curr Med Chem 2012; 19: 118-125.
15. Konturek PC, Brzozowski T, Pajdo R, et al. Ghrelin-a new gastroprotective factor in gastric mucosa. J Physiol Pharmacol 2004; 55: 325-336.
16. Sibilia V, Rindi G, Pagani F, et al. Ghrelin protects against ethanol-induced gastric ulcers in rats: studies on the mechanisms of action. Endocrinology 2003; 144: 353-359.
17. Brzozowski T, Konturek PC, Konturek SJ, et al. Exogenous and endogenous ghrelin in gastroprotection against stress-induced gastric damage. Regul Pept 2004; 120: 39-51.
18. Iseri SO, Sener G, Yuksel M, et al. Ghrelin against alendronate-induced gastric damage in rats. J Endocrinol 2005; 187: 399-406.
19. Ceranowicz P, Warzecha Z, Dembinski A, et al. Treatment with ghrelin accelerates the healing of acetic acid-induced gastric and duodenal ulcers in rats. J Physiol Pharmacol 2009; 60: 87-98.
20. Warzecha Z, Ceranowicz D, Dembinski A, et al. Ghrelin accelerates the healing of cysteamine-induced duodenal ulcers in rats. Med Sci Monit 2012; 18: BR181-BR187.
21. Granata R, Settanni F, Biancone L, et al. Acylated and unacylated ghrelin promote proliferation and inhibit apoptosis of pancreatic beta-cells and human islets: involvement of 3',5'-cyclic adenosine monophosphate/protein kinase A, extracellular signal-regulated kinase 1/2, and phosphatidyl inositol 3-Kinase/Akt signaling. Endocrinology 2007; 148: 512-529.
22. Dembinski A, Warzecha Z, Ceranowicz P, et al. Ghrelin attenuates the development of acute pancreatitis in rats. J Physiol Pharmacol 2003; 54: 561-573.
23. Dembinski A, Warzecha Z, Ceranowicz P, et al. Role of growth hormone and insulin-like growth factor-1 in the protective effect of ghrelin in ischemia/reperfusion-induced acute pancreatitis. Growth Horm IGF Res 2006; 16: 348-356.
24. Zhou X, Xue C. Ghrelin inhibits the development of acute pancreatitis and nuclear factor kappaB activation in pancreas and liver. Pancreas 2009; 38: 752-757.
25. Ceranowicz D, Warzecha Z, Dembinski A, et al. Role of hormonal axis, growth hormone - IGF-1, in the therapeutic effect of ghrelin in the course of cerulein-induced acute pancreatitis. J Physiol Pharmacol 2010; 61: 599-606.
26. Warzecha Z, Ceranowicz P, Dembinski A, et al. Therapeutic effect of ghrelin in the course of cerulein-induced acute pancreatitis in rats. J Physiol Pharmacol 2010; 61: 419-427.
27. Gutierrez-Grobe Y, Villalobos-Blasquez I, Sanchez-Lara K, et al. High ghrelin and obestatin levels and low risk of developing fatty liver. Ann Hepatol 2010; 9: 52-57.
28. Mendez-Sanchez N, Ponciano-Rodriguez G, Bermejo-Martinez L, et al. Low serum levels of ghrelin are associated with gallstone disease. World J Gastroenterol 2006; 12: 3096-3100.
29. Cetin E, Kanbur M, Cetin N, Eraslan G, Atasever A. Hepatoprotective effect of ghrelin on carbon tetrachloride-induced acute liver injury in rats. Regul Pept 2011; 171: 1-5.
30. Golestan Jahromi M, Nabavizadeh F, Vahedian J, Nahrevanian H, Dehpour AR, Zare-Mehrjardi A. Protective effect of ghrelin on acetaminophen-induced liver injury in rat. Peptides 2010; 31: 2114-2117.
31. Gonzalez-Rey E, Chorny A, Delgado M. Therapeutic action of ghrelin in a mouse model of colitis. Gastroenterology 2006; 130: 1707-1720.
32. Konturek PC, Brzozowski T, Engel M, et al. Ghrelin ameliorates colonic inflammation. Role of nitric oxide and sensory nerves. J Physiol Pharmacol 2009; 60: 41-47.
33. De Smet B, 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.
34. Aydin S, Ozercan IH, Geckil H, et al. Ghrelin is present in teeth. J Biochem Mol Biol 2007; 40: 368-372.
35. Li BB, Chen ZB, Li BC, et al. Expression of ghrelin in human salivary glands and its levels in saliva and serum in Chinese obese children and adolescents. Arch Oral Biol 2011; 56: 389-394.
36. Ohta K, Laborde NJ, Kajiya M, et al. Expression and possible immune-regulatory function of ghrelin in oral epithelium. J Dental Res 2011; 90: 1286-1292.
37. Shin YK, Martin B, Kim W, et al. Ghrelin is produced in taste cells and ghrelin receptor null mice show reduced taste responsivity to salty (NaCl) and sour (citric acid) tastants. PLoS One 2010; 5(9): e12729.
38. Groschl M, Topf HG, Bohlender J, et al. Identification of ghrelin in human saliva: production by the salivary glands and potential role in proliferation of oral keratinocytes. Clin Chem 2005; 51: 997-1006.
39. Dynesen AW, Bardow A, Astrup A, Petersson B, Holst JJ, Nauntofte B. Meal-induced compositional changes in blood and saliva in persons with bulimia nervosa. Am J Clin Nutr 2008; 87: 12-22.
40. Monteleone P, Tortorella A, Scognamiglio P, Serino I, Monteleone AM, Maj M. The acute salivary ghrelin response to a psychosocial stress is enhanced in symptomatic patients with bulimia nervosa: a pilot study. Neuropsychobiology 2012; 66: 230-236.
41. Amano O, Mizobe K, Bando Y, Sakiyama K. Anatomy and histology of rodent and human major salivary glands -overview of the Japan salivary gland society-sponsored workshop-. Acta Histochem Cytochem 2012; 45: 241-250.
42. Bodner L. Effect of parotid submandibular and sublingual saliva on wound healing in rats. Comp Biochem Physiol A Comp Physiol 1991; 100: 887-890.
43. Warzecha Z, Dembinski A, Ceranowicz P, et al. Role of sensory nerves in gastroprotective effect of anandamide in rats. J Physiol Pharmacol 2011; 62: 207-217.
44. Warzecha Z, Dembinski A, Ceranowicz P, et al. Heparin inhibits protective effect of ischemic preconditioning in ischemia/reperfusion-induced acute pancreatitis. J Physiol Pharmacol 2012; 63: 355-365.
45. Hamilton AI, Blackwood HJJ. Cell renewal of oral mucosal epithelium of the rat. J Anat 1974; 117: 313-327.
46. Warzecha Z, Dembinski A, Brzozowski T, et al. Gastroprotective effect of histamine and acid secretion on ammonia-induced gastric lesions in rats. Scand J Gastroenterol 2000; 35: 916-924.
47. Sorbye H, Svanes K. The role of blood flow in gastric mucosal defence, damage and healing. Dig Dis 1994; 12: 305-317.
48. Warzecha W, Dembinski A, Brzozowski T, et al. Histamine in stress ulcer prophylaxis in rats. J Physiol Pharmacol 2001; 52: 407-421.
49. West SD, Helmer KS, Chang LK, Cui Y, Greeley GH, Mercer DW. Cholecystokinin secretagogue-induced gastroprotection: role of nitric oxide and blood flow. Am J Physiol Gastrointest Liver Physiol 2003; 284: G399-G410.
50. Orlando RC. The integrity of the esophageal mucosa. Balance between offensive and defensive mechanisms. Best Pract Res Clin Gastroenterol 2010; 24: 873-882.
51. Leung FW, Reedy TJ, Van Deventer GM, Guth PH. Reduction in index of oxygen saturation at margin of active duodenal ulcers may lead to slow healing. Dig Dis Sci 1989; 34: 417-423.
52. Leung FW, Su KC, Pique JM, Thiefin G, Passaro E Jr, Guth PH. Superior mesenteric artery is more important than inferior mesenteric artery in maintaining colonic mucosal perfusion and integrity in rats. Dig Dis Sci 1992; 37: 1329-1335.
53. Ahluwalia A, Li A, Cheng G, Deng X, Tarnawski AS. Reduced ghrelin in endothelial cells plays important mechanistic role in aging-related impairment of angiogenesis. J Physiol Pharmacol 2009; 60: 29-34.
54. Dinarello CA, Simon A, van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov 2012; 11: 633-652.
55. De Koning HD, Schalkwijk J, van der Ven-Jongekrijg J, Stoffels M, van der Meer JW, Simon A. Sustained efficacy of the monoclonal anti-interleukin-1 beta antibody canakinumab in a 9-month trial in Schnitzler's syndrome. Ann Rheum Dis 2012; 72: 1634-1638.
56. Dinarello CA. A clinical perspective of IL-1b as the gatekeeper of inflammation. Eur J Immunol 2011; 41: 1203-1217.
57. Herlin T, Fiirgaard B, Bjerre M, et al. Efficacy of anti-IL-1 treatment in Majeed syndrome. Ann Rheum Dis 2013; 72: 410-413.
58. Norman J, Franz M, Messina J, et al. Interleukin-1 receptor antagonist decreases severity of experimental acute pancreatitis. Surgery 1995; 117: 648-655.
59. Hattori N, Saito T, Yagyu T, Jiang BH, Kitagawa K, Inagaki C. GH receptor, GH secretagogue receptor, and ghrelin expression in human T cells, B cells, and neutrophils. J Clin Endocrinol Metab 2001; 86: 4284-4291.
60. Xia Q, Pang W, Pan H, Zheng Y, Kang JS, Zhu SG. Effects of ghrelin on the proliferation and secretion of splenic T lymphocytes in mice. Regul Pept 2004; 122: 173-178.
61. Chang L, Du JB, Gao LR, Pang YZ, Tang CS. Effect of ghrelin on septic shock in rats. Acta Pharmacol Sin 2003; 24: 45-49.
62. Dixit VD, Yang H, Sun Y, et al. Ghrelin promotes thymopoiesis during aging. J Clin Invest 2007; 117: 2778-2790.
63. Dixit VD, Schaffer EM, Pyle RS, et al. Ghrelin inhibits leptin- and activation-induced proinflammatory cytokine expression by human monocytes and T cells. J Clin Invest 2004; 114: 57-66.
64. Tumer C, Bilgin HM, Obay BD, Diken H, Tasdemir E, Sermet A. Effect of ghrelin administration on phagocytic activity in acute cold-restraint stress exposed rats. Regul Pept 2007; 138: 113-117.
65. Haugsten EM, Wiedlocha A, Olsnes S, Wesche J. Roles of fibroblast growth factor receptors in carcinogenesis. Mol Cancer Res 2010; 8: 1439-1452.
66. Rho O, Kim DJ, Kiguchi K, Digiovanni J. Growth factor signaling pathways as targets for prevention of epithelial carcinogenesis. Mol Carcinog 2011; 50: 264-279.
67. Kuemmerle JF. Insulin-like growth factors in the gastrointestinal tract and liver. Endocrinol Metab Clin North Am 2012; 41: 409-423.
68. Nikolopoulos D, Theocharis S, Kouraklis G. Ghrelin's role on gastrointestinal tract cancer. Surg Oncol 2010; 19: e2-e10.
69. Lanfranco F, Baldi M, Cassoni P, Bosco M, Ghe C, Muccioli G. Ghrelin and prostate cancer. Vitam Horm 2008; 77: 301-324.
70. Tian C, Zhang L, Hu D, Ji J. Ghrelin induces gastric cancer cell proliferation, migration, and invasion through GHS-R/NF-kB signaling pathway. Mol Cell Biochem 2013; 382: 163-172.
71. Murphy G, Kamangar F, Dawsey SM, et al. The relationship between serum ghrelin and the risk of gastric and esophagogastric junctional adenocarcinomas. J Natl Cancer Inst 2011; 103: 1123-1129.
72. Guyton AC. Secretory function of the alimentary tract. In: Textbook of Medical Physiology, A.C. Guyton (ed.) Philadelphia, W.B. Saunders Company, 1991, pp.709-725.
73. Kojima M, Hosoda H, Date Y, Nakazano M, Matsuo H, KangawaK. Ghrelin is a growth-hormone releasing acylated peptide from stomach. Nature 1999; 402: 656-660.
74. Ho KK, O'Sullivan AJ, Hoffman DM. Metabolic actions of growth hormone in man. Endocr J 1996; 43(Suppl): S57-S63.
75. Zapf J, Froesch ER. Insulin-like growth factors/somatomedins: structure, secretion, biological actions and physiological role. Horm Res 1986; 24: 121-130.
76. Skrtic S, Wallenius K, Gressner AM, Jansson JO. Insulinlike growth factor signaling pathways in rat hepatic stellate cells: importance for deoxyribonucleic acid synthesis and hepatocyte growth factor production. Endocrinology 1999; 140: 5729-5735.