The protective effects of calcitonin gene-related peptide on gastric mucosa injury after cerebral ischemia reperfusion in rats

Regulatory Peptides

Volumn 160, Issue 1-3, 2010, Pages 121-128

  Feng, Guoying ^a   Xu, Xiaobo ^a   Wang, Qian ^b   Liu, Zhen ^c   Li, Zhenzhong ^c   Liu, Guixiang ^a  

^a BINZHOU MEDICAL UNIVERSITY   (China)

^b YANTAI UNIVERSITY   (China)

^c SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Aquaporin 4; Basic fibroblast growth factor; Calcitonin gene related peptide; Cerebral ischemia reperfusion; Gastric mucosa; Gastrin; Somatostatin

Indexed keywords

AQUAPORIN 4; BASIC FIBROBLAST GROWTH FACTOR; CALCITONIN GENE RELATED PEPTIDE; GASTRIN; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATORY INFILTRATE; MALE; MAST CELL DEGRANULATION; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STOMACH ANTRUM; STOMACH MUCOSA INJURY; STOMACH MUCOSA LESION; STOMACH PROTECTION;

ANIMALS; BRAIN ISCHEMIA; CALCITONIN GENE-RELATED PEPTIDE; GASTRIC MUCOSA; IMMUNOHISTOCHEMISTRY; MALE; MUCOUS MEMBRANE; RATS; RATS, WISTAR; REPERFUSION INJURY; STOMACH DISEASES; VASODILATOR AGENTS;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 74949100636     PISSN: 01670115     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.regpep.2009.11.008     Document Type: Article

References (69)

1. Colli B.O., Tirapelli D.P., Carlotti Jr. C.G., Lopes L.S., and Tirapelli L.F. Biochemical evaluation of focal non-reperfusion cerebral ischemia by middle cerebral artery occlusion in rats. Arq Neuropsiquiatr 66 (2008) 725-730
2. Liu B., Tian Y., Zhang Y., and Zhang W. Therapeutic effect analysis of acute traumatic brain injuries. Neurol Res 30 (2008) 594-597
3. Toda M., Suzuki T., Hosono K., Kurihara Y., Kurihara H., Hayashi I., Kitasato H., Hoka S., and Majima M. Roles of calcitonin gene-related peptide in facilitation of wound healing and angiogenesis. Biomed Pharmacother 62 (2008) 352-359
4. Edvinsson L. Calcitonin gene-related peptide (CGRP) and the pathophysiology of headache: therapeutic implications. CNS Drugs 15 (2001) 745-753
5. Sato H., Kawashima K., Yuki M., Kazumori H., Rumi M.A., Ortega-Cava C.F., Ishihara S., and Kinoshita Y. Lafutidine, a novel histamine H2-receptor antagonist, increases serum calcitonin gene-related peptide in rats after water immersion-restraint stress. J Lab Clin Med 141 (2003) 102-105
6. Dong Y.L., Vegiraju S., Chauhan M., Gangula P.R., Hankins G.D., Goodrum L., and Yallampalli C. Involvement of calcitonin gene-related peptide in control of human fetoplacental vascular tone. Am J Physiol Heart Circ Physiol 286 (2004) H230-H239
7. Qin X.P., Zeng S.Y., Li D., Chen Q.Q., Luo D., Zhang Z., Hu G.Y., Deng H.W., and Li Y.J. Calcitonin gene-related peptide-mediated depressor effect and inhibiting vascular hypertrophy of rutaecarpine in renovascular hypertensive rats. J Cardiovasc Pharmacol 50 (2007) 654-659
8. Gozalov A., Jansen-Olesen I., Klaerke D., and Olesen J. Role of K ATP channels in cephalic vasodilatation induced by calcitonin gene-related peptide, nitric oxide, and transcranial electrical stimulation in the rat. Headache 48 (2008) 1202-1213
9. Brzozowski T., Konturek P.C., Pajdo R., Kwiecien S., Sliwowski Z., Drozdowicz D., Ptak-Belowska A., Pawlik M., Konturek S.J., Pawlik W.W., and Hahn G.G. Importance of brain-gut axis in the gastroprotection induced by gastric and remote preconditioning. J Physiol Pharmacol 55 (2004) 165-177
10. Nishihara K., Nozawa Y., Nakano M., Ajioka H., and Matsuura N. Sensitizing effects of lafutidine on CGRP-containing afferent nerves in the rat stomach. Br J Pharmacol 135 (2002) 1487-1494
11. Min C., Hesheng L., Jihong C., Qiaoyun T., Xianzhen L., and Chireyeth S. Effects and mechanism of changes of local neurotransmitters in rats' pylorus and bile reflux to the stomach with stress ulcer. Dig Dis Sci 50 (2005) 1898-1903
12. Lin Y.Y., Tseng T.J., Hsieh Y.L., Luo K.R., Lin W.M., Chiang H., and Hsieh S.T. Depletion of peptidergic innervation in the gastric mucosa of streptozotocin-induced diabetic rats. Exp Neurol 213 (2008) 388-396
13. Tan R., Bulbul M., Ongut G., Tosun O., and Izgut-Uysal V.N. Prostaglandins, capsaicin-sensitive sensory nerves and neutrophil infiltration, but not nitric oxide, contribute to cold restraint stress-induced gastric adaptation in rats. Clin Exp Pharmacol Physiol 33 (2006) 946-951
14. Konturek P.C., Konturek S.J., Burnat G., Brzozowski T., Brzozowska I., and Reiter R.J. Dynamic physiological and molecular changes in gastric ulcer healing achieved by melatonin and its precursor L-tryptophan in rats. J Pineal Res 45 (2008) 180-190
15. Harada N., and Okajima K. Inhibition of neutrophil activation by lafutidine, an H2-receptor antagonist, through enhancement of sensory neuron activation contributes to the reduction of stress-induced gastric mucosal injury in rats. Dig Dis Sci 52 (2007) 469-477
16. Shimozawa N., Okajima K., Harada N., Arai M., Ishida Y., Shimada S., Kurihara H., and Nakagata N. Contribution of sensory neurons to sex difference in the development of stress-induced gastric mucosal injury in mice. Gastroenterology 131 (2006) 1826-1834
17. Shimozawa N., Okajima K., and Harada N. Estrogen and isoflavone attenuate stress-induced gastric mucosal injury by inhibiting decreases in gastric tissue levels of CGRP in ovariectomized rats. Am J Physiol Gastrointest Liver Physiol 292 (2007) G615-G619
18. Ikawa K., Shimatani T., Azuma Y., Inoue M., and Morikawa N. Calcitonin gene-related peptide and somatostatin releases correlated with the area under the lafutidine concentration-time curve in human plasma. J Clin Pharm Ther 31 (2006) 351-356
19. Katagiri F., Itoh H., and Takeyama M. Effect of Sho-hange-ka-bukuryo-to on gastrointestinal peptide concentrations in the plasma of healthy human subjects. Biol Pharm Bull 27 (2004) 1674-1678
20. Thompson B.J., Washington M.K., Kurre U., Singh M., Rula E.Y., and Emeson R.B. Protective roles of alpha-calcitonin and beta-calcitonin gene-related peptide in spontaneous and experimentally induced colitis. Dig Dis Sci 53 (2008) 229-241
21. Li Y., Zhang J.F., Zhang Y.M., and Ma X.B. The protective effect of genistein postconditioning on hypoxia/reoxygenation-induced injury in human gastric epithelial cells. Acta Pharmacol Sin 30 (2009) 576-581
22. Evangelista S. Role of sensory neurons in restitution and healing of gastric ulcers. Curr Pharm Des 12 (2006) 2977-2984
23. Liu Y.Z., Zhou Y., Li D., Wang L., Hu G.Y., Peng J., and Li Y.J. Reduction of asymmetric dimethylarginine in the protective effects of rutaecarpine on gastric mucosal injury. Can J Physiol Pharmacol 86 (2008) 675-681
24. Sato Y., Katagiri F., Inoue S., Itoh H., and Takeyama M. Effects of Ninjin-to on levels of calcitonin gene-related peptide and substance P in human plasma. Biol Pharm Bull 27 (2004) 2032-2034
25. Harty R.F., Ancha H.R., Xia Y., Anderson M., and Jazzar A. GABAergic mechanisms of gastroprotection in the rat: role of sensory neurons, prostaglandins, and nitric oxide. Dig Dis Sci 49 (2004) 1875-1881
26. Brzozowski T., Konturek P.C., Sliwowski Z., Drozdowicz D., Burnat G., Pajdo R., Pawlik M., Bielanski W., Kato I., Kuwahara A., Konturek S.J., and Pawlik W.W. Gastroprotective action of orexin-A against stress-induced gastric damage is mediated by endogenous prostaglandins, sensory afferent neuropeptides and nitric oxide. Regul Pept 148 (2008) 6-20
27. Brzozowski T., Konturek P.C., Sliwowski Z., Drozdowicz D., Kwiecien S., Pawlik M., Pajdo R., Konturek S.J., Pawlik W.W., and Hahn E.G. Neural aspects of ghrelin-induced gastroprotection against mucosal injury induced by noxious agents. J Physiol Pharmacol 57 Suppl 6 (2006) 63-76
28. Kang J.M., Kim N., Kim B., Kim J.H., Lee B.Y., Park J.H., Lee M.K., Lee H.S., Jang I.J., Kim J.S., Jung H.C., and Song I.S. Gastroprotective action of cochinchina momordica seed extract is mediated by activation of CGRP and inhibition of cPLA(2)/5-LOX pathway. Dig Dis Sci (2009)
29. Ohno T., Hattori Y., Komine R., Ae T., Mizuguchi S., Arai K., Saeki T., Suzuki T., Hosono K., Hayashi I., Oh-Hashi Y., Kurihara Y., Kurihara H., Amagase K., Okabe S., Saigenji K., and Majima M. Roles of calcitonin gene-related peptide in maintenance of gastric mucosal integrity and in enhancement of ulcer healing and angiogenesis. Gastroenterology 134 (2008) 215-225
30. Kawashima K., Ishihara S., Karim Rumi M.A., Moriyama N., Kazumori H., Suetsugu H., Sato H., Fukuda R., Adachi K., Shibata M., Onodera S., Chiba T., and Kinoshita Y. Localization of calcitonin gene-related peptide receptors in rat gastric mucosa. Peptides 23 (2002) 955-966
31. Tubaro E., Belogi L., and Mezzadri C.M. The mechanism of action of amtolmetin guacyl, a new gastroprotective nonsteroidal anti-inflammatory drug. Eur J Pharmacol 387 (2000) 233-244
32. Zaki M., Koduru S., McCuen R., Vuyyuru L., and Schubert M.L. Amylin, released from the gastric fundus, stimulates somatostatin and thus inhibits histamine and acid secretion in mice. Gastroenterology 123 (2002) 247-255
33. Arai K., Ohno T., Saeki T., Mizuguchi S., Kamata K., Hayashi I., Saigenji K., Murata T., Narumiya S., and Majima M. Endogenous prostaglandin I2 regulates the neural emergency system through release of calcitonin gene related peptide. Gut 52 (2003) 1242-1249
34. Salomone S., Caruso A., Martinez G., Cutuli V.M., Prato A., Bianchi A., Amico-Roxas M., and Clementi G. Secretory and vascular effects of adrenomedullin in gastric ulcer: role of CGRP- and adrenomedullin-receptors. Peptides 24 (2003) 1175-1180
35. Vongthavaravat V., Mesiya S., Saymeh L., Xia Y., and Harty R.F. Mechanisms of transforming growth factor-alpha (TGF-alpha) induced gastroprotection against ethanol in the rat: roles of sensory neurons, sensory neuropeptides, and prostaglandins. Dig Dis Sci 48 (2003) 329-333
36. Cantarella G., Martinez G., Cutuli V.M., Loreto C., D'Alcamo M., Prato A., Amico-Roxas M., Bernardini R., and Clementi G. Adrenomedullin modulates COX-2 and HGF expression in reserpine-injuried gastric mucosa in the rat. Eur J Pharmacol 518 (2005) 221-226
37. Polidori C., Massi M., Guerrini R., Grandi D., Lupo D., and Morini G. Peripheral mechanisms involved in gastric mucosal protection by intracerebroventricular and intraperitoneal nociceptin in rats. Endocrinology 146 (2005) 3861-3867
38. Isbil-Buyukcoskun N., Gulec G., Cam-Etoz B., and Ozluk K. Peripheral GLP-1 gastroprotection against ethanol: the role of exendin, NO, CGRP, prostaglandins and blood flow. Regul Pept 152 (2009) 22-27
39. Isbil Buyukcoskun N., Gulec G., Cam Etoz B., and Ozluk K. Central effects of glucagon-like peptide-1 on cold-restraint stress-induced gastric mucosal lesions. Turk J Gastroenterol 18 (2007) 150-156
40. Brzozowski T., Konturek P.C., Chlopicki S., Sliwowski Z., Pawlik M., Ptak-Belowska A., Kwiecien S., Drozdowicz D., Pajdo R., Slonimska E., Konturek S.J., and Pawlik W.W. Therapeutic potential of 1-methylnicotinamide against acute gastric lesions induced by stress: role of endogenous prostacyclin and sensory nerves. J Pharmacol Exp Ther 326 (2008) 105-116
41. Minowa S., Tsuchiya S., Someya A., Horie S., and Murayama T. Role of neuropeptide receptor systems in vanilloid VR1 receptor-mediated gastric acid secretion in rat brain. Eur J Pharmacol 486 (2004) 317-324
42. Brzozowski T., Konturek P.C., Konturek S.J., Pierzchalski P., Bielanski W., Pajdo R., Drozdowicz D., Kwiecien S., and Hahn E.G. Central leptin and cholecystokinin in gastroprotection against ethanol-induced damage. Digestion 62 (2000) 126-142
43. Brzozowski T., Konturek P.C., Pajdo R., Kwiecien S., Ptak A., Sliwowski Z., Drozdowicz D., Pawlik M., Konturek S.J., and Hahn E.G. Brain-gut axis in gastroprotection by leptin and cholecystokinin against ischemia-reperfusion induced gastric lesions. J Physiol Pharmacol 52 (2001) 583-602
44. Guidobono F., Pagani F., Sibilia V., Soglian A., Rapetti D., and Netti C. The role of sensory neurons in the antiulcer effect of centrally injected amylin in rat. Peptides 21 (2000) 1537-1541
45. Gyires K. Gastric mucosal protection: from prostaglandins to gene-therapy. Curr Med Chem 12 (2005) 203-215
46. Bulloch K., Milner T.A., Prasad A., Hsu M., Buzsaki G., and McEwen B.S. Induction of calcitonin gene-related peptide-like immunoreactivity in hippocampal neurons following ischemia: a putative regional modulator of the CNS injury/immune response. Exp Neurol 150 (1998) 195-205
47. Sugiyama T., Hatanaka Y., Iwatani Y., Jin X., and Kawasaki H. Lafutidine facilitates calcitonin gene-related peptide (CGRP) nerve-mediated vasodilation via vanilloid-1 receptors in rat mesenteric resistance arteries. J Pharmacol Sci 106 (2008) 505-511
48. Boku K., Ohno T., Saeki T., Hayashi H., Hayashi I., Katori M., Murata T., Narumiya S., Saigenji K., and Majima M. Adaptive cytoprotection mediated by prostaglandin I(2) is attributable to sensitization of CRGP-containing sensory nerves. Gastroenterology 120 (2001) 134-143
49. Brzozowska I., Konturek P.C., Brzozowski T., Konturek S.J., Kwiecien S., Pajdo R., Drozdowicz D., Pawlik M., Ptak A., and Hahn E.G. Role of prostaglandins, nitric oxide, sensory nerves and gastrin in acceleration of ulcer healing by melatonin and its precursor, L-tryptophan. J Pineal Res 32 (2002) 149-162
50. Brzozowski T., Konturek P.C., Drozdowicz D., Konturek S.J., Pawlik M., Sliwowski Z., Pawlik W.W., and Hahn E.G. Role of central and peripheral ghrelin in the mechanism of gastric mucosal defence. Inflammopharmacol 13 (2005) 45-62
51. Brzozowski T., Konturek P.C., Konturek S.J., Brzozowska I., and Pawlik T. Role of prostaglandins in gastroprotection and gastric adaptation. J Physiol Pharmacol 56 Suppl 5 (2005) 33-55
52. Zayachkivska O.S., Konturek S.J., Drozdowicz D., Konturek P.C., Brzozowski T., and Ghegotsky M.R. Gastroprotective effects of flavonoids in plant extracts. J Physiol Pharmacol 56 Suppl 1 (2005) 219-231
53. Kawai J., Ando K., Shimosawa T., Harii K., and Fujita T. Regional hemodynamic effects of adrenomedullin in Wistar rats: a comparison with calcitonin gene-related peptide. Hypertens Res 25 (2002) 441-446
54. Imatake K., Matsui T., and Moriyama M. The effect and mechanism of action of capsaicin on gastric acid output. J Gastroenterol 44 (2009) 396-404
55. Preston G.M., and Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci U S A 88 (1991) 11110-11114
56. Jung J.S., Bhat R.V., Preston G.M., Guggino W.B., Baraban J.M., and Agre P. Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci U S A 91 (1994) 13052-13056
57. Papadopoulos M.C., Krishna S., and Verkman A.S. Aquaporin water channels and brain edema. Mt Sinai J Med 69 (2002) 242-248
58. Solenov E., Watanabe H., Manley G.T., and Verkman A.S. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286 (2004) C426-C432
59. Fujita A., Horio Y., Nielsen S., Nagelhus E.A., Hata F., Ottersen O.P., and Kurachi Y. High-resolution immunogold cytochemistry indicates that AQP4 is concentrated along the basal membrane of parietal cell in rat stomach. FEBS Lett 459 (1999) 305-309
60. Ma T., and Verkman A.S. Aquaporin water channels in gastrointestinal physiology. J Physiol 517 Pt 2 (1999) 317-326
61. Zelenin S., Gunnarson E., Alikina T., Bondar A., and Aperia A. Identification of a new form of AQP4 mRNA that is developmentally expressed in mouse brain. Pediatr Res 48 (2000) 335-339
62. Madrid R., Le Maout S., Barrault M.B., Janvier K., Benichou S., and Merot J. Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J 20 (2001) 7008-7021
63. Hull M.A., Brough J.L., Powe D.G., Carter G.I., Jenkins D., and Hawkey C.J. Expression of basic fibroblast growth factor in intact and ulcerated human gastric mucosa. Gut 43 (1998) 525-536
64. Ernst H., Konturek P.C., Hahn E.G., Stosiek H.P., Brzozowski T., and Konturek S.J. Effect of local injection with basic fibroblast growth factor (BFGF) and neutralizing antibody to BFGF on gastric ulcer healing, gastric secretion, angiogenesis and gastric blood flow. J Physiol Pharmacol 52 (2001) 377-390
65. Wierzbicki M., and Brzezinska-Blaszczyk E. The role of mast cells in the development of inflammatory bowel diseases. Postepy Hig Med Dosw (Online) 62 (2008) 642-650
66. Rydning A., Lyng O., Falkmer S., and Gronbech J.E. Histamine is involved in gastric vasodilation during acid back diffusion via activation of sensory neurons. Am J Physiol Gastrointest Liver Physiol 283 (2002) G603-G611
67. O'Connor T.M., O'Connell J., O'Brien D.I., Goode T., Bredin C.P., and Shanahan F. The role of substance P in inflammatory disease. J Cell Physiol 201 (2004) 167-180
68. Okayama T., Yoshida N., Uchiyama K., Takagi T., Ichikawa H., and Yoshikawa T. Mast cells are involved in the pathogenesis of indomethacin-induced rat enteritis. J Gastroenterol 44 Suppl 19 (2009) 35-39
69. Filaretova L. The hypothalamic-pituitary-adrenocortical system: hormonal brain-gut interaction and gastroprotection. Auton Neurosci 125 (2006) 86-93