Exendin-4, a glucagon-like peptide-1 receptor agonist, provides neuroprotection in mice transient focal cerebral ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 31, Issue 8, 2011, Pages 1696-1705

  Teramoto, Shinichiro ^a   Miyamoto, Nobukazu ^a   Yatomi, Kenji ^a   Tanaka, Yasutaka ^a   Oishi, Hidenori ^a   Arai, Hajime ^a   Hattori, Nobutaka ^a   Urabe, Takao ^a  

^a JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cyclic AMP pathway; glucagon like peptide 1 receptor agonist; ischemia reperfusion injury; neuroprotection; oxidative stress

Indexed keywords

CYCLIC AMP; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE; INSULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; CONTROLLED STUDY; CYCLIC AMP BLOOD LEVEL; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN BLOOD LEVEL; MALE; NERVE CELL NECROSIS; NEUROPHYSIOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; SHAM PROCEDURE; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; CYCLIC AMP; GLUCAGON-LIKE PEPTIDE 1; INFLAMMATION; ISCHEMIC ATTACK, TRANSIENT; MICE; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PEPTIDES; VENOMS;

EID: 79960996273     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2011.51     Document Type: Article

References (39)

1. Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF (2004) Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 18:869-71
2. Baggio LL, Drucker DJ (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132:2131-57
3. Baggio LL, Huang Q, Brown TJ, Drucker DJ (2004) A recombinant human glucagon-like peptide (GLP)-1-albumin protein (albugon) mimics peptidergic activation of GLP-1 receptor-dependent pathways coupled with satiety, gastrointestinal motility, and glucose homeostasis. Diabetes 53:2492-500 (Pubitemid 39145610)
4. Bertilsson G, Patrone C, Zachrisson O, Andersson A, Dannaeus K, Heidrich J, Kortesmaa J, Mercer A, Nielsen E, Ronnholm H, Wikstrom L (2008) Peptide hormone exendin-4 stimulates subventricular zone neurogenesis in the adult rodent brain and induces recovery in an animal model of Parkinson's disease. J Neurosci Res 86:326-38 (Pubitemid 351196738)
5. Bose AK, Mocanu MM, Carr RD, Brand CL, Yellon DM (2005) Glucagon-like peptide 1 can directly protect the heart against ischemia/reperfusion injury. Diabetes 54:146-51 (Pubitemid 40105106)
6. Bruno A, Levine SR, Frankel MR, Brott TG, Lin Y, Tilley BC, Lyden PD, Broderick JP, Kwiatkowski TG, Fineberg SE (2002) Admission glucose level and clinical outcomes in the NINDS rt-PA Stroke Trial. Neurology 59:669-74
7. Choi JM, Shin HK, Kim KY, Lee JH, Hong KW (2002) Neuroprotective effect of cilostazol against focal cerebral ischemia via antiapoptotic action in rats. J Pharmacol Exp Ther 300:787-93 (Pubitemid 34164980)
8. During MJ, Cao L, Zuzga DS, Francis JS, Fitzsimons HL, Jiao X, Bland RJ, Klugmann M, Banks WA, Drucker DJ, Haile CN (2003) Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 9:1173-9 (Pubitemid 37173702)
9. Hara H, Huang PL, Panahian N, Fishman MC, Moskowitz MA (1996) Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J Cereb Blood Flow Metab 16:605-11 (Pubitemid 26227069)
10. Harkavyi A, Abuirmeileh A, Lever R, Kingsbury AE, Biggs CS, Whitton PS (2008) Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease. J Neuroinflammation 5:19
11. Hassan M, Eskilsson A, Nilsson C, Jonsson C, Jacobsson H, Refai E, Larsson S, Efendic S (1999) In vivo dynamic distribution of 131I-glucagon-like peptide-1 (7-36) amide in the rat studied by gamma camera. Nucl Med Biol 26:413-20 (Pubitemid 29254028)
12. Hui L, Pei DS, Zhang QG, Guan QH, Zhang GY (2005) The neuroprotection of insulin on ischemic brain injury in rat hippocampus through negative regulation of JNK signaling pathway by PI3K/Akt activation. Brain Res 1052:1-9 (Pubitemid 41116281)
13. Kamada H, Yu F, Nito C, Chan PH (2007) Influence of hyperglycemia on oxidative stress and matrix metallo-proteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 38:1044-9 (Pubitemid 46568472)
14. Kastin AJ, Akerstrom V (2003) Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord 27:313-8 (Pubitemid 36384867)
15. Kastin AJ, Akerstrom V, Pan W (2002) Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 18:7-14 (Pubitemid 34252619)
16. Kitagawa K (2007) CREB and cAMP response element-mediated gene expression in the ischemic brain. FEBS J 274:3210-7 (Pubitemid 47024985)
17. Love S (1999) Oxidative stress in brain ischemia. Brain Pathol 9:119-31 (Pubitemid 29056523)
18. Meeran K, O'Shea D, Edwards CM, Turton MD, Heath MM, Gunn I, Abusnana S, Rossi M, Small CJ, Goldstone AP, Taylor GM, Sunter D, Steere J, Choi SJ, Ghatei MA, Bloom SR (1999) Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat. Endocrinology 140:244-50 (Pubitemid 29011165)
19. Miyamoto N, Tanaka R, Shimosawa T, Yatomi Y, Fujita T, Hattori N, Urabe T (2009) Protein kinase A-dependent suppression of reactive oxygen species in transient focal ischemia in adrenomedullin-deficient mice. J Cereb Blood Flow Metab 29:1769-79
20. Miyamoto N, Zhang N, Tanaka R, Liu M, Hattori N, Urabe T (2008) Neuroprotective role of angiotensin II type 2 receptor after transient focal ischemia in mice brain. Neurosci Res 61:249-56
21. Perry T, Greig NH (2003) The glucagon-like peptides: a double-edged therapeutic sword? Trends Pharmacol Sci 24:377-83 (Pubitemid 37315530)
22. Perry T, Haughey NJ, Mattson MP, Egan JM, Greig NH (2002a) Protection and reversal of excitotoxic neuronal damage by glucagon-like peptide-1 and exendin-4. J Pharmacol Exp Ther 302:881-8 (Pubitemid 34920207)
23. Perry T, Lahiri DK, Chen D, Zhou J, Shaw KT, Egan JM, Greig NH (2002b) A novel neurotrophic property of glucagon-like peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells. J Pharmacol Exp Ther 300:958-66 (Pubitemid 34165002)
24. Perry T, Lahiri DK, Sambamurti K, Chen D, Mattson MP, Egan JM, Greig NH (2003) Glucagon-like peptide-1 decreases endogenous amyloid-beta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 72:603-12 (Pubitemid 36578646)
25. Peters O, Back T, Lindauer U, Busch C, Megow D, Dreier J, Dirnagl U (1998) Increased formation of reactive oxygen species after permanent and reversible middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 18:196-205 (Pubitemid 28082517)
26. Raab EL, Vuguin PM, Stoffers DA, Simmons RA (2009) Neonatal exendin-4 treatment reduces oxidative stress and prevents hepatic insulin resistance in intrauterine growth-retarded rats. Am J Physiol Regul Integr Comp Physiol 297:R1785-94
27. Rizk NN, Rafols JA, Dunbar JC (2006) Cerebral ischemia-induced apoptosis and necrosis in normal and diabetic rats: effects of insulin and C-peptide. Brain Res 1096:204-12 (Pubitemid 43928921)
28. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-48 (Pubitemid 28150661)
29. Szayna M, Doyle ME, Betkey JA, Holloway HW, Spencer RG, Greig NH, Egan JM (2000) Exendin-4 decelerates food intake, weight gain, and fat deposition in Zucker rats. Endocrinology 141:1936-41
30. Takei K, Tokuyama K, Kato M, Morikawa A (1998) Role of cyclic adenosine monophosphate in reducing superoxide anion generation in guinea pig alveolar macrophages. Pharmacology 57:1-7 (Pubitemid 28288862)
31. Tanaka K, Nagata E, Suzuki S, Dembo T, Nogawa S, Fukuuchi Y (1999) Immunohistochemical analysis of cyclic AMP response element binding protein phosphorylation in focal cerebral ischemia in rats. Brain Res 818:520-6 (Pubitemid 29229968)
32. Timmers L, Henriques JP, de Kleijn DP, Devries JH, Kemperman H, Steendijk P, Verlaan CW, Kerver M, Piek JJ, Doevendans PA, Pasterkamp G, Hoefer IE (2009) Exenatide reduces infarct size and improves cardiac function in a porcine model of ischemia and reperfusion injury. J Am Coll Cardiol 53:501-10
33. Tureyen K, Vemuganti R, Sailor KA, Dempsey RJ (2004) Infarct volume quantification in mouse focal cerebral ischemia: a comparison of triphenyltetrazolium chloride and cresyl violet staining techniques. J Neurosci Methods 139:203-7 (Pubitemid 39370846)
34. Turton MD, O'Shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JP, Smith DM, Ghatei MA, Herbert J, Bloom SR (1996) A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379: 69-72 (Pubitemid 26008136)
35. Walton M, Sirimanne E, Williams C, Gluckman P, Dragu-now M (1996) The role of the cyclic AMP-responsive element binding protein (CREB) in hypoxic-ischemic brain damage and repair. Brain Res Mol Brain Res 43:21-9 (Pubitemid 27042388)
36. Warner DS, Sheng H, Batinic-Haberle I (2004) Oxidants, antioxidants and the ischemic brain. J Exp Biol 207:3221-31 (Pubitemid 39275296)
37. Wei Y, Mojsov S (1995) Tissue-specific expression of the human receptor for glucagon-like peptide-I: brain, heart and pancreatic forms have the same deduced amino acid sequences. FEBS Lett 358:219-24
38. Yamada S, Funada T, Shibata N, Kobayashi M, Kawai Y, Tatsuda E, Furuhata A, Uchida K (2004) Protein-bound 4-hydroxy-2-hexenal as a marker of oxidized n-3 polyunsaturated fatty acids. J Lipid Res 45: 626-34 (Pubitemid 38405668)
39. Zander M, Madsbad S, Madsen JL, Holst JJ (2002) Effect of 6-week course of glucagon-like peptide 1 on glycaemic control, insulin sensitivity, and beta-cell function in type 2 diabetes: a parallel-group study. Lancet 359: 824-30 (Pubitemid 34233752)