Repeated administration of exendin-4 reduces focal cerebral ischemia-induced infarction in rats

Brain Research

Volumn 1427, Issue , 2012, Pages 23-34

  Briyal, Seema ^a   Gulati, Kartike ^b,c   Gulati, Anil ^a  

^a MIDWESTERN UNIVERSITY   (United States)

^b MIDWESTERN UNIVERSITY   (United States)

^c Mount Clemens Regional Medical Center   (United States)

Author keywords

BQ123; Cerebral ischemia; Endothelin; Exendin 4; GLP 1; Middle cerebral artery occlusion

Indexed keywords

CYCLO(DEXTRO TRYPTOPHYL DEXTRO ASPARTYLPROLYL DEXTRO VALYLLEUCYL); ENDOTHELIN A RECEPTOR; ENDOTHELIN B RECEPTOR; EXENDIN 4; GLUTATHIONE; MALONALDEHYDE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; GRIP STRENGTH; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROTAROD TEST; SCORING SYSTEM; TREATMENT DURATION;

ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; DOWN-REGULATION; DRUG ADMINISTRATION SCHEDULE; MALE; NEUROPROTECTIVE AGENTS; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; VENOMS;

RATTUS;

EID: 82955195404     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.10.026     Document Type: Article

References (71)

1. A. Arboix, A. Rivas, L. Garcia-Eroles, L. de Marcos, J. Massons, and M. Oliveres Cerebral infarction in diabetes: clinical pattern, stroke subtypes, and predictors of in-hospital mortality BMC Neurol. 5 2005 9
2. L.L. Baggio, and D.J. Drucker Biology of incretins: GLP-1 and GIP Gastroenterology 132 2007 2131 2157 (Pubitemid 46711096)
3. T.A. Baird, M.W. Parsons, P.A. Barber, K.S. Butcher, P.M. Desmond, B.M. Tress, P.G. Colman, G. Jerums, B.R. Chambers, and S.M. Davis The influence of diabetes mellitus and hyperglycaemia on stroke incidence and outcome J. Clin. Neurosci. 9 2002 618 626 (Pubitemid 35364730)
4. T.A. Baird, M.W. Parsons, T. Phanh, K.S. Butcher, P.M. Desmond, B.M. Tress, P.G. Colman, B.R. Chambers, and S.M. Davis Persistent poststroke hyperglycemia is independently associated with infarct expansion and worse clinical outcome Stroke 34 2003 2208 2214 (Pubitemid 37099838)
5. W.A. Banks, M.J. During, and M.L. Niehoff Brain uptake of the glucagon-like peptide-1 antagonist exendin(9-39) after intranasal administration J. Pharmacol. Exp. Ther. 309 2004 469 475 (Pubitemid 38542596)
6. F.C. Barone, E.H. Ohlstein, A.J. Hunter, C.A. Campbell, S.H. Hadingham, A.A. Parsons, Y. Yang, and E. Shohami Selective antagonism of endothelin-A-receptors improves outcome in both head trauma and focal stroke in rat J. Cardiovasc. Pharmacol. 36 2000 S357 S361
7. G.I. Bell, R. Sanchez-Pescador, P.J. Laybourn, and R.C. Najarian Exon duplication and divergence in the human preproglucagon gene Nature 304 1983 368 371 (Pubitemid 13072761)
8. S.C. Biswas, J. Buteau, and L.A. Greene Glucagon-like peptide-1 (GLP-1) diminishes neuronal degeneration and death caused by NGF deprivation by suppressing Bim induction Neurochem. Res. 33 2008 1845 1851
9. S. Briyal, A. Gulati, and Y.K. Gupta Effect of combination of endothelin receptor antagonist (TAK-044) and aspirin in middle cerebral artery occlusion model of acute ischemic stroke in rats Methods Find. Exp. Clin. Pharmacol. 29 2007 257 263 (Pubitemid 47204046)
10. S. Briyal, and A. Gulati Endothelin-A receptor antagonist BQ123 potentiates acetaminophen induced hypothermia and reduces infarction following focal cerebral ischemia in rats Eur. J. Pharmacol. 644 2010 73 79
11. S. Briyal, T. Philip, and A. Gulati Endothelin-A receptor antagonists prevent amyloid-beta-induced increase in ETA receptor expression, oxidative stress, and cognitive impairment J. Alzheimers Dis. 23 2011 491 503
12. L. Brunetti, G. Orlando, L. Recinella, S. Leone, C. Ferrante, A. Chiavaroli, F. Lazzarin, and M. Vacca Glucagon-like peptide 1 (7-36) amide (GLP-1) and exendin-4 stimulate serotonin release in rat hypothalamus Peptides 29 2008 1377 1381
13. A. Bruno, S.R. Levine, M.R. Frankel, T.G. Brott, Y. Lin, B.C. Tilley, P.D. Lyden, J.P. Broderick, T.G. Kwiatkowski, and S.E. Fineberg Admission glucose level and clinical outcomes in the NINDS rt-PA Stroke Trial Neurology 59 2002 669 674
14. A. Chamorro, and J. Hallenbeck The harms and benefits of inflammatory and immune responses in vascular disease Stroke 37 2006 291 293 (Pubitemid 43731945)
15. P.H. Chan Role of oxidants in ischemic brain damage Stroke 27 1996 1124 1129 (Pubitemid 26177617)
16. M.J. During, L. Cao, D.S. Zuzga, J.S. Francis, H.L. Fitzsimons, X. Jiao, R.J. Bland, M. Klugmann, W.A. Banks, D.J. Drucker, and C.N. Haile Glucagon-like peptide-1 receptor is involved in learning and neuroprotection Nat. Med. 9 2003 1173 1179 (Pubitemid 37173702)
17. G.L. Ellman Tissue sulfhydryl groups Arch. Biochem. Biophys. 82 1959 70 77
18. G. Feuerstein, J.L. Gu, E.H. Ohlstein, F.C. Barone, and T.L. Yue Peptidic endothelin-1 receptor antagonist, BQ-123, and neuroprotection Peptides 15 1994 467 469 (Pubitemid 24223323)
19. E.S. Flamm, H.B. Demopoulos, M.L. Seligman, R.G. Poser, and J. Ransohoff Free radicals in cerebral ischemia Stroke 9 1978 445 447 (Pubitemid 8389070)
20. R. Goke, P.J. Larsen, J.D. Mikkelsen, and S.P. Sheikh Distribution of GLP-1 binding sites in the rat brain: evidence that exendin-4 is a ligand of brain GLP-1 binding sites Eur. J. Neurosci. 7 1995 2294 2300
21. C.S. Gray, A.J. Hildreth, G.K. Alberti, and J.E. O'Connell Poststroke hyperglycemia: natural history and immediate management Stroke 35 2004 122 126 (Pubitemid 38057604)
22. W. Guan, A. Kozak, and S.C. Fagan Drug repurposing for vascular protection after acute ischemic stroke Acta Neurochir. Suppl. 111 2011 295 298
23. A. Gulati, A.C. Sharma, G. Robbie, and P.R. Saxena Endothelin ETA receptor antagonist, BQ-123, blocks the vasoconstriction induced by sarafotoxin 6b in the heart but not in other vascular beds Gen. Pharmacol. 26 1995 183 193
24. A. Gulati, A.C. Sharma, and G. Singh Role of endothelin in the cardiovascular effects of diaspirin crosslinked and stroma reduced hemoglobin Crit. Care Med. 24 1996 137 147
25. Y.K. Gupta, S. Briyal, U. Sharma, N.R. Jagannathan, and A. Gulati Effect of endothelin antagonist (TAK-044) on cerebral ischemic volume, oxidative stress markers and neurobehavioral parameters in the middle cerebral artery occlusion model of stroke in rats Life Sci. 77 2005 15 27 (Pubitemid 40546373)
26. S.L. Jin, V.K. Han, J.G. Simmons, A.C. Towle, J.M. Lauder, and P.K. Lund Distribution of glucagonlike peptide I (GLP-I), glucagon, and glicentin in the rat brain: an immunocytochemical study J. Comp. Neurol. 271 1988 519 532
27. P. Kakkar, B. Das, and P.N. Viswanathan A modified spectrophotometric assay of superoxide dismutase Indian J. Biochem. Biophys. 21 1984 130 132 (Pubitemid 15207169)
28. S. Kim, M. Moon, and S. Park Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease J. Endocrinol. 202 2009 431 439
29. H. Kinouchi, C.J. Epstein, T. Mizui, E. Carlson, S.F. Chen, and P.H. Chan Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase Proc. Natl. Acad. Sci. U. S. A. 88 1991 11158 11162 (Pubitemid 21915999)
30. J. Koizumi, Y. Yoshida, T. Nakazawa, and G. Ooneda Experimental studies of ischemic brain edema. 1. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area Jpn. J. Stroke 8 1986 1 8
31. M.G. Lansberg, V.N. Thijs, R. Bammer, S. Kemp, C.A. Wijman, M.P. Marks, and G.W. Albers Risk factors of symptomatic intracerebral hemorrhage after tPA therapy for acute stroke Stroke 38 2007 2275 2278 (Pubitemid 47457568)
32. P.J. Larsen, M. Tang-Christensen, J.J. Holst, and C. Orskov Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem Neuroscience 77 1997 257 270 (Pubitemid 27060323)
33. M.E. Lee, S.M. de la Monte, S.C. Ng, K.D. Bloch, and T. Quertermous Expression of the potent vasoconstrictor endothelin in the human central nervous system J. Clin. Invest. 86 1990 141 147 (Pubitemid 20226986)
34. J.J. Legos, S.C. Lenhard, R.E. Haimbach, T.R. Schaeffer, R.G. Bentley, M.J. McVey, S. Chandra, E.A. Irving, A.P. Andrew, and F.C. Barone SB 234551 selective ET(A) receptor antagonism: perfusion/diffusion MRI used to define treatable stroke model, time to treatment and mechanism of protection Exp. Neurol. 212 2008 53 62
35. R. Leigh, O.O. Zaidat, M.F. Suri, G. Lynch, S. Sundararajan, J.L. Sunshine, R. Tarr, W. Selman, D.M. Landis, and J.I. Suarez Predictors of hyperacute clinical worsening in ischemic stroke patients receiving thrombolytic therapy Stroke 35 2004 1903 1907 (Pubitemid 38971873)
36. R.R. Leker, M. Aharonowiz, N.H. Greig, and H. Ovadia The role of p53-induced apoptosis in cerebral ischemia: effects of the p53 inhibitor pifithrin alpha Exp. Neurol. 187 2004 478 486 (Pubitemid 38610294)
37. F. Li, K. Irie, M.S. Anwer, and M. Fisher Delayed triphenyltetrazolium chloride staining remains useful for evaluating cerebral infarct volume in a rat stroke model J. Cereb. Blood Flow Metab. 17 1997 1132 1135 (Pubitemid 27459342)
38. Y. Li, T. Hansotia, B. Yusta, F. Ris, P.A. Halban, and D.J. Drucker Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis J. Biol. Chem. 278 2003 471 478 (Pubitemid 36043598)
39. Y. Li, T. Perry, M.S. Kindy, B.K. Harvey, D. Tweedie, H.W. Holloway, K. Powers, H. Shen, J.M. Egan, K. Sambamurti, A. Brossi, D.K. Lahiri, M.P. Mattson, B.J. Hoffer, Y. Wang, and N.H. Greig GLP-1 receptor stimulation preserves primary cortical and dopaminergic neurons in cellular and rodent models of stroke and Parkinsonism Proc. Natl. Acad. Sci. U. S. A. 106 2009 1285 1290
40. P.J. Lindsberg, and R.O. Roine Hyperglycemia in acute stroke Stroke 35 2004 363 364 (Pubitemid 38174407)
41. C.C. Liu, Z.C. Chen, B.C. Cheng, and M.T. Lin Prior antagonism of endothelin-1A receptors alleviates circulatory shock and cerebral ischemia during rat heatstroke J. Pharmacol. Sci. 96 2004 177 187
42. J.A. Lovshin, and D.J. Drucker Incretin-based therapies for type 2 diabetes mellitus Nat. Rev. Endocrinol. 5 2009 262 269
43. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
44. C.G. Markgraf, E.J. Green, B.E. Hurwitz, E. Morikawa, W.D. Dietrich, P.M. McCabe, M.D. Ginsberg, and N. Schneiderman Sensorimotor and cognitive consequences of middle cerebral artery occlusion in rats Brain Res. 575 1992 238 246
45. P.L. McClean, V.A. Gault, P. Harriott, and C. Holscher Glucagon-like peptide-1 analogues enhance synaptic plasticity in the brain: a link between diabetes and Alzheimer's disease Eur. J. Pharmacol. 630 2010 158 162
46. I. Merchenthaler, M. Lane, and P. Shughrue Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system J. Comp. Neurol. 403 1999 261 280 (Pubitemid 28566834)
47. P.M. Moran, L.S. Higgins, B. Cordell, and P.C. Moser Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human beta-amyloid precursor protein Proc. Natl. Acad. Sci. U. S. A. 92 1995 5341 5345
48. P.K. Myint, S. Sinha, N.J. Wareham, S.A. Bingham, R.N. Luben, A.A. Welch, and K.T. Khaw Glycated hemoglobin and risk of stroke in people without known diabetes in the European Prospective Investigation into Cancer (EPIC)-Norfolk prospective population study: a threshold relationship? Stroke 38 2007 271 275 (Pubitemid 46184293)
49. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358 (Pubitemid 9194347)
50. A.A. Owji, Z. Khoshdel, F. Sanea, M.R. Panjehshahin, M. Shojaee Fard, D.M. Smith, H.A. Coppock, M.A. Ghatei, and S.R. Bloom Effects of intracerebroventricular injection of glucagon like peptide-1 and its related peptides on serotonin metabolism and on levels of amino acids in the rat hypothalamus Brain Res. 929 2002 70 75 (Pubitemid 34164410)
51. T. Perry, N.J. Haughey, M.P. Mattson, J.M. Egan, and N.H. Greig Protection and reversal of excitotoxic neuronal damage by glucagon-like peptide-1 and exendin-4 J. Pharmacol. Exp. Ther. 302 2002 881 888 (Pubitemid 34920207)
52. T. Perry, and N.H. Greig The glucagon-like peptides: a double-edged therapeutic sword? Trends Pharmacol. Sci. 24 2003 377 383 (Pubitemid 37315530)
53. T. Perry, D.K. Lahiri, K. Sambamurti, D. Chen, M.P. Mattson, J.M. Egan, and N.H. Greig 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 2003 603 612 (Pubitemid 36578646)
54. M.J. Robinson, I.M. Macrae, M. Todd, J.L. Reid, and J. McCulloch Reduction of local cerebral blood flow to pathological levels by endothelin-1 applied to the middle cerebral artery in the rat Neurosci. Lett. 118 1990 269 272 (Pubitemid 20334893)
55. D.C. Rogers, C.A. Campbell, J.L. Stretton, and K.B. Mackay Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat Stroke 28 1997 2060 2065 (discussion 2066)
56. L. Ryden, E. Standl, M. Bartnik, G. Van den Berghe, J. Betteridge, M.J. de Boer, F. Cosentino, B. Jonsson, M. Laakso, K. Malmberg, S. Priori, J. Ostergren, J. Tuomilehto, I. Thrainsdottir, I. Vanhorebeek, M. Stramba-Badiale, P. Lindgren, Q. Qiao, S.G. Priori, J.J. Blanc, A. Budaj, J. Camm, V. Dean, J. Deckers, K. Dickstein, J. Lekakis, K. McGregor, M. Metra, J. Morais, A. Osterspey, J. Tamargo, J.L. Zamorano, J.W. Deckers, M. Bertrand, B. Charbonnel, E. Erdmann, E. Ferrannini, A. Flyvbjerg, H. Gohlke, J.R. Juanatey, I. Graham, P.F. Monteiro, K. Parhofer, K. Pyorala, I. Raz, G. Schernthaner, M. Volpe, and D. Wood Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: executive summary. The Task Force on Diabetes and Cardiovascular Diseases of the European Society of Cardiology (ESC) and of the European Association for the Study of Diabetes (EASD) Eur. Heart J. 28 2007 88 136 (Pubitemid 46137814)
57. S. Sarkar, C. Fekete, G. Legradi, and R.M. Lechan Glucagon like peptide-1 (7-36) amide (GLP-1) nerve terminals densely innervate corticotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus Brain Res. 985 2003 163 168 (Pubitemid 37088181)
58. F. Satoh, S.A. Beak, C.J. Small, M. Falzon, M.A. Ghatei, S.R. Bloom, and D.M. Smith Characterization of human and rat glucagon-like peptide-1 receptors in the neurointermediate lobe: lack of coupling to either stimulation or inhibition of adenylyl cyclase Endocrinology 141 2000 1301 1309 (Pubitemid 32269096)
59. J.W. Schmidley Free radicals in central nervous system ischemia Stroke 21 1990 1086 1090 (Pubitemid 20218176)
60. J.F. Scott, G.M. Robinson, J.M. French, J.E. O'Connell, K.G. Alberti, and C.S. Gray Prevalence of admission hyperglycaemia across clinical subtypes of acute stroke Lancet 353 1999 376 377 (Pubitemid 29088169)
61. E. Selvin, J. Coresh, E. Shahar, L. Zhang, M. Steffes, and A.R. Sharrett Glycaemia (haemoglobin A1c) and incident ischaemic stroke: the Atherosclerosis Risk in Communities (ARIC) Study Lancet Neurol. 4 2005 821 826 (Pubitemid 41619437)
62. M. Spatz, Y. Yasuma, A. Strasser, and R.M. McCarron Cerebral postischemic hypoperfusion is mediated by ETA receptors Brain Res. 726 1996 242 246 (Pubitemid 26292253)
63. E.A. Spencer, K.L. Pirie, R.J. Stevens, V. Beral, A. Brown, B. Liu, J. Green, and G.K. Reeves Diabetes and modifiable risk factors for cardiovascular disease: the prospective Million Women Study Eur. J. Epidemiol. 23 2008 793 799
64. R.J. Stevens, R.L. Coleman, A.I. Adler, I.M. Stratton, D.R. Matthews, and R.R. Holman Risk factors for myocardial infarction case fatality and stroke case fatality in type 2 diabetes: UKPDS 66 Diabetes Care 27 2004 201 207 (Pubitemid 38196733)
65. T. Sugawara, M. Fujimura, N. Noshita, G.W. Kim, A. Saito, T. Hayashi, P. Narasimhan, C.M. Maier, and P.H. Chan Neuronal death/survival signaling pathways in cerebral ischemia NeuroRx. 1 2004 17 25 (Pubitemid 46589339)
66. T. Tatlisumak, R.A. Carano, K. Takano, T.J. Opgenorth, C.H. Sotak, and M. Fisher A novel endothelin antagonist, A-127722, attenuates ischemic lesion size in rats with temporary middle cerebral artery occlusion: a diffusion and perfusion MRI study Stroke 29 1998 850 857 discussion 857-8
67. S. Teramoto, N. Miyamoto, K. Yatomi, Y. Tanaka, H. Oishi, H. Arai, N. Hattori, and T. Urabe Exendin-4, a glucagon-like peptide-1 receptor agonist, provides neuroprotection in mice transient focal cerebral ischemia J. Cereb. Blood Flow Metab. 31 2011 1696 1705
68. M.D. Turton, D. O'Shea, I. Gunn, S.A. Beak, C.M. Edwards, K. Meeran, S.J. Choi, G.M. Taylor, M.M. Heath, P.D. Lambert, J.P. Wilding, D.M. Smith, M.A. Ghatei, J. Herbert, and S.R. Bloom A role for glucagon-like peptide-1 in the central regulation of feeding Nature 379 1996 69 72 (Pubitemid 26008136)
69. I. Viossat, D. Duverger, M. Chapelat, E. Pirotzky, P.E. Chabrier, and P. Braquet Elevated tissue endothelin content during focal cerebral ischemia in the rat J. Cardiovasc. Pharmacol. 22 Suppl 8 1993 S306 S309
70. J.P. Whisnant, D.O. Wiebers, W.M. O'Fallon, J.D. Sicks, and R.L. Frye A population-based model of risk factors for ischemic stroke: Rochester, Minnesota Neurology 47 1996 1420 1428 (Pubitemid 26422530)
71. R.N. Willette, E.H. Ohlstein, M. Pullen, C.F. Sauermelch, A. Cohen, and P. Nambi Transient forebrain ischemia alters acutely endothelin receptor density and immunoreactivity in gerbil brain Life Sci. 52 1993 35 40 (Pubitemid 223039981)