PACAP and a novel stable analog protect rat brain from ischemia: Insight into the mechanisms of action

Peptides

Volumn 32, Issue 6, 2011, Pages 1207-1216

  Dejda, Agnieszka ^a,b   Seaborn, Tommy ^a,b   Bourgault, Steve ^a,b,c   Touzani, Omar ^d   Fournier, Alain ^b,c   Vaudry, Hubert ^a,b,e   Vaudry, David ^a,b,e  

^a UNIVERSITÉ DE ROUEN   (France)

^b INSERM   (France)

^c INRS INSTITUT ARMAND FRAPPIER   (Canada)

^d UNIVERSITÉ DE CAEN   (France)

^e University of Caen ^*  (France)

Author keywords

Apoptosis; Inflammation; Metabolically stable analog; Neuroprotection; Pituitary adenylate cyclase activating polypeptide (PACAP); Stroke

Indexed keywords

ACETYL(ALANINE 15,ALANINE 20)PITUITARY ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE 38 PROPYLAMIDE; CASPASE 3; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUROPROTECTIVE AGENT; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PROTECTION; CELL PROTECTION; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFICACY; GENE EXPRESSION REGULATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BRAIN; CASPASE 3; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG STABILITY; GENE EXPRESSION; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INTERLEUKIN-6; ISCHEMIA; MACROPHAGE INFLAMMATORY PROTEINS; MALE; NEUROPROTECTIVE AGENTS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STROKE; TUMOR NECROSIS FACTOR-ALPHA;

RATTUS;

EID: 79957989551     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2011.04.003     Document Type: Article

References (61)

1. R.M. Adibhatla, and J.F. Hatcher Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia Free Radic Biol Med 40 2006 376 387 (Pubitemid 43139673)
2. A. Arimura Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems Jpn J Physiol 48 1998 301 331 (Pubitemid 28566695)
3. W.A. Banks, A.J. Kastin, G. Komaki, and A. Arimura Passage of pituitary adenylate cyclase activating polypeptide1-27 and pituitary adenylate cyclase activating polypeptide1-38 across the blood-brain barrier J Pharmacol Exp Ther 26777 1993 690 696 (Pubitemid 23352525)
4. S. Bourgault, D. Vaudry, B. Botia, A. Couvineau, M. Laburthe, and H. Vaudry Novel stable PACAP analogs with potent activity towards the PAC1 receptor Peptides 29 2008 919 932
5. S. Bourgault, D. Vaudry, A. Dejda, N.D. Doan, H. Vaudry, and A. Fournier Pituitary adenylate cyclase-activating polypeptide: focus on structure-activity relationships of a neuroprotective peptide Curr Med Chem 16 2009 4462 4480
6. S. Bourgault, D. Vaudry, I. Ségalas-Milazzo, L. Guilhaudis, A. Couvineau, and M. Laburthe Molecular and conformational determinants of pituitary adenylate cyclase-activating polypeptide (PACAP) for activation of the PAC1 receptor J Med Chem 52 2009 3308 3316
7. J.S. Braun, K. Prass, U. Dirnagl, A. Meisel, and C. Meisel Protection from brain damage and bacterial infection in murine stroke by the novel caspase-inhibitor Q-VD-OPH Exp Neurol 206 2007 183 191 (Pubitemid 47103174)
8. W. Chen, V. Jadhav, J. Tang, and J.H. Zhang HIF-1alpha inhibition ameliorates neonatal brain injury in a rat pup hypoxic-ischemic model Neurobiol Dis 31 2008 433 441
9. Y. Chen, B. Samal, C.R. Hamelink, C.C. Xiang, Y. Chen, and M. Chen Neuroprotection by endogenous and exogenous PACAP following stroke Regul Pept 137 2006 4 19 (Pubitemid 44751193)
10. A. Dejda, V. Jolivel, S. Bourgault, T. Seaborn, A. Fournier, and H. Vaudry Inhibitory effect of PACAP on caspase activity in neuronal apoptosis: a better understanding towards therapeutic applications in neurodegenerative diseases J Mol Neurosci 36 2008 26 37
11. A. Dejda, P. Sokolowska, and J.Z. Nowak Neuroprotective potential of three neuropeptides PACAP, VIP and PHI Pharmacol Rep 57 2005 307 320 (Pubitemid 41030690)
12. G. Del Zoppo, I. Ginis, J.M. Hallenbeck, C. Iadecola, X. Wang, and G.Z. Feuerstein Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia Brain Pathol 10 2000 95 112 (Pubitemid 30056398)
13. M. Delgado, J. Leceta, and D. Ganea Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia J Leukoc Biol 73 2003 155 164 (Pubitemid 36125686)
14. C. Didelot, E. Schmitt, M. Brunet, L. Maingret, A. Parcellier, and C. Garrido Heat shock proteins: endogenous modulators of apoptotic cell death Handb Exp Pharmacol 172 2006 171 198
15. D. Dogrukol-Ak, V.B. Kumar, J.S. Ryerse, S.A. Farr, S. Verma, and N. Nonaka Isolation of peptide transport system-6 from brain endothelial cells: therapeutic effects with antisense inhibition in Alzheimer and stroke models J Cereb Blood Flow Metab 29 2009 411 422
16. D. Dogrukol-Ak, F. Tore, and N. Tuncel Passage of VIP/PACAP/secretin family across the blood-brain barrier: therapeutic effects Curr Pharm Des 10 2004 1325 1340 (Pubitemid 38559750)
17. K. Dohi, H. Mizushima, S. Nakajo, H. Ohtaki, S. Matsunaga, and T. Aruga Pituitary adenylate cyclase-activating polypeptide (PACAP) prevents hippocampal neurons from apoptosis by inhibiting JNK/SAPK and p38 signal transduction pathways Regul Pept 109 2002 83 88 (Pubitemid 35292398)
18. A. Falluel-Morel, N. Aubert, D. Vaudry, M. Basille, M. Fontaine, and A. Fournier Opposite regulation of the mitochondrial apoptotic pathway by C2-ceramide and PACAP through a MAP-kinase-dependent mechanism in cerebellar granule cells J Neurochem 91 2004 1231 1243 (Pubitemid 39587461)
19. T.B. Franklin, A.M. Krueger-Naug, D.B. Clarke, A.P. Arrigo, and R.W. Currie The role of heat shock proteins Hsp70 and Hsp27 in cellular protection of the central nervous system Int J Hyperthermia 21 2005 379 392 (Pubitemid 41102938)
20. R. Helton, J. Cui, J.R. Scheel, J.A. Ellison, C. Ames, and C. Gibson Brain-specific knock-out of hypoxia-inducible factor-1alpha reduces rather than increases hypoxic-ischemic damage J Neurosci 25 2005 4099 4107 (Pubitemid 40563385)
21. T. Hirano, K. Ishihara, and M. Hibi Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors Oncogene 19 2000 2548 2556 (Pubitemid 30339210)
22. K. Jeyaseelan, K.Y. Lim, and A. Armugam MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion Stroke 39 2008 959 966 (Pubitemid 351619577)
23. A.J. Kastin, V. Akerstrom, and W. Pan Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier J Mol Neurosci 18 2002 7 14 (Pubitemid 34252619)
24. N. Kawahara, Y. Wang, A. Mukasa, K. Furuya, T. Shimizu, and T. Hamakubo Genome-wide gene expression analysis for induced ischemic tolerance and delayed neuronal death following transient global ischemia in rats J Cereb Blood Flow Metab 24 2004 212 223 (Pubitemid 38199115)
25. J.B. Kim, C.S. Piao, K.W. Lee, P.L. Han, J.I. Ahn, and Y.S. Lee Delayed genomic responses to transient middle cerebral artery occlusion in the rat J Neurochem 89 2004 1271 1282 (Pubitemid 38715845)
26. B. Lai, X.O. Mao, L. Xie, K. Jin, and D.A. Greenberg Electrophysiological neurodifferentiation of subventricular zone-derived precursor cells following stroke Neurosci Lett 442 2008 305 308
27. H. Li, F. Colbourne, P. Sun, Z. Zhao, A.M. Buchan, and C. Iadecola Caspase inhibitors reduce neuronal injury after focal but not global cerebral ischemia in rats Stroke 31 2000 176 182 (Pubitemid 30035772)
28. M. Li, J.L. Maderdrut, J.J. Lertora, and V. Batuman Intravenous infusion of pituitary adenylate cyclase-activating polypeptide (PACAP) in a patient with multiple myeloma and myeloma kidney: a case study Peptides 28 2007 1891 1895 (Pubitemid 47361424)
29. S.A. Loddick, A.V. Turnbull, and N.J. Rothwell Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat J Cereb Blood Flow Metab 18 1998 176 179 (Pubitemid 28082514)
30. E.Z. Longa, P.R. Weinstein, S. Carlson, and R. Cummins Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1989 84 91 (Pubitemid 19040218)
31. X.C.M. Lu, A.J. Williams, C. Yao, R. Berti, J.A. Hartings, and R. Whipple Microarray analysis of acute and delayed gene expression profile in rats after focal ischemic brain injury and reperfusion J Neurosci Res 77 2004 843 857 (Pubitemid 39187067)
32. R. Mentlein Dipeptidyl-peptidase IV (CD26) - role in the inactivation of regulatory peptides Regul Pept 85 1999 9 24 (Pubitemid 29505281)
33. P. Mergenthaler, U. Dirnagl, and A. Meisel Pathophysiology of stroke: lessons from animal models Met Brain Dis 19 2004 151 167 (Pubitemid 39361178)
34. A. Miyata, A. Arimura, R.R. Dahl, N. Minamino, A. Uehara, and L. Jiang Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells Biochem Biophys Res Commun 164 1989 567 574 (Pubitemid 19269770)
35. A. Miyata, L. Jiang, R.D. Dahl, C. Kitada, K. Kubo, and M. Fujino Isolation of a neuropeptide corresponding to the N-terminal 27 residues of the pituitary adenylate cyclase activating polypeptide with 38 residues (PACAP38) Biochem Biophys Res Commun 170 1990 643 648 (Pubitemid 20249468)
36. H. Mizushima, W.A. Banks, K. Dohi, S. Shioda, H. Matsumoto, and K. Matsumoto The effect of cardiac arrest on the permeability of the mouse blood-brain and blood-spinal cord barrier to pituitary adenylate cyclase activating polypeptide (PACAP) Peptides 20 1999 1337 1340
37. T. Nakamachi, H. Ohtaki, S. Yofu, K. Dohi, J. Watanabe, and H. Mori Endogenous pituitary adenylate cyclase activating polypeptide is involved in suppression of edema in the ischemic brain Acta Neurochir Suppl 106 2010 43 46
38. N. Nonaka, W.A. Banks, H. Mizushima, S. Shioda, and J.E. Morley Regional differences in PACAP transport across the blood-brain barrier in mice: a possible influence of strain, amyloid beta protein, and age Peptides 23 2002 2197 2202 (Pubitemid 36092054)
39. H. Ohtaki, T. Nakamachi, K. Dohi, and S. Shioda Role of PACAP in ischemic neural death J Mol Neurosci 36 2008 16 25
40. H. Ohtaki, T. Nakamachi, K. Dohi, Y. Aizawa, A. Takaki, and K. Hodoyama Pituitary adenylate cyclase-activating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6 Proc Natl Acad Sci USA 103 2006 7488 7493 (Pubitemid 43727860)
41. D. Petullo, K. Masonic, C. Lincoln, L. Wibberley, M. Teliska, and D.L. Yao Model development and behavioral assessment of focal cerebral ischemia in rats Life Sci 64 1999 1099 1108 (Pubitemid 29152027)
42. D. Pozo, J.M. Guerrero, and J.R. Calvo Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit LPS-stimulated MIP-1alpha production and mRNA expression Cytokines 18 2002 35 42 (Pubitemid 34762076)
43. B. Racz, Gallyas FJr, P. Kiss, G. Toth, O. Hegyi, and B. Gasz The neuroprotective effects of PACAP in monosodium glutamate-induced retinal lesion involve inhibition of proapoptotic signaling pathways Regul Pept 137 2006 20 26 (Pubitemid 44781242)
44. V.L. Raghavendra Rao, K.K. Bowen, V.K. Dhodda, G. Song, J.L. Franklin, and N.R. Gavva Gene expression analysis of spontaneously hypertensive rat cerebral cortex following transient focal cerebral ischemia J Neurochem 83 2002 1072 1086 (Pubitemid 35397117)
45. D. Reglodi, A. Somogyvari-Vigh, S. Vigh, T. Kozicz, and A. Arimura Delayed systemic administration of PACAP38 is neuroprotective in transient middle cerebral artery occlusion in the rat Stroke 31 2000 1411 1417 (Pubitemid 30351265)
46. D. Reglodi, A. Somogyvari-Vigh, S. Vigh, J.L. Maderdrut, and A. Arimura Neuroprotective effects of PACAP38 in a rat model of transient focal ischemia under various experimental conditions Ann NY Acad Sci 921 2000 119 128 (Pubitemid 32094535)
47. D. Reglodi, A. Tamas, A. Somogyvari-Vigh, Z. Szanto, E. Kertes, and L. Lenard Effects of pretreatment with PACAP on the infarct size and functional outcome in rat permanent focal cerebral ischemia Peptides 23 2002 227 234
48. P. Robberecht, P. Gourlet, P. De Neef, M.C. Woussen-Colle, M.C. Vandermeers-Piret, and A. Vandermeers Receptor occupancy and adenylate cyclase activation in AR 4-2J rat pancreatic acinar cell membranes by analogs of pituitary adenylate cyclase activating peptides amino-terminally shortened or modified at position 1, 2, 3, 20, or 21 Mol Pharmacol 42 1992 347 355 (Pubitemid 23026170)
49. H. Shi Hypoxia inducible factor 1 as a therapeutic target in ischemic stroke Curr Med Chem 16 2009 4593 4600
50. S. Shioda, H. Ohtaki, T. Nakamachi, K. Dohi, J. Watanabe, and S. Nakajo Pleiotropic functions of PACAP in the CNS: neuroprotection and neurodevelopment Ann NY Acad Sci 1070 2006 550 560 (Pubitemid 44126702)
51. S. Shioda, H. Ozawa, K. Dohi, H. Mizushima, K. Matsumoto, and S. Nakajo PACAP protects hippocampal neurons against apoptosis: involvement of JNK/SAPK signaling pathway Ann NY Acad Sci 865 1998 111 117 (Pubitemid 29047818)
52. A. Somogyvari-Vigh, W. Pan, D. Reglodi, A.J. Kastin, and A. Arimura Effect of middle cerebral artery occlusion on the passage of pituitary adenylate cyclase activating polypeptide across the blood brain barrier in the rat Regul Pept 91 2000 89 95
53. S. Suzuki, K. Tanaka, S. Nogawa, E. Nagata, D. Ito, and T. Dembo Temporal profile and cellular localization of interleukin-6 protein after focal cerebral ischemia in rats J Cereb Blood Flow Metab 19 1999 1256 1262 (Pubitemid 30176454)
54. A. Tamas, D. Reglodi, Z. Szanto, B. Borsiczky, J. Nemeth, and I. Lengvari Comparative neuroprotective effects of preischemic PACAP and VIP administration in permanent occlusion of the middle cerebral artery in rats Neuro Endocrinol Lett 23 2002 249 254 (Pubitemid 34741935)
55. D. Uchida, A. Arimura, A. Somogyvári-Vigh, S. Shioda, and W.A. Banks Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide Brain Res 736 1996 280 286 (Pubitemid 26356486)
56. F.J. Van der Staay, K.H. Augstein, and E. Horvath Sensorimotor impairments in rats with cerebral infarction, induced by unilateral occlusion of the left middle cerebral artery: strain differences and effects of the occlusion site Brain Res 735 1996 271 284 (Pubitemid 26345939)
57. D. Vaudry, M. Basille, Y. Anouar, A. Fournier, H. Vaudry, and B.J. Gonzales The neurotrophic activity of PACAP on rat cerebellar granule cells is associated with activation of the protein kinase A pathway and c-fos gene expression Ann NY Acad Sci 865 1998 92 99 (Pubitemid 29047816)
58. D. Vaudry, A. Falluel-Morel, S. Bourgault, M. Basille, D. Burel, and O. Wurtz Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery Pharmacol Rev 61 2009 283 357
59. Q. Wang, X.N. Tang, and M.A. Yenari The inflammatory response in stroke J Neuroimmunol 184 2007 53 68 (Pubitemid 46365991)
60. T. Yamashita, K. Sawamoto, S. Suzuki, N. Suzuki, K. Adachi, and T. Kawase Blockade of interleukin-6 signaling aggravates ischemic cerebral damage in mice: possible involvement of Stat3 activation in the protection of neurons J Neurochem 94 2005 459 468 (Pubitemid 40995261)
61. L. Zhu, C. Tamvakopoulos, D. Xie, J. Dragovic, X. Shen, and J.E. Fenyk-Melody The role of dipeptidyl peptidase IV in the cleavage of glucagon family peptides: in vivo metabolism of pituitary adenylate cyclase activating polypeptide-(1-38) J Biol Chem 278 2003 22418 22423 (Pubitemid 36830293)