Adeno-associated viral vector-induced overexpression of neuropeptide y Y2 receptors in the hippocampus suppresses seizures

Brain

Volumn 133, Issue 9, 2010, Pages 2778-2788

  Woldbye, David P D ^a,b   Ängehagen, Mikael ^a   Gøtzsche, Casper R ^b   Elbrønd Bek, Heidi ^b   Sørensen, Andreas T ^a   Christiansen, Søren H ^b   Olesen, Mikkel V ^b   Nikitidou, Litsa ^a   Hansen, Thomas V O ^b   Kanter Schlifke, Irene ^a   Kokaia, Merab ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

adeno associated viral vectors; anti convulsant; gene therapy; hippocampus; neuropeptides

Indexed keywords

COMPLEMENTARY DNA; KAINIC ACID; NEUROPEPTIDE Y2 RECEPTOR; PARVOVIRUS VECTOR; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); NEUROPEPTIDE Y RECEPTOR; PROTEIN BINDING; SULFUR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRICITY; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HIPPOCAMPUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; TEMPORAL LOBE EPILEPSY; ANALYSIS OF VARIANCE; ANIMAL; DISEASE MODEL; ELECTROSTIMULATION; GENE THERAPY; GENE VECTOR; GENETIC TRANSCRIPTION; GENETICS; KINDLING; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; RADIOGRAPHY; SEIZURES; SPRAGUE DAWLEY RAT; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; GENETIC THERAPY; GENETIC VECTORS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HIPPOCAMPUS; KAINIC ACID; KINDLING, NEUROLOGIC; MALE; PROTEIN BINDING; RADIOGRAPHY; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, NEUROPEPTIDE Y; SEIZURES; SULFUR ISOTOPES; TRANSCRIPTION, GENETIC;

EID: 77956385206     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq219     Document Type: Article

References (45)

1. Altman DG. Practical statistics for medical research. London, UK: Chapman and Hall; 1991.
2. Baraban SC, Hollopeter G, Erickson JC, Schwartzkroin PA, Palmiter RD. Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J Neurosci 1997; 17: 8927-8936
3. Benmaamar R, Pham-Lê B-T, Marescaux C, Pedrazzini T, Depaulis A. Induced down-regulation of neuropeptide Y-Y1 receptors delays initiation of kindling. Eur J Neurosci 2003; 18: 768-774
4. Berglund MM, Hipskind PA, Gehlert DR. Recent developments in our understanding of the physiological role of PP-fold peptide receptor subtypes. Exp Biol Med 2003; 228: 217-244
5. Brodie MJ, Dichter MA. Antiepileptic drugs. N Engl J Med 1996; 334: 168-175
6. 35S]GTPgammaS binding suggests a net increase in NPY signalling after repeated electroconvul-sive seizures in mice. J Neurosci Res 2006; 84: 1282-1291
7. Duncan JS, Sander JW, Sisodiya SM, Walker MC. Adult epilepsy. Lancet 2006; 367: 1087-1100
8. El Bahh B, Balosso S, Hamilton T, Herzog H, Beck-Sickinger AG, Sperk G, et al. The anti-epileptic actions of neuropeptide Y in the hippocampus are mediated by Y2 and not Y5 receptors. Eur J Neurosci 2005; 22: 1417-1430
9. Elmér E, Kokaia M, Kokaia Z, McIntyre DC, Lindvall O. Epileptogenesis induced by rapidly recurring seizures in genetically fast\but not slow\kindling rats. Brain Res 1998; 789: 111-117
10. Engel J Jr, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy. Epilepsia 2003; 44: 741-751
11. Foti S, Haberman RP, Samulski RJ, McCown TJ. Adeno-associated virus-mediated expression and constitutive secretion of NPY or NPY13-36 suppresses seizure activity in vivo. Gene Ther 2007; 14: 1534-1536
12. Furtinger S, Pirker S, Czech T, Baumgartner C, Ransmayr G, Sperk G. Plasticity of Y1 and Y2 receptors and neuropeptide Y fibers in patients with temporal lobe epilepsy. J Neurosci 2001; 21: 5804-5812
13. Gariboldi M, Conti M, Cavaleri D, Samanin R, Vezzani A. Anticonvulsant properties of BIBP3226, a non-peptide selective antagonist at neuropeptide Y Y1 receptors. Eur J Neurosci 1998; 10: 757-759
14. Gobbi M, Gariboldi M, Piwko C, Hoyer D, Sperk G, Vezzani A. Distinct changes in peptide YY binding to, and mRNA levels of, Y1 and Y2 receptors in the rat hippocampus associated with kindling epileptogen-esis. J Neurochem 1998; 70: 1615-1622
15. Greber S, Schwarzer C, Sperk G. Neuropeptide Y inhibits potassium-stimulated glutamate release through Y2 receptors in rat hippocampal slices in vitro. Br J Pharmacol 1994; 113: 737-740
16. Haberman RP, Samulski RJ, McCown TJ. Attenuation of seizures and neuronal death by adeno-associated virus vector galanin expression and secretion. Nature Med 2003; 9: 1076-1080
17. Kanter-Schlifke I, Georgievska B, Kirik D, Kokaia M. Seizure suppression by GDNF gene therapy in animal models of epilepsy. Mol Ther 2007a; 15: 1106-1113
18. Kanter-Schlifke I, Sørensen AT, Ledri M, Kuteeva E, Hö kfelt T, Kokaia M. Galanin gene transfer curtails generalized seizures in kindled rats without altering hippocampal synaptic plasticity. Neuroscience 2007b; 150: 984-992
19. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, et al. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 2007; 369: 2097-2105
20. Kopp J, Nanobashvili A, Kokaia Z, Lindvall O, Hö kfelt T. Differential regulation of mRNAs for neuropeptide Y and its receptor subtypes in widespread areas of the rat limbic system during kindling epileptogen-esis. Mol Brain Res 1999; 72: 17-29.
21. Lin EJ, Young D, Baer K, Herzog H, During MJ. Differential actions of NPY on seizure modulation via Y1 and Y2 receptors: evidence from receptor knockout mice. Epilepsia 2006; 47: 773-780
22. Lö scher W, Gernert M, Heinemann U. Cell and gene therapies in epilepsy-promising avenues or blind alleys? Trends Neurosci 2008; 31: 62-73.
23. Marks WJ Jr, Ostrem JL, Verhagen L, Starr PA, Larson PS, Bakay RA, et al. Safety and tolerability of intraputaminal delivery of CERE-120 (adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open-label, phase I trial. Lancet Neurol 2008; 7: 400-408
24. McCown TJ. Adeno-associated virus-mediated expression and constitutive secretion of galanin suppresses limbic seizure activity in vivo. Mol Ther 2006; 14: 63-68
25. Noé F, Pool AH, Nissinen J, Gobbi M, Bland R, Rizzi M, et al. Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain 2008; 131: 1506-1515
26. Noé F, Vaghi V, Balducci C, Fitzsimons H, Bland R, Zardoni D, et al. Anticonvulsant effects and behavioural outcomes of rAAV serotype 1 vector-mediated neuropeptide Y overexpression in rat hippocampus. Gene Ther 2010; 17: 643-652
27. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic; 2005.
28. Racine RJ. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972; 32: 281-294
29. Redrobe JP, Dumont Y, Herzog H, Quirion R. Characterization of neuropeptide Y, Y(2) receptor knockout mice in two animal models of learning and memory processing. J Mol Neurosci 2004; 22: 159-166
30. Richichi C, Lin EJ, Stefanin D, Colella D, Ravizza T, Grignaschi G, et al. Anticonvulsant and antiepileptogenic effects mediated by adeno-associated virus vector neuropeptide Y expression in the rat hippocampus. J Neurosci 2004; 24: 3051-3059
31. Rö der C, Schwarzer C, Vezzani A, Gobbi M, Mennini T, Sperk G. Autoradiographic analysis of neuropeptide Y receptor binding sites in the rat hippocampus after kainic acid-induced limbic seizures. Neuroscience 1996; 70: 47-55.
32. Silva AP, Lourenço J, Xapelli S, Ferreira R, Kristiansen H, Woldbye DP, et al. Protein kinase C activity blocks neuropeptide Y-mediated inhibition of glutamate release and contributes to excitability of the hippocampus in status epilepticus. Faseb J 2007; 21: 671-681
33. Sørensen AT, Kanter-Schlifke I, Carli M, Balducci C, Noé F, During MJ, et al. NPY gene transfer in the hippocampus attenuates synaptic plasticity and learning. Hippocampus 2008a; 18: 564-574
34. Sørensen AT, Kanter-Schlifke I, Lin EJ, During MJ, Kokaia M. Activity-dependent volume transmission by transgene NPY attenuates glutamate release and LTP in the subiculum. Mol Cell Neurosci 2008b; 39: 229-237
35. Sørensen AT, Nikitidou L, Ledri M, Lin ED, During MJ, Kanter-Schlifke I, et al. Hippocampal NPY gene transfer attenuates seizures without affecting epilepsy-induced impairment of LTP. Exp Neurol 2009; 215: 328-333
36. Vezzani A, Sperk G. Overexpression of NPY and Y2 receptors in epileptic brain tissue: an endogenous neuroprotective mechanism in temporal lobe epilepsy? Neuropeptides 2004; 38: 245-252
37. Vezzani A, Sperk G, Colmers WF. Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci 1999; 22: 25-30.
38. Warrington KH, Herzog RW. Treatment of human disease by adeno-associated viral gene transfer. Hum Genet 2006; 119: 571-603.
39. Wieser HG, Yasergil NG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol 1982; 17: 445-447
40. Woldbye DP, Kokaia M. Neuropeptide Y and seizures: effects of exogen-ously applied ligands. Neuropeptides 2004; 38: 253-260
41. Woldbye DP, Larsen PJ, Mikkelsen JD, Klemp K, Madsen TM, Bolwig TG. Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nature Med 1997; 3: 761-764
42. Woldbye DP, Madsen TM, Larsen PJ, Mikkelsen JD, Bolwig TG. Neuropeptide Y inhibits hippocampal seizures and wet dog shakes. Brain Res 1996; 737: 162-168
43. Woldbye DP, Nanobashvili A, Sørensen AT, Husum H, Bolwig TG, Sørensen G, et al. Differential suppression of seizures via Y2 and Y5 neuropeptide Y receptors. Neurobiol Dis 2005; 20: 760-772
44. Xapelli S, Agasse F, Ferreira R, Silva AP, Malva JO. Neuropeptide Y as an endogenous antiepileptic, neuroprotective and pro-neurogenic pep-tide. Recent Pat CNS Drug Discov 2006; 1: 315-324
45. Yilmazer-Hanke DM, Wolf HK, Schramm J, Elger CE, Wiestler OD, Blü mkce I. Subregional pathology of the amygdala complex and entorhinal region in surgical specimens from patients with pharmacore-sistant temporal lobe epilepsy. J Neuropathol Exp Neurol 2000; 59: 907-920