Adult-onset hippocampal-specific neuropeptide Y overexpression confers mild anxiolytic effect in mice

European Neuropsychopharmacology

Volumn 20, Issue 3, 2010, Pages 164-175

  Lin, En Ju Deborah ^a,b   Lin, Shu ^a   Aljanova, Aygul ^a   During, Matthew J ^b   Herzog, Herbert ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Anxiety; Behavior; Gene transfer; Neuropeptide; rAAV

Indexed keywords

CORTICOSTERONE; NEUROPEPTIDE Y; NEUROPEPTIDE Y1 RECEPTOR; PARVOVIRUS VECTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DRUG BRAIN LEVEL; DRUG EFFECT; DRUG MECHANISM; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; MAZE TEST; MOTOR ACTIVITY; MOUSE; NONHUMAN; ONSET AGE; OPEN FIELD TEST; PASSIVE AVOIDANCE; PHYSICAL EXAMINATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TEMPORAL LOBE EPILEPSY; TRANQUILIZING ACTIVITY; VIRUS RECOMBINANT; WILD TYPE;

AGE FACTORS; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY DISORDERS; AVOIDANCE LEARNING; GENE EXPRESSION REGULATION; GENE THERAPY; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPEPTIDE Y;

EID: 75149168274     PISSN: 0924977X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2009.08.004     Document Type: Article

References (78)

1. Baiardi G., Ruiz A.M., Beling A., Borgonovo J., Martinez G., Landa A.I., Sosa M.A., and Gargiulo P.A. Glutamatergic ionotropic blockade within accumbens disrupts working memory and might alter the endocytic machinery in rat accumbens and prefrontal cortex. J. Neural. Transm. 114 (2007) 1519-1528
2. Balasubramaniam A.A. Neuropeptide Y family of hormones: receptor subtypes and antagonists. Peptides 18 (1997) 445-457
3. Baldock P.A., Sainsbury A., Allison S., Lin E.J., Couzens M., Boey D., Enriquez R., During M., Herzog H., and Gardiner E.M. Hypothalamic control of bone formation: distinct actions of leptin and y2 receptor pathways. J. Bone Miner. Res. 20 (2005) 1851-1857
4. Bannon A.W., Seda J., Carmouche M., Francis J.M., Norman M.H., Karbon B., and McCaleb M.L. Behavioral characterization of neuropeptide Y knockout mice. Brain Res. 868 (2000) 79-87
5. Baraban S.C., Hollopeter G., Erickson J.C., Schwartzkroin P.A., and Palmiter R.D. Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J. Neurosci. 17 (1997) 8927-8936
6. Beck H., Goussakov I.V., Lie A., Helmstaedter C., and Elger C.E. Synaptic plasticity in the human dentate gyrus. J. Neurosci. 20 (2000) 7080-7086
7. Bellmann R., Widmann R., Olenik C., Meyer D.K., Maas D., Marksteiner J., and Sperk G. Enhanced rate of expression and biosynthesis of neuropeptide Y after kainic acid-induced seizures. J. Neurochem. 56 (1991) 525-530
8. Belzung C., and Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res. 125 (2001) 141-149
9. Benaroya-Milshtein N., Hollander N., Apter A., Kukulansky T., Raz N., Wilf A., Yaniv I., and Pick C.G. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur. J. NeuroSci. 20 (2004) 1341-1347
10. Bird C.M., and Burgess N. The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 9 (2008) 182-194
11. Caberlotto L., and Hurd Y.L. Reduced neuropeptide Y mRNA expression in the prefrontal cortex of subjects with bipolar disorder. NeuroReport 10 (1999) 1747-1750
12. Caberlotto L., Jimenez P., Overstreet D.H., Hurd Y.L., Mathe A.A., and Fuxe K. Alterations in neuropeptide Y levels and Y1 binding sites in the Flinders Sensitive Line rats, a genetic animal model of depression. Neurosci. Lett. 265 (1999) 191-194
13. Cavadas C., Cefai D., Rosmaninho-Salgado J., Vieira-Coelho M.A., Moura E., Busso N., Pedrazzini T., Grand D., Rotman S., Waeber B., Aubert J.F., and Grouzmann E. Deletion of the neuropeptide Y (NPY) Y1 receptor gene reveals a regulatory role of NPY on catecholamine synthesis and secretion. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10497-10502
14. Clark K.R., Liu X., McGrath J.P., and Johnson P.R. Highly purified recombinant adeno-associated virus vectors are biologically active and free of detectable helper and wild-type viruses. Hum. Gene Ther. 10 (1999) 1031-1039
15. Costall B., Jones B.J., Kelly M.E., Naylor R.J., and Tomkins D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol. Biochem. Behav. 32 (1989) 777-785
16. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci. Biobehav. Rev. 9 (1985) 37-44
17. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 835 (1999) 18-26
18. DeFries J.C., Hegmann J.P., and Weir M.W. Open-field behavior in mice: evidence for a major gene effect mediated by the visual system. Science 154 (1966) 1577-1579
19. do-Rego J.C., Viana A.F., Le Maitre E., Deniel A., Rates S.M., Leroux-Nicollet I., and Costentin J. Comparisons between anxiety tests for selection of anxious and non anxious mice. Behav. Brain Res. 169 (2006) 282-288
20. Drevets W.C., Price J.L., and Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 213 (2008) 93-118
21. Duman C.H., Schlesinger L., Russell D.S., and Duman R.S. Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res. 1199 (2008) 148-158
22. Dumont Y., Jacques D., Bouchard P., and Quirion R. Species differences in the expression and distribution of the neuropeptide Y Y1, Y2, Y4, and Y5 receptors in rodents, guinea pig, and primates brains. J. Comp. Neurol. 402 (1998) 372-384
23. During M.J., Young D., Baer K., Lawlor P., and Klugmann M. Development and optimization of adeno-associated virus vector transfer into the central nervous system. Methods Mol. Med. 76 (2003) 221-236
24. Elger C.E., Helmstaedter C., and Kurthen M. Chronic epilepsy and cognition. Lancet Neurol. 3 (2004) 663-672
25. Foti S., Haberman R.P., Samulski R.J., and McCown T.J. Adeno-associated virus-mediated expression and constitutive secretion of NPY or NPY13-36 suppresses seizure activity in vivo. Gene Ther. 14 (2007) 1534-1536
26. Fox C., Merali Z., and Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav. Brain Res. 175 (2006) 1-8
27. Franklin K.B.J., and Paxinos G. The Mouse Brain in Stereotaxic Coordinates (1997), Academic Press, San Diego
28. Furtinger S., Pirker S., Czech T., Baumgartner C., and Sperk G. Altered expression of neuropeptide Y, -Y(1), and -Y(2) receptors in the hippocampus of patients with mesial temporal lobe epilepsy. Epilepsia 43 Suppl 5 (2002) 152
29. Gariboldi M., Conti M., Cavaleri D., Samanin R., and Vezzani A. Anticonvulsant properties of BIBP3226, a non-peptide selective antagonist at neuropeptide Y Y1 receptors. Eur. J. NeuroSci. 10 (1998) 757-759
30. Heilig M. Antisense inhibition of neuropeptide Y (NPY)-Y1 receptor expression blocks the anxiolytic-like action of NPY in amygdala and paradoxically increases feeding. Regul. Pept. 59 (1995) 201-205
31. Heilig M., and Widerlov E. Neuropeptide Y: an overview of central distribution, functional aspects, and possible involvement in neuropsychiatric illnesses. Acta Psychiatr. Scand. 82 (1990) 95-114
32. Heilig M., McLeod S., Brot M., Heinrichs S.C., Menzaghi F., Koob G.F., and Britton K.T. Anxiolytic-like action of neuropeptide Y: mediation by Y1 receptors in amygdala, and dissociation from food intake effects. Neuropsychopharmacology 8 (1993) 357-363
33. Helmstaedter C., Kurthen M., Lux S., Reuber M., and Elger C.E. Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Ann. Neurol. 54 (2003) 425-432
34. Holmes A., Wrenn C.C., Harris A.P., Thayer K.E., and Crawley J.N. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav. 1 (2002) 55-69
35. Howell O.W., Scharfman H.E., Herzog H., Sundstrom L.E., Beck-Sickinger A., and Gray W.P. Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 86 (2003) 646-659
36. Howell O.W., Doyle K., Goodman J.H., Scharfman H.E., Herzog H., Pringle A., Beck-Sickinger A.G., and Gray W.P. Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem. 93 (2005) 560-570
37. Husum H., Mikkelsen J.D., Hogg S., Mathe A.A., and Mork A. Involvement of hippocampal neuropeptide Y in mediating the chronic actions of lithium, electroconvulsive stimulation and citalopram. Neuropharmacology 39 (2000) 1463-1473
38. Ishida H., Shirayama Y., Iwata M., Katayama S., Yamamoto A., Kawahara R., and Nakagome K. Infusion of neuropeptide Y into CA3 region of hippocampus produces antidepressant-like effect via Y1 receptor. Hippocampus 17 (2007) 271-280
39. Karl T., Burne T.H., and Herzog H. Effect of Y1 receptor deficiency on motor activity, exploration, and anxiety. Behav. Brain Res. 167 (2006) 87-93
40. Karl T., Duffy L., and Herzog H. Behavioural profile of a new mouse model for NPY deficiency. Eur. J. NeuroSci. 28 (2008) 173-180
41. Karlsson R.M., Choe J.S., Cameron H.A., Thorsell A., Crawley J.N., Holmes A., and Heilig M. The neuropeptide Y Y1 receptor subtype is necessary for the anxiolytic-like effects of neuropeptide Y, but not the antidepressant-like effects of fluoxetine, in mice. Psychopharmacology (Berl.) 195 (2008) 547-557
42. Kask A., Harro J., von Horsten S., Redrobe J.P., Dumont Y., and Quirion R. The neurocircuitry and receptor subtypes mediating anxiolytic-like effects of neuropeptide Y. Neurosci. Biobehav. Rev. 26 (2002) 259-283
43. Koob G.F., Heinrichs S.C., Pich E.M., Menzaghi F., Baldwin H., Miczek K., and Britton K.T. The role of corticotropin-releasing factor in behavioural responses to stress. Ciba Found. Symp. 172 (1993) 277-289 discussion 290-275
44. Lin S., Boey D., and Herzog H. NPY and Y receptors: lessons from transgenic and knockout models. Neuropeptides 38 (2004) 189-200
45. Lin E.J., Young D., Baer K., Herzog H., and During M.J. Differential actions of NPY on seizure modulation via Y1 and Y2 receptors: evidence from receptor knockout mice. Epilepsia 47 (2006) 773-780
46. Mikkelsen J.D., Woldbye D., Kragh J., Larsen P.J., and Bolwig T.G. Electroconvulsive shocks increase the expression of neuropeptide Y (NPY) mRNA in the piriform cortex and the dentate gyrus. Brain Res. Mol. Brain Res. 23 (1994) 317-322
47. Moncek F., Duncko R., Johansson B.B., and Jezova D. Effect of environmental enrichment on stress related systems in rats. J. Neuroendocrinol. 16 (2004) 423-431
48. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behavior. J. Comp. Physiol. Psychol. 48 (1955) 254-260
49. Noe F., Pool A.H., Nissinen J., Gobbi M., Bland R., Rizzi M., Balducci C., Ferraguti F., Sperk G., During M.J., Pitkanen A., and Vezzani A. Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain 131 (2008) 1506-1515
50. Ohl F., Roedel A., Binder E., and Holsboer F. Impact of high and low anxiety on cognitive performance in a modified hole board test in C57BL/6 and DBA/2 mice. Eur. J. NeuroSci. 17 (2003) 128-136
51. Palmiter R.D., Erickson J.C., Hollopeter G., Baraban S.C., and Schwartz M.W. Life without neuropeptide Y. Recent Prog. Horm. Res. 53 (1998) 163-199
52. Patrylo P.R., van den Pol A.N., Spencer D.D., and Williamson A. NPY inhibits glutamatergic excitation in the epileptic human dentate gyrus. J. Neurophysiol. 82 (1999) 478-483
53. Pedrazzini T., Seydoux J., Kunstner P., Aubert J.F., Grouzmann E., Beermann F., and Brunner H.R. Cardiovascular response, feeding behavior and locomotor activity in mice lacking the NPY Y1 receptor. Nat. Med. 4 (1998) 722-726
54. Perez J.A., Clinton S.M., Turner C.A., Watson S.J., and Akil H. A new role for FGF2 as an endogenous inhibitor of anxiety. J. Neurosci. 29 (2009) 6379-6387
55. Redrobe J.P., Dumont Y., Fournier A., and Quirion R. The neuropeptide Y (NPY) Y1 receptor subtype mediates NPY-induced antidepressant-like activity in the mouse forced swimming test. Neuropsychopharmacology 26 (2002) 615-624
56. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., and Abrous D.N. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol. Psychiatry 14 (2009) 959-967
57. Richichi C., Lin E.J., Stefanin D., Colella D., Ravizza T., Grignaschi G., Veglianese P., Sperk G., During M.J., and Vezzani A. Anticonvulsant and antiepileptogenic effects mediated by adeno-associated virus vector neuropeptide Y expression in the rat hippocampus. J. Neurosci. 24 (2004) 3051-3059
58. Saitoh A., Hirose N., Yamada M., Nozaki C., Oka T., and Kamei J. Changes in emotional behavior of mice in the hole-board test after olfactory bulbectomy. J. Pharmacol. Sci. 102 (2006) 377-386
59. Sajdyk T.J., Vandergriff M.G., and Gehlert D.R. Amygdalar neuropeptide Y Y1 receptors mediate the anxiolytic-like actions of neuropeptide Y in the social interaction test. Eur. J. Pharmacol. 368 (1999) 143-147
60. Salam J.N., Fox J.H., Detroy E.M., Guignon M.H., Wohl D.F., and Falls W.A. Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety. Behav. Brain Res. 197 (2009) 31-40
61. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
62. Shannon H.E., and Yang L. Seizure susceptibility of neuropeptide-Y null mutant mice in amygdala kindling and chemical-induced seizure models. Epilepsy Res. 61 (2004) 49-62
63. Smialowska M., Bijak M., Sopala M., and Tokarski K. Inhibitory effect of NPY on the picrotoxin-induced activity in the hippocampus: a behavioural and electrophysiological study. Neuropeptides 30 (1996) 7-12
64. Smialowska M., Wieronska J.M., Domin H., and Zieba B. The effect of intrahippocampal injection of group II and III metobotropic glutamate receptor agonists on anxiety; the role of neuropeptide Y. Neuropsychopharmacology 32 (2007) 1242-1250
65. Sorensen A.T., Kanter-Schlifke I., Carli M., Balducci C., Noe F., During M.J., Vezzani A., and Kokaia M. NPY gene transfer in the hippocampus attenuates synaptic plasticity and learning. Hippocampus 18 (2008) 564-574
66. Sorensen A.T., Kanter-Schlifke I., Lin E.J., During M.J., and Kokaia M. Activity-dependent volume transmission by transgene NPY attenuates glutamate release and LTP in the subiculum. Mol. Cell. Neurosci. 39 (2008) 229-237
67. Sorensen A.T., Nikitidou L., Ledri M., Lin E.J., During M.J., Kanter-Schlifke I., and Kokaia M. Hippocampal NPY gene transfer attenuates seizures without affecting epilepsy-induced impairment of LTP. Exp. Neurol. 215 (2009) 328-333
68. Sperk G., Marksteiner J., Gruber B., Bellmann R., Mahata M., and Ortler M. Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience 50 (1992) 831-846
69. Stogner K.A., and Holmes P.V. Neuropeptide-Y exerts antidepressant-like effects in the forced swim test in rats. Eur. J. Pharmacol. 387 (2000) R9-R10
70. Takeda H., Tsuji M., and Matsumiya T. Changes in head-dipping behavior in the hole-board test reflect the anxiogenic and/or anxiolytic state in mice. Eur. J. Pharmacol. 350 (1998) 21-29
71. Thorsell A., Michalkiewicz M., Dumont Y., Quirion R., Caberlotto L., Rimondini R., Mathe A.A., and Heilig M. Behavioral insensitivity to restraint stress, absent fear suppression of behavior and impaired spatial learning in transgenic rats with hippocampal neuropeptide Y overexpression. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12852-12857
72. Vezzani A., Sperk G., and Colmers W.F. Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci. 22 (1999) 25-30
73. Vezzani A., Michalkiewicz M., Michalkiewicz T., Moneta D., Ravizza T., Richichi C., Aliprandi M., Mule F., Pirona L., Gobbi M., Schwarzer C., and Sperk G. Seizure susceptibility and epileptogenesis are decreased in transgenic rats overexpressing neuropeptide Y. Neuroscience 110 (2002) 237-243
74. Wahlestedt C., Blendy J.A., Kellar K.J., Heilig M., Widerlov E., and Ekman R. Electroconvulsive shocks increase the concentration of neocortical and hippocampal neuropeptide Y (NPY)-like immunoreactivity in the rat. Brain Res. 507 (1990) 65-68
75. Wahlestedt C., Pich E.M., Koob G.F., Yee F., and Heilig M. Modulation of anxiety and neuropeptide Y-Y1 receptors by antisense oligodeoxynucleotides. Science 259 (1993) 528-531
76. Woldbye D.P. Antiepileptic effects of NPY on pentylenetetrazole seizures. Regul. Pept. 75-76 (1998) 279-282
77. Woldbye D.P., Larsen P.J., Mikkelsen J.D., Klemp K., Madsen T.M., and Bolwig T.G. Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nat. Med. 3 (1997) 761-764
78. Xu R., Janson C.G., Mastakov M., Lawlor P., Young D., Mouravlev A., Fitzsimons H., Choi K.L., Ma H., Dragunow M., Leone P., Chen Q., Dicker B., and During M.J. Quantitative comparison of expression with adeno-associated virus (AAV-2) brain-specific gene cassettes. Gene Ther. 8 (2001) 1323-1332