Rapid change of neuropeptide Y levels and gene-expression in the brain of ovariectomized mice after administration of 17β-estradiol

Neuropeptides

Volumn 43, Issue 4, 2009, Pages 327-332

  Hilke, Susanne ^a   Holm, Lovisa ^a   Åman, Katarina ^b   Hökfelt, Tomas ^b   Theodorsson, Elvar ^a  

^a Fac Hlth Sci   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Estrogen; In situ hybridization; Limbic system; Neuropeptide; Radioimmunoassay

Indexed keywords

ESTRADIOL; NEUROPEPTIDE Y;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CAUDATE NUCLEUS; COGNITION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENTATE GYRUS; FEMALE; FOREBRAIN; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MOOD; MOTOR PERFORMANCE; MOUSE; NONHUMAN; OVARIECTOMY; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; RADIOIMMUNOASSAY;

ANIMALS; BRAIN; ESTRADIOL; FEMALE; GENE EXPRESSION; MICE; NEUROPEPTIDE Y; OVARIECTOMY; RADIOIMMUNOASSAY; RATS;

MUS; RATTUS;

EID: 67651001740     PISSN: 01434179     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.npep.2009.04.005     Document Type: Article

References (67)

1. Allen Y.S., Adrian T.E., Allen J.M., Tatemoto K., Crow T.J., Bloom S.R., and Polak J.M. Neuropeptide Y distribution in the rat brain. Science 221 (1983) 877-879
2. Berglund M.M., Hipskind P.A., and Gehlert D.R. Recent developments in our understanding of the physiological role of PP-fold peptide receptor subtypes. Exp. Biol. Med (Maywood) 228 (2003) 217-244
3. Brake W.G., Alves S.E., Dunlop J.C., Lee S.J., Bulloch K., Allen P.B., Greengard P., and McEwen B.S. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 142 (2001) 1284-1289
4. Chronwall B.M., DiMaggio D.A., Massari V.J., Pickel V.M., Ruggiero D.A., and O'Donohue T.L. The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15 (1985) 1159-1181
5. Colmers W.F., Lukowiak K., and Pittman Q.J. Neuropeptide Y action in the rat hippocampal slice: site and mechanism of presynaptic inhibition. J. Neurosci. 8 (1988) 3827-3837
6. de Quidt M.E., and Emson P.C. Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system - II. Immunohistochemical analysis. Neuroscience 18 (1986) 545-618
7. Duval P., Lenoir V., Moussaoui S., Garret C., and Kerdelhue B. Substance P and neurokinin A variations throughout the rat estrous cycle; comparison with ovariectomized and male rats: I. Plasma, hypothalamus, anterior and posterior pituitary. J. Neurosci. Res. 45 (1996) 598-609
8. Everitt B.J., Hökfelt T., Terenius L., Tatemoto K., Mutt V., and Goldstein M. Differential co-existence of neuropeptide Y (NPY)-like immunoreactivity with catecholamines in the central nervous system of the rat. Neuroscience 11 (1984) 443-462
9. Frankfurt M., Gould E., Woolley C.S., and McEwen B.S. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendocrinology 51 (1990) 530-535
10. Gehlert D.R., Chronwall B.M., Schafer M.P., and O'Donohue T.L. Localization of neuropeptide Y messenger ribonucleic acid in rat and mouse brain by in situ hybridization. Synapse 1 (1987) 25-31
11. Greber S., Schwarzer C., and Sperk G. Neuropeptide Y inhibits potassium-stimulated glutamate release through Y2 receptors in rat hippocampal slices in vitro. Brit. J. Pharmacol. 113 (1994) 737-740
12. Gresack J.E., and Frick K.M. Effects of continuous and intermittent estrogen treatments on memory in aging female mice. Brain Res. 1115 (2006) 135-147
13. Gu Q., Korach K.S., and Moss R.L. Rapid action of 17beta-estradiol on kainate-induced currents in hippocampal neurons lacking intracellular estrogen receptors. Endocrinology 140 (1999) 660-666
14. Hart S.A., Snyder M.A., Smejkalova T., and Woolley C.S. Estrogen mobilizes a subset of estrogen receptor-alpha-immunoreactive vesicles in inhibitory presynaptic boutons in hippocampal CA1. J. Neurosci. 27 (2007) 2102-2111
15. Heilig M. The NPY system in stress, anxiety and depression. Neuropeptides 38 (2004) 213-224
16. Heilig M., Koob G.F., Ekman R., and Britton K.T. Corticotropin-releasing factor and neuropeptide Y: role in emotional integration. Trends Neurosci. 17 (1994) 80-85
17. Hendry S.H., Jones E.G., DeFelipe J., Schmechel D., Brandon C., and Emson P.C. Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. Proc. Natl. Acad. Sci. USA 81 (1984) 6526-6530
18. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., and Greengard P. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999) 269-279
19. Hilke S., Hökfelt T., Åman K., and Theodorsson E. Rapid effects of estrogen on the concentrations of galanin and neuropeptide Y in the mouse brain - effects not seen after prolonged treatment. Soc. Neurosci. 34 (2004) #829_3
20. Hilke S., Theodorsson A., Fetissov S., Åman K., Holm L., Hökfelt T., and Theodorsson E. Estrogen induces a rapid increase in galanin levels in female rat hippocampal formation - possibly a nongenomic/indirect effect. Eur. J. Neurosci. 21 (2005) 2089-2099
21. Hilke S., Hökfelt T., Darwish M., and Theodorsson E. Cholecystokinin levels in the rat brain during the estrous cycle. Brain Res. 1144 (2007) 70-73
22. Holets V.R., Hökfelt T., Rökaeus A., Terenius L., and Goldstein M. Locus coeruleus neurons in the rat containing neuropeptide Y, tyrosine hydroxylase or galanin and their efferent projections to the spinal cord, cerebral cortex and hypothalamus. Neuroscience 24 (1988) 893-906
23. Holliday N.D., Michel M.C., and Cox H.M. NPY receptor subtypes and their signal transduction. Neuropeptide Y and Related Peptides (2004), Springer, Berlin 45-74
24. 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
25. Ishii H., Tsurugizawa T., Ogiue-Ikeda M., Asashima M., Mukai H., Murakami G., Hojo Y., Kimoto T., and Kawato S. Local production of sex hormones and their modulation of hippocampal synaptic plasticity. Neuroscientist 13 (2007) 323-334
26. Jasnow A.M., Mong J.A., Romeo R.D., and Pfaff D.W. Estrogenic regulation of gene and protein expression within the amygdala of female mice. Endocrine 32 (2007) 271-279
27. Jensen E.V. Steroid hormones, receptors, and antagonists. Ann. NY Acad. Sci. 784 (1996) 1-17
28. Kalra S.P., and Kalra P.S. NPY - an endearing journey in search of a neurochemical on/off switch for appetite, sex and reproduction. Peptides 25 (2004) 465-471
29. Kask A., Rago L., and Harro J. Anxiogenic-like effect of the neuropeptide Y Y1 receptor antagonist BIBP3226: antagonism with diazepam. Eur. J. Pharmacol. 317 (1996) R3-R4
30. Kask A., Rago L., and Harro J. Anxiolytic-like effect of neuropeptide Y (NPY) and NPY13-36 microinjected into vicinity of locus coeruleus in rats. Brain Res. 788 (1998) 345-348
31. Kelly M.J., and Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 12 (2001) 152-156
32. Kelly M.J., Moss R.L., and Dudley C.A. The effects of microelectrophoretically applied estrogen, cortisol and acetylcholine on medial preoptic-septal unit activity throughout the estrous cycle of the female rat. Exp. Brain Res. 30 (1977) 53-64
33. Köhler C., Eriksson L.G., Davies S., and Chan-Palay V. Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region. Neurosci. Lett. 78 (1987) 1-6
34. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., and Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA 93 (1996) 5925-5930
35. Larhammar D., Ericsson A., and Persson H. Structure and expression of the rat neuropeptide Y gene. Proc. Natl. Acad. Sci. USA 84 (1987) 2068-2072
36. Larhammar D., Wraith A., Berglund M.M., Holmberg S.K., and Lundell I. Origins of the many NPY-family receptors in mammals. Peptides 22 (2001) 295-307
37. Ledouc V.A., Smejkalova T., May R.M., Cooke M., and Woolley C.S. Estradiol facilitates the release of neuropeptide Y to suppress hippocampus-dependent seizures. J. Neurosci. 29 (2009) 1457-1468
38. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., Chen L., Chen L., Chen T.M., Chin M.C., Chong J., Crook B.E., Czaplinska A., Dang C.N., Datta S., Dee N.R., Desaki A.L., Desta T., Diep E., Dolbeare T.A., Donelan M.J., Dong H.W., Dougherty J.G., Duncan B.J., Ebbert A.J., Eichele G., Estin L.K., Faber C., Facer B.A., Fields R., Fischer S.R., Fliss T.P., Frensley C., Gates S.N., Glattfelder K.J., Halverson K.R., Hart M.R., Hohmann J.G., Howell M.P., Jeung D.P., Johnson R.A., Karr P.T., Kawal R., Kidney J.M., Knapik R.H., Kuan C.L., Lake J.H., Laramee A.R., Larsen K.D., Lau C., Lemon T.A., Liang A.J., Liu Y., Luong L.T., Michaels J., Morgan J.J., Morgan R.J., Mortrud M.T., Mosqueda N.F., Ng L.L., Ng R., Orta G.J., Overly C.C., Pak T.H., Parry S.E., Pathak S.D., Pearson O.C., Puchalski R.B., Riley Z.L., Rockett H.R., Rowland S.A., Royall J.J., Ruiz M.J., Sarno N.R., Schaffnit K., Shapovalova N.V., Sivisay T., Slaughterbeck C.R., Smith S.C., Smith K.A., Smith B.I., Sodt A.J., Stewart N.N., Stumpf K.R., Sunkin S.M., Sutram M., Tam A., Teemer C.D., Thaller C., Thompson C.L., Varnam L.R., Visel A., Whitlock R.M., Wohnoutka P.E., Wolkey C.K., Wong V.Y., Wood M., Yaylaoglu M.B., Young R.C., Youngstrom B.L., Yuan X.F., Zhang B., Zwingman T.A., and Jones A.R. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445 (2007) 168-176
39. Liu R., Wang X., Liu Q., Yang S.H., and Simpkins J.W. Dose dependence and therapeutic window for the neuroprotective effects of 17beta-estradiol when administered after cerebral ischemia. Neurosci. Lett. 415 (2007) 237-241
40. Malberg J.E., Eisch A.J., Nestler E.J., and Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000) 9104-9110
41. McQuiston A.R., and Colmers W.F. Neuropeptide Y2 receptors inhibit the frequency of spontaneous but not miniature EPSCs in CA3 pyramidal cells of rat hippocampus. J. Neurophysiol. 76 (1996) 3159-3168
42. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., and Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 429 (2001) 355-371
43. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491 (2005) 81-95
44. Morris B.J. Neuronal localisation of neuropeptide Y gene expression in rat brain. J. Comp. Neurol. 290 (1989) 358-368
45. Mosselman S., Polman J., and Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 392 (1996) 49-53
46. Nakamura N.H., and McEwen B.S. Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: a potential role for neuropeptide Y. Neuroscience 136 (2005) 357-369
47. Overstreet D.H., Friedman E., Mathe A.A., and Yadid G. The flinders sensitive line rat: a selectively bred putative animal model of depression. Neurosci. Biobehav. Rev. 29 (2005) 739-759
48. Pietras R.J., and Szego C.M. Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265 (1977) 69-72
49. Redrobe J.P., Dumont Y., and Quirion R. Neuropeptide Y (NPY) and depression: from animal studies to the human condition. Life Sci. 71 (2002) 2921-2937
50. Rugarn O., Hammar M., Theodorsson A., Theodorsson E., and Stenfors C. Sex differences in neuropeptide distribution in the rat brain. Peptides 20 (1999) 81-86
51. Sajdyk T.J., Shekhar A., and Gehlert D.R. Interactions between NPY and CRF in the amygdala to regulate emotionality. Neuropeptides 38 (2004) 225-234
52. Scharfman H.E., and Gray W.P. Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its relevance to seizure-induced neurogenesis. EXS (2006) 193-211
53. Scharfman H.E., and MacLusky N.J. Estrogen-growth factor interactions and their contributions to neurological disorders. Headache 48 Suppl. 2 (2008) S77-S89
54. Scharfman H.E., Mercurio T.C., Goodman J.H., Wilson M.A., and MacLusky N.J. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J. Neurosci. 23 (2003) 11641-11652
55. Silva A.P., Cavadas C., and Grouzmann E. Neuropeptide Y and its receptors as potential therapeutic drug targets. Clin. Chim. Acta 326 (2002) 3-25
56. Sperk G., Hamilton T., and Colmers W.F. Neuropeptide Y in the dentate gyrus. Prog. Brain Res. 163 (2007) 285-297
57. Ström J.O., Theodorsson A., and Theodorsson E. Substantial discrepancies in 17beta-oestradiol concentrations obtained with three different commercial direct radioimmunoassay kits in rat sera. Scand. J. Clin. Lab. Invest. 68 (2008) 806-813
58. Tatemoto K. Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc. Natl. Acad. Sci. USA 79 (1982) 5485-5489
59. Tatemoto K., Carlquist M., and Mutt V. Neuropeptide Y - a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296 (1982) 659-660
60. Tatemoto K., Rökaeus A., Jörnvall H., McDonald T.J., and Mutt V. Galanin - a novel biologically active peptide from porcine intestine. FEBS Lett. 164 (1983) 124-128
61. Theodorsson-Norheim E., Hemsen A., and Lundberg J.M. Radioimmunoassay for neuropeptide Y (NPY): chromatographic characterization of immunoreactivity in plasma and tissue extracts. Scand. J. Clin. Lab. Invest. 45 (1985) 355-365
62. Titolo D., Mayer C.M., Dhillon S.S., Cai F., and Belsham D.D. Estrogen facilitates both phosphatidylinositol 3-kinase/Akt and ERK1/2 mitogen-activated protein kinase membrane signaling required for long-term neuropeptide Y transcriptional regulation in clonal, immortalized neurons. J. Neurosci. 28 (2008) 6473-6482
63. 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
64. Warner M., and Gustafsson J.A. Nongenomic effects of estrogen: why all the uncertainty?. Steroids 71 (2006) 91-95
65. Weiser T., Wieland H.A., and Doods H.N. Effects of the neuropeptide Y Y(2) receptor antagonist BIIE0246 on presynaptic inhibition by neuropeptide Y in rat hippocampal slices. Eur. J. Pharmacol. 404 (2000) 133-136
66. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12 (1992) 2549-2554
67. Woolley C.S., Weiland N.G., McEwen B.S., and Schwartzkroin P.A. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci. 17 (1997) 1848-1859