Estrogen decreases 5-HT1B autoreceptor mRNA in selective subregion of rat dorsal raphe nucleus: Inverse association between gene expression and anxiety behavior in the open field

Neuroscience

Volumn 158, Issue 2, 2009, Pages 456-464

  Hiroi, R ^a,b   Neumaier, J F ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

5 HT; 5 HT1A; in situ hybridization; ovarian hormones; ovariectomy; tryptophan hydroxylase

Indexed keywords

ESTRADIOL; MESSENGER RNA; PLACEBO; SEROTONIN 1A RECEPTOR; SEROTONIN 1B RECEPTOR; TRYPTOPHAN HYDROXYLASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DORSAL RAPHE NUCLEUS; DRUG MECHANISM; FEMALE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; TISSUE DISTRIBUTION;

ANIMALS; DOWN-REGULATION; ESTROGENS; EXPLORATORY BEHAVIOR; FEMALE; OVARIECTOMY; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTOR, SEROTONIN, 5-HT1B; RNA, MESSENGER; STATISTICS AS TOPIC; TRYPTOPHAN HYDROXYLASE;

EID: 58149458416     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.10.016     Document Type: Article

References (91)

1. Abrams J.K., Johnson P.L., Hollis J.H., and Lowry C.A. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018 (2004) 46-57
2. Alves S.E., Weiland N.G., Hayashi S., and McEwen B.S. Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J Comp Neurol 391 (1998) 322-334
3. Anderson N.L., and Hughes R.N. Increased emotional reactivity in rats following exposure to caffeine during adolescence. Neurotoxicol Teratol 30 3 (2008) 195-201
4. Anthony J.P., Sexton T.J., and Neumaier J.F. Antidepressant-induced regulation of 5-HT(1b) mRNA in rat dorsal raphe nucleus reverses rapidly after drug discontinuation. J Neurosci Res 61 (2000) 82-87
5. Arpels J.C. The female brain hypoestrogenic continuum from the premenstrual syndrome to menopause. A hypothesis and review of supporting data. J Reprod Med 41 (1996) 633-639
6. Auerbach S.B., Rutter J.J., and Juliano P.J. Substituted piperazine and indole compounds increase extracellular serotonin in rat diencephalon as determined by in vivo microdialysis. Neuropharmacology 30 (1991) 307-311
7. Barnes N.M., and Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 38 (1999) 1083-1152
8. Best N.R., Rees M.P., Barlow D.H., and Cowen P.J. Effect of estradiol implant on noradrenergic function and mood in menopausal subjects. Psychoneuroendocrinology 17 (1992) 87-93
9. Birzniece V., Johansson I.M., Wang M.D., Seckl J.R., Backstrom T., and Olsson T. Serotonin 5-HT(1A) receptor mRNA expression in dorsal hippocampus and raphe nuclei after gonadal hormone manipulation in female rats. Neuroendocrinology 74 (2001) 135-142
10. Boschert U., Amara D.A., Segu L., and Hen R. The mouse 5-hydroxytryptamine1B receptor is localized predominantly on axon terminals. Neuroscience 58 (1994) 167-182
11. Bouwknecht J.A., Spiga F., Staub D.R., Hale M.W., Shekhar A., and Lowry C.A. Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull 72 (2007) 32-43
12. Boyer W.F., and Feighner J.P. An overview of paroxetine. J Clin Psychiatry 53 Suppl (1992) 3-6
13. Bridges R.S. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114 (1984) 930-940
14. Bruinvels A.T., Landwehrmeyer B., Gustafson E.L., Durkin M.M., Mengod G., Branchek T.A., Hoyer D., and Palacios J.M. Localization of 5-HT1B, 5-HT1D alpha, 5-HT1E and 5-HT1F receptor messenger RNA in rodent and primate brain. Neuropharmacology 33 (1994) 367-386
15. Burghardt N.S., Sullivan G.M., McEwen B.S., Gorman J.M., and LeDoux J.E. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiatry 55 (2004) 1171-1178
16. Clark M.S., McDevitt R.A., Hoplight B.J., and Neumaier J.F. Chronic low dose ovine corticotropin releasing factor or urocortin II into the rostral dorsal raphe alters exploratory behavior and serotonergic gene expression in specific subregions of the dorsal raphe. Neuroscience 146 (2007) 1888-1905
17. Clark M.S., McDevitt R.A., and Neumaier J.F. Quantitative mapping of tryptophan hydroxylase-2, 5-HT1A, 5-HT1B, and serotonin transporter expression across the anteroposterior axis of the rat dorsal and median raphe nuclei. J Comp Neurol 498 (2006) 611-623
18. Clark M.S., Sexton T.J., McClain M., Root D., Kohen R., and Neumaier J.F. Overexpression of 5-HT1B receptor in dorsal raphe nucleus using herpes simplex virus gene transfer increases anxiety behavior after inescapable stress. J Neurosci 22 (2002) 4550-4562
19. Clark M.S., Vincow E.S., Sexton T.J., and Neumaier J.F. Increased expression of 5-HT1B receptor in dorsal raphe nucleus decreases fear-potentiated startle in a stress dependent manner. Brain Res 1007 (2004) 86-97
20. Daws L.C., Gould G.G., Teicher S.D., Gerhardt G.A., and Frazer A. 5-HT(1B) receptor-mediated regulation of serotonin clearance in rat hippocampus in vivo. J Neurochem 75 (2000) 2113-2122
21. Day H.E., Greenwood B.N., Hammack S.E., Watkins L.R., Fleshner M., Maier S.F., and Campeau S. Differential expression of 5HT-1A, alpha 1b adrenergic, CRF-R1, and CRF-R2 receptor mRNA in serotonergic, gamma-aminobutyric acidergic, and catecholaminergic cells of the rat dorsal raphe nucleus. J Comp Neurol 474 (2004) 364-378
22. Doucet E., Pohl M., Fattaccini C.M., Adrien J., Mestikawy S.E., and Hamon M. In situ hybridization evidence for the synthesis of 5-HT1B receptor in serotoninergic neurons of anterior raphe nuclei in the rat brain. Synapse 19 (1995) 18-28
23. Durand M., Berton O., Aguerre S., Edno L., Combourieu I., Mormede P., and Chaouloff F. Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis axis in SHR and WKY rats. Neuropharmacology 38 (1999) 893-907
24. Fernandez-Guasti A., and Picazo O. Changes in burying behavior during the estrous cycle: effect of estrogen and progesterone. Psychoneuroendocrinology 17 (1992) 681-689
25. Freeman M.E. The neuroendocrine control of the ovarian cycle of the rat. In: Knobil E., and Neill J.D. (Eds). The physiology of reproduction (1994), Raven Press, Ltd, New York 613-648
26. Frye C.A., Petralia S.M., and Rhodes M.E. Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP. Pharmacol Biochem Behav 67 (2000) 587-596
27. Gordon J.A., and Hen R. The serotonergic system and anxiety. Neuromol Med 5 (2004) 27-40
28. Gorman J.M., Liebowitz M.R., Fyer A.J., Goetz D., Campeas R.B., Fyer M.R., Davies S.O., and Klein D.F. An open trial of fluoxetine in the treatment of panic attacks. J Clin Psychopharmacol 7 (1987) 329-332
29. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., Maier S.F., and Fleshner M. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 23 (2003) 2889-2898
30. Gregoire A.J., Kumar R., Everitt B., Henderson A.F., and Studd J.W. Transdermal oestrogen for treatment of severe postnatal depression. Lancet 347 (1996) 930-933
31. Gundlah C., Simon L.D., and Auerbach S.B. Differences in hypothalamic serotonin between estrous phases and gender: an in vivo microdialysis study. Brain Res 785 (1998) 91-96
32. Halbreich U., Rojansky N., Palter S., Tworek H., Hissin P., and Wang K. Estrogen augments serotonergic activity in postmenopausal women. Biol Psychiatry 37 (1995) 434-441
33. Hamblin M.W., Metcalf M.A., McGuffin R.W., and Karpells S. Molecular cloning and functional characterization of a human 5-HT1B serotonin receptor: a homologue of the rat 5-HT1B receptor with 5-HT1D-like pharmacological specificity. Biochem Biophys Res Commun 184 (1992) 752-759
34. Hammack S.E., Richey K.J., Schmid M.J., LoPresti M.L., Watkins L.R., and Maier S.F. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 22 (2002) 1020-1026
35. Hiroi R., McDevitt R.A., and Neumaier J.F. Estrogen selectively increases tryptophan hydroxylase-2 mRNA expression in distinct subregions of rat midbrain raphe nucleus: association between gene expression and anxiety behavior in the open field. Biol Psychiatry 60 (2006) 288-295
36. Hiroi R., and Neumaier J.F. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav Brain Res 166 (2006) 93-100
37. Hjorth S., Suchowski C.S., and Galloway M.P. Evidence for 5-HT autoreceptor-mediated, nerve impulse-independent, control of 5-HT synthesis in the rat brain. Synapse 19 (1995) 170-176
38. Hjorth S., and Tao R. The putative 5-HT1B receptor agonist CP-93,129 suppresses rat hippocampal 5-HT release in vivo: comparison with RU 24969. Eur J Pharmacol 209 (1991) 249-252
39. Hope W.G., Bruns M.E., and Thomas M.L. Regulation of duodenal insulin-like growth factor I and active calcium transport by ovariectomy in female rats. Proc Soc Exp Biol Med 200 (1992) 528-535
40. Hoplight B.J., Vincow E.S., and Neumaier J.F. The effects of SB 224289 on anxiety and cocaine-related behaviors in a novel object task. Physiol Behav 84 (2005) 707-714
41. Hoyer D., and Middlemiss D.N. Species differences in the pharmacology of terminal 5-HT autoreceptors in mammalian brain. Trends Pharmacol Sci 10 (1989) 130-132
42. Izumi J., Washizuka M., Hayashi-Kuwabara Y., Yoshinaga K., Tanaka Y., Ikeda Y., Kiuchi Y., and Oguchi K. Evidence for a depressive-like state induced by repeated saline injections in Fischer 344 rats. Pharmacol Biochem Behav 57 (1997) 883-888
43. Johnston A.L., and File S.E. 5-HT and anxiety: promises and pitfalls. Pharmacol Biochem Behav 24 (1986) 1467-1470
44. Kaiyala K.J., Vincow E.S., Sexton T.J., and Neumaier J.F. 5-HT1B receptor mRNA levels in dorsal raphe nucleus: inverse association with anxiety behavior in the elevated plus maze. Pharmacol Biochem Behav 75 (2003) 769-776
45. Kirby L.G., Rice K.C., and Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 22 (2000) 148-162
46. Lowry C.A., Evans A., Gasser P., Hale M., Staub D., and Shekhar A. Topographic organization and chemoarchitecture of the dorsal raphe nucleus and the median raphe nucleus. In: Monti J., et al. (Ed). Serotonin and sleep: Molecular, functional and clinical aspects, Vol. 001 (2008), Birkhauser Verlag AG, Basel, Switzerland 25-68
47. Lowry C.A. Functional subsets of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14 (2002) 911-923
48. Lu H., Ozawa H., Nishi M., Ito T., and Kawata M. Serotonergic neurones in the dorsal raphe nucleus that project into the medial preoptic area contain oestrogen receptor beta. J Neuroendocrinol 13 (2001) 839-845
49. Lund T.D., Rovis T., Chung W.C., and Handa R.J. Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146 (2005) 797-807
50. Maes M., and Meltzer H.Y. The serotonin hypothesis of major depression. In: Bloom F.E., and Kupfer D.J. (Eds). Psychopharmacology: The fourth generation of progress (1995), Raven Press, New York 933-944
51. Maier S.F., Grahn R.E., and Watkins L.R. 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock. Behav Neurosci 109 (1995) 404-412
52. Martin K.F., Hannon S., Phillips I., and Heal D.J. Opposing roles for 5-HT1B and 5-HT3 receptors in the control of 5-HT release in rat hippocampus in vivo. Br J Pharmacol 106 (1992) 139-142
53. Masand P.S., and Gupta S. Selective serotonin-reuptake inhibitors: an update. Harv Rev Psychiatry 7 (1999) 69-84
54. Maswood S., Barter J.E., Watkins L.R., and Maier S.F. Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 783 (1998) 115-120
55. Maswood S., Truitt W., Hotema M., Caldarola-Pastuszka M., and Uphouse L. Estrous cycle modulation of extracellular serotonin in mediobasal hypothalamus: role of the serotonin transporter and terminal autoreceptors. Brain Res 831 (1999) 146-154
56. McQueen J.K., Wilson H., and Fink G. Estradiol-17 beta increases serotonin transporter (SERT) mRNA levels and the density of SERT-binding sites in female rat brain. Brain Res Mol Brain Res 45 (1997) 13-23
57. Molliver M.E. Serotonergic neuronal systems: what their anatomic organization tells us about function. J Clin Psychopharmacol 7 (1987) 3S-23S
58. Morgan M.A., Schulkin J., and Pfaff D.W. Estrogens and non-reproductive behaviors related to activity and fear. Neurosci Biobehav Rev 28 (2004) 55-63
59. Neumaier J.F., Edwards E., and Plotsky P.M. 5-HT(1B) mRNA regulation in two animal models of altered stress reactivity. Biol Psychiatry 51 (2002) 902-908
60. Neumaier J.F., Root D.C., and Hamblin M.W. Chronic fluoxetine reduces serotonin transporter mRNA and 5-HT1B mRNA in a sequential manner in the rat dorsal raphe nucleus. Neuropsychopharmacology 15 (1996) 515-522
61. Neumaier J.F., Szot P., Peskind E.R., Dorsa D.M., and Hamblin M.W. Serotonergic lesioning differentially affects presynaptic and postsynaptic 5-HT1B receptor mRNA levels in rat brain. Brain Res 722 (1996) 50-58
62. Neumaier J.F., Sexton T.J., Hamblin M.W., and Beck S.G. Corticosteroids regulate 5-HT(1A) but not 5-HT(1B) receptor mRNA in rat hippocampus. Brain Res Mol Brain Res 82 (2000) 65-73
63. Palanza P. Animal models of anxiety and depression: how are females different?. Neurosci Biobehav Rev 25 (2001) 219-233
64. Pare W.P. Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiol Behav 55 (1994) 433-439
65. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic Press, Inc, San Diego
66. Pigott T.A. Anxiety disorders in women. Psychiatr Clin North Am 26 (2003) 621-672 vi-vii
67. Pohorecky L.A., Patel V., and Roberts P. Effects of ethanol in an open field apparatus: modification by U50488H and WIN 44441-3. Physiol Behav 45 (1989) 273-287
68. Pohorecky L.A., Roberts P., Cotler S., and Carbone J.J. Alteration of the effects of caffeine by prenatal stress. Pharmacol Biochem Behav 33 (1989) 55-62
69. Price M.L., Curtis A.L., Kirby L.G., Valentino R.J., and Lucki I. Effects of corticotropin-releasing factor on brain serotonergic activity. Neuropsychopharmacology 18 (1998) 492-502
70. Ramos A., Berton O., Mormede P., and Chaouloff F. A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85 (1997) 57-69
71. Robichaud M., and Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 17 (2005) 179-185
72. Roche M., Commons K.G., Peoples A., and Valentino R.J. Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23 (2003) 970-977
73. Rubinow D.R., Schmidt P.J., and Roca C.A. Estrogen-serotonin interactions: implications for affective regulation. Biol Psychiatry 44 (1998) 839-850
74. Sandford J.J., Argyropoulos S.V., and Nutt D.J. The psychobiology of anxiolytic drugs. Part 1: Basic neurobiology. Pharmacol Ther 88 (2000) 197-212
75. Sari Y. Serotonin1B receptors: from protein to physiological function and behavior. Neurosci Biobehav Rev 28 (2004) 565-582
76. Schneider L.S., Small G.W., Hamilton S.H., Bystritsky A., Nemeroff C.B., and Meyers B.S. Estrogen replacement and response to fluoxetine in a multicenter geriatric depression trial. Fluoxetine Collaborative Study Group. Am J Geriatr Psychiatry 5 (1997) 97-106
77. Schneider T., and Popik P. Attenuation of estrous cycle-dependent marble burying in female rats by acute treatment with progesterone and antidepressants. Psychoneuroendocrinology 32 (2007) 651-659
78. Sell S.L., Scalzitti J.M., Thomas M.L., and Cunningham K.A. Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats. J Pharmacol Exp Ther 293 (2000) 879-886
79. Sharp T., Bramwell S.R., and Grahame-Smith D.G. 5-HT1 agonists reduce 5-hydroxytryptamine release in rat hippocampus in vivo as determined by brain microdialysis. Br J Pharmacol 96 (1989) 283-290
80. Sharp T., and Hjorth S. Application of brain microdialysis to study the pharmacology of the 5-HT1A autoreceptor. J Neurosci Methods 34 (1990) 83-90
81. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
82. Sichel D.A., Cohen L.S., Robertson L.M., Ruttenberg A., and Rosenbaum J.F. Prophylactic estrogen in recurrent postpartum affective disorder. Biol Psychiatry 38 (1995) 814-818
83. Smith M.S., Freeman M.E., and Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96 (1975) 219-226
84. Steiner M., Dunn E., and Born L. Hormones and mood: from menarche to menopause and beyond. J Affect Disord 74 (2003) 67-83
85. Sumner B.E., Grant K.E., Rosie R., Hegele-Hartung C., Fritzemeier K.H., and Fink G. Effects of tamoxifen on serotonin transporter and 5-hydroxytryptamine(2A) receptor binding sites and mRNA levels in the brain of ovariectomized rats with or without acute estradiol replacement. Brain Res Mol Brain Res 73 (1999) 119-128
86. Svenningsson P., Chergui K., Rachleff I., Flajolet M., Zhang X., El Yacoubi M., Vaugeois J.M., Nomikos G.G., and Greengard P. Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 311 (2006) 77-80
87. Walf A.A., and Frye C.A. ERbeta-selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30 (2005) 1598-1609
88. Xu D., Buehner A., Xu J., Lambert T., Nekl C., Nielsen M.K., and Zhou Y. A polymorphic glucocorticoid receptor in a mouse population may explain inherited altered stress response and increased anxiety-type behaviors. FASEB J 20 (2006) 2414-2416
89. Zanardi R., Rossini D., Magri L., Malaguti A., Colombo C., and Smeraldi E. Response to SSRIs and role of the hormonal therapy in post-menopausal depression. Eur Neuropsychopharmacol 17 (2007) 400-405
90. Zhou W., Cunningham K.A., and Thomas M.L. Estrogen regulation of gene expression in the brain: a possible mechanism altering the response to psychostimulants in female rats. Brain Res Mol Brain Res 100 (2002) 75-83
91. Zweifel J.E., and O'Brien W.H. A meta-analysis of the effect of hormone replacement therapy upon depressed mood. Psychoneuroendocrinology 22 (1997) 189-212