Estrogen alters c-Fos response to immobilization stress in the brain of ovariectomized rats

Brain Research

Volumn 1084, Issue 1, 2006, Pages 67-79

  Ueyama, Takashi ^a   Tanioku, Tadashi ^a   Nuta, Junya ^a   Kujira, Kazuto ^a   Ito, Takao ^a   Nakai, Saori ^a   Tsuruo, Yoshihiro ^a  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

c Fos; Emotional stress; Estrogen; Heart failure; Takotsubo cardiomyopathy

Indexed keywords

ESTRADIOL; ESTROGEN; PLACEBO; PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN FUNCTION; BRAIN LEVEL; BRAIN REGION; CELL ACTIVITY; CELL COUNT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMOTIONAL STRESS; ESTROGEN ACTIVITY; ESTROGEN BLOOD LEVEL; FEMALE; HYPOTHALAMUS; HYPOTHALAMUS NUCLEUS; IMMOBILIZATION STRESS; IMMUNOREACTIVITY; LOCUS CERULEUS; MEDULLA OBLONGATA; MESENCEPHALON; NERVE CELL; NEUROMODULATION; NONHUMAN; OVARIECTOMY; PERIAQUEDUCTAL GRAY MATTER; PONS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; SEPTUM PELLUCIDUM; SOLITARY TRACT NUCLEUS; STIMULUS RESPONSE; TEGMENTUM; THALAMUS;

ANIMALS; BRAIN; ESTRADIOL; FEMALE; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; IMMOBILIZATION; IMMUNOHISTOCHEMISTRY; OVARIECTOMY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL;

ANIMALIA;

EID: 33646405468     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.02.008     Document Type: Article

References (82)

1. Akashi Y.J., Nakazawa K., Sakakibara M., Miyake F., Koike H., and Sasaka K. The clinical features of takotsubo cardiomyopathy. QJM 96 (2003) 563-573
2. Bailey T.W., and Dimicco J.A. Chemical stimulation of the dorsomedial hypothalamus elevates plasma ACTH in conscious rats. Am. J. Physiol. 280 (2001) R8-R15
3. Berridge C.W., and Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Rev. 42 (2003) 33-84
4. Bubser M., and Deutch A.Y. Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites. Synapse 32 (1999) 13-22
5. Bybee K.A., Kara T., Prasad A., Lerman A., Barsness G.W., Wright R.S., and Rihal C.S. Systemic review: transient left ventricular apical ballooning: a syndrome that mimics ST-segment elevation myocardial infarction. Ann. Intern. Med. 141 (2004) 858-865
6. Ceccatelli S., Villar M.J., Goldstein M., and Hökfelt T. Expression of c-Fos immunoreactivity in transmitter-characterized neurons after stress. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 9569-9573
7. Chambliss K.L., and Shaul P.W. Estrogen modulation of endothelial nitric oxide synthase. Endocr. Rev. 23 (2002) 665-686
8. Chen X., and Herbert J. Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64 (1995) 675-685
9. Chowdhury G.M., Fujioka T., and Nakamura S. Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress. Brain Res. Bull. 52 (2000) 171-182
10. Condé G.L., Bicknell R.J., and Herbison A.E. Changing patterns of Fos expression in brainstem catecholaminergic neurons during the rat oestrous cycle. Brain Res. 672 (1995) 68-76
11. Cullinan W.E., Herman J.P., Battaglia D.F., Akil H., and Watson S.J. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64 (1995) 477-505
12. da Silva L.G., de Menezes R.C., dos Santos R.A., Campagnole-Santos M.J., and Fontes M.A. Role of periaqueductal gray on the cardiovascular response evoked by disinhibition of the dorsomedial hypothalamus. Brain Res. 984 (2003) 206-214
13. Dayas C.V., and Day T.A. Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor. Eur. J. Neurosci. 15 (2002) 1712-1718
14. Dayas C.V., Buller K.M., and Day T.A. Neuroendocrine responses to an emotional stressor: evidence for involvement of the medial but not the central amygdala. Eur. J. Neurosci. 11 (1999) 2312-2322
15. Dayas C.V., Xu Y., Buller K.M., and Day T.A. Effects of chronic oestrogen replacement on stress-induced activation of hypothalamic-pituitary-adrenal axis control pathways. J. Neuroendocrinol. 12 (2000) 784-794
16. Dayas C.V., Buller K.M., and Day T.A. Medullary neurons regulate hypothalamic corticotropin-releasing factor cell responses to an emotional stressor. Neuroscience 105 (2001) 707-719
17. Dayas C.V., Buller K.M., Crane J.W., Xu Y., and Day T.A. Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur. J. Neurosci. 14 (2001) 1143-1152
18. Dayas C.V., Buller K.M., and Day T.A. Hypothalamic paraventricular nucleus neurons regulate medullary catecholamine cell responses to restraint stress. J. Comp. Neurol. 478 (2004) 22-34
19. DiMicco J.A., Samuels B.C., Zaretskaia M.V., and Zaretsky D.V. The dorsomedial hypothalamus and the response to stress. Part renaissance, part revolution. Pharmacol. Biochem. Behav. 71 (2002) 469-480
20. Estacio M.A., Yamada S., Tsukamura H., Hirunagi K., and Maeda K. Effect of fasting and immobilization stress on estrogen receptor immunoreactivity in the brain in ovariectomized female rats. Brain Res. 717 (1996) 55-61
21. Estacio M.A., Tsukamura H., Reyes B.A., Uenoyama Y., I'anson H., and Maeda K. Involvement of brainstem catecholaminergic inputs to the hypothalamic paraventricular nucleus in estrogen receptor alpha expression in this nucleus during different stress conditions in female rats. Endocrinology 145 (2004) 4917-4926
22. Fontes M.A., Tagawa T., Polson J.W., Cavanagh S.J., and Dampney R.A. Descending pathways mediating cardiovascular response from dorsomedial hypothalamic nucleus. Am. J. Physiol. 280 (2001) H2891-H2901
23. Gréco B., Allegretto E.A., Tetel M.J., and Blaustein J.D. Coexpression of ERβ with ERα and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 142 (2001) 5172-5181
24. Haywood S.A., Simonian S.X., van der Beek E.M., Bicknell R.J., and Herbison A.E. Fluctuating estrogen and progesterone receptor expression in brainstem norepinephrine neurons through the rat estrous cycle. Endocrinology 140 (1999) 3255-3263
25. He X.R., Wang W., Crofton J.T., and Share L. Effects of 17β-estradiol on sympathetic activity and pressor response to phenylephrine in ovariectomized rats. Am. J. Physiol. 275 (1998) R1202-R1208
26. Horiuchi J., McAllen R.M., Allen A.M., Killinger S., Fontes M.A., and Dampney R.A. Descending vasomotor pathways from the dorsomedial hypothalamic nucleus: role of medullary raphe and RVLM. Am. J. Physiol. 287 (2004) R824-R832
27. Isgor C., Cecchi M., Kabbaj M., Akil H., and Watson S.J. Estrogen receptor β in the paraventricular nucleus of hypothalamus regulates the neuroendocrine response to stress and is regulated by corticosterone. Neuroscience 121 (2003) 837-845
28. Jennes L., Jennes M.E., Purvis C., and Nees M. c-fos expression in noradrenergic A2 neurons of the rat during the estrous cycle and after steroid hormone treatments. Brain Res. 586 (1992) 171-175
29. Komesaroff P.A., Esler E.D., and Sudhir K. Estrogen supplementation attenuates glucocorticoid and catecholamine responses to mental stress in perimenopausal women. J. Clin. Endocrinol. Metab. 84 (1999) 606-610
30. Krout K.E., Belzer R.E., and Loewy A.D. Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 448 (2002) 53-101
31. Kubo T., Kanaya T., Numakura H., Okajima H., Hagiwara Y., and Fukumori R. The lateral septal area is involved in mediation of immobilization stress-induced blood pressure increase in rats. Neurosci. Lett. 318 (2002) 25-28
32. Kubo T., Okatani H., Kanaya T., Hagiwara Y., Fukumori R., and Goshima Y. Cholinergic mechanism in the lateral septal area is involved in the stress-induced blood pressure increase in rats. Brain Res. Bull. 59 (2003) 359-364
33. Kubo T., Okatani H., Nishigori Y., Hagiwara Y., Fukumori R., and Goshima Y. Involvement of the medial amygdaloid nucleus in restraint stress-induced pressor responses in rats. Neurosci. Lett. 354 (2004) 84-86
34. Kurisu S., Sato H., Kawagoe T., Ishihara M., Shimatani Y., Nishioka K., Kono Y., Umemura T., and Nakamura S. Tako-tsubo-like left ventricular dysfunction with ST-segment elevation: a novel cardiac syndrome mimicking acute myocardial infarction. Am. Heart J. 143 (2002) 448-455
35. Kvetnansky R., Pacak K., Fukuhara K., Viskupic E., Hiremagalur B., Nankova B., Goldstein D.S., Sabban E.L., and Kopin I.J. Sympathoadrenal system in stress. Interaction with the hypothalamic-pituitary-adrenocortical system. Ann. N. Y. Acad. Sci. 771 (1995) 131-158
36. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERα and ERβ) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J. Neurobiol. 36 (1998) 357-378
37. Li R., and Shen Y. Estrogen and brain: synthesis, function and diseases. Front. Biosci. 10 (2005) 257-267
38. Luque J.M., de Blas M.R., Segovia S., and Guillamon A. Sexual dimorphism of the dopamine-beta-hydroxylase-immunoreactive neurons in the rat locus ceruleus. Dev. Brain Res. 67 (1992) 211-215
39. Ma S., and Morilak D.A. Induction of FOS expression by acute immobilization stress is reduced in locus coeruleus and medial amygdala of Wistar-Kyoto rats compared to Sprague-Dawley rats. Neuroscience 124 (2004) 963-972
40. Merchenthaler I., Dellovade T.L., and Shughrue P.J. Neuroprotection by estrogen in animal models of global and focal ischemia. Ann. N. Y. Acad. Sci. 1007 (2003) 89-100
41. Morimoto K., Kurahashi Y., Shintani-Ishida K., Kawamura N., Miyashita M., Uji M., Tan N., and Yoshida K. Estrogen replacement suppresses stress-induced cardiovascular responses in ovariectomized rats. Am. J. Physiol. 287 (2004) H1950-H1956
42. Morin S.M., Stotz-Potter E.H., and DiMicco J.A. Injection of muscimol in dorsomedial hypothalamus and stress-induced Fos expression in paraventricular nucleus. Am. J. Physiol. 280 (2001) R1276-R1284
43. Osterlund M., Kuiper G.G., Gustafsson J.A., and Hurd Y.L. Differential distribution and regulation of estrogen receptor-α and -β mRNA within the female rat brain. Mol. Brain Res. 54 (1998) 175-180
44. Östlund H., Keller E., and Hurd Y.L. Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann. N. Y. Acad. Sci. 1007 (2003) 54-63
45. Otake K., Kin K., and Nakamura Y. Fos expression in afferents to the rat midline thalamus following immobilization stress. Neurosci. Res. 43 (2002) 269-282
46. Palmer A.A., and Printz M.P. Strain differences in Fos expression following airpuff startle in spontaneously hypertensive and Wistar Kyoto rats. Neuroscience 89 (1999) 965-978
47. Patisaul H.B., Whitten P.L., and Young L.J. Regulation of estrogen receptor β mRNA in the brain: opposite effects of 17β-estradiol and the phytoestrogen, coumestrol. Mol. Brain Res. 67 (1999) 165-171
48. Paxinos G., and Watson C. The Rat Brain in Stereotactic Coordinates. 4th ed. (1998), Academic Press, San Diego
49. Rachman I.M., Unnerstall J.R., Pfaff D.W., and Cohen R.S. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 13941-13946
50. Saleh M.C., Connell B.J., and Saleh T.M. Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats. Brain Res. 879 (2000) 105-114
51. Saleh T.M., Connell B.J., and Saleh M.C. Acute injection of 17β-estradiol enhances cardiovascular reflexes and autonomic tone in ovariectomized female rats. Auton. Neurosci. 84 (2000) 78-88
52. Saleh T.M., Saleh M.C., and Connell B.J. Estrogen blocks the cardiovascular and autonomic changes following vagal stimulation in ovariectomized rats. Auton. Neurosci. 88 (2001) 25-35
53. Samuels B.C., Zaretsky D.V., and DiMicco J.A. Dorsomedial hypothalamic sites where disinhibition evokes tachycardia correlate with location of raphe-projecting neurons. Am. J. Physiol. 287 (2004) R472-R478
54. Senba E., and Ueyama T. Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci. Res. 29 (1997) 183-207
55. Serova L.I., Maharjan S., and Sabban E.L. Estrogen modifies stress response of catecholamine biosynthetic enzyme genes and cardiovascular system in ovariectomized female rats. Neuroscience 132 (2005) 249-259
56. Shughrue P.J., and Merchenthaler I. Distribution of estrogen receptor β immunoreactivity in the rat central nervous system. J. Comp. Neurol. 436 (2001) 64-81
57. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997) 507-525
58. Shughrue P.J., Scrimo P.J., and Merchenthaler I. Evidence for the colocalization of estrogen receptor-β mRNA and estrogen receptor-α immunoreactivity in neurons of the rat forebrain. Endocrinology 139 (1998) 5267-5270
59. A and excitatory amino acid receptors controlling heart rate in rats. Am. J. Physiol. 261 (1991) R427-R433
60. Soltis R.P., and DiMicco J.A. Hypothalamic excitatory amino acid receptors mediate stress-induced tachycardia in rats. Am. J. Physiol. 262 (1992) R689-R697
61. Stern J.E., and Zhang W. Preautonomic neurons in the paraventricular nucleus of the hypothalamus contain estrogen receptor β. Brain Res. 975 (2003) 99-109
62. Stotz-Potter E.H., Morin S.M., and DiMicco J.A. Effect of microinjection of muscimol into the dorsomedial or paraventricular hypothalamic nucleus on air stress-induced neuroendocrine and cardiovascular changes in rats. Brain Res. 742 (1996) 219-224
63. Stotz-Potter E.H., Willis L.R., and DiMicco J.A. Muscimol acts in dorsomedial but not paraventricular hypothalamic nucleus to suppress cardiovascular effects of stress. J. Neurosci. 16 (1996) 1173-1179
64. Suzuki S., and Handa R.J. Regulation of estrogen receptor-β expression in the female rat hypothalamus: differential effects of dexamethasone and estradiol. Endocrinology 145 (2004) 3658-3670
65. Thompson R.H., and Swanson L.W. Organization of inputs to the dorsomedial nucleus of the hypothalamus: a reexamination with Fluorogold and PHAL in the rat. Brain Res. Rev. 27 (1998) 89-118
66. Thompson R.H., Canteras N.S., and Swanson L.W. Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J. Comp. Neurol. 376 (1996) 143-173
67. Tseng J.Y., Kolb P.E., Raskind M.A., and Miller M.A. Estrogen regulates galanin but not tyrosine hydroxylase gene expression in the rat locus ceruleus. Mol. Brain Res. 50 (1997) 100-106
68. Tsuchihashi K., Ueshima K., Uchida T., Oh-mura N., Kimura K., Owa M., Yoshiyama M., Miyazaki S., Haze K., Ogawa H., Honda T., Hase M., Kai R., and Morii I. Transient left ventricular apical ballooning without coronary artery stenosis: a novel heart syndrome mimicking acute myocardial infarction. Angina Pectoris-Myocardial Infarction Investigations in Japan. J. Am. Coll. Cardiol. 38 (2001) 11-18
69. Tsuda K., Yokoo H., and Goldstein M. Neuropeptide Y and galanin in norepinephrine release in hypothalamic slices. Hypertension 14 (1989) 81-86
70. Tsukahara S., and Yamanouchi K. Sex difference in septal neurons projecting axons to midbrain central gray in rats: a combined double retrograde tracing and ER-immunohistochemical study. Endocrinology 143 (2002) 285-294
71. Ueyama T. Emotional stress-induced tako-tsubo cardiomyopathy-Animal model and molecular mechanism. Ann. N. Y. Acad. Sci. 1018 (2004) 437-444
72. Ueyama T., Yoshida K., and Senba E. Emotional stress induces expression of immediate early genes in rat heart via activation of α- and β-adrenoceptors. Am. J. Physiol. 277 (1999) H1553-H1561
73. Ueyama T., Yoshida K., and Senba E. Stress-induced elevation of the ST segment in the rat electrocardiogram is normalized by an adrenoceptor blocker. Clin. Exp. Pharmacol. Physiol. 27 (2000) 384-386
74. Ueyama T., Kasamatsu K., Yamamoto K., Hano T., Tsuruo Y., and Nishio I. Emotional stress induces transient left ventricular hypo-contraction in the rat via activation of cardiac adrenoceptors-A possible animal model of tako-tsubo cardiomyopathy. Circ. J. 66 (2002) 712-713
75. Ueyama T., Hano T., Kasamatsu K., Yamamoto K., Tsuruo Y., and Nishio I. Estrogen attenuates the emotional stress-induced cardiac responses in the animal model of tako-tsubo (Ampulla) cardiomyopathy. J. Cardiovasc. Pharmacol. 42 (2003) S117-S119
76. Ueyama T., Ito T., and Tsuruo Y. Estrogen alters c-Fos response to immobilization stress in the brain of ovariectomized rats. Neurosci. Res. 52 (2005) S200
77. Vongpatanasin W., Tuncel M., Mansour Y., Arbique D., and Victor R.G. Transdermal estrogen replacement therapy decreases sympathetic activity in postmenopausal women. Circulation 103 (2001) 2903-2908
78. Weitz G., Elam M., Born J., Fehm H.L., and Dodt C. Postmenopausal estrogen administration suppresses muscle sympathetic nerve activity. J. Clin. Endocrinol. Metab. 86 (2001) 344-348
79. Westerhaus M.J., and Loewy A.D. Central representation of the sympathetic nervous system in the cerebral cortex. Brain Res. 903 (2001) 117-127
80. Wittstein I.S., Thiemann D.R., Lima J.A., Baughman K.L., Schulman S.P., Gerstenblith G., Wu K.C., Rade J.J., Bivalacqua T.J., and Champion H.C. Neurohumoral features of myocardial stunning due to sudden emotional stress. N. Engl. J. Med. 352 (2005) 539-548
81. Xue B., and Hay M. 17β-estradiol inhibits excitatory amino acid-induced activity of neurons of the nucleus tractus solitarius. Brain Res. 976 (2003) 41-52
82. Zaretsky D.V., Zaretskaia M.V., Samuels B.C., Cluxton L.K., and DiMicco J.A. Microinjection of muscimol into raphe pallidus suppresses tachycardia associated with air stress in conscious rats. J. Physiol. 546 (2003) 243-250