17β-Estradiol alters the response of subfornical organ neurons that project to supraoptic nucleus to plasma angiotensin II and hypernatremia

Brain Research

Volumn 1526, Issue , 2013, Pages 54-64

  Ciriello, John ^a   Roder, Stefanie ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

Arterial pressure; Body fluid homeostasis; Cardiovascular regulation; Circumventricular organ; Steroids; Vasopressin

Indexed keywords

ANGIOTENSIN II; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; CIRCULATION; HYPERNATREMIA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULATION; SUBFORNICAL ORGAN; SUPRAOPTIC NUCLEUS; VASOPRESSIN RELEASE;

17Β-ESTRADIOL; 17Β-ESTRADIOL TREATED OVARIECTOMIZED RAT; 3RD VENTRICLE; 3V; AHA; ANTERIOR HYPOTHALAMIC AREA; ARTERIAL PRESSURE; AT(1)R; BODY FLUID HOMEOSTASIS; CARDIOVASCULAR REGULATION; CIRCUMVENTRICULAR ORGAN; E(2); FORNIX; FX; NACL; OPTIC TRACT; OT; OVARIECTOMIZED RAT; OVX; OVX+E(2); PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PARAVENTRICULAR THALAMIC NUCLEUS, ANTERIOR COMPONENT; PVA; PVH; SCH; SFO; SM; SODIUM CHLORIDE; SON; STEROIDS; STRIA MEDULLARIS; SUBFORNICAL ORGAN; SUPRACHIASMATIC NUCLEUS; SUPRAOPTIC NUCLEUS; TRANSIENT RECEPTOR POTENTIAL VANILLOID-4 CHANNEL; TRPV-4; TYPE-1 ANGIOTENSIN II RECEPTOR; VASOPRESSIN; VENTRAL HSIPPOCAMPAL COMMISSURE; VHC;

ANGIOTENSIN II; ANIMALS; ESTRADIOL; FEMALE; HYPERNATREMIA; NEURAL PATHWAYS; NEURONS; OVARIECTOMY; RATS; RATS, WISTAR; SUBFORNICAL ORGAN; SUPRAOPTIC NUCLEUS;

ANIMALIA; RATTUS;

EID: 84880918568     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.06.038     Document Type: Article

References (96)

1. T. Akaishi, and S. Homma Osmolality- and angiotensin-induced responses in the AV3V neurons are affected by estrogen in the ovariectomized rat Neurosci. Lett. 202 1996 153 156
2. T. Akaishi, and Y. Sakuma Estrogen-induced modulation of hypothalamic osmoregulation in female rats Am. J. Physiol. 258 1990 R924 R929
3. J.W. Anderson, D.L. Washburn, and A.V. Ferguson Intrinsic osmosensitivity of subfornical organ neurons Neuroscience 100 2000 539 547
4. L.A. Arbogast Estrogen genomic and membrane actions at an intersection Trends Endocrinol. Metab. 19 2008 1 2
5. W.M. Barron, J. Schreiber, and M.D. Lindheimer Effect of ovarian sex steroid on osmoregulation and vasopressin secretion in the rat Am. J. Physiol. 250 1986 E352 E361
6. F.M. Chen, and M.P. Printz Chronic estrogen treatment reduces angiotensin II receptors in the anterior pituitary Endocrinology 113 1983 1503 1510
7. J. Chen, S. Yang, S. Hu, M.A. Choudhry, K.I. Bland, and I.H. Chaudry Estrogen prevents intestinal inflammation after trauma-hemorrhage via downregulation of angiotensin II and angiotensin II subtype I receptor Am. J. Physiol. Gastrointest. Liver Physiol. 295 2008 G1131 G1137
8. J. Ciriello Afferent renal inputs onto subfornical organ neurons responsive to angiotensin II Am. J. Physiol. 272 1997 R1684 R1689
9. J. Ciriello Caudal ventrolateral medulla mediates baroreceptor afferent inputs to subfornical organ angiotensin II responsive neurons Brain Res. 1491 2013 127 135
10. J. Ciriello, and L.A. Wilk Effect of oestrogen on the depressor responses elicited by stimulation of nucleus tractus solitarius FASEB J. (Abstr.) 10 1996 A408
11. G.T. Cottrell, and A.V. Ferguson Sensory circumventricular organs: central roles in integrated autonomic regulation Regul. Peptides 117 2004 11 23
12. C.V. De Oliveira, M.P. Rosas-Arellano, L.P. Solano-Flores, T. Babic, Z. Li, and J. Ciriello Estrogen alters the bradycardia response to hypocretin-1 in the nucleus tractus solitarius of the ovariectomized female Brain Res. 978 2003 14 23
13. P. Dhanarajan A Quantitative Study of the Negative Feedback Control of Luteinizing Hormone and Follicle-stimulating Hormone by Estrogen and Progesterone in the Ovariectomized Rat 1978 University of Western Ontario London, Canada (M. Sc. Thesis)
14. S Diano, F Naftolin, and TL. Horvath Gonadal steroids target AMPA glutamate receptor-containing neurons in the rat hypothalamus, septum and amygdala: a morphological and biochemical study Endocrinology 138 1997 778 789
15. R. Dominguez, and P. Micevych Estradiol rapidly regulates membrane estrogen receptor levels in hypothalamic neurons J. Neurosci. 30 2010 12589 12596
16. X.-J. Du, R.A. Riemersma, and A.M. Dart Cardiovascular protection by estrogen is partly mediated through modulation of autonomic nervous function Cardiovasc. Res. 30 1995 161 165
17. M. Fatehi, J.A. Zidichouski, S.B. Kombian, and T.M. Saleh 17beta-estradiol attenuates excitatory neurotransmission and enhances the excitability of rat parabrachial neurons in vitro J. Neurosci. Res. 84 2006 666 674
18. A.V. Ferguson, and C. Loucks Cardiovascular and single-unit responses to subfornical organ stimulation are abolished by pentobarbital anesthesia Can. J. Physiol. Pharmacol. 72 1994 1031 1034
19. A.V. Ferguson, and N.W. Kasting Electrical stimulation in subfornical organ increases plasma vasopressin concentrations in the conscious rat Am. J. Physiol. 251 1986 R425 R428
20. A.V. Ferguson, and L.P. Renaud Systemic angiotensin acts at subfornical organ to facilitate activity of neurohypophyseal neurons Am. J. Physiol. 251 1986 R712 R717
21. A.L.R. Findlay, J.T Fitzsimons, and J. Kucharczyk Dependence of spontaneous and angiotensin-induced drinking in the rat upon the oestrous cycle and ovarian hormones J. Endocrinol. 82 1979 215 225
22. J.T. Fitzsimons Angiotensin, thirst, and sodium appetite Physiol. Rev. 78 1998 583 686
23. M.J. Fregly Effect of chronic treatment with estrogen on the dipsogenic responses of rats to angiotensin Pharmacol. Biochem. Behav. 12 1980 131 136
24. M.J. Fregly, and T.N. Thrasher Attenuation of angiotensin-induced water intake in estrogen-treated rats Pharmacol. Biochem. Behav. 9 1978 509 514
25. P.M. Gross The subfornical organ as a model of neurohumoral integration Brain Res. Bull. 15 1985 65 70
26. M.B. Gutman, J. Ciriello, and G.J. Mogenson Electrophysiological identification of forebrain connections of subfornical organ Brain Res. 382 1986 119 128
27. M.B. Gutman, J. Ciriello, and G.J. Mogenson Effect of paraventricular nucleus lesions on cardiovascular responses elicited by stimulation of the subfornical organ in the rat Can. J. Physiol. Pharmacol. 63 1985 816 824
28. M.B. Gutman, J. Ciriello, and G.J. Mogenson Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons Am. J. Physiol. 254 1988 R746 R754
29. M.B. Gutman, D.L. Jones, and J. Ciriello Contribution of nucleus medianus to drinking and pressor responses to angiotensin II acting at subfornical organ Brain Res. 488 1989 49 56
30. D.P. Healy, and M.P. Printz Autoradiographic localization of angiotensin II binding sites I the brain, pituitary, kidney and adrenal gland of the rat J. Hypertens. Suppl. 2 1984 S57 S61
31. A.E. Herbison, and V.S. Fénelon Estrogen regulation of GABAA receptor subunit mRNA expression in preoptic area and bed nucleus of the stria terminalis of female rat brain J. Neurosci. 15 1995 2328 2337
32. H. Hashimoto, H. Otsubo, H. Fujihara, H. Suzuki, T. Ohbuchi, T. Yokoyama, Y. Takei, and Y. Ueta Centrally administered ghrelin potently inhibits water intake induced by angiotensin II and hypovolemia in rats J. Physiol. Sci. 60 2010 19 25
33. J. Huang, S.I. Chowhdury, and M.L. Weiss Distribution of sympathetic preganglionic neurons innervating the kidney in the rat: PRV transneuronal tracing and serial reconstruction Auton. Neurosci. 95 2002 57 70
34. K. Inenaga, T. Nagatomo, E. Honda, Y. Ueta, and H. Yamashita Gabaergic inhibitory inputs to subfornical organ neurons in rat slice preparations Brain. Res. 705 1995 85 90
35. S. Ishibashi, and S. Nicolaidis Hypertension induced by electrical stimulation of the subfornical organ (SFO) Brain Res. Bull. 6 1981 135 139
36. J Jacob, K.S. Sebastian, S. Devassy, L. Priyadarsini, M.F. Farook, A. Shameem, D. Mathew, S. Sreeja, and R.V. Thampan Membrane estrogen receptors: genomic actions and post transcriptional regulation Mol. Cell. Endocrinol. 2006 24634 24641
37. A.K. Johnson The periventricular anteroventral third ventricle (AV3V): its relationship with the subfornical organ and neural systems involved in maintaining body fluid homeostasis Brain Res. Bull. 15 1985 595 601
38. A.K. Johnson, A.M. Zardetto-Smith, and G.L. Edwards Integrative mechanisms and the maintenance of cardiovascular and body fluid homeostasis: the central processing of sensory input derived from the circumventricular organs of the lamina terminalis Prog. Brain Res. 91 1992 381 393
39. J. Jonklass, and J. Buggy Angiotensin-estrogen interaction in female brain reduces drinking and pressor responses Am. J. Physiol. 247 1984 R167 R172
40. M. Kawata Roles of steroid hormones and their receptors in structural organization in the nervous system Neurosci. Res. 24 1995 1 46
41. R. Khakpay, S. Semnanian, M. Javan, and M. Janahmadi The effect of intra-locus coeruleus injection of 17beta-estradiol on inflammatory pain modulation in male rat Behav. Brain Res. 214 2010 409 416
42. L. Kisley, R.R.R. Sakai, and S.J. Fluharty Estrogen decreases hypothalamic angiotensin II AT1 receptor binding and mRNA in the female rat Brain Res. 844 1999 34 42
43. E.G. Krause, S.J. Melhorn, J.F. Davis, K.A. Scott, L.Y. Ma, A.D. de Kloet, S.C. Benoit, S.C. Woods, and R.R. Sakai Angiotensin type 1 receptors in the subfornical organ mediate the drinking and hypothalamic-pituitary-adrenal response to systemic isoproterenol Endocrinology 149 2008 6416 6424
44. K. Kubo, R.A. Gorski, and M. Kawakami Effects of estrogen on neuronal excitability in the hippocampal-septal-hypothalamic system Neuroendocrinology 18 1975 176 191
45. P.J. Larsen, W.L. Enquist, and J.P. Card Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing Eur. J. Neurosci. 10 1998 128 145
46. T.K. Lee, J.H. Lois, J.H. Troupe, T.D. Wilson, and B.J. Yates Transneuronal tracing of neural pathways that regulate hindlimb muscle blood flow Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R1532 R1541
47. S.J. Legan, C.A. Coon, and F.J. Karsch Role of estrogen as initiator of daily LH surges in the ovariectomized rat Endocrinology 96 1975 50 56
48. W. Liedtke, Y. Choe, M.A. Martí-Renom, A.M. Bell, Charlotte S. Denis, Andrej Šali, A.J. Hudspeth, J.M. Friedman, and S. Stefan Heller Vanilloid receptor-related osmotically activated channel (VROAC), a candidate vertebrate osmoreceptor Cell 103 2000 525 535
49. Z. Li, and M. Hay 17-Estradiol modulation of area postrema potassium currents J. Neurophysiol. 84 2000 1385 1391
50. R.W. Lind, and A.K. Johnson Subfornical organ-median preoptic connections and drinking and pressor responses to angiotensin II J. Neurosci. 2 1982 1043 1051
51. VN Luine, and M. Frankfurt Estrogens facilitate memory processing through membrane mediated mechanisms and alterations in spine density Front. Neuroendocrinol. 33 2012 388 402
52. M.L. Mangiapane, and J.B. Simpson Subfornical organ: forebrain site of pressor and dipsogenic action of angiotensin II Am. J. Physiol. 239 1980 R382 R389
53. M. Marean, C.E. Cumming, E.E. Fox, and D.C. Cumming Fluid intake in women with premenstrual syndrome Women Health 23 3 1995 75 78
54. M.J. McKinley, A.M. Allen, C.N. May, R.M. McAllen, B.J. Oldfield, D. Sly, and F.A. Mendelsohn Neural pathways from the lamina terminalis influencing cardiovascular and body fluid homeostasis Clin. Exp. Pharmacol. Physiol. 28 2001 990 992
55. F.A. Mendelsohn, R. Quirion, J.M. Saavedra, G. Aguilera, and K.J. Catt Autoradiographic localization of angiotensin II receptors in rat brain Proc. Natl. Acad. Sci. USA 81 1984 1575 1579
56. P.G. Mermelstein, J.B. Becker, and D.J. Sürmeier Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor J. Neurosci. 16 1996 595 604
57. R.R. Miselis The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance Brain Res. 230 1981 1 23
58. J.A. Mong, E. Glaser, and M.M. McCarthy Gonadal steroids promote glial differentiation and alter neuronal morphology in the developing hypothalamus in a regionally specific manner J. Neurosci. 19 1999 1464 1472
59. E.J. Mufson, W.J. Cai, S. Jaffar, E. Chen, G. Stebbins, T. Sendra, and J.H. Kordowen Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetytransferase Brain Res. 849 1999 253 274
60. J. Pamidimukkala, and M. Hay 17β-estradiol inhibits angiotensin II activation of area postrema neurons Am. J. Physiol. 285 2003 H1515 H1520
61. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 1986 Academic Press Sydney
62. M.I. Phillips, L. Shen, E.M. Richards, and M.K. Raizada Immunohistochemical mapping of angiotensin AT1 receptors in the brain Regul. Peptides 44 1993 95 107
63. V. Ramirez, D.J. Zheng, and K.M. Siddique Membrane receptors for estrogen, progesterone, and testosterone in the rat brain: fantasy or reality Cell. Mol. Neurobiol. 16 1996 175 198
64. D.J. Ramsay The importance of thirst in maintenance of fluid balance Baillieres Clin. Endocrinol. Metab. 3 1989 371 391
65. A. Robertson, J. Kucharczyk, and G.J. Mogenson Drinking behaviour following electrical stimulation of the subfornical organ in the rat Brain Res. 274 1983 197 200
66. C. Rollin, J. Kucharczyk, J. Lemoine, D. Bichet, and B.K. Tsang Osmoregulation of vasopressin secretion and thirst during the estrous cycle of pigs Am. J. Physiol. 256 1989 R270 R275
67. M.P. Rosas-Arellano, L.P. Solano-Flores, and J. Ciriello Co-localization of estrogen and angiotensin receptors within subfornical organ Brain Res. 837 1999 254 262
68. B.P. Rowe, D.L. Saylor, and R.C. Speth Analysis of angiotensin II receptor subtypes in individual rat brain nuclei Neuroendocrinology 55 1992 563 573
69. W.A. Saad, L.A. Camargo, I.F. Guarda, and T.A. Santos Subfornical organ mediates pressor effect of angiotensin: influence of nitric oxide synthase inhibitors, AT(1) and AT(2) angiotensin antagonist's receptors J. Am. Soc. Hypertens. 2 2008 326 331
70. T.M. Saleh, B.J. Connell, T. McQuaid, and A.E. Cribb Estrogen-induced neurochemical and electrophysiological changes in the parabrachial nucleus of the male rat Brain Res. 990 2003 58 65
71. T.M. Saleh, and M.C. Saleh Inhibitory effect of 17β-estradiol in the parabrachial nucleus mediated by GABA Brain Res. 911 2001 116 124
72. S.J. Sample, M.A. Racette1, Z. Hao, C.F. Cathy F. Thomas, M. Behan, and M. Muir Functional adaptation in female rats: the role of estrogen signalling PLoS ONE 9 2012 e43215
73. M.C. Schiess, M. Joels, and P. Shinnick-Gallagher Estrogen priming affects active membrane properties of medial amygdala neurons Brain Res. 440 1988 380 385
74. H. Schunkert, A.H.J. Danser, H.-W. Hense, F.H.M. Derkx, S. Kurzinger, and G.A.J. Riegger Effects of estrogen replacement therapy on the renin-angiotensin system in postmenopausal women Circulation 95 1997 39 45
75. A. Seltzer, J.E.B. Pinto, P.N. Viglione, F.M.A. Correa, C. Liertun, K. Tsutsumi, M.K. Steele, and J.M. Saavedra Estrogen regulates angiotensin- converting enzyme and angiotensin receptors in female rat anterior pituitary Neuroendocrinology 55 1992 460 467
76. T. Shahar, and M. Palkovits Cross over of forebrain and brainstem neuronal projections to spinal cord sympathetic preganglionic neurons in the rat Stress 10 2007 145 152
77. R.B. Simerly, C. Chang, M. Muramatsu, and L.W. Swanson Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study J. Comp. Neurol. 294 1990 76 95
78. J.B. Simpson, and A. Routtenberg Subfornical organ: site of drinking elicitation by angiotensin II Science 181 1973 1172 1175
79. J.B. Simpson, A.N. Epstein, and J.S. Camardo Localization of receptors for the dipsogenic action of angiotensin II in the subfornical organ of the rat J. Comp. Physiol. Psychol. 92 1978 561 608
80. C.D. Sladek, and S.J. Somponpun Estrogen receptors: their roles in regulation of vasopressin release for maintenance of fluid and electrolyte homeostasis Front. Neuroendocrinol. 29 2008 114 127
81. P.M. Smith, G. Rozanski, and A.V. Ferguson Acute electrical stimulation of the subfornical organ induces feeding in satiated rats Physiol. Behav. 99 2010 534 537
82. S.S. Smith, B.D. Waterhouse, and D.J. Woodward Locally applied estrogens potentiate glutamate-evoked excitation of cerebellar purkinje cells Brain Res. 475 1988 272 282
83. S.J. Somponpun, A.K. Johnson, and T. Beltz Sladek C.D., Estrogen receptor-alpha expression in osmosensitive elements of the lamina terminalis: regulation by hypertonicity Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 2004 R661 669
84. K.A. Song, A.M. Allen, G. Paxinos, and F.A.O. Mendelsohn Mapping of angiotensin II receptor subtype heterogenity in rat brain J. Comp. Neurol. 316 1992 467 484
85. K. Song, A.M. Allen, G. Paxinos, and F.A. Mendelsohn Angiotensin II receptor subtypes in rat brain Clin. Exp. Pharmacol. Physiol. 18 1991 93 96
86. J. Tanaka, K. Kariya, H. Miyakubo, K. Sakamaki, and M. Nomura Attenuated drinking response induced by angiotensinergic activation of subfornical organ projections to the paraventricular nucleus in estrogen-treated rats Neurosci. Lett. 324 2002 242 246
87. J. Tanaka, H. Miyakubo, T. Okumura, K. Sakamaki, and Y. Hayashi Estrogen decreases the responsiveness of subfornical organ neurons projecting to the hypothalamic paraventricular nucleus to angiotensin II in female rats Neurosci. Lett. 307 2001 155 158
88. T.J. Teyler, R.M. Vardaris, D. Lewis, and A.B. Rawitch Gonadal steroids. Effects on the excitability of hippocampal and pyramidal cells Science 209 1980 1017 1019
89. G.M. Toney, and J.P. Porter Functional role of brain AT1 and AT2 receptors in the central angiotensin II pressor response Brain Res. 603 1993 57 63
90. T.N. Thrasher, and M.J. Fregly Effect of chronic treatment with estrogen-progestin combination on beta adrenergic induced thirst Pharmacol. Biochem. Behav. 8 1978 117 183
91. G.N. Wade, J.D. Blaustein, J.M. Gray, and J.M. Meredith ICI 182,780: a pure antiestrogen that affects behaviors and energy balance in rats without acting in the brain Am. J. Physiol. 265 1993 R1392 R1398
92. P.J. Weatherill, A.P.M. Wilson, R.I. Nicholson, P. Davies, and A.E. Wakeling Interaction of the antioestrogen ICI 164,384 with the oestrogen receptor J. Steroid Biochem. Mol. Biol. 30 1988 263 266
93. M. Wehling Specific, nongenomic actions of steroid hormones Ann. Rev. Physiol. 59 1997 365 393
94. S. Xu, Y. Cheng, J.R. Keast, and P.B. Osborne 17β-estradiol activates estrogen receptor β-signalling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons Endocrinology 149 2008 5540 5548
95. S. Zarate, G. Jaita, J. Ferraris, G. Eijo, M.L. Magri, D. Pisera, and A. Seilicovich Estrogens induce expression of membrane-associated estrogen receptor α isoforms in lactotropes PLoS ONE 7 2012 e41299
96. Y. Zhang, X. Xiao, X.-M. Zhang, Z.-Q. Zhao, and Y.-Q. Zhang Estrogen facilitates spinal cord synaptic transmission via membrane-bound estrogen receptors. Implications for pain hypersensitivity J. Biol. Chem. 287 2012 33268 33281