Cited by 436Estrogen and related hormone effectsNeurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behavior

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Novel Actions of Estrogen Receptor-β on Anxiety-Related Behaviors

Lund, Trent D., Rovis, Tomislav, Chung, Wilson C. J., Handa, Robert J.·2005·Endocrinology

DOI 10.1210/en.2004-1158

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Abstract

Estrogens are reported to have both anxiogenic and anxiolytic properties. This dichotomous neurobiological response to estrogens may be mediated by the existence of two distinct estrogen receptor (ER) systems, ERalpha and ERbeta. In brain, ERalpha plays a critical role in regulating reproductive neuroendocrine function, whereas ERbeta may be more important in regulating nonreproductive functions. To determine whether estrogen's anxiolytic actions could be mediated by ERbeta, we examined anxiety-related behaviors after treatment with ER subtype-selective agonists. Ovariectomized female rats, divided into four treatment groups, were injected with the selective ERbeta agonist diarylpropionitrile (DPN), the ERalpha-selective agonist propyl-pyrazole-triol (PPT), 17beta-estradiol, or vehicle daily for 4d. After injections, behavior was monitored in the elevated plus maze or open field. Rats treated with DPN showed significantly decreased anxiety-related behaviors in both behavioral paradigms. In the elevated plus maze, DPN significantly increased the number of open arm entries and time spent on the open arms of the maze. Furthermore, DPN significantly reduced, whereas PPT increased, anxiogenic behaviors such as the number of fecal boli and time spent grooming. In the open field, DPN-treated females made more rears, interacted more with a novel object, and spent more time in the middle of the open field than did control or PPT-treated rats. To confirm that DPN's anxiolytic actions a…

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17β-Estradiol Is Required for the Sexually Dimorphic Effects of Repeated Binge-Pattern Alcohol Exposure on the HPA Axis during Adolescence
Przybycien–Szymanska, M. M., Gillespie, R. A., & Pak, T. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032263 · Cited by 17
Effects of castration on aggression and levels of serum sex hormones and their central receptors in mandarin voles (Microtus mandarinus)
He, F., Tai, F., Zhang, Y., & Zhang, X. (2012) · Journal of Comparative Physiology A · doi:10.1007/s00359-012-0713-6 · Cited by 17
NO EFFECT OF DIFFERENT ESTROGEN RECEPTOR LIGANDS ON COGNITION IN ADULT FEMALE MONKEYS
Lacreuse, A., Wilson, M., & Herndon, J. (2008) · Physiology and Behavior · doi:10.1016/j.physbeh.2008.11.018 · Cited by 16
No detectable changes in anxiety-related and locomotor behaviors in adult ovariectomized female rats exposed to estradiol, the ERβ agonist DPN or the ERα agonist PPT
Miller, C. K., & Meitzen, J. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105363 · Cited by 15
The neurons expressing calcium-binding proteins in the amygdala of the guinea pig: precisely designed interface for sex hormones
Równiak, M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1432-0 · Cited by 17
“Moreover, selective ERb agonists typically exert potent anxiolytic activity (Lund et al. 2005; Oyola et al. 2012).”
Background
Aromatized testosterone attenuates contextual generalization of fear in male rats
Lynch, J. F., Vanderhoof, T. S., Winiecki, P., Latsko, M. S., Riccio, D. C., & Jasnow, A. M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.06.007 · Cited by 17
“For example, administration of an ERβ, but not ERα, agonist reduces anxiety-like behavior in gonadectomizedmale and female rats asmeasured by the elevated-plus maze and open field (Kudwa et al., 2014; Lund et al., 2005).”
Background
Involvement of Estrogen Receptors in the Anxiolytic-Like Effect of Phytoestrogen Genistein in Rats with 12-Weeks Postovariectomy
Rodríguez-Landa, J., Hernández-López, F., & Saavedra, M. (2012) · doi:10.4236/pp.2012.34059 · Cited by 15
“, 17β-estradiol, diarylpropionitrile, and dihydrocoumes, among others) exert anxiolytic-like effects at the preclinical level [23,24].”
Background
Specific Activation of Estrogen Receptor Alpha and Beta Enhances Male Sexual Behavior and Neuroplasticity in Male Japanese Quail
Seredynski, A. L., Ball, G. F., Balthazart, J., & Charlier, T. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018627 · Cited by 16
Oestrogen Receptor β is Involved in the Actions of Oestrogens in the Brain for Affective Behaviour, but not Trophic Effects in Peripheral Tissues
Walf, A. A. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01945.x · Cited by 15
Selective estrogen receptor‐α but not ‐β agonist treatment modulates brain α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid receptors
Saux, M. L., Estrada-Camarena, E. M., & Paolo, T. D. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.21007 · Cited by 18
“…(DPN) are estrogenic compounds considered as specific agonists for ERa and ERb, respectively, that have been used in in vivo and in vitro studies (Stauffer et al., 2000; Meyers et al., 2001; D’Astous et al., 2004; Le Saux and Di Paolo, 2005; Lund et al., 2005).”
BackgroundMethodInfluential
Sex differences in androgen receptor, estrogen receptor alpha, and c-Fos co-expression with corticotropin releasing factor expressing neurons in restrained adult mice
Rybka, K. A., Lafrican, J. J., Rosinger, Z. J., Ariyibi, D. O., Brooks, M. R., Jacobskind, J. S., & Zuloaga, D. G. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105448 · Cited by 15
Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats
Chowdhury, T. G., Fenton, A. A., & Aoki, C. J. (2020) · Hippocampus · doi:10.1002/hipo.23275 · Cited by 18
Prepubertal Ovariectomy Exaggerates Adult Affective Behaviors and Alters the Hippocampal Transcriptome in a Genetic Rat Model of Depression
Raghavan, N. S., Chen, H., Schipma, M. J., Luo, W., Chung, S., Wang, L., & Redei, E. E. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00373 · Cited by 13
Viral-mediated overexpression of the Myelin Transcription Factor 1 (MyT1) in the dentate gyrus attenuates anxiety- and ethanol-related behaviors in rats
Bahi, A., & Dreyer, J. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4588-7 · Cited by 14
Effects of selective estrogen receptor alpha and beta modulators on prepulse inhibition in male mice
Labouesse, M. A., Langhans, W., & Meyer, U. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3935-9 · Cited by 16
“…their effects on uterine weight and sexual behaviors (Frasor et al. 2003; Harris et al. 2002; Lundholm et al. 2008; Mazzucco et al. 2008), metabolic parameters (Santollo et al. 2007), fear-and anxiety-related behavior (Lund et al. 2005; Lynch et al. 2014), and brain physiology (Waters et al. 2011).”
BackgroundMethod
The aromatase inhibitor 1,4,6-androstatriene-3,17-dione (ATD) reduces disinhibitory behavior in intact adult male rats treated with a high dose of testosterone.
Svensson, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.020 · Cited by 14
Estradiol and orexin-2 saporin actions on multiple forms of behavioral arousal in female mice.
Easton, A., Dwyer, E., & Pfaff, D. W. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.1 · Cited by 27
Participation of estrogen receptors in the antidepressant-like effect of prolame on the forced swimming test.
Lemini, C., Cruz-López, B., & Martínez-Mota, L. (2013) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2012.11.004 · Cited by 14
Sex and interspecies differences in ESR2-expressing cell distributions in mouse and rat brains
Morishita, M., Higo, S., Iwata, K., & Ishii, H. (2023) · Biology of Sex Differences · doi:10.1186/s13293-023-00574-z · Cited by 15
Improvement of depression-like behavior and memory impairment with the ethanol extract of Pleurotus eryngii in ovariectomized rats.
Minami, A., Matsushita, H., Horii, Y., Ieno, D., Matsuda, Y., Saito, M., Kanazawa, H., Ohyama, Y., Wakatsuki, A., Takeda, A., et al. (2013) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b13-00657 · Cited by 13
Estradiol responsiveness of synaptopodin in hippocampal neurons is mediated by estrogen receptor β.
Fester, L., Labitzke, J., Hinz, R., Behem, C., Horling, K., Bernhard, T., Bader, M., Vollmer, G., & Rune, G. (2013) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2013.09.004 · Cited by 13
Influence of ERβ selective agonism during the neonatal period on the sexual differentiation of the rat hypothalamic-pituitary-gonadal (HPG) axis
Patisaul, H. B., Losa-Ward, S. M., Todd, K. L., McCaffrey, K. A., & Mickens, J. A. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-2 · Cited by 13
“They are also well within the range of what other investigators have used to evaluate the functional role of ERb in other estrogen sensitive neuroendocrine pathways in vivo [33-36] and thus below a dose that might generate activity through ERa.”
Influential
Functions of habenula in reproduction and socio-reproductive behaviours
Ogawa, S., & Parhar, I. S. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100964 · Cited by 10
Differential interactions of antiretroviral agents with LXR , ER and GR nuclear receptors: potential contributing factors to adverse events
Svärd, J., Blanco, F., Nevin, D. K., Fayne, D., Mulcahy, F. M., Hennessy, M., & Spiers, P. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12480 · Cited by 11
“Moreover, ERα-selective activation results in anxiogenic responses in female rats, while ERβ-selective activation is anxiolytic (Lund et al., 2005).”
Background
Reproductive Experience Alters Neural and Behavioural Responses to Acute Oestrogen Receptor α Activation
Byrnes, E. M., Casey, K. M., Carini, L. M., & Bridges, R. S. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12113 · Cited by 11
Isolation and Characterization of 13 New Nine-Spined Stickleback, Pungitius pungitius, Microsatellites Located Nearby Candidate Genes for Behavioural Variation
Laine, V., Primmer, C., Herczeg, G., Merilä, J., & Shikano, T. (2012) · doi:10.5735/086.049.0112 · Cited by 12
Complex Roles of Estrogen in Emotion: Sex Matters
Hiroi, R., & Neumaier, J. F. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.017 · Cited by 11
Evaluating the Cognitive Impacts of Drospirenone, a Spironolactone-Derived Progestin, Independently and in Combination With Ethinyl Estradiol in Ovariectomized Adult Rats
Koebele, S. V., Poisson, M., Palmer, J. M., Berns-Leone, C., Northup-Smith, S. N., Pena, V., Strouse, I. M., Bulen, H. L., Patel, S., Croft, C., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.885321 · Cited by 11
“E2 levels are known to impact locomotor and anxiety-like behavior, and thus this finding is concordant with prior research in surgical and transitional menopause models (Blizard et al., 1975; Lund et al., 2005; Hiroi et al., 2006; Hiroi and Neumaier, 2006; McLaughlin et al., 2008; Koebele et al., 2021a).”
Result
Expression of Calbindin, a Marker of Gamma-Aminobutyric Acid Neurons, Is Reduced in the Amygdala of Oestrogen Receptor β-Deficient Female Mice
Kalinowski, D. A., Bogus-Nowakowska, K., Kozłowska, A., & Równiak, M. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11071760 · Cited by 11
“behavioural and neurobiological studies [25,50,51].”
Background
5-HT1A receptors of the prelimbic cortex mediate the hormonal impact on learned fear expression in high-anxious female rats.
Ferreira, R., Brandão, M., & Nobre, M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.05.017 · Cited by 11
“Also, ovarian hormone fluctuations can greatly influence anxiety in humans (Arpels, 1996), as well as the expression of anxietyrelated behavior in rodents (Lund et al., 2005; Mora et al., 1996).”
Background
Maternal exposure to bisphenol S reduces anxiety and impairs collective antipredator behavior of male zebrafish (Danio rerio) offspring through dysregulation of their serotonergic system.
Salahinejad, A., Meuthen, D., Attaran, A., Niyogi, S., Chivers, D., & Ferrari, M. (2023) · Aquatic Toxicology · doi:10.1016/j.aquatox.2023.106800 · Cited by 10
Impact of pubertal onset on region‐specific Esr2 expression
Drzewiecki, C. M., Sellinger, E. P., & Juraska, J. M. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13029 · Cited by 14
Neonatal agonism of ERα masculinizes serotonergic (5-HT) projections to the female rat ventromedial nucleus of the hypothalamus (VMN) but does not impair lordosis
Patisaul, H. B., Adewale, H. B., & Mickens, J. A. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.026 · Cited by 10
Anxiolytic-like effect of hydroalcoholic extract of ripe pistachio hulls in adult female Wistar rats and its possible mechanisms
Rostampour, M., Hadipour, E., Oryan, S., Soltani, B., & Saadat, F. (2016) · Research in Pharmaceutical Sciences · doi:10.4103/1735-5362.194870 · Cited by 9
“Moreover, anxiogenic behaviors including the time spent grooming were decreased by ER β agonist and increased by ER α selective agonist (18,20).”

Authors: Lund, T. D., Rovis, T., Chung, W. C. J., & Handa, R. J.
Affiliations: Colorado State University (US)
Corresponding author: Lund, Trent D.
ORCID: Rovis, Tomislav
Chung, Wilson C. J.
Handa, Robert J.
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2005-02
Volume: 146
Issue: 2
Pages: 797-807
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2004-1158
OpenAlex: W2162934389
Cited by: 436
References: 0
Citations by year: 2026: 5 · 2025: 8 · 2024: 20 · 2023: 13 · 2022: 19 · 2021: 16 · 2020: 14 · 2019: 10 · 2018: 34 · 2017: 17 · 2016: 18 · 2015: 18 · 2014: 20 · 2013: 29 · 2012: 25
FWCI: 11.07
Type: journal article
Language: en
Open access: closed
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS039951)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Keywords: estrogen receptor beta, anxiety-like behavior, diarylpropionitrile, propyl pyrazole triol, estradiol, tamoxifen, elevated plus maze, open field, ovariectomized rats, estrogen receptor alpha
MeSH terms: Animals, Anxiety, Behavior, Animal, Binding, Competitive, Blood-Brain Barrier, Brain, Fear, Female, Male, Nitriles, Phenols, Propionates, Pyrazoles, Receptors, Progesterone, Uterus, Up-Regulation, Rats, Sprague-Dawley, Estrogen Receptor alpha, Estrogen Receptor beta, Rats

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Novel Actions of Estrogen Receptor-β on Anxiety-Related Behaviors

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