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

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

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

Open this paper in CoChat — free account

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…

Integrity signals

Registry

Crossref · 10.1210/en.2004-1158

Cites

0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid
Burton, K. (1956) · Biochemical Journal · doi:10.1042/bj0620315 · Cited by 14,090
Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome
Schmidt, P. J., Nieman, L. K., Danaceau, M. A., Adams, L. F., & Rubinow, D. R. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801223380401 · Cited by 765
Characterization of the Biological Roles of the Estrogen Receptors, ERα and ERβ, in Estrogen Target Tissues in Vivo through the Use of an ERα-Selective Ligand
Harris, H. A., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2002) · Endocrinology · doi:10.1210/en.2002-220403 · Cited by 357
Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors
Handa, R. J., Nunley, K. M., Lorens, S. A., Louie, J. P., McGivern, R. F., & Bollnow, M. R. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90018-3 · Cited by 325
Self-citation
Adrenocortical Function in the Hamster: Sex Differences and Effects of Gonadal Hormones1
GASKIN, J. H., & KITAY, J. I. (1970) · Endocrinology · doi:10.1210/endo-87-4-779 · Cited by 76

Flagged first, then by citations

Show all 0 references

Sorted by citations

Items 101–200 of 368

Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters
Macbeth, A. H., Gautreaux, C., & Luine, V. N. (2008) · Brain Research · doi:10.1016/j.brainres.2008.09.006 · Cited by 71
“…(Walf and Frye, 2007), anxiogenic (Patisaul and Bateman, 2008) or has no effect on anxiety (Luine et al., 2006); the differences may be due to whether estradiol acts on the alpha or beta estrogen receptor (Lund et al., 2005), or dose and timing of administration (seeWalf and Frye, 2006 for review).”
Background
Age, sex, and gonadal hormones differently influence anxiety- and depression-related behavior during puberty in mice
Boivin, J. R., Piekarski, D. J., Wahlberg, J. K., & Wilbrecht, L. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.08.009 · Cited by 73
“…studies in adult female rodents, estradiol, progesterone, and androgens reduce anxiety- and depression-related behavior (Bitran et al., 1995; Frye and Wawrzycki, 2003; HilakiviClarke, 1996; Lund et al., 2005; Martinez-Mota et al., 1999; Mora et al., 1996; Okada et al., 1997; Walf et al., 2009).”
Is HPA axis reactivity in childhood gender-specific? A systematic review
Hollanders, J. J., van der Voorn, B., Rotteveel, J., & Finken, M. J. J. (2017) · Biology of Sex Differences · doi:10.1186/s13293-017-0144-8 · Cited by 80
Photoperiod affects estrogen receptor α, estrogen receptor β and aggressive behavior
Trainor, B., Rowland, M. R., & Nelson, R. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05654.x · Cited by 68
“Several recent studies have demonstrated that ERb activation can reduce anxiety-like behavior in female rats and mice (Imwalle et al., 2005; Lund et al., 2005; Walf & Frye, 2005).”
Background
Estrogen Receptor β, but not α, Mediates Estrogen's Effect on Cocaine-Induced Reinstatement of Extinguished Cocaine-Seeking Behavior in Ovariectomized Female Rats
Larson, E. B., & Carroll, M. E. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301249 · Cited by 71
“…mating and reproduction (Ogawa et al, 1998, 1999; Hewitt and Korach, 2003), anxiety (Krezel et al, 2001; Walf and Frye, 2005; Imwalle et al, 2005; Lund et al, 2005), learning and memory (Fugger et al, 2000; Rissman et al, 2002), wheel running (Ogawa et al, 2003), and food intake (Geary et al,…”
BackgroundMethodInfluential
Estrogen receptor beta activation prevents glucocorticoid receptor-dependent effects of the central nucleus of the amygdala on behavior and neuroendocrine function
Weiser, M. J., Foradori, C. D., & Handa, R. J. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.098 · Cited by 66
“DPN has been shown to pass the blood-brain barrier, and thus likely exerts its effect centrally (Lund et al., 2005).”
BackgroundMethodInfluentialSelf-citation
The anxiolytic effect of testosterone in the rat is mediated via the androgen receptor.
Hodosy, J., Zelmanová, D., Majzúnová, M., Fiľová, B., Malinova, M., Ostatníková, D., & Celec, P. (2012) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2012.04.005 · Cited by 63
Evidence that estrogen directly and indirectly modulates C1 adrenergic bulbospinal neurons in the rostral ventrolateral medulla.
Wang, G., Drake, C., Rozenblit, M., Zhou, P., Alves, S. E., Herrick, S. P., Hayashi, S., Warrier, S., Iadecola, C., & Milner, T. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.089 · Cited by 62
ERβ in CNS: New Roles in Development and Function
Fan, X., Xu, H., Warner, M. N., & Gustafsson, J.-Å. (2010) · Progress in brain research · doi:10.1016/s0079-6123(08)81013-8 · Cited by 65
“Comparison of behavior of ER knockout and WT mice has revealed that intact female ERbKO mice spent less time in the open arms of the elevated plus maze compared to WT and ERaKO mice (Lund et al., 2005).”
Method
Both Estrogen Receptor-α and -β Are Required for Sexual Differentiation of the Anteroventral Periventricular Area in Mice
Bodo, C., Kudwa, A. E., & Rissman, E. F. (2005) · Endocrinology · doi:10.1210/en.2005-0834 · Cited by 78
Sex-dependent programming effects of prenatal glucocorticoid treatment on the developing serotonin system and stress-related behaviors in adulthood
Hiroi, R., Carbone, D. L., Zuloaga, D. G., Bimonte‐Nelson, H. A., & Handa, R. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.055 · Cited by 62
“Estradiol has been shown to decrease anxiety-like and depressive- like behaviors (Frye and Walf, 2004, Hiroi and Neumaier, 2005, Lund et al., 2005).”
BackgroundSelf-citation
Contributions of estrogen receptor-α and estrogen receptor-β to the regulation of behavior
Tetel, M. J., & Pfaff, D. W. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2010.01.008 · Cited by 68
“Anxiogenic behaviors, including the time spent grooming, were decreased by DPN and increased byPPT [28].”
BackgroundMethod
Genetic, epigenetic and environmental impact on sex differences in social behavior
Shepard, K. N., Michopoulos, V., Toufexis, D. J., & Wilson, M. E. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.016 · Cited by 61
Sex-specific Esr2 mRNA expression in the rat hypothalamus and amygdala is altered by neonatal bisphenol A exposure
Cao, J., Joyner, L., Mickens, J. A., Leyrer, S. M., & Patisaul, H. B. (2014) · Reproduction · doi:10.1530/rep-13-0501 · Cited by 61
“Esr2 , particularly in the PVN, is important for modulating affective and mood-related behaviors, including anxiety, aggression, and social interactions (Lund et al .”
Background
Anxiolytic-like effect of phytoestrogen genistein in rats with long-term absence of ovarian hormones in the black and white model
Rodríguez‐Landa, J. F., Hernández-Figueroa, J. D., Hernández-Calderón, B. D. C., & Saavedra, M. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.12.024 · Cited by 57
Ovarian hormones, but not fluoxetine, impart resilience within a chronic unpredictable stress model in middle-aged female rats
Mahmoud, R., Wainwright, S. R., Chaiton, J. A., Lieblich, S. E., & Galea, L. A. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.01.033 · Cited by 63
“This is in concert with the previously established anxiolytic effects of 617 estradiol and estrogen receptor agonists (Lund et al., 2005; Walf and Frye, 2005), and with 618 studies indicating enhanced anxiety-like behavior with longer periods of ovarian hormone 619 depletion (Lagunas et al., 2010b;…”
Result
Estrogen receptor‐β regulates human tryptophan hydroxylase‐2 through an estrogen response element in the 5′ untranslated region
Hiroi, R., & Handa, R. J. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12401 · Cited by 65
“In rats, selective agonists for ERb are anxiolytic- and antidepressant-like, whereas activation of ERa increases anxiety- and depressivelike behaviors (Walf et al. 2004; Lund et al. 2005; Walf and Frye 2005).”
BackgroundSelf-citation
Chronic stress and a cyclic regimen of estradiol administration separately facilitate spatial memory: Relationship with hippocampal CA1 spine density and dendritic complexity.
Conrad, C. D., McLaughlin, K. J., Huynh, T. N., El-Ashmawy, M., & Sparks, M. (2011) · Behavioral Neuroscience · doi:10.1037/a0025770 · Cited by 55
Regulation of Aryl Hydrocarbon Receptor Function by Selective Estrogen Receptor Modulators
DuSell, C. D., Nelson, E. R., Wittmann, B. M., Fretz, J. A., Kazmin, D. A., Thomas, R. S., Pike, J. W., & McDonnell, D. P. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0339 · Cited by 56
Estrogen receptor β deficiency impairs gut microbiota: a possible mechanism of IBD-induced anxiety-like behavior
Ma, Y., Liu, T., Li, X., Kong, A., Xiao, R., Xie, R., Gao, J., Wang, Z., Yun, C., Zou, J., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01356-2 · Cited by 73
Estradiol after Cardiac Arrest and Cardiopulmonary Resuscitation is Neuroprotective and Mediated through Estrogen Receptor-β
Noppens, R. R., Kofler, J., Grafe, M. R., Hurn, P. D., & Traystman, R. J. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.116 · Cited by 51
“Diarylpropionitrile was also found to reduce anxiety in estrogen-deficient female rats (Lund et al, 2005).”
Background
Estrogen Action in Mood and Neurodegenerative Disorders: Estrogenic Compounds with Selective Properties–The Next Generation of Therapeutics
Österlund, M. K., Witt, M., & Gustafsson, J.-Α. (2005) · Endocrine · doi:10.1385/endo:28:3:235 · Cited by 65
Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety-related behavior and corticosterone response to mild stress
Zuloaga, D., Poort, J. E., Jordan, C. L., & Breedlove, S. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.008 · Cited by 56
“Specific activation of sex hormone receptors ERα and ERβ increases and decreases HPA axis activity respectively, while AR activation also appears to decrease HPA activity, although its role is less clear (Handa et al., 1994b; Lund et al., 2004, 2005, 2006).”
Influential
Neuromodulation by soy diets or equol: Anti-depressive & anti-obesity-like influences, age- & hormone-dependent effects
Blake, C., Fabick, K., Setchell, K., Lund, T. D., & Lephart, E. (2011) · BMC Neuroscience · doi:10.1186/1471-2202-12-28 · Cited by 56
“It is noteworthy that ERb-deficient mice express increased anxiety [49] while administration of specific ERb modulators in animal studies decrease anxiety and depression [40,41,50,51].”
BackgroundSelf-citation
Postovariectomy weight gain in female rats is reversed by estrogen receptor α agonist, propylpyrazoletriol
Wegorzewska, I., Walters, K., Weiser, M. J., Cruthirds, D. F., Ewell, E., Larco, D. O., Handa, R. J., & Wu, T. J. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.11.054 · Cited by 57
Self-citation
Suitability of tamoxifen-induced mutagenesis for behavioral phenotyping.
Vogt, M., Chourbaji, S., Brandwein, C., Dormann, C., Sprengel, R., & Gass, P. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2007.12.012 · Cited by 56
Enhanced pelvic responses to stressors in female CRF-overexpressing mice.
Million, M., Wang, L.-X., Stenzel-Poore, M., Coste, S., Yuan, P.-Q., Lamy, C., Rivier, J., Buffington, T., & Taché, Y. (2007) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00626.2006 · Cited by 56
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54
Activation of the G-protein-coupled receptor GPR30 induces anxiogenic effects in mice, similar to oestradiol
Kastenberger, I., Lutsch, C., & Schwarzer, C. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2599-3 · Cited by 54
“1 to 1 μM and therefore are on the lower end of the scale of doses used for in vivo testing (Lund et al. 2005; Rocha et al. 2005; Kocic et al. 2010; Intapad et al. 2011).”
BackgroundMethodInfluential
Distribution and chemical composition of estrogen receptor β neurons in the paraventricular nucleus of the female and male mouse hypothalamus
Oyola, M. G., Thompson, M. K., Handa, A. Z., & Handa, R. J. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24295 · Cited by 53
“For example, Lund et al. (2005) studied the activation of the HPA axis in ovariectomized rats using selective ERa and ERb agonists.”
BackgroundInfluentialSelf-citation
Neuropsychiatric effects of tamoxifen: Challenges and opportunities
Novick, A. M., Scott, A. T., Epperson, C. N., & Schneck, C. D. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100869 · Cited by 61
New knockout model confirms a role for androgen receptors in regulating anxiety-like behaviors and HPA response in mice
Chen, C. V., Brummet, J. L., Lonstein, J. S., Jordan, C. L., & Breedlove, S. M. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.01.001 · Cited by 57
Rapid Oestrogenic Regulation of Social and Nonsocial Learning
Ervin, K., Phan, A., Gabor, C. S., & Choleris, E. (2013) · Journal of neuroendocrinology · doi:10.1111/jne.12079 · Cited by 53
Intrahypothalamic estradiol modulates hypothalamus-pituitary-adrenal-axis activity in female rats.
Liu, J., Bisschop, P., Eggels, L., Foppen, E., Fliers, E., Zhou, J.-N., & Kalsbeek, A. (2012) · Endocrinology · doi:10.1210/en.2011-2176 · Cited by 53
Pharmacological enhancement of fear reduction: preclinical models
Graham, B. M., Langton, J. M., & Richardson, R. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01175.x · Cited by 57
“The female sex hormone estrogen plays a key role in modulating state levels of anxiety (Lund et al., 2005), and has been shown to be involved in regulating the function and morphology of the neural circuitry underlying extinction learning (Goldstein et al., 2001; Shansky et al., 2010).”
Background
Estrogen receptors beta and alpha have specific pro- and anti-nociceptive actions.
Coulombe, M., Spooner, M., Gaumond, I., Carrier, J. C., & Marchand, S. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.02.057 · Cited by 53
Sex Steroid Hormone Gene Polymorphisms and Depressive Symptoms in Women at Midlife
Kravitz, H. M., Janssen, İ., Lotrich, F. E., Kado, D. M., & Bromberger, J. T. (2006) · The American Journal of Medicine · doi:10.1016/j.amjmed.2006.07.010 · Cited by 78
A Role for the Androgen Metabolite, 5alpha Androstane 3beta, 17beta Diol (3?-Diol) in the Regulation of the Hypothalamo-Pituitary?Adrenal Axis
Handa, R. J., Sharma, D., & Uht, R. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00065 · Cited by 55
“Unknown at present are the mechanisms by which the HPA axis distinguishes enhancing from inhibiting actions of estradiol, a hormone that binds with similar high affinity to both ERalpha and ERbeta (Kuiper et al., 1997; Lund et al., 2005).”
BackgroundSelf-citation
Modulation of responses to stress by estradiol benzoate and selective estrogen receptor agonists
Serova, L. I., Harris, H. A., Maharjan, S., & Sabban, E. L. (2010) · Journal of Endocrinology · doi:10.1677/joe-10-0029 · Cited by 57
“A similar dose of WAY-200070 or DPN was found to significantly decrease anxiety-related behavior (Lund et al. 2005, Weiser et al. 2009).”
History of Estrogen: Its Purification, Structure, Synthesis, Biologic Actions, and Clinical Implications
Santen, R. J., & Simpson, E. R. (2018) · Endocrinology · doi:10.1210/en.2018-00529 · Cited by 64
Activation of the G-protein coupled receptor 30 (GPR30) has different effects on anxiety in male and female mice.
Hart, D., Nilges, M., Pollard, K., Lynn, T., Patsos, O. P., Shiel, C., Clark, S., & Vasudevan, N. (2014) · Steroids · doi:10.1016/j.steroids.2013.11.004 · Cited by 51
Anxiety-like behaviors and expression of SERT and TPH in the dorsal raphé of estrogen- and fluoxetine-treated ovariectomized rats.
Charoenphandhu, J., Teerapornpuntakit, J., Nuntapornsak, A., Krishnamra, N., & Charoenphandhu, N. (2011) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2011.02.023 · Cited by 51
Tryptophan and Its Metabolite Serotonin Impact Metabolic and Mental Disorders via the Brain–Gut–Microbiome Axis: A Focus on Sex Differences
Xu, M., Zhou, E. Y., & Shi, H. (2025) · Cells · doi:10.3390/cells14050384 · Cited by 58
Chronic exposure to bisphenol S induces oxidative stress, abnormal anxiety, and fear responses in adult zebrafish (Danio rerio)
Salahinejad, A., Attaran, A., Naderi, M., Meuthen, D., Niyogi, S., & Chivers, D. P. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.141633 · Cited by 57
Benefits of Hormone Therapy Estrogens Depend on Estrogen Type: 17β-Estradiol and Conjugated Equine Estrogens Have Differential Effects on Cognitive, Anxiety-Like, and Depressive-Like Behaviors and Increase Tryptophan Hydroxylase-2 mRNA Levels in Dorsal Raphe Nucleus Subregions
Hiroi, R., Weyrich, G., Koebele, S. V., Mennenga, S., Talboom, J., Hewitt, L. T., Lavery, C. N., Mendoza, P., Jordan, A., & Bimonte-Nelson, H. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00517 · Cited by 50
“In the rodent, E2 also has been shown to decrease anxiety-like behaviors, as measured by increased center time in the open field test (OFT; Lund et al., 2005; Hiroi et al., 2006; Hiroi and Neumaier, 2006) and increased open arm time in the elevated plus maze (EPM; Nomikos and Spyraki, 1988; Lund et…”
Background
ESR1 and ESR2 Differentially Regulate Daily and Circadian Activity Rhythms in Female Mice
Royston, S. E., Yasui, N., Kondilis, A., Lord, S., Katzenellenbogen, J. A., & Mahoney, M. M. (2014) · Endocrinology · doi:10.1210/en.2014-1101 · Cited by 55
Reduction of dendritic spines and elevation of GABAergic signaling in the brains of mice treated with an estrogen receptor β ligand
Tan, X.-J., Dai, Y.-B., Wu, W., Kim, H.-J., Barros, R., Richardson, T. I., Yaden, B., Warner, M., McKinzie, D., Krishnan, V., et al. (2012) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1121162109 · Cited by 50
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
Hiroi, R., & Neumaier, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.016 · Cited by 50
“…bimodal effect of serotonergic activity in distinct subregions on anxiety may be expected as estrogen, like 5-HT, has been shown to be anxiolytic or anxiogenic, partly depending on the relative actions of estrogen on two estrogen receptor types, ERα and ERβ (Lund et al., 2005, Walf and Frye, 2005).”
Background
Estradiol-17β-Induced Human Neural Progenitor Cell Proliferation Is Mediated by an Estrogen Receptor β-Phosphorylated Extracellularly Regulated Kinase Pathway
Wang, J. M., Liu, L., & Brinton, R. D. (2007) · Endocrinology · doi:10.1210/en.2007-1155 · Cited by 52
Estrogen Receptor β Activation Is Antinociceptive in a Model of Visceral Pain in the Rat
Cao, D., Ji, Y., Tang, B., & Traub, R. J. (2012) · Journal of Pain · doi:10.1016/j.jpain.2012.04.010 · Cited by 47
Conceptualizing the role of estrogens and serotonin in the development and maintenance of bulimia nervosa
Hildebrandt, T., Alfano, L., Tricamo, M., & Pfaff, D. W. (2010) · Clinical Psychology Review · doi:10.1016/j.cpr.2010.04.011 · Cited by 54
Effects of estrogens on sex differentiation in Japanese quail and chicken.
Brunström, B., Axelsson, J., Mattsson, A., & Halldin, K. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.01.006 · Cited by 48
The Androgen Metabolite, 5α-Androstane-3β,17β-Diol (3β-Diol), Activates the Oxytocin Promoter Through an Estrogen Receptor-β Pathway
Hiroi, R., Lacagnina, A. F., Hinds, L. R., Carbone, D. G., Uht, R. M., & Handa, R. J. (2013) · Endocrinology · doi:10.1210/en.2012-2253 · Cited by 48
Self-citation
Comparison of the Adulthood Chronic Stress Effect on Hippocampal BDNF Signaling in Male and Female Rats
Niknazar, S., Nahavandi, A., Peyvandi, A. A., Peyvandi, H., Akhtari, A. S., & Karimi, M. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9345-5 · Cited by 42
Review: neuroestrogen regulation of socio-sexual behavior of males
Ubuka, T., & Tsutsui, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00323 · Cited by 45
Gonadal hormones modulate the HPA‐axis and the SNS in response to psychosocial stress
Barel, E., Abu‐Shkara, R., Colodner, R., Masalha, R., Mahagna, L., Zemel, O. C., & Cohen, A. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24259 · Cited by 45
Cyclic estradiol replacement attenuates stress-induced c-Fos expression in the PVN of ovariectomized rats.
Gerrits, M., Grootkarijn, A., Bekkering, B. F., Bruinsma, M., den Boer, J. D., & ter Horst, G. T. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.06.021 · Cited by 44
“The anxiolytic effects of estradiol are specifically attributed to estrogen receptor β (ERβ) (Walf et al., 2004; Lund et al., 2005).”
BackgroundResult
Is basic research providing answers if adjuvant anti-estrogen treatment of breast cancer can induce cognitive impairment?
Buwalda, B., & Schagen, S. B. (2013) · Life Sciences · doi:10.1016/j.lfs.2012.12.012 · Cited by 43
A Dominant Negative ERβ Splice Variant Determines the Effectiveness of Early or Late Estrogen Therapy after Ovariectomy in Rats
Wang, J. M., Hou, X., Adeosun, S. O., Hill, R., Henry, S., Paul, I. A., Irwin, R. W., Ou, X., Bigler, S. A., Stockmeier, C. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033493 · Cited by 36
Cardiovascular Implications of Immune Disorders in Women
Moran, C. A., Collins, L. F., Beydoun, N., Mehta, P. K., Fatade, Y., Isiadinso, I., Lewis, T. T., Weber, B., Goldstein, J. M., Ofotokun, I., et al. (2022) · Circulation Research · doi:10.1161/circresaha.121.319877 · Cited by 57
A Concerted Action Of Estradiol And Insulin Like Growth Factor I Underlies Sex Differences In Mood Regulation By Exercise
Munive, V., Santi, A., & Torres‐Alemán, I. (2016) · Scientific Reports · doi:10.1038/srep25969 · Cited by 44
Estrogen receptor gene variants are associated with anxiety disorders in older women.
Ryan, J., Scali, J., Carrière, I., Scarabin, P., Ritchie, K., & Ancelin, M. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.04.011 · Cited by 42
“…studies using ER subtype-specific compounds or animals deficient in one of the receptors suggest that ESR2 plays an important role in mediating estrogen’s anxiolytic effects, and ESR1 may actually mediate estrogen’s anxiogenic actions (Lund et al., 2005; Walf and Frye, 2006; Weiser et al., 2008).”
Background
Effects of chronic exposure to bisphenol-S on social behaviors in adult zebrafish: Disruption of the neuropeptide signaling pathways in the brain
Salahinejad, A., Naderi, M., Attaran, A., Meuthen, D., Niyogi, S., & Chivers, D. P. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.113992 · Cited by 50
Activation of GPR30 attenuates chronic pain-related anxiety in ovariectomized mice
Liu, S., Tian, Z., Guo, Y., Zhang, N., Feng, B., & Zhao, M. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.12.021 · Cited by 45
Modification of female and male social behaviors in estrogen receptor beta knockout mice by neonatal maternal separation
Tsuda, M. C., Yamaguchi, N., Nakata, M., & Ogawa, S. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00274 · Cited by 37
“However, behavioral phenotypes of βERKO mice were overturned by MS stress in exception to nonsocial anxiety. βERKO mice could be more sensitive to the stressful effects of MS because ERβ also functions to attenuate HPA reactivity to stress (Lund et al., 2005, 2006).”
Background
Estrogen receptor (ER) subtype agonists alter monoamine levels in the female rat brain
Lubbers, L. S., Zafian, P., Gautreaux, C., Gordon, M., Alves, S. E., Correa, L. D., Lorrain, D. S., Hickey, G. J., & Luine, V. N. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.08.005 · Cited by 40
Estrogen Receptor (ER) β Modulates ERα Responses to Estrogens in the Developing Rat Ventromedial Nucleus of the Hypothalamus
Gonzales, K. L., Tetel, M. J., & Wagner, C. K. (2008) · Endocrinology · doi:10.1210/en.2008-0511 · Cited by 42
Early developmental exposure to bisphenol A and bisphenol S disrupts socio-cognitive function, isotocin equilibrium, and excitation-inhibition balance in developing zebrafish
Naderi, M., Puar, P., JavadiEsfahani, R., & Kwong, R. W. M. (2021) · NeuroToxicology · doi:10.1016/j.neuro.2021.11.009 · Cited by 49
Effects of Puerarin on the Ovariectomy-Induced Depressive-Like Behavior in ICR Mice and Its Possible Mechanism of Action
Tantipongpiradet, A., Monthakantirat, O., Vipatpakpaiboon, O., Khampukdee, C., Umehara, K., Noguchi, H., Fujiwara, H., Matsumoto, K., Sekeroglu, N., Kijjoa, A., et al. (2019) · Molecules · doi:10.3390/molecules24244569 · Cited by 39
Beyond the HPA-axis: The role of the gonadal steroid hormone receptors in modulating stress-related responses in an animal model of PTSD
Fenchel, D., Levkovitz, Y., Vainer, E., Kaplan, Z., Zohar, J., & Cohen, H. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.02.004 · Cited by 42
Activation of ERβ modulates fear generalization through an effect on memory retrieval.
Lynch, J., Dejanovic, D., Winiecki, P., Mulvany, J., Ortiz, S., Riccio, D., & Jasnow, A. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.06.017 · Cited by 39
“…al., 2004; Rhodes and Frye, 2006), ERβ activation underlies estradiolmediated effects on spatial learning and anxiety (Bodo and Rissman, 2006; Lephart et al., 2002; Lund et al., 2005;Walf et al., 2004), whereas both receptors are thought to play a role in emotional memory (Rhodes and Frye, 2006).”
Background
Systemic administration of diarylpropionitrile (DPN) or phytoestrogens does not affect anxiety-related behaviors in gonadally intact male rats
Patisaul, H. B., Burke, K. T., Hinkle, R. E., Adewale, H. B., & Shea, D. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.11.004 · Cited by 38
“Next, we compared the effect of DPN (1mg/kg) with the ERα agonist PPT (1mg/ kg) and two phytoestrogens on anxiety related behavior and plasma androgen levels in gonadally intact male rats.”
Influential
Estrogen receptors α and β in the central amygdala and the ventromedial nucleus of the hypothalamus: Sociosexual behaviors, fear and arousal in female rats during emotionally challenging events
Moëne, O. L., Stavarache, M. A., Ogawa, S., Musatov, S. A., & Ågmo, A. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.045 · Cited by 42
Effects of lorazepam and WAY-200070 in larval zebrafish light/dark choice test
Chen, F., Chen, S., Liu, S., Zhang, C., & Peng, G. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.03.022 · Cited by 43
Impact of estrogen receptor alpha and beta agonists on delayed alternation in middle-aged rats
Neese, S. L., Korol, D. L., Katzenellenbogen, J. A., & Schantz, S. L. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.08.017 · Cited by 37
“…been shown to improve performance on a reference memory version of the water maze task, and also to reduce anxiety and fear behaviors in a variety of other tasks in rats (Lund et al., 2005; Rhodes and Frye, 2006; Weiser et al., 2009), suggesting that ERβ activation is critical for these effects.”
Influential
Oestrogen Receptor β Contributes to the Transient Sex Difference in Tyrosine Hydroxylase Expression in the Mouse Locus Coeruleus
Pendergast, J. S., Tuesta, L. M., & Bethea, J. R. (2008) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.2008.01776.x · Cited by 38
Effect of daidzein on anxiety, social behavior and spatial learning in male Balb/cJ mice.
Zeng, S., Tai, F.-D., Zhai, P.-Y., Yuan, A., Jia, R., & Zhang, X. (2010) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2010.03.015 · Cited by 37
Estradiol and the control of feeding behavior
Rivera, H. M., & Stincic, T. L. (2017) · Steroids · doi:10.1016/j.steroids.2017.11.011 · Cited by 46
Effects of Long-Term Treatment with Estradiol and Estrogen Receptor Subtype Agonists on Serotonergic Function in Ovariectomized Rats
Benmansour, S., Adeniji, O. S., Privratsky, A. A., & Frazer, A. (2015) · Neuroendocrinology · doi:10.1159/000437268 · Cited by 36
Estradiol-Induced Conditioned Place Preference may Require Actions at Estrogen Receptors in the Nucleus Accumbens
Walf, A., Rhodes, M. E., Meade, J. R., Harney, J., & Frye, C. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301124 · Cited by 35
“S.c. administration of ERb, but not ERa, SERMs decrease anxiety and depressive behavior of OVX rats (Lund et al, 2005; Walf and Frye, 2005b; Walf et al, 2004).”
Background
Enteric Microbiota–Gut–Brain Axis from the Perspective of Nuclear Receptors
Duszka, K., & Wahli, W. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082210 · Cited by 37
“In contrast, treatment with the ERα agonist propylpyrazoletriol (PPT) was anxiogenic in the elevated plus maze test and, in a consistent manner, stimulated corticosterone stress hormone response [590,593].”
Background
Long-term alteration of anxiolytic effects of ovarian hormones in female mice by a peripubertal immune challenge
Olesen, K. M., Ismail, N., Merchasin, E. D., & Blaustein, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.06.005 · Cited by 34
Underlying mechanisms mediating the antidepressant effects of estrogens
Österlund, M. K. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.11.001 · Cited by 92
The special extract ERr 731 of the roots of Rheum rhaponticum decreases anxiety and improves health state and general well-being in perimenopausal women
Kaszkin-Bettag, M., Ventskovskiy, B. M., Kravchenko, A., Rettenberger, R., Richardson, A., Heger, P., & Heger, M. (2007) · Menopause · doi:10.1097/01.gme.0000251932.48426.35 · Cited by 34
Neurologic links between epilepsy and depression in women
Hajszán, T., & MacLusky, N. J. (2006) · Neurology · doi:10.1212/wnl.66.66_suppl_3.s13 · Cited by 35
Inhibition of neointima formation by local delivery of estrogen receptor alpha and beta specific agonists.
Krom, Y., Pires, N. M. M., Jukema, J., de Vries, M. D., Frants, R., Havekes, L., van Dijk, K. V., & Quax, P. (2007) · Cardiovascular Research · doi:10.1016/j.cardiores.2006.10.024 · Cited by 34
“For example, systemic administration of the relatively high dose of 1 mg/kg/day DPN to rats does not alter uterine weight, which is regarded as a true ERα target tissue [34].”
Background
Neonatal testosterone partially organizes sex differences in stress-induced emotionality in mice
Seney, M. L., Walsh, C., Stolakis, R., & Sibille, E. L. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.02.014 · Cited by 34
“For instance, treatment of GDX female rats with an ERα-specific agonist increases anxiety-like behavior, while treatment with an ERβ-specific agonist decreases anxiety-like behavior (Lund et al., 2005).”
The Organizational Role of Testicular Hormones and the Androgen Receptor in Anxiety-Related Behaviors and Sensorimotor Gating in Rats
Zuloaga, D. G., Jordan, C. L., & Breedlove, S. M. (2011) · Endocrinology · doi:10.1210/en.2010-1016 · Cited by 33
Estrogen receptor beta agonist diarylpropiolnitrile (DPN) does not mediate neuroprotection in a rat model of permanent focal ischemia.
Farr, T. D., Carswell, H., Gsell, W., & Macrae, I. M. (2007) · Brain Research · doi:10.1016/j.brainres.2007.09.009 · Cited by 33
Bisphenol A exposure remodels cognition of male rats attributable to excitatory alterations in the hippocampus and visual cortex
Chen, Z., Li, T., Zhang, L., Wang, H., & Hu, F. (2018) · Toxicology · doi:10.1016/j.tox.2018.10.002 · Cited by 34
Estradiol-mediated protection against high-fat diet induced anxiety and obesity is associated with changes in the gut microbiota in female mice
Acharya, K. D., Graham, M. E., Raman, H. N., Parakoyi, A. E. R., Corcoran, A., Belete, M. K., Ramaswamy, B., Koul, S., Sachar, I., Derendorf, K., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-31783-6 · Cited by 35
Estrogen Receptor-Selective Agonists Modulate Learning in Female Rats in a Dose- and Task-Specific Manner
Pisani, S. L., Neese, S. L., Katzenellenbogen, J. A., Schantz, S. L., & Korol, D. L. (2015) · Endocrinology · doi:10.1210/en.2015-1616 · Cited by 31
Progestin receptor expression in the developing rat brain depends upon activation of estrogen receptor α and not estrogen receptor β
Chung, W. C. J., Pak, T. R., Weiser, M. J., Hinds, L. R., Andersen, M. E., & Handa, R. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.01.109 · Cited by 29
Self-citation
Oxytocin and Steroid Actions
Jirikowski, G. F., Ochs, S. D., & Caldwell, J. D. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_9 · Cited by 32
The sex-dependent response to psychosocial stress and ischaemic heart disease
Helman, T. J., Headrick, J. P., Stapelberg, N. J. C., & Braidy, N. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1072042 · Cited by 36
Reproductive experience modifies the effects of estrogen receptor alpha activity on anxiety-like behavior and corticotropin releasing hormone mRNA expression
Byrnes, E. M., Casey, K. M., & Bridges, R. S. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.001 · Cited by 28
“Several studies suggest differential roles for the two ER subtypes (ERα and ERβ) in the modulation of anxiety-like behavior (Imwalle et al., 2002; Lund et al., 2005; Weiser et al., 2009).”
BackgroundMethodResultInfluential
Estradiol-induced desensitization of 5-HT1A receptor signaling in the paraventricular nucleus of the hypothalamus is independent of estrogen receptor-beta
Rossi, D. V., Dai, Y., Thomas, P., Carrasco, G. A., Doncarlos, L., Muma, N., & Li, Q. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.003 · Cited by 29
“…experiments is comparable to an effective dose used by other investigators in female rats to activate ERβ as demonstrated by decreases in anxiety behaviors, regulation of dopamine-2 receptors, and increases in cell proliferation (Le Saux et al., 2006; Lund et al., 2005; Mazzucco et al., 2006).”
Effects of estrogens and progesterone on the synaptic organization of the hypothalamic ventromedial nucleus
Sá, S. I., Lukoyanova, E. A., & Madeira, M. D. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.066 · Cited by 32
Preclinical Characterization of Selective Estrogen Receptor β Agonists: New Insights into Their Therapeutic Potential
Harris, H. A. (2007) · Ernst Schering Research Foundation workshop/Ernst Schering Foundation Symposium proceedings · doi:10.1007/2789_2006_021 · Cited by 27
Functional hypothalamic amenorrhea: Impact on bone and neuropsychiatric outcomes
Pedreira, C. C., Maya, J., & Misra, M. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.953180 · Cited by 37
“Adequate estrogen status is essential for optimal cognitive function and may also impact mood and emotion (141, 142).”
Background

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Metadata

Record

About these checks