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Novel Actions of Estrogen Receptor-β on Anxiety-Related Behaviors
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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“Although the functional role of limbic ERβ remains ambiguous, ERβ in the PVN and associated structures, including the BnST, plays a fundamental role in mediating motivational and anxiety-related behaviors (134–136).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [134]
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Cites
Burton, K. (1956) · Biochemical Journal · doi:10.1042/bj0620315 · Cited by 14,090
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
Harris, H. A., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2002) · Endocrinology · doi:10.1210/en.2002-220403 · Cited by 357
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-citationAdrenocortical 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
Cited by
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The pros and cons of phytoestrogens
Patisaul, H. B., & Jefferson, W. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.03.003 · Cited by 746
Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., & Champagne, F. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214056110 · Cited by 490
Walf, A. A., & Frye, C. A. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301067 · Cited by 477
“We and others have shown that administration of 17b-E 2 (which has high affinity for both ERa and ERb), compared to vehicle or ERa-specific SERMs, similarly increases antianxiety and antidepressant-like effects in several tasks as do SERMs with greater specificity for ERb than ERa (Lund et al, 2005; Walf et al, 2004;…”
BackgroundInfluentialHeck, A., & Handa, R. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0167-9 · Cited by 567
Self-citationSheng, J. A., Bales, N. J., Myers, S. A., Bautista, A. I., Roueinfar, M., Hale, T. M., & Handa, R. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.601939 · Cited by 418
Self-citationEstrous cycle phase and gonadal hormones influence conditioned fear extinction
Milad, M. R., Igoe, S. A., Lebron-Milad, K., & Novales, J. E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.011 · Cited by 417
“We speculate that the facilitative ffects of estrogen on fear extinction are mediated by the strogen receptor beta (ER-beta), as several studies have hown that the anxiolytic effects of estrogen are mediated y the ER-beta (Toufexis et al., 2007; Lund et al., 2005; omihara et al., 2009).”
BackgroundGonadal steroid hormones and the hypothalamo–pituitary–adrenal axis
Handa, R. J., & Weiser, M. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.11.001 · Cited by 408
“The ERβ agonist, WAY200070 has also been shown to have anti-depressant actions in the tail suspension test in male mice (Hughes et al., 2008).”
BackgroundInfluentialSelf-citationAcetylcholine–Dopamine Interactions in the Pathophysiology and Treatment of CNS Disorders
Lester, D. B., Rogers, T. D., & Blaha, C. D. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00142.x · Cited by 267
Hormonal Cycle Modulates Arousal Circuitry in Women Using Functional Magnetic Resonance Imaging
Goldstein, J. M., Jerram, M., Poldrack, R., Ahern, T., Kennedy, D. N., Seidman, L. J., & Makris, N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2239-05.2005 · Cited by 368
“…of ER␣, ER has shown nonexcitatory effects, thus suggesting that, through these receptors, estrogen may modulate autonomic and mood-related functions in relation to corticotropin-releasing factor (CRF) and norepinephrine (NE) release (Ostlund et al., 2003; Bao et al., 2005; Lund et al., 2005).”
Sex Differences in Stress Response Circuitry Activation Dependent on Female Hormonal Cycle
Goldstein, J. M., Jerram, M. W., Abbs, B., Whitfield, S., & Makris, N. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3021-09.2010 · Cited by 376
“…2001; Lund et al., 2005), this does not negate an inhibitory role for estradiol, which has been associated with estrogen receptor (Ostlund et al., 2003; Shansky et al., 2004; Bao et al., 2005; Lund et al., 2005) while the excitatory role may be associated with estrogen receptor (Lund et al., 2006).”
BackgroundInfluentialThe influence of gonadal hormones on conditioned fear extinction in healthy humans
Milad, M. R., Zeidan, M. A., Contero, A., Pitman, R. K., Klibanski, A., Rauch, S. L., & Goldstein, J. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.030 · Cited by 320
Estrogen Receptor-β: Recent Lessons from in Vivo Studies
Harris, H. A. (2006) · Molecular Endocrinology · doi:10.1210/me.2005-0459 · Cited by 284
“(70) showed that all rats tested in the elevated plus maze had increased levels of corticosterone, but the levels seen in the DPN-treated animals were significantly lower than those treated with estradiol or PPT (which were significantly higher than vehicle-treated rats in contrast to the findings of Ref.”
Blockade of Estrogen by Hormonal Contraceptives Impairs Fear Extinction in Female Rats and Women
Graham, B. M., & Milad, M. R. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.018 · Cited by 281
Sex differences in psychopathology: of gonads, adrenals and mental illness
Solomon, M. B., & Herman, J. P. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.033 · Cited by 272
The endocrine manifestations of anorexia nervosa: mechanisms and management
Haines, M. S., & Miller, K. K. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.175 · Cited by 342
Weiser, M. J., & Handa, R. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.12.058 · Cited by 250
“Animals where both pellets were >0.5 mm away from the PVN were excluded based on previous studies using the same pellet hormone concentration and resulting spread (~0.5 mm for estradiol) (Lund et al., 2005).”
InfluentialSelf-citationTests of unconditioned anxiety — Pitfalls and disappointments
Ennaceur, A. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.05.032 · Cited by 280
Estrogen receptor beta in the brain: From form to function
Weiser, M. J., Foradori, C. D., & Handa, R. J. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.013 · Cited by 250
“Furthermore, treatment of gonadectomized male rats with estrogen increases stress-induced c-fos mRNA, CRH hnRNA, AVP hnRNA, and CORT, whereas DHT treatment inhibits the response when compared to control animals (Lund et al., 2004b).”
BackgroundMethodInfluentialSelf-citationWalf, A. A., & Frye, C. A. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300713 · Cited by 229
“…of anxiety behavior (Frye et al, 2000; Frye and Walf, 2002, 2005; Shughrue et al, 1997), and recent findings which suggests that ERb-selective SERMs are more effective than ERa-selective SERMs or vehicle to modulate affective behavior of ovx female rats (Lund et al, 2005; Walf et al, 2004).”
BackgroundMethodLund, T. D., Hinds, L. R., & Handa, R. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3777-05.2006 · Cited by 236
Self-citationZuloaga, D. G., Puts, D. A., Jordan, C. L., & Breedlove, S. M. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.013 · Cited by 236
“…also play a role in the display of anxietyrelated behavior in rodents as assessed by open field testing, exposure to a novel object, the elevated plus maze task, and light dark box (Edinger and Frye, 2004; Walf and Frye, 2005; Lund et al., 2005; Bridges and Starkey, 2004; Frye and Lacey, 2001).”
BackgroundInfluentialFear conditioning and extinction: Influence of sex and menstrual cycle in healthy humans.
Milad, M. R., Goldstein, J. M., Orr, S. P., Wedig, M. M., Klibanski, A., Pitman, R. K., & Rauch, S. L. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.5.1196 · Cited by 212
Effects of Estradiol Withdrawal on Mood in Women With Past Perimenopausal Depression
Schmidt, P. J., Dor, R. R. B., Martinez, P. E., Guerrieri, G. M., Harsh, V., Thompson, K., Koziol, D. E., Nieman, L. K., & Rubinow, D. R. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.0111 · Cited by 265
Handa, R. J., Pak, T. R., Kudwa, A. E., Lund, T. D., & Hinds, L. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.012 · Cited by 205
“Previous studies have shown that ERbeta agonists such as DPN can prevent anxiety related behaviors in female and male rats (Lund et al., 2005).”
BackgroundSelf-citationEstrogen modulates sexually dimorphic contextual fear extinction in rats through estrogen receptor β
Chang, Y., Yang, C., Liang, Y., Yeh, C.-M., Huang, C., & Hsu, K. (2009) · Hippocampus · doi:10.1002/hipo.20581 · Cited by 203
“vated plus maze and open field test (Lund et al., 2005).”
Emotion recognition accuracy in healthy young females is associated with cycle phase
Derntl, B., Kryspin‐Exner, I., Fernbach, E., Moser, E., & Habel, U. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.09.006 · Cited by 202
Donner, N. C., & Handa, R. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.046 · Cited by 202
“…the number of closed and open arm entries (locomotor activity), the time spent grooming, and the number of fecal boli were recorded as described in Lund et al. (2005) To measure despair-like behavior, rats were tested in the FST (Porsolt et al., 2001) for 5 min on day 7, using 25 °C tap water.”
InfluentialSelf-citationAntenatal prediction of postpartum depression with blood DNA methylation biomarkers
Guintivano, J., Arad, M., Gould, T. D., Payne, J. L., & Kaminsky, Z. A. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.62 · Cited by 188
Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice
Ryan, B. C., & Vandenbergh, J. G. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.01.007 · Cited by 180
Roles of estrogen receptors α and β in differentiation of mouse sexual behavior
Kudwa, A. E., Michopoulos, V., Gatewood, J. D., & Rissman, E. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.018 · Cited by 196
Adewale, H. B., & Patisaul, H. B. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2008.06.008 · Cited by 163
“…and reproductive function (Hewitt and Korach, 2003; Ogawa et al., 1998; Rissman et al., 1999), while ERb plays a more significant role in the modulation of estrogen action on anxiety and stress (Lund et al., 2005) although by no means do they do so exclusively of the other (Choleris et al., 2006).”
BackgroundResultSex Hormones and Mood in the Perimenopause
Schmidt, P. J., & Rubinow, D. R. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04982.x · Cited by 175
Walf, A. A., & Frye, C. A. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.003 · Cited by 175
Hiroi, R., McDevitt, R. A., & Neumaier, J. F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.019 · Cited by 161
Estrogenic encounters: How interactions between aromatase and the environment modulate aggression
Trainor, B. C., Kyomen, H. H., & Marler, C. A. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.11.001 · Cited by 147
Jacome, L. F., Gautreaux, C., Inagaki, T., Mohan, G., Alves, S. E., Lubbers, L. S., & Luine, V. N. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.016 · Cited by 160
“Although the current experiments did not verify that the ER selective agonists occupied the ERs in the brain, studies indicate that PPT and DPN can penetrate the blood brain barrier and alter ER-dependent pathways (Harris et al., 2002; Lund et al., 2005).”
BackgroundMethodInfluentialWalf, A., Koonce, C. J., Manley, K., & Frye, C. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.016 · Cited by 153
“These results are supported by previous findings that show that subcutaneous administration of E2 or an ERβ agonist reduces plasma corticosterone levels of rats [30] or WT, but not βERKO, mice [47].”
ResultPatisaul, H. B., & Adewale, H. B. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.008 · Cited by 146
“Agonism of ERβ has been shown in a pair of studies to reduce anxiety in adult gonadectomized male and female rats (Lund et al., 2005; Walf et al., 2004), while mice lacking ERβ (ERβKO mice) have been observed to be more aggressive towards conspecifics (Nomura et al., 2002; Ogawa et al., 1999).”
Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice
Gracia-Rubio, I., Moscoso-Castro, M., Pozo, O. J., Marcos, J., Nadal, R., & Valverde, O. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.09.003 · Cited by 144
Heitkemper, M. M., & Chang, L. (2009) · Gender Medicine · doi:10.1016/j.genm.2009.03.004 · Cited by 161
Estrogen Receptors Modulation of Anxiety-Like Behavior
Borrow, A. P., & Handa, R. J. (2017) · Vitamins and Hormones · doi:10.1016/bs.vh.2016.08.004 · Cited by 146
“…and mice in a number of tests, including the open field test (Lund et al., 2005; Oyola et al., 2012; Walf et al., 2008), elevated zero maze test (Walf et al., 2008), elevated plus maze test (Lund et al., 2005; Oyola et al., 2012), and light–dark box test (Lund et al., 2005; Oyola et al., 2012).”
BackgroundMethodInfluentialSelf-citationNew roles for estrogen receptor β in behavior and neuroendocrinology☆
Bodo, C., & Rissman, E. F. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.004 · Cited by 144
Hiroi, R., & Neumaier, J. F. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.07.021 · Cited by 151
Estrogen recruits the endocannabinoid system to modulate emotionality
Hill, M. N., Karacabeyli, E., & Gorzalka, B. B. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.003 · Cited by 153
“…to modulate emotional behavior is mediated by activation of bestrogen receptors, and not a-estrogen receptors (Walf et al., 2004;Walf and Frye, 2005b; Lund et al., 2005), examination of whether the FAAH gene is a molecular target of b-estrogen receptors is a necessary step in this line of research.”
BackgroundWalf, A., Koonce, C. J., & Frye, C. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.01.008 · Cited by 137
Spiteri, T., Musatov, S., Ogawa, S., Ribeiro, A., Pfaff, D., & Ǻgmo, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.033 · Cited by 136
Steroids‐Dopamine Interactions in the Pathophysiology and Treatment of CNS Disorders
Sanchez, M. G. D. B., Bourque, M., Morissette, M., & Paolo, T. D. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00163.x · Cited by 137
Estrogen receptor β ligands: Recent advances and biomedical applications
Minutolo, F., Macchia, M., Katzenellenbogen, B. S., & Katzenellenbogen, J. A. (2009) · Medicinal Research Reviews · doi:10.1002/med.20186 · Cited by 151
Weiser, M. J., Wu, T. J., & Handa, R. J. (2009) · Endocrinology · doi:10.1210/en.2008-1355 · Cited by 124
Self-citationOxytocin and Estrogen Receptor β in the Brain: An Overview
Acevedo-Rodriguez, A., Mani, S. K., & Handa, R. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00160 · Cited by 124
Self-citationCognitive Decline in Early and Premature Menopause
Sochocka, M., Karska, J., Pszczołowska, M., Ochnik, M., Fułek, M., Fułek, K., Kurpas, D., Chojdak-Łukasiewicz, J., Rosner‐Tenerowicz, A., & Leszek, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076566 · Cited by 144
Waters, E. M., Mitterling, K. L., Spencer-Segal, J. L., Mazid, S., McEwen, B. S., & Milner, T. A. (2009) · Brain Research · doi:10.1016/j.brainres.2009.06.090 · Cited by 129
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript DPN and PPT (Lund et al., 2005; Gonzales et al., 2008; Morissette et al., 2008); however, the DPN plus PPT treated animals may have experienced pharmacological effects due to the higher levels of steroids…”
BackgroundInfluentialHammond, R., Mauk, R., Ninaci, D., Nelson, D. A., & Gibbs, R. B. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.06.008 · Cited by 121
“In contrast, daily injections of PPT have been reported to increase anxiogenic behaviors such as the number of fecal boli and time spent grooming (Lund et al., 2005).”
BackgroundPhotoperiod reverses the effects of estrogens on male aggression via genomic and nongenomic pathways
Trainor, B. C., Lin, S., Finy, M. S., Rowland, M. R., & Nelson, R. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701819104 · Cited by 122
Walf, A., Koonce, C. J., & Frye, C. (2008) · Behavioral Neuroscience · doi:10.1037/a0012749 · Cited by 118
The premenstrual syndrome revisited.
Campagne, D., & Campagne, G. (2007) · European Journal of Obstetrics, Gynecology, and Reproductive Biology · doi:10.1016/j.ejogrb.2006.06.020 · Cited by 117
Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats
Donner, N. C., Bredewold, R., Maloumby, R., & Neumann, I. D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05416.x · Cited by 127
“It is well accepted that the rat stress response as well as anxiety behaviour is regulated by gonadal steroid hormones (Dayas et al., 2000; Popeski et al., 2003; Adachi et al., 2005; Lund et al., 2005; Ueyama et al., 2006).”
BackgroundGreendale, G. A., Derby, C. A., & Maki, P. M. (2011) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2011.05.007 · Cited by 122
Xu, X., Yang, Y., Wang, R., Wang, Y., Ruan, Q., & Yang, L. (2014) · Chemosphere · doi:10.1016/j.chemosphere.2014.10.056 · Cited by 124
“Testosterone in the male brain can be aromatized to 17b-E2 which is well-established regulators of mood in humans and animals of both sexes (Lund et al., 2005).”
BackgroundSynaptic regulation of affective behaviors; role of BDNF
Ninan, I. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.011 · Cited by 114
“The notion that estrogen receptor signaling might be critical for the regulation of affective behaviors is supported by the recent finding that estrogen receptor b agonists facilitate fear extinction and exert anxiolytic effects (Lund et al., 2005; Zeidan et al., 2011).”
Diversity of ovarian steroid signaling in the hypothalamus
Rønnekleiv, O. K., & Kelly, M. J. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.05.001 · Cited by 102
Endocrine disruption by dietary phyto-oestrogens: impact on dimorphic sexual systems and behaviours
Patisaul, H. B. (2017) · Proceedings of the Nutrition Society · doi:10.1017/s0029665116000677 · Cited by 107
Patisaul, H. B., Sullivan, A. W., Radford, M. E., Walker, D. M., Adewale, H. B., Winnik, B., Coughlin, J. L., Buckley, B., & Gore, A. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043890 · Cited by 106
Estrogen receptor β expression in the mouse forebrain: Age and sex differences
Zuloaga, D. G., Zuloaga, K. L., Hinds, L. R., Carbone, D. L., & Handa, R. J. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23400 · Cited by 109
“…many nonreproductive functions, including learning and memory (Jacome et al., 2010), depressive- and anxiety-like behaviors (Donner and Handa, 2009; Lund et al., 2005; Oyola et al., 2012; Weiser et al., 2009), hypothalamic–pituitary–adrenal (HPA) axis reactivity (Lund et al., 2006; Weiser et al.,…”
BackgroundSelf-citationLong-term alterations in neural and endocrine processes induced by motherhood in mammals
Bridges, R. S. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.09.001 · Cited by 100
“Previous research had indicated a role for ERβ in regulating anxiety in rats (Lund et al., 2005).”
McLaughlin, K. J., Bimonte‐Nelson, H. A., Neisewander, J. L., & Conrad, C. D. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.04.010 · Cited by 101
“In addition, the time spent in each zone and fecal boli were counted as an anxiety index (Hill and Gorzalka, 2006; Lund et al., 2005) because estradiol benzoate can influence anxiety during open field testing (Morgan and Pfaff, 2001).”
BackgroundOyola, M. G., Portillo, W., Reyna, A., Foradori, C. D., Kudwa, A., Hinds, L., Handa, R. J., & Mani, S. K. (2012) · Endocrinology · doi:10.1210/en.2011-1674 · Cited by 99
“Support for ER ’s role in anxiety, stems from the studies on anxiety-related behaviors in female rats, treated with an ER subtype-selective agonist (12).”
BackgroundMethodInfluentialSelf-citationCarroll, J. C., & Pike, C. J. (2008) · Endocrinology · doi:10.1210/en.2007-1346 · Cited by 103
Roles for Oestrogen Receptor β in Adult Brain Function
Handa, R. J., Ogawa, S., Wang, J. M., & Herbison, A. E. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02206.x · Cited by 97
Self-citationZhao, L.-Q., Mao, Z.-S., & Brinton, R. (2009) · Endocrinology · doi:10.1210/en.2008-0715 · Cited by 96
“In addition to its cognitive role, ER has also been suggested as a novel therapeutic target for the development of therapies for a range of pathological conditions mediated by ER , including menopausal vasomotor symptoms (30) and other brain disorders such as anxiety (31) and depressive behavior (32).”
BackgroundSelective Oestrogen Receptor Modulators Differentially Potentiate Brain Mitochondrial Function
Irwin, R. W., Yao, J., To, J., Hamilton, R. T., Cadenas, E., & Brinton, R. D. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02251.x · Cited by 92
Anchan, M., Clark, S. M., Pollard, K. J., & Vasudevan, N. (2013) · Brain and Behavior · doi:10.1002/brb3.197 · Cited by 92
“Doses of estradiol as well as routes of administration in female rodents vary widely (Lund et al. 2005), depending on the study’s endpoints.”
BackgroundAmbiguity aversion and familiarity bias: Evidence from behavioral and gene association studies
Chew, S. H., Ebstein, R. P., & Zhong, S. (2011) · Journal of Risk and Uncertainty · doi:10.1007/s11166-011-9134-0 · Cited by 83
“In rat pharmacological studies the anxiolytic properties of estrogens are ESR2 mediated (Lund et al. 2005).”
BackgroundHughes, Z. A., Liu, F., Platt, B. J., Dwyer, J. M., Pulicicchio, C. M., Zhang, G., Schechter, L. E., Rosenzweig-Lipson, S., & Day, M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.03.004 · Cited by 88
“Again, it is likely that ERb receptors mediate the effects of estrogen on anxiety state as the ERb preferring SERM, DPN decreases anxiety-like behaviour in elevated plus maze and the open field whereas the ERa preferring PPT had an anxiogenic-like profile ( Lund et al., 2005 ).”
BackgroundSex and gender in psychoneuroimmunology research: Past, present and future
Darnall, B. D., & Suarez, E. C. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.02.019 · Cited by 85
“For example, estrogen has also been shown to modulate both anxiety (Bodo and Rissman, 2006; Lund et al., 2005) and depression (via neurotransmitters 5HT [serotonin] and dopamine) (Zhou et al., 2002) whereas testosterone has been more frequently linked with sexual behavior and behavioral aggression…”
BackgroundNumakawa, T., Richards, M., Nakajima, S., Adachi, N., Furuta, M., Odaka, H., & Kunugi, H. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00136 · Cited by 86
Luine, V. N., Attalla, S., Mohan, G., Costa, A. L. L., & Frankfurt, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.016 · Cited by 79
Zuloaga, D. G., Heck, A., Guzman, R. M. D., & Handa, R. J. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00319-2 · Cited by 99
Self-citationZebrafish sexual behavior: role of sex steroid hormones and prostaglandins
Pradhan, A., & Olsson, P. (2015) · Behavioral and Brain Functions · doi:10.1186/s12993-015-0068-6 · Cited by 84
Spiteri, T., Ogawa, S., Musatov, S. A., Pfaff, D. W., & Ågmo, A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.048 · Cited by 100
Toufexis, D. J., Myers, K. M., Bowser, M. E., & Davis, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2529-07.2007 · Cited by 83
“ER activation increases fear and anxiety behaviors, and ER activation reduces these behaviors (Morgan and Pfaff, 2001; Walf et al., 2004; Lund et al., 2005; Walf and Frye, 2005).”
BackgroundMethodReproductive experience alters anxiety-like behavior in the female rat.
Byrnes, E. M., & Bridges, R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.01.006 · Cited by 83
Zuloaga, D., Morris, J. A., Jordan, C. L., & Breedlove, S. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.08.004 · Cited by 81
“…from the pituitary and corticosterone from the adrenal cortex) following exposure to a stressful situation (Handa et al., 1994; Lund et al., 2004; Lund et al., 2005; Lund et al., 2006), suggesting androgens can influence HPA axis activity, and in turn, may potentially influence anxiety-related…”
BackgroundInfluentialEstrogen Receptor beta in Health and Disease1
Imamov, O., Shim, G.-J., Warner, M. N., & Gustafsson, J.-Å. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.043497 · Cited by 117
Menstrual-cycle dependent fluctuations in ovarian hormones affect emotional memory
Bayer, J., Schultz, H., Gamer, M., & Sommer, T. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.017 · Cited by 81
ERβ: recent understanding of estrogen signaling
Sugiyama, N., Barros, R. P. A., Warner, M. N., & Gustafsson, J.-Å. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2010.05.001 · Cited by 82
Sex, hormones and affective arousal circuitry dysfunction in schizophrenia
Goldstein, J. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.029 · Cited by 73
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79
Hisasue, S.-I., Seney, M. L., Immerman, E., & Forger, N. G. (2010) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01669.x · Cited by 78
Byrnes, E. M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0122-4 · Cited by 77
“Several studies have shown that gonadal hormone levels can significantly affect behavior on the elevated plus maze and on novelty tasks (Frye and Walf 2004; Lund et al. 2005).”
BackgroundEffect of ER-β gene disruption on estrogenic regulation of anxiety in female mice
Tomihara, K., Soga, T., Nomura, M., Korach, K., Gustafsson, J., Pfaff, D., & Ogawa, S. (2008) · Physiology and Behavior · doi:10.1016/j.physbeh.2008.10.014 · Cited by 76
Roles of Oestrogen Receptors α and β in Behavioural Neuroendocrinology: Beyond Yin/Yang
Rissman, E. F. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01738.x · Cited by 78
Heger, M., Ventskovskiy, B. M., Borzenko, I., Kneis, K. C., Rettenberger, R., Kaszkin-Bettag, M., & Heger, P. W. (2006) · Menopause The Journal of The North American Menopause Society · doi:10.1097/01.gme.0000240632.08182.e4 · Cited by 74
Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms
Immonen, E., Hämäläinen, A., Schuett, W., & Tarka, M. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2462-1 · Cited by 97
“…anxiety: Studies in rodents discovered that a particular isoform of the estrogen receptor (ERβ) decreases anxiety in females (Imwalle et al. 2005; Lund et al. 2005) while increased levels of circulating testosterone decrease anxiety in both sexes (Celec et al. 2015) via androgen receptors…”
BackgroundXu, X., Dong, F., Yang, Y., Wang, Y., Wang, R., & Xiuying, S. (2014) · Chemosphere · doi:10.1016/j.chemosphere.2014.07.021 · Cited by 86
Kudwa, A. E., McGivern, R. F., & Handa, R. J. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.03.004 · Cited by 73
Self-citationWalf, A. A., & Frye, C. A. (2007) · Stress · doi:10.1080/00958970701220416 · Cited by 74
“…estradiol’s effects occur via actions at two well-described isoforms of the estrogen receptor (ER), ERa or ERb, which are expressed in different regions of the brain, and may drive HPA axis function in opposing ways, are not clear (Miller et al. 2004; Suzuki and Handa 2004, 2005; Lund et al. 2005).”
BackgroundRegulation of estrogen receptor beta activity and implications in health and disease
Swedenborg, E., Power, K. A., Cai, W., Pongratz, I., & Rüegg, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0118-z · Cited by 69
Furuta, M., Numakawa, T., Chiba, S., Ninomiya, M., Kajiyama, Y., Adachi, N., Akema, T., & Kunugi, H. (2013) · Endocrinology · doi:10.1210/en.2012-2136 · Cited by 72
Estrogen Receptors and the Regulation of Neural Stress Responses
Handa, R. J., Mani, S. K., & Uht, R. M. (2012) · Neuroendocrinology · doi:10.1159/000338397 · Cited by 72
Self-citation
Metadata
- Authors
- Lund, T. D., Rovis, T., Chung, W. C. J., & Handa, R. J.
- Affiliations
- Colorado State University (US)
- Corresponding author
- Lund, Trent D.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2005-02
- Volume
- 146
- Issue
- 2
- Pages
- 797-807
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- 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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