The estrogen receptor α colocalizes with proopiomelanocortin in hypothalamic neurons and binds to a conserved motif present in the neuron-specific enhancer nPE2
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The gene encoding the prohormone proopiomelanocortin (POMC) is mainly expressed in two regions in vertebrates, namely corticotrophs and melanotrophs in the pituitary and a small population of neurons in the arcuate nucleus of the hypothalamus. In this latter region, POMC-derived peptides participate in the control of energy balance and sensitivity to pain. Neuronal expression of POMC is conferred by two enhancers, nPE1 and nPE2, which are conserved in most mammals, but no transcription factors are yet known to bind to these enhancers. In this work, by means of a one-hybrid screening, we identify that nPE2 possesses an element recognized by transcription factors of the nuclear receptor superfamily. This element, named NRBE, is conserved in all known nPE2 enhancers and is necessary to confer full enhancer strength to nPE2-driven reporter gene expression in transgenic mice assays, indicating that the phylogenetic conservation of the element is indicative of its functional importance. In a search for candidate nuclear receptors that might control POMC we observed that estrogen receptor alpha (ESR1) - a known regulator of energy balance at the hypothalamic level - can bind to the NRBE element in vitro. In addition we observed by immunofluorescence that ESR1 is coexpressed with POMC in around 25-30% of hypothalamic neurons of males and females during late embryonic stages and adulthood. Thus, our results indicate that hypothalamic expression of POMC is controlled by nuclear receptors and establish ESR1 as a candidate regulator of POMC.
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NPY exhibits decreased orexigenic activity after exposure to estrogens, due to estrogen modulation of NPY mRNA expression and receptor activity.
“NPY exhibits decrease orexigenic activity after exposure to estrogens. This inhibitory action is due to the estrogen modulation of NPY mRNA expression and receptor activity [93, 94].”
From Estrogen deficiency and the origin of obesity during menopause (2014) · cites this paper as [94]
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The nuclear receptor superfamily: the second decade
Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schütz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90199-x · Cited by 6,964 · see citing works
Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus
Cowley, M. A., Smart, J. L., Rubinstein, M., Cerdán, M. G., Diano, S., Horvath, T. L., Cone, R. D., & Low, M. J. (2001) · Nature · doi:10.1038/35078085 · Cited by 2,356 · see citing works
Self-citationCarroll, J. S., Liu, X. S., Brodsky, A. S., Li, W., Meyer, C. A., Szary, A. J., Eeckhoute, J., Shao, W., Hestermann, E. V., Geistlinger, T. R., et al. (2005) · Cell · doi:10.1016/j.cell.2005.05.008 · Cited by 1,384 · see citing works
Increased adipose tissue in male and female estrogen receptor-α knockout mice
Heine, P. A., Taylor, J. A., Iwamoto, G. A., Lubahn, D. B., & Cooke, P. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.23.12729 · Cited by 1,282 · see citing works
Leptin Increases Hypothalamic Pro-opiomelanocortin mRNA Expression in the Rostral Arcuate Nucleus
Schwartz, M. W., Seeley, R. J., Woods, S. C., Weigle, D. S., Campfield, L. A., Burn, P., & Baskin, D. G. (1997) · Diabetes · doi:10.2337/diab.46.12.2119 · Cited by 879 · see citing works
Orphan Nuclear Receptors: From Gene to Function
Giguère, V. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.5.0378 · Cited by 848 · see citing works
Exploring the opioid system by gene knockout
Kieffer, B. L., & Gavériaux-Ruff, C. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00008-4 · Cited by 620 · see citing works
The Hormonal Control of Food Intake
Coll, A. P., Farooqi, I. S., & O’Rahilly, S. (2007) · Cell · doi:10.1016/j.cell.2007.04.001 · Cited by 605 · see citing works
Whole-Genome Cartography of Estrogen Receptor α Binding Sites
Lin, C., Vega, V. B., Thomsen, J. S., Zhang, T., Kong, S. L., Xie, M., Chiu, K. P., Lipovich, L., Barnett, D., Stossi, F., et al. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030087 · Cited by 459 · see citing works
Forkhead protein FoxO1 mediates Agrp-dependent effects of leptin on food intake
Kitamura, T., Feng, Y., Kitamura, Y., Chua, S. C., Xu, A. W., Barsh, G. S., Rossetti, L., & Accili, D. (2006) · Nature Medicine · doi:10.1038/nm1392 · Cited by 449 · see citing works
Regulation of hypothalamic proopiomelanocortin mRNA by leptin in ob/ob mice
Thornton, J. E., Cheung, C. C., Clifton, D. K., & Steiner, R. A. (1997) · Endocrinology · doi:10.1210/endo.138.11.5651 · Cited by 437 · cited 2× · see citing works
“Part of the anorectic effect that leptin exerts on the central control of food intake is thought to be mediated by an increase in POMC expression (Schwartz et al., 1997; Thornton et al., 1997) and the activation of POMCneurons in”
Orphan Nuclear Receptors: From Gene to Function
Giguère, V. (1999) · Endocrine Reviews · doi:10.1210/er.20.5.689 · Cited by 423 · see citing works
Gao, Q., Mezei, G., Nie, Y., Rao, Y., Choi, C. S., Bechmann, I., Leranth, C., Toran-Allerand, D., Priest, C. A., Roberts, J. L., et al. (2007) · Nature Medicine · doi:10.1038/nm1525 · Cited by 416 · see citing works
Williams, K. W., Margatho, L. O., Lee, C. E., Choi, M., Lee, S., Scott, M. M., Elias, C. F., & Elmquist, J. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3118-09.2010 · Cited by 352 · see citing works
Vanacker, J.-M., Pettersson, K., Gustafsson, J.-Α., & Laudet, V. (1999) · The EMBO Journal · doi:10.1093/emboj/18.15.4270 · Cited by 340 · see citing works
Münzberg, H., Huo, L., Nillni, E. A., Hollenberg, A. N., & Bjørbæk, C. (2003) · Endocrinology · doi:10.1210/en.2002-221037 · Cited by 328 · see citing works
Japón, M. Á., Rubinstein, M., & Low, M. J. (1994) · Journal of Histochemistry & Cytochemistry · doi:10.1177/42.8.8027530 · Cited by 323 · see citing works
Self-citationPadilla, S. L., Carmody, J. S., & Zeltser, L. M. (2010) · Nature Medicine · doi:10.1038/nm.2126 · Cited by 312 · see citing works
Lehman, M. N., & Karsch, F. J. (1993) · Endocrinology · doi:10.1210/endo.133.2.8102098 · Cited by 254 · see citing works
Cross-talk between estrogen and leptin signaling in the hypothalamus
Gao, Q., & Horváth, T. L. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00733.2007 · Cited by 249 · see citing works
Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral arcuate nucleus
Schwartz, M. W., Seeley, R. J., Woods, S. C., et al. (1997) · Diabetes · doi:10.2337/diabetes.46.12.2119 · Cited by 206 · see citing works
Proopiomelanocortin Expression in both GABA and Glutamate Neurons
Hentges, S. T., Otero-Corchón, V., Pennock, R. L., King, C. M., & Low, M. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3770-09.2009 · Cited by 171 · see citing works
Self-citationGofflot, F., Chartoire, N., Vasseur, L., Heikkinen, S., Dembélé, D., Merrer, J. L., & Auwerx, J. H. (2007) · Cell · doi:10.1016/j.cell.2007.09.012 · Cited by 164 · see citing works
Skinner, D. C., & Herbison, A. E. (1997) · Endocrinology · doi:10.1210/endo.138.6.5208 · Cited by 148 · see citing works
Santangelo, A. M., de Souza, F. S. J., Franchini, L. F., Bumaschny, V. F., Low, M. J., & Rubinstein, M. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030166 · Cited by 126 · see citing works
Self-citationPelletier, G., Li, S.-Y., Luu-The, V., & Labrie, F. (2007) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.2007.01548.x · Cited by 102 · see citing works
de Souza, F. S. J., Santangelo, A. M., Bumaschny, V. F., Avale, M. E., Smart, J. L., Low, M. J., & Rubinstein, M. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.8.3076-3086.2005 · Cited by 100 · see citing works
Self-citationWarnecke, M., Oster, H., Revelli, J.-P., Álvarez-Bolado, G., & Gregor Eichele, C. (2005) · Genes & Development · doi:10.1101/gad.317905 · Cited by 95 · see citing works
Chakraborty, T. R., Hof, P. R., Ng, L., & Gore, A. C. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10906 · Cited by 94 · see citing works
Oestrogen Modulates Hypothalamic Control of Energy Homeostasis Through Multiple Mechanisms
Roepke, T. A. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01814.x · Cited by 90 · see citing works
Genes Associated with Membrane-Initiated Signaling of Estrogen and Energy Homeostasis
Roepke, T. A., Xue, C., Bosch, M. A., Scanlan, T. S., Kelly, M. J., & Rønnekleiv, O. K. (2008) · Endocrinology · doi:10.1210/en.2008-0769 · Cited by 85 · see citing works
Regulation of Proopiomelanocortin Gene Expression
Jenks, B. G. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03620.x · Cited by 70 · see citing works
Thornton, J. E., Loose, M. D., Kelly, M. J., & Rønnekleiv, O. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410107 · Cited by 63 · see citing works
Gelman, D. M., Noaín, D., Avale, M. E., Otero, V., Low, M. J., & Rubinstein, M. (2003) · genesis · doi:10.1002/gene.10217 · Cited by 51 · see citing works
Self-citationPro-opiomelanocortin (POMC)-derived peptides and the regulation of energy homeostasis
Coll, A. P., & Tung, Y. C. L. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.09.007 · Cited by 47 · see citing works
The LIM/Homeodomain Protein Islet-1 Modulates Estrogen Receptor Functions
Gay, F., Anglade, I., Gong, Z., & Salbert, G. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.10.0538 · Cited by 43 · see citing works
Skinner, D. C. (1997) · Endocrinology · doi:10.1210/en.138.6.2585 · Cited by 38 · see citing works
Nuclear Receptor Location Analyses in Mammalian Genomes: From Gene Regulation to Regulatory Networks
Deblois, G., & Giguère, V. (2008) · Molecular Endocrinology · doi:10.1210/me.2007-0546 · Cited by 36 · see citing works
Davis, A. M., Seney, M. L., Walker, H. J., & Tobet, S. A. (2003) · Endocrinology · doi:10.1210/en.2003-0996 · Cited by 29 · see citing works
Dynorphin in pro-opiomelanocortin neurons of the hypothalamic arcuate nucleus
Maolood, N., & Meister, B. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.011 · Cited by 27 · see citing works
Yaghmaie, F., Saeed, O., Garan, S. A., Voelker, M. A., Sternberg, H., & Timiras, P. S. (2010) · PubMed · Cited by 9 · see citing works
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Barros, R. P. A., & Gustafsson, J.-Å. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.08.005 · Cited by 458 · see citing works
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Xu, Y., Elmquist, J. K., & Fukuda, M. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06248.x · Cited by 133 · see citing works
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Florant, G., & Healy, J. E. (2012) · Journal of Comparative Physiology □ B · doi:10.1007/s00360-011-0630-y · Cited by 108 · see citing works
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Lam, D. D., de Souza, F. S. J., Nasif, S., Yamashita, M., López‐Leal, R., Otero-Corchón, V., Meece, K., Sampath, H., Mercer, A. J., Wardlaw, S. L., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004935 · Cited by 115 · see citing works
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Dey, P., Barros, R. P. A., Warner, M. N., Ström, A., & Gustafsson, J.-Α. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0150 · Cited by 98 · see citing works
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Herber, C. B., Krause, W. C., Wang, L., Bayrer, J. R., Li, A., Schmitz, M. T., Fields, A. J., Ford, B., Zhang, Z., Reid, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-08046-4 · Cited by 86 · see citing works
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Fuente-Martín, E., García‐Cáceres, C., Morselli, E., Clegg, D. J., Chowen, J. A., Finan, B., Brinton, R. D., & Tschöp, M. H. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-013-9263-7 · Cited by 87 · see citing works
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Helena, C. V. V., Toporikova, N., Kalil, B., Stathopoulos, A. M., Pogrebna, V. V., Carolino, R. O. G., Anselmo-Franci, J. A., & Bertram, R. (2015) · Endocrinology · doi:10.1210/en.2015-1070 · Cited by 65 · see citing works
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Harris, R. M., Dijkstra, P. D., & Hofmann, H. A. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.007 · Cited by 41 · see citing works
Blood-to-brain communication in the hypothalamus for energy intake regulation
Takemura, S., & Wanaka, A. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.04.007 · Cited by 40 · see citing works
Rubinstein, M., & Low, M. J. (2017) · FEBS Letters · doi:10.1002/1873-3468.12776 · Cited by 38 · see citing works
Self-citationDNA Methylation of Tumor Suppressor Genes in Pituitary Neuroendocrine Tumors
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Anthwal, N., Pelling, M., Claxton, S., Mellitzer, G., Collin, C., Kessaris, N., Richardson, W. D., Gradwohl, G., & Ang, S. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.011916 · Cited by 33 · see citing works
MacKay, H., & Abizaid, A. B. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.09.004 · Cited by 34 · see citing works
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Lazzarino, G. P., Andreoli, M. F., Rossetti, M. F., Stoker, C., Tschopp, M. V., Luque, E. H., & Ramos, J. G. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.05.005 · Cited by 32 · see citing works
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Conde, K., Meza, C., Kelly, M. J., Sinchak, K., & Wagner, E. J. (2016) · Neuroendocrinology · doi:10.1159/000443765 · Cited by 26 · see citing works
Hypothalamic Perineuronal Nets Are Regulated by Sex and Dietary Interventions
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Eckstrum, K. S., Edwards, W. D., Banerjee, A., Wang, W., Flaws, J. A., Katzenellenbogen, J. A., Kim, S. H., & Raetzman, L. T. (2017) · Endocrinology · doi:10.1210/en.2017-00565 · Cited by 26 · see citing works
Samodien, E., Pheiffer, C., Erasmus, M., Mabasa, L., Louw, J., & Johnson, R. (2019) · Food Science & Nutrition · doi:10.1002/fsn3.1169 · Cited by 25 · see citing works
Metz, L., Isacco, L., & Redman, L. M. (2021) · Metabolism · doi:10.1016/j.metabol.2021.154919 · Cited by 24 · see citing works
Sakurazawa, N., Mano‐Otagiri, A., Nemoto, T., & Shibasaki, T. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.02.006 · Cited by 24 · see citing works
Marraudino, M., Bo, E., Carlini, E., Farinetti, A., Ponti, G., Zanella, I., Lorenzo, D. D., Panzica, G., & Gotti, S. (2021) · Metabolites · doi:10.3390/metabo11060368 · Cited by 23 · see citing works
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Self-citationBorgquist, A., Meza, C., & Wagner, E. J. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00615.2014 · Cited by 18 · see citing works
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Xu, Y. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-70178-3_16 · Cited by 8 · see citing works
Leyrer‐Jackson, J. M., Hood, L. E., & Olive, M. F. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108674 · Cited by 8 · see citing works
Ovarian Hormonal Change-Related Energy Metabolism and Obesity in Menopausal Women
Zhu, J., Ji, M., Xing, L., Yu, Z., Guo, X., Chen, X., & Shu, J. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.89336 · Cited by 7 · see citing works
Rojo, D., Hael, C. E., Soria, A., de Souza, F. S. J., Low, M. J., Franchini, L. F., & Rubinstein, M. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2322692121 · Cited by 5 · see citing works
Self-citationTorres, D. J., Pitts, M. W., Seale, L. A., Hashimoto, A. C., An, K. J., Hanato, A. N., Hui, K. W., Remigio, S. M. A., Carlson, B. A., Hatfield, D. L., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011010 · Cited by 5 · see citing works
Sexual dimorphism in the development and function of the melanocortin system
Claret, M., & Haddad-Tóvolli, R. (2025) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-025-09983-4 · Cited by 5 · see citing works
Escarcena, L. V., Neufeld, M., Rietschel, M., Spanagel, R., & Scholz, H. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.655816 · Cited by 4 · see citing works
Alejandro, E. U. (2019) · Diabetes · doi:10.2337/dbi18-0046 · Cited by 4 · see citing works
Nguyen, H. P., Chan, C. S. Y., Cintrón, D. L., Sheng, R. R., Harshman, L., Nobuhara, M., Ushiki, A., Biellak, C., An, K., Gordon, G., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.06.515311 · Cited by 4 · see citing works
Dax1 in AgRP neurons regulates thermogenesis via GR-HDAC3-mediated CRFR1 suppression
Wei, Z., Cha, J., & Lee, S. (2025) · Molecular Metabolism · doi:10.1016/j.molmet.2025.102258 · Cited by 3 · see citing works
Rebouças, E. C. C., Leal, S. M., Silva, S. M., & Sá, S. I. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2016.05.001 · Cited by 3 · see citing works
Neuroendocrine Control of Energy Stores
Cone, R. D., & Elmquist, J. K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-29738-7.00035-6 · Cited by 2 · see citing works
Regulation of POMC and ACTH Secretion
Zhang, D., & Heaney, A. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.65220-0 · Cited by 2 · see citing works
Aerts, E. G., Griesgraber, M. J., Thomson, A. L., Brown, M. B., Bowdridge, E. C., Hardy, S. L., Seman, A., Goodman, R. L., Nestor, C. C., & Hileman, S. M. (2025) · Biology of Reproduction · doi:10.1093/biolre/ioaf074 · Cited by 1 · see citing works
Growing Up POMC: Pro-opiomelanocortin in the Developing Brain
Padilla, S. L. (2011) · doi:10.7916/d80g3s3v
Liu, J. (2013) · UvA-DARE (University of Amsterdam)
NKX2.1 is critical for melanocortin neuron identity, hypothalamic Pomc expression and body weightPreprint
Orquera, D. P., Tavella, M. B., de Souza, F. S. J., Nasif, S., Low, M. J., & Rubinstein, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/460501
Self-citationJones, G. L. (2019) · Deep Blue (University of Michigan)
Regulation of POMC and ACTH secretion
Zhang, D., & Heaney, A. P. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13825-6.00148-5
Mahla, S., Chhabra, A., Bano, F., Yadav, U. C. S., & Tyagi, R. K. (2026) · Food and Chemical Toxicology · doi:10.1016/j.fct.2026.116284
- Authors
- de Souza, F. S. J., Nasif, S., López-Leal, R., Levi, D. H., Low, M. J., & Rubinsten, M.
- Affiliations
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- University of Michigan (US)
- Corresponding author
- Rubinsten, Marcelo
- ORCID
- Low, Malcolm J.
- Venue
- European Journal of Pharmacology
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 660
- Issue
- 1
- Pages
- 181-187
- ISSN
- 0014-2999 (ISSN-L)
- PMC
- PMC3097136
- OpenAlex
- W2089174173
- Cited by
- 75
- References
- 39
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 4 · 2021: 7 · 2020: 3 · 2019: 10 · 2018: 6 · 2017: 5 · 2016: 5 · 2015: 5 · 2014: 4 · 2013: 8 · 2012: 4
- FWCI
- 3.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK068400, DK068400)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- estrogen receptor alpha, proopiomelanocortin, hypothalamic neurons, arcuate nucleus, transcriptional regulation, energy balance, melanotrophs, corticotrophs, colocalization, enhancer conservation
- MeSH terms
- Animals, Base Sequence, Enhancer Elements, Genetic, Female, Humans, Hypothalamus, Male, Molecular Sequence Data, Neurons, Pro-Opiomelanocortin, Protein Binding, Conserved Sequence, Gene Expression Regulation, Developmental, Protein Transport, Estrogen Receptor alpha, Mice
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