Brain region-specific methylation in the promoter of the murine oxytocin receptor gene is involved in its expression regulation
Abstract
Oxytocin is a nine amino acid neuropeptide that is known to play a critical role in fetal expulsion and breast-feeding, and has been recently implicated in mammalian social behavior. The actions of both central and peripheral oxytocin are mediated through the oxytocin receptor (Oxtr), which is encoded by a single gene. In contrast to the highly conserved expression of oxytocin in specific hypothalamic nuclei, the expression of its receptor in the brain is highly diverse among different mammalian species or even within individuals of the same species. The diversity in the pattern of brain Oxtr expression among mammals is thought to contribute to the broad range of social systems and organizations. Yet, the mechanisms underlying this diversity are poorly understood. DNA methylation is a major epigenetic mechanism that regulates gene transcription, and has been linked to reduced expression levels of the Oxtr in individuals with autism. Here we hypothesize that DNA methylation is involved in the expression regulation of Oxtr in the mouse brain. By combining bisulfite DNA conversion and Next-Generation Sequencing we found that specific CpG sites are differentially methylated between distinct brain regions expressing different levels of Oxtr mRNA. Some of these CpG sites are located within putative binding sites of transcription factors known to regulate Oxtr expression, including estrogen receptor α (ERα) and SP1. Specifically, methylation of the SP1 site was found to positively correlate with Oxtr expression. Furthermore, we revealed that the methylation levels of these sites in the various brain regions predict the relationship between ERα and Oxtr mRNA levels. Collectively, our results suggest that brain region-specific expression of the mouse Oxtr gene is epigenetically regulated by DNA methylation of its promoter.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Transgenic mice carrying a reporter gene driven by 5 kb of prairie vole Oxtr 5' flanking sequence express the reporter in a brain pattern resembling prairie voles, suggesting the sequence may suffice for some aspects of brain-region-specific expression.
“Transgenic mice carrying a reporter gene driven by 5 kb of the prairie vole Oxtr 5’ flanking sequence express the reporter in the brain in a pattern resembling prairie voles (64), suggesting the sequence may suffice for some aspects of brain region-specific expression.”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [64]
Cites
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
DNA methylation landscapes: Provocative insights from epigenomics
Suzuki, M. M., & Bird, A. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2341 · Cited by 3,039 · see citing works
Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688 · see citing works
Insel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044 · see citing works
Oxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037 · see citing works
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833 · see citing works
The vertebrate social behavior network: Evolutionary themes and variations
Goodson, J. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.003 · Cited by 771 · see citing works
Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
Genomic and epigenetic evidence for oxytocin receptor deficiency in autism
Gregory, S. G., Connelly, J. J., Towers, A. J., Johnson, J., Biscocho, D., Markunas, C. A., Lintas, C., Abramson, R. K., Wright, H. H., Ellis, P., et al. (2009) · BMC Medicine · doi:10.1186/1741-7015-7-62 · Cited by 576 · see citing works
Epigenetics and the environmental regulation of the genome and its function
Zhang, T.-Y., & Meaney, M. J. (2010) · Annual Review of Psychology · doi:10.1146/annurev.psych.60.110707.163625 · Cited by 565 · see citing works
Positive Association of the Oxytocin Receptor Gene (OXTR) with Autism in the Chinese Han Population
Wu, S., Jia, M., Ruan, Y., Liu, J., Guo, Y., Mei, S., Gong, X., Zhang, Y., Yang, X., & Zhang, D. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.013 · Cited by 553 · see citing works
Francis, D. D., Champagne, F. C., & Meaney, M. J. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00599.x · Cited by 496 · see citing works
Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice
Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A., & Chen, A. (2010) · Nature Neuroscience · doi:10.1038/nn.2642 · Cited by 436 · see citing works
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432 · see citing works
Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism
Jacob, S., Brune, C. W., Carter, C. S., Leventhal, B. L., Lord, C., & Cook, E. H. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.02.001 · Cited by 425 · see citing works
Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00776.x · Cited by 415 · see citing works
Lukas, M., Toth, I., Reber, S. O., Slattery, D. A., Veenema, A. H., & Neumann, I. D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.95 · Cited by 403 · see citing works
Lerer, E., Levi, S., Salomon, S., Darvasi, A., Yirmiya, N., & Ebstein, R. P. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002087 · Cited by 349 · see citing works
Central vasopressin and oxytocin release: regulation of complex social behaviours
VEENEMA, A., & NEUMANN, I. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00422-6 · Cited by 338 · see citing works
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
Epigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273 · see citing works
Unternaehrer, E., Luers, P., Mill, J., Dempster, E., Meyer, A. H., Staehli, S., Lieb, R., Hellhammer, D. H., & Meinlschmidt, G. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.77 · Cited by 250 · see citing works
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230 · see citing works
Oxytocin and Vasopressin Receptors and Species-Typical Social Behaviors
Young, L. J. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1548 · Cited by 211 · see citing works
Insel, T. R., Gelhard, R., & Shapiro, L. E. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90321-e · Cited by 209 · see citing works
Deconstructing sociality, social evolution and relevant nonapeptide functions
Goodson, J. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.12.005 · Cited by 206 · see citing works
Constraints and flexibility in mammalian social behaviour: introduction and synthesis
Kappeler, P. M., Barrett, L., Blumstein, D. T., & Clutton-Brock, T. H. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0337 · Cited by 206 · see citing works
Goodson, J. L., & Kabelik, D. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.007 · Cited by 204 · see citing works
Kusui, C., Kimura, T., Ogita, K., Nakamura, H., Matsumura, Y., Koyama, M., Azuma, C., & Murata, Y. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.6024 · Cited by 196 · see citing works
Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain
Meddle, S. L., Bishop, V. R., Gkoumassi, E., van Leeuwen, F. W., & Douglas, A. J. (2007) · Endocrinology · doi:10.1210/en.2007-0615 · Cited by 195 · see citing works
DNA methylation of the oxytocin receptor gene predicts neural response to ambiguous social stimuli
Jack, A., Connelly, J. J., & Morris, J. P. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00280 · Cited by 192 · cited 1× · see citing works
“In humans, DNA methylation of the OXTR in blood cells predicted the neural response to ambiguous social stimuli and rapidly changed following acute psycho-social stress (Jack et al., 2012; Unternaehrer et al., 2012).”
Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles
Wang, H., Duclot, F., Liu, Y., Wang, Z., & Kabbaj, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3420 · Cited by 173 · see citing works
Oxytocin receptor density is associated with male mating tactics and social monogamy
Ophir, A. G., Gessel, A., Zheng, D.-J., & Phelps, S. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.007 · Cited by 161 · see citing works
Young, L. J., Muns, S., Wang, Z., & Insel, T. R. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.00654.x · Cited by 160 · see citing works
Larcher, A., Neculcea, J., Breton, C., Arslan, A., Rozen, F., Russo, C., & Zingg, H. H. (1995) · Endocrinology · doi:10.1210/endo.136.12.7588281 · Cited by 140 · see citing works
Oxytocin and experimental therapeutics in autism spectrum disorders
BARTZ, J., & HOLLANDER, E. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00435-4 · Cited by 139 · see citing works
Gould, B. R., & Zingg, H. H. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00283-5 · Cited by 138 · cited 1× · see citing works
“To approach this question, we began by analyzing the cerebellum (Cer) and olfactory bulb (OB) because they are easily accessible for extraction, and were previously shown to exhibit marked differences in Oxtr expression (Gould and Zingg, 2003).”
Central vasopressin and oxytocin receptor distributions in two species of singing mice
Polly Campbell, A., Ophir, A. G., & Phelps, S. M. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22116 · Cited by 128 · see citing works
Sexually dimorphic expression of oxytocin binding sites in forebrain and spinal cord of the rat
Uhl-Bronner, S., Waltisperger, E., Martínez-Lorenzana, G., Condes Lara, M., & Freund-Mercier, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.025 · Cited by 123 · see citing works
Fleming, J. G. W., Spencer, T. E., Safe, S. H., & Bazer, F. W. (2005) · Endocrinology · doi:10.1210/en.2005-1120 · Cited by 111 · see citing works
Mamrut, S., Harony‐Nicolas, H., Sood, R., Shahar-Gold, H., Gainer, H., Shi, Y.-J., Barki‐Harrington, L., & Wagner, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056869 · Cited by 102 · see citing works
Structure and expression of the mouse oxytocin receptor gene
Kubota, Y., Kimura, T., Hashimoto, K., Tokugawa, Y., Nobunaga, K., Azuma, C., Saji, F., & Murata, Y. (1996) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(96)03923-8 · Cited by 93 · see citing works
Kalamatianos, T., Faulkes, C. G., Oosthuizen, M. K., Poorun, R., Bennett, N. C., & Coen, C. W. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22302 · Cited by 92 · see citing works
The role of sex steroids in the oxytocin hormone system
Ivell, R., & Walther, N. (1999) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(99)00025-8 · Cited by 86 · see citing works
Interplay Between Social Experiences and the Genome: Epigenetic Consequences for Behavior
Champagne, F. A. (2012) · Advances in genetics · doi:10.1016/b978-0-12-387687-4.00002-7 · Cited by 72 · see citing works
Oxytocin receptor binding in the hypothalamus during gestation in rats
Bealer, S. L., Lipschitz, D. L., Ramoz, G., & Crowley, W. R. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00766.2005 · Cited by 54 · see citing works
The Structure and Regulation of the Oxytocin Receptor
Ivell, R., Kimura, T., Müller, D., Augustin, K., Abend, N., Bathgate, R. A. D., Telgmann, R., Balvers, M., Tillmann, G., & Fuchs, A. (2001) · Experimental Physiology · doi:10.1113/eph8602185 · Cited by 47 · see citing works
Postweaning, forebrain-specific perturbation of the oxytocin system impairs fear conditioning
Pagani, J. H., Lee, H.-J., & Young, W. S. (2011) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2011.00709.x · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999 · see citing works
Feldman, R., Monakhov, M., Pratt, M., & Ebstein, R. P. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.008 · Cited by 352 · see citing works
King, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“DNA methylation of Oxtr differs between brain regions in rodents (64,65).”
Developmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 177 · see citing works
Smearman, E. L., Almli, L. M., Conneely, K. N., Brody, G. H., Sales, J. M., Bradley, B., Ressler, K. J., & Smith, A. K. (2016) · Child Development · doi:10.1111/cdev.12493 · Cited by 173 · see citing works
Maud, C., Ryan, J., McIntosh, J. E., & Olsson, C. A. (2018) · BMC Psychiatry · doi:10.1186/s12888-018-1740-9 · Cited by 151 · see citing works
Miller, J. L., Tamura, R., Butler, M. G., Kimonis, V. E., Sulsona, C. R., Gold, J., & Driscoll, D. J. (2017) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.38160 · Cited by 149 · see citing works
Griffiths, B. B., & Hunter, R. G. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.041 · Cited by 111 · see citing works
Oxytocin receptor DNA methylation in postpartum depression
Kimmel, M., Clive, M. L., Gispen, F. E., Guintivano, J., Brown, T., Cox, O., Beckmann, M. W., Kornhuber, J., Fasching, P. A., Osborne, L. M., et al. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.04.008 · Cited by 111 · see citing works
Epigenetic evidence for involvement of the oxytocin receptor gene in obsessive–compulsive disorder
Cappi, C., Diniz, J. B., Requena, G. D. L., Lourenço, T., Lisbôa, B. C. G., Batistuzzo, M. C., Marques, A. H., Hoexter, M. Q., Pereira, C. A. D. B., Miguel, E. C., et al. (2016) · BMC Neuroscience · doi:10.1186/s12868-016-0313-4 · Cited by 84 · see citing works
Beery, A. K., McEwen, L. M., MacIsaac, J. L., Francis, D. D., & Kobor, M. S. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.022 · Cited by 81 · see citing works
Reiner, I., Van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Bleich, S., Beutel, M., & Frieling, H. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.03.012 · Cited by 83 · see citing works
Oxytocin receptor dynamics in the brain across development and species
Vaidyanathan, R., & Hammock, E. A. D. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22403 · Cited by 82 · see citing works
The effects of acute social isolation on long-term social recognition memory
Leser, N., & Wagner, S. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.002 · Cited by 82 · see citing works
Epigenetics of childhood trauma: Long term sequelae and potential for treatment
Thumfart, K. M., Jawaid, A., Bright, K., Flachsmann, M., & Mansuy, I. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.042 · Cited by 78 · see citing works
Oxytocin Modulation of Neural Circuits
Mitre, M., Minder, J. L., Morina, E., Chao, M. V., & Froemke, R. C. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_7 · Cited by 76 · see citing works
Zhang, R., Zhang, H.-F., Han, J., & Han, S. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0120-7 · Cited by 78 · see citing works
Rubin, L. H., Connelly, J. J., Reilly, J. L., Carter, C. S., Drogos, L. L., Pournajafi‐Nazarloo, H., Ruocco, A. C., Keedy, S., Matthew, I., Tandon, N., et al. (2015) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2015.10.003 · Cited by 72 · see citing works
Sexually dimorphic oxytocin receptor-expressing neurons in the preoptic area of the mouse brain
Sharma, K., LeBlanc, R. M., Haque, M., Nishimori, K., Reid, M. M., & Teruyama, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0219784 · Cited by 63 · see citing works
Oxytocin as Treatment for Social Cognition, Not There Yet
Erdozain, A. M., & Peñagarikano, O. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00930 · Cited by 61 · see citing works
Kraaijenvanger, E. J., He, Y., Spencer, H., Smith, A. K., Bos, P. A., & Boks, M. P. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.016 · Cited by 57 · see citing works
The interplay of oxytocin and sex hormones
Quintana, D. S., Glaser, B. D., Kang, H., Kildal, E. S.-M., Audunsdottir, K., Sartorius, A. M., & Barth, C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105765 · Cited by 54 · see citing works
Interactions Between Genetics, Lifestyle, and Environmental Factors for Healthcare
Lin, Y., Chen, J., & Shen, B. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5717-5_8 · Cited by 39 · see citing works
Childhood emotional neglect and oxytocin receptor variants: Association with limbic brain volumes
Womersley, J. S., Hemmings, S. M. J., Ziegler, C., Gutridge, A., Ahmed-Leitao, F., Rosenstein, D., Domschke, K., & Seedat, S. (2019) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2019.1584331 · Cited by 40 · see citing works
Danoff, J. S., Connelly, J. J., Morris, J. P., & Perkeybile, A. M. (2021) · Comprehensive Psychoneuroendocrinology · doi:10.1016/j.cpnec.2021.100098 · Cited by 36 · see citing works
Social Behavior of Pet Dogs Is Associated with Peripheral OXTR Methylation
Cimarelli, G., Virányi, Z., Turcsán, B., Rónai, Z., Sasvári‐Székely, M., & Bánlaki, Z. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00549 · Cited by 36 · see citing works
Intertwined associations between oxytocin, immune system and major depressive disorder
Jiang, J., Yang, M., Tian, M., Chen, Z., Xiao, L., & Gong, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114852 · Cited by 36 · see citing works
Towers, A. J., Tremblay, M. W., Chung, L., Li, X.-L., Bey, A. L., Zhang, W., Cao, X., Wang, X., Wang, P., Duffney, L. J., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.120592 · Cited by 34 · see citing works
Genetic architecture, epigenetic influence and environment exposure in the pathogenesis of Autism
Yu, L., Wu, Y., & Wu, B.-L. (2015) · Science China Life Sciences · doi:10.1007/s11427-015-4941-1 · Cited by 31 · see citing works
Frankiensztajn, L. M., Gur-Pollack, R., & Wagner, S. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.04.006 · Cited by 27 · see citing works
Bánlaki, Z., Cimarelli, G., Virányi, Z., Kubinyi, E., Sasvári‐Székely, M., & Rónai, Z. (2017) · Molecular Genetics and Genomics · doi:10.1007/s00438-017-1305-5 · Cited by 23 · see citing works
Borie, A. M., Theofanopoulou, C., & Andari, E. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819973-2.00009-5 · Cited by 18 · see citing works
Fan, X., Xu, T., Ding, H., Li, H., Yang, Y., He, Y., Tang, J., Liu, Y., Chen, X., Chen, J., et al. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14299 · Cited by 18 · see citing works
Oxytocin Receptor in Cerebellar Purkinje Cells Does Not Engage in Autism-Related Behaviors
Shen, L.-P., Li, W., Pei, L.-Z., Yin, J., Xie, S.-T., Li, H.-Z., Yan, C., Wang, J., Zhang, Q., Zhang, X., et al. (2022) · The Cerebellum · doi:10.1007/s12311-022-01466-5 · Cited by 16 · see citing works
Dogra, S., Sona, C., Kumar, A., & Yadav, P. N. (2016) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2016.03.012 · Cited by 16 · see citing works
Vasotocin and the origins of the vasopressin/oxytocin receptor gene family
Mayasich, S. A., & Clarke, B. L. (2020) · Vitamins and hormones · doi:10.1016/bs.vh.2019.08.018 · Cited by 16 · see citing works
Qin, X., Lin, H., Cao, Y., Wu, R. S. S., Lai, K. P., & Kong, R. Y. C. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.160594 · Cited by 14 · see citing works
Xie, S., Hu, Y., Fang, L., Chen, S., Botchway, B. O. A., Tan, X., Fang, M., & Hu, Z. (2021) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0128 · Cited by 14 · see citing works
Hofmann, J. P., Huber, C. W., Novak, B., Schreckenbach, M., Schubert, C. F., Touma, C., Rutten, B. P. F., & Schmidt, U. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105242 · Cited by 12 · see citing works
Aiba, T., Saito, T., Hayashi, A., Sato, S., Yunokawa, H., Maruyama, T., Fujibuchi, W., Kurita, H., Tohyama, C., & Ohsako, S. (2017) · BMC Molecular Biology · doi:10.1186/s12867-017-0083-2 · Cited by 11 · see citing works
Sharma, K., Govar, A. A., Ghimire, B., Nishimori, K., Hammock, E. A. D., & Teruyama, R. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13337 · Cited by 8 · see citing works
Lee, Y.-J., Lin, H., Chaudhary, M. A., Lee, Y., & Wang, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189847 · Cited by 8 · see citing works
Lemche, E. (2020) · acta ethologica · doi:10.1007/s10211-020-00346-7 · Cited by 6 · see citing works
Ludwig, B., Carlberg, L., Kienesberger, K., Swoboda, P., Swoboda, M. M. M., Bernegger, A., Koller, R., Inaner, M., Fuxjäger, M., Zotter, M., et al. (2022) · BMC Psychiatry · doi:10.1186/s12888-022-04031-w · Cited by 7 · see citing works
Methylation of OXT and OXTR genes, central oxytocin, and social behavior in female macaques
Leon, D. D., Nishitani, S., Walum, H., McCormack, K. M., Wilson, M. E., Smith, A. K., Young, L. J., & Sánchez, M. M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104856 · Cited by 7 · see citing works
Zorenko, T., & KAIJA, L. P. (2024) · TURKISH JOURNAL OF ZOOLOGY · doi:10.55730/1300-0179.3168 · Cited by 6 · see citing works
Mayasich, S. A., Bemis, L., & Clarke, B. L. (2016) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2016.07.007 · Cited by 6 · see citing works
Malone, C. L., Rieger, N. S., Spool, J. A., Payette, A., Riters, L. V., & Marler, C. A. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114556 · Cited by 5 · see citing works
Lauby, S. C., Agarwal, I., Lapp, H. E., Salazar, M., Semyrenko, S., Chauhan, D., Margolis, A. E., & Champagne, F. A. (2025) · Hormones and Behavior · doi:10.1016/j.yhbeh.2025.105745 · Cited by 4 · see citing works
Teruyama, R., & Govar, A. A. (2024) · Peptides · doi:10.1016/j.peptides.2024.171283 · Cited by 1 · see citing works
Genetic predisposition of behavioral response
Gregory, S. G. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323421111
Oxytocin Receptors and Neurobehavior
Kumsta, R., Zang, J. C. S., & Moser, D. (2016) · Epigenetics and human health · doi:10.1007/978-3-319-29901-3_10
Hutchinson, D. M., Manno, L. D., Fransquet, P., & Teague, S. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-815350-5.00006-1
Pharmacological Characterisation of Novel Oxytocin and Vasopressin Receptor Ligands
Gulliver, D. W. (2021) · The Sydney eScholarship Repository (The University of Sydney)
Ludwig, B., Carlberg, L., Kienesberger, K., Swoboda, P., Swoboda, M. M. M., Bernegger, A., Koller, R., Inaner, M., Fuxjäger, M., Zotter, M., et al. (2022) · Figshare · doi:10.6084/m9.figshare.20023196
Ludwig, B., Carlberg, L., Kienesberger, K., Swoboda, P., Swoboda, M. M. M., Bernegger, A., Koller, R., Inaner, M., Fuxjäger, M., Zotter, M., et al. (2022) · Figshare · doi:10.6084/m9.figshare.20023193
Ludwig, B., Carlberg, L., Kienesberger, K., Swoboda, P., Swoboda, M. M. M., Bernegger, A., Koller, R., Inaner, M., Fuxjäger, M., Zotter, M., et al. (2022) · Figshare · doi:10.6084/m9.figshare.20023190
Attenuating neuropsychiatric disorders of early-life stress: The protective role of oxytocin
Zhang, Y., Wang, S., & Hei, M. (2026) · World Journal of Psychiatry · doi:10.5498/wjp.v16.i4.115109
The oxytocinergic descending control of pain and its modulation by neonatal maternal separation
Melchior, M. (2018) · theses.fr (ABES) · doi:10.70675/368c73c0ze731z4b57zb52cz8f31049fb33c
Circuits neuronaux sous-tendant la régulation émotionnelle par le système ocytocinergique
Goyon, S. (2018) · theses.fr (ABES) · doi:10.70675/c8c9bec0z7b79z4826z862az93b128e1ada6
- Authors
- Harony-Nicolas, H., Mamrut, S., Brodsky, L., Shahar-Gold, H., Barki-Harrington, L., & Wagner, S.
- Affiliations
- University of Haifa (IL)
- Corresponding author
- Wagner, Shlomo
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 39
- Pages
- 121-131
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2135606779
- Cited by
- 61
- References
- 48
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 5 · 2019: 3 · 2018: 7 · 2017: 7 · 2016: 7 · 2015: 7 · 2014: 3
- FWCI
- 8.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Autism Speaks (3613)
- Israel Science Foundation (1901/08)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- oxytocin receptor, DNA methylation, promoter methylation, brain region-specific gene expression, epigenetic regulation, estrogen receptor alpha, Sp1, CpG sites, transcription factor binding sites, mouse brain, autism spectrum disorder
- MeSH terms
- Animals, Brain, Female, Gene Expression Regulation, Male, Promoter Regions, Genetic, RNA, Messenger, Receptors, Oxytocin, DNA Methylation, Epigenesis, Genetic, Estrogen Receptor alpha, Mice
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
