Mapping oxytocin receptor gene expression in the mouse brain and mammary gland using an oxytocin receptor-LacZ reporter mouse
Abstract
The hypothalamic nonapeptide oxytocin (OT) has an established role as a circulating hormone but can also act as a neurotransmitter and as a neuromodulator by interacting with its central OT receptor (OTR). To understand the role of the OTR in the mouse brain we investigated the expression of the OTR gene at the cellular level. We targeted the lacZ reporter gene to the OTR gene locus downstream of the endogenous OTR regulatory elements. Using lactating mouse mammary gland as a control for OTR promoter directed specificity of lacZ gene expression, X-gal histochemistry on tissue sections confirmed that gene expression was restricted to the myoepithelial cells. We also identified for the first time in mice the expression of the OTR gene in neighbouring adipocytes. Further, investigation in the mouse brain identified numerous nuclei containing neurons expressing the OTR gene. Whilst some of these regions had been described for rat or sheep, the OTR-LacZ reporter mouse enabled the identification of novel sites of central OTR gene expression. These regions include the accessory olfactory bulb, the medial septal nucleus, the posterolateral cortical amygdala nucleus, the posterior aspect of the basomedial amygdala nucleus, the medial part of the supramammillary nucleus, the dorsotuberomammillary nucleus, the medial and lateral entorhinal cortices, as well as specific dorsal tegmental, vestibular, spinal trigeminal, and solitary tract subnuclei. By mapping the distribution of OTR gene…
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Adipocytes and fat progenitor cells have receptors for oxytocin.
“It has been previously shown that adipocytes and fat progenitor cells have receptors for oxytocin(35, 36).”
From Oxytocin reduces caloric intake in men (2015) · cites this paper as [35]
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“Third, does OT act on the presynaptic or postsynaptic site of the mitral-to-granule cell synapse? The OT receptor-LacZ reporter mouse exhibited OT receptor-expressing neurons in regions that have not been described previously [15].”
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“Numerous reports have shown widespread distribution of the OT receptor throughout the brain and, importantly, specific sites involved in reward processing, such as the nucleus accumbens and the ventral tegmental area, appear to be prominent central targets of OT signaling (39, 40).”
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“Brain regions known to be involved in appetite regulation, such as the dorsomedial and ventromedial hypothalamic nuclei, are also rich in OT receptors (Gould and Zingg, 2003).”
BackgroundEmerging role of astrocytes in oxytocin-mediated control of neural circuits and brain functions
Baudon, A., Creusot, E. C., Althammer, F., Schaaf, C. P., & Charlet, A. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102328 · Cited by 40 · see citing works
“It must be noted here that albeit OTR expression in neurons is observed in a myriad of species and brain regions (Gould and Zingg, 2003; Mitre et al., 2016; Newmaster et al., 2020; Young and Song, 2020), these studies did not investigate actual OTR expression levels in neurons on a quantitative,…”
BackgroundHypothalamic Supramammillary Control of Cognition and Motivation
Kesner, A. J., Mozaffarilegha, M., Thirtamara Rajamani, K., Arima, Y., Harony-Nicolas, H., Hashimotodani, Y., Ito, H. T., Song, J., & Ikemoto, S. (2023) · The Journal of Neuroscience · doi:10.1523/jneurosci.1320-23.2023 · Cited by 35 · see citing works
Rajamani, K. T., Barbier, M., Lefèvre, A., Niblo, K., Cordero, N., Netser, S., Grinevich, V., Wagner, S., & Harony‐Nicolas, H. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02336-0 · Cited by 44 · see citing works
Alpha-Melanocyte-Stimulating Hormone-Mediated Appetite Regulation in the Central Nervous System
Wu, Q., Chen, J., Hua, T., & Cai, J. (2023) · Neuroendocrinology · doi:10.1159/000530804 · Cited by 45 · see citing works
Novel oxytocin receptor variants in laboring women requiring high doses of oxytocin
Reinl, E. L., Goodwin, Z. A., Raghuraman, N., Lee, G. Y., Jo, E. Y., Gezahegn, B. M., Pillai, M. K., Cahill, A. G., Strong, C. D. G., & England, S. K. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.04.036 · Cited by 40 · see citing works
Jungnickel, S., & Gundlach, A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.11.023 · Cited by 32 · see citing works
Oxytocin and Sensory Network Plasticity
Pekarek, B. T., Hunt, P. J., & Arenkiel, B. R. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00030 · Cited by 37 · see citing works
“Notably, work in the hippocampus links local neuropeptide release to environmental and social learning stressors or enrichment (Ögren et al., 2010; Grégoire et al., 2014; Li et al., 2017).”
BackgroundDunigan, A. I., & Roseberry, A. G. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100011 · Cited by 28 · see citing works
The Neuropeptide Hormone Oxytocin in Eating Disorders
Plessow, F., Eddy, K. T., & Lawson, E. A. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0957-0 · Cited by 32 · see citing works
D’Addario, C., Pucci, M., Bellia, F., Girella, A., Sabatucci, A., Fanti, F., Vismara, M. E. M., Benatti, B., Ferrara, L., Fasciana, F., et al. (2022) · Clinical Epigenetics · doi:10.1186/s13148-022-01264-0 · Cited by 31 · see citing works
Oxytocin as an Anti-obesity Treatment
Niu, J., Tong, J., & Blevins, J. E. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.743546 · Cited by 30 · see citing works
Diversity of central oxytocinergic projections
Jirikowski, G. F. (2019) · Cell and Tissue Research · doi:10.1007/s00441-018-2960-5 · Cited by 27 · see citing works
Fujiwara, T., Sanada, M., Kofuji, T., & Akagawa, K. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13634 · Cited by 25 · see citing works
“In humans, single nucleotide polymorphism variants in OXTR may be associated with social behavioral phenotypes (Tost et al. 2010), and high levels of methylation of OXTR, which decrease gene expression, may be associated with individual variability in social behavior (Jack et al. 2012).”
BackgroundInfluentialBlockade of pro-cognitive effects of angiotensin IV and physostigmine in mice by oxytocin antagonism
Gard, P. R., Naylor, C., Ali, S., & Partington, C. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.02.048 · Cited by 25 · see citing works
Localization of oxytocin receptors in the prairie vole (Microtus ochrogaster) neocortex
Duchemin, A., Seelke, A. M. H., Simmons, T. C., Freeman, S. M., & Bales, K. L. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.017 · Cited by 19 · see citing works
“…including but not limited to: rats, mice, several vole species, marmosets, coppery titi monkeys, rhesus macaques, and humans (Insel and Shapiro 1992, Freeman, et al. 2016, Vaccari, et al. 1998, Gould and Zingg 2003, Freeman, et al. 2014, Freeman, et al. 2014, Schorscher-Petcu, et al. 2009).”
BackgroundFreeman, S. M., Ngo, J., Singh, B., Masnaghetti, M., Bales, K. L., & Blevins, J. E. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.07.037 · Cited by 37 · see citing works
The ventromedial hypothalamus oxytocin induces locomotor behavior regulated by estrogen
Narita, K., Murata, T., & Matsuoka, S. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.047 · Cited by 18 · see citing works
“Murata), Oxtr exists within various brain regions including the PVN, SON, septum, hippocampus, and olfactory bulb [11,21,42].”
Arakawa, H. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100011 · Cited by 24 · see citing works
Wang, Y.-F., Negoro, H., & Higuchi, T. (2013) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.2012.02368.x · Cited by 20 · see citing works
Using transgenic mouse models to study oxytocin's role in the facilitation of species propagation
Lee, H., Pagani, J. H., & Young, W. S. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.042 · Cited by 19 · see citing works
“We will focus on a subset, the knockout (KO) mouse, as various transgenic lines expressing reporter constructs based on the oxytocin or oxytocin receptor gene have not yet lead to significant advances (Gould and Zingg, 2003; Katoh et al., 2009; Young et al., 1990).”
A neuromodulatory role for oxytocin within the supramammillary nucleus.
Cumbers, M., Chung, S., & Wakerley, J. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.04.004 · Cited by 17 · see citing works
Welch, M. G., & Ruggiero, D. A. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)71012-6 · Cited by 16 · see citing works
Edwards, M. M., Nguyen, H. K., Dodson, A. D., Herbertson, A. J., Wietecha, T., Wolden‐Hanson, T., Graham, J. L., Honeycutt, M. K., Slattery, J. D., O’Brien, K. D., et al. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.725912 · Cited by 16 · see citing works
Medial prefrontal cortex oxytocin-opioid receptors interaction in spatial memory processing in rats
Salighedar, R., Erfanparast, A., Tamaddonfard, E., & Soltanalinejad, F. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112599 · Cited by 15 · see citing works
Maternal Brain Adaptations in Pregnancy
Brunton, P. J., & Russell, J. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00044-2 · Cited by 18 · see citing works
Dayı, A., Kıray, M., Şişman, A. R., Özbal, S., Baykara, B., Aksu, İ., & Uysal, N. (2019) · Biotechnic & Histochemistry · doi:10.1080/10520295.2018.1528384 · Cited by 9 · see citing works
“The PFC possesses oxytocin-sensitive neurons (Ninan 2011) and expresses oxytocin receptors (Gould and Zingg 2003; Liu et al. 2005).”
BackgroundAntonucci, L. A., Taurisano, P., Coppola, G., & Cassibba, R. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.002 · Cited by 20 · see citing works
“Accordingly, OXTR is highly expressed in key brain regions for emotion processing and recognition, such as the amygdala (Gimpl and Fahrenholz, 2001; Skuse and Gallagher, 2009) and the prefrontal cortex (Gould and Zingg, 2003; Liu et al., 2005; Meyer-Lindenberg et al., 2011; Mitre et al., 2016).”
Paletta, P., Bass, N., Kavaliers, M., & Choleris, E. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0058 · Cited by 15 · see citing works
Chronic Ambient Ozone Exposure Aggravates Autism-Like Symptoms in a Susceptible Mouse Model
Ling, W., Ren, Z., Wang, W., Lü, D., Zhou, Q., Liu, Q. S., & Jiang, G. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c00607 · Cited by 14 · see citing works
Asker, M., Krieger, J., Liles, A., Tinsley, I. C., Borner, T., Marić, I., Doebley, S. A., Furst, C. D., Börchers, S., Longo, F., et al. (2022) · Diabetes Obesity and Metabolism · doi:10.1111/dom.14937 · Cited by 14 · see citing works
Oxytocin: A Potential Therapeutic for Obesity
Hong, S. M., Ko, J.-K., Moon, J., & Kim, Y. (2021) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes20098 · Cited by 13 · see citing works
Maroun, M., Sarussi-Elyahu, A., Yaseen, A., Hatoum, O. A., & Kritman, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01040-9 · Cited by 16 · see citing works
- Authors
- Gould, B. R., & Zingg, H. H.
- Affiliations
- Royal Victoria Hospital (CA)
- Corresponding author
- Zingg, H.H
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2003-11
- Volume
- 122
- Issue
- 1
- Pages
- 155-167
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2035269878
- Cited by
- 138
- References
- 0
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 11 · 2021: 11 · 2020: 7 · 2019: 4 · 2018: 10 · 2017: 7 · 2016: 10 · 2015: 8 · 2014: 12 · 2013: 10 · 2012: 4
- FWCI
- 3.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- oxytocin receptor, gene expression mapping, myoepithelial cells, mammary gland, amygdala, accessory olfactory bulb, supramammillary nucleus, entorhinal cortex, oxytocinergic system, adipocytes
- MeSH terms
- Animals, Brain, Female, Lac Operon, Mammary Glands, Animal, Mice, Transgenic, Blotting, Southern, Gene Expression, Receptors, Oxytocin, Reverse Transcriptase Polymerase Chain Reaction, Mice
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