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Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats
Open accessAbstract
Accumulation of continuous life stress (chronic stress) often causes gastric symptoms. Although central oxytocin has antistress effects, the role of central oxytocin in stress-induced gastric dysmotility remains unknown. Solid gastric emptying was measured in rats receiving acute restraint stress, 5 consecutive days of repeated restraint stress (chronic homotypic stress), and 7 consecutive days of varying types of stress (chronic heterotypic stress). Oxytocin and oxytocin receptor antagonist were administered intracerebroventricularly (icv). Expression of corticotropin-releasing factor (CRF) mRNA and oxytocin mRNA in the paraventricular nucleus (PVN) of the hypothalamus was evaluated by real-time RT-PCR. The changes of oxytocinergic neurons in the PVN were evaluated by immunohistochemistry. Acute stress delayed gastric emptying, and the delayed gastric emptying was completely restored after 5 consecutive days of chronic homotypic stress. In contrast, delayed gastric emptying persisted following chronic heterotypic stress. The restored gastric emptying following chronic homotypic stress was antagonized by icv injection of an oxytocin antagonist. Icv injection of oxytocin restored delayed gastric emptying induced by chronic heterotypic stress. CRF mRNA expression, which was significantly increased in response to acute stress and chronic heterotypic stress, returned to the basal levels following chronic homotypic stress. In contrast, oxytocin mRNA expression was significantly increased following chronic homotypic stress. The number of oxytocin-immunoreactive cells was increased following chronic homotypic stress at the magnocellular part of the PVN. Icv injection of oxytocin reduced CRF mRNA expression induced by acute stress and chronic heterotypic stress. It is suggested that the adaptation mechanism to chronic stress may involve the upregulation of oxytocin expression in the hypothalamus, which in turn attenuates CRF expression.
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“Animal studies have demonstrated that oxytocin plays an important role in lowering the physiological stress and anxiety response by activating a negative feedback loop (Onaka et al., 2012;Zheng et al., 2010).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Zheng et al., 2010
In the citing paper
“Elevated oxytocin secretion from the paraventricular nucleus of the hypothalamus following a stressful event is believed to lead to increased availability of gamma-aminobutyric acid (GABA), which in turn is believed to inhibit the HPA axis and amygdala activation (Onaka et al., 2012;Zheng et al., 2010).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Zheng et al., 2010
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Sensory Stimulation of Oxytocin Release Is Associated With Stress Management and Maternal Care
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“Previous studies (Zheng et al. 2010) have shown that exogenous administration of an OXT receptor antagonist prevented the restoration of the delayed gastric emptying observed following chronic homotypic”
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“In a series of brilliant experiments, Takahashi’s group correlated the GI adaptive changes observed upon chronic homotypic stress to increased levels of OXT-IR and OXT mRNA containing neurons in the PVN (Zheng et al., 2010; Babygirija et al., 2012).”
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“Additionally, it is well known that OXT/AVP systems could be affected by acute or chronic restraint stress [28] [29], as well as other types of stressors such as forced swimming [30], dehydration [31] or electric footshock [32].”
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“The administration of an OTR agonist or antagonist by icv. or local injection (in the PVN, central amygdala and prefrontal cortex) consistently produces an anxiolytic effect similar to that of synthetic or endogenous OT in male and female rodents, especially during periods of robust activation and increased central re…”
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“For instance, a number of recent studies have shown that restraint stress induces c-fos expression in oxytocinergic neurons in PVN in rats (Miyata et al., 1995; Zheng et al., 2010; Yoshimoto et al., 2012).”
InfluentialOxytocin Signaling Acts as a Marker for Environmental Stressors in Zebrafish
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“Intracerebroventricular injection of OT significantly attenuates the increase in CRF mRNA expression in the PVN induced by restraint stress [40].”
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Babygirija, R., Cerjak, D., Yoshimoto, S., Gribovskaja‐Rupp, I., Bülbül, M., Ludwig, K., & Takahashi, T. (2012) · Autonomic Neuroscience · doi:10.1016/j.autneu.2012.03.001 · Cited by 14
“To mimic complex stress exposure in humans, we utilized chronic stress models in rats (Choudhury et al., 2009; Zheng et al., 2010).”
BackgroundMethodResultInfluentialVagally mediated gastric effects of brain stem α2-adrenoceptor activation in stressed rats
Jiang, Y., Browning, K. N., Toti, L., & Travagli, R. A. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00382.2017 · Cited by 14
Can oxytocin inhibit stress-induced hyperalgesia?
Li, Y.-X., An, H. Y., Wen, Z., Tao, Z.-Y., & Cao, D. (2019) · Neuropeptides · doi:10.1016/j.npep.2019.101996 · Cited by 13
Yu, Y., Yu, H., Babygirija, R., Shi, B., Sun, W., Zheng, X., & Zheng, J. (2019) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm19065 · Cited by 12
“For CCS loading, the rats (n = 6-8) received different types of stressors for 7 consecutive days, as previously reported.(8) The stress paradigms used were fasten restraint stress (FRS), force swimming stress (FSS), cold restraint stress (CRS), and water avoidance stress (WAS).”
BackgroundMethodResultInfluentialKanada, Y., Katayama, A., Ikemoto, H., Takahashi, K., Tsukada, M., Nakamura, A., Ishino, S., Hisamitsu, T., & Sunagawa, M. (2018) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s156795 · Cited by 10
“These doses were determined by referring to a previous study.(24) It was reported that intraperitoneal administration of OT (500 pmol per rat) inhibited water-avoidance stress-induced colonic contraction in rats.”
BackgroundLuna, D., Calderón-Amor, J., González, C., Byrd, C. J., Palomo, R., Huenul, E., & Figueroa, J. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106221 · Cited by 10
Dual autonomic inhibitory action of central Apelin on gastric motor functions in rats
Bülbül, M., & Sinen, O. (2018) · Autonomic Neuroscience · doi:10.1016/j.autneu.2018.03.005 · Cited by 10
Cantabella, E., Camilleri, V., Cavalié, I., Dubourg, N., Gagnaire, B., Charlier, T. D., Adam‐Guillermin, C., Cousin, X., & Armant, O. (2022) · Cancers · doi:10.3390/cancers14153793 · Cited by 11
“Other experiments in rodents revealed that repeated defeat experiences increased the number of oxytocinergic neurons in the PVN as well as after chronic homotypic stress [107,108].”
BackgroundJovanović, P., Stefanović, B., Spasojević, N., Puškaš, N., & Dronjak, S. (2016) · Endocrine Research · doi:10.3109/07435800.2015.1094086 · Cited by 9
“The results of some other authors also suggest that oxytocin plays a pivotal role in mediating the adaptation mechanism in animals following chronic stress (37,38).”
ResultMagnetic Resonance Imaging of Gastric Motility in Conscious Rats
Wang, X., Alkaabi, F., Cornett, A. M., Choi, M., Scheven, U. M., Natale, M. R. D., Furness, J. B., & Liu, Z. (2024) · Neurogastroenterology & Motility · doi:10.1111/nmo.14982 · Cited by 7
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“Generally, intestinal ion secretion [40,59], macromolecular permeability [60,61], inflammation [40,59], visceral hypersensivity and colonic motility increased [40], while gastric motility decreased in various animal models of stress [62-64].”
BackgroundWhy is pharma so scared of psychiatric drug discovery?
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“A study by Zhang et al, reasoned that it is the CRF receptors in a specific area of the hypothalamus (Para ventricular nucleus) which are markedly involved in controlling CRF secretion [24].”
BackgroundStress-induced neuroplasticity in the gastric response to brainstem oxytocin in male rats
Jiang, Y., Zimmerman, J. E., Browning, K. N., & Travagli, R. A. (2022) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00347.2021 · Cited by 6
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“Real time-PCR study showed that OT mRNA expression is upregulated in the paraventricular nucleus of the hypothalamus following chronic homotypic stress in rats [21].”
Oxytocin und die suchterhaltenden Mechanismen der Alkoholabhängigkeit
Faehrmann, T., Zernig, G., & Mechtcheriakov, S. (2017) · Neuropsychiatrie · doi:10.1007/s40211-017-0229-y · Cited by 5
“Hohe Oxytocinspiegel sind demnach mit erniedrigten CRFSpiegeln assoziiert [32].”
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“However, oxytocin can also restore gastric motility and reverse the delay in gastric emptying that is caused by stress (31, 66, 78).”
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“Delayed gastric emptying and accelerated colonic transit induced by acute restraint stress are abolished by intracerebroventricular (icv)-injection of OXT in rats([11,12]).”
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Oxytocin and Social Isolation: Nonapeptide Regulation of Social Homeostasis
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Malocclusion impairs cognitive behavior via AgRP signaling in adolescent mice
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“Although malocclusion is a stressor, no hypothalamic CRF mRNA upregulation was observed in the Malocclusion/powder group here.”
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Environment and Behavior: Neurochemical Effects of Different Diets in the Calf Brain
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Oxytocin and Social Sensitivity: Implications for Vulnerability to Stress and Depressive Symptoms
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The Neuroendocrine and Cardiovascular Responses to a Pup in Male Prairie Voles (M. ochrogaster)
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Oxytocin, Social Interactions and Coping: Implications for Depression
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The oxytocinergic descending control of pain and its modulation by neonatal maternal separation
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Metadata
- Authors
- Zheng, J., Babygirija, R., Bülbül, M., Cerjak, D., Ludwig, K., & Takahashi, T.
- Affiliations
- Medical College of Wisconsin (US)
- Corresponding author
- Takahashi, Toku
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2010-10
- Volume
- 299
- Issue
- 4
- Pages
- G946-G953
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- PMC
- PMC2957337
- OpenAlex
- W2143119886
- Cited by
- 104
- References
- 53
- Citations by year
- 2026: 2 · 2024: 7 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 3 · 2019: 5 · 2018: 12 · 2017: 10 · 2016: 7 · 2015: 9 · 2014: 8 · 2013: 7 · 2012: 8
- FWCI
- 12.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK 62768, R01DK062768)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- chronic stress, stress adaptation, gastric emptying, corticotropin-releasing factor, paraventricular nucleus, hypothalamus, oxytocin receptor antagonist, magnocellular neurons, acute restraint stress
- MeSH terms
- Animals, Brain, Brain Chemistry, Chronic Disease, Gene Expression Regulation, Hypothalamus, Immunohistochemistry, Injections, Intraventricular, Male, Oxytocics, Oxytocin, Restraint, Physical, RNA, Messenger, Stress, Physiological, Rats, Sprague-Dawley, Receptors, Oxytocin, Rats
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