Vulnerability to stress in mouse offspring is ameliorated when pregnant dams are provided a chewing stick during prenatal stress

Kubo, Kin‐ya; Suzuki, Ayumi; Iinuma, Mitsuo; Sato, Yuichi; Nagashio, Ryo; Ohta, Emi; Chen, Huayue

doi:10.1016/j.archoralbio.2018.10.014

Cited by 5 publications

(8 citation statements)

References 54 publications

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“…BDNF-GC equilibrium is crucial throughout life as a major mechanism for stress response regulation [36]. Prenatal stress downregulates hippocampal BDNF [18] and GR expression [19]. The combination of low BDNF and low GR expression results in vulnerability to stress-related disorders.…”

Section: Discussionmentioning

confidence: 99%

“…In rodents, chewing during restraint stress alleviates anxiety-like behavior and cognitive impairments induced by restraint stress [16,17]. Maternal chewing also ameliorates prenatal stress-induced spatial learning impairment and deficiencies in hippocampal neurogenesis, myelination and synaptic plasticity in the offspring [18][19][20][21], but the underlying mechanisms have remained unclear.…”

Section: Introductionmentioning

confidence: 99%

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Effects of Maternal Chewing on Prenatal Stress-Induced Cognitive Impairments in the Offspring via Multiple Molecular Pathways

Zhou

Suzuki

Iinuma

et al. 2020

IJMS

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We aimed to investigate the effects of maternal chewing on prenatal stress-induced cognitive impairments in the offspring and to explore the molecular pathways of maternal chewing in a mice model. Maternal chewing ameliorated spatial learning impairments in the offspring in a Morris water maze test. Immunohistochemistry and Western blot findings revealed that maternal chewing alleviated hippocampal neurogenesis impairment and increased the expression of hippocampal brain-derived neurotrophic factor in the offspring. In addition, maternal chewing increased the expression of glucocorticoid receptor (GR) and 11β-hydroxysteroid dehydrogenase isozyme 2 (11β-HSD2) and decreased the expression of 11β-HSD1 in the placenta, thereby attenuating the increase of glucocorticoid in the offspring. Furthermore, maternal chewing increased the expression of 11β-HSD2, FK506-binding protein 51 (FKBP51) and FKBP52 and decreased the expression of 11β-HSD1, thereby increasing hippocampal nuclear GR level. In addition, maternal chewing attenuated the increase in expression of DNMT1 and DNMT3a and the decrease in expression of histone H3 methylation at lysine 4, 9, 27 and histone H3 acetylation at lysine 9 induced by prenatal stress in the offspring. Our findings suggest that maternal chewing could ameliorate prenatal stress-induced cognitive impairments in the offspring at least in part by protecting placenta barrier function, alleviating hippocampal nuclear GR transport impairment and increasing the hippocampal brain-derived neurotrophic factor (BDNF) level.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Effects of Maternal Chewing on Prenatal Stress-Induced Cognitive Impairments in the Offspring via Multiple Molecular Pathways

Zhou

Suzuki

Iinuma

et al. 2020

IJMS

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“…These findings are consistent with our results. Glucocorticoids are central regulators that affect the prenatal stress response by modulating the negative feedback system of the HPA axis via binding to glucocorticoid receptors [22,24,40]. The presence of glucocorticoid receptors in hippocampal microglia has been confirmed both in vivo and in vitro [41].…”

Section: Discussionmentioning

confidence: 99%

“…The STRESS and STRESS/CHEWING animals were subjected to restraint stress for 45 min three times a day from gestational day 12 to parturition. The STRESS/CHEWING animals were given a wooden stick (diameter: 2 mm; length: 65 mm) for chewing during the restraint stress period, as described in previous studies [19][20][21][22]24]. The CONTROL animals were neither subjected to restraint stress nor given sticks for chewing.…”

Section: Animal Modelsmentioning

confidence: 99%

“…Animal experiments have revealed that chewing under stress conditions ameliorates stress-associated cognitive deficits and anxiety behavior [19][20][21][22]. Maternal chewing improves the stress-associated decrease in hippocampal neurogenesis, alterations of myelination and synaptic plasticity, and hippocampus-dependent memory impairments produced by prenatal stress in mouse pups [19,[22][23][24]. The precise mechanisms underlying the effects of maternal chewing on stress-related cognitive deficits remain unclear.…”

Section: Introductionmentioning

confidence: 99%

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Maternal chewing alleviates prenatal stress-related neuroinflammation mediated by microglia in the hippocampus of the mouse offspring

et al. 2023

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Prenatal stress affects the hippocampal structure and function in pups. Maternal chewing ameliorates hippocampus-dependent cognitive impairments induced by prenatal stress. In this study, we investigated hippocampal microglia-mediated neuroinflammation in pups of dams exposed to prenatal stress with or without chewing during gestation. Methods: Pregnant mice were randomly assigned to control, stress, and stress/chewing groups. Stress and stress/chewing animals were subjected to restraint stress for 45 min three times daily from gestation day 12 to parturition, and were given a wooden stick to chew during the stress period. Four-month-old male pups were intraperitoneally administered with lipopolysaccharide (LPS). Serum corticosterone levels were determined 24 h after administration. The expression levels of hippocampal inflammatory cytokines were measured, and the microglia were analyzed morphologically. Results: Prenatal stress increased serum corticosterone levels, induced hippocampal microglia priming, and facilitated the release of interleukin-1β and tumor necrosis factor-α in the offspring. LPS treatment significantly increased the effects of prenatal stress on serum corticosterone levels, hippocampal microglial activation, and hippocampal neuroinflammation. Maternal chewing significantly inhibited the increase in serum corticosterone levels, suppressed microglial overactivation, and normalized inflammatory cytokine levels under basal prenatal stress conditions as well as after LPS administration. Conclusions: Our findings indicate that maternal chewing can alleviate the increase in corticosterone levels and inhibit hippocampal microglia-mediated neuroinflammation induced by LPS administration and prenatal stress in adult offspring.

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Maternal chewing improves prenatal stress-induced cognitive deficit and anxiety-like behavior associated with alterations of the apoptotic response and serotonin pathway in mouse offspring

Kajimoto

Hisada

Ochi

et al. 2021

Archives of Oral Biology

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Vulnerability to stress in mouse offspring is ameliorated when pregnant dams are provided a chewing stick during prenatal stress

Cited by 5 publications

References 54 publications

Effects of Maternal Chewing on Prenatal Stress-Induced Cognitive Impairments in the Offspring via Multiple Molecular Pathways

Effects of Maternal Chewing on Prenatal Stress-Induced Cognitive Impairments in the Offspring via Multiple Molecular Pathways

Maternal chewing alleviates prenatal stress-related neuroinflammation mediated by microglia in the hippocampus of the mouse offspring

Maternal chewing improves prenatal stress-induced cognitive deficit and anxiety-like behavior associated with alterations of the apoptotic response and serotonin pathway in mouse offspring

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