Sleep deprivation enhances peripheral serotonin secretion to regulate the large follicle steroidogenesis of rats

Yang, Chia‐Ning; Wu, Rick Sai-Chuen; Wu, Cheng-Hsuan; Lin, Theodore R.; Tsai, Horng‐Der

doi:10.1016/j.tjog.2014.10.007

Cited by 8 publications

(3 citation statements)

References 30 publications

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“…On one hand, it may be due to the inhibition of the hypothalamic-pituitary-adrenal (HPG) axis caused by elevated corticosteroids under certain stress conditions [24]. On the other hand, it was suggested that sleep deprivation could activate the serotonergic nervous system and promote the release of serotonin, therefore, serotonin suppressed FSH-induced estradiol release in large follicles [39]. Because serotonin inhibits estradiol production and decreases the expression of STAR protein in large follicles, estradiol concentrations may decrease during sleep deprivation [39].…”

Section: Discussionmentioning

confidence: 99%

Maternal total sleep deprivation causes oxidative stress and mitochondrial dysfunction in oocytes associated with fertility decline in mice

Yi,

Liang,

Zhou

et al. 2024

Preprint

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Previous studies have shown sleep deprivation has an impact on several aspects of health and disease. Sleep deprivation suppresses melatonin production and excessive HPA activation in women, which may reduce the chances of fertility. However, little is known about how and by what relevant mechanisms it affects female fertility. In this study, female mice underwent 72 hours of total sleep deprivation (TSD) caused by rotating wheel or 2 different controls: a stationary wheel, or forced movement at night. Even though, there was no evident anomaly of natural ovulation, the TSD female mice showed impaired early embryo development . Overall levels of estrogen and FSH were lower throughout the estrus cycle (especially in proestrus). RNA Sequencing (RNA-Seq) was used to discover differentially expressed genes (DEGs) that might be involved in oocyte quality after TSD. A total of 42 genes showed significant differential expression in GV oocytes after TSD. These included genes such asUsmg5, Atp5k, Ccnd2andTpm3, which were enriched in gene ontology terms of mitochondrial protein complex, oxidoreductase activity, cell division, cell cycle G1/S phase transition, as well as others. The increased concentrations of reactive oxygen species (ROS) in germinal vesicle (GV) and metaphase II (MII) oocytes from TSD mice were observed, which might be induced by impaired mitochondrial function caused by TSD. The GV oocytes displayed increased mitochondrial DNA (mtDNA) copy number and a significant transient increase in inner mitochondrial membrane potential (△ψm) from the TSD mice probably due to compensatory effect. In contrast, MII oocytes in the TSD group showed a decrease in the mtDNA copy number and a lower △ ψm compared with the controls. Furthermore, abnormal distribution of mitochondria in the GV and MII oocytes was also observed in TSD mice, suggesting mitochondrial dysfunction. In addition, abnormal spindle and abnormal arrangement of chromosomes in MII oocytes were markedly increased in the TSD mice compared with the control mice. In conclusion, our results suggest that TSD significantly alters the oocyte transcriptome, contributing to oxidative stress and disrupted mitochondrial function, which then resulted in oocyte defects and impaired early embryo development in female mice.

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Section: Discussionmentioning

confidence: 99%

Maternal total sleep deprivation causes oxidative stress and mitochondrial dysfunction in oocytes associated with fertility decline in mice

Yi,

Liang,

Zhou

et al. 2024

Preprint

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“…When ketanserin, an inhibitor of 5‐HT 2 receptors, is present in culture medium for the follicles, production of progesterone and testosterone decreases, and this effect is reversed by addition of pregnenolone (Tanaka et al., 1993 ). In contrast, addition of 5‐HT to the medium modifies expression of the protein that mobilizes cholesterol to the mitochondria, the steroidogenic acute regulatory protein (StAR), and the production of estradiol (Yang et al., 2015 ).…”

Section: Discussionmentioning

confidence: 99%

The differential sensitivity of the hypothalamic–hypophysial–ovarian axis to 5‐hydroxytryptophan alters the secretion of estradiol

Monroy,

Cortés,

Domínguez

et al. 2023

Experimental Physiology

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Serotonin [5‐hydroxytryptamine (5‐HT)] modulates ovarian function. The precursor of 5‐HT, 5‐hydroxytryptophan (5‐HTP), has been used to treat depression. However, the effects of 5‐HTP on ovarian and reproductive physiology remain unknown. In this research, we analysed the impact of 5‐HTP on the monoaminergic system and its interactions with the reproductive axis and ovarian estradiol secretion when administered by distinct routes. Female rats 30 days of age were injected with 5‐HTP i.p. (100 mg/kg), into the ovarian bursa (1.5 µg/40 µL) or into the median raphe nucleus (20 µg/2.5 µL) and were killed 60 or 120 min after injection. As controls, we used rats of the same age injected with vehicle (0.9% NaCl). Monoamine, gonadotrophin and steroid ovarian hormone concentrations were measured. The injection of 5‐HTP either i.p. or directly into the ovarian bursa increased the concentrations of 5‐HT and the metabolite 5‐hydroxyindole‐3‐acetic acid in the ovary. For both routes of administration, the serum concentration of estradiol increased. After i.p. injection of 5‐HTP, the concentrations of luteinizing hormone were decreased and follicle‐stimulating hormone increased after 120 min. Micro‐injection of 5‐HTP into the median raphe nucleus increased the concentrations of 5‐HT in the anterior hypothalamus and dopamine in the medial hypothalamus after 120 min. Our results suggest that the administration of 5‐HTP either i.p. or directly into the ovarian bursa enhances ovarian estradiol secretion.

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“…Partial similarity with this study’s results about the association of elevated T with serum serotonin in the SD group was observed in animal models. Although elevated serum serotonin levels were noted in sleep deprivation–induced rats ( Yang, Wu, Wu, Lin, & Tsai, 2015 ), luteinizing hormone (LH) secretion was inhibited. Lopez-Rodriguez, Wilson, Maidment, Poland, and Engel Jr. (2003) reported that sleep deprivation increased extracellular serotonin in the rat hippocampus.…”

Section: Discussionmentioning

confidence: 99%

Associations Between Sleep Deprivation and Salivary Testosterone Levels in Male University Students: A Prospective Cohort Study

et al. 2017

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Sleep deprivation is a common health problem that is growing rapidly worldwide and it is associated with short- and long-term impacts on health. The aim of this study was to detect potential predictors of salivary testosterone (sT) association with sleep deprivation in Arab male university students. In this prospective cohort study, 77 university male students in the age range of 18 to 26 years were divided into two groups, sleep-deprived (SD) participants and non-sleep-deprived (NSD) participants. Sleep deprivation was defined as sleeping less than 5 hr per night. Blood samples and sT were collected from fasting participants to measure serum levels of glucose, lipid profile, leptin, serotonin, sT, and body mass index (BMI) values. The multiple linear correlation model of high-density lipoprotein cholesterol (HDL-C), BMI, and serotonin was positively correlated with sT (r = .977, p < .05) in the SD group. No correlations were identified with sT in the NSD group. In the SD study group, the multiple linear regression model of HDL-C, BMI, and serotonin was significantly influenced by sT (R² = .955, p < .05). These predictors together explained approximately 96% of the variance in sT levels in the SD study group. No predictive variables for sT were reported in the NSD group. Results indirectly confirmed the presence of a positive association between sT and sleep deprivation in young men. This association is mediated by three factors, HDL-C, BMI, and serum serotonin, which are collectively considered as part of a significant physiological adaptation to sleep deprivation in young men.

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Sleep deprivation enhances peripheral serotonin secretion to regulate the large follicle steroidogenesis of rats

Abstract: These findings suggest that decreased serum estradiol concentrations in SD rats may be the result of serotonin-related inhibition of estradiol production and decreased large follicle expression of StAR protein.

Cited by 8 publications

References 30 publications

Maternal total sleep deprivation causes oxidative stress and mitochondrial dysfunction in oocytes associated with fertility decline in mice

Maternal total sleep deprivation causes oxidative stress and mitochondrial dysfunction in oocytes associated with fertility decline in mice

The differential sensitivity of the hypothalamic–hypophysial–ovarian axis to 5‐hydroxytryptophan alters the secretion of estradiol

Associations Between Sleep Deprivation and Salivary Testosterone Levels in Male University Students: A Prospective Cohort Study

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