دورية أكاديمية
أعرض في EDS

Circadian regulation of mTORC1 signaling via Per2 dependent mechanism disrupts folliculogenesis and oocyte maturation in female mice.

التفاصيل البيبلوغرافية
العنوان: Circadian regulation of mTORC1 signaling via Per2 dependent mechanism disrupts folliculogenesis and oocyte maturation in female mice.
المؤلفون: Bora G; Department of Histology and Embryology, Yeditepe University Faculty of Medicine, 34755, İstanbul, Turkey., Önel T; Department of Histology and Embryology, Yeditepe University Faculty of Medicine, 34755, İstanbul, Turkey., Yıldırım E; Department of Histology and Embryology, Yeditepe University Faculty of Medicine, 34755, İstanbul, Turkey., Yaba A; Department of Histology and Embryology, Yeditepe University Faculty of Medicine, 34755, İstanbul, Turkey. aylinyaba@hotmail.com.
المصدر: Journal of molecular histology [J Mol Histol] 2023 Jun; Vol. 54 (3), pp. 217-229. Date of Electronic Publication: 2023 May 10.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Netherlands Country of Publication: Netherlands NLM ID: 101193653 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1567-2387 (Electronic) Linking ISSN: 15672379 NLM ISO Abbreviation: J Mol Histol Subsets: MEDLINE
أسماء مطبوعة: Publication: Dordrecht, The Netherlands : Springer Netherlands
Original Publication: Dordrecht, The Netherlands : Kluwer Academic Publishers, 2004-
مواضيع طبية MeSH: Mechanistic Target of Rapamycin Complex 1* , Oocytes* , Period Circadian Proteins*/genetics , Period Circadian Proteins*/metabolism, Animals ; Female ; Mice ; Mammals/metabolism ; Ribosomal Protein S6 Kinases, 70-kDa/metabolism ; Signal Transduction ; TOR Serine-Threonine Kinases/metabolism
مستخلص: mTOR (mammalian target of Rapamycin) is an important signaling pathway involved in several crucial ovarian functions including folliculogenesis and oocyte maturation. The circadian rhythm regulates multiple physiological processes and PER2 is one of the core circadian rhythm components. mTOR is regulated by the circadian clock and in turn, the rhythmic mTOR activities strengthen the clock function. Our current study aims to investigate a possible interconnection between the circadian clock and the mTORC1 signaling pathway in folliculogenesis and oocyte maturation. Here we demonstrate that the circadian system regulates mTORC1 signaling via Per2 dependent mechanism in the mouse ovary. To investigate the effect of constant light on ovarian and oocyte morphology, animals were housed 12:12 h L:D group in standard lightening conditions and the 12:12 h L:L group in constant light for one week. Food intake and body weight changes were measured. Ovarian morphology, follicle counting, and oocyte aging were evaluated. Afterward, western blot for mTOR, p-mTOR, p70S6K, p-p70S6K, PER2, and Caspase-3 protein levels was performed. The study demonstrated that circadian rhythm disruption caused an alteration in their food intake and decrease in primordial follicle numbers and an increase in the number of atretic follicles. It caused an increase in oxidative stress and a decrease in ZP3 expression in oocytes. Decreased protein levels of mTOR, p-mTOR, p70S6K, and PER2 were shown. The results showed that the circadian clock regulates mTORC1 through PER2 dependent mechanism and that decreased mTORC1 activity can contribute to premature aging of mouse ovary. In conclusion, these results suggest that the circadian clock may control ovarian aging by regulating mTOR signaling pathway through Per2 expression.
(© 2023. The Author(s), under exclusive licence to Springer Nature B.V.)
References: Arble DM et al (2009) Circadian timing of food intake contributes to weight gain. Obes (Silver Spring) 17(11):2100–2102. (PMID: 10.1038/oby.2009.264)
Brainard J et al (2015) Health implications of disrupted circadian rhythms and the potential for daylight as therapy. Anesthesiology 122(5):1170–1175. (PMID: 2563559210.1097/ALN.0000000000000596)
Cao R (2018) mTOR Signaling, Translational Control, and the circadian clock. Front Genet 9:367. (PMID: 30250482613929910.3389/fgene.2018.00367)
Castillo MR et al (2004) Entrainment of the master circadian clock by scheduled feeding. Am J Physiol Regul Integr Comp Physiol 287(3):R551–555. (PMID: 1515528010.1152/ajpregu.00247.2004)
Cissé YM et al (2017) Effects of Dim Light at Night on Food Intake and Body Mass in developing mice. Front Neurosci 11:294. (PMID: 28603481544516310.3389/fnins.2017.00294)
Fahrenkrug J et al (2006) Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147(8):3769–3776. (PMID: 1667551710.1210/en.2006-0305)
Fonken LK, Nelson RJ (2014) The effects of light at night on circadian clocks and metabolism. Endocr Rev 35(4):648–670. (PMID: 2467319610.1210/er.2013-1051)
Fonken LK et al (2010) Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci 107(43):18664–18669. (PMID: 20937863297298310.1073/pnas.1008734107)
Fonken LK et al (2013) Dim light at night disrupts molecular circadian rhythms and increases body weight. J Biol Rhythms 28(4):262–271. (PMID: 23929553403330510.1177/0748730413493862)
Ford EA et al (2020) Advances in human primordial follicle activation and premature ovarian insufficiency. Reproduction 159(1):R15–r29. (PMID: 3137681410.1530/REP-19-0201)
Guo J et al (2018) Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice. Proc Natl Acad Sci 115(23):E5326–E5333. (PMID: 29784807600335710.1073/pnas.1800352115)
Hepler C et al (2022) Time-restricted feeding mitigates obesity through adipocyte thermogenesis. Science 378(6617):276–284. (PMID: 3626481110.1126/science.abl8007)
Herta AC et al (2018) In vitro follicle culture in the context of IVF. Reproduction 156(1):F59–f73. (PMID: 2998058410.1530/REP-18-0173)
Holmes MM, Mistlberger RE (2000) Food anticipatory activity and photic entrainment in food-restricted BALB/c mice. Physiol Behav 68(5):655–666. (PMID: 1076489510.1016/S0031-9384(99)00231-0)
Jain MV et al (2013) Interconnections between apoptotic, autophagic and necrotic pathways: implications for cancer therapy development. J Cell Mol Med 17(1):12–29. (PMID: 23301705382313410.1111/jcmm.12001)
Jiao ZX et al (2012) Age-associated alteration of oocyte-specific gene expression in polar bodies: potential markers of oocyte competence. Fertil Steril 98(2):480–486. (PMID: 22633262340930210.1016/j.fertnstert.2012.04.035)
Jiao X et al (2018) Molecular Genetics of premature ovarian insufficiency. Trends Endocrinol Metab 29(11):795–807. (PMID: 3007869710.1016/j.tem.2018.07.002)
Kennaway DJ (2005) The role of circadian rhythmicity in reproduction. Hum Reprod Update 11(1):91–101. (PMID: 1556969810.1093/humupd/dmh054)
Lananna BV, Musiek ES (2020) The wrinkling of time: aging, inflammation, oxidative stress, and the circadian clock in neurodegeneration. Neurobiol Dis 139:104832. (PMID: 32179175772787310.1016/j.nbd.2020.104832)
Liu J et al (2018) The role of mTOR in ovarian Neoplasms, polycystic ovary syndrome, and ovarian aging. 31(6):891–898.
Meng L et al (2018) Preantral follicular atresia occurs mainly through autophagy, while antral follicles degenerate mostly through apoptosis. Biol Reprod 99(4):853–863. (PMID: 29767707)
Miao YL et al (2009) Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update 15(5):573–585. (PMID: 1942963410.1093/humupd/dmp014)
Miller BH, Takahashi JS (2013) Central circadian control of female reproductive function. Front Endocrinol (Lausanne) 4:195. (PMID: 24478756)
Mills J, Kuohung W (2019) Impact of circadian rhythms on female reproduction and infertility treatment success. Curr Opin Endocrinol Diabetes Obes 26(6):317–321. (PMID: 3164447010.1097/MED.0000000000000511)
Myers M et al (2004) Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127(5):569–580. (PMID: 1512901210.1530/rep.1.00095)
Palaniappan M, Menon KM (2012) Luteinizing hormone/human chorionic gonadotropin-mediated activation of mTORC1 signaling is required for androgen synthesis by theca-interstitial cells. Mol Endocrinol 26(10):1732–1742. (PMID: 22827930345822410.1210/me.2012-1106)
Percie du Sert N et al (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. 18(7). e3000410.
Pickel L, Sung HK (2020) Feeding Rhythms and the circadian regulation of metabolism. Front Nutr 7:39. (PMID: 32363197718203310.3389/fnut.2020.00039)
Prasad S et al (2016) Impact of stress on oocyte quality and reproductive outcome. J Biomed Sci 23:36. (PMID: 27026099481265510.1186/s12929-016-0253-4)
Ramanathan C et al (2018) mTOR signaling regulates central and peripheral circadian clock function. 14(5):e1007369.
Reinke H, Asher G (2019) Crosstalk between metabolism and circadian clocks. 20(4):227–241.
Richards J, Gumz ML (2013) Mechanism of the circadian clock in physiology. Am J Physiol Regul Integr Comp Physiol 304(12):R1053–1064. (PMID: 23576606407389110.1152/ajpregu.00066.2013)
Sacks D et al (2018) Multisociety Consensus Quality Improvement revised Consensus Statement for Endovascular Therapy of Acute ischemic stroke. Int J Stroke 13(6):612–632. (PMID: 29786478)
Sellix MT, Menaker M (2010) Circadian clocks in the ovary. Trends Endocrinol Metab 21(10):628–636. (PMID: 20599392294946410.1016/j.tem.2010.06.002)
Shaw E et al (2019) Temporal pattern of eating in night shift workers. Chronobiol Int 36(12):1613–1625. (PMID: 3149523210.1080/07420528.2019.1660358)
Stangherlin A, Reddy AB (2013) Regulation of circadian clocks by redox homeostasis. J Biol Chem 288(37):26505–26511. (PMID: 23861436377219810.1074/jbc.R113.457564)
Sudo M et al (2003) Constant light housing attenuates circadian rhythms of mPer2 mRNA and mPER2 protein expression in the suprachiasmatic nucleus of mice. Neuroscience 121(2):493–499. (PMID: 1452200810.1016/S0306-4522(03)00457-3)
Turek FW et al (2005) Obesity and metabolic syndrome in circadian clock mutant mice. Science 308(5724):1043–1045. (PMID: 15845877376450110.1126/science.1108750)
Vollenhoven B, Hunt S (2018) Ovarian ageing and the impact on female fertility. F1000Res, p 7.
Wang J et al (2016) Bridges between mitochondrial oxidative stress, ER stress and mTOR signaling in pancreatic β cells. Cell Signal 28(8):1099–1104. (PMID: 2718518810.1016/j.cellsig.2016.05.007)
Wang Z et al (2020) The circadian rhythm and core gene Period2 regulate the chemotherapy effect and multidrug resistance of ovarian cancer through the PI3K signaling pathway.Biosci Rep, 40(11).
Wu R et al (2019) The circadian protein Period2 suppresses mTORC1 activity via recruiting Tsc1 to mTORC1 complex. Cell Metab 29(3):653–667e656. (PMID: 3052774210.1016/j.cmet.2018.11.006)
Yaba A, Demir N (2012) The mechanism of mTOR (mammalian target of rapamycin) in a mouse model of polycystic ovary syndrome (PCOS). J Ovarian Res 5(1):38. (PMID: 23185989353852810.1186/1757-2215-5-38)
Yaba A et al (2008) A putative mitotic checkpoint dependent on mTOR function controls cell proliferation and survival in ovarian granulosa cells. Reprod Sci 15(2):128–138. (PMID: 1827694910.1177/1933719107312037)
Yaba A et al (2015) Expression of CCM2 and CCM3 during mouse gonadogenesis. J Assist Reprod Genet 32(10):1497–1507. (PMID: 26386873461591910.1007/s10815-015-0559-2)
Yang S et al (2009) The role of mPer2 clock gene in glucocorticoid and feeding rhythms. Endocrinology 150(5):2153–2160. (PMID: 19179447267190110.1210/en.2008-0705)
Yu J et al (2011) mTOR controls ovarian follicle growth by regulating granulosa cell proliferation.PLoS One, 6(7), e21415.
Zhang XM et al (2013) Rapamycin preserves the follicle pool reserve and prolongs the ovarian lifespan of female rats via modulating mTOR activation and sirtuin expression. Gene 523(1):82–87. (PMID: 2356683710.1016/j.gene.2013.03.039)
Zheng Y et al (2019) Loss-of-function mutations with circadian rhythm regulator Per1/Per2 lead to premature ovarian insufficiency†. Biol Reprod 100(4):1066–1072. (PMID: 3045254610.1093/biolre/ioy245)
فهرسة مساهمة: Keywords: Circadian rhythm; Ovarian aging; PER2; mTORC1
المشرفين على المادة: EC 2.7.11.1 (Mechanistic Target of Rapamycin Complex 1)
0 (Per2 protein, mouse)
0 (Period Circadian Proteins)
EC 2.7.11.1 (Ribosomal Protein S6 Kinases, 70-kDa)
EC 2.7.11.1 (TOR Serine-Threonine Kinases)
تواريخ الأحداث: Date Created: 20230510 Date Completed: 20230605 Latest Revision: 20230704
رمز التحديث: 20231215
DOI: 10.1007/s10735-023-10126-9
PMID: 37162693
قاعدة البيانات: MEDLINE
الوصف
تدمد:1567-2387
DOI:10.1007/s10735-023-10126-9