{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T19:12:39Z","timestamp":1783105959348,"version":"3.54.6"},"reference-count":127,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2023,3,6]],"date-time":"2023-03-06T00:00:00Z","timestamp":1678060800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,5,10]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Sirtuin 1 (SIRT1) is a nicotinamide adenine dinucleotide\u2013dependent deacetylase that modifies gene expression through histone deacetylation. It also deacetylates nonhistone substrates, e.g., tumor suppressor p53, NOS3, HIF1A, NFKB, FOXO3a, PGC-1\u03b1, and PPAR\u03b3. Consequently, it regulates a wide range of physiological functions including cell cycle control, energy expenditure, oxidative stress response, apoptosis, and aging. SIRT1 is expressed in ovarian granulosa cells (GCs) of various species including humans at different stages of the reproductive cycle. The importance of SIRT1 in female reproduction is supported by the findings that SIRT1-knockout mice exhibit defects in reproductive tissue development. These mice were found to have a thin-walled uterus, small ovaries, with follicles present but no corpora lutea. This review aims to provide state-of-the-art information on SIRT1\u2019s mode of action and its roles in human granulosa-lutein cells and GCs from other species where data are available. It also discusses the overlapping actions of SIRT1 and human chorionic gonadotropin on the production of critical GC-borne factors.<\/jats:p>","DOI":"10.1093\/biolre\/ioad026","type":"journal-article","created":{"date-parts":[[2023,3,7]],"date-time":"2023-03-07T19:05:47Z","timestamp":1678215947000},"page":"720-730","source":"Crossref","is-referenced-by-count":11,"title":["Divergent roles of sirtuin 1 in human granulosa-lutein cells: similarities to human chorionic gonadotropin"],"prefix":"10.1093","volume":"108","author":[{"given":"Rina","family":"Meidan","sequence":"first","affiliation":[{"name":"Department of Animal Sciences , The Robert H. Smith Faculty of Agriculture, Food and Environment, , Rehovot , Israel"},{"name":"The Hebrew University of Jerusalem , The Robert H. Smith Faculty of Agriculture, Food and Environment, , Rehovot , Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magdalena","family":"Szymanska","sequence":"additional","affiliation":[{"name":"Department of Animal Sciences , The Robert H. Smith Faculty of Agriculture, Food and Environment, , Rehovot , Israel"},{"name":"The Hebrew University of Jerusalem , The Robert H. Smith Faculty of Agriculture, Food and Environment, , Rehovot , Israel"},{"name":"Department of Hormonal Action Mechanisms, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences , Olsztyn , Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,3,6]]},"reference":[{"key":"2023051502250789700_ref1","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1210\/me.2007-0246","article-title":"Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway","volume":"22","author":"Panigone","year":"2008","journal-title":"Mol Endocrinol"},{"key":"2023051502250789700_ref2","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.mce.2005.01.004","article-title":"Ovulation: new factors that prepare the oocyte for fertilization","volume":"234","author":"Richards","year":"2005","journal-title":"Mol Cell Endocrinol"},{"key":"2023051502250789700_ref3","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1172\/JCI41350","article-title":"The ovary: basic biology and clinical implications","volume":"120","author":"Richards","year":"2010","journal-title":"J Clin Invest"},{"key":"2023051502250789700_ref4","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1530\/REP-14-0337","article-title":"Regulation of ovulatory genes in bovine granulosa cells: lessons from siRNA silencing of PTGS2","volume":"149","author":"Shrestha","year":"2015","journal-title":"Reproduction"},{"key":"2023051502250789700_ref5","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1093\/humupd\/dmh032","article-title":"Cyclooxygenase-2 and its role in ovulation: a 2004 account","volume":"10","author":"Sirois","year":"2004","journal-title":"Hum Reprod Update"},{"key":"2023051502250789700_ref6","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.repbio.2013.08.002","article-title":"Endocrine and local control of the primate corpus luteum","volume":"13","author":"Stouffer","year":"2013","journal-title":"Reprod Biol"},{"key":"2023051502250789700_ref7","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1002\/mrd.20878","article-title":"Effect of local neutralization of basic fibroblast growth factor or vascular endothelial growth factor by a specific antibody on the development of the corpus luteum in the cow","volume":"75","author":"Yamashita","year":"2008","journal-title":"Mol Reprod Dev"},{"key":"2023051502250789700_ref8","doi-asserted-by":"crossref","first-page":"e42406","DOI":"10.1371\/journal.pone.0042406","article-title":"The effect of gonadotropin on glucose transport and apoptosis in rat ovary","volume":"7","author":"Zhang","year":"2012","journal-title":"PLoS One"},{"key":"2023051502250789700_ref9","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1530\/REP-14-0409","article-title":"HIF1A-dependent increase in endothelin 2 levels in granulosa cells: role of hypoxia, LH\/cAMP, and reactive oxygen species","volume":"149","author":"Yalu","year":"2015","journal-title":"Reproduction"},{"key":"2023051502250789700_ref10","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.jri.2009.04.007","article-title":"hCG and hyperglycosylated hCG in the establishment and evolution of hemochorial placentation","volume":"82","author":"Cole","year":"2009","journal-title":"J Reprod Immunol"},{"key":"2023051502250789700_ref11","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1186\/1477-7827-8-102","article-title":"Biological functions of hCG and hCG-related molecules","volume":"8","author":"Cole","year":"2010","journal-title":"Reprod Biol Endocrinol"},{"key":"2023051502250789700_ref12","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.tem.2018.02.012","article-title":"Endocrine, paracrine, and autocrine signaling pathways that regulate ovulation","volume":"29","author":"Richards","year":"2018","journal-title":"Trends Endocrinol Metab"},{"key":"2023051502250789700_ref13","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1016\/B978-0-12-397175-3.00020-X","volume-title":"Knobil and Neill\u2019s Physiology of Reproduction (Fourth Edition)","author":"Hunzicker-Dunn","year":"2015"},{"key":"2023051502250789700_ref14","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1146\/annurev-physiol-022516-034102","article-title":"Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle","volume":"79","author":"Jaffe","year":"2017","journal-title":"Annu Rev Physiol"},{"key":"2023051502250789700_ref15","doi-asserted-by":"crossref","first-page":"2784","DOI":"10.1210\/me.2006-0093","article-title":"A novel pathway involving progesterone receptor, endothelin-2, and endothelin receptor B controls ovulation in mice","volume":"20","author":"Palanisamy","year":"2006","journal-title":"Mol Endocrinol"},{"key":"2023051502250789700_ref16","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.1210\/en.2009-0767","article-title":"Induction of endothelin-2 expression by luteinizing hormone and hypoxia: possible role in bovine corpus luteum formation","volume":"151","author":"Klipper","year":"2010","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref17","doi-asserted-by":"crossref","first-page":"e96115","DOI":"10.1371\/journal.pone.0096115","article-title":"Loss of function of endothelin-2 leads to reduced ovulation and CL formation","volume":"9","author":"Cacioppo","year":"2014","journal-title":"PLoS One"},{"key":"2023051502250789700_ref18","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1071\/RD12139","article-title":"The role of hypoxia-induced genes in ovarian angiogenesis","volume":"25","author":"Meidan","year":"2013","journal-title":"Reprod Fertil Dev"},{"key":"2023051502250789700_ref19","doi-asserted-by":"crossref","DOI":"10.3390\/ijms22158216","article-title":"Reduced endothelin-2 and hypoxic signaling pathways in granulosa-lutein cells of PCOS women","volume":"22","author":"Szymanska","year":"2021","journal-title":"Int J Mol Sci"},{"key":"2023051502250789700_ref20","doi-asserted-by":"crossref","first-page":"1770","DOI":"10.1210\/en.2005-1228","article-title":"Endothelin-2 in ovarian follicle rupture","volume":"147","author":"Ko","year":"2006","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref21","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.repbio.2020.07.010","article-title":"The cAMP pathway promotes sirtuin-1 expression in human granulosa-lutein cells","volume":"20","author":"Szymanska","year":"2020","journal-title":"Reprod Biol"},{"key":"2023051502250789700_ref22","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1016\/j.molcel.2011.12.005","article-title":"The cAMP\/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+)","volume":"44","author":"Gerhart-Hines","year":"2011","journal-title":"Mol Cell"},{"key":"2023051502250789700_ref23","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1038\/embor.2011.151","article-title":"CREB and ChREBP oppositely regulate SIRT1 expression in response to energy availability","volume":"12","author":"Noriega","year":"2011","journal-title":"EMBO Rep"},{"key":"2023051502250789700_ref24","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1016\/j.chembiol.2008.09.009","article-title":"Mechanisms and molecular probes of sirtuins","volume":"15","author":"Smith","year":"2008","journal-title":"Chem Biol"},{"key":"2023051502250789700_ref25","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1007\/s10059-013-0130-x","article-title":"Do sirtuins promote mammalian longevity? A critical review on its relevance to the longevity effect induced by calorie restriction","volume":"35","author":"Park","year":"2013","journal-title":"Mol Cells"},{"key":"2023051502250789700_ref26","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.tem.2013.12.001","article-title":"SIRT1 and other sirtuins in metabolism","volume":"25","author":"Chang","year":"2014","journal-title":"Trends Endocrinol Metab"},{"key":"2023051502250789700_ref27","doi-asserted-by":"crossref","first-page":"e76","DOI":"10.1371\/journal.pmed.0040076","article-title":"Calorie restriction increases muscle mitochondrial biogenesis in healthy humans","volume":"4","author":"Civitarese","year":"2007","journal-title":"PLoS Med"},{"key":"2023051502250789700_ref28","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.ccr.2009.11.023","article-title":"SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress","volume":"17","author":"Kim","year":"2010","journal-title":"Cancer Cell"},{"key":"2023051502250789700_ref29","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1007\/s10495-017-1386-y","article-title":"SIRT1 induces resistance to apoptosis in human granulosa cells by activating the ERK pathway and inhibiting NF-\u03baB signaling with anti-inflammatory functions","volume":"22","author":"Han","year":"2017","journal-title":"Apoptosis"},{"key":"2023051502250789700_ref30","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/1477-7827-10-14","article-title":"Resveratrol promotes expression of SIRT1 and StAR in rat ovarian granulosa cells: an implicative role of SIRT1 in the ovary","volume":"10","author":"Morita","year":"2012","journal-title":"Reprod Biol Endocrinol"},{"key":"2023051502250789700_ref31","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.anireprosci.2014.10.002","article-title":"Roles of SIRT1 in granulosa cell apoptosis during the process of follicular atresia in porcine ovary","volume":"151","author":"Zhao","year":"2014","journal-title":"Anim Reprod Sci"},{"key":"2023051502250789700_ref32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.freeradbiomed.2022.05.010","article-title":"Mitochondrial and glucose metabolic dysfunctions in granulosa cells induce impaired oocytes of polycystic ovary syndrome through Sirtuin 3","volume":"187","author":"Zhang","year":"2022","journal-title":"Free Radic Biol Med"},{"key":"2023051502250789700_ref33","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/j.fertnstert.2013.10.041","article-title":"Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization","volume":"101","author":"Wang","year":"2014","journal-title":"Fertil Steril"},{"key":"2023051502250789700_ref34","article-title":"Celastrol and melatonin modify SIRT1, SIRT6 and SIRT7 Gene Expression and Improve the Response of Human Granulosa-Lutein Cells to Oxidative Stress","volume":"10","author":"Mart\u00edn-Ram\u00edrez","year":"2021","journal-title":"Antioxidants (Basel)"},{"key":"2023051502250789700_ref35","article-title":"Effects of vinclozolin exposure on the expression and activity of SIRT1 and SIRT6 in the porcine ovary","volume":"70","author":"Gorczyca","year":"2019","journal-title":"J Physiol Pharmacol"},{"key":"2023051502250789700_ref36","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.niox.2013.04.001","article-title":"Role of SIRT1 and FOXO factors in eNOS transcriptional activation by resveratrol","volume":"32","author":"Xia","year":"2013","journal-title":"Nitric Oxide"},{"key":"2023051502250789700_ref37","doi-asserted-by":"crossref","first-page":"4614","DOI":"10.1038\/s41598-017-04847-7","article-title":"Identifying human SIRT1 substrates by integrating heterogeneous information from various sources","volume":"7","author":"Zhai","year":"2017","journal-title":"Sci Rep"},{"key":"2023051502250789700_ref38","doi-asserted-by":"crossref","first-page":"87","DOI":"10.14348\/molcells.2016.2318","article-title":"Sirt1 and the mitochondria","volume":"39","author":"Tang","year":"2016","journal-title":"Mol Cells"},{"key":"2023051502250789700_ref39","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1038\/nature02583","article-title":"Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma","volume":"429","author":"Picard","year":"2004","journal-title":"Nature"},{"key":"2023051502250789700_ref40","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.cmet.2007.08.014","article-title":"SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B","volume":"6","author":"Sun","year":"2007","journal-title":"Cell Metab"},{"key":"2023051502250789700_ref41","doi-asserted-by":"crossref","first-page":"e31","DOI":"10.1371\/journal.pbio.0040031","article-title":"Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells","volume":"4","author":"Bordone","year":"2006","journal-title":"PLoS Biol"},{"key":"2023051502250789700_ref42","doi-asserted-by":"crossref","first-page":"27628","DOI":"10.1074\/jbc.M805711200","article-title":"SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation","volume":"283","author":"Lan","year":"2008","journal-title":"J Biol Chem"},{"key":"2023051502250789700_ref43","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1093\/humupd\/dmy003","article-title":"Sirtuins in gamete biology and reproductive physiology: emerging roles and therapeutic potential in female and male infertility","volume":"24","author":"Tatone","year":"2018","journal-title":"Hum Reprod Update"},{"key":"2023051502250789700_ref44","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1128\/MCB.23.1.38-54.2003","article-title":"The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis","volume":"23","author":"McBurney","year":"2003","journal-title":"Mol Cell Biol"},{"key":"2023051502250789700_ref45","doi-asserted-by":"crossref","first-page":"R1","DOI":"10.1186\/bcr1632","article-title":"SirT1 modulates the estrogen-insulin-like growth factor-1 signaling for postnatal development of mammary gland in mice","volume":"9","author":"Li","year":"2007","journal-title":"Breast Cancer Res"},{"key":"2023051502250789700_ref46","doi-asserted-by":"crossref","first-page":"e13204","DOI":"10.1111\/acel.13204","article-title":"Sirt1 sustains female fertility by slowing age-related decline in oocyte quality required for post-fertilization embryo development","volume":"19","author":"Iljas","year":"2020","journal-title":"Aging Cell"},{"key":"2023051502250789700_ref47","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1007\/s00441-014-1940-7","article-title":"Interrelationships between sirtuin 1 and transcription factors p53 and NF-\u03baB (p50\/p65) in the control of ovarian cell apoptosis and proliferation","volume":"358","author":"Sirotkin","year":"2014","journal-title":"Cell Tissue Res"},{"key":"2023051502250789700_ref48","doi-asserted-by":"crossref","DOI":"10.1071\/RD18425","article-title":"Resveratrol directly affects ovarian cell sirtuin, proliferation, apoptosis, hormone release and response to follicle-stimulating hormone (FSH) and insulin-like growth factor I (IGF-I)","volume":"31","author":"Sirotkin","year":"2019","journal-title":"Reprod Fertil Dev"},{"key":"2023051502250789700_ref49","doi-asserted-by":"crossref","first-page":"2006","DOI":"10.1093\/humrep\/deu160","article-title":"SIRT1 signalling protects mouse oocytes against oxidative stress and is deregulated during aging","volume":"29","author":"Di Emidio","year":"2014","journal-title":"Hum Reprod"},{"key":"2023051502250789700_ref50","doi-asserted-by":"crossref","first-page":"8362","DOI":"10.18632\/aging.102324","article-title":"Mogroside V protects porcine oocytes from in vitro ageing by reducing oxidative stress through SIRT1 upregulation","volume":"11","author":"Nie","year":"2019","journal-title":"Aging (Albany NY)"},{"key":"2023051502250789700_ref51","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1186\/s12958-022-00970-x","article-title":"Diverse actions of sirtuin-1 on ovulatory genes and cell death pathways in human granulosa cells","volume":"20","author":"Sapuleni","year":"2022","journal-title":"Reprod Biol Endocrinol"},{"key":"2023051502250789700_ref52","doi-asserted-by":"crossref","DOI":"10.3390\/ijms22042047","article-title":"Sirtuin 1 and Sirtuin 3 in granulosa cell tumors","volume":"22","author":"Schmid","year":"2021","journal-title":"Int J Mol Sci"},{"key":"2023051502250789700_ref53","doi-asserted-by":"crossref","DOI":"10.1093\/biolre\/ioaa199","article-title":"Sirtuin-1 inhibits endothelin-2 expression in human granulosa-lutein cells via hypoxia inducible factor 1 alpha and epigenetic modifications\u2020","volume":"104","author":"Szymanska","year":"2021","journal-title":"Biol Reprod"},{"key":"2023051502250789700_ref54","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.livsci.2015.06.014","article-title":"Effect of SIRT1 on cellular apoptosis and steroidogenesis in bovine ovarian granulosa cells in vitro","volume":"180","author":"Tan","year":"2015","journal-title":"Livest Sci"},{"key":"2023051502250789700_ref55","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1071\/RD21069","article-title":"Resveratrol protects human luteinised granulosa cells against hydrogen peroxide-induced oxidative injury through the Sirt1","volume":"33","author":"Nie","year":"2021","journal-title":"Reprod Fertil Dev"},{"key":"2023051502250789700_ref56","first-page":"1923","article-title":"TOPK inhibition accelerates oxidative stress-induced granulosa cell apoptosis via the p53\/SIRT1 axis","volume":"46","author":"Park","year":"2020","journal-title":"Int J Mol Med"},{"key":"2023051502250789700_ref57","article-title":"Role of the SIRT1\/p53 regulatory axis in oxidative stress-mediated granulosa cell apoptosis","volume":"23","author":"Park","year":"2021","journal-title":"Mol Med Rep"},{"key":"2023051502250789700_ref58","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.reprotox.2022.03.007","article-title":"Inhibition of Sirtuin-1 hyperacetylates p53 and abrogates Sirtuin-1-p53 interaction in Cr(VI)-induced apoptosis in the ovary","volume":"109","author":"Sivakumar","year":"2022","journal-title":"Reprod Toxicol"},{"key":"2023051502250789700_ref59","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1038\/nature06261","article-title":"Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes","volume":"450","author":"Milne","year":"2007","journal-title":"Nature"},{"key":"2023051502250789700_ref60","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1038\/nature01960","article-title":"Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan","volume":"425","author":"Howitz","year":"2003","journal-title":"Nature"},{"key":"2023051502250789700_ref61","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/1752-0509-3-31","article-title":"Small molecule activators of SIRT1 replicate signaling pathways triggered by calorie restriction in vivo","volume":"3","author":"Smith","year":"2009","journal-title":"BMC Syst Biol"},{"key":"2023051502250789700_ref62","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.bbagrm.2010.06.005","article-title":"Sirtuin activators: designing molecules to extend life span","volume":"1799","author":"Camins","year":"2010","journal-title":"Biochim Biophys Acta"},{"key":"2023051502250789700_ref63","doi-asserted-by":"crossref","DOI":"10.3390\/molecules25194554","article-title":"The role of resveratrol in mammalian reproduction","volume":"25","author":"Pasquariello","year":"2020","journal-title":"Molecules"},{"key":"2023051502250789700_ref64","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1002\/biof.1032","article-title":"Sirtuin activators and inhibitors","volume":"38","author":"Villalba","year":"2012","journal-title":"Biofactors"},{"key":"2023051502250789700_ref65","doi-asserted-by":"crossref","first-page":"17187","DOI":"10.1074\/jbc.M501250200","article-title":"Mechanism of human SIRT1 activation by resveratrol","volume":"280","author":"Borra","year":"2005","journal-title":"J Biol Chem"},{"key":"2023051502250789700_ref66","doi-asserted-by":"crossref","DOI":"10.3390\/nu11010143","article-title":"Resveratrol and its human metabolites-effects on metabolic health and obesity","volume":"11","author":"Springer","year":"2019","journal-title":"Nutrients"},{"key":"2023051502250789700_ref67","doi-asserted-by":"crossref","DOI":"10.3390\/nu14142870","article-title":"Implications of resveratrol in obesity and insulin resistance: a state-of-the-art review","volume":"14","author":"Barber","year":"2022","journal-title":"Nutrients"},{"key":"2023051502250789700_ref68","doi-asserted-by":"crossref","first-page":"970","DOI":"10.5551\/jat.4333","article-title":"Resveratrol protects human endothelium from H(2)O(2)-induced oxidative stress and senescence via SirT1 activation","volume":"17","author":"Kao","year":"2010","journal-title":"J Atheroscler Thromb"},{"key":"2023051502250789700_ref69","doi-asserted-by":"crossref","first-page":"2654","DOI":"10.1002\/jcb.25868","article-title":"Resveratrol ameliorates palmitate-induced inflammation in skeletal muscle cells by attenuating oxidative stress and JNK\/NF-\u03baB pathway in a SIRT1-independent mechanism","volume":"118","author":"Sadeghi","year":"2017","journal-title":"J Cell Biochem"},{"key":"2023051502250789700_ref70","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.ejphar.2010.01.025","article-title":"Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice","volume":"633","author":"S\u00e1nchez-Fidalgo","year":"2010","journal-title":"Eur J Pharmacol"},{"key":"2023051502250789700_ref71","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1530\/JOE-17-0672","article-title":"SRT2104 attenuates diabetes-induced aortic endothelial dysfunction via inhibition of P53","volume":"237","author":"Wu","year":"2018","journal-title":"J Endocrinol"},{"key":"2023051502250789700_ref72","doi-asserted-by":"crossref","first-page":"147236","DOI":"10.1016\/j.brainres.2020.147236","article-title":"Sirt1 activator SRT2104 protects against oxygen-glucose deprivation\/reoxygenation-induced injury via regulating microglia polarization by modulating Sirt1\/NF-\u03baB pathway","volume":"1753","author":"Fu","year":"2021","journal-title":"Brain Res"},{"key":"2023051502250789700_ref73","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1007\/s10384-020-00731-6","article-title":"Axonal protection by a small molecule SIRT1 activator, SRT2104, with alteration of autophagy in TNF-induced optic nerve degeneration","volume":"64","author":"Kitaoka","year":"2020","journal-title":"Jpn J Ophthalmol"},{"key":"2023051502250789700_ref74","doi-asserted-by":"crossref","first-page":"1566","DOI":"10.1007\/s00125-017-4318-z","article-title":"Metformin: historical overview","volume":"60","author":"Bailey","year":"2017","journal-title":"Diabetologia"},{"key":"2023051502250789700_ref75","doi-asserted-by":"crossref","first-page":"657","DOI":"10.3389\/fendo.2018.00657","article-title":"Metformin is a direct SIRT1-activating compound: computational modeling and experimental validation","volume":"9","author":"Cuy\u00e0s","year":"2018","journal-title":"Front Endocrinol (Lausanne)"},{"key":"2023051502250789700_ref76","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/ncomms1001","article-title":"Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer","volume":"1","author":"Herranz","year":"2010","journal-title":"Nat Commun"},{"key":"2023051502250789700_ref77","first-page":"789","article-title":"Establishment and characterization of an estrogen-producing human ovarian granulosa tumor cell line","volume":"72","author":"Ishiwata","year":"1984","journal-title":"J Natl Cancer Inst"},{"key":"2023051502250789700_ref78","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1210\/endo.142.1.7862","article-title":"Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor","volume":"142","author":"Nishi","year":"2001","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref79","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1002\/ijc.2910530415","article-title":"Establishment and characterization of 7 ovarian carcinoma cell lines and one granulosa tumor cell line: growth features and cytogenetics","volume":"53","author":"Berg-Bakker","year":"1993","journal-title":"Int J Cancer"},{"key":"2023051502250789700_ref80","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.mce.2004.04.018","article-title":"Ovarian granulosa cell lines","volume":"228","author":"Havelock","year":"2004","journal-title":"Mol Cell Endocrinol"},{"key":"2023051502250789700_ref81","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/0303-7207(96)03835-X","article-title":"Long-term growth and steroidogenic potential of human granulosa-lutein cells immortalized with SV40 large T antigen","volume":"120","author":"Lie","year":"1996","journal-title":"Mol Cell Endocrinol"},{"key":"2023051502250789700_ref82","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1006\/gyno.2000.6084","article-title":"Characterization and tumorigenicity of human ovarian surface epithelial cells immortalized by SV40 large T antigen","volume":"81","author":"Nitta","year":"2001","journal-title":"Gynecol Oncol"},{"key":"2023051502250789700_ref83","first-page":"705","article-title":"Transformation of human granulosa cells with the E6 and E7 regions of human papillomavirus","volume":"78","author":"Rainey","year":"1994","journal-title":"J Clin Endocrinol Metab"},{"key":"2023051502250789700_ref84","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1093\/molehr\/8.1.48","article-title":"Establishment of FSH-responsive cell lines by transfection of pre-ovulatory human granulosa cells with mutated p53 (p53val135) and ha-ras genes","volume":"8","author":"Tajima","year":"2002","journal-title":"Mol Hum Reprod"},{"key":"2023051502250789700_ref85","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1530\/REP-17-0574","article-title":"miR-210 and GPD1L regulate EDN2 in primary and immortalized human granulosa-lutein cells","volume":"155","author":"Shrestha","year":"2018","journal-title":"Reproduction"},{"key":"2023051502250789700_ref86","doi-asserted-by":"crossref","first-page":"2190","DOI":"10.1093\/humrep\/dev175","article-title":"Transforming growth factor-\u03b21 up-regulates connexin43 expression in human granulosa cells","volume":"30","author":"Chen","year":"2015","journal-title":"Hum Reprod"},{"key":"2023051502250789700_ref87","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.ymgmr.2017.05.003","article-title":"Resveratrol attenuates triglyceride accumulation associated with upregulation of Sirt1 and lipoprotein lipase in 3T3-L1 adipocytes","volume":"12","author":"Imamura","year":"2017","journal-title":"Mol Genet Metab Rep"},{"key":"2023051502250789700_ref88","doi-asserted-by":"crossref","first-page":"14105","DOI":"10.3390\/ijms140714105","article-title":"Resveratrol inhibits ionising irradiation-induced inflammation in MSCs by activating SIRT1 and limiting NLRP-3 inflammasome activation","volume":"14","author":"Fu","year":"2013","journal-title":"Int J Mol Sci"},{"key":"2023051502250789700_ref89","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.ebiom.2017.03.019","article-title":"Specific Sirt1 activator-mediated improvement in glucose homeostasis requires Sirt1-independent activation of AMPK","volume":"18","author":"Park","year":"2017","journal-title":"EBioMedicine"},{"key":"2023051502250789700_ref90","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.cell.2012.01.017","article-title":"Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases","volume":"148","author":"Park","year":"2012","journal-title":"Cell"},{"key":"2023051502250789700_ref91","doi-asserted-by":"crossref","first-page":"12012","DOI":"10.1038\/srep12012","article-title":"Cyclic AMP mimics the anti-ageing effects of calorie restriction by up-regulating Sirtuin","volume":"5","author":"Wang","year":"2015","journal-title":"Sci Rep"},{"key":"2023051502250789700_ref92","doi-asserted-by":"crossref","first-page":"39","DOI":"10.2174\/138161209787185841","article-title":"Cellular regulation of SIRT1","volume":"15","author":"Milner","year":"2009","journal-title":"Curr Pharm Des"},{"key":"2023051502250789700_ref93","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.toxrep.2014.06.006","article-title":"Excessive levels of diverse phytoestrogens can modulate steroidogenesis and cell migration of KGN human granulosa-derived tumor cells","volume":"1","author":"Solak","year":"2014","journal-title":"Toxicol Rep"},{"key":"2023051502250789700_ref94","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1126\/science.1231097","article-title":"Evidence for a common mechanism of SIRT1 regulation by allosteric activators","volume":"339","author":"Hubbard","year":"2013","journal-title":"Science"},{"key":"2023051502250789700_ref95","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1007\/978-1-4939-9434-2_8","article-title":"Molecular and cellular characterization of SIRT1 allosteric activators","volume":"1983","author":"Schultz","year":"2019","journal-title":"Methods Mol Biol"},{"key":"2023051502250789700_ref96","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1046\/j.1365-2613.1997.d01-247.x","article-title":"Regulation of angiogenesis by hypoxic stress: from solid tumours to the ovarian follicle","volume":"78","author":"Neeman","year":"1997","journal-title":"Int J Exp Pathol"},{"key":"2023051502250789700_ref97","doi-asserted-by":"crossref","first-page":"90","DOI":"10.2174\/092986712803413944","article-title":"Critical role of hypoxia sensor--HIF-1\u03b1 in VEGF gene activation. Implications for angiogenesis and tissue injury healing","volume":"19","author":"Ahluwalia","year":"2012","journal-title":"Curr Med Chem"},{"key":"2023051502250789700_ref98","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1139\/Y08-025","article-title":"Role of hypoxia in the regulation of periovulatory EDN2 expression in the mouse","volume":"86","author":"Na","year":"2008","journal-title":"Can J Physiol Pharmacol"},{"key":"2023051502250789700_ref99","doi-asserted-by":"crossref","first-page":"4304","DOI":"10.1073\/pnas.90.9.4304","article-title":"General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia","volume":"90","author":"Wang","year":"1993","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023051502250789700_ref100","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1182\/blood-2004-07-2958","article-title":"Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1","volume":"105","author":"Manalo","year":"2005","journal-title":"Blood"},{"key":"2023051502250789700_ref101","first-page":"215","article-title":"Expression and localization of hypoxia inducible factor-1alpha mRNA in the porcine ovary","volume":"69","author":"Boonyaprakob","year":"2005","journal-title":"Can J Vet Res"},{"key":"2023051502250789700_ref102","doi-asserted-by":"crossref","first-page":"3313","DOI":"10.1210\/en.2007-1649","article-title":"Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1alpha in the follicle and corpus luteum","volume":"149","author":"Duncan","year":"2008","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref103","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1093\/molehr\/gan040","article-title":"HCG up-regulates hypoxia inducible factor-1 alpha in luteinized granulosa cells: implications for the hormonal regulation of vascular endothelial growth factor a in the human corpus luteum","volume":"14","author":"Driesche","year":"2008","journal-title":"Mol Hum Reprod"},{"key":"2023051502250789700_ref104","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1262\/jrd.09-162E","article-title":"Hypoxia is important for establishing vascularization during corpus luteum formation in cattle","volume":"56","author":"Nishimura","year":"2010","journal-title":"J Reprod Dev"},{"key":"2023051502250789700_ref105","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.mce.2010.06.008","article-title":"Hormonally regulated follicle differentiation and luteinization in the mouse is associated with hypoxia inducible factor activity","volume":"327","author":"Tam","year":"2010","journal-title":"Mol Cell Endocrinol"},{"key":"2023051502250789700_ref106","doi-asserted-by":"crossref","first-page":"3392","DOI":"10.1210\/en.2008-0948","article-title":"Signaling by hypoxia-inducible factors is critical for ovulation in mice","volume":"150","author":"Kim","year":"2009","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref107","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1038\/35001622","article-title":"Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase","volume":"403","author":"Imai","year":"2000","journal-title":"Nature"},{"key":"2023051502250789700_ref108","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nature08197","article-title":"Recent progress in the biology and physiology of sirtuins","volume":"460","author":"Finkel","year":"2009","journal-title":"Nature"},{"key":"2023051502250789700_ref109","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.mce.2016.08.010","article-title":"Low oxygen level increases proliferation and metabolic changes in bovine granulosa cells","volume":"437","author":"Shiratsuki","year":"2016","journal-title":"Mol Cell Endocrinol"},{"key":"2023051502250789700_ref110","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1016\/j.molcel.2010.05.023","article-title":"Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha","volume":"38","author":"Lim","year":"2010","journal-title":"Mol Cell"},{"key":"2023051502250789700_ref111","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.bbrc.2015.04.119","article-title":"SIRT1 deacetylates and stabilizes hypoxia-inducible factor-1\u03b1 (HIF-1\u03b1) via direct interactions during hypoxia","volume":"462","author":"Joo","year":"2015","journal-title":"Biochem Biophys Res Commun"},{"key":"2023051502250789700_ref112","doi-asserted-by":"crossref","first-page":"e33433","DOI":"10.1371\/journal.pone.0033433","article-title":"Inhibition of SIRT1 impairs the accumulation and transcriptional activity of HIF-1\u03b1 protein under hypoxic conditions","volume":"7","author":"Laemmle","year":"2012","journal-title":"PLoS One"},{"key":"2023051502250789700_ref113","doi-asserted-by":"crossref","first-page":"e25","DOI":"10.1111\/odi.12275","article-title":"Cyclic nucleotide phosphodiesterases: important signaling modulators and therapeutic targets","volume":"21","author":"Ahmad","year":"2015","journal-title":"Oral Dis"},{"key":"2023051502250789700_ref114","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1152\/physrev.1995.75.4.725","article-title":"Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms","volume":"75","author":"Beavo","year":"1995","journal-title":"Physiol Rev"},{"key":"2023051502250789700_ref115","doi-asserted-by":"crossref","first-page":"256","DOI":"10.4161\/adip.21158","article-title":"Metabolic benefits of inhibiting cAMP-PDEs with resveratrol","volume":"1","author":"Chung","year":"2012","journal-title":"Adipocyte"},{"key":"2023051502250789700_ref116","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1210\/me.2005-0504","article-title":"Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor","volume":"20","author":"Shimada","year":"2006","journal-title":"Mol Endocrinol"},{"key":"2023051502250789700_ref117","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1530\/rep.1.00798","article-title":"Changes in fibroblast growth factor 2 and its receptors in bovine follicles before and after GnRH application and after ovulation","volume":"131","author":"Berisha","year":"2006","journal-title":"Reproduction"},{"key":"2023051502250789700_ref118","doi-asserted-by":"crossref","first-page":"3482","DOI":"10.1210\/en.2018-00527","article-title":"The cAMP-EPAC pathway mediates PGE2-induced FGF2 in bovine granulosa cells","volume":"159","author":"Shrestha","year":"2018","journal-title":"Endocrinology"},{"key":"2023051502250789700_ref119","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1530\/rep.0.1210217","article-title":"Characterization of adenylyl cyclases in cultured human granulosa cells","volume":"121","author":"Asb\u00f3th","year":"2001","journal-title":"Reproduction"},{"key":"2023051502250789700_ref120","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1262\/jrd.2012-089","article-title":"Regulatory effect of hypoxia-inducible factor-1\u03b1 on hCG-stimulated endothelin-2 expression in granulosa cells from the PMSG-treated rat ovary","volume":"58","author":"Zhang","year":"2012","journal-title":"J Reprod Dev"},{"key":"2023051502250789700_ref121","doi-asserted-by":"crossref","first-page":"e7988","DOI":"10.1371\/journal.pone.0007988","article-title":"The specificity of the FOXL2 c.402C&gt;G somatic mutation: a survey of solid tumors","volume":"4","author":"Schrader","year":"2009","journal-title":"PLoS One"},{"key":"2023051502250789700_ref122","article-title":"p53: from fundamental biology to clinical applications in cancer","volume":"11","author":"Capuozzo","year":"2022","journal-title":"Biology (Basel)"},{"key":"2023051502250789700_ref123","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1158\/1535-7163.MCT-09-0971","article-title":"SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2","volume":"9","author":"Peck","year":"2010","journal-title":"Mol Cancer Ther"},{"key":"2023051502250789700_ref124","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.arr.2018.02.004","article-title":"Role of Sirtuin1-p53 regulatory axis in aging, cancer and cellular reprogramming","volume":"43","author":"Ong","year":"2018","journal-title":"Ageing Res Rev"},{"key":"2023051502250789700_ref125","doi-asserted-by":"crossref","first-page":"5871","DOI":"10.2174\/092986712804143303","article-title":"Current advances in the synthesis and antitumoral activity of SIRT1-2 inhibitors by modulation of p53 and pro-apoptotic proteins","volume":"19","author":"Botta","year":"2012","journal-title":"Curr Med Chem"},{"key":"2023051502250789700_ref126","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1023\/A:1017958028256","article-title":"Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene","volume":"222","author":"Bagchi","year":"2001","journal-title":"Mol Cell Biochem"},{"key":"2023051502250789700_ref127","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.molcel.2007.01.011","article-title":"Phosphorylation of HuR by Chk2 regulates SIRT1 expression","volume":"25","author":"Abdelmohsen","year":"2007","journal-title":"Mol Cell"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioad026\/49623182\/ioad026.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/108\/5\/720\/50265621\/ioad026.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/108\/5\/720\/50265621\/ioad026.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,15]],"date-time":"2023-05-15T02:25:55Z","timestamp":1684117555000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/108\/5\/720\/7070576"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,6]]},"references-count":127,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,3,6]]},"published-print":{"date-parts":[[2023,5,10]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioad026","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,5]]},"published":{"date-parts":[[2023,3,6]]}}}