{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T20:41:09Z","timestamp":1789072869532,"version":"build-2803163510"},"reference-count":60,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2023,6,5]],"date-time":"2023-06-05T00:00:00Z","timestamp":1685923200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"AIRG-Suisse"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Individuals born after intrauterine growth restriction (IUGR) are at risk of developing cardiovascular diseases (CVDs). Endothelial dysfunction plays a role in the pathogenesis of CVDs; and endothelial colony-forming cells (ECFCs) have been identified as key factors in endothelial repair. In a rat model of IUGR induced by a maternal low-protein diet, we observed an altered functionality of ECFCs in 6-month-old males, which was associated with arterial hypertension related to oxidative stress and stress-induced premature senescence (SIPS). Resveratrol (R), a polyphenol compound, was found to improve cardiovascular function. In this study, we investigated whether resveratrol could reverse ECFC dysfunctions in the IUGR group. ECFCs were isolated from IUGR and control (CTRL) males and were treated with R (1 \u03bcM) or dimethylsulfoxide (DMSO) for 48 h. In the IUGR-ECFCs, R increased proliferation (5\u2032-bromo-2\u2032-deoxyuridine (BrdU) incorporation, p &lt; 0.001) and improved capillary-like outgrowth sprout formation (in Matrigel), nitric oxide (NO) production (fluorescent dye, p &lt; 0.01), and endothelial nitric oxide synthase (eNOS) expression (immunofluorescence, p &lt; 0.001). In addition, R decreased oxidative stress with reduced superoxide anion production (fluorescent dye, p &lt; 0.001); increased Cu\/Zn superoxide dismutase expression (Western blot, p &lt; 0.05); and reversed SIPS with decreased beta-galactosidase activity (p &lt; 0.001), and decreased p16ink4a (p &lt; 0.05) and increased Sirtuin-1 (p &lt; 0.05) expressions (Western blot). No effects of R were observed in the CTRL-ECFCs. These results suggest that R reverses long-term ECFC dysfunctions related to IUGR.<\/jats:p>","DOI":"10.3390\/ijms24119747","type":"journal-article","created":{"date-parts":[[2023,6,5]],"date-time":"2023-06-05T04:01:47Z","timestamp":1685937707000},"page":"9747","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Resveratrol Reverses Endothelial Colony-Forming Cell Dysfunction in Adulthood in a Rat Model of Intrauterine Growth Restriction"],"prefix":"10.3390","volume":"24","author":[{"given":"Estelle","family":"Guillot","sequence":"first","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Lemay","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manon","family":"Allouche","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Vitorino Silva","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanna","family":"Coppola","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florence","family":"Sabatier","sequence":"additional","affiliation":[{"name":"Center from Cardiovascular and Nutrition Research (C2VN), Institut National de la Sant\u00e9 Et de la Recherche M\u00e9dicale (INSERM), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"},{"name":"Institut National de Recherche pour L\u2019Agriculture, L\u2019Alimentation et L\u2019Environnement (INRAe), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7oise","family":"Dignat-George","sequence":"additional","affiliation":[{"name":"Center from Cardiovascular and Nutrition Research (C2VN), Institut National de la Sant\u00e9 Et de la Recherche M\u00e9dicale (INSERM), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"},{"name":"Institut National de Recherche pour L\u2019Agriculture, L\u2019Alimentation et L\u2019Environnement (INRAe), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexandre","family":"Sarre","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2051-1126","authenticated-orcid":false,"given":"Anne-Christine","family":"Peyter","sequence":"additional","affiliation":[{"name":"Neonatal Research Laboratory, Clinic of Neonatology, Department Woman-Mother-Child, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8062-5005","authenticated-orcid":false,"given":"St\u00e9phanie","family":"Simoncini","sequence":"additional","affiliation":[{"name":"Center from Cardiovascular and Nutrition Research (C2VN), Institut National de la Sant\u00e9 Et de la Recherche M\u00e9dicale (INSERM), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"},{"name":"Institut National de Recherche pour L\u2019Agriculture, L\u2019Alimentation et L\u2019Environnement (INRAe), Aix Marseille Universit\u00e9, UMR-S 1263, UFR de Pharmacie, Campus Sant\u00e9, 13385 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0617-7558","authenticated-orcid":false,"given":"Catherine","family":"Yzydorczyk","sequence":"additional","affiliation":[{"name":"DOHaD Laboratory, Division of pediatrics, Department 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Toxicol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1097\/00003081-200606000-00009","article-title":"Adult Consequences of Fetal Growth Restriction","volume":"49","author":"Barker","year":"2006","journal-title":"Clin. Obstet. Gynecol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Peyter, A.-C., Armengaud, J.-B., Guillot, E., and Yzydorczyk, C. (2021). Endothelial Progenitor Cells Dysfunctions and Cardiometabolic Disorders: From Mechanisms to Therapeutic Approaches. Int. J. Mol. 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Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"233","DOI":"10.3109\/14767058.2013.807237","article-title":"Altered angiogenesis in low birth weight individuals: A role for anti-angiogenic circulating factors","volume":"27","author":"Ligi","year":"2013","journal-title":"J. Matern. Neonatal Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1182\/blood-2010-12-325142","article-title":"A switch toward angiostatic gene expression impairs the angiogenic properties of endothelial progenitor cells in low birth weight preterm infants","volume":"118","author":"Ligi","year":"2011","journal-title":"Blood"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Keshavjee, B., Lambelet, V., Coppola, H., Viertl, D., Prior, J.O., Kappeler, L., Armengaud, J.-B., Chouraqui, J.-P., Chehade, H., and Vanderriele, P.-E. (2022). Stress-Induced Premature Senescence Related to Oxidative Stress in the Developmental Programming of Nonalcoholic Fatty Liver Disease in a Rat Model of Intrauterine Growth Restriction. Antioxidants, 11.","DOI":"10.3390\/antiox11091695"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2116","DOI":"10.1182\/blood-2013-02-484956","article-title":"Accelerated senescence of cord blood endothelial progenitor cells in premature neonates is driven by SIRT1 decreased expression","volume":"123","author":"Vassallo","year":"2014","journal-title":"Blood"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Simoncini, S., Coppola, H., Rocca, A., Bachmann, I., Guillot, E., Zippo, L., Dignat-George, F., Sabatier, F., Bedel, R., and Wilson, A. (2021). Endothelial Colony-Forming Cells Dysfunctions Are Associated with Arterial Hypertension in a Rat Model of Intrauterine Growth Restriction. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms221810159"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1016\/0140-6736(92)91277-F","article-title":"Wine, alcohol, platelets, and the French paradox for coronary heart disease","volume":"339","author":"Renaud","year":"1992","journal-title":"Lancet"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1016\/j.bbadis.2014.10.016","article-title":"Preclinical and clinical evidence for the role of resveratrol in the treatment of cardiovascular diseases","volume":"1852","author":"Zordoky","year":"2015","journal-title":"Biochim. Biophys. Acta BBA\u2014Mol. Basis Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1186\/s13063-016-1426-x","article-title":"The efficacy of resveratrol in controlling hypertension: Study protocol for a randomized, crossover, double-blinded, placebo-controlled trial","volume":"17","author":"Movahed","year":"2016","journal-title":"Trials"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Bonnefont-Rousselot, D. (2016). Resveratrol and Cardiovascular Diseases. Nutrients, 8.","DOI":"10.3390\/nu8050250"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1016\/j.bbadis.2013.05.018","article-title":"Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice","volume":"1832","author":"Dolinsky","year":"2013","journal-title":"Biochim. et Biophys. Acta (BBA)\u2014Mol. Basis Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"292","DOI":"10.3389\/fphys.2014.00292","article-title":"Systemic and renal oxidative stress in the pathogenesis of hypertension: Modulation of long-term control of arterial blood pressure by resveratrol","volume":"5","author":"Hamza","year":"2014","journal-title":"Front. Physiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"965","DOI":"10.5114\/aoms.2017.69326","article-title":"Lipid lowering nutraceuticals in clinical practice: Position paper from an International Lipid Expert Panel","volume":"13","author":"Cicero","year":"2017","journal-title":"Arch. Med. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2076","DOI":"10.1039\/C7FO00178A","article-title":"Food and plant bioactives for reducing cardiometabolic disease risk: An evidence based approach","volume":"8","author":"Cicero","year":"2017","journal-title":"Food Funct."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/bcp.12902","article-title":"Nutraceuticals with a clinically detectable blood pressure-lowering effect: A review of available randomized clinical trials and their meta-analyses","volume":"83","author":"Borghi","year":"2017","journal-title":"Br. J. Clin. Pharmacol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"16102","DOI":"10.3390\/molecules191016102","article-title":"Resveratrol and Endothelial Nitric Oxide","volume":"19","author":"Xia","year":"2014","journal-title":"Molecules"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Serreli, G., and Deiana, M. (2023). Role of Dietary Polyphenols in the Activity and Expression of Nitric Oxide Synthases: A Review. Antioxidants, 12.","DOI":"10.3390\/antiox12010147"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5502","DOI":"10.1002\/ptr.7185","article-title":"Effects of resveratrol on female reproduction: A review","volume":"35","author":"Sirotkin","year":"2021","journal-title":"Phytother. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1111\/jog.13680","article-title":"Mechanism of resveratrol in improving ovarian function in a rat model of premature ovarian insufficiency","volume":"44","author":"Li","year":"2018","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Pasquariello, R., Verdile, N., Brevini, T.A.L., Gandolfi, F., Boiti, C., Zerani, M., and Maranesi, M. (2020). The Role of Resveratrol in Mammalian Reproduction. Molecules, 25.","DOI":"10.20944\/preprints202009.0003.v1"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1177\/0300060518811228","article-title":"Serum and follicular fluid levels of sirtuin 1, sirtuin 6, and resveratrol in women undergoing in vitro fertilization: An observational, clinical study","volume":"47","author":"Bodis","year":"2019","journal-title":"J. Int. Med. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1111\/rda.12946","article-title":"Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production","volume":"52","author":"Sovernigo","year":"2017","journal-title":"Reprod. Domest. Anim."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1262\/jrd.2013-102","article-title":"Resveratrol Improves the Mitochondrial Function and Fertilization Outcome of Bovine Oocytes","volume":"60","author":"Takeo","year":"2014","journal-title":"J. Reprod. Dev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1262\/jrd.2015-001","article-title":"Resveratrol-induced mitochondrial synthesis and autophagy in oocytes derived from early antral follicles of aged cows","volume":"61","author":"Sugiyama","year":"2015","journal-title":"J. Reprod. Dev."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1002\/jat.1456","article-title":"Effects of resveratrol analogs on steroidogenesis and mitochondrial function in rat Leydig cells in vitro","volume":"29","author":"Svechnikov","year":"2009","journal-title":"J. Appl. Toxicol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/s12272-008-1124-7","article-title":"trans-resveratrol relaxes the corpus cavernosum ex vivo and enhances testosterone levels and sperm quality in vivo","volume":"31","author":"Shin","year":"2008","journal-title":"Arch. Pharmacal. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1055\/s-2005-865757","article-title":"Resveratrol May Reduce Apoptosis of Rat Testicular Germ Cells After Experimental Testicular Torsion","volume":"15","author":"Uguralp","year":"2005","journal-title":"Eur. J. Pediatr. Surg."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1113\/JP271133","article-title":"Effect of resveratrol on metabolic and cardiovascular function in male and female adult offspring exposed to prenatal hypoxia and a high-fat diet","volume":"594","author":"Shah","year":"2016","journal-title":"J. Physiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e13109","DOI":"10.14814\/phy2.13109","article-title":"Postnatal resveratrol supplementation improves cardiovascular function in male and female intrauterine growth restricted offspring","volume":"5","author":"Shah","year":"2017","journal-title":"Physiol. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"9045976","DOI":"10.1155\/2018\/9045976","article-title":"Resveratrol Improves Tube Formation in AGE-Induced Late Endothelial Progenitor Cells by Suppressing Syndecan-4 Shedding","volume":"2018","author":"Wu","year":"2018","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7675","DOI":"10.12659\/MSM.917013","article-title":"Resveratrol Induces Endothelial Progenitor Cells Angiogenesis via MiR-542-3p by Targeting Angiopoietin-2 and Involves in Recanalization of Venous Thrombosis","volume":"25","author":"Lu","year":"2019","journal-title":"Med. Sci. Monit."},{"key":"ref_37","first-page":"5708","article-title":"Resveratrol protects late endothelial progenitor cells from TNF-alpha-induced inflammatory damage by upregulating Kruppel-like factor-2","volume":"17","author":"Chu","year":"2018","journal-title":"Mol. Med. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5528","DOI":"10.3892\/mmr.2016.5929","article-title":"Resveratrol prevents endothelial progenitor cells from senescence and reduces the oxidative reaction via PPAR-gamma\/HO-1 pathways","volume":"14","author":"Shen","year":"2016","journal-title":"Mol. Med. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1174","DOI":"10.1038\/aps.2013.60","article-title":"Trans-3,4,5,4\u2032-tetramethoxystilbene, a resveratrol analog, potently inhibits angiogenesis in vitro and in vivo","volume":"34","author":"Chen","year":"2013","journal-title":"Acta Pharmacol. Sin."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"105725","DOI":"10.1016\/j.phrs.2021.105725","article-title":"Resveratrol and endothelial function: A literature review","volume":"170","author":"Parsamanesh","year":"2021","journal-title":"Pharmacol. Res."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Li, H., Xia, N., Hasselwander, S., and Daiber, A. (2019). Resveratrol and Vascular Function. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20092155"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"6517","DOI":"10.2147\/IJN.S174989","article-title":"Inducing angiogenesis with the controlled release of nitric oxide from biodegradable and biocompatible copolymeric nanoparticles","volume":"13","author":"Yang","year":"2018","journal-title":"Int. J. Nanomed."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1002\/cbin.10405","article-title":"The role of eNOS in the migration and proliferation of bone-marrow derived endothelial progenitor cells and in vitro angiogenesis","volume":"39","author":"Lu","year":"2015","journal-title":"Cell Biol. Int."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"112164","DOI":"10.1016\/j.biopha.2021.112164","article-title":"Resveratrol (RV): A pharmacological review and call for further research","volume":"143","author":"Zhang","year":"2021","journal-title":"Biomed. Pharmacother."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/s11010-008-9756-y","article-title":"EPR studies on the superoxide-scavenging capacity of the nutraceutical resveratrol","volume":"313","author":"Jia","year":"2008","journal-title":"Mol. Cell. Biochem."},{"key":"ref_46","first-page":"111","article-title":"Resveratrol reduces endothelial oxidative stress by modulating the gene expression of superoxide dismutase 1 (SOD1), glutathione peroxidase 1 (GPx1) and NADPH oxidase subunit (Nox4)","volume":"60","author":"Spanier","year":"2009","journal-title":"J. Physiol. Pharmacol. Off. J. Pol. Physiol. Soc."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"H1876","DOI":"10.1152\/ajpheart.00375.2009","article-title":"Resveratrol attenuates mitochondrial oxidative stress in coronary arterial endothelial cells","volume":"297","author":"Ungvari","year":"2009","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1111\/bph.13492","article-title":"Antioxidant effects of resveratrol in the cardiovascular system","volume":"174","author":"Xia","year":"2016","journal-title":"Br. J. Pharmacol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"455","DOI":"10.3389\/fped.2020.00455","article-title":"Sirt1 Regulates Oxidative Stress in Oxygen-Glucose Deprived Hippocampal Neurons","volume":"8","author":"Shi","year":"2020","journal-title":"Front. Pediatr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.3389\/fphar.2020.01225","article-title":"SIRT1 Activation by Natural Phytochemicals: An Overview","volume":"11","author":"Iside","year":"2020","journal-title":"Front. Pharmacol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"12911","DOI":"10.1038\/s41598-017-11756-2","article-title":"Transient postnatal overfeeding causes liver stress-induced premature senescence in adult mice","volume":"7","author":"Yzydorczyk","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Li, Y., and Tollefsbol, T.O. (2011). p16INK4a Suppression by Glucose Restriction Contributes to Human Cellular Lifespan Extension through SIRT1-Mediated Epigenetic and Genetic Mechanisms. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0017421"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Yzydorczyk, C., Li, N., Rigal, E., Chehade, H., Mosig, D., Armengaud, J.B., Rolle, T., Krishnasamy, A., Orozco, E., and Siddeek, B. (2019). Calorie Restriction in Adulthood Reduces Hepatic Disorders Induced by Transient Postnatal Overfeeding in Mice. Nutrients, 11.","DOI":"10.3390\/nu11112796"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3180","DOI":"10.1038\/s41598-017-03635-7","article-title":"Induction of sirtuin-1 signaling by resveratrol induces human chondrosarcoma cell apoptosis and exhibits antitumor activity","volume":"7","author":"Chao","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Eren, M.K., Kilincli, A., and Eren, \u00d6. (2015). Resveratrol Induced Premature Senescence Is Associated with DNA Damage Mediated SIRT1 and SIRT2 Down-Regulation. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0124837"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1111\/j.1474-9726.2006.00199.x","article-title":"Senescence-associated beta-galactosidase is lysosomal beta-galactosidase","volume":"5","author":"Lee","year":"2006","journal-title":"Aging Cell."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Safwan-Zaiter, H., Wagner, N., and Wagner, K.-D. (2022). P16INK4A\u2014More Than a Senescence Marker. Life, 12.","DOI":"10.3390\/life12091332"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1111\/1348-0421.12833","article-title":"Resveratrol ameliorates thymus senescence changes in D-galactose induced mice","volume":"64","author":"Wei","year":"2020","journal-title":"Microbiol. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"64","DOI":"10.4103\/ijpvm.IJPVM_139_17","article-title":"Short-term high dose of quercetin and resveratrol alters aging markers in human kidney cells","volume":"8","author":"Hemmati","year":"2017","journal-title":"Int. J. Prev. Med."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1017\/S000711452000015X","article-title":"Intra-uterine growth restriction induced by maternal low-protein diet causes long-term alterations of thymic structure and function in adult male rat offspring","volume":"123","author":"Armengaud","year":"2020","journal-title":"Br. J. Nutr."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/11\/9747\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:48:20Z","timestamp":1760125700000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/11\/9747"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,5]]},"references-count":60,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["ijms24119747"],"URL":"https:\/\/doi.org\/10.3390\/ijms24119747","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,5]]}}}