{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T19:53:29Z","timestamp":1790970809717,"version":"4.1.0"},"reference-count":56,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T00:00:00Z","timestamp":1729814400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation of China","award":["32272880"],"award-info":[{"award-number":["32272880"]}]},{"name":"National Natural Science Foundation of China","award":["2024NC-YBXM-088"],"award-info":[{"award-number":["2024NC-YBXM-088"]}]},{"name":"Key Project of Research and Development Program in Shaanxi Province, China","award":["32272880"],"award-info":[{"award-number":["32272880"]}]},{"name":"Key Project of Research and Development Program in Shaanxi Province, China","award":["2024NC-YBXM-088"],"award-info":[{"award-number":["2024NC-YBXM-088"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antioxidants"],"abstract":"<jats:p>The zinc oxide nanoparticles (ZnO NPs) is one of the most extensively utilized metal oxide nanoparticles in biomedicine, human food, cosmetics and livestock farming. However, growing evidence suggests that there is a potential risk for humans and animals because of the accumulation of ZnO NPs in cells, which leads to cell death through several different pathways. Nevertheless, the effects of ZnO NPs on porcine granulosa cells (PGCs) and how ZnO NPs regulate the follicular cells are unknown. In this study, we aimed to elucidate the role of ZnO NPs in the porcine ovary by using PGCs. Firstly, we identified the characterization of ZnO NPs used in this study and the results showed that the size of ZnO NPs was 29.0 nm. The results also demonstrated that ZnO NPs impaired cell viability and decreased steroid hormone secretion in PGCs. In addition, ZnO NPs induced reactive oxygen species (ROS) production, leading to oxidative stress of PGCs. Meanwhile, ZnO NPs also triggered autophagy in PGCs by increasing the ratio of LC3-II\/LC3-I, along with the expression of SQSTM1 and ATG7. Finally, the results from N-acetylcysteine (NAC) addition suggested that ZnO NPs promoted autophagy through the enhancement of ROS production. In summary, this study demonstrates that ZnO NPs impair the viability and function of PGCs through autophagy, which is regulated by ROS production.<\/jats:p>","DOI":"10.3390\/antiox13111295","type":"journal-article","created":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T03:46:04Z","timestamp":1729827964000},"page":"1295","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["ZnO NPs Impair the Viability and Function of Porcine Granulosa Cells Through Autophagy Regulated by ROS Production"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6534-4531","authenticated-orcid":false,"given":"Yifan","family":"Wang","sequence":"first","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Lv","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2479-3047","authenticated-orcid":false,"given":"Guangyu","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qichun","family":"Yao","sequence":"additional","affiliation":[{"name":"Animal Husbandry and Veterinary Station of Zhenba County, Hanzhong 723600, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziqi","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2948-8161","authenticated-orcid":false,"given":"Ning","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yutao","family":"He","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry","family":"Il","sequence":"additional","affiliation":[{"name":"Department of Food Security, Agrotechnological Faculty, Kozybayev University, 86, Pushkin Street, Petropavlovsk 150000, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9373-2520","authenticated-orcid":false,"given":"Jakupov Isatay","family":"Tusupovich","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, Seifullin Kazakh Agro Technical Research University, 62, Zhenis Avenue, Astana 010011, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongliang","family":"Jiang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Animal Genetic, Breeding and Reproduction in Shaanxi Province, College of Animal Science and Technology, Northwest Agriculture and Forestry University, Xianyang 712100, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Wang, C., Zhang, L., Su, W., Ying, Z., He, J., Zhang, L., Zhong, X., and Wang, T. (2017). Zinc Oxide Nanoparticles as a Substitute for Zinc Oxide or Colistin Sulfate: Effects on Growth, Serum Enzymes, Zinc Deposition, Intestinal Morphology and Epithelial Barrier in Weaned Piglets. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0181136"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1111\/asj.12329","article-title":"Effects of Dietary Supplementation of Modified Zinc Oxide on Growth Performance, Nutrient Digestibility, Blood Profiles, Fecal Microbial Shedding and Fecal Score in Weanling Pigs","volume":"86","author":"Cho","year":"2015","journal-title":"Anim. Sci. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1111\/jpn.12871","article-title":"Effects of Zinc Oxide Nanoparticles on the Egg Quality, Immune Response, Zinc Retention, and Blood Parameters of Laying Hens in the Late Phase of Production","volume":"102","author":"Abedini","year":"2018","journal-title":"J. Anim. Physiol. Anim. Nutr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"275","DOI":"10.12988\/asb.2015.5425","article-title":"Histopathological Evaluation of the Toxic Effects of Zinc Oxide (ZnO) Nanoparticles on Testicular Tissue of NMRI Adult Mice","volume":"7","author":"Mozaffari","year":"2015","journal-title":"Adv. Stud. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1007\/s10495-012-0705-6","article-title":"Zinc Oxide Nanoparticles Induce Oxidative DNA Damage and ROS-Triggered Mitochondria Mediated Apoptosis in Human Liver Cells (HepG2)","volume":"17","author":"Sharma","year":"2012","journal-title":"Apoptosis"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"8085","DOI":"10.2147\/IJN.S149070","article-title":"Zinc Oxide Nanoparticles Induce Toxic Responses in Human Neuroblastoma SHSY5Y Cells in a Size-Dependent Manner","volume":"12","author":"Liu","year":"2017","journal-title":"Int. J. Nanomed."},{"key":"ref_7","first-page":"195","article-title":"Immunotoxicity of Zinc Oxide Nanoparticles with Different Size and Electrostatic Charge","volume":"9","author":"Kim","year":"2014","journal-title":"Int. J. Nanomed."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4433","DOI":"10.2147\/IJN.S134897","article-title":"Zinc Oxide Nanoparticle-Induced Atherosclerotic Alterations in Vitro and in Vivo","volume":"12","author":"Yan","year":"2017","journal-title":"Int. J. Nanomed."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2850","DOI":"10.3390\/ma5122850","article-title":"The Toxic Effects and Mechanisms of CuO and ZnO Nanoparticles","volume":"5","author":"Chang","year":"2012","journal-title":"Materials"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1007\/s10815-013-0078-y","article-title":"The Effect of Zinc Oxide Nanoparticles on Mouse Spermatogenesis","volume":"30","author":"Talebi","year":"2013","journal-title":"J. Assist. Reprod. Gen."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"2170","DOI":"10.18632\/aging.101539","article-title":"Exposure to Zinc Oxide Nanoparticles during Pregnancy Induces Oocyte DNA Damage and Affects Ovarian Reserve of Mouse Offspring","volume":"10","author":"Zhai","year":"2018","journal-title":"Aging"},{"key":"ref_12","first-page":"107","article-title":"Subchronic Effects of Different Doses of Zinc Oxide Nanoparticle on Reproductive Organs of Female Rats: An Experimental Study","volume":"17","author":"Amani","year":"2019","journal-title":"Int. J. Reprod. Biomed."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1146\/annurev.physiol.59.1.349","article-title":"Regulation of Ovarian Follicle Atresia","volume":"59","author":"Kaipia","year":"1997","journal-title":"Annu. Rev. Physiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"726","DOI":"10.7150\/ijbs.30369","article-title":"Autophagy in Ovarian Follicular Development and Atresia","volume":"15","author":"Zhou","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_15","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":"ref_16","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1002\/mrd.22676","article-title":"Effects of Melatonin on Follicular Atresia and Granulosa Cell Apoptosis in the Porcine","volume":"83","author":"He","year":"2016","journal-title":"Mol. Reprod. Dev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.1080\/15548627.2021.2005415","article-title":"Autophagy Regulates Differentiation of Ovarian Granulosa Cells through Degradation of WT1","volume":"18","author":"Shao","year":"2022","journal-title":"Autophagy"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"C231","DOI":"10.1152\/ajpcell.00267.2021","article-title":"Circadian Clock Regulates Granulosa Cell Autophagy through NR1D1-Mediated Inhibition of ATG5","volume":"322","author":"Zhang","year":"2022","journal-title":"Am. J. Physiol-Cell Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1080\/15376516.2018.1553221","article-title":"Zinc Oxide Nanoparticles Impacts: Cytotoxicity, Genotoxicity, Developmental Toxicity, and Neurotoxicity","volume":"29","author":"Singh","year":"2019","journal-title":"Toxicol. Mech. Method."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Rahman, M.A., Ahmed, K.R., Haque, F., Park, M.N., and Kim, B. (2023). Recent Advances in Cellular Signaling Interplay between Redox Metabolism and Autophagy Modulation in Cancer: An Overview of Molecular Mechanisms and Therapeutic Interventions. Antioxidants, 12.","DOI":"10.3390\/antiox12020428"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Yun, H.R., Jo, Y.H., Kim, J., Shin, Y., Kim, S.S., and Choi, T.G. (2020). Roles of Autophagy in Oxidative Stress. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21093289"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Wang, S., Yao, Q., Zhao, F., Cui, W., Price, C.A., Wang, Y., Lv, J., Tang, H., and Jiang, Z. (2023). 1\u03b1,25(OH)2D3 Promotes the Autophagy of Porcine Ovarian Granulosa Cells as a Protective Mechanism against ROS through the BNIP3\/PINK1 Pathway. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24054364"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1002\/smll.200700595","article-title":"Cytotoxicity of Nanoparticles","volume":"4","author":"Lewinski","year":"2008","journal-title":"Small"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.toxlet.2022.01.010","article-title":"Zinc Oxide Nanoparticle Causes Toxicity to the Development of Mouse Oocyte and Early Embryo","volume":"358","author":"Huang","year":"2022","journal-title":"Toxicol. Lett."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.tiv.2016.05.017","article-title":"Sublethal Effects of Zinc Oxide Nanoparticles on Male Reproductive Cells","volume":"35","author":"Liu","year":"2016","journal-title":"Toxicol. In Vitro"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Liu, G., Lv, J., Wang, Y., Sun, K., Gao, H., Li, Y., Yao, Q., Ma, L., Kochshugulova, G., and Jiang, Z. (2024). ZnO NPs Induce miR-342-5p Mediated Ferroptosis of Spermatocytes through the NF-\u03baB Pathway in Mice. J. Nanobiotechnol., 22.","DOI":"10.1186\/s12951-024-02672-5"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"69416","DOI":"10.1007\/s11356-021-15257-8","article-title":"ZnO Nanoparticles Alter Redox Metabolism of Limnoperna Fortunei","volume":"28","author":"Girardello","year":"2021","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"529","DOI":"10.2174\/138955751507150424104334","article-title":"Nanotoxicity: The Toxicity Research Progress of Metal and Metal-Containing Nanoparticles","volume":"15","author":"Ding","year":"2015","journal-title":"Mini Rev. Med. Chem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"110454","DOI":"10.1016\/j.ecoenv.2020.110454","article-title":"Bioaccumulation Kinetics and Tissue Distribution of Silver Nanoparticles in Zebrafish: The Mechanisms and Influence of Natural Organic Matter","volume":"194","author":"Xiao","year":"2020","journal-title":"Ecotoxicol. Environ. Safe"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/1743-8977-10-9","article-title":"Comparative Absorption, Distribution, and Excretion of Titanium Dioxide and Zinc Oxide Nanoparticles after Repeated Oral Administration","volume":"10","author":"Cho","year":"2013","journal-title":"Part. Fibre Toxicol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"781","DOI":"10.3382\/ps\/peu008","article-title":"Ovarian Follicle Selection and Granulosa Cell Differentiation","volume":"94","author":"Johnson","year":"2015","journal-title":"Poult. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.theriogenology.2018.02.008","article-title":"The Impact of Sex Steroid Agonists and Antagonists on Folliculogenesis in the Neonatal Porcine Ovary via Cell Proliferation and Apoptosis","volume":"113","author":"Grzesiak","year":"2018","journal-title":"Theriogenology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1262\/jrd.2011-012","article-title":"Follicular Growth and Atresia in Mammalian Ovaries: Regulation by Survival and Death of Granulosa Cells","volume":"58","author":"Matsuda","year":"2012","journal-title":"J. Reprod. Dev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1210\/me.2010-0260","article-title":"Estrogen Promotes the Development of Mouse Cumulus Cells in Coordination with Oocyte-Derived GDF9 and BMP15","volume":"24","author":"Sugiura","year":"2010","journal-title":"Mol. Endocrinol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Santacruz-M\u00e1rquez, R., and Flaws, J.A. (2023). Exposure to Zinc Oxide Nanoparticles Increases Estradiol Levels and Induces an Antioxidant Response in Antral Ovarian Follicles In Vitro. Toxics, 11.","DOI":"10.3390\/toxics11070602"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.envpol.2016.09.067","article-title":"Exposure of Juvenile Turbot (Scophthalmus Maximus) to Silver Nanoparticles and 17\u03b1-Ethinylestradiol Mixtures: Implications for Contaminant Uptake and Plasma Steroid Hormone Levels","volume":"220","author":"Farkas","year":"2017","journal-title":"Environ. Pollut."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1146\/annurev.physiol.63.1.193","article-title":"StAR Protein and the Regulation of Steroid Hormone Biosynthesis","volume":"63","author":"Stocco","year":"2001","journal-title":"Annu. Rev. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1007\/s11373-007-9177-z","article-title":"Transcriptional Regulation of Human CYP11A1 in Gonads and Adrenals","volume":"14","author":"Guo","year":"2007","journal-title":"J. Biomed. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Aventaggiato, M., Preziosi, A., Cheraghi Bidsorkhi, H., Schifano, E., Vespa, S., Mardente, S., Zicari, A., Uccelletti, D., Mancini, P., and Lotti, L.V. (2023). ZnO Nanorods Create a Hypoxic State with Induction of HIF-1 and EPAS1, Autophagy, and Mitophagy in Cancer and Non-Cancer Cells. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24086971"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2106049","DOI":"10.1002\/advs.202106049","article-title":"Cytotoxicity of Metal-Based Nanoparticles: From Mechanisms and Methods of Evaluation to Pathological Manifestations","volume":"9","author":"Xiong","year":"2022","journal-title":"Adv. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1080\/15548627.2018.1509171","article-title":"Necrotic, Apoptotic and Autophagic Cell Fates Triggered by Nanoparticles","volume":"15","author":"Mohammadinejad","year":"2019","journal-title":"Autophagy"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"114371","DOI":"10.1016\/j.ecoenv.2022.114371","article-title":"Toxicity of Polystyrene Nanoparticles for Mouse Ovary and Cultured Human Granulosa Cells","volume":"249","author":"Huang","year":"2023","journal-title":"Ecotoxicol. Environ. Safe"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"106908","DOI":"10.1016\/j.anireprosci.2021.106908","article-title":"Silver Nanoparticles Induce Oxidative Stress, Apoptosis and Impaired Steroidogenesis in Ovarian Granulosa Cells of Cattle","volume":"236","author":"Tabandeh","year":"2022","journal-title":"Anim. Reprod. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"114578","DOI":"10.1016\/j.envpol.2020.114578","article-title":"Exposure to Low Dose ZnO Nanoparticles Induces Hyperproliferation and Malignant Transformation through Activating the CXCR2\/NF-\u03baB\/STAT3\/ERK and AKT Pathways in Colonic Mucosal Cells","volume":"263","author":"Meng","year":"2020","journal-title":"Environ. Pollut."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1038\/s41419-020-2384-5","article-title":"\u201cIron Free\u201d Zinc Oxide Nanoparticles with Ion-Leaking Properties Disrupt Intracellular ROS and Iron Homeostasis to Induce Ferroptosis","volume":"11","author":"Zhang","year":"2020","journal-title":"Cell Death Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2407","DOI":"10.1021\/acs.est.1c07198","article-title":"Mitochondria-Dependent Oxidative Stress Mediates ZnO Nanoparticle (ZnO NP)-Induced Mitophagy and Lipotoxicity in Freshwater Teleost Fish","volume":"56","author":"Chen","year":"2022","journal-title":"Environ. Sci. Technol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.biomaterials.2009.09.028","article-title":"Oxidative Stress in the Brain of Mice Caused by Translocated Nanoparticulate TiO2 Delivered to the Abdominal Cavity","volume":"31","author":"Ma","year":"2010","journal-title":"Biomaterials"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"R647","DOI":"10.1186\/bcr929","article-title":"Genetic Polymorphism in the Manganese Superoxide Dismutase Gene, Antioxidant Intake, and Breast Cancer Risk: Results from the Shanghai Breast Cancer Study","volume":"6","author":"Cai","year":"2004","journal-title":"Breast Cancer Res."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Tripathi, A., Khatun, S., Pandey, A.N., Mishra, S.K., Chaube, R., Shrivastav, T.G., and Chaube, S.K. (2009). Intracellular Levels of Hydrogen Peroxide and Nitric Oxide in Oocytes at Various Stages of Meiotic Cell Cycle and Apoptosis. Free Radic. Res.","DOI":"10.1080\/10715760802695985"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Lu, J., Wang, Z., Cao, J., Chen, Y., and Dong, Y. (2018). A Novel and Compact Review on the Role of Oxidative Stress in Female Reproduction. Reprod. Biol. Endocrinol., 16.","DOI":"10.1186\/s12958-018-0391-5"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1093\/molehr\/5.5.409","article-title":"Oxidative Stress Markers in Preovulatory Follicular Fluid in Humans","volume":"5","author":"Jozwik","year":"1999","journal-title":"Mol. Hum. Reprod."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s12192-015-0639-3","article-title":"Autophagy as a Defense Strategy against Stress: Focus on Paracentrotus Lividus Sea Urchin Embryos Exposed to Cadmium","volume":"21","author":"Chiarelli","year":"2016","journal-title":"Cell Stress Chaperones"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"24131","DOI":"10.1074\/jbc.M702824200","article-title":"P62\/SQSTM1 Binds Directly to Atg8\/LC3 to Facilitate Degradation of Ubiquitinated Protein Aggregates by Autophagy","volume":"282","author":"Pankiv","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Mawed, S.A., Marini, C., Alagawany, M., Farag, M.R., Reda, R.M., El-Saadony, M.T., Elhady, W.M., Magi, G.E., Di Cerbo, A., and El-Nagar, W.G. (2022). Zinc Oxide Nanoparticles (ZnO-NPs) Suppress Fertility by Activating Autophagy, Apoptosis, and Oxidative Stress in the Developing Oocytes of Female Zebrafish. Antioxidants, 11.","DOI":"10.3390\/antiox11081567"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"4062","DOI":"10.1080\/15548627.2021.1900498","article-title":"Combination of Autophagy and NFE2L2\/NRF2 Activation as a Treatment Approach for Neuropathic Pain","volume":"17","author":"Li","year":"2021","journal-title":"Autophagy"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"110354","DOI":"10.1016\/j.celrep.2022.110354","article-title":"K48\/K63-Linked Polyubiquitination of ATG9A by TRAF6 E3 Ligase Regulates Oxidative Stress-Induced Autophagy","volume":"38","author":"Wang","year":"2022","journal-title":"Cell Rep."}],"container-title":["Antioxidants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3921\/13\/11\/1295\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:20:14Z","timestamp":1760113214000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3921\/13\/11\/1295"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,25]]},"references-count":56,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["antiox13111295"],"URL":"https:\/\/doi.org\/10.3390\/antiox13111295","relation":{},"ISSN":["2076-3921"],"issn-type":[{"value":"2076-3921","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,25]]}}}