{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T06:26:50Z","timestamp":1781072810431,"version":"3.54.1"},"reference-count":50,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2025,12,1]],"date-time":"2025-12-01T00:00:00Z","timestamp":1764547200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"funder":[{"DOI":"10.13039\/501100004826","name":"Natural Science Foundation of Beijing Municipality","doi-asserted-by":"publisher","award":["7232240"],"award-info":[{"award-number":["7232240"]}],"id":[{"id":"10.13039\/501100004826","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32270519"],"award-info":[{"award-number":["32270519"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Comparative Biochemistry and Physiology Part A: Molecular &amp; Integrative Physiology"],"published-print":{"date-parts":[[2025,12]]},"DOI":"10.1016\/j.cbpa.2025.111927","type":"journal-article","created":{"date-parts":[[2025,9,10]],"date-time":"2025-09-10T14:36:57Z","timestamp":1757515017000},"page":"111927","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":2,"special_numbering":"C","title":["Up-regulation of cell apoptosis, autophagy and mitochondrial dynamics in ovarian granulosa cells of Daurian ground squirrels during the pre-hibernation period"],"prefix":"10.1016","volume":"310","author":[{"given":"Xi","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hao","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaomei","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjing","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jirui","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haolin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhengrong","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuning","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiang","family":"Weng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingying","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.cbpa.2025.111927_bb0005","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.semcdb.2019.05.022","article-title":"Mitochondria as playmakers of apoptosis, autophagy and senescence","volume":"98","author":"Abate","year":"2020","journal-title":"Semin. Cell Dev. Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0010","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1002\/cbin.11036","article-title":"Clinical correlation of apoptosis in human granulosa cells-a review","volume":"42","author":"Almeida","year":"2018","journal-title":"Cell Biol. Int."},{"key":"10.1016\/j.cbpa.2025.111927_bb0015","doi-asserted-by":"crossref","first-page":"R106","DOI":"10.1186\/gb-2010-11-10-r106","article-title":"Differential expression analysis for sequence count data","volume":"11","author":"Anders","year":"2010","journal-title":"Genome Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0020","first-page":"60","article-title":"Observations on the ovary of the hedgehog (Erinaceus europaeus) in physiological and experimental hibernation and awakening","volume":"73","author":"Balboni","year":"1969","journal-title":"Acta Anat. Suppl."},{"key":"10.1016\/j.cbpa.2025.111927_bb0025","doi-asserted-by":"crossref","DOI":"10.1111\/brv.12378","article-title":"Structure, function, and regulation of mitofusin-2 in health and disease","volume":"93","author":"Chandhok","year":"2018","journal-title":"Biol. Rev."},{"key":"10.1016\/j.cbpa.2025.111927_bb0030","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/s00360-019-01245-5","article-title":"Autophagy and Akt-mTOR signaling display periodic oscillations during torpor-arousal cycles in oxidative skeletal muscle of Daurian ground squirrels","volume":"190","author":"Chang","year":"2020","journal-title":"J. Comp. Physiol. B."},{"key":"10.1016\/j.cbpa.2025.111927_bb0035","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1126\/science.1231031","article-title":"PINK1-phosphorylated Mitofusin 2 is a Parkin receptor for culling damaged mitochondria","volume":"340","author":"Chen","year":"2013","journal-title":"Science"},{"key":"10.1016\/j.cbpa.2025.111927_bb0040","doi-asserted-by":"crossref","first-page":"2532","DOI":"10.1016\/j.fertnstert.2009.11.021","article-title":"The role of autophagy in follicular development and atresia in rat granulosa cells","volume":"93","author":"Choi","year":"2010","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.cbpa.2025.111927_bb0045","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1095\/biolreprod.111.091314","article-title":"The role of autophagy in Corpus luteum regression in the rat","volume":"85","author":"Choi","year":"2011","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.cbpa.2025.111927_bb0050","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1007\/s10815-013-0068-0","article-title":"Plasticity of granulosa cells: on the crossroad of stemness and transdifferentiation potential","volume":"30","author":"Dzafic","year":"2013","journal-title":"J. Assist. Reprod. Genet."},{"key":"10.1016\/j.cbpa.2025.111927_bb0055","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1007\/s10495-008-0248-z","article-title":"Combined apoptosis and autophagy, the process that eliminates the oocytes of atretic follicles in immature rats","volume":"13","author":"Escobar","year":"2008","journal-title":"Apoptosis"},{"key":"10.1016\/j.cbpa.2025.111927_bb0060","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","article-title":"CD-HIT: accelerated for clustering the next-generation sequencing data","volume":"28","author":"Fu","year":"2012","journal-title":"Bioinformatics"},{"key":"10.1016\/j.cbpa.2025.111927_bb0065","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.tcb.2010.03.002","article-title":"The Beclin 1-VPS34 complex - at the crossroads of autophagy and beyond","volume":"20","author":"Funderburk","year":"2010","journal-title":"Trends Cell Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0070","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/ncb2886","article-title":"Autophagy variation within a cell population determines cell fate through selective degradation of Fap-1","volume":"16","author":"Gump","year":"2014","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0075","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1016\/j.cell.2010.04.009","article-title":"Mitochondria supply membranes for autophagosome biogenesis during starvation","volume":"141","author":"Hailey","year":"2010","journal-title":"Cell"},{"key":"10.1016\/j.cbpa.2025.111927_bb0080","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1071\/RD16063","article-title":"Proliferation and apoptosis processes in the seasonal testicular development of the wild Daurian ground squirrel (Brandt, 1844)","volume":"29","author":"Han","year":"2017","journal-title":"Reprod. Fert. Develop."},{"key":"10.1016\/j.cbpa.2025.111927_bb0085","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1017\/S1431927622000484","article-title":"Transformation of mitochondrial architecture and dynamics in the Chinese soft-shelled turtle during hibernation","volume":"28","author":"Huang","year":"2022","journal-title":"Microsc. Microanal."},{"key":"10.1016\/j.cbpa.2025.111927_bb0090","doi-asserted-by":"crossref","first-page":"22847","DOI":"10.1074\/jbc.M802182200","article-title":"Structural basis for sorting mechanism of p62 in selective autophagy","volume":"283","author":"Ichimura","year":"2008","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.cbpa.2025.111927_bb0095","first-page":"1","article-title":"Location of enzymes of androgen and estrogen biosynthesis in the testis of the ground squirrel (Citellus Lateralis)","volume":"33","author":"Jeffrey","year":"1985","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.cbpa.2025.111927_bb0100","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":"10.1016\/j.cbpa.2025.111927_bb0105","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1095\/biolreprod31.4.637","article-title":"Environmental and endogenous control of reproductive function in the Great Basin pocket mouse Perognathus parvus","volume":"31","author":"Kenagy","year":"1984","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.cbpa.2025.111927_bb0110","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1038\/s41556-018-0176-2","article-title":"Mechanisms of mitophagy in cellular homeostasis, physiology and pathology","volume":"20","author":"Konstantinos","year":"2018","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0115","first-page":"27","article-title":"Mitochondrial contributions to oocyte and embryonic quality in bovine","volume":"7","author":"L","year":"2017","journal-title":"SPERMOVA"},{"key":"10.1016\/j.cbpa.2025.111927_bb0120","doi-asserted-by":"crossref","first-page":"3557","DOI":"10.3390\/ijms22073557","article-title":"Pseudo-starvation driven energy expenditure negatively affects ovarian follicle development","volume":"22","author":"Li","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.cbpa.2025.111927_bb0125","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.theriogenology.2023.02.021","article-title":"METTL3-mediated m6A methylation regulates granulosa cells autophagy during follicular atresia in pig ovaries","volume":"201","author":"Li","year":"2023","journal-title":"Theriogenology"},{"key":"10.1016\/j.cbpa.2025.111927_bb0130","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1038\/s41418-017-0017-z","article-title":"Autophagy induced during apoptosis degrades mitochondria and inhibits type I interferon secretion","volume":"25","author":"Lindqvist","year":"2018","journal-title":"Cell Death Differ."},{"key":"10.1016\/j.cbpa.2025.111927_bb0135","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2023.1123699","article-title":"Seasonal changes in endoplasmic reticulum stress and ovarian steroidogenesis in the muskrats","volume":"14","author":"Lu","year":"2023","journal-title":"Front. Endocrinol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0140","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nbt.1883","article-title":"Full-length transcriptome assembly from RNA-Seq data without a reference genome","volume":"29","author":"Manfred","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0145","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1038\/s41580-020-0210-7","article-title":"The cell biology of mitochondrial membrane dynamics","volume":"21","author":"Marta","year":"2020","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0150","doi-asserted-by":"crossref","first-page":"e21620","DOI":"10.1096\/fj.202100067R","article-title":"Mitochondrial fusion and fission: the fine-tune balance for cellular homeostasis","volume":"35","author":"Mary","year":"2021","journal-title":"FASEB J."},{"key":"10.1016\/j.cbpa.2025.111927_bb0155","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1262\/jrd.18069","article-title":"The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules","volume":"52","author":"Matsuda","year":"2006","journal-title":"J. Reprod. Develop."},{"key":"10.1016\/j.cbpa.2025.111927_bb0160","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1530\/REP-08-0090","article-title":"Follicular development in European ground squirrels (Spermophilus citellus) in different phases of the annual cycle","volume":"136","author":"Millesi","year":"2008","journal-title":"Reproduction"},{"key":"10.1016\/j.cbpa.2025.111927_bb0165","doi-asserted-by":"crossref","first-page":"e12","DOI":"10.1097\/PAI.0000000000000370","article-title":"IHC optical density score: a new practical method for quantitative immunohistochemistry image analysis","volume":"25","author":"Morteza","year":"2017","journal-title":"Appl. Immunohistochem. Mol. Morphol.: AIMM"},{"key":"10.1016\/j.cbpa.2025.111927_bb0170","doi-asserted-by":"crossref","first-page":"1822","DOI":"10.1016\/j.cub.2022.02.032","article-title":"Ground squirrels initiate sexual maturation during hibernation","volume":"32","author":"Rafael","year":"2022","journal-title":"Curr. Biol.: CB"},{"key":"10.1016\/j.cbpa.2025.111927_bb0175","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.theriogenology.2024.06.024","article-title":"Autophagy is involved in granulosa cell death and follicular atresia in ewe ovaries","volume":"226","author":"Scudieri","year":"2024","journal-title":"Theriogenology"},{"key":"10.1016\/j.cbpa.2025.111927_bb0180","first-page":"47","article-title":"Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation","volume":"53","author":"Strauss","year":"2008","journal-title":"Mammal Res."},{"key":"10.1016\/j.cbpa.2025.111927_bb0185","first-page":"1","article-title":"Hormonal orchestra: mastering mitochondria's role in health and disease","author":"Suhaimi","year":"2024","journal-title":"Endocrine"},{"key":"10.1016\/j.cbpa.2025.111927_bb0190","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1016\/0011-2240(88)90296-9","article-title":"Changes in interstitial gland in the ovary of the bat Rinolaphus eurale Blas: arousal from hibernation","volume":"25","author":"Tsvetkov","year":"1988","journal-title":"Cryobiology"},{"key":"10.1016\/j.cbpa.2025.111927_bb0195","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/s00401-020-02234-7","article-title":"Accumulation of amyloid precursor protein C-terminal fragments triggers mitochondrial structure, function, and mitophagy defects in Alzheimer\u2019s disease models and human brains","volume":"141","author":"Vaillant-Beuchot","year":"2021","journal-title":"Acta Neuropathol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0200","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21239210","article-title":"Regulation of Beclin 1-mediated autophagy by oncogenic tyrosine kinases","volume":"21","author":"Vega-Rub\u00edn-de-Celis","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.cbpa.2025.111927_bb0205","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1038\/s41556-018-0133-0","article-title":"Mitochondrial dynamics in adaptive and maladaptive cellular stress responses","volume":"20","author":"Ver\u00f3nica","year":"2018","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.cbpa.2025.111927_bb0210","first-page":"75","article-title":"Seasonal expressions of androgen receptor, estrogen receptors and cytochrome P450 aromatase in the uteri of the wild Daurian ground squirrels","volume":"62","author":"Wang","year":"2018","journal-title":"Eur. J. Histochem."},{"key":"10.1016\/j.cbpa.2025.111927_bb0215","article-title":"High levels of mitochondrial dynamics, autophagy, and apoptosis contribute to stable testicular status in hibernating Daurian ground squirrels","volume":"111705","author":"Wang","year":"2024","journal-title":"Comp. Biochem. Phys. A"},{"key":"10.1016\/j.cbpa.2025.111927_bb0220","doi-asserted-by":"crossref","first-page":"3227","DOI":"10.1093\/hmg\/ddr235","article-title":"The PINK1\/Parkin pathway regulates mitochondrial dynamics and function in mammalian hippocampal and dopaminergic neurons","volume":"20","author":"Wendou","year":"2011","journal-title":"Hum. Mol. Genet."},{"key":"10.1016\/j.cbpa.2025.111927_bb0225","article-title":"Seasonal expressions of ER\u03b1, ER\u03b2, EGF, EGFR, PI3K and Akt in the scent glands of the muskrats","volume":"213","author":"Xie","year":"2021","journal-title":"J. Steroid Biochem."},{"key":"10.1016\/j.cbpa.2025.111927_bb0230","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1042\/CS20220408","article-title":"Ferredoxin 1 regulates granulosa cell apoptosis and autophagy in polycystic ovary syndrome","volume":"137","author":"Xing","year":"2023","journal-title":"Clin. Sci."},{"key":"10.1016\/j.cbpa.2025.111927_bb0235","doi-asserted-by":"crossref","first-page":"12854","DOI":"10.3390\/ijms241612854","article-title":"Melatonin attenuates oxidative stress-induced apoptosis of bovine ovarian granulosa cells by promoting Mitophagy via SIRT1\/FoxO1 signaling pathway. International Jou","volume":"24","author":"Xu","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"10.1016\/j.cbpa.2025.111927_bb0240","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1186\/s12929-018-0438-0","article-title":"Germ cell depletion from mammalian ovary: possible involvement of apoptosis and autophagy","volume":"25","author":"Yadav","year":"2018","journal-title":"J. Biomed. Sci."},{"key":"10.1016\/j.cbpa.2025.111927_bb0245","doi-asserted-by":"crossref","first-page":"2522","DOI":"10.4081\/ejh.2015.2522","article-title":"Testicular expression of NGF, TrkA and p75 during seasonal spermatogenesis of the wild ground squirrel (Citellus dauricus Brandt)","volume":"59","author":"Zhang","year":"2015","journal-title":"Eur. J. Histochem."},{"key":"10.1016\/j.cbpa.2025.111927_bb0250","doi-asserted-by":"crossref","first-page":"8187","DOI":"10.1038\/s41467-023-43889-6","article-title":"GRAF1 integrates PINK1-Parkin signaling and actin dynamics to mediate cardiac mitochondrial","volume":"14","author":"Zhu","year":"2023","journal-title":"Nat. Commun."}],"container-title":["Comparative Biochemistry and Physiology Part A: Molecular &amp; Integrative Physiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1095643325001266?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1095643325001266?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,5,11]],"date-time":"2026-05-11T17:08:03Z","timestamp":1778519283000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1095643325001266"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12]]},"references-count":50,"alternative-id":["S1095643325001266"],"URL":"https:\/\/doi.org\/10.1016\/j.cbpa.2025.111927","relation":{},"ISSN":["1095-6433"],"issn-type":[{"value":"1095-6433","type":"print"}],"subject":[],"published":{"date-parts":[[2025,12]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Up-regulation of cell apoptosis, autophagy and mitochondrial dynamics in ovarian granulosa cells of Daurian ground squirrels during the pre-hibernation period","name":"articletitle","label":"Article Title"},{"value":"Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.cbpa.2025.111927","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 Elsevier Inc. All rights are reserved, including those for text and data mining, AI training, and similar technologies.","name":"copyright","label":"Copyright"}],"article-number":"111927"}}