{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,16]],"date-time":"2026-01-16T02:11:03Z","timestamp":1768529463902,"version":"3.49.0"},"reference-count":99,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T00:00:00Z","timestamp":1768435200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Institute of Cytology RAS","award":["124022700004-0"],"award-info":[{"award-number":["124022700004-0"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JDB"],"abstract":"<jats:p>Cumulus cells (CCs) are a distinct population of granulosa cells (GCs) that surround the developing and ovulated mammalian oocyte. The features of their structural organization and the expression pattern of key genes significantly affect oocyte viability. Changes in the functional activity of the nucleus are often expressed in changes in the structure of nuclear bodies (NBs), including Cajal bodies (CBs). The diagnostic protein of CBs is coilin, which maintains their structural integrity. Using fluorescent and electron microscopy, we examined maternal aging-associated changes in coilin pattern in mouse CCs. We found that older mice had a decrease in the number of coilin-positive bodies, while external transcriptome data analysis revealed no significant changes in Coil and Smn1 gene expression. We hypothesized that the age-related dynamics of coilin-containing bodies are determined not by changes in the expression level of key components of these bodies, but by age-related changes in CC metabolism. Considering that CCs are a by-product of IVF protocols, making them available for analysis in sufficient quantities, age-related changes in the number and size of coilin-positive NBs in CCs may serve as a promising biomarker for assessing ovarian functional aging.<\/jats:p>","DOI":"10.3390\/jdb14010006","type":"journal-article","created":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T08:26:36Z","timestamp":1768465596000},"page":"6","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Female Aging Affects Coilin Pattern in Mouse Cumulus Cells"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-3213-7082","authenticated-orcid":false,"given":"Alexey S.","family":"Anisimov","sequence":"first","affiliation":[{"name":"Department of Cytology and Histology, Faculty of Biology, Saint Petersburg State University, 199034 St. Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7179-9487","authenticated-orcid":false,"given":"Dmitry S.","family":"Bogolyubov","sequence":"additional","affiliation":[{"name":"Institute of Cytology of the Russian Academy of Sciences, 194064 St. Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0795-8222","authenticated-orcid":false,"given":"Irina O.","family":"Bogolyubova","sequence":"additional","affiliation":[{"name":"Institute of Cytology of the Russian Academy of Sciences, 194064 St. Petersburg, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2026,1,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1007\/s43032-021-00829-3","article-title":"The future of IVF: The new normal in human reproduction","volume":"29","author":"Kushnir","year":"2022","journal-title":"Reprod. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"24","DOI":"10.31080\/ASWH.2020.02.0146","article-title":"Follicular fluid aspiration and oocyte retrieval techniques, several flushing, difficulty situations damage risk to the cumulus complex and complications","volume":"2","author":"Zarqaoui","year":"2020","journal-title":"Acta Sci. Women\u2019s Health"},{"key":"ref_3","first-page":"43","article-title":"Cumulus cells","volume":"Volume 2","author":"Skinner","year":"2018","journal-title":"Encyclopedia of Reproduction"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"A471","DOI":"10.1016\/j.autrev.2011.11.010","article-title":"Ovarian failure and polycystic ovary syndrome","volume":"11","year":"2012","journal-title":"Autoimmun. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1210\/er.2015-1104","article-title":"The pathogenesis of polycystic ovary syndrome (PCOS): The hypothesis of PCOS as functional ovarian hyperandrogenism revisited","volume":"37","author":"Rosenfield","year":"2016","journal-title":"Endocr. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Dridi, M., Chraiet, N., Batti, R., Ayadi, M., Mokrani, A., Meddeb, K., Yahiaoui, Y., Raies, H., and Mezlini, A. (2018). Granulosa cell tumor of the ovary: A retrospective study of 31 cases and a review of the literature. Int. J. Surg. Oncol., 2018.","DOI":"10.1155\/2018\/4547892"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1097\/PGP.0000000000000325","article-title":"Granulosa cell tumors: Novel predictors of recurrence in early-stage patients","volume":"36","author":"Sakr","year":"2017","journal-title":"Int. J. Gynecol. Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Shi, W., Wang, D., Xue, X., Qiao, S., Zhang, W., Shi, J., and Huang, C. (2024). Epigenomic landscape of human cumulus cells in premature ovarian insufficiency using single-base resolution methylome and hydroxymethylome. J. Cell. Mol. Med., 28.","DOI":"10.1111\/jcmm.70284"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1007\/s10815-023-02984-9","article-title":"Biomarkers assessing the role of cumulus cells on IVF outcomes: A systematic review","volume":"41","author":"Massoud","year":"2024","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s10577-006-1086-x","article-title":"Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks","volume":"14","author":"Albiez","year":"2006","journal-title":"Chromosome Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3425","DOI":"10.1091\/mbc.10.10.3425","article-title":"Coilin shuttles between the nucleus and cytoplasm in Xenopus oocytes","volume":"10","author":"Bellini","year":"1999","journal-title":"Mol. Biol. Cell"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1080\/15476286.2015.1034923","article-title":"Coilin: The first 25 years","volume":"12","author":"Machyna","year":"2015","journal-title":"RNA Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2461","DOI":"10.1091\/mbc.02-03-0034","article-title":"Large-scale isolation of Cajal bodies from HeLa cells","volume":"13","author":"Lam","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1146\/annurev.cellbio.16.1.273","article-title":"Cajal bodies: The first 100 years","volume":"16","author":"Gall","year":"2000","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1080\/15476286.2016.1243648","article-title":"Specific genomic cues regulate Cajal body assembly","volume":"14","author":"Sawyer","year":"2017","journal-title":"RNA Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1080\/15476286.2016.1231359","article-title":"Cajal bodies and snRNPs\u2014Friends with benefits","volume":"14","year":"2017","journal-title":"RNA Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1002\/wrna.1139","article-title":"Cajal bodies: Where form meets function","volume":"4","author":"Machyna","year":"2013","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Stan\u011bk, D. (2023). Coilin and Cajal bodies. Nucleus, 14.","DOI":"10.1080\/19491034.2023.2256036"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev-biochem-011116-110806","article-title":"Cellular homeostasis and aging","volume":"85","author":"Hartl","year":"2016","journal-title":"Annu. Rev. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"16083","DOI":"10.1038\/ncomms16083","article-title":"Small nucleoli are a cellular hallmark of longevity","volume":"8","author":"Tiku","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4959","DOI":"10.18632\/aging.204107","article-title":"Time makes histone H3 modifications drift in mouse liver","volume":"14","author":"Hillje","year":"2022","journal-title":"Aging"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1093\/biolre\/ioab241","article-title":"Age-associated changes in cumulus cells and follicular fluid: The local oocyte microenvironment as a determinant of gamete quality","volume":"106","author":"Babayev","year":"2022","journal-title":"Biol. Reprod."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"El Osmani, N., Pr\u00e9vostel, C., Picque Lasorsa, L., El Harakeh, M., Radwan, Z., Mawlawi, H., El Sabban, M., Shirinian, M., and Dassouki, Z. (2024). Vitamin C enhances co-localization of novel TET1 nuclear bodies with both Cajal and PML bodies in colorectal cancer cells. Epigenetics, 19.","DOI":"10.1080\/15592294.2024.2337142"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"21320","DOI":"10.1074\/jbc.M115.659359","article-title":"Dynamics of human telomerase holoenzyme assembly and subunit exchange across the cell cycle","volume":"290","author":"Vogan","year":"2015","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/j.molcel.2007.07.020","article-title":"Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation","volume":"27","author":"Cristofari","year":"2007","journal-title":"Mol. Cell"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Rubtsova, M., and Dontsova, O. (2020). Human telomerase RNA: Telomerase component or more?. Biomolecules, 10.","DOI":"10.3390\/biom10060873"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1840","DOI":"10.1093\/bioinformatics\/btt276","article-title":"TANGO: A generic tool for high-throughput 3D image analysis for studying nuclear organization","volume":"29","author":"Ollion","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_28","unstructured":"(2025, November 20). Zenodo. Available online: https:\/\/zenodo.org\/records\/15395330."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/s43587-023-00552-5","article-title":"A single-cell atlas of the aging mouse ovary","volume":"4","author":"Isola","year":"2024","journal-title":"Nat. Aging"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/978-1-4939-6988-3_10","article-title":"Detection of RNA polymerase II in mouse embryos during zygotic genome activation using immunocytochemistry","volume":"1605","author":"Bogolyubova","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1407","DOI":"10.1084\/jem.173.6.1407","article-title":"Human antibody to a novel protein of the nuclear coiled body: Immunological characterization and cDNA cloning of p80-coilin","volume":"173","author":"Andrade","year":"1991","journal-title":"J. Exp. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1007\/s10577-008-1236-4","article-title":"Spatial quantitative analysis of fluorescently labeled nuclear structures: Problems, methods, pitfalls","volume":"16","author":"Ronneberger","year":"2008","journal-title":"Chromosome Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1038\/s41587-023-01767-y","article-title":"Dictionary learning for integrative, multimodal and scalable single-cell analysis","volume":"42","author":"Hao","year":"2024","journal-title":"Nat. Biotechnol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/s13059-015-0844-5","article-title":"MAST: A flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data","volume":"16","author":"Finak","year":"2015","journal-title":"Genome Biol."},{"key":"ref_35","unstructured":"(2025, November 20). Bioconductor. Available online: https:\/\/bioconductor.org\/packages\/release\/data\/annotation\/html\/org.Mm.eg.db.html."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/S0022-5320(69)80017-1","article-title":"Fine structural organization of the interphase nucleus in some mammalian cells","volume":"27","author":"Monneron","year":"1969","journal-title":"J. Ultrastruct. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1006\/dbio.2001.0216","article-title":"Intercellular communication via connexin 43 gap junctions is required for ovarian folliculogenesis in the mouse","volume":"233","author":"Ackert","year":"2001","journal-title":"Dev. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1186\/s12958-015-0091-3","article-title":"Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development","volume":"13","author":"Li","year":"2015","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1080\/19396368.2020.1725685","article-title":"Versican expression level in cumulus cells is associated with human oocyte developmental competence","volume":"66","author":"Shen","year":"2020","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.mce.2010.07.019","article-title":"ADAMTS-1: A new human ovulatory gene and a cumulus marker for fertilization capacity","volume":"328","author":"Yung","year":"2010","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1095\/biolreprod.106.057471","article-title":"Oocyte-secreted factor activation of SMAD 2\/3 signaling enables initiation of mouse cumulus cell expansion","volume":"76","author":"Dragovic","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"365","DOI":"10.4103\/0366-6999.198931","article-title":"Ovarian fibrosis: A phenomenon of concern","volume":"130","author":"Zhou","year":"2017","journal-title":"Chin. Med. J."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Jiang, D., Guo, B., Lin, F., Hui, Q., and Tao, K. (2020). Effect of THBS1 on the biological function of hypertrophic scar fibroblasts. BioMed Res. Int., 2020.","DOI":"10.1155\/2020\/8605407"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Wang, H., Zhou, Z., Liu, Y., Wang, P., Chen, L., Qi, S., Xie, J., and Tang, J. (2022). Identification and validation of HOXD3 and UNC5C as molecular signatures in keloid based on weighted gene co-expression network analysis. Genomics, 114.","DOI":"10.1016\/j.ygeno.2022.110403"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Shang, Y., Li, Y., Han, D., Deng, K., Gao, W., and Wu, M. (2025). LRRC4 deficiency drives premature ovarian insufficiency by disrupting metabolic homeostasis in granulosa cells. Adv. Sci., 12.","DOI":"10.1002\/advs.202417717"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1016\/j.kint.2016.06.032","article-title":"Loss of endogenous thymosin \u03b24 accelerates glomerular disease","volume":"90","author":"Vasilopoulou","year":"2016","journal-title":"Kidney Int."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1016\/j.expneurol.2010.02.005","article-title":"EphA4 deficient mice maintain astroglial\u2013fibrotic scar formation after spinal cord injury","volume":"223","author":"Herrmann","year":"2010","journal-title":"Exp. Neurol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Zhu, S., Hou, S., Lu, Y., Sheng, W., Cui, Z., Dong, T., Feng, H., and Wan, Q. (2021). USP36-mediated deubiquitination of DOCK4 contributes to the diabetic renal tubular epithelial cell injury via Wnt\/\u03b2-catenin signaling pathway. Front. Cell Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.638477"},{"key":"ref_49","first-page":"61","article-title":"Review on the role of glutathione on oxidative stress and infertility","volume":"22","author":"Adeoye","year":"2018","journal-title":"JBRA Assist. Reprod."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Lu, L., Pandey, A.K., Houseal, M.T., and Mulligan, M.K. (2016). The genetic architecture of murine glutathione transferases. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0148230"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Arrigo, A., Regua, A.T., Najjar, M.K., and Lo, H.-W. (2023). Tumor Suppressor Candidate 2 (TUSC2): Discovery, functions, and cancer therapy. Cancers, 15.","DOI":"10.3390\/cancers15092455"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Zhang, K., Zhao, Y., Chen, X., Li, Y., Lan, T., Chang, M., Wang, W., Wang, C., Zhuang, X., and Zhang, B. (2025). p53 promote oxidative stress, neuroinflammation and behavioral disorders via DDIT4-NF-\u03baB signaling pathway. Redox Biol., 86.","DOI":"10.1016\/j.redox.2025.103836"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1038\/s41586-023-06049-w","article-title":"Structural basis of catalytic activation in human splicing","volume":"617","author":"Cretu","year":"2023","journal-title":"Nature"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.tibs.2015.03.005","article-title":"Integrator: Surprisingly diverse functions in gene expression","volume":"40","author":"Baillat","year":"2015","journal-title":"Trends Biochem. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/s00412-006-0056-6","article-title":"The Cajal body: A meeting place for spliceosomal snRNPs in the nuclear maze","volume":"115","author":"Neugebauer","year":"2006","journal-title":"Chromosoma"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2534","DOI":"10.1091\/mbc.e07-12-1259","article-title":"Spliceosomal small nuclear ribonucleoprotein particles repeatedly cycle through Cajal bodies","volume":"19","author":"Wen","year":"2008","journal-title":"Mol. Biol. Cell"},{"key":"ref_57","first-page":"939","article-title":"The SMN Tudor SIM-like domain is key to SmD1 and coilin interactions and to Cajal body biogenesis","volume":"127","author":"Tapia","year":"2014","journal-title":"J. Cell Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"R862","DOI":"10.1016\/S0960-9822(01)00517-6","article-title":"Macromolecular complexes: SMN\u2014The master assembler","volume":"11","author":"Terns","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1006\/jsbi.2000.4234","article-title":"Structure and characterization of the murine p80 coilin gene","volume":"129","author":"Tucker","year":"2000","journal-title":"Coil. J. Struct. Biol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Turathum, B., Gao, E.-M., and Chian, R.-C. (2021). The function of cumulus cells in oocyte growth and maturation and in subsequent ovulation and fertilization. Cells, 10.","DOI":"10.3390\/cells10092292"},{"key":"ref_61","unstructured":"Fox, J.G., Barthold, S.W., Davisson, M.T., Newcomer, C.E., Quimby, F.W., and Smith, A.L. (2007). The mouse in aging research. The Mouse in Biomedical Research, American College Laboratory Animal Medicine. [2nd ed.]."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1038\/s43587-024-00769-y","article-title":"Hallmarks of female reproductive aging in physiologic aging mice","volume":"4","author":"Balough","year":"2024","journal-title":"Nat. Aging"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.rbmo.2009.04.002","article-title":"Assisted reproduction in women over 40 years of age: How old is too old?","volume":"19","author":"Hourvitz","year":"2009","journal-title":"Reprod. BioMed. Online"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1111\/j.1479-828X.1994.tb01267.x","article-title":"The impact of maternal age on clinical pregnancy and spontaneous abortion in women undergoing in vitro fertilization and gamete intra-fallopian transfer","volume":"34","author":"Kenny","year":"1994","journal-title":"Aust. N. Z. J. Obstet. Gynaecol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/0014-4827(92)90068-J","article-title":"Nuclear bodies (NBs): A newly \u201crediscovered\u201d organelle","volume":"202","author":"Brasch","year":"1992","journal-title":"Exp. Cell Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.gde.2011.11.004","article-title":"A view of nuclear Polycomb bodies","volume":"22","author":"Pirrotta","year":"2012","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"219","DOI":"10.4161\/nucl.2.3.15737","article-title":"Fine structure of the \u201cPcG body\u201d in human U-2 OS cells established by correlative light-electron microscopy","volume":"2","author":"Juda","year":"2011","journal-title":"Nucleus"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1038\/nsmb.1783","article-title":"Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis","volume":"17","author":"Strzelecka","year":"2010","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1080\/15476286.2016.1255397","article-title":"Activation of transcription enforces the formation of distinct nuclear bodies in zebrafish embryos","volume":"14","author":"Heyn","year":"2017","journal-title":"RNA Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2298","DOI":"10.1101\/gad.829500","article-title":"Cell cycle-regulated phosphorylation of p220 (NPAT) by cyclin E\/Cdk2 in Cajal bodies promotes histone gene transcription","volume":"14","author":"Ma","year":"2000","journal-title":"Genes Dev."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2283","DOI":"10.1101\/gad.827700","article-title":"NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription","volume":"14","author":"Zhao","year":"2000","journal-title":"Genes Dev."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1080\/15476286.2016.1265198","article-title":"Coordinating cell cycle-regulated histone gene expression through assembly and function of the Histone Locus Body","volume":"14","author":"Duronio","year":"2017","journal-title":"RNA Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"14802","DOI":"10.1073\/pnas.0604225103","article-title":"FLASH is an essential component of Cajal bodies","volume":"103","author":"Barcaroli","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1071\/RD9960935","article-title":"Alterations in the cell cycle of mouse cumulus granulosa cells during expansion and mucification in vivo and in vitro","volume":"8","author":"Schuetz","year":"1996","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1561","DOI":"10.1083\/jcb.151.7.1561","article-title":"In Vivo analysis of Cajal body movement, separation, and joining in live human cells","volume":"151","author":"Platani","year":"2000","journal-title":"J. Cell Biol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1006\/excr.1998.4135","article-title":"Dynamic interaction between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein","volume":"243","author":"Sleeman","year":"1998","journal-title":"Exp. Cell Res."},{"key":"ref_77","first-page":"739","article-title":"The Cajal body and the nucleolus: \u201cIn a relationship\u201d or \u201cIt\u2019s complicated\u201d?","volume":"14","author":"Sleeman","year":"2016","journal-title":"RNA Biol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1091\/mbc.e10-08-0731","article-title":"Coilin participates in the suppression of RNA polymerase I in response to cisplatin-induced DNA damage","volume":"22","author":"Gilder","year":"2011","journal-title":"Mol. Biol. Cell"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1016\/S0962-8924(99)01606-2","article-title":"Nuclear bodies: Multifaceted subdomains of the interchromatin space","volume":"9","author":"Matera","year":"1999","journal-title":"Trends Cell Biol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.molcel.2014.10.004","article-title":"The coilin interactome identifies hundreds of small noncoding RNAs that traffic through Cajal bodies","volume":"56","author":"Machyna","year":"2014","journal-title":"Mol. Cell"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1080\/15476286.2016.1243646","article-title":"Assembly and trafficking of box C\/D and H\/ACA snoRNPs","volume":"14","author":"Massenet","year":"2017","journal-title":"RNA Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"5775","DOI":"10.1016\/j.cell.2021.10.014","article-title":"RNA promotes the formation of spatial compartments in the nucleus","volume":"184","author":"Quinodoz","year":"2021","journal-title":"Cell"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1083\/jcb.201605049","article-title":"Nuclear bodies: Built to boost","volume":"213","author":"Sawyer","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1002\/jcb.240590408","article-title":"U2 and U1 snRNA gene loci associate with coiled bodies","volume":"59","author":"Smith","year":"1995","journal-title":"J. Cell. Biochem."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1091\/mbc.10.5.1653","article-title":"Coiled bodies preferentially associate with U4, U11, and U12 small nuclear RNA genes in interphase HeLa cells but not with U6 and U7 genes","volume":"10","author":"Jacobs","year":"1999","journal-title":"Mol. Biol. Cell"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1002\/(SICI)1097-4644(19980801)70:2<181::AID-JCB4>3.0.CO;2-K","article-title":"Of coiled bodies, gems, and salmon","volume":"70","author":"Matera","year":"1998","journal-title":"J. Cell. Biochem."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/S0960-9822(99)80066-9","article-title":"Association of snRNA genes with coiled bodies is mediated by nascent snRNA transcripts","volume":"9","author":"Frey","year":"1999","journal-title":"Curr. Biol."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Cadenas, J., Adrados, C.S., Kristensen, S.G., Macklon, K.T., Greve, V.H., Fedder, J., Mamsen, L.S., and Andersen, C.Y. (2025). Transcriptional changes in cumulus cells during in vitro maturation of human oocytes. Mol. Reprod. Dev., 92.","DOI":"10.1002\/mrd.70035"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1016\/j.cell.2006.11.026","article-title":"SnapShot: Cellular bodies","volume":"127","author":"Spector","year":"2006","journal-title":"Cell"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1006\/excr.1994.1106","article-title":"Is the coiled body involved in nucleolar functions?","volume":"211","author":"Malatesta","year":"1994","journal-title":"Exp. Cell Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1096\/fasebj.14.5.828","article-title":"Heterogeneous ectopic RNP-derived structures (HERDS) are markers of transcriptional arrest","volume":"14","author":"Biggiogera","year":"2000","journal-title":"FASEB J."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/j.molcel.2006.07.011","article-title":"A spliceosomal intron binding protein, IBP160, links position-dependent assembly of intron-encoded box C\/D snoRNP to pre-mRNA splicing","volume":"23","author":"Hirose","year":"2006","journal-title":"Mol. Cell"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/nsmb.2951","article-title":"The RNA helicase Aquarius exhibits structural adaptations mediating its recruitment to spliceosomes","volume":"22","author":"De","year":"2015","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.cell.2005.08.019","article-title":"Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II","volume":"123","author":"Baillat","year":"2005","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1242\/jcs.090837","article-title":"The integrator complex is required for integrity of Cajal bodies","volume":"125","author":"Takata","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"4241","DOI":"10.1093\/nar\/gky100","article-title":"Integrator subunit 4 is a \u2018Symplekin-like\u2019 scaffold that associates with INTS9\/11 to form the Integrator cleavage module","volume":"46","author":"Albrecht","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1093\/humupd\/dmy002","article-title":"The importance of DNA repair for maintaining oocyte quality in response to anti-cancer treatments, environmental toxins and maternal ageing","volume":"24","author":"Winship","year":"2018","journal-title":"Hum. Reprod. Update"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1006","DOI":"10.1016\/S0015-0282(02)02951-5","article-title":"The apoptotic profile of human cumulus cells changes with patient age and after exposure to sperm but not in relation to oocyte maturity","volume":"77","author":"Moffatt","year":"2002","journal-title":"Fertil. Steril."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Herencia-Lagunar, E., Carrera-Bravo, C., Castano, E., and Sztacho, M. (2025). Unveiling the role of biomolecular condensates in cellular function and cancer. Adv. Biol. Regul., 98.","DOI":"10.1016\/j.jbior.2025.101104"}],"container-title":["Journal of Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2221-3759\/14\/1\/6\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T09:59:30Z","timestamp":1768471170000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2221-3759\/14\/1\/6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,1,15]]},"references-count":99,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,3]]}},"alternative-id":["jdb14010006"],"URL":"https:\/\/doi.org\/10.3390\/jdb14010006","relation":{},"ISSN":["2221-3759"],"issn-type":[{"value":"2221-3759","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,1,15]]}}}