{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T13:04:44Z","timestamp":1789650284222,"version":"4.0.0"},"reference-count":55,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,3,8]],"date-time":"2024-03-08T00:00:00Z","timestamp":1709856000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,3,8]],"date-time":"2024-03-08T00:00:00Z","timestamp":1709856000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32170973"],"award-info":[{"award-number":["32170973"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32070809"],"award-info":[{"award-number":["32070809"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002855","name":"Ministry of Science and Technology of the People's Republic of China","doi-asserted-by":"publisher","award":["2021ZD0204003"],"award-info":[{"award-number":["2021ZD0204003"]}],"id":[{"id":"10.13039\/501100002855","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell. Mol. Life Sci."],"published-print":{"date-parts":[[2024,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Maintaining genomic stability is a prerequisite for proliferating NPCs to ensure genetic fidelity. Though histone arginine methylation has been shown to play important roles in safeguarding genomic stability, the underlying mechanism during brain development is not fully understood. Protein arginine N-methyltransferase 5 (PRMT5) is a type II protein arginine methyltransferase that plays a role in transcriptional regulation. Here, we identify PRMT5 as a key regulator of DNA repair in response to double-strand breaks (DSBs) during NPC proliferation. <jats:italic>Prmt5<\/jats:italic><jats:sup><jats:italic>F\/F<\/jats:italic><\/jats:sup><jats:italic>; Emx1-Cre<\/jats:italic> (cKO-Emx1) mice show a distinctive microcephaly phenotype, with partial loss of the dorsal medial cerebral cortex and complete loss of the corpus callosum and hippocampus. This phenotype is resulted from DSBs accumulation in the medial dorsal cortex followed by cell apoptosis. Both RNA sequencing and in vitro DNA repair analyses reveal that PRMT5 is required for DNA homologous recombination (HR) repair. PRMT5 specifically catalyzes H3R2me2s in proliferating NPCs in the developing mouse brain to enhance HR-related gene expression during DNA repair. Finally, overexpression of BRCA1 significantly rescues DSBs accumulation and cell apoptosis in PRMT5-deficient NSCs. Taken together, our results show that PRMT5 maintains genomic stability by regulating histone arginine methylation in proliferating NPCs.<\/jats:p>","DOI":"10.1007\/s00018-024-05154-x","type":"journal-article","created":{"date-parts":[[2024,3,8]],"date-time":"2024-03-08T18:02:14Z","timestamp":1709920934000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["PRMT5-mediated homologous recombination repair is essential to maintain genomic integrity of neural progenitor cells"],"prefix":"10.1007","volume":"81","author":[{"given":"Ya-Jun","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian-Bo","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tong","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua-Li","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zi-Xuan","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shi-Lai","family":"Bao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao-Xiao","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8386-8064","authenticated-orcid":false,"given":"Xiao-Juan","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,3,8]]},"reference":[{"issue":"7","key":"5154_CR1","doi-asserted-by":"publisher","first-page":"730","DOI":"10.3390\/genes11070730","volume":"11","author":"CF Charlier","year":"2020","unstructured":"Charlier CF, Martins RAP (2020) Protective mechanisms against DNA replication stress in the nervous system. Genes (Basel) 11(7):730. https:\/\/doi.org\/10.3390\/genes11070730","journal-title":"Genes (Basel)"},{"issue":"11","key":"5154_CR2","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.1038\/nn.3537","volume":"16","author":"PJ McKinnon","year":"2013","unstructured":"McKinnon PJ (2013) Maintaining genome stability in the nervous system. Nat Neurosci 16(11):1523\u20131529. https:\/\/doi.org\/10.1038\/nn.3537","journal-title":"Nat Neurosci"},{"issue":"1","key":"5154_CR3","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/j.yexcr.2014.09.030","volume":"329","author":"A Mazouzi","year":"2014","unstructured":"Mazouzi A, Velimezi G, Loizou JI (2014) DNA replication stress: causes, resolution and disease. Exp Cell Res 329(1):85\u201393. https:\/\/doi.org\/10.1016\/j.yexcr.2014.09.030","journal-title":"Exp Cell Res"},{"issue":"12","key":"5154_CR4","doi-asserted-by":"publisher","first-page":"1180","DOI":"10.1101\/gad.301325.117","volume":"31","author":"PJ McKinnon","year":"2017","unstructured":"McKinnon PJ (2017) Genome integrity and disease prevention in the nervous system. Genes Dev 31(12):1180\u20131194. https:\/\/doi.org\/10.1101\/gad.301325.117","journal-title":"Genes Dev"},{"issue":"13","key":"5154_CR5","doi-asserted-by":"publisher","first-page":"3300","DOI":"10.1111\/febs.16535","volume":"290","author":"X Qing","year":"2023","unstructured":"Qing X, Zhang G, Wang ZQ (2023) DNA damage response in neurodevelopment and neuromaintenance. FEBS J 290(13):3300\u20133310. https:\/\/doi.org\/10.1111\/febs.16535","journal-title":"FEBS J"},{"issue":"1","key":"5154_CR6","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.tcb.2015.07.009","volume":"26","author":"R Ceccaldi","year":"2016","unstructured":"Ceccaldi R, Rondinelli B, D\u2019Andrea AD (2016) Repair pathway choices and consequences at the double-strand break. Trends Cell Biol 26(1):52\u201364. https:\/\/doi.org\/10.1016\/j.tcb.2015.07.009","journal-title":"Trends Cell Biol"},{"issue":"11","key":"5154_CR7","doi-asserted-by":"publisher","first-page":"a012740","DOI":"10.1101\/cshperspect.a012740","volume":"5","author":"M Jasin","year":"2013","unstructured":"Jasin M, Rothstein R (2013) Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol 5(11):a012740. https:\/\/doi.org\/10.1101\/cshperspect.a012740","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"26","key":"5154_CR8","doi-asserted-by":"publisher","first-page":"10017","DOI":"10.1073\/pnas.0602436103","volume":"103","author":"KE Orii","year":"2006","unstructured":"Orii KE, Lee Y, Kondo N, McKinnon PJ (2006) Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc Natl Acad Sci U S A 103(26):10017\u201310022. https:\/\/doi.org\/10.1073\/pnas.0602436103","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"17","key":"5154_CR9","doi-asserted-by":"publisher","first-page":"9780","DOI":"10.3390\/ijms23179780","volume":"23","author":"C Brobbey","year":"2022","unstructured":"Brobbey C, Liu L, Yin S, Gan W (2022) The role of protein arginine methyltransferases in DNA damage response. Int J Mol Sci 23(17):9780. https:\/\/doi.org\/10.3390\/ijms23179780","journal-title":"Int J Mol Sci"},{"issue":"1","key":"5154_CR10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.molcel.2008.12.013","volume":"33","author":"MT Bedford","year":"2009","unstructured":"Bedford MT, Clarke SG (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33(1):1\u201313. https:\/\/doi.org\/10.1016\/j.molcel.2008.12.013","journal-title":"Mol Cell"},{"issue":"24","key":"5154_CR11","doi-asserted-by":"publisher","first-page":"2772","DOI":"10.1101\/gad.606110","volume":"24","author":"WW Tee","year":"2010","unstructured":"Tee WW, Pardo M, Theunissen TW, Yu L, Choudhary JS, Hajkova P, Surani MA (2010) Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev 24(24):2772\u20132777. https:\/\/doi.org\/10.1101\/gad.606110","journal-title":"Genes Dev"},{"issue":"51","key":"5154_CR12","doi-asserted-by":"publisher","first-page":"42995","DOI":"10.1074\/jbc.M112.392746","volume":"287","author":"A Chittka","year":"2012","unstructured":"Chittka A, Nitarska J, Grazini U, Richardson WD (2012) Transcription factor positive regulatory domain 4 (PRDM4) recruits protein arginine methyltransferase 5 (PRMT5) to mediate histone arginine methylation and control neural stem cell proliferation and differentiation. J Biol Chem 287(51):42995\u201343006. https:\/\/doi.org\/10.1074\/jbc.M112.392746","journal-title":"J Biol Chem"},{"issue":"12","key":"5154_CR13","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.tibs.2011.09.001","volume":"36","author":"V Karkhanis","year":"2011","unstructured":"Karkhanis V, Hu YJ, Baiocchi RA, Imbalzano AN, Sif S (2011) Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem Sci 36(12):633\u2013641. https:\/\/doi.org\/10.1016\/j.tibs.2011.09.001","journal-title":"Trends Biochem Sci"},{"issue":"11","key":"5154_CR14","doi-asserted-by":"publisher","first-page":"2041","DOI":"10.1007\/s00018-015-1847-9","volume":"72","author":"N Stopa","year":"2015","unstructured":"Stopa N, Krebs JE, Shechter D (2015) The PRMT5 arginine methyltransferase: many roles in development, cancer and beyond. Cell Mol Life Sci 72(11):2041\u20132059. https:\/\/doi.org\/10.1007\/s00018-015-1847-9","journal-title":"Cell Mol Life Sci"},{"issue":"2","key":"5154_CR15","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/nsmb.2209","volume":"19","author":"V Migliori","year":"2012","unstructured":"Migliori V, Muller J, Phalke S, Low D, Bezzi M, Mok WC, Sahu SK, Gunaratne J, Capasso P, Bassi C, Cecatiello V, De Marco A, Blackstock W, Kuznetsov V, Amati B, Mapelli M, Guccione E (2012) Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat Struct Mol Biol 19(2):136\u2013144. https:\/\/doi.org\/10.1038\/nsmb.2209","journal-title":"Nat Struct Mol Biol"},{"issue":"1","key":"5154_CR16","doi-asserted-by":"publisher","first-page":"100750","DOI":"10.1016\/j.isci.2019.100750","volume":"23","author":"JL Owens","year":"2020","unstructured":"Owens JL, Beketova E, Liu S, Tinsley SL, Asberry AM, Deng X, Huang J, Li C, Wan J, Hu CD (2020) PRMT5 cooperates with pICln to function as a master epigenetic activator of DNA double-strand break repair genes. iScience 23(1):100750. https:\/\/doi.org\/10.1016\/j.isci.2019.100750","journal-title":"iScience"},{"issue":"10","key":"5154_CR17","doi-asserted-by":"publisher","first-page":"2643","DOI":"10.1016\/j.celrep.2018.08.002","volume":"24","author":"PJ Hamard","year":"2018","unstructured":"Hamard PJ, Santiago GE, Liu F, Karl DL, Martinez C, Man N, Mookhtiar AK, Duffort S, Greenblatt S, Verdun RE, Nimer SD (2018) PRMT5 regulates DNA repair by controlling the alternative splicing of histone-modifying enzymes. Cell Rep 24(10):2643\u20132657. https:\/\/doi.org\/10.1016\/j.celrep.2018.08.002","journal-title":"Cell Rep"},{"issue":"5","key":"5154_CR18","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1016\/j.molcel.2017.01.019","volume":"65","author":"TL Clarke","year":"2017","unstructured":"Clarke TL, Sanchez-Bailon MP, Chiang K, Reynolds JJ, Herrero-Ruiz J, Bandeiras TM, Matias PM, Maslen SL, Skehel JM, Stewart GS, Davies CC (2017) PRMT5-dependent methylation of the TIP60 coactivator RUVBL1 is a key regulator of homologous recombination. Mol Cell 65(5):900-916 e7. https:\/\/doi.org\/10.1016\/j.molcel.2017.01.019","journal-title":"Mol Cell"},{"issue":"1","key":"5154_CR19","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1038\/s42003-020-01157-z","volume":"3","author":"JW Hwang","year":"2020","unstructured":"Hwang JW, Kim SN, Myung N, Song D, Han G, Bae GU, Bedford MT, Kim YK (2020) PRMT5 promotes DNA repair through methylation of 53BP1 and is regulated by Src-mediated phosphorylation. Commun Biol 3(1):428. https:\/\/doi.org\/10.1038\/s42003-020-01157-z","journal-title":"Commun Biol"},{"issue":"11","key":"5154_CR20","doi-asserted-by":"publisher","first-page":"1742","DOI":"10.1158\/2159-8290.cd-20-0026","volume":"10","author":"F Pastore","year":"2020","unstructured":"Pastore F, Bhagwat N, Pastore A, Radzisheuskaya A, Karzai A, Krishnan A, Li B, Bowman RL, Xiao W (2020) PRMT5 inhibition modulates E2F1 methylation and gene-regulatory networks leading to therapeutic efficacy in JAK2(V617F)-mutant MPN. Cell Discov 10(11):1742\u20131757. https:\/\/doi.org\/10.1158\/2159-8290.cd-20-0026","journal-title":"Cell Discov"},{"issue":"17","key":"5154_CR21","doi-asserted-by":"publisher","first-page":"1903","DOI":"10.1101\/gad.219899.113","volume":"27","author":"M Bezzi","year":"2013","unstructured":"Bezzi M, Teo SX, Muller J, Mok WC, Sahu SK, Vardy LA, Bonday ZQ, Guccione E (2013) Regulation of constitutive and alternative splicing by PRMT5 reveals a role for Mdm4 pre-mRNA in sensing defects in the spliceosomal machinery. Genes Dev 27(17):1903\u20131916. https:\/\/doi.org\/10.1101\/gad.219899.113","journal-title":"Genes Dev"},{"issue":"6","key":"5154_CR22","doi-asserted-by":"publisher","first-page":"3414","DOI":"10.1093\/cercor\/bhx042","volume":"27","author":"Y Guo","year":"2017","unstructured":"Guo Y, He X, Zhao L, Liu L, Song H, Wang X, Xu J, Ju X, Guo W, Zhu X (2017) G\u03b22 Regulates the multipolar-bipolar transition of newborn neurons in the developing neocortex. Cereb Cortex 27(6):3414\u20133426. https:\/\/doi.org\/10.1093\/cercor\/bhx042","journal-title":"Cereb Cortex"},{"issue":"6","key":"5154_CR23","doi-asserted-by":"publisher","first-page":"183509","DOI":"10.1242\/dev.183509","volume":"147","author":"YF Zhao","year":"2020","unstructured":"Zhao YF, He XX, Song ZF, Guo Y, Zhang YN, Yu HL, He ZX, Xiong WC, Guo W, Zhu XJ (2020) Human antigen R-regulated mRNA metabolism promotes the cell motility of migrating mouse neurons. Development 147(6):183509. https:\/\/doi.org\/10.1242\/dev.183509","journal-title":"Development"},{"issue":"11","key":"5154_CR24","doi-asserted-by":"publisher","first-page":"2005","DOI":"10.1038\/nprot.2012.123","volume":"7","author":"W Guo","year":"2012","unstructured":"Guo W, Patzlaff NE, Jobe EM, Zhao X (2012) Isolation of multipotent neural stem or progenitor cells from both the dentate gyrus and subventricular zone of a single adult mouse. Nat Protoc 7(11):2005\u20132012. https:\/\/doi.org\/10.1038\/nprot.2012.123","journal-title":"Nat Protoc"},{"issue":"10","key":"5154_CR25","doi-asserted-by":"publisher","first-page":"1765","DOI":"10.1016\/j.dnarep.2008.06.018","volume":"7","author":"Z Mao","year":"2008","unstructured":"Mao Z, Bozzella M, Seluanov A, Gorbunova V (2008) Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair (Amst) 7(10):1765\u20131771. https:\/\/doi.org\/10.1016\/j.dnarep.2008.06.018","journal-title":"DNA Repair (Amst)"},{"issue":"6","key":"5154_CR26","doi-asserted-by":"publisher","first-page":"e1000110","DOI":"10.1371\/journal.pgen.1000110","volume":"4","author":"N Bennardo","year":"2008","unstructured":"Bennardo N, Cheng A, Huang N, Stark JM (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4(6):e1000110. https:\/\/doi.org\/10.1371\/journal.pgen.1000110","journal-title":"PLoS Genet"},{"issue":"6","key":"5154_CR27","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1038\/cr.2017.76","volume":"27","author":"X Yao","year":"2017","unstructured":"Yao X, Wang X, Hu X, Liu Z, Liu J, Zhou H, Shen X, Wei Y, Huang Z, Ying W, Wang Y, Nie YH, Zhang CC, Li S, Cheng L, Wang Q, Wu Y, Huang P, Sun Q, Shi L, Yang H (2017) Homology-mediated end joining-based targeted integration using CRISPR\/Cas9. Cell Res 27(6):801\u2013814. https:\/\/doi.org\/10.1038\/cr.2017.76","journal-title":"Cell Res"},{"issue":"9","key":"5154_CR28","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1038\/onc.2016.287","volume":"36","author":"X Deng","year":"2017","unstructured":"Deng X, Shao G, Zhang HT, Li C, Zhang D, Cheng L, Elzey BD, Pili R, Ratliff TL, Huang J, Hu CD (2017) Protein arginine methyltransferase 5 functions as an epigenetic activator of the androgen receptor to promote prostate cancer cell growth. Oncogene 36(9):1223\u20131231. https:\/\/doi.org\/10.1038\/onc.2016.287","journal-title":"Oncogene"},{"issue":"2","key":"5154_CR29","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1006\/bbrc.2000.2870","volume":"273","author":"H Guo","year":"2000","unstructured":"Guo H, Hong S, Jin XL, Chen RS, Avasthi PP, Tu YT, Ivanco TL, Li Y (2000) Specificity and efficiency of Cre-mediated recombination in Emx1-Cre knock-in mice. Biochem Biophys Res Commun 273(2):661\u2013665. https:\/\/doi.org\/10.1006\/bbrc.2000.2870","journal-title":"Biochem Biophys Res Commun"},{"issue":"12","key":"5154_CR30","doi-asserted-by":"publisher","first-page":"1200","DOI":"10.1242\/bio.20122287","volume":"1","author":"H Liang","year":"2012","unstructured":"Liang H, Hippenmeyer S, Ghashghaei HT (2012) A Nestin-cre transgenic mouse is insufficient for recombination in early embryonic neural progenitors. Biol Open 1(12):1200\u20131203. https:\/\/doi.org\/10.1242\/bio.20122287","journal-title":"Biol Open"},{"issue":"12","key":"5154_CR31","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1002\/dvg.20256","volume":"44","author":"S Goebbels","year":"2006","unstructured":"Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44(12):611\u2013621. https:\/\/doi.org\/10.1002\/dvg.20256","journal-title":"Genesis"},{"issue":"3","key":"5154_CR32","first-page":"171","volume":"17","author":"J Bosq","year":"1997","unstructured":"Bosq J, Bourhis J (1997) Bromodeoxyuridine (BrdU) Analysis of cellular proliferation. Ann Pathol 17(3):171\u2013178","journal-title":"Ann Pathol"},{"issue":"1","key":"5154_CR33","doi-asserted-by":"publisher","first-page":"1554","DOI":"10.3390\/ijms15011554","volume":"15","author":"S Barral","year":"2014","unstructured":"Barral S, Beltramo R, Salio C, Aimar P, Lossi L, Merighi A (2014) Phosphorylation of histone H2AX in the mouse brain from development to senescence. Int J Mol Sci 15(1):1554\u20131573. https:\/\/doi.org\/10.3390\/ijms15011554","journal-title":"Int J Mol Sci"},{"issue":"23","key":"5154_CR34","doi-asserted-by":"publisher","first-page":"7198","DOI":"10.3390\/molecules26237198","volume":"26","author":"A Merighi","year":"2021","unstructured":"Merighi A, Gionchiglia N, Granato A, Lossi L (2021) The phosphorylated form of the histone H2AX (gammaH2AX) in the brain from embryonic life to old age. Molecules 26(23):7198. https:\/\/doi.org\/10.3390\/molecules26237198","journal-title":"Molecules"},{"issue":"15","key":"5154_CR35","doi-asserted-by":"publisher","first-page":"6870","DOI":"10.1073\/pnas.1002175107","volume":"107","author":"S de Feraudy","year":"2010","unstructured":"de Feraudy S, Revet I, Bezrookove V, Feeney L, Cleaver JE (2010) A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc Natl Acad Sci U S A 107(15):6870\u20136875. https:\/\/doi.org\/10.1073\/pnas.1002175107","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"5154_CR36","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1158\/1541-7786.mcr-11-0134","volume":"10","author":"D White","year":"2012","unstructured":"White D, Rafalska-Metcalf IU, Ivanov AV, Corsinotti A, Peng H, Lee SC, Trono D, Janicki SM, Rauscher FJ 3rd (2012) The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473\/824 phosphorylation. Mol Cancer Res 10(3):401\u2013414. https:\/\/doi.org\/10.1158\/1541-7786.mcr-11-0134","journal-title":"Mol Cancer Res"},{"issue":"6381","key":"5154_CR37","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1038\/358015a0","volume":"358","author":"DP Lane","year":"1992","unstructured":"Lane DP (1992) Cancer p53, guardian of the genome. Nature 358(6381):15\u201316. https:\/\/doi.org\/10.1038\/358015a0","journal-title":"Nature"},{"issue":"28","key":"5154_CR38","doi-asserted-by":"publisher","first-page":"3943","DOI":"10.1038\/onc.2016.502","volume":"36","author":"M Fischer","year":"2017","unstructured":"Fischer M (2017) Census and evaluation of p53 target genes. Oncogene 36(28):3943\u20133956. https:\/\/doi.org\/10.1038\/onc.2016.502","journal-title":"Oncogene"},{"issue":"12","key":"5154_CR39","doi-asserted-by":"publisher","first-page":"1431","DOI":"10.1038\/ncb1802","volume":"10","author":"M Jansson","year":"2008","unstructured":"Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, Kessler B, La Thangue NB (2008) Arginine methylation regulates the p53 response. Nat Cell Biol 10(12):1431\u20131439. https:\/\/doi.org\/10.1038\/ncb1802","journal-title":"Nat Cell Biol"},{"issue":"6","key":"5154_CR40","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1038\/nchembio.1810","volume":"11","author":"E Chan-Penebre","year":"2015","unstructured":"Chan-Penebre E, Kuplast KG, Majer CR, Boriack-Sjodin PA, Wigle TJ, Johnston LD, Rioux N, Munchhof MJ, Jin L, Jacques SL, West KA, Lingaraj T, Stickland K, Ribich SA, Raimondi A, Scott MP, Waters NJ, Pollock RM, Smith JJ, Barbash O, Pappalardi M, Ho TF, Nurse K, Oza KP, Gallagher KT, Kruger R, Moyer MP, Copeland RA, Chesworth R, Duncan KW (2015) A selective inhibitor of PRMT5 with in vivo and in vitro potency in MCL models. Nat Chem Biol 11(6):432\u2013437. https:\/\/doi.org\/10.1038\/nchembio.1810","journal-title":"Nat Chem Biol"},{"issue":"1","key":"5154_CR41","doi-asserted-by":"publisher","first-page":"3839","DOI":"10.1038\/s41467-020-17551-4","volume":"11","author":"JM Keil","year":"2020","unstructured":"Keil JM, Doyle DZ, Qalieh A, Lam MM, Funk OH, Qalieh Y, Shi L, Mohan N, Sorel A, Kwan KY (2020) Symmetric neural progenitor divisions require chromatin-mediated homologous recombination DNA repair by Ino80. Nat Commun 11(1):3839. https:\/\/doi.org\/10.1038\/s41467-020-17551-4","journal-title":"Nat Commun"},{"key":"5154_CR42","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1146\/annurev-genet-110410-132435","volume":"45","author":"LS Symington","year":"2011","unstructured":"Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247\u2013271. https:\/\/doi.org\/10.1146\/annurev-genet-110410-132435","journal-title":"Annu Rev Genet"},{"issue":"1","key":"5154_CR43","doi-asserted-by":"publisher","first-page":"2840","DOI":"10.1038\/s41467-018-04863-9","volume":"9","author":"A Scaglione","year":"2018","unstructured":"Scaglione A, Patzig J, Liang J, Frawley R, Bok J, Mela A, Yattah C, Zhang J, Teo SX, Zhou T, Chen S, Bernstein E, Canoll P, Guccione E, Casaccia P (2018) PRMT5-mediated regulation of developmental myelination. Nat Commun 9(1):2840. https:\/\/doi.org\/10.1038\/s41467-018-04863-9","journal-title":"Nat Commun"},{"issue":"1","key":"5154_CR44","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1038\/s41467-018-07884-6","volume":"10","author":"LC Litzler","year":"2019","unstructured":"Litzler LC, Zahn A, Meli AP, H\u00e9bert S, Patenaude AM, Methot SP, Sprumont A, Bois T, Kitamura D, Costantino S, King IL, Kleinman CL, Richard S, Noia JM (2019) PRMT5 is essential for B cell development and germinal center dynamics. Nat Commun 10(1):22. https:\/\/doi.org\/10.1038\/s41467-018-07884-6","journal-title":"Nat Commun"},{"key":"5154_CR45","doi-asserted-by":"publisher","first-page":"621","DOI":"10.3389\/fimmu.2020.00621","volume":"11","author":"Y Tanaka","year":"2020","unstructured":"Tanaka Y, Nagai Y, Okumura M, Greene MI, Kambayashi T (2020) PRMT5 is required for T cell survival and proliferation by maintaining cytokine signaling. Front Immunol 11:621. https:\/\/doi.org\/10.3389\/fimmu.2020.00621","journal-title":"Front Immunol"},{"issue":"9","key":"5154_CR46","doi-asserted-by":"publisher","first-page":"2316","DOI":"10.1016\/j.celrep.2019.02.001","volume":"26","author":"DQ Tan","year":"2019","unstructured":"Tan DQ, Li Y, Yang C, Li J, Tan SH, Chin DWL, Nakamura-Ishizu A, Yang H, Suda T (2019) PRMT5 modulates splicing for genome integrity and preserves proteostasis of hematopoietic stem cells. Cell Rep 26(9):2316-2328.e6. https:\/\/doi.org\/10.1016\/j.celrep.2019.02.001","journal-title":"Cell Rep"},{"issue":"10","key":"5154_CR47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s12276-019-0325-0","volume":"51","author":"SY Lee","year":"2019","unstructured":"Lee SY, Vuong TA, Wen X, Jeong HJ, So HK, Kwon I, Kang JS, Cho H (2019) Methylation determines the extracellular calcium sensitivity of the leak channel NALCN in hippocampal dentate granule cells. Exp Mol Med 51(10):1\u201314. https:\/\/doi.org\/10.1038\/s12276-019-0325-0","journal-title":"Exp Mol Med"},{"issue":"8","key":"5154_CR48","doi-asserted-by":"publisher","first-page":"768","DOI":"10.3390\/life11080768","volume":"11","author":"L Halabelian","year":"2021","unstructured":"Halabelian L, Barsyte-Lovejoy D (2021) Structure and function of protein arginine methyltransferase PRMT7. Life (Basel) 11(8):768. https:\/\/doi.org\/10.3390\/life11080768","journal-title":"Life (Basel)"},{"issue":"6","key":"5154_CR49","doi-asserted-by":"publisher","first-page":"1528","DOI":"10.1016\/j.celrep.2016.01.022","volume":"14","author":"RS Blanc","year":"2016","unstructured":"Blanc RS, Vogel G, Chen T, Crist C, Richard S (2016) PRMT7 preserves satellite cell regenerative capacity. Cell Rep 14(6):1528\u20131539. https:\/\/doi.org\/10.1016\/j.celrep.2016.01.022","journal-title":"Cell Rep"},{"issue":"3","key":"5154_CR50","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1038\/nsmb.1568","volume":"16","author":"Q Zhao","year":"2009","unstructured":"Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, Cerruti L, Curtis DJ, Patel DJ, Allis CD, Cunningham JM, Jane SM (2009) PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 16(3):304\u2013311. https:\/\/doi.org\/10.1038\/nsmb.1568","journal-title":"Nat Struct Mol Biol"},{"key":"5154_CR51","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1038\/ncomms1155","volume":"2","author":"Y Arai","year":"2011","unstructured":"Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154. https:\/\/doi.org\/10.1038\/ncomms1155","journal-title":"Nat Commun"},{"issue":"3","key":"5154_CR52","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1002\/ar.1091600311","volume":"160","author":"SP Hicks","year":"1968","unstructured":"Hicks SP, D\u2019Amato CJ (1968) Cell migrations to the isocortex in the rat. Anat Rec 160(3):619\u2013634. https:\/\/doi.org\/10.1002\/ar.1091600311","journal-title":"Anat Rec"},{"key":"5154_CR53","first-page":"1","volume":"144","author":"GM McSherry","year":"1986","unstructured":"McSherry GM, Smart IH (1986) Cell production gradients in the developing ferret isocortex. J Anat 144:1\u201314","journal-title":"J Anat"},{"issue":"11","key":"5154_CR54","doi-asserted-by":"publisher","first-page":"1859","DOI":"10.1242\/dev.033498","volume":"136","author":"JN Pulvers","year":"2009","unstructured":"Pulvers JN, Huttner WB (2009) Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors. Development 136(11):1859\u20131868. https:\/\/doi.org\/10.1242\/dev.033498","journal-title":"Development"},{"issue":"7","key":"5154_CR55","doi-asserted-by":"publisher","first-page":"891","DOI":"10.1016\/s0092-8674(00)81714-6","volume":"95","author":"Y Gao","year":"1998","unstructured":"Gao Y, Sun Y, Frank KM, Dikkes P, Fujiwara Y, Seidl KJ, Sekiguchi JM, Rathbun GA, Swat W, Wang J, Bronson RT, Malynn BA, Bryans M, Zhu C, Chaudhuri J, Davidson L, Ferrini R, Stamato T, Orkin SH, Greenberg ME, Alt FW (1998) A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95(7):891\u2013902. https:\/\/doi.org\/10.1016\/s0092-8674(00)81714-6","journal-title":"Cell"}],"container-title":["Cellular and Molecular Life Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00018-024-05154-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00018-024-05154-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00018-024-05154-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,8]],"date-time":"2024-03-08T18:04:17Z","timestamp":1709921057000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00018-024-05154-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,8]]},"references-count":55,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,12]]}},"alternative-id":["5154"],"URL":"https:\/\/doi.org\/10.1007\/s00018-024-05154-x","relation":{},"ISSN":["1420-682X","1420-9071"],"issn-type":[{"value":"1420-682X","type":"print"},{"value":"1420-9071","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,8]]},"assertion":[{"value":"14 November 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 January 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 February 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 March 2024","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare that they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"All the animal experiments were approved and operated in strict compliance with the requirements of the Institutional Animal Care and Use Committee of the Northeast Normal University, China (NENU\/IACUC, AP20171008).","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"All authors consent to the publication of this study.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}}],"article-number":"123"}}