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ATXN3 has multiple functions, such as regulating transcription or controlling genomic stability after DNA damage. Here we report the role of ATXN3 in chromatin organization during unperturbed conditions, in a catalytic-independent manner. The lack of ATXN3 leads to abnormalities in nuclear and nucleolar morphology, alters DNA replication timing and increases transcription. Additionally, indicators of more open chromatin, such as increased mobility of histone H1, changes in epigenetic marks and higher sensitivity to micrococcal nuclease digestion were detected in the absence of ATXN3. Interestingly, the effects observed in cells lacking ATXN3 are epistatic to the inhibition or lack of the histone deacetylase 3 (HDAC3), an interaction partner of ATXN3. The absence of ATXN3 decreases the recruitment of endogenous HDAC3 to the chromatin, as well as the HDAC3 nuclear\/cytoplasm ratio after HDAC3 overexpression, suggesting that ATXN3 controls the subcellular localization of HDAC3. Importantly, the overexpression of a PolyQ-expanded version of ATXN3 behaves as a null mutant, altering DNA replication parameters, epigenetic marks and the subcellular distribution of HDAC3, giving new insights into the molecular basis of the disease.<\/jats:p>","DOI":"10.1093\/nar\/gkad212","type":"journal-article","created":{"date-parts":[[2023,3,27]],"date-time":"2023-03-27T10:50:49Z","timestamp":1679914249000},"page":"5396-5413","source":"Crossref","is-referenced-by-count":18,"title":["ATXN3 controls DNA replication and transcription by regulating chromatin structure"],"prefix":"10.1093","volume":"51","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0653-3583","authenticated-orcid":false,"given":"Esperanza","family":"Hern\u00e1ndez-Carralero","sequence":"first","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Escuela de Doctorado y Estudios de Posgrado, Universidad de la Laguna , Santa Cruz de Tenerife , Spain"},{"name":"Instituto de Tecnolog\u00edas Biom\u00e9dicas , Centro de Investigaciones Biom\u00e9dicas de Canarias, Facultad de Medicina, Campus Ciencias de la Salud, Universidad de La Laguna, Santa Cruz de Tenerife , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elisa","family":"Cabrera","sequence":"additional","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gara","family":"Rodr\u00edguez-Torres","sequence":"additional","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Escuela de Doctorado y Estudios de Posgrado, Universidad de la Laguna , Santa Cruz de Tenerife , Spain"},{"name":"Instituto de Tecnolog\u00edas Biom\u00e9dicas , Centro de Investigaciones Biom\u00e9dicas de Canarias, Facultad de Medicina, Campus Ciencias de la Salud, Universidad de La Laguna, Santa Cruz de Tenerife , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yeray","family":"Hern\u00e1ndez-Reyes","sequence":"additional","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Escuela de Doctorado y Estudios de Posgrado, Universidad de la Laguna , Santa Cruz de Tenerife , Spain"},{"name":"Instituto de Tecnolog\u00edas Biom\u00e9dicas , Centro de Investigaciones Biom\u00e9dicas de Canarias, Facultad de Medicina, Campus Ciencias de la Salud, Universidad de La Laguna, Santa Cruz de Tenerife , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abhay\u00a0N","family":"Singh","sequence":"additional","affiliation":[{"name":"MRC Oxford Institute for Radiation Oncology, Department of Oncology, University of Oxford , Oxford , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cristina","family":"Santa-Mar\u00eda","sequence":"additional","affiliation":[{"name":"Centro de Biolog\u00eda Molecular Severo Ochoa (CBMSO), Consejo Superior de Investigaciones Cient\u00edficas\/Universidad Aut\u00f3noma de Madrid (CSIC\/UAM) , Madrid , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9\u00a0Miguel","family":"Fern\u00e1ndez-Justel","sequence":"additional","affiliation":[{"name":"Centro de Biolog\u00eda Molecular Severo Ochoa (CBMSO), Consejo Superior de Investigaciones Cient\u00edficas\/Universidad Aut\u00f3noma de Madrid (CSIC\/UAM) , Madrid , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roel\u00a0C","family":"Janssens","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, Oncode Institute, Erasmus MC, University Medical Center Rotterdam , Rotterdam , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9321-518X","authenticated-orcid":false,"given":"Jurgen\u00a0A","family":"Marteijn","sequence":"additional","affiliation":[{"name":"Department of Molecular Genetics, Oncode Institute, Erasmus MC, University Medical Center Rotterdam , Rotterdam , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernd\u00a0O","family":"Evert","sequence":"additional","affiliation":[{"name":"Department of Neurology, University Hospital Bonn , Bonn , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Niels","family":"Mailand","sequence":"additional","affiliation":[{"name":"Protein Signaling Program, Novo Nordisk Foundation Center for Protein Research, University of Copenhagen , Copenhagen, Denmark"},{"name":"Center for Chromosome Stability, Department of Cellular and Molecular Medicine, University of Copenhagen , Copenhagen, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda","family":"G\u00f3mez","sequence":"additional","affiliation":[{"name":"Centro de Biolog\u00eda Molecular Severo Ochoa (CBMSO), Consejo Superior de Investigaciones Cient\u00edficas\/Universidad Aut\u00f3noma de Madrid (CSIC\/UAM) , Madrid , Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5522-021X","authenticated-orcid":false,"given":"Kristijan","family":"Ramadan","sequence":"additional","affiliation":[{"name":"MRC Oxford Institute for Radiation Oncology, Department of Oncology, University of Oxford , Oxford , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9160-4525","authenticated-orcid":false,"given":"Veronique\u00a0A J","family":"Smits","sequence":"additional","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Instituto de Tecnolog\u00edas Biom\u00e9dicas , Centro de Investigaciones Biom\u00e9dicas de Canarias, Facultad de Medicina, Campus Ciencias de la Salud, Universidad de La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Universidad Fernando Pessoa Canarias , Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4473-8894","authenticated-orcid":false,"given":"Raimundo","family":"Freire","sequence":"additional","affiliation":[{"name":"Unidad de Investigaci\u00f3n, Hospital Universitario de Canarias , La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Instituto de Tecnolog\u00edas Biom\u00e9dicas , Centro de Investigaciones Biom\u00e9dicas de Canarias, Facultad de Medicina, Campus Ciencias de la Salud, Universidad de La Laguna, Santa Cruz de Tenerife , Spain"},{"name":"Universidad Fernando Pessoa Canarias , Las Palmas de Gran Canaria, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,3,27]]},"reference":[{"key":"2023062304191829700_B1","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/j.pneurobio.2011.11.006","article-title":"Toward understanding Machado-Joseph disease","volume":"97","author":"Costa","year":"2012","journal-title":"Prog. 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Biol."},{"key":"2023062304191829700_B6","doi-asserted-by":"crossref","first-page":"43563","DOI":"10.1371\/journal.pone.0043563","article-title":"Valosin-containing protein (VCP\/p97) is an activator of wild-type ataxin-3","volume":"7","author":"La\u00e7o","year":"2012","journal-title":"PLoS One"},{"key":"2023062304191829700_B7","doi-asserted-by":"crossref","first-page":"18392","DOI":"10.1074\/jbc.M117.806281","article-title":"Interaction between the AAA atpase p97 and its cofactor ataxin3 in health and disease: nucleotide-induced conformational changes regulate cofactor binding","volume":"292","author":"Rao","year":"2017","journal-title":"J. Biol. Chem."},{"key":"2023062304191829700_B8","doi-asserted-by":"crossref","first-page":"2409","DOI":"10.1093\/hmg\/ddl164","article-title":"Ataxin-3 binds VCP\/p97 and regulates retrotranslocation of ERAD substrates","volume":"15","author":"Zhong","year":"2006","journal-title":"Hum. Mol. Genet."},{"key":"2023062304191829700_B9","doi-asserted-by":"crossref","first-page":"3195","DOI":"10.1093\/hmg\/ddg344","article-title":"The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity","volume":"12","author":"Burnett","year":"2003","journal-title":"Hum. Mol. Genet."},{"key":"2023062304191829700_B10","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1016\/j.bbrc.2007.08.062","article-title":"Inactivation of the mouse Atxn3 (ataxin-3) gene increases protein ubiquitination","volume":"362","author":"Schmitt","year":"2007","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023062304191829700_B11","doi-asserted-by":"crossref","first-page":"3605","DOI":"10.1074\/jbc.M310939200","article-title":"Poly-ubiquitin binding by the polyglutamine disease protein ataxin-3 links its normal function to protein surveillance pathways","volume":"279","author":"Chai","year":"2004","journal-title":"J. Biol. Chem."},{"key":"2023062304191829700_B12","doi-asserted-by":"crossref","first-page":"5389","DOI":"10.1523\/JNEUROSCI.21-15-05389.2001","article-title":"Inflammatory genes are upregulated in expanded ataxin-3-expressing cell lines and spinocerebellar ataxia type 3 brains","volume":"21","author":"Evert","year":"2001","journal-title":"J. Neurosci."},{"key":"2023062304191829700_B13","doi-asserted-by":"crossref","first-page":"1006","DOI":"10.1093\/jnen\/62.10.1006","article-title":"Gene expression profiling in ataxin-3 expressing cell lines reveals distinct effects of normal and mutant ataxin-3","volume":"62","author":"Evert","year":"2003","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"2023062304191829700_B14","doi-asserted-by":"crossref","first-page":"11474","DOI":"10.1523\/JNEUROSCI.2053-06.2006","article-title":"Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase 3, and histone deacetylation","volume":"26","author":"Evert","year":"2006","journal-title":"J. Neurosci."},{"key":"2023062304191829700_B15","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.nbd.2008.03.011","article-title":"Polyglutamine-expanded ataxin-3 causes cerebellar dysfunction of SCA3 transgenic mice by inducing transcriptional dysregulation","volume":"31","author":"Chou","year":"2008","journal-title":"Neurobiol. Dis."},{"key":"2023062304191829700_B16","doi-asserted-by":"crossref","first-page":"e102361","DOI":"10.15252\/embj.2019102361","article-title":"The p97\u2013Ataxin 3 complex regulates homeostasis of the DNA damage response E3 ubiquitin ligase RNF8","volume":"38","author":"Singh","year":"2019","journal-title":"EMBO J."},{"key":"2023062304191829700_B17","doi-asserted-by":"crossref","first-page":"1066","DOI":"10.15252\/embj.201695151","article-title":"Ataxin-3 consolidates the MDC1-dependent DNA double-strand break response by counteracting the SUMO-targeted ubiquitin ligase RNF4","volume":"36","author":"Pfeiffer","year":"2017","journal-title":"EMBO J."},{"key":"2023062304191829700_B18","doi-asserted-by":"crossref","first-page":"4532","DOI":"10.1093\/nar\/gkx095","article-title":"Ataxin-3 promotes genome integrity by stabilizing Chk1","volume":"45","author":"Tu","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"2023062304191829700_B19","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1002\/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X","article-title":"Histone acetylation and an epigenetic code","volume":"22","author":"Turner","year":"2000","journal-title":"Bioessays"},{"key":"2023062304191829700_B20","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.gde.2011.01.022","article-title":"Chromatin higher-order structures and gene regulation","volume":"21","author":"Li","year":"2011","journal-title":"Curr. 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