{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T17:54:33Z","timestamp":1792000473841,"version":"4.4.0"},"reference-count":96,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,4,7]],"date-time":"2023-04-07T00:00:00Z","timestamp":1680825600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Human TOR1AIP1 encodes LAP1, a nuclear envelope protein expressed in most human tissues, which has been linked to various biological processes and human diseases. The clinical spectrum of diseases related to mutations in TOR1AIP1 is broad, including muscular dystrophy, congenital myasthenic syndrome, cardiomyopathy, and multisystemic disease with or without progeroid features. Although rare, these recessively inherited disorders often lead to early death or considerable functional impairment. Developing a better understanding of the roles of LAP1 and mutant TOR1AIP1-associated phenotypes is paramount to allow therapeutic development. To facilitate further studies, this review provides an overview of the known interactions of LAP1 and summarizes the evidence for the function of this protein in human health. We then review the mutations in the TOR1AIP1 gene and the clinical and pathological characteristics of subjects with these mutations. Lastly, we discuss challenges to be addressed in the future.<\/jats:p>","DOI":"10.3390\/ijms24086911","type":"journal-article","created":{"date-parts":[[2023,4,10]],"date-time":"2023-04-10T03:26:06Z","timestamp":1681097166000},"page":"6911","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["TOR1AIP1-Associated Nuclear Envelopathies"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2132-3736","authenticated-orcid":false,"given":"Laurane","family":"Mackels","sequence":"first","affiliation":[{"name":"MDUK Oxford Neuromuscular Center, Department of Paediatrics, University of Oxford, Oxford OX3 9DU, UK"},{"name":"Adult Neurology Department, Citadelle Hospital, 4000 Li\u00e8ge, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xincheng","family":"Liu","sequence":"additional","affiliation":[{"name":"MDUK Oxford Neuromuscular Center, Department of Paediatrics, University of Oxford, Oxford OX3 9DU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2516-3258","authenticated-orcid":false,"given":"Gis\u00e8le","family":"Bonne","sequence":"additional","affiliation":[{"name":"Sorbonne University, INSERM, Institut de Myologie, Centre de Recherche en Myologie, 75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9270-4061","authenticated-orcid":false,"given":"Laurent","family":"Servais","sequence":"additional","affiliation":[{"name":"Neuromuscular Center, Division of Paediatrics, University Hospital of Li\u00e8ge, University of Li\u00e8ge, 4000 Li\u00e8ge, Belgium"},{"name":"MDUK Oxford Neuromuscular Center, Department of Paediatrics, NIHR Oxford Biomedical Research Centre, University of Oxford, Oxford OX3 9DU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2029","DOI":"10.1083\/jcb.107.6.2029","article-title":"Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina","volume":"107","author":"Senior","year":"1988","journal-title":"J. Cell Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1016\/S0006-291X(02)00563-6","article-title":"Molecular cloning of one isotype of human lamina-associated polypeptide 1s and a topological analysis using its deletion mutants","volume":"294","author":"Kondo","year":"2002","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1186\/s13023-014-0174-9","article-title":"Severe dystonia, cerebellar atrophy, and cardiomyopathy likely caused by a missense mutation in TOR1AIP1","volume":"9","author":"Dorboz","year":"2014","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e12743","DOI":"10.1111\/nan.12743","article-title":"A TOR1AIP1 variant segregating with an early onset limb girdle myasthenia\u2014Support for the role of LAP1 in NMJ function and disease","volume":"48","author":"Malfatti","year":"2021","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s10048-020-00632-3","article-title":"Selective loss of a LAP1 isoform causes a muscle-specific nuclear envelopathy","volume":"22","author":"Lornage","year":"2021","journal-title":"Neurogenetics"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Feng, X., Wu, J., Xian, W., Liao, B., Liao, S., Yao, X., and Zhang, W. (2020). Muscular involvement and tendon contracture in limb-girdle muscular dystrophy 2Y: A mild adult phenotype and literature review. BMC Musculoskelet. Disord., 21.","DOI":"10.1186\/s12891-020-03616-4"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"fcaa174","DOI":"10.1093\/braincomms\/fcaa174","article-title":"Congenital myasthenic syndrome due to a TOR1AIP1 mutation: A new disease pathway for impaired synaptic transmission","volume":"2","author":"Cossins","year":"2020","journal-title":"Brain Commun."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1016\/j.nmd.2016.05.013","article-title":"TOR1AIP1 as a cause of cardiac failure and recessive limb-girdle muscular dystrophy","volume":"26","author":"Ghaoui","year":"2016","journal-title":"Neuromuscul. Disord."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/s00439-019-02105-6","article-title":"Two novel cases further expand the phenotype of TOR1AIP1-associated nuclear envelopathies","volume":"139","author":"Lessel","year":"2020","journal-title":"Hum. Genet."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1038\/s41467-019-08493-7","article-title":"Combined loss of LAP1B and LAP1C results in an early onset multisystemic nuclear envelopathy","volume":"10","author":"Fichtman","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.clinimag.2019.06.010","article-title":"Magnetic Resonance Imaging characteristics in case of TOR1AIP1 muscular dystrophy","volume":"58","author":"Bhatia","year":"2019","journal-title":"Clin. Imaging"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/j.nmd.2014.04.007","article-title":"Mutation in TOR1AIP1 encoding LAP1B in a form of muscular dystrophy: A novel gene related to nuclear envelopathies","volume":"24","author":"Talim","year":"2014","journal-title":"Neuromuscul. Disord."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Santos, M., Domingues, S.C., Costa, P., Muller, T., Galozzi, S., Marcus, K., da Cruz e Silva, E.F., da Cruz e Silva, O.A., and Rebelo, S. (2014). Identification of a Novel Human LAP1 Isoform That Is Regulated by Protein Phosphorylation. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0113732"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1007\/s10038-005-0261-9","article-title":"Frequent occurrence of protein isoforms with or without a single amino acid residue by subtle alternative splicing: The case of Gln in DRPLA affects subcellular localization of the products","volume":"50","author":"Tadokoro","year":"2005","journal-title":"J. Hum. Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1016\/0092-8674(93)90355-T","article-title":"Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation","volume":"73","author":"Foisner","year":"1993","journal-title":"Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"8822","DOI":"10.1074\/jbc.270.15.8822","article-title":"cDNA Cloning and Characterization of Lamina-associated Polypeptide 1C (LAP1C), an Integral Protein of the Inner Nuclear Membrane","volume":"270","author":"Martin","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1083\/jcb.200411026","article-title":"The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein","volume":"168","author":"Goodchild","year":"2005","journal-title":"J. Cell Biol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Santos, M., Rebelo, S., Van Kleeff, P.J.M., Kim, C.E., Dauer, W.T., Fardilha, M., da Cruz e Silva, O.A., and da Cruz e Silva, E.F. (2013). The Nuclear Envelope Protein, LAP1B, Is a Novel Protein Phosphatase 1 Substrate. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076788"},{"key":"ref_19","first-page":"65","article-title":"Lamina-associated polypeptide 1 is dispensable for embryonic myogenesis but required for postnatal skeletal muscle growth","volume":"26","author":"Shin","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.semcdb.2014.01.010","article-title":"Lamina-associated polypeptide 1: Protein interactions and tissue-selective functions","volume":"29","author":"Shin","year":"2014","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1006\/jsbi.2000.4216","article-title":"Review: Nuclear Lamins\u2014Structural Proteins with Fundamental Functions","volume":"129","author":"Gruenbaum","year":"2000","journal-title":"J. Struct. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0074-7696(03)01001-5","article-title":"The Nuclear Lamina and Its Functions in the Nucleus","volume":"226","author":"Gruenbaum","year":"2003","journal-title":"Int. Rev. Cytol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1038\/nrm879","article-title":"Life at the edge: The nuclear envelope and human disease","volume":"3","author":"Burke","year":"2002","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1083\/jcb.153.3.479","article-title":"Involvement of the Lamin Rod Domain in Heterotypic Lamin Interactions Important for Nuclear Organization","volume":"153","author":"Schirmer","year":"2001","journal-title":"J. Cell Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1615\/CritRevEukarGeneExpr.v9.i3-4.130","article-title":"The Nuclear Lamina: Molecular Organization and Interaction with Chromatin","volume":"9","author":"Goldberg","year":"1999","journal-title":"Crit. Rev. Eukaryot. Gene Expr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1380","DOI":"10.1126\/science.1088176","article-title":"Nuclear Membrane Proteins with Potential Disease Links Found by Subtractive Proteomics","volume":"301","author":"Schirmer","year":"2003","journal-title":"Science"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Serrano, J.B., Da Cruz e Silva, O.A., and Rebelo, S. (2016). Lamina Associated Polypeptide 1 (LAP1) Interactome and Its Functional Features. Membranes, 6.","DOI":"10.3390\/membranes6010008"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/0014-4827(90)90223-W","article-title":"On the cell-free association of lamins A and C with metaphase chromosomes","volume":"186","author":"Burke","year":"1990","journal-title":"Exp. Cell Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1083\/jcb.111.3.1047","article-title":"Lamins A and C bind and assemble at the surface of mitotic chromosomes","volume":"111","author":"Glass","year":"1990","journal-title":"J. Cell Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/nrm3488","article-title":"The nuclear lamins: Flexibility in function","volume":"14","author":"Burke","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.ceb.2017.12.009","article-title":"Messages from the voices within: Regulation of signaling by proteins of the nuclear lamina","volume":"52","author":"Gerace","year":"2018","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2121","DOI":"10.1016\/j.yexcr.2007.03.028","article-title":"\u201cLaminopathies\u201d: A wide spectrum of human diseases","volume":"313","author":"Worman","year":"2007","journal-title":"Exp. Cell Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/B978-0-12-397920-9.00006-8","article-title":"Functional Architecture of the Cell\u2019s Nucleus in Development, Aging, and Disease","volume":"109","author":"Burke","year":"2014","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1007\/s00018-021-04084-2","article-title":"The wide and growing range of lamin B-related diseases: From laminopathies to cancer","volume":"79","author":"Evangelisti","year":"2022","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Storey, E.C., and Fuller, H.R. (2022). Genotype-Phenotype Correlations in Human Diseases Caused by Mutations of LINC Complex-Associated Genes: A Systematic Review and Meta-Summary. Cells, 11.","DOI":"10.3390\/cells11244065"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4839","DOI":"10.1093\/emboj\/16.16.4839","article-title":"The inner nuclear membrane protein LAP1 forms a native complex with B-type lamins and partitions with spindle-associated mitotic vesicles","volume":"16","author":"Maison","year":"1997","journal-title":"EMBO J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1146\/annurev.cellbio.13.1.669","article-title":"Nuclear assembly","volume":"13","author":"Gant","year":"1997","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1016\/j.devcel.2013.08.012","article-title":"Lamina-Associated Polypeptide-1 Interacts with the Muscular Dystrophy Protein Emerin and Is Essential for Skeletal Muscle Maintenance","volume":"26","author":"Shin","year":"2013","journal-title":"Dev. Cell"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1038\/ng0396-254","article-title":"Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy","volume":"12","author":"Nagano","year":"1996","journal-title":"Nat. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1093\/hmg\/5.6.801","article-title":"The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein","volume":"5","author":"Manilal","year":"1996","journal-title":"Hum. Mol. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/ng1294-323","article-title":"Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy","volume":"8","author":"Bione","year":"1994","journal-title":"Nat. Genet."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1093\/hmg\/ddi479","article-title":"Loss of emerin at the nuclear envelope disrupts the Rb1\/E2F and MyoD pathways during muscle regeneration","volume":"15","author":"Melcon","year":"2006","journal-title":"Hum. Mol. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"907","DOI":"10.2353\/ajpath.2006.050564","article-title":"Emerin-Lacking Mice Show Minimal Motor and Cardiac Dysfunctions with Nuclear-Associated Vacuoles","volume":"168","author":"Ozawa","year":"2006","journal-title":"Am. J. Pathol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1007\/s12192-010-0173-2","article-title":"The early-onset torsion dystonia-associated protein, torsinA, displays molecular chaperone activity in vitro","volume":"15","author":"Burdette","year":"2010","journal-title":"Cell Stress Chaperones"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1001\/archneur.58.6.921","article-title":"Cellular distribution of torsin A and torsin B in normal human brain","volume":"58","author":"Konakova","year":"2001","journal-title":"Arch. Neurol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"27866","DOI":"10.1074\/jbc.M109.020164","article-title":"Interaction of torsinA with its major binding partners is impaired by the dystonia-associated DeltaGAG deletion","volume":"284","author":"Naismith","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1093\/hmg\/ddp557","article-title":"Relative tissue expression of homologous torsinB correlates with the neuronal specific importance of DYT1 dystonia-associated torsinA","volume":"19","author":"Jungwirth","year":"2009","journal-title":"Hum. Mol. Genet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"9861","DOI":"10.1073\/pnas.0912877107","article-title":"A molecular mechanism underlying the neural-specific defect in torsinA mutant mice","volume":"107","author":"Kim","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"E1545","DOI":"10.1073\/pnas.1300676110","article-title":"Regulation of Torsin ATPases by LAP1 and LULL1","volume":"110","author":"Zhao","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"E4822","DOI":"10.1073\/pnas.1415271111","article-title":"The mechanism of Torsin ATPase activation","volume":"111","author":"Brown","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e03239","DOI":"10.7554\/eLife.03239","article-title":"How lamina-associated polypeptide 1 (LAP1) activates Torsin","volume":"3","author":"Demircioglu","year":"2014","journal-title":"eLife"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"15","DOI":"10.7554\/eLife.63614","article-title":"Torsin ATPases influence chromatin interaction of the Torsin regulator LAP1","volume":"9","author":"Luithle","year":"2020","journal-title":"eLife"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1038\/ng0997-40","article-title":"The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein","volume":"17","author":"Ozelius","year":"1997","journal-title":"Nat. Genet."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1006\/geno.1999.6039","article-title":"The TOR1A (DYT1) Gene Family and Its Role in Early Onset Torsion Dystonia","volume":"62","author":"Ozelius","year":"1999","journal-title":"Genomics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"37271","DOI":"10.1074\/jbc.M110.123471","article-title":"A Unique Redox-sensing Sensor II Motif in TorsinA Plays a Critical Role in Nucleotide and Partner Binding*","volume":"285","author":"Zhu","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1083\/jcb.201507113","article-title":"TorsinA controls TAN line assembly and the retrograde flow of dorsal perinuclear actin cables during rearward nuclear movement","volume":"216","author":"Saunders","year":"2017","journal-title":"J. Cell Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4885","DOI":"10.1172\/JCI129769","article-title":"Nuclear envelope-localized torsinA-LAP1 complex regulates hepatic VLDL secretion and steatosis","volume":"129","author":"Shin","year":"2019","journal-title":"J. Clin. Investig."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"\u00d6stlund, C., Hernandez-Ono, A., and Shin, J.-Y. (2020). The Nuclear Envelope in Lipid Metabolism and Pathogenesis of NAFLD. Biology, 9.","DOI":"10.3390\/biology9100338"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"2589","DOI":"10.1016\/j.cellsig.2015.08.007","article-title":"Protein phosphatase 1 is a key player in nuclear events","volume":"27","author":"Rebelo","year":"2015","journal-title":"Cell. Signal."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Pereira, C.D., Martins, F., Santos, M., M\u00fceller, T., Da Cruz e Silva, O.A., and Rebelo, S. (2020). Nuclear Accumulation of LAP1:TRF2 Complex During DNA Damage Response Uncovers a Novel Role for LAP1. Cells, 9.","DOI":"10.3390\/cells9081804"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e11321","DOI":"10.7717\/peerj.11321","article-title":"Identification of key genes and biological processes contributing to colitis associated dysplasia in ulcerative colitis","volume":"9","author":"Zhang","year":"2021","journal-title":"PeerJ"},{"key":"ref_62","first-page":"269","article-title":"Gene co-expression network analysis of dysferlinopathy: Altered cellular processes and functional prediction of TOR1AIP1, a novel muscular dystrophy gene","volume":"27","author":"Dincer","year":"2016","journal-title":"Neuromuscul. Disord."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"761562","DOI":"10.3389\/fmolb.2022.761562","article-title":"Urinary Proteomics Analysis of Active Vitiligo Patients: Biomarkers for Steroid Treatment Efficacy Prediction and Monitoring","volume":"9","author":"Qian","year":"2022","journal-title":"Front. Mol. Biosci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1083\/jcb.201112098","article-title":"A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells","volume":"196","author":"Roux","year":"2012","journal-title":"J. Cell Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1016\/j.bbrc.2005.10.020","article-title":"Novel progerin-interactive partner proteins hnRNP E1, EGF, Mel 18, and UBC9 interact with lamin A\/C","volume":"338","author":"Zhong","year":"2005","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"R797","DOI":"10.1016\/j.cub.2004.09.021","article-title":"Mechanisms and Molecules of the Mitotic Spindle","volume":"14","author":"Gadde","year":"2004","journal-title":"Curr. Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1126\/science.1063488","article-title":"The Mitotic Spindle: A Self-Made Machine","volume":"294","author":"Karsenti","year":"2001","journal-title":"Science"},{"key":"ref_68","unstructured":"Serrano, J.B., Martins, F., Marafona, A.M., da Cruz e Silva, O.A.B., and Rebelo, S. (2018). Encyclopedia of Signaling Molecules, Springer."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1038\/nature08869","article-title":"Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes","volume":"464","author":"Neumann","year":"2010","journal-title":"Nature"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1007\/s11010-014-2241-x","article-title":"LAP1 is a crucial protein for the maintenance of the nuclear envelope structure and cell cycle progression","volume":"399","author":"Santos","year":"2014","journal-title":"Mol. Cell. Biochem."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1126\/science.1181348","article-title":"Systematic Analysis of Human Protein Complexes Identifies Chromosome Segregation Proteins","volume":"328","author":"Hutchins","year":"2010","journal-title":"Science"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1016\/j.cellsig.2014.02.011","article-title":"A systems wide mass spectrometric based linear motif screen to identify dominant in-vivo interacting proteins for the ubiquitin ligase MDM2","volume":"26","author":"Nicholson","year":"2014","journal-title":"Cell. Signal."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.cell.2005.02.022","article-title":"Nuclear Movement Regulated by Cdc42, MRCK, Myosin, and Actin Flow Establishes MTOC Polarization in Migrating Cells","volume":"121","author":"Gomes","year":"2005","journal-title":"Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1016\/j.cell.2013.02.031","article-title":"Nuclear Positioning","volume":"152","author":"Gundersen","year":"2013","journal-title":"Cell"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/j.ceb.2011.08.001","article-title":"Orientation and function of the nuclear\u2013centrosomal axis during cell migration","volume":"23","author":"Luxton","year":"2011","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1126\/science.1140321","article-title":"ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage","volume":"316","author":"Matsuoka","year":"2007","journal-title":"Science"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.tibs.2006.05.004","article-title":"The ATM-mediated DNA-damage response: Taking shape","volume":"31","author":"Shiloh","year":"2006","journal-title":"Trends Biochem. Sci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1038\/nature03097","article-title":"Cell-cycle checkpoints and cancer","volume":"432","author":"Kastan","year":"2004","journal-title":"Nature"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1644","DOI":"10.1074\/mcp.M114.038596","article-title":"Proteomic Analysis of the Epidermal Growth Factor Receptor (EGFR) Interactome and Post-translational Modifications Associated with Receptor Endocytosis in Response to EGF and Stress","volume":"13","author":"Tong","year":"2014","journal-title":"Mol. Cell. Proteom."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"ra40","DOI":"10.1126\/scisignal.2005769","article-title":"Temporal proteomics of NGF-TrkA signaling identifies an inhibitory role for the E3 ligase Cbl-b in neuroblastoma cell differentiation","volume":"8","author":"Emdal","year":"2015","journal-title":"Sci. Signal."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.cell.2014.01.064","article-title":"Ribosomal Protein s15 Phosphorylation Mediates LRRK2 Neurodegeneration in Parkinson\u2019s Disease","volume":"157","author":"Martin","year":"2014","journal-title":"Cell"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1074\/mcp.M110.001628","article-title":"Genome-wide YFP Fluorescence Complementation Screen Identifies New Regulators for Telomere Signaling in Human Cells","volume":"10","author":"Lee","year":"2011","journal-title":"Mol. Cell. Proteom."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1016\/j.cell.2012.08.011","article-title":"A Census of Human Soluble Protein Complexes","volume":"150","author":"Havugimana","year":"2012","journal-title":"Cell"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1186\/gb-2008-9-9-232","article-title":"The telosome\/shelterin complex and its functions","volume":"9","author":"Xin","year":"2008","journal-title":"Genome Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2100","DOI":"10.1101\/gad.1346005","article-title":"Shelterin: The protein complex that shapes and safeguards human telomeres","volume":"19","year":"2005","journal-title":"Genes Dev."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Serrano, J., Martins, F., Sousa, J., Pereira, C., Van Pelt, A., Rebelo, S., and da Cruz e Silva, O.A.B. (2017). Descriptive Analysis of LAP1 Distribution and That of Associated Proteins throughout Spermatogenesis. Membranes, 7.","DOI":"10.3390\/membranes7020022"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1111\/brv.12498","article-title":"Nuclear envelope dynamics during mammalian spermatogenesis: New insights on male fertility","volume":"94","author":"Pereira","year":"2019","journal-title":"Biol. Rev."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"260","DOI":"10.4161\/nucl.29227","article-title":"Depletion of lamina-associated polypeptide 1 from cardiomyocytes causes cardiac dysfunction in mice","volume":"5","author":"Shin","year":"2014","journal-title":"Nucleus"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1051\/medsci\/2021196","article-title":"A case of congenital limb girdle myasthenia solved through a tripartite collaboration","volume":"37","author":"Nouioua","year":"2021","journal-title":"Medecine\/Sciences"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1016\/j.nmd.2021.11.004","article-title":"The 2022 version of the gene table of neuromuscular disorders (nuclear genome)","volume":"31","author":"Cohen","year":"2021","journal-title":"Neuromuscul. Disord."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1136\/practneurol-2012-000404","article-title":"Congenital myasthenic syndromes: An update","volume":"13","author":"Finlayson","year":"2013","journal-title":"Pract. Neurol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1242\/dmm.024711","article-title":"Hallmarks of progeroid syndromes: Lessons from mice and reprogrammed cells","volume":"9","author":"Carrero","year":"2016","journal-title":"Dis. Model. Mech."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1122","DOI":"10.1016\/j.nmd.2014.08.001","article-title":"Response (to Sewry and Goebel)","volume":"24","author":"Korkusuz","year":"2014","journal-title":"Neuromuscul. Disord."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"869","DOI":"10.3233\/JND-200560","article-title":"Emerging Oligonucleotide Therapeutics for Rare Neuromuscular Diseases","volume":"8","author":"Aoki","year":"2021","journal-title":"J. Neuromuscul. Dis."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1016\/S1474-4422(22)00125-9","article-title":"Emerging therapies for Duchenne muscular dystrophy","volume":"21","author":"Markati","year":"2022","journal-title":"Lancet Neurol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1080\/14728222.2022.2157258","article-title":"Early clinical and pre-clinical therapy development in Nemaline Myopathy","volume":"26","author":"Fisher","year":"2022","journal-title":"Expert Opin. Ther. Targets"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/6911\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:12:13Z","timestamp":1760123533000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/6911"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,7]]},"references-count":96,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["ijms24086911"],"URL":"https:\/\/doi.org\/10.3390\/ijms24086911","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,7]]}}}