{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T23:13:12Z","timestamp":1780528392354,"version":"3.54.1"},"reference-count":62,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,16]],"date-time":"2023-01-16T00:00:00Z","timestamp":1673827200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ligue contre la Cardiomyopathie"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>A single missense variant of the TMPO\/LAP2\u03b1 gene, encoding LAP2 proteins, has been associated with cardiomyopathy in two brothers. To further evaluate its role in cardiac muscle, we included TMPO in our cardiomyopathy diagnostic gene panel. A screening of ~5000 patients revealed three novel rare TMPO heterozygous variants in six males diagnosed with hypertrophic or dilated cardiomypathy. We identified in different cellular models that (1) the frameshift variant LAP2\u03b1 p.(Gly395Glufs*11) induced haploinsufficiency, impeding cell proliferation and\/or producing a truncated protein mislocalized in the cytoplasm; (2) the C-ter missense variant LAP2\u03b1 p.(Ala240Thr) led to a reduced proximity events between LAP2\u03b1 and the nucleosome binding protein HMGN5; and (3) the LEM-domain missense variant p.(Leu124Phe) decreased both associations of LAP2\u03b1\/\u03b2 with the chromatin-associated protein BAF and inhibition of the E2F1 transcription factor activity which is known to be dependent on Rb, partner of LAP2\u03b1. Additionally, the LAP2\u03b1 expression was lower in the left ventricles of male mice compared to females. In conclusion, our study reveals distinct altered properties of LAP2 induced by these TMPO\/LAP2 variants, leading to altered cell proliferation, chromatin structure or gene expression-regulation pathways, and suggests a potential sex-dependent role of LAP2 in myocardial function and disease.<\/jats:p>","DOI":"10.3390\/cells12020337","type":"journal-article","created":{"date-parts":[[2023,1,16]],"date-time":"2023-01-16T05:30:07Z","timestamp":1673847007000},"page":"337","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Abnormal Cellular Phenotypes Induced by Three TMPO\/LAP2 Variants Identified in Men with Cardiomyopathies"],"prefix":"10.3390","volume":"12","author":[{"given":"Nathalie","family":"Vadrot","sequence":"first","affiliation":[{"name":"Basic and Translational Myology Laboratory, Universit\u00e9 Paris Cit\u00e9, BFA, UMR 8251, CNRS, F-75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7891-3385","authenticated-orcid":false,"given":"Flavie","family":"Ader","sequence":"additional","affiliation":[{"name":"APHP\u2014Sorbonne Universit\u00e9, Unit\u00e9 Fonctionnelle de Cardiog\u00e9n\u00e9tique et Myog\u00e9n\u00e9tique Mol\u00e9culaire, Service de Biochimie M\u00e9tabolique, HU Piti\u00e9 Salp\u00eatri\u00e8re\u2014Charles Foix, F-75013 Paris, France"},{"name":"INSERM, UMR_S 1166, Sorbonne Universit\u00e9, F-75005 Paris, France"},{"name":"Facult\u00e9 de Pharmacie Paris Descartes, D\u00e9partement 3, Universit\u00e9 Paris Cit\u00e9, F-75006 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1851-8727","authenticated-orcid":false,"given":"Maryline","family":"Moulin","sequence":"additional","affiliation":[{"name":"Basic and Translational Myology Laboratory, Universit\u00e9 Paris Cit\u00e9, BFA, UMR 8251, CNRS, F-75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Merlant","sequence":"additional","affiliation":[{"name":"Basic and Translational Myology Laboratory, Universit\u00e9 Paris Cit\u00e9, BFA, UMR 8251, CNRS, F-75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7oise","family":"Chapon","sequence":"additional","affiliation":[{"name":"Service d\u2019anatomopathologie, CHU de Caen, F-14000 Caen, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Estelle","family":"Gandjbakhch","sequence":"additional","affiliation":[{"name":"INSERM, UMR_S 1166, Sorbonne Universit\u00e9, F-75005 Paris, France"},{"name":"D\u00e9partement de cardiologie, APHP\u2014Sorbonne Universit\u00e9, HU Piti\u00e9 Salp\u00eatri\u00e8re- Charles Foix, F-75610 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabien","family":"Labombarda","sequence":"additional","affiliation":[{"name":"Service de Cardiologie, CHU de Caen, Universit\u00e9 de Caen Normandie, F-14000 Caen, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pascale","family":"Maragnes","sequence":"additional","affiliation":[{"name":"Cardiologie p\u00e9diatrique, Service de p\u00e9diatrie, CHU de Caen, F-14000 Caen, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia","family":"R\u00e9ant","sequence":"additional","affiliation":[{"name":"Service de Cardiologie, H\u00f4pital Haut L\u00e9v\u00eaque, CHU de Bordeaux, INSERM 1045, Universit\u00e9 de Bordeaux, F-33000 Bordeaux, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9789-3591","authenticated-orcid":false,"given":"Caroline","family":"Rooryck","sequence":"additional","affiliation":[{"name":"Service de G\u00e9n\u00e9tique M\u00e9dicale, CHU Bordeaux, F-33000 Bordeaux, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5492-8619","authenticated-orcid":false,"given":"Vincent","family":"Probst","sequence":"additional","affiliation":[{"name":"Centre de r\u00e9f\u00e9rence des maladies rythmiques cardiaques, CHU de Nantes, F-44000 Nantes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erwan","family":"Donal","sequence":"additional","affiliation":[{"name":"Centre Cardio-Pneumologique, CHU de Rennes H\u00f4pital de Pontchaillou, F-35000 Rennes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pascale","family":"Richard","sequence":"additional","affiliation":[{"name":"APHP\u2014Sorbonne Universit\u00e9, Unit\u00e9 Fonctionnelle de Cardiog\u00e9n\u00e9tique et Myog\u00e9n\u00e9tique Mol\u00e9culaire, Service de Biochimie M\u00e9tabolique, HU Piti\u00e9 Salp\u00eatri\u00e8re\u2014Charles Foix, F-75013 Paris, France"},{"name":"INSERM, UMR_S 1166, Sorbonne Universit\u00e9, F-75005 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2806-5386","authenticated-orcid":false,"given":"Ana","family":"Ferreiro","sequence":"additional","affiliation":[{"name":"Basic and Translational Myology Laboratory, Universit\u00e9 Paris Cit\u00e9, BFA, UMR 8251, CNRS, F-75013 Paris, France"},{"name":"APHP, Centre de r\u00e9f\u00e9rence des Maladies Neuromusculaires, Institut de Myologie, Neuromyology Department, CHU Piti\u00e9 Salp\u00eatri\u00e8re\u2014Charles Foix, F-75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brigitte","family":"Buendia","sequence":"additional","affiliation":[{"name":"Basic and Translational Myology Laboratory, Universit\u00e9 Paris Cit\u00e9, BFA, UMR 8251, CNRS, F-75013 Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Worman:, H.J., \u00d6stlund, C., and Wang, Y. (2010). Diseases of the Nuclear Envelope. Cold Spring Harb. Perspect. Biol., 2.","DOI":"10.1101\/cshperspect.a000760"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/s13023-017-0698-x","article-title":"Nuclear Envelopathies: A Complex LINC between Nuclear Envelope and Pathology","volume":"12","author":"Janin","year":"2017","journal-title":"Orphanet J. Rare Dis."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Dorboz, I., Coutelier, M., Bertrand, A.T., Caberg, J.-H., Elmaleh-Berg\u00e8s, M., Lain\u00e9, J., Stevanin, G., Bonne, G., Boespflug-Tanguy, O., and Servais, L. (2014). Severe Dystonia, Cerebellar Atrophy, and Cardiomyopathy Likely Caused by a Missense Mutation in TOR1AIP1. Orphanet J. Rare Dis., 9.","DOI":"10.1186\/s13023-014-0174-9"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1161\/CIRCRESAHA.117.309711","article-title":"Classification, Epidemiology, and Global Burden of Cardiomyopathies","volume":"121","author":"McKenna","year":"2017","journal-title":"Circ. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1093\/cvr\/cvy122","article-title":"Complex Roads from Genotype to Phenotype in Dilated Cardiomyopathy: Scientific Update from the Working Group of Myocardial Function of the European Society of Cardiology","volume":"114","author":"Bondue","year":"2018","journal-title":"Cardiovasc. Res."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Ingles, J., Burns, C., Bagnall, R.D., Lam, L., Yeates, L., Sarina, T., Puranik, R., Briffa, T., Atherton, J.J., and Driscoll, T. (2017). Nonfamilial Hypertrophic Cardiomyopathy: Prevalence, Natural History, and Clinical Implications. Circ. Cardiovasc. Genet., 10.","DOI":"10.1161\/CIRCGENETICS.116.001620"},{"key":"ref_7","first-page":"3461","article-title":"Defining the Genetic Architecture of Hypertrophic Cardiomyopathy: Re-Evaluating the Role of Non-Sarcomeric Genes","volume":"38","author":"Walsh","year":"2017","journal-title":"Eur. Heart J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"22","DOI":"10.15420\/aer.2012.1.22","article-title":"What Should the Cardiologist Know about Lamin Disease?","volume":"1","author":"Charron","year":"2012","journal-title":"Arrhythm. Electrophysiol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1111\/j.1742-4658.2007.05695.x","article-title":"Nucleoplasmic Lamins and Their Interaction Partners, LAP2\u03b1, Rb, and BAF, in Transcriptional Regulation: Nucleoplasmic Lamins and Their Interactions","volume":"274","author":"Dorner","year":"2007","journal-title":"FEBS J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1006\/geno.1995.1131","article-title":"Structure and Mapping of the Human Thymopoietin (TMPO) Gene and Relationship of Human TMPO Beta to Rat Lamin-Associated Polypeptide 2","volume":"28","author":"Harris","year":"1995","journal-title":"Genomics"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3473","DOI":"10.1242\/jcs.113.19.3473","article-title":"Lamina-Associated Polypeptide 2alpha Binds Intranuclear A-Type Lamins","volume":"113 Pt. 19","author":"Dechat","year":"2000","journal-title":"J. Cell. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1101\/gad.1652708","article-title":"Nuclear Lamins: Major Factors in the Structural Organization and Function of the Nucleus and Chromatin","volume":"22","author":"Dechat","year":"2008","journal-title":"Genes Dev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev-biochem-060614-034115","article-title":"Lamins: Nuclear Intermediate Filament Proteins with Fundamental Functions in Nuclear Mechanics and Genome Regulation","volume":"84","author":"Gruenbaum","year":"2015","journal-title":"Annu. Rev. Biochem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1240104","DOI":"10.1126\/science.1240104","article-title":"Nuclear Lamin-A Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation","volume":"341","author":"Swift","year":"2013","journal-title":"Science"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5797","DOI":"10.1242\/jcs.02701","article-title":"LEM2 Is a Novel MAN1-Related Inner Nuclear Membrane Protein Associated with A-Type Lamins","volume":"118","author":"Brachner","year":"2005","journal-title":"J. Cell Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/bs.mie.2015.07.008","article-title":"Purification and Structural Analysis of LEM-Domain Proteins","volume":"569","author":"Herrada","year":"2016","journal-title":"Meth. Enzymol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4399","DOI":"10.1093\/emboj\/20.16.4399","article-title":"Solution Structure of the Constant Region of Nuclear Envelope Protein LAP2 Reveals Two LEM-Domain Structures: One Binds BAF and the Other Binds DNA","volume":"20","author":"Cai","year":"2001","journal-title":"EMBO J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1006\/jsbi.2000.4212","article-title":"Review: Lamina-Associated Polypeptide 2 Isoforms and Related Proteins in Cell Cycle-Dependent Nuclear Structure Dynamics","volume":"129","author":"Dechat","year":"2000","journal-title":"J. Struct. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"18104","DOI":"10.1074\/jbc.C113.469544","article-title":"High Mobility Group Protein N5 (HMGN5) and Lamina-Associated Polypeptide 2\u03b1 (LAP2\u03b1) Interact and Reciprocally Affect Their Genome-Wide Chromatin Organization","volume":"288","author":"Zhang","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1161\/CIRCRESAHA.109.205724","article-title":"Lamina-Associated Polypeptide 2alpha Loss Impairs Heart Function and Stress Response in Mice","volume":"106","author":"Gotic","year":"2010","journal-title":"Circ. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1002\/humu.20250","article-title":"Thymopoietin (Lamina-Associated Polypeptide 2) Gene Mutation Associated with Dilated Cardiomyopathy","volume":"26","author":"Taylor","year":"2005","journal-title":"Hum. Mutat."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1038\/gim.2016.90","article-title":"Reassessment of Mendelian Gene Pathogenicity Using 7,855 Cardiomyopathy Cases and 60,706 Reference Samples","volume":"19","author":"Walsh","year":"2017","journal-title":"Genet. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"6138","DOI":"10.1038\/ncomms7138","article-title":"Chromatin De-Compaction By The Nucleosomal Binding Protein HMGN5 Impairs Nuclear Sturdiness","volume":"6","author":"Furusawa","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1083\/jcb.200511149","article-title":"Lamina-Associated Polypeptide 2alpha Regulates Cell Cycle Progression and Differentiation via the Retinoblastoma-E2F Pathway","volume":"173","author":"Dorner","year":"2006","journal-title":"J. Cell Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"311","DOI":"10.3389\/fendo.2017.00311","article-title":"E2F1, a Novel Regulator of Metabolism","volume":"8","author":"Denechaud","year":"2017","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"ref_26","first-page":"1","article-title":"G\u00e9n\u00e9tique des cardiomyopathies h\u00e9r\u00e9ditaires","volume":"13","author":"Richard","year":"2018","journal-title":"EMC-Cardiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"10460","DOI":"10.1093\/nar\/gky736","article-title":"Structural Analysis of the Ternary Complex between Lamin A\/C, BAF and Emerin Identifies an Interface Disrupted in Autosomal Recessive Progeroid Diseases","volume":"46","author":"Samson","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1128\/MCB.24.4.1481-1492.2004","article-title":"Expression of a Mutant Lamin A That Causes Emery-Dreifuss Muscular Dystrophy Inhibits in Vitro Differentiation of C2C12 Myoblasts","volume":"24","author":"Favreau","year":"2004","journal-title":"Mol. Cell. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1093\/hmg\/ddu728","article-title":"The p.R482W Substitution in A-Type Lamins Deregulates SREBP1 Activity in Dunnigan-Type Familial Partial Lipodystrophy","volume":"24","author":"Vadrot","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/0092-8674(91)90456-9","article-title":"G1\/S Phosphorylation of the Retinoblastoma Protein Is Associated with an Altered Affinity for the Nuclear Compartment","volume":"65","author":"Mittnacht","year":"1991","journal-title":"Cell"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/978-1-4939-3530-7_9","article-title":"In Situ Detection of Interactions Between Nuclear Envelope Proteins and Partners","volume":"1411","author":"Barateau","year":"2016","journal-title":"Methods Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Barateau, A., Vadrot, N., Vicart, P., Ferreiro, A., Mayer, M., H\u00e9ron, D., Vigouroux, C., and Buendia, B. (2017). A Novel Lamin A Mutant Responsible for Congenital Muscular Dystrophy Causes Distinct Abnormalities of the Cell Nucleus. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0169189"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2936","DOI":"10.1093\/bioinformatics\/btw361","article-title":"STRUM: Structure-Based Prediction of Protein Stability Changes upon Single-Point Mutation","volume":"32","author":"Quan","year":"2016","journal-title":"Bioinformatics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1016\/j.str.2007.04.007","article-title":"Structural Basis for Dimerization of LAP2\u03b1, a Component of the Nuclear Lamina","volume":"15","author":"Bradley","year":"2007","journal-title":"Structure"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4401","DOI":"10.1091\/mbc.e02-07-0450","article-title":"Lamin A\/C Binding Protein LAP2\u03b1 Is Required for Nuclear Anchorage of Retinoblastoma Protein","volume":"13","author":"Markiewicz","year":"2002","journal-title":"MBoC"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1038\/ejhg.2013.16","article-title":"Doubly Heterozygous LMNA and TTN Mutations Revealed by Exome Sequencing in a Severe Form of Dilated Cardiomyopathy","volume":"21","author":"Roncarati","year":"2013","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Abdallah, A.M., Carlus, S.J., Al-Mazroea, A.H., Alluqmani, M., Almohammadi, Y., Bhuiyan, Z.A., and Al-Harbi, K.M. (2019). Digenic Inheritance of LAMA4 and MYH7 Mutations in Patient with Infantile Dilated Cardiomyopathy. Medicina, 55.","DOI":"10.3390\/medicina55010017"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Ren, M., Chai, X., Li, L., Wang, X., and Yin, C. (2020). Potential Digenic Inheritance of Familial Hypertrophic Cardiomyopathy Identified by Whole-exome Sequencing. Mol. Genet. Genom. Med., 8.","DOI":"10.1002\/mgg3.1150"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"S140","DOI":"10.1016\/j.hlc.2019.06.019","article-title":"Penetrance of Dilated Cardiomyopathy in Families with Truncating TTN Variants: A National Perspective","volume":"28","author":"Johnson","year":"2019","journal-title":"Heart Lung Circ."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e004133","DOI":"10.1161\/CIRCHEARTFAILURE.117.004133","article-title":"Sex Differences at the Time of Myectomy in Hypertrophic Cardiomyopathy","volume":"11","author":"Nijenkamp","year":"2018","journal-title":"Circ. Heart Fail."},{"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":"239","DOI":"10.1016\/j.ijcard.2018.10.091","article-title":"Sex-Related Differences in Cardiomyopathies","volume":"286","author":"Pelliccia","year":"2019","journal-title":"Int. J. Cardiol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"InanlooRahatloo, K., Liang, G., Vo, D., Ebert, A., Nguyen, I., and Nguyen, P.K. (2017). Sex-Based Differences in Myocardial Gene Expression in Recently Deceased Organ Donors with No Prior Cardiovascular Disease. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0183874"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e63476","DOI":"10.7554\/eLife.63476","article-title":"LAP2alpha Maintains a Mobile and Low Assembly State of A-Type Lamins in the Nuclear Interior","volume":"10","author":"Naetar","year":"2021","journal-title":"eLife"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Gonz\u00e1lez-Garrido, A., Rosas-Madrigal, S., Rojo-Dom\u00ednguez, A., Arellanes-Robledo, J., L\u00f3pez-Mora, E., Carnevale, A., Arregui, L., Rosendo-Guti\u00e9rrez, R., Romero-Hidalgo, S., and Villarreal-Molina, M.T. (2022). Leukocyte Nuclear Morphology Alterations in Dilated Cardiomyopathy Caused by a Lamin AC Truncating Mutation (LMNA\/Ser431*) Are Modified by the Presence of a LAP2 Missense Polymorphism (TMPO\/Arg690Cys). IJMS, 23.","DOI":"10.3390\/ijms232113626"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"647343","DOI":"10.3389\/fgene.2021.647343","article-title":"Interaction of HLA Class II Rs9272219 and TMPO Rs17028450 (Arg690Cys) Variants Affects Neuromyelitis Optica Spectrum Disorder Susceptibility in an Admixed Mexican Population","volume":"12","author":"Barquera","year":"2021","journal-title":"Front. Genet."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1083\/jcb.200606139","article-title":"Nucleoplasmic LAP2\u03b1\u2013Lamin A Complexes Are Required to Maintain a Proliferative State in Human Fibroblasts","volume":"176","author":"Pekovic","year":"2007","journal-title":"J. Cell Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1161\/CIRCRESAHA.109.201251","article-title":"Nonsense-Mediated MRNA Decay and Ubiquitin\u2013Proteasome System Regulate Cardiac Myosin-Binding Protein C Mutant Levels in Cardiomyopathic Mice","volume":"105","author":"Vignier","year":"2009","journal-title":"Circ. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1101\/gr.196220.115","article-title":"A-Type Lamins Bind Both Hetero- and Euchromatin, the Latter Being Regulated by Lamina-Associated Polypeptide 2 Alpha","volume":"26","author":"Gesson","year":"2016","journal-title":"Genome Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1006\/abbi.2001.2663","article-title":"Age-Dependent Declines in Proteasome Activity in the Heart","volume":"397","author":"Bulteau","year":"2002","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1097\/00001573-200205000-00006","article-title":"Modifier Genes for Hypertrophic Cardiomyopathy","volume":"17","author":"Marian","year":"2002","journal-title":"Curr. Opin. Cardiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1002\/hep.29522","article-title":"Nuclear Lamina Genetic Variants, Including a Truncated LAP2, in Twins and Siblings with Nonalcoholic Fatty Liver Disease","volume":"67","author":"Brady","year":"2018","journal-title":"Hepatology"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"327","DOI":"10.5483\/BMBRep.2018.51.7.113","article-title":"Laminopathies; Mutations on Single Gene and Various Human Genetic Diseases","volume":"51","author":"Kang","year":"2018","journal-title":"BMB Rep."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/s41586-018-0534-z","article-title":"Nuclear Envelope Assembly Defects Link Mitotic Errors to Chromothripsis","volume":"561","author":"Liu","year":"2018","journal-title":"Nature"},{"key":"ref_55","first-page":"204","article-title":"Characterization of a Unique Form of Arrhythmic Cardiomyopathy Caused by Recessive Mutation in LEMD2","volume":"4","author":"Abdelfatah","year":"2019","journal-title":"JACC: Basic Transl. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.cell.2017.09.018","article-title":"Genome-Nuclear Lamina Interactions Regulate Cardiac Stem Cell Lineage Restriction","volume":"171","author":"Poleshko","year":"2017","journal-title":"Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.mrrev.2015.07.004","article-title":"Genetic Mutations Strengthen Functional Association of LAP1 with DYT1 Dystonia and Muscular Dystrophy","volume":"766","author":"Rebelo","year":"2015","journal-title":"Mutat. Res. \/Rev. Mutat. Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"298","DOI":"10.4161\/nucl.25751","article-title":"The Nuclear Envelope LEM-Domain Protein Emerin","volume":"4","author":"Berk","year":"2013","journal-title":"Nucleus"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1883","DOI":"10.1212\/01.wnl.0000263138.57257.6a","article-title":"Multitissular Involvement in a Family with LMNA and EMD Mutations: Role of Digenic Mechanism?","volume":"68","author":"Toutain","year":"2007","journal-title":"Neurology"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1111\/j.1540-8167.2007.01081.x","article-title":"X-Linked Nonsyndromic Sinus Node Dysfunction and Atrial Fibrillation Caused by Emerin Mutation","volume":"19","author":"Karst","year":"2008","journal-title":"J. Cardiovasc. Electrophysiol."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Essawy, N., Samson, C., Petitalot, A., Moog, S., Bigot, A., Herrada, I., Marcelot, A., Arteni, A.-A., Coirault, C., and Zinn-Justin, S. (2019). An Emerin LEM-Domain Mutation Impairs Cell Response to Mechanical Stress. Cells, 8.","DOI":"10.3390\/cells8060570"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1038\/ncb1793","article-title":"Loss of Nucleoplasmic LAP2\u03b1\u2013Lamin A Complexes Causes Erythroid and Epidermal Progenitor Hyperproliferation","volume":"10","author":"Naetar","year":"2008","journal-title":"Nat. Cell Biol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/2\/337\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:07:21Z","timestamp":1760119641000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/2\/337"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,16]]},"references-count":62,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["cells12020337"],"URL":"https:\/\/doi.org\/10.3390\/cells12020337","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,16]]}}}