A recurrent homozygous LMNA missense variant p.Thr528Met causes atypical progeroid syndrome characterized by mandibuloacral dysostosis, severe muscular dystrophy, and skeletal deformities.
cell nucleus
lamins
muscular dystrophy
premature aging
progeria
Journal
American journal of medical genetics. Part A
ISSN: 1552-4833
Titre abrégé: Am J Med Genet A
Pays: United States
ID NLM: 101235741
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
05
06
2023
received:
21
12
2022
accepted:
12
06
2023
medline:
21
8
2023
pubmed:
30
6
2023
entrez:
30
6
2023
Statut:
ppublish
Résumé
Atypical progeroid syndromes (APS) are premature aging syndromes caused by pathogenic LMNA missense variants, associated with unaltered expression levels of lamins A and C, without accumulation of wild-type or deleted prelamin A isoforms, as observed in Hutchinson-Gilford progeria syndrome (HGPS) or HGPS-like syndromes. A specific LMNA missense variant, (p.Thr528Met), was previously identified in a compound heterozygous state in patients affected by APS and severe familial partial lipodystrophy, whereas heterozygosity was recently identified in patients affected by Type 2 familial partial lipodystrophy. Here, we report four unrelated boys harboring homozygosity for the p.Thr528Met, variant who presented with strikingly homogeneous APS clinical features, including osteolysis of mandibles, distal clavicles and phalanges, congenital muscular dystrophy with elevated creatine kinase levels, and major skeletal deformities. Immunofluorescence analyses of patient-derived primary fibroblasts showed a high percentage of dysmorphic nuclei with nuclear blebs and typical honeycomb patterns devoid of lamin B1. Interestingly, in some protrusions emerin or LAP2α formed aberrant aggregates, suggesting pathophysiology-associated clues. These four cases further confirm that a specific LMNA variant can lead to the development of strikingly homogeneous clinical phenotypes, in these particular cases a premature aging phenotype with major musculoskeletal involvement linked to the homozygous p.Thr528Met variant.
Identifiants
pubmed: 37387251
doi: 10.1002/ajmg.a.63335
doi:
Substances chimiques
Lamin Type A
0
LMNA protein, human
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2274-2289Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Agarwal, A. K., Fryns, J. P., Auchus, R. J., & Garg, A. (2003). Zinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Human Molecular Genetics, 12(16), 995-2001. https://doi.org/10.1093/hmg/ddg213
Agarwal, A. K., Kazachkova, I., Ten, S., & Garg, A. (2008). Severe mandibuloacral dysplasia-associated lipodystrophy and progeria in a young girl with a novel homozygous Arg527Cys LMNA mutation. The Journal of Clinical Endocrinology and Metabolism, 93(12), 4617-4623. https://doi.org/10.1210/jc.2008-0123.jc.2008-0123
Araújo-Vilar, D., Fernández-Pombo, A., Berta Victoria, B., Mosquera-Orgueira, A., Cobelo-Gómez, S., Castro-Pais, A., Hermida-Ameijeiras, A., Loidi, L., Sánchez-Iglesias, S., & Sánchez-Iglesias, S. (2021). Variable Expressivity and Allelic Heterogeneity in Type 2 Familial Partial Lipodystrophy: The p.(Thr528Met) LMNA Variant. Journal of Clinical Medicine, 10(7), 1497. https://doi.org/10.3390/jcm10071497
Barthélémy, F., Navarro, C., Fayek, R., Da Silva, N., Roll, P., Sigaudy, S., Oshima, J., Bonne, G., Papadopoulou-Legbelou, K., Evangeliou, A. E., Spilioti, M., Lemerrer, M., Wevers, R. A., Morava, E., Robaglia-Schlupp, A., Lévy, N., Bartol, I. M., & De Sandre-Giovannoli, A. (2015). Truncated prelamin A expression in HGPS-like patients: a transcriptional study. European Journal of Human Genetics, 23(8), 1051-1061. https://doi.org/10.1038/ejhg.2014.239ejhg2014239
Ben Yaou, R., Navarro, C., Quijano-Roy, S., Bertrand, A. T., Massart, C., De Sandre-Giovannoli, A., Cadiñanos, J., Mamchaou, K., Butler-Browne, G., Estournet, B., Richard, P., Barois, A., Lévy, N., & Bonne, G. (2011). Type B mandibuloacral dysplasia with congenital myopathy due to homozygous ZMPSTE24 missense mutation. European Journal of Human Genetics, 19(6), 647-654. https://doi.org/10.1038/ejhg.2010.256
Benedetti, S., Bertini, E., Iannaccone, S., Angelini, C., Trisciani, M., Toniolo, D., Sferrazza, B., Carrera, P., Comi, G., Ferrari, M., Quattrini, A., & Previtali, S. C. (2005). Dominant LMNA mutations can cause combined muscular dystrophy and peripheral neuropathy. Journal of Neurology Neurosurgery and Psychiatry, 76(7), 1019-1021. https://doi.org/10.1136/jnnp.2004.046110
Bercht Pfleghaar, K., Taimen, P., Butin-Israeli, V., Shimi, T., Langer-Freitag, S., Markaki, Y. E., Goldman, A., Wehnert, M., & Goldman, R. (2015). Gene-rich chromosomal regions are preferentially localized in the lamin B deficient nuclear blebs of atypical progeria cells. Nucleus, 6(1), 66-76. https://doi.org/10.1080/19491034.2015.1004256
Bonne, G., Di Barletta, M. R., Varnous, S., Bécane, H. M., Hammouda, E. H., Merlini, L., Muntoni, F., Greenberg, C. R., Gary, F., Urtizberea, J. A., Duboc, D., Fardeau, M., Toniolo, D., & Schwartz, K. (1999). Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nature Genetics, 21(3), 285-288. https://doi.org/10.1038/6799
Bonne, G., Mercuri, E., Muchir, A., Urtizberea, A., Bécane, H. M., Recan, D., Merlini, L., Wehnert, M., Boor, R., Reuner, U., Vorgerd, M., Wicklein, E. M., Eymard, B., Duboc, D., Penisson-Besnier, I., Cuisset, J. M., Ferrer, X., Desguerre, I., Lacombe, D., … Muntoni, F. (2000). Clinical and molecular genetic spectrum of autosomal dominant Emery-Dreifuss muscular dystrophy due to mutations of the lamin A/C gene. Annals of Neurology, 48(2), 170-180. https://doi.org/10.1002/1531-8249
Broers, J. L., Hutchison, C. J., & Ramaekers, F. C. (2004). Laminopathies. The journal of Pathology, 204(4), 478-488. https://doi.org/10.1002/path.1655
Cao, H., & Hegele, R. A. (2003). LMNA is mutated in Hutchinson-Gilford progeria (MIM 176670) but not in Wiedemann-Rautenstrauch progeroid syndrome (MIM 264090). Journal of Human Genetics, 48(5), 271-274. https://doi.org/10.1007/s10038-003-0025-3
Chen, L., Lee, L., Kudlow, B. A., Dos Santos, H. G., Sletvold, O., Shafeghati, Y., Botha, E. G., Garg, A., Hanson, N. B., Martin, G. M., Saira Mian, I., Kennedy, B. K., & Oshima, J. (2003). LMNA mutations in atypical Werner's syndrome. Lancet, 362(9382), 440-445. https://doi.org/10.1016/S0140-6736(03)14069-X
Columbaro, M., Capanni, C., Mattioli, E., Novelli, G., Parnaik, V. K., Squarzoni, S., Maraldi, N. M., & Lattanzi, G. (2005). Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cellular and Molecular Life Sciences, 62(22), 2669-2678. https://doi.org/10.1007/s00018-005-5318-6
De Sandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C. L., Munnich, A., Le Merrer, M., & Lévy, N. (2003). Lamin a truncation in Hutchinson-Gilford progeria. Science, 300(5628), 2055. https://doi.org/10.1126/science.1084125
Dechat, T., Korbei, B., Vaughan, O. A., Vlcek, S., Hutchison, C. J., & Foisner, R. (2000). Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. Journal of Cell Science, 113(Pt 19), 3473-3484. https://doi.org/10.1242/jcs.113.19.3473
Dhe-Paganon, S., Werner, E. D., Chi, Y. I., & Shoelson, S. E. (2002). Structure of the globular tail of nuclear lamin. The journal of Biological Chemistry, 277(20), 17381-17384. https://doi.org/10.1074/jbc.C200038200
Doubaj, Y., De Sandre-Giovannoli, A., Vera, E. V., Navarro, C. L., Elalaoui, S. C., Tajir, M., Levy, N., & Sefiani, A. (2012). An inherited LMNA gene mutation in atypical Progeria syndrome. American Journal of Medical Genetics A, 158A(11), 2881-2887. https://doi.org/10.1002/ajmg.a.35557
Eriksson, M., Brown, W. T., Gordon, L. B., Glynn, M. W., Singer, J., Scott, L., Erdos, M. R., Robbins, C. M., Moses, T. Y., Berglund, P., Dutra, A., Pak, E., Durkin, S., Csoka, A. B., Boehnke, M., Glover, T. W., & Collins, F. S. (2003). Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature, 423(6937), 293-298. https://doi.org/10.1038/nature01629
Garg, A., Speckman, R. A., & Bowcock, A. M. (2002). Multisystem dystrophy syndrome due to novel missense mutations in the amino-terminal head and alpha-helical rod domains of the lamin A/C gene. American Journal of Medicine, 112(7), 549-555. https://doi.org/10.1016/S0002-9343(02)01070-7
Garg, A., Subramanyam, L., Agarwal, A. K., Simha, V., Levine, B., & Rosaria D'Apice, M. (2009). Atypical progeroid syndrome due to heterozygous missense LMNA mutations. The Journal of Clinical Endocrinology and Metabolism, 94(12), 4971-4983. https://doi.org/10.1210/jc.2009-0472
Guo, H., Luo, N., Hao, F., Hao, F., & Bai, Y. (2014). p.Pro4Arg mutation in LMNA gene: a new atypical progeria phenotype without metabolism abnormalities. Gene, 546(1), 35-39. https://doi.org/10.1016/j.gene.2014.05.042
Guo, X., Ling, C., Liu, Y., Zhang, X., & Zhang, S. (2016). A Case of Novel Lamin A/C Mutation Manifesting as Atypical Progeroid Syndrome and Cardiomyopathy. Canadian Journal of Cardiology, 32(9), 1166-e29. https://doi.org/10.1016/j.cjca.2015.11.011
Hennekam, R. C. (2006). Hutchinson-Gilford progeria syndrome: review of the phenotype. American Journal of Medical Genetics A, 140(23), 2603-2624. https://doi.org/10.1002/ajmg.a.31346
Hisama, F. M., Lessel, D., Leistritz, D., Friedrich, K., McBride, K. L., Matthew, T., Gary, S. P., Saha, B., Martin, G. M., Kubisch, C., & Oshima, J. (2011). Coronary artery disease in a Werner syndrome-like form of progeria characterized by low levels of progerin, a splice variant of lamin A. American journal of Medical Genetics A, 155A(12), 3002-3006. https://doi.org/10.1002/ajmg.a.34336
Jacob, K. N., & Garg, A. (2006). Laminopathies: multisystem dystrophy syndromes. Molecular Genetics and Metabolism, 87(4), 289-302. https://doi.org/10.1016/j.ymgme.2005.10.018
Kane, M. S., Lindsay, M. E., Judge, D. P., Barrowman, J., Ap Rhys, C., Simonson, L., Dietz, H. C., & Michaelis, S. (2013). LMNA-Associated Cardiocutaneous Progeria: An Inherited Autosomal Dominant Premature Aging Syndrome With Late Onset. American Journal of Medical Genetics A, 161A(7), 1599-1611. https://doi.org/10.1002/ajmg.a.35971
Karczewski, K. J., Francioli, L. C., Cummings, B. B., Alföldi, J., Wang, Q., Collins, R. L., Laricchia, K. M., Ganna, A., Birnbaum, D. P., Gauthier, L. D., Brand, H., Solomonson, M., Watts, N. A., Rhodes, D. A., Singer-Berk, M., England, E. M., Seaby, E. G., Kosmicki, J. A., Walters, R. K., & MacArthur, D. G. (2020). The mutational constraint spectrum quantified from variation in 141,456 humans. Nature, 581(7809), 434-443. https://doi.org/10.1038/s41586-020-2308-7
Kirschner, J., Brune, T., Wehnert, M., Denecke, J., Wasner, C., Feuer, A., Marquardt, T., Ketelsen, U. P., & Wieacker, P. (2005). p.S143F mutation in lamin A/C: a new phenotype combining myopathy and progeria. Annals of Neurology, 57(1), 148-151. https://doi.org/10.1002/ana.20359
Krimm, I., Ostlund, C., Gilquin, B., Couprie, J., Hossenlopp, P., Mornon, J. P., Bonne, G., Courvalin, J. C., Worman, H. J., & Zinn-Justin, S. (2002). The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure, 10(6), 811-823. https://doi.org/10.1016/s0969-2126(02)00777-3
Liang, L., Zhang, H., & Xuefan, G. (2009). Homozygous LMNA mutation R527C in atypical Hutchinson-Gilford progeria syndrome: evidence for autosomal recessive inheritance. Acta Paediatrica, 98(8), 1365-1368. https://doi.org/10.1111/j.1651-2227.2009.01324.x
Lombardi, F., Gullotta, F., Columbaro, M., Filareto, A., D'Adamo, M., Vielle, A., Guglielmi, V., Nardone, A. M., Azzolini, V., Grosso, E., Lattanzi, G., Rosaria D’Apice, M., Masala, S., Maraldi, N. M., Sbraccia, P., & Novelli, G. (2007). Compound heterozygosity for mutations in LMNA in a patient with a myopathic and lipodystrophic mandibuloacral dysplasia type a phenotype. The Journal of Clinical Endocrinology and Metabolism, 92(11), 4467-4471. https://doi.org/10.1210/jc.2007-0116
Luo, D. Q., Wang, X. Z., Meng, Y., He, D. Y., Chen, Y. M., Ke, Z. Y., Yan, M., Huang, Y., & Chen, D. F. (2014). Mandibuloacral dysplasia type A-associated progeria caused by homozygous LMNA mutation in a family from Southern China. BMC Pediatrics, Oct 7, 14(1), 256. https://doi.org/10.1186/1471-2431-14-256
Madej-Pilarczyk, A., Kmiec, T., Fidzianska, A., Rekawek, I., Niebrój-Dobosz, I., Turska-Kmieć, A., Nestorowicz, K., Jóźwiak, S., & Hausmanowa-Petrusewicz, I. (2008). Progeria caused by a rare LMNA mutation p.S143F associated with mild myopathy and atrial fibrillation. European Journal of Paediatric Neurology, 12(5), 427-430. https://doi.org/10.1016/j.ejpn.2007.11.011
Madej-Pilarczyk, A., Rosinska-Borkowska, D., Rekawek, J., Marchel, M., Szaluś, E., Jabłońska, S., & Hausmanowa-Petrusewicz, I. (2009). Progeroid syndrome with scleroderma-like skin changes associated with homozygous R435C LMNA mutation. American Journal of Medical Genetics A, 149A(11), 2387-2392. https://doi.org/10.1002/ajmg.a.33018
Merideth, M. A., Gordon, L. B., Clauss, S., Sachdev, V., Smith, A. C., Perry, M. B., Brewer, C. C., Zalewski, C., Kim, H. J., Solomon, B., Brooks, B. P., Gerber, L. H., Turner, M. L., Domingo, D. L., Hart, T. C., Graf, J., Reynolds, J. C., Gropman, A., Yanovski, J. A., … Introne, W. J. (2008). Phenotype and course of Hutchinson-Gilford progeria syndrome. The New England Journal of Medicine, 358(6), 592-604. https://doi.org/10.1056/NEJMoa0706898
Navarro, C. L., Cadinanos, J., De Sandre-Giovannoli, A., Bernard, R., Courrier, S., Boccaccio, I., Boyer, A., Kleijer, W. J., Wagner, A., Giuliano, F., Beemer, F. A., Freije, J. M., Cau, P., Hennekam, R. C. M., López-Otín, C., Badens, C., & Lévy, N. (2005). Loss of ZMPSTE24 (FACE-1) causes autosomal recessive restrictive dermopathy and accumulation of Lamin A precursors. Human Molecular Genetics, 14(11), 1503-1513. https://doi.org/10.1093/hmg/ddi159
Navarro, C. L., De Sandre-Giovannoli, A., Bernard, R., Boccaccio, I., Boyer, A., Geneviève, D., Hadj-Rabia, S., Gaudy-Marqueste, C., Smitt, H. S., Vabres, P., Faivre, L., Verloes, A., Van Essen, T., Flori, E., Hennekam, R., Beemer, F. A., Laurent, N., Le Merrer, M., Cau, P., & Lévy, N. (2004). Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Human Molecular Genetics, 13(20), 2493-2503. https://doi.org/10.1093/hmg/ddh265
Novelli, G., Muchir, A., Sangiuolo, F., Helbling-Leclerc, A., Rosaria D'Apice, M., Massart, C., Capon, F., Sbraccia, P., Federici, M., Lauro, R., Tudisco, C., Pallotta, R., Scarano, G., Dallapiccola, B., Merlini, L., & Bonne, G. (2002). Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. American Journal of Human Genetics, 71(2), 426-431. https://doi.org/10.1086/341908
Plasilova, M., Chattopadhyay, C., Pal, P., Buechner, S. A., Mueller, H., Miny, P., Ghosh, A., & Heinimann, K. (2004). Homozygous missense mutation in the lamin A/C gene causes autosomal recessive Hutchinson-Gilford progeria syndrome. Journal of Medical Genetics, 41(8), 609-614. https://doi.org/10.1136/jmg.2004.019661.41/8/609
Prokocimer, M., Davidovich, M., Nissim-Rafinia, M., Wiesel-Motiuk, N., Z Bar, D., Barkan, R., Meshorer, E., Gruenbaum, Y. (2009). Nuclear lamins: key regulators of nuclear structure and activities. Journal of Cellular and Molecular Medicine, 13(6), 1059-1085. https://doi.org/10.1111/j.1582-4934.2008.00676.x
Renard, D., Fourcade, G., Milhaud, D., Bessis, D., Esteves-Vieira, V., Boyer, A., Roll, P., Bourgeois, P., Levy, N., & Sandre-Giovannoli, A. (2009). Novel LMNA mutation in atypical Werner syndrome presenting with ischemic disease. Stroke, 40(2), e11-e14. https://doi.org/10.1161/STROKEAHA.108.531780
Richards, S., Aziz, N., Bale, S., Bick, D., Das, S., Gastier-Foster, J., Grody, W. W., Hegde, M., Lyon, E., Spector, E., Voelkerding, K., Rehm, H. L. (2015). ACMG Laboratory Quality Assurance Committee. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genetics in Medicine, 17(5), 405-424. https://doi.org/10.1038/gim.2015.30
Sakaki, M., Koike, H., Takahashi, N., Sasagawa, N., Tomioka, S., Arahata, K., & Ishiura, S. (2001). Interaction between emerin and nuclear lamins. Journal of Biochemistry, 129(2), 321-327. https://doi.org/10.1093/oxfordjournals.jbchem.a002860
Savage, D. B., Soos, M. A., Powlson, A., O'Rahilly, S., McFarlane, I., Halsall, D. J., Barroso, I., Thomas, E. L., Bell, J. D., Scobie, I., Belchetz, P. E., Kelly, W. F., & Schafer, A. J. (2004). Familial partial lipodystrophy associated with compound heterozygosity for novel mutations in the LMNA gene. Diabetologia, 47(4), 753-756. https://doi.org/10.1007/s00125-004-1360-4
Schreiber, K. H., & Kennedy, B. K. (2013). When lamins go bad: nuclear structure and disease. Cell, 152(6), 1365-1375. https://doi.org/10.1016/j.cell.2013.02.015
Schultz, B., Miller, D. D., & Maguiness, S. (2019). Diffuse, mottled hyperpigmentation and mutations in LMNA gene in a 5-year-old boy, his mother, and his grandmother: Atypical progeroid syndrome. Pediatric Dermatology, 36(6), 913-917. https://doi/10.1111/pde.13917
Shackleton, S., Smallwood, D. T., Clayton, P., Wilson, C., Agarwal, A. K., Garg, A., & Trembath, R. C. Compound heterozygous ZMPSTE24 mutations reduce prelamin A processing and result in a severe progeroid phenotype. Journal of Medical Genetics, 42(6), e36. https://doi.org/10.1136/jmg.2004.029751
Simha, V., Agarwal, A. K., Oral, E. A., Oral, E. A., Fryns, J. P., & Garg, A. (2003). Genetic and phenotypic heterogeneity in patients with mandibuloacral dysplasia-associated lipodystrophy. Journal of Clinical Endocrinology and Metabolism, 88(6), 2821-2824. https://doi.org/10.1210/jc.2002-021575
Simon, D. N., Zastrow, M. S., & Wilson, K. L. (2010). Direct actin binding to A- and B-type lamin tails and actin filament bundling by the lamin A tail. Nucleus, 1(3), 264-272. https://doi.org/10.4161/nucl.1.3.11799
Sinensky, M., Fantle, K., Trujillo, M., McLain, T., Kupfer, A., & Dalton, M. (1994). The processing pathway of prelamin A. Journal of Cell Science, 107(Pt 1), 61-67.
Soria-Valles, C., Carrero, D., Gabau, E., Velasco, G., Quesada, V., Bárcena, C., Moens, M., Fieggen, K., Möhrcken, S., Owens, M., Puente, D. A., Asensio, O., Loeys, B., Pérez, A., Benoit, V., Wuyts, W., Lévy, N., Hennekam, R. C., De Sandre-Giovannoli, A., & López-Otín, C. (2016). Novel LMNA mutations cause an aggressive atypical neonatal progeria without progerin accumulation. Journal of Medical Genetics, 53(11), 776-785. https://doi.org/10.1136/jmedgenet-2015-103695
Taylor, M. R., Slavov, D., Gajewski, A., Vlcek, S., Ku, L., Fain, P. R., Carniel, E., Di Lenarda, A., Sinagra, G., Boucek, M. M., Cavanaugh, J., Graw, S. L., Ruegg, P., Feiger, J., Zhu, X., Ferguson, D. A., Bristow, M. R., Gotzmann, J., Foisner, R., … Familial Cardiomyopathy Registry Research Group Mestroni. (2005). Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Human Mutation, 26(6), 566-574. https://doi.org/10.1002/humu.20250
Toni, L., Dušátková, P., Novotná, D., Zemková, D., Průhová, Š., & Lebl, J. (2019). Short stature in a boy with atypical progeria syndrome due to LMNA c.433G>A [p.(Glu145Lys)]: apparent growth hormone deficiency but poor response to growth hormone therapy. Journal of Pediatric Endocrinology and Metabolism, 32(7), 775-779. https://doi.org/10.1515/jpem-2019-0107
Tu, Y., Sánchez-Iglesias, S., Araújo-Vilar, D., Fong, L. G., & Young, S. G. (2016). LMNA missense mutations causing familial partial lipodystrophy do not lead to an accumulation of prelamin A. Nucleus, 7(5), 512-521. https://doi.org/10.1080/19491034.2016.1242542
Van der Kooi, A. J., Bonne, G., Eymard, B., Duboc, D., Talim, B., Van der Valk, M., Reiss, P., Richard, P., Demay, L., Merlini, L., Schwartz, K., Busch, H. F., & de Visser, M. (2002). Lamin A/C mutations with lipodystrophy, cardiac abnormalities, and muscular dystrophy. Neurology, 59(4), 620-623. https://doi.org/10.1212/wnl.59.4.620
Vantyghem, M. C., Pigny, P., Maurage, C. A., Rouaix-Emery, N., Stojkovic, T., Cuisset, J. M., Millaire, A., Lascols, O., Vermersch, P., Wemeau, J. L., Capeau, J., & Vigouroux, C. (2004). Patients with familial partial lipodystrophy of the Dunnigan type due to a LMNA R482W mutation show muscular and cardiac abnormalities. The Journal of Clinical Endocrinology and Metabolism, 89(11), 5337-5346. https://doi.org/10.1210/jc.2003-031658
Verstraeten, V. L., Broers, J. L., van Steensel, M. A., Zinn-Justin, S., Ramaekers, F. C., Steijlen, P. M., Kamps, M., Kuijpers, H. J. H., Merckx, D., Smeets, H. J. M., Hennekam, R. C. M., Marcelis, C. L. M., & van den Wijngaard, A. (2006). Compound heterozygosity for mutations in LMNA causes a progeria syndrome without prelamin A accumulation. Human Molecular Genetics, 15(16), 2509-2522. https://doi.org/10.1093/hmg/ddl172
Vytopil, M., Benedetti, S., Ricci, E., Galluzzi, G., Dello Russo, A., Merlini, L., Boriani, G., Gallina, M., Morandi, L., Politano, L., Moggio, M., Chiveri, L., Hausmanova-Petrusewicz, I., Ricotti, R., Vohanka, S., Toman, J., & Toniolo, D. (2003). Mutation analysis of the lamin A/C gene (LMNA) among patients with different cardiomuscular phenotypes. Journal of Medical Genetics, 40(12), e132. https://doi.org/10.1136/jmg.40.12.e132
Worman, H. J., & Bonne, G. (2007). "Laminopathies": a wide spectrum of human diseases. Experimental Cell Research, 313(10), 2121-2133. https://doi.org/10.1016/j.yexcr.2007.03.028
Young, L. W., Radebaugh, J. F., Rubin, P., Sensenbrenner, J. A., Fiorelli, G., & McKusick, V. A. (1971). New syndrome manifested by mandibular hypoplasia, acroosteolysis, stiff joints and cutaneous atrophy (mandibuloacral dysplasia) in two unrelated boys. Birth Defects Original Article Series, 7(7), 291-297.
Yukina, M., Nuralieva, N., Sorkina, E., Troshina, E., Tiulpakov, A., Belaya, Z., & Melnichenko, G. (2021). Atypical progeroid syndrome (p.E262K LMNA mutation): a rare cause of short stature and osteoporosis. Endocrinology Diabetes and Metabolism Case Reports, 14, 20-0188. https://doi.org/10.1530/EDM-20-0188
Zirn, B., Kress, W., Grimm, T., Berthold, L. D., Neubauer, B., Kuchelmeister, K., Müller, U., & Hahn, A. (2008). Association of homozygous LMNA mutation R471C with new phenotype: mandibuloacral dysplasia, progeria, and rigid spine muscular dystrophy. American Journal of Medical Genetics A, 146A(8), 1049-1054. https://doi.org/10.1002/ajmg.a.32259