Selective loss of a LAP1 isoform causes a muscle-specific nuclear envelopathy.
Emerin
LAP1
Lamin
Myopathy
Nuclear envelopathy
TOR1AIP1
Journal
Neurogenetics
ISSN: 1364-6753
Titre abrégé: Neurogenetics
Pays: United States
ID NLM: 9709714
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
14
10
2020
accepted:
24
12
2020
pubmed:
7
1
2021
medline:
19
11
2021
entrez:
6
1
2021
Statut:
ppublish
Résumé
The nuclear envelope (NE) separates the nucleus from the cytoplasm in all eukaryotic cells. A disruption of the NE structure compromises normal gene regulation and leads to severe human disorders collectively classified as nuclear envelopathies and affecting skeletal muscle, heart, brain, skin, and bones. The ubiquitous NE component LAP1B is encoded by TOR1AIP1, and the use of an alternative start codon gives rise to the shorter LAP1C isoform. TOR1AIP1 mutations have been identified in patients with diverging clinical presentations such as muscular dystrophy, progressive dystonia with cerebellar atrophy, and a severe multi-systemic disorder, but the correlation between the mutational effect and the clinical spectrum remains to be determined. Here, we describe a novel TOR1AIP1 patient manifesting childhood-onset muscle weakness and contractures, and we provide clinical, histological, ultrastructural, and genetic data. We demonstrate that the identified TOR1AIP1 frameshift mutation leads to the selective loss of the LAP1B isoform, while the expression of LAP1C was preserved. Through comparative review of all previously reported TOR1AIP1 cases, we delineate a genotype/phenotype correlation and conclude that LAP1B-specific mutations cause a progressive skeletal muscle phenotype, while mutations involving a loss of both LAP1B and LAP1C isoforms induce a syndromic disorder affecting skeletal muscle, brain, eyes, ear, skin, and bones.
Identifiants
pubmed: 33405017
doi: 10.1007/s10048-020-00632-3
pii: 10.1007/s10048-020-00632-3
doi:
Substances chimiques
Nuclear Proteins
0
Protein Isoforms
0
Class I Phosphatidylinositol 3-Kinases
EC 2.7.1.137
PIK3CA protein, human
EC 2.7.1.137
Types de publication
Case Reports
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
33-41Références
Hetzer MW (2010) The nuclear envelope. Cold Spring Harb Perspect Biol 2(3):a000539. https://doi.org/10.1101/cshperspect.a000539
doi: 10.1101/cshperspect.a000539
pubmed: 20300205
pmcid: 2829960
Burke B, Stewart CL (2013) The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14(1):13–24. https://doi.org/10.1038/nrm3488
doi: 10.1038/nrm3488
pubmed: 23212477
Bonne G, Quijano-Roy S (2013) Emery-Dreifuss muscular dystrophy, laminopathies, and other nuclear envelopathies. Handb Clin Neurol 113:1367–1376. https://doi.org/10.1016/B978-0-444-59565-2.00007-1
doi: 10.1016/B978-0-444-59565-2.00007-1
pubmed: 23622360
De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, Lyonnet S, Stewart CL, Munnich A, Le Merrer M, Levy N (2003) Lamin a truncation in Hutchinson-Gilford progeria. Science 300(5628):2055. https://doi.org/10.1126/science.1084125
doi: 10.1126/science.1084125
pubmed: 12702809
Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P, Dutra A, Pak E, Durkin S, Csoka AB, Boehnke M, Glover TW, Collins FS (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
doi: 10.1038/nature01629
pubmed: 12714972
Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D (1994) Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 8(4):323–327. https://doi.org/10.1038/ng1294-323
doi: 10.1038/ng1294-323
pubmed: 7894480
Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, Ragnauth CD, Yi Q, Mellad JA, Warren DT, Wheeler MA, Ellis JA, Skepper JN, Vorgerd M, Schlotter-Weigel B, Weissberg PL, Roberts RG, Wehnert M, Shanahan CM (2007) Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet 16(23):2816–2833. https://doi.org/10.1093/hmg/ddm238
doi: 10.1093/hmg/ddm238
pubmed: 17761684
Puente XS, Quesada V, Osorio FG, Cabanillas R, Cadinanos J, Fraile JM, Ordonez GR, Puente DA, Gutierrez-Fernandez A, Fanjul-Fernandez M, Levy N, Freije JM, Lopez-Otin C (2011) Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am J Hum Genet 88(5):650–656. https://doi.org/10.1016/j.ajhg.2011.04.010
doi: 10.1016/j.ajhg.2011.04.010
pubmed: 21549337
pmcid: 3146734
Santos M, Domingues SC, Costa P, Muller T, Galozzi S, Marcus K, da Cruz e Silva EF, da Cruz e Silva OA, Rebelo S (2014) Identification of a novel human LAP1 isoform that is regulated by protein phosphorylation. PLoS One 9 (12):e113732. https://doi.org/10.1371/journal.pone.0113732
Senior A, Gerace L (1988) Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. J Cell Biol 107(6 Pt 1):2029–2036. https://doi.org/10.1083/jcb.107.6.2029
doi: 10.1083/jcb.107.6.2029
pubmed: 3058715
Goodchild RE, Dauer WT (2005) The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol 168(6):855–862. https://doi.org/10.1083/jcb.200411026
doi: 10.1083/jcb.200411026
pubmed: 15767459
pmcid: 2171781
Martin L, Crimaudo C, Gerace L (1995) cDNA cloning and characterization of lamina-associated polypeptide 1C (LAP1C), an integral protein of the inner nuclear membrane. J Biol Chem 270(15):8822–8828. https://doi.org/10.1074/jbc.270.15.8822
doi: 10.1074/jbc.270.15.8822
pubmed: 7721789
Sosa BA, Demircioglu FE, Chen JZ, Ingram J, Ploegh HL, Schwartz TU (2014) How lamina-associated polypeptide 1 (LAP1) activates Torsin. Elife 3:e03239. https://doi.org/10.7554/eLife.03239
doi: 10.7554/eLife.03239
pubmed: 25149450
pmcid: 4358337
Shin JY, Dauer WT, Worman HJ (2014) Lamina-associated polypeptide 1: protein interactions and tissue-selective functions. Semin Cell Dev Biol 29:164–168. https://doi.org/10.1016/j.semcdb.2014.01.010
doi: 10.1016/j.semcdb.2014.01.010
pubmed: 24508913
Rebelo S, da Cruz ESEF, da Cruz ESOA (2015) Genetic mutations strengthen functional association of LAP1 with DYT1 dystonia and muscular dystrophy. Mutat Res Rev Mutat Res 766:42–47. https://doi.org/10.1016/j.mrrev.2015.07.004
doi: 10.1016/j.mrrev.2015.07.004
pubmed: 26596547
Kayman-Kurekci G, Talim B, Korkusuz P, Sayar N, Sarioglu T, Oncel I, Sharafi P, Gundesli H, Balci-Hayta B, Purali N, Serdaroglu-Oflazer P, Topaloglu H, Dincer P (2014) Mutation in TOR1AIP1 encoding LAP1B in a form of muscular dystrophy: a novel gene related to nuclear envelopathies. Neuromuscul Disord 24(7):624–633. https://doi.org/10.1016/j.nmd.2014.04.007
doi: 10.1016/j.nmd.2014.04.007
pubmed: 24856141
Ghaoui R, Benavides T, Lek M, Waddell LB, Kaur S, North KN, MacArthur DG, Clarke NF, Cooper ST (2016) TOR1AIP1 as a cause of cardiac failure and recessive limb-girdle muscular dystrophy. Neuromuscul Disord 26(8):500–503. https://doi.org/10.1016/j.nmd.2016.05.013
doi: 10.1016/j.nmd.2016.05.013
pubmed: 27342937
Feng X, Wu J, Xian W, Liao B, Liao S, Yao X, 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(1):588. https://doi.org/10.1186/s12891-020-03616-4
doi: 10.1186/s12891-020-03616-4
pubmed: 32873274
pmcid: 7466787
Dorboz I, Coutelier M, Bertrand AT, Caberg JH, Elmaleh-Berges M, Laine J, Stevanin G, Bonne G, Boespflug-Tanguy O, Servais L (2014) Severe dystonia, cerebellar atrophy, and cardiomyopathy likely caused by a missense mutation in TOR1AIP1. Orphanet J Rare Dis 9:174. https://doi.org/10.1186/s13023-014-0174-9
doi: 10.1186/s13023-014-0174-9
pubmed: 25425325
pmcid: 4302636
Fichtman B, Zagairy F, Biran N, Barsheshet Y, Chervinsky E, Ben Neriah Z, Shaag A, Assa M, Elpeleg O, Harel A, Spiegel R (2019) Combined loss of LAP1B and LAP1C results in an early onset multisystemic nuclear envelopathy. Nat Commun 10(1):605. https://doi.org/10.1038/s41467-019-08493-7
doi: 10.1038/s41467-019-08493-7
pubmed: 30723199
pmcid: 6363790
Lessel I, Chen MJ, Luttgen S, Arndt F, Fuchs S, Meien S, Thiele H, Jones JR, Shaw BR, Crossman DK, Nurnberg P, Korf BR, Kubisch C, Lessel D (2020) Two novel cases further expand the phenotype of TOR1AIP1-associated nuclear envelopathies. Hum Genet 139(4):483–498. https://doi.org/10.1007/s00439-019-02105-6
doi: 10.1007/s00439-019-02105-6
pubmed: 32055997
pmcid: 7078146
Orngreen MC, Duno M, Ejstrup R, Christensen E, Schwartz M, Sacchetti M, Vissing J (2005) Fuel utilization in subjects with carnitine palmitoyltransferase 2 gene mutations. Ann Neurol 57(1):60–66. https://doi.org/10.1002/ana.20320
doi: 10.1002/ana.20320
pubmed: 15622536
Bhatia A, Mobley BC, Cogan J, Koziura ME, Brokamp E, Phillips J, Newman J, Undiagnosed Diseases N, Moore SA, Hamid R, Members of the Undiagnosed Diseases N (2019) Magnetic resonance imaging characteristics in case of TOR1AIP1 muscular dystrophy. Clin Imaging 58:108–113. https://doi.org/10.1016/j.clinimag.2019.06.010
doi: 10.1016/j.clinimag.2019.06.010
Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XO (1997) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 17(1):40–48. https://doi.org/10.1038/ng0997-40
doi: 10.1038/ng0997-40
pubmed: 9288096
Lornage X, Schartner V, Balbueno I, Biancalana V, Willis T, Echaniz-Laguna A, Scheidecker S, Quinlivan R, Fardeau M, Malfatti E, Lannes B, Sewry C, Romero NB, Laporte J, Bohm J (2019) Clinical, histological, and genetic characterization of PYROXD1-related myopathy. Acta Neuropathol Commun 7(1):138. https://doi.org/10.1186/s40478-019-0781-8
doi: 10.1186/s40478-019-0781-8
pubmed: 31455395
pmcid: 6710884
de Noronha CM, Sherman MP, Lin HW, Cavrois MV, Moir RD, Goldman RD, Greene WC (2001) Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science 294(5544):1105–1108. https://doi.org/10.1126/science.1063957
doi: 10.1126/science.1063957
pubmed: 11691994
Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Dumenil AM, Manel N, Piel M (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352(6283):359–362. https://doi.org/10.1126/science.aad7611
doi: 10.1126/science.aad7611
pubmed: 27013426
Schreiber KH, Kennedy BK (2013) When lamins go bad: nuclear structure and disease. Cell 152(6):1365–1375. https://doi.org/10.1016/j.cell.2013.02.015
doi: 10.1016/j.cell.2013.02.015
pubmed: 23498943
pmcid: 3706202
Malhas AN, Lee CF, Vaux DJ (2009) Lamin B1 controls oxidative stress responses via Oct-1. J Cell Biol 184(1):45–55. https://doi.org/10.1083/jcb.200804155
doi: 10.1083/jcb.200804155
pubmed: 19139261
pmcid: 2615091
Reddy KL, Zullo JM, Bertolino E, Singh H (2008) Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452(7184):243–247. https://doi.org/10.1038/nature06727
doi: 10.1038/nature06727
pubmed: 18272965