Current advance on distal myopathy genetics.
Journal
Current opinion in neurology
ISSN: 1473-6551
Titre abrégé: Curr Opin Neurol
Pays: England
ID NLM: 9319162
Informations de publication
Date de publication:
17 Jul 2024
17 Jul 2024
Historique:
medline:
17
7
2024
pubmed:
17
7
2024
entrez:
17
7
2024
Statut:
aheadofprint
Résumé
Distal myopathies are a clinically heterogenous group of rare, genetic muscle diseases, that present with weakness in hands and/or feet at onset. Some of these diseases remain accentuated in the distal muscles whereas others may later progress to the proximal muscles. In this review, the latest findings related to genetic and clinical features of distal myopathies are summarized. Variants in SMPX, DNAJB2, and HSPB6 have been identified as a novel cause of late-onset distal myopathy and neuromyopathy. In oculopharyngodistal myopathies, repeat expansions were identified in two novel disease-causing genes, RILPL1 and ABCD3. In multisystem proteinopathies, variants in HNRNPA1 and TARDBP, genes previously associated with amyotrophic lateral sclerosis, have been shown to cause late-onset distal myopathy without ALS. In ACTN2-related distal myopathy, the first recessive forms of the disease have been described, adding it to the growing list of genes were both dominant and recessive forms of myopathy are present. The identification of novel distal myopathy genes and pathogenic variants contribute to our ability to provide a final molecular diagnosis to a larger number of patients and increase our overall understanding of distal myopathy genetics and pathology.
Identifiants
pubmed: 39017652
doi: 10.1097/WCO.0000000000001299
pii: 00019052-990000000-00182
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 The Author(s). Published by Wolters Kluwer Health, Inc.
Références
Savarese M, Sarparanta J, Vihola A, et al. Panorama of the distal myopathies. Acta Myol 2020; 39:245–265.
Udd B. Genetics and pathogenesis of distal muscular dystrophies. Adv Exp Med Biol 2009; 652:23–38.
Milone M, Liewluck T. The unfolding spectrum of inherited distal myopathies. Muscle Nerve 2019; 59:283–294.
Savara J, Novosad T, Gajdos P, Kriegova E. Comparison of structural variants detected by optical mapping with long-read next-generation sequencing. Bioinformatics 2021; 37:3398–3404.
Palmer S, Groves N, Schindeler A, et al. The small muscle-specific protein Csl modifies cell shape and promotes myocyte fusion in an insulin-like growth factor 1-dependent manner. J Cell Biol 2001; 153:985–998.
Ervasti JM. Costameres: the Achilles’ heel of Herculean muscle. J Biol Chem 2003; 278:13591–13594.
Schraders M, Haas SA, Weegerink NJ, et al. Next-generation sequencing identifies mutations of SMPX, which encodes the small muscle protein, X-linked, as a cause of progressive hearing impairment. Am J Hum Genet 2011; 88:628–634.
Huebner AK, Gandia M, Frommolt P, et al. Nonsense mutations in SMPX, encoding a protein responsive to physical force, result in X-chromosomal hearing loss. Am J Hum Genet 2011; 88:621–627.
Johari M, Sarparanta J, Vihola A, et al. Missense mutations in small muscle protein X-linked (SMPX) cause distal myopathy with protein inclusions. Acta Neuropathol 2021; 142:375–393.
Salman D, Bolano-Diaz C, Muni-Lofra R, et al. Axial involvement as a prominent feature in SMPX-related distal myopathy. Neuromuscul Disord 2024; 39:3–4.
Kampinga HH, Craig EA. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 2010; 11:579–592.
Kampinga HH, Andreasson C, Barducci A, et al. Function, evolution, and structure of J-domain proteins. Cell Stress Chaperones 2019; 24:7–15.
Cheetham ME, Brion JP, Anderton BH. Human homologues of the bacterial heat-shock protein DnaJ are preferentially expressed in neurons. Biochem J 1992; 284 (Pt 2):469–476.
Claeys KG, Sozanska M, Martin JJ, et al. DNAJB2 expression in normal and diseased human and mouse skeletal muscle. Am J Pathol 2010; 176:2901–2910.
Chen HJ, Mitchell JC, Novoselov S, et al. The heat shock response plays an important role in TDP-43 clearance: evidence for dysfunction in amyotrophic lateral sclerosis. Brain 2016; 139 (Pt 5):1417–1432.
Blumen SC, Astord S, Robin V, et al. A rare recessive distal hereditary motor neuropathy with HSJ1 chaperone mutation. Ann Neurol 2012; 71:509–519.
Gess B, Auer-Grumbach M, Schirmacher A, et al. HSJ1-related hereditary neuropathies: novel mutations and extended clinical spectrum. Neurology 2014; 83:1726–1732.
Schabhuttl M, Wieland T, Senderek J, et al. Whole-exome sequencing in patients with inherited neuropathies: outcome and challenges. J Neurol 2014; 261:970–982.
Gonzaga-Jauregui C, Harel T, Gambin T, et al. Exome sequence analysis suggests that genetic burden contributes to phenotypic variability and complex neuropathy. Cell Rep 2015; 12:1169–1183.
Sanchez E, Darvish H, Mesias R, et al. Identification of a large DNAJB2 deletion in a family with spinal muscular atrophy and parkinsonism. Hum Mutat 2016; 37:1180–1189.
Liu X, Duan X, Zhang Y, et al. Molecular analysis and clinical diversity of distal hereditary motor neuropathy. Eur J Neurol 2020; 27:1319–1326.
Frasquet M, Rojas-Garcia R, Argente-Escrig H, et al. Distal hereditary motor neuropathies: mutation spectrum and genotype-phenotype correlation. Eur J Neurol 2021; 28:1334–1343.
Sharifi Z, Taheri M, Fallah MS, et al. Comprehensive mutation analysis and report of 12 novel mutations in a cohort of patients with spinal muscular atrophy in Iran. J Mol Neurosci 2021; 71:2281–2298.
Liu M, Xu Y, Hong D, et al. DNAJB2 c.184C>T mutation associated with distal hereditary motor neuropathy with rimmed vacuolar myopathy. Clin Neuropathol 2022; 41:226–232.
Sarparanta J, Jonson PH, Reimann J, et al. Extension of the DNAJB2a isoform in a dominant neuromyopathy family. Hum Mol Genet 2023; 32:3029–3039.
Yu J, Deng J, Wang Z. Oculopharyngodistal myopathy. Curr Opin Neurol 2022; 35:637–644.
Ishiura H, Shibata S, Yoshimura J, et al. Noncoding CGG repeat expansions in neuronal intranuclear inclusion disease, oculopharyngodistal myopathy and an overlapping disease. Nat Genet 2019; 51:1222–1232.
Ogasawara M, Iida A, Kumutpongpanich T, et al. CGG expansion in NOTCH2NLC is associated with oculopharyngodistal myopathy with neurological manifestations. Acta Neuropathol Commun 2020; 8:204.
Yu J, Shan J, Yu M, et al. The CGG repeat expansion in RILPL1 is associated with oculopharyngodistal myopathy type 4. Am J Hum Genet 2022; 109:533–541.
Gu X, Yu J, Jiao K, et al. Noncoding CGG repeat expansion in LOC642361/NUTM2B-AS1 is associated with a phenotype of oculopharyngodistal myopathy. J Med Genet 2024; 61:340–346.
Deng J, Yu J, Li P, et al. Expansion of GGC repeat in GIPC1 is associated with oculopharyngodistal myopathy. Am J Hum Genet 2020; 106:793–804.
Schaub JR, Stearns T. The Rilp-like proteins Rilpl1 and Rilpl2 regulate ciliary membrane content. Mol Biol Cell 2013; 24:453–464.
Wang T, Wong KK, Hong W. A unique region of RILP distinguishes it from its related proteins in its regulation of lysosomal morphology and interaction with Rab7 and Rab34. Mol Biol Cell 2004; 15:815–826.
Dhekne HS, Yanatori I, Gomez RC, et al. A pathway for Parkinson's disease LRRK2 kinase to block primary cilia and Sonic hedgehog signaling in the brain. Elife 2018; 7:e40202.
Zeng YH, Yang K, Du GQ, et al. GGC repeat expansion of RILPL1 is associated with oculopharyngodistal myopathy. Ann Neurol 2022; 92:512–526.
Roerig P, Mayerhofer P, Holzinger A, Gartner J. Characterization and functional analysis of the nucleotide binding fold in human peroxisomal ATP binding cassette transporters. FEBS Lett 2001; 492:66–72.
Okamoto T, Kawaguchi K, Watanabe S, et al. Characterization of human ATP-binding cassette protein subfamily D reconstituted into proteoliposomes. Biochem Biophys Res Commun 2018; 496:1122–1127.
Cortese A, Beecroft SJ, Facchini S, et al. A CCG expansion in ABCD3 causes oculopharyngodistal myopathy in individuals of European ancestry. medRxiv 2023.
Li C, Pittman S, Maltby C, et al. RAN translation of expanded CGG repeat in LRP12 may contribute to oculopharyngodistal myopathy. Neuromuscul Disord 2023; 33:S66–S192.
Rodriguez CM, Wright SE, Kearse MG, et al. A native function for RAN translation and CGG repeats in regulating fragile X protein synthesis. Nat Neurosci 2020; 23:386–397.
Mayeda A, Helfman DM, Krainer AR. Modulation of exon skipping and inclusion by heterogeneous nuclear ribonucleoprotein A1 and premRNA splicing factor SF2/ASF. Mol Cell Biol 1993; 13:2993–3001.
Paronetto MP, Achsel T, Massiello A, et al. The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. J Cell Biol 2007; 176:929–939.
Kim HJ, Kim NC, Wang YD, et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013; 495:467–473.
Hackman P, Rusanen SM, Johari M, et al. Dominant distal myopathy 3 (MPD3) caused by a deletion in the HNRNPA1 gene. Neurol Genet 2021; 7:e632.
Beijer D, Kim HJ, Guo L, et al. Characterization of HNRNPA1 mutations defines diversity in pathogenic mechanisms and clinical presentation. JCI Insight 2021; 6:148363.
Chompoopong P, Oskarsson B, Madigan NN, et al. Multisystem proteinopathies (MSPs) and MSP-like disorders: clinical-pathological-molecular spectrum. Ann Clin Transl Neurol 2023; 10:632–643.
Tollervey JR, Curk T, Rogelj B, et al. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 2011; 14:452–458.
Wang A, Conicella AE, Schmidt HB, et al. A single N-terminal phosphomimic disrupts TDP-43 polymerization, phase separation, and RNA splicing. EMBO J 2018; 37:e97452.
Vogler TO, Wheeler JR, Nguyen ED, et al. TDP-43 and RNA form amyloid-like myo-granules in regenerating muscle. Nature 2018; 563:508–513.
Mackenzie IR, Bigio EH, Ince PG, et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol 2007; 61:427–434.
Van] Deerlin VM, Leverenz JB, Bekris LM, et al. TARDBP mutations in amyotrophic lateral sclerosis with TDP-43 neuropathology: a genetic and histopathological analysis. Lancet Neurol 2008; 7:409–416.
Kabashi E, Valdmanis PN, Dion P, et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat Genet 2008; 40:572–574.
Sreedharan] J, Blair IP, Tripathi VB, et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008; 319:1668–1672.
Zibold J, Lessard LER, Picard F, et al. The new missense G376V-TDP-43 variant induces late-onset distal myopathy but not amyotrophic lateral sclerosis. Brain 2023; 147:1768–1783.
Ervilha Pereira P, Schuermans N, Meylemans A, et al. C-terminal frameshift variant of TDP-43 with pronounced aggregation-propensity causes rimmed vacuole myopathy but not ALS/FTD. Acta Neuropathol 2023; 145:793–814.
Beggs AH, Byers TJ, Knoll JH, et al. Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11. J Biol Chem 1992; 267:9281–9288.
Murphy AC, Young PW. The actinin family of actin cross-linking proteins - a genetic perspective. Cell Biosci 2015; 5:49.
Ribeiro Ede A Jr, Pinotsis N, Ghisleni A, et al. The structure and regulation of human muscle alpha-actinin. Cell 2014; 159:1447–1460.
Young P, Gautel M. The interaction of titin and alpha-actinin is controlled by a phospholipid-regulated intramolecular pseudoligand mechanism. EMBO J 2000; 19:6331–6340.
Savarese M, Palmio J, Poza JJ, et al. Actininopathy: a new muscular dystrophy caused by ACTN2 dominant mutations. Ann Neurol 2019; 85:899–906.
Lornage X, Romero NB, Grosgogeat CA, et al. ACTN2 mutations cause “Multiple structured Core Disease” (MsCD). Acta Neuropathol 2019; 137:501–519.
Ranta-Aho J, Olive M, Vandroux M, et al. Mutation update for the ACTN2 gene. Hum Mutat 2022; 43:1745–1756.
Savarese M, Jokela M, Udd B. Distal myopathy. Handb Clin Neurol 2023; 195:497–519.
Savarese M, Vihola A, Jokela ME, et al. Out-of-frame mutations in ACTN2 last exon cause a dominant distal myopathy with facial weakness. Neurol Genet 2021; 7:e619.
Chen L, Chen DF, Dong HL, et al. A novel frameshift ACTN2 variant causes a rare adult-onset distal myopathy with multiminicores. CNS Neurosci Ther 2021; 27:1198–1205.
Ranta-aho J, Felice KJ, Jonson PH, et al. Protein-extending ACTN2 frameshift variants cause variable myopathy phenotypes by protein aggregation. Ann Clin Transl Neurol 2024.
Inoue M, Noguchi S, Sonehara K, et al. A recurrent homozygous ACTN2 variant associated with core myopathy. Acta Neuropathol 2023; 142:785–788.
Donkervoort S, Mohassel P, O’Leary M, et al. Recurring homozygous ACTN2 variant (p.Arg506Gly) causes a recessive myopathy. Ann Clin Transl Neurol 2024; 11:629–640.