Marked neuropsychiatric involvement and dysmorphic features in nemaline myopathy.

Acta1 Congenital myopathy Nebulin Nemaline myopathy

Journal

Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175

Informations de publication

Date de publication:
18 Oct 2023
Historique:
received: 23 04 2023
accepted: 08 10 2023
medline: 18 10 2023
pubmed: 18 10 2023
entrez: 18 10 2023
Statut: aheadofprint

Résumé

Inherited nemaline myopathy is one of the most common congenital myopathies. This genetically heterogeneous disease is defined by the presence of nemaline bodies in muscle biopsy. The phenotypic spectrum is wide and cognitive involvement has been reported, although not extensively evaluated. We report two nemaline myopathy patients presenting pronounced central nervous system involvement leading to functional compromise and novel facial and skeletal dysmorphic findings, possibly expanding the disease phenotype. One patient had two likely pathogenic NEB variants, c.2943G > A and c.8889 + 1G > A, and presented cognitive impairment and dysmorphic features, and the other had one pathogenic variant in ACTA1, c.169G > C (p.Gly57Arg), presenting autism spectrum disorder and corpus callosum atrophy. Both patients had severe cognitive involvement despite milder motor dysfunction. We raise the need for further studies regarding the role of thin filament proteins in the central nervous system and for a systematic cognitive assessment of congenital myopathy patients.

Sections du résumé

BACKGROUND BACKGROUND
Inherited nemaline myopathy is one of the most common congenital myopathies. This genetically heterogeneous disease is defined by the presence of nemaline bodies in muscle biopsy. The phenotypic spectrum is wide and cognitive involvement has been reported, although not extensively evaluated.
METHODS METHODS
We report two nemaline myopathy patients presenting pronounced central nervous system involvement leading to functional compromise and novel facial and skeletal dysmorphic findings, possibly expanding the disease phenotype.
RESULTS RESULTS
One patient had two likely pathogenic NEB variants, c.2943G > A and c.8889 + 1G > A, and presented cognitive impairment and dysmorphic features, and the other had one pathogenic variant in ACTA1, c.169G > C (p.Gly57Arg), presenting autism spectrum disorder and corpus callosum atrophy. Both patients had severe cognitive involvement despite milder motor dysfunction.
CONCLUSION CONCLUSIONS
We raise the need for further studies regarding the role of thin filament proteins in the central nervous system and for a systematic cognitive assessment of congenital myopathy patients.

Identifiants

pubmed: 37851294
doi: 10.1007/s10072-023-07128-6
pii: 10.1007/s10072-023-07128-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. Fondazione Società Italiana di Neurologia.

Références

Wallgren-Pettersson C, Sewry CA, Nowak KJ, Laing NG (2011) Nemaline myopathies. Seminars Paediatr Neurol 18(4):230–238. https://doi.org/10.1016/j.spen.2011.10.004
doi: 10.1016/j.spen.2011.10.004
Amburgey K, Acker M, Saeed S, Amin R, Beggs AH, Bönnemann CG et al (2021) A cross-sectional study of nemaline myopathy. Neurol 96(10):e1425–e1436. https://doi.org/10.1212/WNL.0000000000011458
doi: 10.1212/WNL.0000000000011458
Moreno CAM, Abath Neto O, Donkervoort S, Hu Y, Reed UC, Oliveira ASB et al (2017) Clinical and histologic findings in ACTA1-related nemaline myopathy: case series and review of the literature. Pediatr Neurol 75:11–16. https://doi.org/10.1016/j.pediatrneurol.2017.04.002
doi: 10.1016/j.pediatrneurol.2017.04.002 pubmed: 28780987
Ryan MM, Schnell C, Strickland CD, Shield LK, Morgan G, Iannaccone ST et al (2001) Nemaline myopathy: a clinical study of 143 cases. Ann Neurol 50(3):312–320. https://doi.org/10.1002/ana.1080
doi: 10.1002/ana.1080 pubmed: 11558787
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38(16):e164–e164. https://doi.org/10.1093/nar/gkq603
doi: 10.1093/nar/gkq603 pubmed: 20601685 pmcid: 2938201
McLaren W, Gil L, Hunt SE, Riat HS, Ritchie GRS, Thormann A et al (2016) The ensemble variant effect predictor. Genome Biol 17(122):1–14. https://doi.org/10.1186/s13059-016-0974-4
doi: 10.1186/s13059-016-0974-4
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I et al (2005) The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x
doi: 10.1111/j.1532-5415.2005.53221.x pubmed: 15817019
Pike NA, Poulsen MK, Woo MA (2017) Validity of the Montreal cognitive assessment screener in adolescents and young adults with and without congenital heart disease. Nurs Res 66(3):222–230. https://doi.org/10.1097/NNR.0000000000000192
doi: 10.1097/NNR.0000000000000192 pubmed: 28448372 pmcid: 5408464
Schopler E, Reichler RJ, DeVellis RF, Daly K (1980) Toward objective classification of childhood autism: childhood autism rating scale (CARS). J Autism Dev Disord 10(1):91–103. https://doi.org/10.1007/BF02408436
doi: 10.1007/BF02408436 pubmed: 6927682
Lehtokari VL, Kiiski K, Sandaradura SA, Laporte J, Repo P, Frey JA et al (2014) Mutation update: the spectra of nebulin variants and associated myopathies. Hum Mutat 35(12):1418–1926. https://doi.org/10.1002/humu.22693
doi: 10.1002/humu.22693 pubmed: 25205138 pmcid: 4295925
Banihani R, Smile S, Yoon G, Dupuis A, Mosleh M, Snider A et al (2015) Cognitive and neurobehavioral profile in boys with duchenne muscular dystrophy. J Child Neurol 30(11):1472–1482. https://doi.org/10.1177/0883073815570154
doi: 10.1177/0883073815570154 pubmed: 25660133
Douniol M, Jacquette A, Cohen D, Bodeau N, Rachidi L, Angeard N et al (2012) Psychiatric and cognitive phenotype of childhood myotonic dystrophy type 1. Dev Med Child Neurol 54(10):905–911. https://doi.org/10.1111/j.1469-8749.2012.04379.x
doi: 10.1111/j.1469-8749.2012.04379.x pubmed: 22861906
Brun BN, Mockler SRH, Laubscher KM, Stephan CM, Wallace AM, Collison JA, et al (2017) Comparison of brain MRI findings with language and motor function in the dystroglycanopathies. Neurology 88(7):623–629. https://doi.org/10.1212/WNL.0000000000003609
Specht S, Straub V (2021) Intellectual disability in paediatric patients with genetic muscle diseases. Neuromuscul Disord 31(10):988–997. https://doi.org/10.1016/j.nmd.2021.08.012
doi: 10.1016/j.nmd.2021.08.012 pubmed: 34736636
Wallgren-Pettersson C (1989) Congenital nemaline myopathy: a clinical follow-up of twelve patients. J Neurol Sci 89(1):1–14. https://doi.org/10.1016/0022-510x(89)90002-6
doi: 10.1016/0022-510x(89)90002-6 pubmed: 2926439
Moreno CAM, Artilheiro MC, Fonseca ATQSM, Camelo CG, de Medeiros GC, Sassi FC et al (2023) Clinical manifestation of nebulin-associated nemaline myopathy. Neurol Genet 9(1):1–10. https://doi.org/10.1212/NXG.0000000000200056
Saito Y, Komaki H, Hattori A, Takeuchi F, Sasaki M, Kawabata K et al (2011) Extramuscular manifestations in children with severe congenital myopathy due to ACTA1 gene mutations. Neuromuscul Disord 21(7):489–493. https://doi.org/10.1016/j.nmd.2011.03.004
doi: 10.1016/j.nmd.2011.03.004 pubmed: 21514153
Shmueli O, Horn-Saban S, Chalifa-Caspi V, Shmoish M, Ophir R, Benjamin-Rodrig H et al (2003) GeneNote: whole genome expression profiles in normal human tissues C R Biol 326(10,11):1067–1072. https://doi.org/10.1016/j.crvi.2003.09.012
Kalajzic I, Kalajzic Z, Wang L, Jiang X, Lamothe K, San Miguel SM et al (2007) Pericyte/myoblast phenotype of osteoprogenitor cell. J Musculoskelet Neuronal Interact 7(4):320–322
pubmed: 18094492
Chandra M, Mamidi R, Ford S, Hidalgo C, Witt C, Ottenheijm C et al (2009) Nebulin alters cross-bridge cycling kinetics and increases thin filament activation: a novel mechanism for increasing tension and reducing tension cost. J Biol Chem 284(45):30889–30896. https://doi.org/10.1074/jbc.M109.049718
doi: 10.1074/jbc.M109.049718 pubmed: 19736309 pmcid: 2781488
Laitila J, Hanif M, Paetau A, Hujanen S, Keto J, Somervuo P et al (2012) Expression of multiple nebulin isoforms in human skeletal muscle and brain. Muscle Nerve 46(5):730–777
doi: 10.1002/mus.23380 pubmed: 22941678
Blokhuis AM, Deenen JCW, Voermans NC, van Engelen BGM, Kievit W, Groothuis JT (2021) The socioeconomic burden of facioscapulohumeral muscular dystrophy. J Neurol 268(12):4778–4788. https://doi.org/10.1007/s00415-021-10591-w
doi: 10.1007/s00415-021-10591-w pubmed: 34043041 pmcid: 8563627
Gaugler T, Klei L, Sanders SJ, Bodea CA, Goldberg AP, Lee AB et al (2014) Most genetic risk for autism resides with common variation. Nat Genet 46(8):881–885. https://doi.org/10.1038/ng.3039
doi: 10.1038/ng.3039 pubmed: 25038753 pmcid: 4137411
Astrea G, Battini R, Lenzi S, Frosini S, Bonetti S, Moretti E et al (2016) Learning disabilities in neuromuscular disorders: a springboard for adult life. Acta Myol 35(2):90–95
pubmed: 28344438 pmcid: 5343745
D’Angelo MG, Bresolin N (2006) Cognitive impairment in neuromuscular disorders. Muscle Nerve 34(1):16–33. https://doi.org/10.1002/mus.20535
doi: 10.1002/mus.20535 pubmed: 16544320

Auteurs

Paulo Ribeiro Nóbrega (PR)

Department of Neurology, Faculdade de Medicina, Universidade Federal do Ceará, R. Alexandre Baraúna, 949, Rodolfo Teófilo, Fortaleza, CE, 60430-160, Brazil. paulo_r_med@yahoo.com.br.
Department of Neurology, Faculdade de Medicina, Universidade de São Paulo (FMUSP), Av. Dr. Arnaldo, 455, Cerqueira César, Pacaembu, São Paulo, 01246-903, Brazil. paulo_r_med@yahoo.com.br.
Faculty of Medicine, Unichristus University, Rua Vereador Paulo Mamede, 131, Fortaleza, CE, 60160-196, Brazil. paulo_r_med@yahoo.com.br.

Jorge Luiz de Brito de Souza (JL)

Center of Health Sciences, Universidade Estadual do Ceará, Av. Dr. Silas Munguba, 1700, Itaperi, Fortaleza, CE, 60714-903, Brazil.

Rebeca Bessa Maurício (RB)

Center of Health Sciences, Universidade Estadual do Ceará, Av. Dr. Silas Munguba, 1700, Itaperi, Fortaleza, CE, 60714-903, Brazil.

Anderson Rodrigues Brandão de Paiva (ARB)

Department of Neurology, Faculdade de Medicina, Universidade de São Paulo (FMUSP), Av. Dr. Arnaldo, 455, Cerqueira César, Pacaembu, São Paulo, 01246-903, Brazil.
Mendelics Genomic Analysis, Av. Braz Leme, 1631, Casa Verde, São Paulo, SP, 02511-000, Brazil.

Daniel Aguiar Dias (DA)

Department of Radiology, Faculdade de Medicina da Universidade Federal do Ceará, R. Alexandre Baraúna, 949, Rodolfo Teófilo, Fortaleza, CE, 60430-160, Brazil.

Clara Gontijo Camelo (CG)

Department of Neurology, Faculdade de Medicina, Universidade de São Paulo (FMUSP), Av. Dr. Arnaldo, 455, Cerqueira César, Pacaembu, São Paulo, 01246-903, Brazil.

Edmar Zanotelli (E)

Department of Neurology, Faculdade de Medicina, Universidade de São Paulo (FMUSP), Av. Dr. Arnaldo, 455, Cerqueira César, Pacaembu, São Paulo, 01246-903, Brazil.

David Schlesinger (D)

Mendelics Genomic Analysis, Av. Braz Leme, 1631, Casa Verde, São Paulo, SP, 02511-000, Brazil.

Pedro Braga-Neto (P)

Department of Neurology, Faculdade de Medicina, Universidade Federal do Ceará, R. Alexandre Baraúna, 949, Rodolfo Teófilo, Fortaleza, CE, 60430-160, Brazil.
Center of Health Sciences, Universidade Estadual do Ceará, Av. Dr. Silas Munguba, 1700, Itaperi, Fortaleza, CE, 60714-903, Brazil.

Cristiane Araujo Martins Moreno (CAM)

Department of Neurology, Faculdade de Medicina, Universidade de São Paulo (FMUSP), Av. Dr. Arnaldo, 455, Cerqueira César, Pacaembu, São Paulo, 01246-903, Brazil.
Mendelics Genomic Analysis, Av. Braz Leme, 1631, Casa Verde, São Paulo, SP, 02511-000, Brazil.

Classifications MeSH