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Cross-sectional, Neuromuscular Phenotyping Study of Arhinia Patients With SMCHD1 Variants
Journal article   Open access   Peer reviewed

Cross-sectional, Neuromuscular Phenotyping Study of Arhinia Patients With SMCHD1 Variants

Payam Mohassel, Ning Chang, Kaoru Inoue, Angela Delaney, Ying Hu, Sandra Donkervoort, Dimah Saade, B Jeanne Billioux, Brooke Meader, Rita Volochayev, …
Neurology, Vol.98(13), pp.e1384-e1396
02/04/2022
DOI: 10.1212/WNL.0000000000200032
PMCID: PMC8967428
PMID: 35121673
url
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8967428View
Published (Version of record) Open Access

Abstract

Facioscapulohumeral muscular dystrophy type 2 (FSHD2) and arhinia are two distinct disorders caused by pathogenic variants in the same gene, . The mechanism underlying this phenotypic divergence remains unclear. In this study, we characterize the neuromuscular phenotype of individuals with arhinia caused by variants and analyze their complex genetic and epigenetic criteria to assess their risk for FSHD2. Eleven individuals with congenital nasal anomalies, including arhinia, nasal hypoplasia, or anosmia, underwent a neuromuscular exam, genetic testing, muscle ultrasound, and muscle MRI. Risk for FSHD2 was determined by combined genetic and epigenetic analysis of 4q35 haplotype, D4Z4 repeat length and methylation profile. We also compared expression levels of pathogenic DUX4 mRNA in primary myoblasts or dermal fibroblasts (upon myogenic differentiation or epigenetic transdifferentiation, respectively) in these individuals to those with confirmed FSHD2. Among the eleven individuals with rare, pathogenic, heterozygous missense variants in exons 3-11 of only a subset (n=3/11; 1 male, 2 females; age 25-51 years) met the strict genetic and epigenetic criteria for FSHD2 (D4Z4 repeat unit length <21 in with a 4qA haplotype, and D4Z4 methylation <30%). None of the 3 individuals had typical clinical manifestations or muscle imaging findings consistent with FSHD2. However, the arhinia patients meeting the permissive genetic and epigenetic criteria for FSHD2 displayed some DUX4 expression in dermal fibroblasts under the epigenetic de-repression by drug treatment and in the primary myoblasts undergoing myogenic differentiation. In this cross-sectional study, we identified arhinia patients who meet the full genetic and epigenetic criteria for FSHD2 and display the molecular hallmark of FSHD, that is de-repression and expression but who do not manifest with the typical clinicopathologic phenotype of FSHD2. The distinct dichotomy between FSHD2 and arhinia phenotypes despite an otherwise poised locus implies the presence of novel disease-modifying factors that seem to operate as a "switch", resulting in one phenotype and not the other. Identification and further understanding of these disease-modifying factors will likely provide valuable insight with therapeutic implications for both diseases.

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