Deenen, J. C. et al. Population-based incidence and prevalence of facioscapulohumeral dystrophy. Neurology 83, 1056–1059 (2014).
Google Scholar
Lemmers, R. J. et al. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329, 1650–1653 (2010).
Google Scholar
Lemmers, R. J. et al. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat. Genet. 44, 1370–1374 (2012).
Google Scholar
Tawil, R. et al. Clinical trial preparedness in facioscapulohumeral muscular dystrophy: clinical, tissue, and imaging outcome measures 29–30 May 2015, Rochester, New York. Neuromuscul. Disord. 26, 181–186 (2016).
Google Scholar
Mul, K. et al. What’s in a name? The clinical features of facioscapulohumeral muscular dystrophy. Pract. Neurol. 16, 201–207 (2016).
Google Scholar
Tawil, R. & Van Der Maarel, S. M. Facioscapulohumeral muscular dystrophy. Muscle Nerve 34, 1–15 (2006).
Google Scholar
Statland, J. M. & Tawil, R. Risk of functional impairment in facioscapulohumeral muscular dystrophy. Muscle Nerve 49, 520–527 (2014).
Google Scholar
Lemmers, R. J. et al. Somatic mosaicism in FSHD often goes undetected. Ann. Neurol. 55, 845–850 (2004).
Google Scholar
Tonini, M. M. et al. Asymptomatic carriers and gender differences in facioscapulohumeral muscular dystrophy (FSHD). Neuromuscul. Disord. 14, 33–38 (2004).
Google Scholar
Ricci, G. et al. Large scale genotype–phenotype analyses indicate that novel prognostic tools are required for families with facioscapulohumeral muscular dystrophy. Brain https://doi.org/10.1093/brain/awt226 (2013).
Google Scholar
Salort-Campana, E. et al. Low penetrance in facioscapulohumeral muscular dystrophy type 1 with large pathological D4Z4 alleles: a cross-sectional multicenter study. Orphanet J. Rare Dis. 10, 2 (2015).
Google Scholar
Wohlgemuth, M. et al. A family-based study into penetrance in facioscapulohumeral muscular dystrophy type 1. Neurology 91, e444–e454 (2018).
Google Scholar
Zatz, M. et al. The facioscapulohumeral muscular dystrophy (FSHD1) gene affects males more severely and more frequently than females. Am. J. Med. Genet. 77, 155–161 (1998).
Google Scholar
van der Maarel, S. M. et al. De novo facioscapulohumeral muscular dystrophy: frequent somatic mosaicism, sex-dependent phenotype, and the role of mitotic transchromosomal repeat interaction between chromosomes 4 and 10. Am. J. Hum. Genet. 66, 26–35 (2000).
Google Scholar
Sakellariou, P. et al. Mutation spectrum and phenotypic manifestation in FSHD Greek patients. Neuromuscul. Disord. 22, 339–349 (2012).
Google Scholar
Mul, K. et al. Phenotype–genotype relations in facioscapulohumeral muscular dystrophy type 1. Clin. Genet. 94, 521–527 (2018).
Google Scholar
Monforte, M. et al. Tracking muscle wasting and disease activity in facioscapulohumeral muscular dystrophy by qualitative longitudinal imaging. J. Cachexia Sarcopenia Muscle 10, 1258–1265 (2019).
Google Scholar
Katz, N. K. et al. Predictors of functional outcomes in patients with facioscapulohumeral muscular dystrophy. Brain 144, 3451–3460 (2021).
Google Scholar
Teveroni, E. et al. Estrogens enhance myoblast differentiation in facioscapulohumeral muscular dystrophy by antagonizing DUX4 activity. J. Clin. Invest. 127, 1531–1545 (2017).
Google Scholar
Mul, K., Horlings, C. G. C., Voermans, N. C., Schreuder, T. H. A. & van Engelen, B. G. M. Lifetime endogenous estrogen exposure and disease severity in female patients with facioscapulohumeral muscular dystrophy. Neuromuscul. Disord. 28, 508–511 (2018).
Google Scholar
Goselink, R. J. M. et al. Early onset as a marker for disease severity in facioscapulohumeral muscular dystrophy. Neurology 92, e378–e385 (2019).
Google Scholar
Klinge, L. et al. Severe phenotype in infantile facioscapulohumeral muscular dystrophy. Neuromuscul. Disord. 16, 553–558 (2006).
Google Scholar
Brouwer, O. F., Padberg, G. W., Wijmenga, C. & Frants, R. R. Facioscapulohumeral muscular dystrophy in early childhood. Arch. Neurol. 51, 387–394 (1994).
Google Scholar
Goselink, R. J. M. et al. Early onset facioscapulohumeral dystrophy — a systematic review using individual patient data. Neuromuscul. Disord. 27, 1077–1083 (2017).
Google Scholar
Tawil, R. et al. Evidence-based guideline summary: evaluation, diagnosis, and management of facioscapulohumeral muscular dystrophy: report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology and the Practice Issues Review Panel of the American Association of Neuromuscular and Electrodiagnostic Medicine. Neurology 85, 357–364 (2015).
Google Scholar
Aprile, I. et al. Balance and walking involvement in facioscapulohumeral dystrophy: a pilot study on the effects of custom lower limb orthoses. Eur. J. Phys. Rehab. Med. 49, 169–178 (2013).
Google Scholar
Voet, N. et al. Both aerobic exercise and cognitive-behavioral therapy reduce chronic fatigue in FSHD: an RCT. Neurology 83, 1914–1922 (2014).
Google Scholar
Andersen, G., Prahm, K. P., Dahlqvist, J. R., Citirak, G. & Vissing, J. Aerobic training and postexercise protein in facioscapulohumeral muscular dystrophy: RCT study. Neurology 85, 396–403 (2015).
Google Scholar
Andersen, G., Heje, K., Buch, A. E. & Vissing, J. High-intensity interval training in facioscapulohumeral muscular dystrophy type 1: a randomized clinical trial. J. Neurol. 264, 1099–1106 (2017).
Google Scholar
Wijmenga, C. et al. Location of facioscapulohumeral muscular dystrophy gene on chromosome 4. Lancet 336, 651–653 (1990).
Google Scholar
Wijmenga, C. et al. Mapping of facioscapulohumeral muscular dystrophy gene to chromosome 4q35-qter by multipoint linkage analysis and in situ hybridization. Genomics 9, 570–575 (1991).
Google Scholar
Wijmenga, C. et al. Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat. Genet. 2, 26–30 (1992).
Google Scholar
van Deutekom, J. C. et al. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum. Mol. Genet. 2, 2037–2042 (1993).
Google Scholar
Hewitt, J. E. et al. Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum. Mol. Genet. 3, 1287–1295 (1994).
Google Scholar
van Deutekom, J. C. et al. Identification of the first gene (FRG1) from the FSHD region on human chromosome 4q35. Hum. Mol. Genet. 5, 581–590 (1996).
Google Scholar
van Geel, M. et al. The FSHD region on human chromosome 4q35 contains potential coding regions among pseudogenes and a high density of repeat elements. Genomics 61, 55–65 (1999).
Google Scholar
van Geel, M. et al. Identification of a novel β-tubulin subfamily with one member (TUBB4Q) located near the telomere of chromosome region 4q35. Cytogenet. Cell Genet. 88, 316–321 (2000).
Google Scholar
Rijkers, T. et al. FRG2, an FSHD candidate gene, is transcriptionally upregulated in differentiating primary myoblast cultures of FSHD patients. J. Med. Genet. 41, 826–836 (2004).
Google Scholar
Tupler, R. et al. Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy. J. Med. Genet. 33, 366–370 (1996).
Google Scholar
Gabellini, D., Green, M. R. & Tupler, R. Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110, 339–348 (2002).
Google Scholar
Bodega, B. et al. Remodeling of the chromatin structure of the facioscapulohumeral muscular dystrophy (FSHD) locus and upregulation of FSHD-related gene 1 (FRG1) expression during human myogenic differentiation. BMC Biol. 7, 41 (2009).
Google Scholar
Klooster, R. et al. Comprehensive expression analysis of FSHD candidate genes at the mRNA and protein level. Eur. J. Hum. Genet. 17, 1615–1624 (2009).
Google Scholar
Jiang, G. et al. Testing the position-effect variegation hypothesis for facioscapulohumeral muscular dystrophy by analysis of histone modification and gene expression in subtelomeric 4q. Hum. Mol. Genet. 12, 2909–2921 (2003).
Google Scholar
Cheli, S. et al. Expression profiling of FSHD-1 and FSHD-2 cells during myogenic differentiation evidences common and distinctive gene dysregulation patterns. PLoS ONE 6, e20966 (2011).
Google Scholar
Thijssen, P. E. et al. DUX4 promotes transcription of FRG2 by directly activating its promoter in facioscapulohumeral muscular dystrophy. Skelet. Muscle 4, 19 (2014).
Google Scholar
Ferri, G., Huichalaf, C. H., Caccia, R. & Gabellini, D. Direct interplay between two candidate genes in FSHD muscular dystrophy. Hum. Mol. Genet. 24, 1256–1266 (2015).
Google Scholar
Lemmers, R. et al. Chromosome 10q-linked FSHD identifies DUX4 as principal disease gene. J. Med. Genet. 59, 180–188 (2021).
Google Scholar
Gabriels, J. et al. Nucleotide sequence of the partially deleted D4Z4 locus in a patient with FSHD identifies a putative gene within each 3.3 kb element. Gene 236, 25–32 (1999).
Google Scholar
van Geel, M. et al. Genomic analysis of human chromosome 10q and 4q telomeres suggests a common origin. Genomics 79, 210–217 (2002).
Google Scholar
Lemmers, R. J. et al. Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere. Nat. Genet. 32, 235–236 (2002).
Google Scholar
Lemmers, R. J. et al. Contractions of D4Z4 on 4qB subtelomeres do not cause facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 75, 1124–1130 (2004).
Google Scholar
Dixit, M. et al. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc. Natl Acad. Sci. USA 104, 18157–18162 (2007).
Google Scholar
Snider, L. et al. RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum. Mol. Genet. 18, 2414–2430 (2009).
Google Scholar
Bakker, E. et al. The FSHD-linked locus D4F104S1 (p13E-11) on 4q35 has a homologue on 10qter. Muscle Nerve. 2, S39–S44 (1995).
Google Scholar
Deidda, G. et al. Physical mapping evidence for a duplicated region on chromosome 10qter showing high homology with the facioscapulohumeral muscular dystrophy locus on chromosome 4qter. Eur. J. Hum. Genet. 3, 155–167 (1995).
Google Scholar
Lemmers, R. J. et al. Worldwide population analysis of the 4q and 10q subtelomeres identifies only four discrete interchromosomal sequence transfers in human evolution. Am. J. Hum. Genet. 86, 364–377 (2010).
Google Scholar
Jones, T. I. et al. Facioscapulohumeral muscular dystrophy family studies of DUX4 expression: evidence for disease modifiers and a quantitative model of pathogenesis. Hum. Mol. Genet. 21, 4419–4430 (2012).
Google Scholar
Snider, L. et al. Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet. 6, e1001181 (2010).
Google Scholar
Huichalaf, C., Micheloni, S., Ferri, G., Caccia, R. & Gabellini, D. DNA methylation analysis of the macrosatellite repeat associated with FSHD muscular dystrophy at single nucleotide level. PLoS ONE 9, e115278 (2014).
Google Scholar
Das, S. & Chadwick, B. P. Influence of repressive histone and DNA methylation upon D4Z4 transcription in non-myogenic cells. PLoS ONE 11, e0160022 (2016).
Google Scholar
Zeng, W. et al. Specific loss of histone H3 lysine 9 trimethylation and HP1γ/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 5, e1000559 (2009).
Google Scholar
Boros, J., Arnoult, N., Stroobant, V., Collet, J. F. & Decottignies, A. Polycomb repressive complex 2 and H3K27me3 cooperate with H3K9 methylation to maintain heterochromatin protein 1α at chromatin. Mol. Cell Biol. 34, 3662–3674 (2014).
Google Scholar
Chen, K. et al. Genome-wide binding and mechanistic analyses of Smchd1-mediated epigenetic regulation. Proc. Natl Acad. Sci. USA 112, E3535–E3544 (2015).
Google Scholar
Campbell, A. E. et al. NuRD and CAF-1-mediated silencing of the D4Z4 array is modulated by DUX4-induced MBD3L proteins. eLife 7, e31023 (2018).
Google Scholar
Casa, V. et al. Polycomb repressive complex 1 provides a molecular explanation for repeat copy number dependency in FSHD muscular dystrophy. Hum. Mol. Genet. 26, 753–767 (2017).
Google Scholar
Haynes, P., Bomsztyk, K. & Miller, D. G. Sporadic DUX4 expression in FSHD myocytes is associated with incomplete repression by the PRC2 complex and gain of H3K9 acetylation on the contracted D4Z4 allele. Epigenet. Chromatin 11, 47 (2018).
Google Scholar
Sacconi, S. et al. FSHD1 and FSHD2 form a disease continuum. Neurology 92, e2273–e2285 (2019).
Google Scholar
van Overveld, P. G. et al. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat. Genet. 35, 315–317 (2003).
Google Scholar
Calandra, P. et al. Allele-specific DNA hypomethylation characterises FSHD1 and FSHD2. J. Med. Genet. 53, 348–355 (2016).
Google Scholar
Rieken, A., Bossler, A. D., Mathews, K. D. & Moore, S. A. CLIA Laboratory testing for facioscapulohumeral dystrophy: a retrospective analysis. Neurology 96, e1054–e1062 (2021).
Google Scholar
Lemmers, R. J. et al. Hemizygosity for SMCHD1 in facioscapulohumeral muscular dystrophy type 2: consequences for 18p deletion syndrome. Hum. Mutat. 36, 679–683 (2015).
Google Scholar
van den Boogaard, M. L. et al. Mutations in DNMT3B modify epigenetic repression of the D4Z4 repeat and the penetrance of facioscapulohumeral dystrophy. Am. J. Hum. Genet. 98, 1020–1029 (2016).
Google Scholar
Hamanaka, K. et al. Homozygous nonsense variant in LRIF1 associated with facioscapulohumeral muscular dystrophy. Neurology 94, e2441–e2447 (2020).
Google Scholar
Sacconi, S. et al. The FSHD2 gene SMCHD1 is a modifier of disease severity in families affected by FSHD1. Am. J. Hum. Genet. 93, 744–751 (2013).
Google Scholar
van Deutekom, J. C. et al. Evidence for subtelomeric exchange of 3.3 kb tandemly repeated units between chromosomes 4q35 and 10q26: implications for genetic counselling and etiology of FSHD1. Hum. Mol. Genet. 5, 1997–2003 (1996).
Google Scholar
Nguyen, K. et al. Deciphering the complexity of the 4q and 10q subtelomeres by molecular combing in healthy individuals and patients with facioscapulohumeral dystrophy. J. Med. Genet. 56, 590–601 (2019).
Google Scholar
Goossens, R. et al. Intronic SMCHD1 variants in FSHD: testing the potential for CRISPR-Cas9 genome editing. J. Med. Genet. 56, 828–837 (2019).
Google Scholar
Lemmers, R. J. L. F. et al. Cis D4Z4 repeat duplications associated with facioscapulohumeral muscular dystrophy type 2. Hum. Mol. Genet. 27, 3488–3497 (2018).
Google Scholar
Lemmers, R. et al. High-resolution breakpoint junction mapping of proximally extended D4Z4 deletions in FSHD1 reveals evidence for a founder effect. Hum. Mol. Genet. 31, 748–760 (2022).
Google Scholar
Lemmers, R. J. et al. D4F104S1 deletion in facioscapulohumeral muscular dystrophy: phenotype, size, and detection. Neurology 61, 178–183 (2003).
Google Scholar
van den Boogaard, M. L. et al. Double SMCHD1 variants in FSHD2: the synergistic effect of two SMCHD1 variants on D4Z4 hypomethylation and disease penetrance in FSHD2. Eur. J. Hum. Genet. 24, 78–85 (2016).
Google Scholar
Mocciaro, E., Runfola, V., Ghezzi, P., Pannese, M. & Gabellini, D. DUX4 role in normal physiology and in FSHD muscular dystrophy. Cells https://doi.org/10.3390/cells10123322 (2021).
Google Scholar
Geng, L. N. et al. DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev. Cell 22, 38–51 (2012).
Google Scholar
Hendrickson, P. G. et al. Conserved roles of mouse DUX and human DUX4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons. Nat. Genet. 49, 925–934 (2017).
Google Scholar
De Iaco, A. et al. DUX-family transcription factors regulate zygotic genome activation in placental mammals. Nat. Genet. 49, 941–994 (2017).
Google Scholar
Choi, S. H. et al. DUX4 recruits p300/CBP through its C-terminus and induces global H3K27 acetylation changes. Nucleic Acids Res. 44, 5161–5173 (2016).
Google Scholar
Resnick, R. et al. DUX4-induced histone variants H3.X and H3.Y mark DUX4 target genes for expression. Cell Rep. 29, 1812–1820.e5 (2019).
Google Scholar
Gannon, O. M., Merida de Long, L. & Saunders, N. A. DUX4 is derepressed in late-differentiating keratinocytes in conjunction with loss of H3K9me3 epigenetic repression. J. Invest. Dermatol. 136, 1299–1302 (2016).
Google Scholar
Kowaljow, V. et al. The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul. Disord. 17, 611–623 (2007).
Google Scholar
Knopp, P. et al. DUX4 induces a transcriptome more characteristic of a less-differentiated cell state and inhibits myogenesis. J. Cell Sci. 129, 3816–3831 (2016).
Google Scholar
Wallace, L. M. et al. DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann. Neurol. 69, 540–552 (2011).
Google Scholar
Lek, A. et al. Applying genome-wide CRISPR–Cas9 screens for therapeutic discovery in facioscapulohumeral muscular dystrophy. Sci. Transl. Med. https://doi.org/10.1126/scitranslmed.aay0271 (2020).
Google Scholar
Bosnakovski, D. et al. p53-independent DUX4 pathology in cell and animal models of facioscapulohumeral muscular dystrophy. Dis. Model. Mech. 10, 1211–1216 (2017).
Google Scholar
Shadle, S. C. et al. DUX4-induced dsRNA and MYC mRNA stabilization activate apoptotic pathways in human cell models of facioscapulohumeral dystrophy. PLoS Genet. 13, e1006658 (2017).
Google Scholar
Grow, E. J. et al. p53 convergently activates Dux/DUX4 in embryonic stem cells and in facioscapulohumeral muscular dystrophy cell models. Nat. Genet. 53, 1207–1220 (2021).
Google Scholar
Vogelstein, B., Lane, D. & Levine, A. J. Surfing the p53 network. Nature 408, 307–310 (2000).
Google Scholar
Winokur, S. T. et al. Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum. Mol. Genet. 12, 2895–2907 (2003).
Google Scholar
Sasaki-Honda, M. et al. A patient-derived iPSC model revealed oxidative stress increases facioscapulohumeral muscular dystrophy-causative DUX4. Hum. Mol. Genet. 27, 4024–4035 (2018).
Google Scholar
Tsumagari, K. et al. Gene expression during normal and FSHD myogenesis. BMC Med. Genom. 4, 67 (2011).
Google Scholar
Jagannathan, S., Ogata, Y., Gafken, P. R., Tapscott, S. J. & Bradley, R. K. Quantitative proteomics reveals key roles for post-transcriptional gene regulation in the molecular pathology of facioscapulohumeral muscular dystrophy. eLife 8, e41740 (2019).
Google Scholar
Beermann, M. L., Homma, S. & Miller, J. B. Proximity ligation assay to detect DUX4 protein in FSHD1 muscle: a pilot study. BMC Res. Notes 15, 163 (2022).
Google Scholar
Tassin, A. et al. DUX4 expression in FSHD muscle cells: how could such a rare protein cause a myopathy. J. Cell. Mol. Med. 17, 76–89 (2013).
Google Scholar
Rickard, A. M., Petek, L. M. & Miller, D. G. Endogenous DUX4 expression in FSHD myotubes is sufficient to cause cell death and disrupts RNA splicing and cell migration pathways. Hum. Mol. Genet. 24, 5901–5914 (2015).
Google Scholar
Yao, Z. et al. DUX4-induced gene expression is the major molecular signature in FSHD skeletal muscle. Hum. Mol. Genet. 23, 5342–5352 (2014).
Google Scholar
Jagannathan, S. et al. Model systems of DUX4 expression recapitulate the transcriptional profile of FSHD cells. Hum. Mol. Genet. 25, 4419–4431 (2016).
Google Scholar
Heuvel, A. V. D. et al. Single-cell RNA-sequencing in facioscapulohumeral muscular dystrophy disease etiology and development. Hum. Mol. Genet. 28, 1064–1075 (2018).
Google Scholar
Jiang, S. et al. Single-nucleus RNA-seq identifies divergent populations of FSHD2 myotube nuclei. PLoS Genet 16, e1008754 (2020).
Google Scholar
Nikolic, A. et al. Clinical expression of facioscapulohumeral muscular dystrophy in carriers of 1-3 D4Z4 reduced alleles: experience of the FSHD Italian National Registry. BMJ Open 6, e007798 (2016).
Google Scholar
Statland, J. M. et al. Milder phenotype in facioscapulohumeral dystrophy with 7–10 residual D4Z4 repeats. Neurology 85, 2147–2150 (2015).
Google Scholar
Lemmers, R. J. et al. Inter-individual differences in CpG methylation at D4Z4 correlate with clinical variability in FSHD1 and FSHD2. Hum. Mol. Genet. 24, 659–669 (2014).
Google Scholar
Scionti, I. et al. Large-scale population analysis challenges the current criteria for the molecular diagnosis of fascioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 90, 628–635 (2012).
Google Scholar
Lemmers, R. J. et al. Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 81, 884–894 (2007).
Google Scholar
Nikolic, A. et al. Interpretation of the epigenetic signature of facioscapulohumeral muscular dystrophy in light of genotype–phenotype studies. Int. J. Mol. Sci. 21, 2635 (2020).
Google Scholar
Salsi, V., Magdinier, F. & Tupler, R. Does DNA methylation matter in FSHD. Genes 11, 258 (2020).
Google Scholar
van Overveld, P. G. et al. Variable hypomethylation of D4Z4 in facioscapulohumeral muscular dystrophy. Ann. Neurol. 58, 569–576 (2005).
Google Scholar
de Greef, J. C. et al. Hypomethylation is restricted to the D4Z4 repeat array in phenotypic FSHD. Neurology 69, 1018–1026 (2007).
Google Scholar
de Greef, J. C. et al. Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum. Mutat. 30, 1449–1459 (2009).
Google Scholar
Gaillard, M. C. et al. Differential DNA methylation of the D4Z4 repeat in patients with FSHD and asymptomatic carriers. Neurology 83, 733–742 (2014).
Google Scholar
Larsen, M. et al. Diagnostic approach for FSHD revisited: SMCHD1 mutations cause FSHD2 and act as modifiers of disease severity in FSHD1. Eur. J. Hum. Genet. 23, 808–816 (2014).
Google Scholar
Jones, T. I. et al. Individual epigenetic status of the pathogenic D4Z4 macrosatellite correlates with disease in facioscapulohumeral muscular dystrophy. Clin. Epigenet. 7, 37 (2015).
Google Scholar
Roche, S. et al. Methylation hotspots evidenced by deep sequencing in patients with facioscapulohumeral dystrophy and mosaicism. Neurol. Genet. 5, e372–e372 (2019).
Google Scholar
Jones, T. I. et al. Identifying diagnostic DNA methylation profiles for facioscapulohumeral muscular dystrophy in blood and saliva using bisulfite sequencing. Clin. Epigenet. 6, 23 (2014).
Google Scholar
Erdmann, H. et al. Methylation of the 4q35 D4Z4 repeat defines disease status in facioscapulohumeral muscular dystrophy. Brain https://doi.org/10.1093/brain/awac336 (2022).
Google Scholar
Mason, A. G. et al. SMCHD1 regulates a limited set of gene clusters on autosomal chromosomes. Skelet. Muscle 7, 12 (2017).
Google Scholar
Hartweck, L. M. et al. A focal domain of extreme demethylation within D4Z4 in FSHD2. Neurology 80, 392–399 (2013).
Google Scholar
Lemmers, R. J. L. F. et al. Inter-individual differences in CpG methylation at D4Z4 correlate with clinical variability in FSHD1 and FSHD2. Hum. Mol. Genet. 24, 659–669 (2015).
Google Scholar
Balog, J. et al. Increased DUX4 expression during muscle differentiation correlates with decreased SMCHD1 protein levels at D4Z4. Epigenetics 10, 1133–1142 (2015).
Google Scholar
Balog, J. et al. Monosomy 18p is a risk factor for facioscapulohumeral dystrophy. J. Med. Genet. 55, 469–478 (2018).
Google Scholar
Gordon, C. T. et al. De novo mutations in SMCHD1 cause bosma arhinia microphthalmia syndrome and abrogate nasal development. Nat. Genet. 49, 249–255 (2017).
Google Scholar
Shaw, N. D. et al. SMCHD1 mutations associated with a rare muscular dystrophy can also cause isolated arhinia and bosma arhinia microphthalmia syndrome. Nat. Genet. 49, 238–248 (2017).
Google Scholar
Kinjo, K. et al. Rare variant of the epigenetic regulator SMCHD1 in a patient with pituitary hormone deficiency. Sci. Rep. 10, 10985 (2020).
Google Scholar
Lemmers, R. J. L. F. et al. SMCHD1 mutation spectrum for facioscapulohumeral muscular dystrophy type 2 (FSHD2) and bosma arhinia microphthalmia syndrome (BAMS) reveals disease-specific localisation of variants in the ATPase domain. J. Med. Genet. 56, 693–700 (2019).
Google Scholar
Gurzau, A. D. et al. FSHD2- and BAMS-associated mutations confer opposing effects on SMCHD1 function. J. Biol. Chem. 293, 9841–9853 (2018).
Google Scholar
Dion, C. et al. SMCHD1 is involved in de novo methylation of the DUX4-encoding D4Z4 macrosatellite. Nucleic Acids Res 47, 2822–2839 (2019).
Google Scholar
Mul, K. et al. FSHD type 2 and bosma arhinia microphthalmia syndrome: two faces of the same mutation. Neurology 91, e562–e570 (2018).
Google Scholar
Mohassel, P. et al. Cross-sectional neuromuscular phenotyping study of patients with arhinia with SMCHD1 variants. Neurology 98, e1384–e1396 (2022).
Google Scholar
Hansen, R. S. et al. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl Acad. Sci. USA 96, 14412–14417 (1999).
Google Scholar
Xu, G. L. et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187–191 (1999).
Google Scholar
Gendrel, A. V. et al. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev. Cell 23, 265–279 (2012).
Google Scholar
Thijssen, P. E. et al. Mutations in CDCA7 and HELLS cause immunodeficiency-centromeric instability-facial anomalies syndrome. Nat. Commun. 6, 7870 (2015).
Google Scholar
Jeanpierre, M. et al. An embryonic-like methylation pattern of classical satellite DNA is observed in ICF syndrome. Hum. Mol. Genet. 2, 731–735 (1993).
Google Scholar
Kondo, T. et al. Whole-genome methylation scan in ICF syndrome: hypomethylation of non-satellite DNA repeats D4Z4 and NBL2. Hum. Mol. Genet. 9, 597–604 (2000).
Google Scholar
Nozawa, R. S. et al. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1–HBiX1 pathway. Nat. Struct. Mol. Biol. 20, 566–573 (2013).
Google Scholar
Brideau, N. J. et al. Independent mechanisms target SMCHD1 to H3K9me3-modified chromatin and the inactive X chromosome. Mol. Cell Biol. 35, 4053–4068 (2015).
Google Scholar
Balog, J. et al. Correlation analysis of clinical parameters with epigenetic modifications in the DUX4 promoter in FSHD. Epigenetics 7, 579–584 (2012).
Google Scholar
Cabianca, D. S. et al. A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149, 819–831 (2012).
Google Scholar
Himeda, C. L. et al. Identification of epigenetic regulators of DUX4-fl for targeted therapy of facioscapulohumeral muscular dystrophy. Mol. Ther. 26, 1797–1807 (2018).
Google Scholar
Olsen, D. B., Ørngreen, M. C. & Vissing, J. Aerobic training improves exercise performance in facioscapulohumeral muscular dystrophy. Neurology 64, 1064–1066 (2005).
Google Scholar
Janssen, B., Voet, N., Geurts, A., van Engelen, B. & Heerschap, A. Quantitative MRI reveals decelerated fatty infiltration in muscles of active FSHD patients. Neurology 86, 1700–1707 (2016).
Google Scholar
Wang, L. H. et al. MRI-informed muscle biopsies correlate MRI with pathology and DUX4 target gene expression in FSHD. Hum. Mol. Genet. 28, 476–486 (2019).
Google Scholar
Dahlqvist, J. R. et al. Evaluation of inflammatory lesions over 2 years in facioscapulohumeral muscular dystrophy. Neurology 95, e1211–e1221 (2020).
Google Scholar
van den Heuvel, A. et al. Facioscapulohumeral dystrophy transcriptome signatures correlate with different stages of disease and are marked by different MRI biomarkers. Sci. Rep. 12, 1426 (2022).
Google Scholar
Mul, K. et al. Quantitative muscle MRI and ultrasound for facioscapulohumeral muscular dystrophy: complementary imaging biomarkers. J. Neurol. 265, 2646–2655 (2018).
Google Scholar
Lassche, S. et al. Correlation between quantitative MRI and muscle histopathology in muscle biopsies from healthy controls and patients with IBM, FSHD and OPMD. J. Neuromuscul. Dis. 7, 495–504 (2020).
Google Scholar
Wong, C. J. et al. Longitudinal measures of RNA expression and disease activity in FSHD muscle biopsies. Hum. Mol. Genet. 29, 1030–1043 (2020).
Google Scholar
Andersen, G. et al. MRI as outcome measure in facioscapulohumeral muscular dystrophy: 1-year follow-up of 45 patients. J. Neurol. 264, 438–447 (2017).
Google Scholar
Fatehi, F. et al. Long-term follow-up of MRI changes in thigh muscles of patients with facioscapulohumeral dystrophy: a quantitative study. PLoS One 12, e0183825 (2017).
Google Scholar
Mul, K. et al. Adding quantitative muscle MRI to the FSHD clinical trial toolbox. Neurology 89, 2057–2065 (2017).
Google Scholar
Frisullo, G. et al. CD8+ T cells in facioscapulohumeral muscular dystrophy patients with inflammatory features at muscle MRI. J. Clin. Immunol. 31, 155–166 (2011).
Google Scholar
Tasca, G. et al. Different molecular signatures in magnetic resonance imaging-staged facioscapulohumeral muscular dystrophy muscles. PLoS ONE 7, e38779 (2012).
Google Scholar
Ferguson, M. R. et al. MRI change metrics of facioscapulohumeral muscular dystrophy: STIR and T1. Muscle Nerve 57, 905–912 (2018).
Google Scholar
Dahlqvist, J. R. et al. Relationship between muscle inflammation and fat replacement assessed by MRI in facioscapulohumeral muscular dystrophy. J. Neurol. 266, 1127–1135 (2019).
Google Scholar
Friedman, S. D. et al. Longitudinal features of STIR bright signal in FSHD. Muscle Nerve 49, 257–260 (2014).
Google Scholar
Janssen, B. H. et al. Distinct disease phases in muscles of facioscapulohumeral dystrophy patients identified by MR detected fat infiltration. PLoS ONE 9, e85416 (2014).
Google Scholar
Cohen, J., DeSimone, A., Lek, M. & Lek, A. Therapeutic approaches in facioscapulohumeral muscular dystrophy. Trends Mol. Med. 27, 123–137 (2020).
Google Scholar
Kissel, J. T. et al. Randomized, double-blind, placebo-controlled trial of albuterol in facioscapulohumeral dystrophy. Neurology 57, 1434–1440 (2001).
Google Scholar
van der Kooi, E. L. et al. Strength training and albuterol in facioscapulohumeral muscular dystrophy. Neurology 63, 702–708 (2004).
Google Scholar
Campbell, A. E. et al. BET bromodomain inhibitors and agonists of the β2 adrenergic receptor identified in screens for compounds that inhibit DUX4 expression in FSHD muscle cells. Skelet. Muscle 7, 16 (2017).
Google Scholar
Oliva, J. et al. Clinically advanced p38 inhibitors suppress DUX4 expression in cellular and animal models of facioscapulohumeral muscular dystrophy. J. Pharmacol. Exp. Ther. 370, 219–223 (2019).
Google Scholar
Rojas, L. A. et al. p38α regulates expression of DUX4 in a model of facioscapulohumeral muscular dystrophy. J. Pharmacol. Exp. Ther. 374, 489–498 (2020).
Google Scholar
Mellion, M. L. et al. Phase 1 clinical trial of losmapimod in facioscapulohumeral dystrophy: safety, tolerability, pharmacokinetics, and target engagement. Br. J. Clin. Pharmacol. 87, 4658–4669 (2021).
Google Scholar
Tawil, R. & Wagner, K. Clinical research: O.5 A phase 2, randomized, double-blind, placebo-controlled, 48-week study of the efficacy and safety of losmapimod in subjects with FSHD: ReDUX4. Neuromuscul. Disord. 31, S48–S49 (2021).
Google Scholar
Jagannathan, S. et al. Meeting report: the 2021 FSHD International Research Congress. Skelet. Muscle 12, 1 (2022).
Google Scholar
Wang, N., Wu, R., Tang, D. & Kang, R. The BET family in immunity and disease. Signal. Transduct. Target. Ther. 6, 23 (2021).
Google Scholar
Yang, H., Wei, L., Xun, Y., Yang, A. & You, H. BRD4: an emerging prospective therapeutic target in glioma. Mol. Ther. Oncolyt. 21, 1–14 (2021).
Google Scholar
Lim, J. W. et al. DICER/AGO-dependent epigenetic silencing of D4Z4 repeats enhanced by exogenous siRNA suggests mechanisms and therapies for FSHD. Hum. Mol. Genet. 24, 4817–4828 (2015).
Google Scholar
Saad, N. Y. et al. Human miRNA miR-675 inhibits DUX4 expression and may be exploited as a potential treatment for facioscapulohumeral muscular dystrophy. Nat. Commun. 12, 7128 (2021).
Google Scholar
Kuijper, E. C., Bergsma, A. J., Pijnappel, W. W. M. P. & Aartsma-Rus, A. Opportunities and challenges for antisense oligonucleotide therapies. J. Inherit. Metab. Dis. 44, 72–87 (2021).
Google Scholar
Marsollier, A. C. et al. Antisense targeting of 3ʹ end elements involved in DUX4 mRNA processing is an efficient therapeutic strategy for facioscapulohumeral dystrophy: a new gene-silencing approach. Hum. Mol. Genet. 25, 1468–1478 (2016).
Google Scholar
Chen, J. C. et al. Morpholino-mediated knockdown of DUX4 toward facioscapulohumeral muscular dystrophy therapeutics. Mol. Ther. 24, 1405–1411 (2016).
Google Scholar
Ansseau, E. et al. Antisense oligonucleotides used to target the DUX4 mRNA as therapeutic approaches in faciosscapulohumeral muscular dystrophy (FSHD). Genes 8, 93 (2017).
Google Scholar
Lu-Nguyen, N., Dickson, G., Malerba, A. & Popplewell, L. Long-term systemic treatment of a mouse model displaying chronic FSHD-like pathology with antisense therapeutics that inhibit DUX4 expression. Biomedicines 10, 1623 (2022).
Google Scholar
Lu-Nguyen, N., Malerba, A., Antoni Pineda, M., Dickson, G. & Popplewell, L. Improving molecular and histopathology in diaphragm muscle of the double transgenic ACTA1-MCM/FLExDUX4 mouse model of FSHD with systemic antisense therapy. Hum. Gene Ther. 33, 923–935 (2022).
Google Scholar
Lu-Nguyen, N., Malerba, A., Herath, S., Dickson, G. & Popplewell, L. Systemic antisense therapeutics inhibiting DUX4 expression ameliorates FSHD-like pathology in an FSHD mouse model. Hum. Mol. Genet. 30, 1398–1412 (2021).
Google Scholar
Bouwman, L. F. et al. Systemic delivery of a DUX4-targeting antisense oligonucleotide to treat facioscapulohumeral muscular dystrophy. Mol. Ther. Nucleic Acids 26, 813–827 (2021).
Google Scholar
George, L. A. et al. Long-term follow-up of the first in human intravascular delivery of AAV for gene transfer: AAV2-hFIX16 for severe hemophilia B. Mol. Ther. 28, 2073–2082 (2020).
Google Scholar
Wallace, L. M. et al. RNA interference inhibits DUX4-induced muscle toxicity in vivo: implications for a targeted FSHD therapy. Mol. Ther. 20, 1417–1423 (2012).
Google Scholar
Wallace, L. M. et al. Pre-clinical safety and off-target studies to support translation of AAV-mediated RNAi therapy for FSHD. Mol. Ther. Methods Clin. Dev. 8, 121–130 (2018).
Google Scholar
Rashnonejad, A., Amini-Chermahini, G., Taylor, N. K., Wein, N. & Harper, S. Q. Designed U7 snRNAs inhibit DUX4 expression and improve FSHD-associated outcomes in DUX4 overexpressing cells and FSHD patient myotubes. Mol. Ther. Nucleic Acids 23, 476–486 (2021).
Google Scholar
Bosnakovski, D. et al. A novel P300 inhibitor reverses DUX4-mediated global histone H3 hyperacetylation, target gene expression, and cell death. Sci. Adv. 5, eaaw7781 (2019).
Google Scholar
Mariot, V. et al. A deoxyribonucleic acid decoy trapping DUX4 for the treatment of facioscapulohumeral muscular dystrophy. Mol. Ther. Nucleic Acids 22, 1191–1199 (2020).
Google Scholar
Klingler, C. et al. DNA aptamers against the DUX4 protein reveal novel therapeutic implications for FSHD. FASEB J. https://doi.org/10.1096/fj.201902696 (2020).
Google Scholar
Ran, F. A. et al. Genome engineering using the CRISPR–Cas9 system. Nat. Protoc. 8, 2281–2308 (2013).
Google Scholar
Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819–823 (2013).
Google Scholar
Richardson, C. D., Ray, G. J., DeWitt, M. A., Curie, G. L. & Corn, J. E. Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol. 34, 339–344 (2016).
Google Scholar
Larson, M. H. et al. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8, 2180–2196 (2013).
Google Scholar
Himeda, C. L., Jones, T. I. & Jones, P. L. CRISPR/dCas9-mediated transcriptional inhibition ameliorates the epigenetic dysregulation at D4Z4 and represses DUX4-fl in FSH muscular dystrophy. Mol. Ther. 24, 527–535 (2016).
Google Scholar
Joubert, R., Mariot, V., Charpentier, M., Concordet, J. P. & Dumonceaux, J. Gene editing targeting the DUX4 polyadenylation signal: a therapy for FSHD? J. Pers. Med. https://doi.org/10.3390/jpm11010007 (2020).
Google Scholar
Das, S. & Chadwick, B. P. CRISPR mediated targeting of DUX4 distal regulatory element represses DUX4 target genes dysregulated in facioscapulohumeral muscular dystrophy. Sci. Rep. 11, 12598 (2021).
Google Scholar
Gaudelli, N. M. et al. Programmable base editing of A*T to G*C in genomic DNA without DNA cleavage. Nature 551, 464–471 (2017).
Google Scholar
Komor, A. C., Kim, Y. B., Packer, M. S., Zuris, J. A. & Liu, D. R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533, 420–424 (2016).
Google Scholar
Ran, F. A. et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380–1389 (2013).
Google Scholar
Šikrová, D. et al. Adenine base editing of the DUX4 polyadenylation signal for targeted genetic therapy in facioscapulohumeral muscular dystrophy. Mol. Ther. Nucleic Acids 25, 342–354 (2021).
Google Scholar
Himeda, C. L., Jones, T. I. & Jones, P. L. Targeted epigenetic repression by CRISPR/dSaCas9 suppresses pathogenic DUX4-fl expression in FSHD. Mol. Ther. Methods Clin. Dev. 20, 298–311 (2021).
Google Scholar
Tawil, R., Shaw, D. W., van der Maarel, S. M. & Tapscott, S. J. Clinical trial preparedness in facioscapulohumeral dystrophy: outcome measures and patient access: 8–9 April 2013, Leiden, The Netherlands. Neuromuscul. Disord. 24, 79–85 (2014).
Google Scholar
The FSH-DY group. A prospective, quantitative study of the natural history of facioscapulohumeral muscular dystrophy (FSHD): implications for therapeutic trials. Neurology 48, 38–46 (1997).
Google Scholar
Kinoshita, J., Magdinier, F. & Padberg, G. W. 26th Annual Facioscapulohumeral Dystrophy International Research Congress Marseille, France, 19–20 June 2019. Neuromuscul. Disord. 29, 811–817 (2019).
Google Scholar
Mul, K. et al. 225th ENMC international workshop: a global FSHD registry framework, 18–20 November 2016, Heemskerk, The Netherlands. Neuromuscul. Disord. 27, 782–790 (2017).
Google Scholar
Tassin, A. et al. FSHD myotubes with different phenotypes exhibit distinct proteomes. PLoS ONE 7, e51865 (2012).
Google Scholar
Jones, T. I. et al. Transgenic mice expressing tunable levels of DUX4 develop characteristic facioscapulohumeral muscular dystrophy-like pathophysiology ranging in severity. Skelet. Muscle 10, 8 (2020).
Google Scholar
Jones, T. & Jones, P. L. A cre-inducible DUX4 transgenic mouse model for investigating facioscapulohumeral muscular dystrophy. PLoS One 13, e0192657 (2018).
Google Scholar
Banerji, C. R. S. et al. PAX7 target genes are globally repressed in facioscapulohumeral muscular dystrophy skeletal muscle. Nat. Commun. 8, 2152 (2017).
Google Scholar
Bosnakovski, D. et al. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J. 27, 2766–2779 (2008).
Google Scholar
Banerji, C. R. S. & Zammit, P. S. PAX7 target gene repression is a superior FSHD biomarker than DUX4 target gene activation, associating with pathological severity and identifying FSHD at the single-cell level. Hum. Mol. Genet. 28, 2224–2236 (2019).
Google Scholar
Banerji, C. R. S. PAX7 target gene repression associates with FSHD progression and pathology over one year. Hum. Mol. Genet. 29, 2124–2133 (2020).
Google Scholar
Petek, L. M. et al.A cross sectional study of two independent cohorts identifies serum biomarkers for facioscapulohumeral muscular dystrophy (FSHD). Neuromuscul. Disord. 26, 405–413 (2016).
Google Scholar
Statland, J., Donlin-Smith, C. M., Tapscott, S. J., van der Maarel, S. & Tawil, R. Multiplex screen of serum biomarkers in facioscapulohumeral muscular dystrophy. J. Neuromuscul. Dis. 1, 181–190 (2014).
Google Scholar
Signorelli, M. et al. Evaluation of blood gene expression levels in facioscapulohumeral muscular dystrophy patients. Sci. Rep. 10, 17547 (2020).
Google Scholar
Heier, C. R. et al. Multi-omics identifies circulating miRNA and protein biomarkers for facioscapulohumeral dystrophy. J. Pers. Med. 10, 236 (2020).
Google Scholar
Corasolla Carregari, V. et al. Proteomics of muscle microdialysates identifies potential circulating biomarkers in facioscapulohumeral muscular dystrophy. Int. J. Mol. Sci. 22, 290 (2020).
Google Scholar
Gros, M. et al. Identification of serum interleukin 6 levels as a disease severity biomarker in facioscapulohumeral muscular dystrophy. J. Neuromuscul. Dis. 9, 83–93 (2022).
Google Scholar
Wong, C. J. et al. Elevated plasma complement components in facioscapulohumeral dystrophy. Hum. Mol. Genet. 31, 1821–1829 (2022).
Google Scholar
Nunes, A. M., Ramirez, M., Jones, T. I. & Jones, P. L. Identification of candidate miRNA biomarkers for facioscapulohumeral muscular dystrophy using DUX4-based mouse models. Dis. Model. Mech. 14, dmm049016 (2021).
Google Scholar
Tasca, G. et al. Magnetic resonance imaging in a large cohort of facioscapulohumeral muscular dystrophy patients: pattern refinement and implications for clinical trials. Ann. Neurol. 79, 854–864 (2016).
Google Scholar
Regula, J. U. et al. Clinical muscle testing compared with whole-body magnetic resonance imaging in facio-scapulo-humeral muscular dystrophy. Clin. Neuroradiol. 26, 445–455 (2016).
Google Scholar
Olsen, D. B., Gideon, P., Jeppesen, T. D. & Vissing, J. Leg muscle involvement in facioscapulohumeral muscular dystrophy assessed by MRI. J. Neurol. 253, 1437–1441 (2006).
Google Scholar
Leung, D. G., Carrino, J. A., Wagner, K. R. & Jacobs, M. A. Whole-body magnetic resonance imaging evaluation of facioscapulohumeral muscular dystrophy. Muscle Nerve 52, 512–520 (2015).
Google Scholar
Lareau-Trudel, E. et al. Muscle quantitative MR imaging and clustering analysis in patients with facioscapulohumeral muscular dystrophy type 1. PLoS ONE 10, e0132717 (2015).
Google Scholar
Dahlqvist, J. R., Vissing, C. R., Thomsen, C. & Vissing, J. Severe paraspinal muscle involvement in facioscapulohumeral muscular dystrophy. Neurology 83, 1178–1183 (2014).
Google Scholar
Goselink, R. J. M. et al. Muscle ultrasound is a responsive biomarker in facioscapulohumeral dystrophy. Neurology 94, e1488–e1494 (2020).
Google Scholar
Vera, K. A., McConville, M., Kyba, M. & Keller-Ross, M. L. Sarcopenic obesity in facioscapulohumeral muscular dystrophy. Front. Physiol. 11, 1008 (2020).
Google Scholar
U.S. Food and Drug Administration. Guidance document: patient-reported outcome measures: use in medical product development to support labeling claims. Guidance for Industry (docket number FDA-2006-D-0362). https://www.fda.gov/regulatory-information/search-fda-guidance-documents/patient-reported-outcome-measures-use-medical-product-development-support-labeling-claims (2009).
European Medicines Agency. Appendix 2 to the guideline on the evaluation of anticancer medicinal products in man. The use of patient-reported outcome (PRO) measures in oncology studies (EMA/CHMP/292464/2014). https://www.ema.europa.eu/en/documents/other/appendix-2-guideline-evaluation-anticancer-medicinal-products-man_en.pdf (2016).
Mul, K., Horlings, C. G. C., Faber, C. G., van Engelen, B. G. M. & Merkies, I. S. J. Rasch analysis to evaluate the motor function measure for patients with facioscapulohumeral muscular dystrophy. Int. J. Rehabil. Res. 44, 38–44 (2020).
Google Scholar
Eichinger, K. et al. Facioscapulohumeral muscular dystrophy functional composite outcome measure. Muscle Nerve 58, 72–78 (2018).
Google Scholar
Han, J. J. et al. Reachable workspace reflects dynamometer-measured upper extremity strength in facioscapulohumeral muscular dystrophy. Muscle Nerve 52, 948–955 (2015).
Google Scholar
Hatch, M. N. et al. Longitudinal study of upper extremity reachable workspace in fascioscapulohumeral muscular dystrophy. Neuromuscul. Disord. 29, 503–513 (2019).
Google Scholar
Hatch, M. N., Kurillo, G., Chan, V. & Han, J. J. Motion sensor-acquired reachable workspace correlates with patient-reported upper extremity activities of daily living (ADL) function in facioscapulohumeral dystrophy. Muscle Nerve 63, 250–257 (2021).
Google Scholar
Hamel, J. et al. Patient-reported symptoms in facioscapulohumeral muscular dystrophy (PRISM-FSHD). Neurology 93, e1180–e1192 (2019).
Google Scholar