Double SMCHD1 variants in FSHD2: The synergistic effect of two SMCHD1 variants on D4Z4 hypomethylation and disease penetrance in FSHD2

European Journal of Human Genetics

Volumn 24, Issue 1, 2016, Pages 78-85

  Van Den Boogaard, Marlinde L ^a   Lemmers, Richard J F L ^a   Camaño, Pilar ^b   Van Der Vliet, Patrick J ^a   Voermans, Nicol ^c   Van Engelen, Baziel G M ^c   Lopez De Munain, Adolfo ^b   Tapscott, Stephen J ^d   Van Der Stoep, Nienke ^a   Tawil, Rabi ^e   Van Der Maarel, Silvère M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d USA   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN; CHROMOSOME 4; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EXON; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY 2; FAMILY; FEMALE; GENE; GENE FUNCTION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; MALE; MISSENSE MUTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SMCHD1 GENE; X CHROMOSOME INACTIVATION; CHEMISTRY; CLASSIFICATION; DISEASE COURSE; GENE EXPRESSION; GENE LOCUS; GENETICS; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; ONSET AGE; PATHOLOGY; PEDIGREE; PENETRANCE; SKELETAL MUSCLE;

CHROMATIN; DUX4 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; NONHISTONE PROTEIN; SMCHD1 PROTEIN, HUMAN;

ADULT; AGE OF ONSET; AGED; BASE SEQUENCE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN, PAIR 4; DISEASE PROGRESSION; DNA METHYLATION; EXONS; FEMALE; GENE EXPRESSION; GENETIC LOCI; HOMEODOMAIN PROTEINS; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; MUTATION; PEDIGREE; PENETRANCE; PHENOTYPE;

EID: 84951573807     PISSN: 10184813     EISSN: 14765438     Source Type: Journal    
DOI: 10.1038/ejhg.2015.55     Document Type: Article

References (38)

1. Deenen JC, Arnts H, Van Der Maarel SM et al. Population-based incidence and prevalence of facioscapulohumeral dystrophy. Neurology 2014; 83: 1056-1059
2. Padberg GW, Lunt PW, Koch M, Fardeau M. Diagnostic criteria for facioscapulohumeral muscular dystrophy. Neuromuscul Disord 1991; 1: 231-234
3. Statland JM, Tawil R. Facioscapulohumeral muscular dystrophy: molecular pathological advances and future directions. Curr Opin Neurol 2011; 24: 423-428
4. De Greef JC, Lemmers RJ, Camano P et al. Clinical features of facioscapulohumeral muscular dystrophy 2. Neurology 2010; 75: 1548-1554
5. Van Overveld PG, Lemmers RJ, Sandkuijl La et al. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet 2003; 35: 315-317
6. Zeng W, De Greef JC, Chen YY et al. Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 2009; 5: e1000559
7. Snider L, Geng LN, Lemmers RJ et al. Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet 2010; 6: e1001181
8. Lemmers RJ, Van Der Vliet PJ, Klooster R et al. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 2010; 329: 1650-1653
9. Balog J, Thijssen PE, De Greef JC et al. Correlation analysis of clinical parameters with epigenetic modifications in the DUX4 promoter in FSHD. Epigenetics 2012; 7: 579-584
10. Bosnakovski D, Xu Z, Gang EJ et al. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 2008; 27: 2766-2779
11. Kowaljow V, Marcowycz A, Ansseau E et al. The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul Disord 2007; 17: 611-623
12. Geng LN, Yao Z, Snider L et al. DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 2012; 22: 38-51
13. Lemmers RJ, De Kievit P, Sandkuijl L et al. Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere. Nat Genet 2002; 32: 235-236
14. Lemmers RJ, Tawil R, Petek LM et al. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat Genet 2012; 44: 1370-1374
15. Van Deutekom JC, Wijmenga C, Van Tienhoven EA et al. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum Mol Genet 1993; 2: 2037-2042
16. Wijmenga C, Hewitt JE, Sandkuijl La et al. Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 1992; 2: 26-30
17. Hirano T. SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 2005; 360: 507-514
18. Hirano T. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 2006; 7: 311-322
19. Ball ARJr., Chen YY, Yokomori K. Mechanisms of cohesin-mediated gene regulation and lessons learned from cohesinopathies. Biochim Biophys Acta 2014; 1839: 191-202
20. Sacconi S, Lemmers RJ, Balog J et al. The FSHD2 gene SMCHD1 is a modifier of disease severity in families affected by FSHD1. Am J Hum Genet 2013; 93: 744-751
21. Lemmers RJ, Goeman JJ, Van Der Vliet PJ et al. Inter-individual differences in CpG methylation at D4Z4 correlate with clinical variability in FSHD1 and FSHD2. Hum Mol Genet 2015; 24: 659-669
22. Mitsuhashi S, Boyden SE, Estrella EA et al. Exome sequencing identifies a novel SMCHD1 mutation in facioscapulohumeral muscular dystrophy 2. Neuromuscul Disord 2013; 23: 975-980
23. Winston J, Duerden L, Mort M, Frayling IM, Rogers MT, Upadhyaya M. Identification of two novel SMCHD1 sequence variants in families with FSHD-like muscular dystrophy. Eur J Hum Genet 2015; 23: 67-71
24. Larsen M, Rost S, El Hajj N et al. Diagnostic approach for FSHD revisited: SMCHD1 mutations cause FSHD2 and act as modifiers of disease severity in FSHD1. Eur J Hum Genet 2015; 23: 808-816
25. Ricci E, Galluzzi G., Deidda G. et al. Progress in the molecular diagnosis of facioscapulohumeral dystrophy and correlation between the number of KpnI repeat at the 4q35 locus and clinical phenotype. Ann Neurol 1999; 45: 751-757
26. Hill KA, Wang J, Farwell KD, Scaringe WA, Sommer SS. Spontaneous multiple mutations show both proximal spacing consistent with chronocoordinate events and alterations with p53-deficiency. Mutat Res 2004; 554: 223-240
27. Colgin LM, Hackmann AF, Emond MJ, Monnat RJ Jr. The unexpected landscape of in vivo somatic mutation in a human epithelial cell lineage. Proc Natl Acad Sci USA 2002; 99: 1437-1442
28. Chen Z, Feng J, Buzin CH, Sommer SS. Epidemiology of doublet/multiplet mutations in lung cancers: evidence that a subset arises by chronocoordinate events. PLoS One 2008; 3: e3714
29. Buettner VL, Hill KA, Scaringe WA, Sommer SS. Evidence that proximal multiple mutations in Big Blue transgenic mice are dependent events. Mutat Res 2000; 452: 219-229
30. Zatz M, Marie SK, Cerqueira A, Vainzof M, Pavanello RC, Passos-Bueno MR. The facioscapulohumeral muscular dystrophy (FSHD1) gene affects males more severely and more frequently than females. Am J Med Genet 1998; 77: 155-161
31. Van Der Maarel SM, Deidda G, Lemmers RJ 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 2000; 66: 26-35
32. Tonini MM, Passos-Bueno MR, Cerqueira A, Matioli SR, Pavanello R, Zatz M. Asymptomatic carriers and gender differences in facioscapulohumeral muscular dystrophy (FSHD). Neuromuscul Disord 2004; 14: 33-38
33. Blewitt ME, Gendrel AV, Pang Z et al. SmcHD1, containing a structural-maintenanceof-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 2008; 40: 663-669
34. Gendrel AV, Apedaile A, Coker H et al. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev cell 2012; 23: 265-279
35. Gendrel AV, Tang YA, Suzuki M et al. Epigenetic functions of smchd1 repress gene clusters on the inactive X chromosome and on autosomes. Mol Cell Biol 2013; 33: 3150-3165
36. Nozawa RS, Nagao K, Igami KT et al. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struct Mol Biol 2013; 20: 566-573
37. Mould AW, Pang Z, Pakusch M et al. Smchd1 regulates a subset of autosomal genes subject to monoallelic expression in addition to being critical for X inactivation. Epigenetics Chromatin 2013; 6: 19
38. Blewitt ME, Vickaryous NK, Hemley SJ et al. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. Proc Natl Acad Sci USA 2005; 102: 7629-7634