Genetic and Epigenetic Characteristics of FSHD-Associated 4q and 10q D4Z4 that are Distinct from Non-4q/10q D4Z4 Homologs

Human Mutation

Volumn 35, Issue 8, 2014, Pages 998-1010

  Zeng, Weihua ^a,b   Chen, Yen Yun ^a   Newkirk, Daniel A ^a   Wu, Beibei ^a   Balog, Judit ^c   Kong, Xiangduo ^a   Ball, Alexander R ^a   Zanotti, Simona ^d   Tawil, Rabi ^e   Hashimoto, Naohiro ^f   Mortazavi, Ali ^b   van der Maarel, Silvère M ^c   Yokomori, Kyoko ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^f NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

Author keywords

D4Z4; DUX4; FSHD1; FSHD2; H3K9me3; Heterochromatin; SMCHD1

Indexed keywords

DUX4 PROTEIN, HUMAN; HETEROCHROMATIN; HISTONE; HOMEODOMAIN PROTEIN; NONHISTONE PROTEIN; SATELLITE DNA; SMCHD1 PROTEIN, HUMAN;

ANIMAL; CELL LINE; CHROMOSOME 10; CHROMOSOME 4; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; HAMSTER; HETEROCHROMATIN; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; MUTATION; MYOBLAST; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOLOGY; PRIMARY CELL CULTURE; SEQUENCE HOMOLOGY;

ANIMALS; BASE SEQUENCE; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN, PAIR 10; CHROMOSOMES, HUMAN, PAIR 4; CRICETINAE; DNA, SATELLITE; EPIGENESIS, GENETIC; GENE EXPRESSION; HETEROCHROMATIN; HISTONES; HOMEODOMAIN PROTEINS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; MUTATION; MYOBLASTS; OPEN READING FRAMES; PRIMARY CELL CULTURE; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84904401389     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22593     Document Type: Article

References (59)

1. Ashe A, Morgan DK, Whitelaw NC, Bruxner TJ, Vickaryous NK, Cox LL, Butterfield NC, Wicking C, Blewitt ME, Wilkins SJ, Anderson GJ, Cox TC, et al. 2008. A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development. Genome Biol 9:R182.
2. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N, Craig JM, Apedaile A, Hilton DJ, Dunwoodie SL, Brockdorff N, Kay GF, Whitelaw E. 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 40:663-669.
3. Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, Simsek T, Garner HR, Agha-Mohammadi S, Tassin A, Coppée F, Belayew A, Perlingeiro RR, et al. 2008. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 27:2766-2779.
4. Broucqsault N, Morere J, Gaillard MC, Dumonceaux J, Torrents J, Salort-Campana E, Maues De Paula A, Bartoli M, Fernandez C, Chesnais AL, Ferreboeuf M, Sarda L, et al. 2013. Dysregulation of 4q35- and muscle-specific genes in fetuses with a short D4Z4 array linked to facio-scapulo-humeral dystrophy. Hum Mol Genet 22:4206-4214.
5. Cacurri S, Piazzo N, Deidda G, Vigneti E, Galluzzi G, Colantoni L, Merico B, Ricci E, Felicetti L. 1998. Sequence homology between 4qter and 10qter loci facilitates the instability of subtelomeric KpnI repeat units implicated in facioscapulohumeral muscular dystrophy. Am J Hum Genet 63:181-190.
6. Clapp J, Mitchell LM, Bolland DJ, Fantes J, Corcoran AE, Scotting PJ, Armour JA, Hewitt JE. 2007. Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am J Hum Genet 81:264-279.
7. de Greef JC, Lemmers RJ, Camaño P, Day JW, Sacconi S, Dunand M, van Engelen BG, Kiuru-Enari S, Padberg GW, Rosa AL, Desnuelle C, Spuler S, et al. 2010. Clinical features of facioscapulohumeral muscular dystrophy 2. Neurology 75:1548-1554.
8. de Greef JC, Lemmers RJ, van Engelen BG, Sacconi S, Venance SL, Frants RR, Tawil R, van der Maarel SM. 2009. Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum Mol Genet 30:1449-1459.
9. de Greef JC, Wohlgemuth M, Chan OA, Hansson KB, Smeets D, Frants RR, Weemaes CM, Padberg GW, van der Maarel SM. 2007. Hypomethylation is restricted to the D4Z4 repeat array in phenotypic FSHD. Neurology 69:1018-1026.
10. Dixit M, Ansseau E, Tassin A, Winokur S, Shi R, Qian H, Sauvage S, Mattéotti C, van Acker AM, Leo O, Figlewicz D, Barro M, et al. 2007. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc Natl Acad Sci USA 104:18157-18162.
11. Duan Z, Zarebski A, Montoya-Durango D, Grimes HL, Horwitz M. 2005. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol Cell Biol 25:10338-10351.
12. Feinberg AP. 2007. Phenotypic plasticity and the epigenetics of human disease. Nature 447:433-440.
13. Ferreboeuf M, Mariot V, Bessières B, Vasiljevic A, Attié-Bitach T, Collardeau S, Morere J, Roche S, Magdinier F, Robin-Ducellier J, Rameau P, Whalen S, et al. 2014. DUX4 and DUX4 downstream target genes are expressed in fetal FSHD muscles. Hum Mol Genet 23: 171-181.
14. Gabriëls J, Beckers MC, Ding H, De Vriese A, Plaisance S, van der Maarel SM, Padberg GW, Frants RR, Hewitt JE, Collen D, Belayew A. 1999. 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.
15. Gendrel AV, Apedaile A, Coker H, Termanis A, Zvetkova I, Godwin J, Tang YA, Huntley D, Montana G, Taylor S, Giannoulatou E, Heard E, et al. 2012. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev Cell 23:265-279.
16. Geng LN, Yao Z, Snider L, Fong AP, Cech JN, Young JM, van der Maarel SM, Ruzzo WL, Gentleman RC, Tawil R, Tapscott SJ. 2012. DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 22:38-51.
17. Gregson HC, Schmiesing JA, Kim J-S, Kobayashi T, Zhou S, Yokomori K. 2001. A potential role for human cohesin in mitotic spindle aster assembly. J Biol Chem 276:47575-47582.
18. Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CM, Gartler SM. 1999. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc Natl Acad Sci USA 96:14412-14417.
19. Hewitt JE, Lyle R, Clark LN, Valleley EM, Wright TJ, Wijmenga C, van Deutekom JC, Francis F, Sharpe PT, Hofker M, Frants RR, Williamson R. 1994. Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet 3:1287-1295.
20. Iwasa E, Hamashima Y, Fujishiro S, Higuchi E, Ito A, Yoshida M, Sodeoka M. 2010. Total synthesis of (+)-chaetocin and its analogues: their histone methyltransferase G9a inhibitory activity. J Am Chem Soc 132:4078-4079.
21. Jones TI, Chen JC, Rahimov F, Homma S, Arashiro P, Beermann ML, King OD, Miller JB, Kunkel LM, Emerson CPJ, Wagner KR, Jones PL. 2012. Facioscapulohumeral muscular dystrophy family studies of DUX4 expression: evidence for disease modifiers and a quantitative model of pathogenesis. Hum Mol Genet 21:4419-4430.
22. Krom YD, Thijssen PE, Young JM, den Hamer B, Balog J, Yao Z, Maves L, Snider L, Knopp P, Zammit PS, Rijkers T, van Engelen BG, et al. 2013. Intrinsic epigenetic regulation of the D4Z4 macrosatellite repeat in a transgenic mouse model for FSHD. PLoS Genet 9:e1003415.
23. Lemmers RJ, de Kievit P, Sandkuijl L, Padberg GW, van Ommen GJ, Frants RR, van der Maarel SM. 2002. Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere. Nat Genet 32:235-236.
24. Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camaño P, Dauwerse JG, Snider L, Straasheijm KR, van Ommen GJ, Padberg GW, Miller DG, Tapscott SJ, et al. 2010a. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329:1650-1653.
25. Lemmers RJ, van der Vliet PJ, van der Gaag KJ, Zuniga S, Frants RR, de Knijff P, van der Maarel SM. 2010b. 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.
26. Lemmers RJ, Wohlgemuth M, Frants RR, Padberg GW, Morava E, van der Maarel SM. 2004. Contractions of D4Z4 on 4qB subtelomeres do not cause facioscapulohumeral muscular dystrophy. Am J Hum Genet 75:1124-1130.
27. Lemmers RJ, Wohlgemuth M, van der Gaag KJ, van der Vliet PJ, van Teijlingen CM, de Knijff P, Padberg GW, Frants RR, van der Maarel SM. 2007. Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am J Hum Genet 81:884-894.
28. Lemmers RJL, de Kievit P, van Geel M, van der Wielen MJ, Bakker E, Padberg GW, Frants RR, van der Maarel SM. 2001. Complete allele information in the diagnosis of facioscapulohumeral muscular dystrophy by triple DNA analysis. Ann Neurol 50:816-819.
29. Lemmers RJLF, Tawil R, Petek LM, Balog J, Block GJ, Santen GWE, Amell AM, van der Vliet PJ, Almomani R, Straasheijm KR, Krom YD, Klooster R, et al. 2012. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat Genet 44:1370-1374.
30. Liao D. 1999. Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 64:24-30.
31. Lyle R, Wright TJ, Clark LN, Hewitt JE. 1995. The FSHD-associated repeat, D4Z4, is a member of a dispersed family of homeobox-containing repeats, subsets of which are clustered on the short arms of the acrocentric chromosomes. Genomics 28:389-397.
32. Mitsuhashi H, Mitsuhashi S, Lynn-Jones T, Kawahara G, Kunkel LM. 2013. Expression of DUX4 in zebrafish development recapitulates facioscapulohumeral muscular dystrophy. Hum Mol Genet 22:568-577.
33. Mostert V, Hill KE, Burk RF. 2003. Loss of activity of the selenoenzyme thioredoxin reductase causes induction of hepatic heme oxygenase-1. FEBS Lett 541:85-88.
34. Mugal CF, Ellegren H. 2011. Substitution rate variation at human CpG sites correlates with non-CpG divergence, methylation level and GC content. Genome Biol 12:R58.
35. Nozawa RS, Nagao K, Igami KT, Shibata S, Shirai N, Nozaki N, Sado T, Kimura H, Obuse C. 2013. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struc Mol Biol 20:566-573.
36. Rahimov F, King OD, Leung DG, Bibat GM, Emerson CPJ, Kunkel LM, Wagner KR. 2012. Transcriptional profiling in facioscapulohumeral muscular dystrophy to identify candidate biomarkers. Proc Natl Acad Sci USA 109:16234-16239.
37. Rideout WMr, Coetzee GA, Olumi AF, Jones PA. 1990. 5-Methylcytosine as an endogenous mutagen in the human LDL receptor and p53 genes. Science 249:1288-1290.
38. Sacconi S, Lemmers RJ, Balog J, van der Vliet PJ, Lahaut P, van Nieuwenhuizen MP, Straasheijm KR, Debipersad RD, Vos-Versteeg M, Salviati L, Casarin A, Pegoraro E, et al. 2013. The FSHD2 gene smchd1 is a modifier of disease severity in families affected by FSHD1. Am J Hum Genet 93:744-751.
39. Scionti I, Greco F, Ricci G, Govi M, Arashiro P, Vercelli L, Berardinell iA, Angelini C, Antonini G, Cao M, Di Muzio A, Moggio M, et al. 2012. Large-scale population analysis challenges the current criteria for the molecular diagnosis of fascioscapulohumeral muscular dystrophy. Am J Hum Genet 90:628-635.
40. Sharon N, Mor I, Zahavi E, Benvenisty N. 2012. DUXO, a novel double homeobox transcription factor, is a regulator of the gastrula organizer in human embryonic stem cells. Stem Cell Res 9:261-269.
41. Shiomi K, Kiyono T, Okamura K, Uezumi M, Goto Y, Yasumoto S, Shimizu S, Hashimoto N. 2011. CDK4 and cyclin D1 allow human myogenic cells to recapture growth property without compromising differentiation potential. Gene Ther 18:857-866.
42. Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, Maves L, Miller DG, Lemmers RJ, Winokur ST, Tawil R, van der Maarel SM, Filippova GN, et al. 2009. 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.
43. Snider L, Geng LN, Lemmers RJ, Kyba M, Ware CB, Nelson AM, Tawil R, Filippova GN, van der Maarel SM, Tapscott SJ, Miller DG. 2010. Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet 6:e1001181.
44. Tam R, Smith KP, Lawrence JB. 2004. The 4q subtelomere harboring the FSHD locus is specifically anchored with peripheral heterochromatin unlike most human telomeres. J Cell Biol 167:269-279.
45. Thijssen PE, Tobi EW, Balog J, Schouten SG, Kremer D, Bouazzaoui FE, Henneman P, Putter H, Slagboom PE, Heijmans BT, van der Maarel SM. 2013. Chromatin remodeling of human subtelomeres and TERRA promoters upon cellular senescence: commonalities and differences between chromosomes. Epigenetics 8:512-521.
46. Tibodeau JD, Benson LM, Isham CR, Owen WG, Bible KC. 2009. The anticancer agent chaetocin is a competitive substrate and inhibitor of thioredoxin reductase. Antioxid Redox Signal 11:1097-1106.
47. Trigona WL, Mullarky IK, Cao Y, Sordillo LM. 2006. Thioredoxin reductase regulates the induction of haem oxygenase-1 expression in aortic endothelial cells. Biochem J 394:207-216.
48. Turki A, Hayot M, Carnac G, Pillard F, Passerieux E, Bommart S, Raynaud de Mauverger E, Hugon G, Pincemail J, Pietri S, Lambert K, Belayew A, et al. 2012. Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 53:1068-1079.
49. van der Maarel SM, Frants RR. 2005. The D4Z4 repeat-mediated pathogenesis of facioscapulohumeral muscular dystrophy. Am J Hum Genet 76:375-386.
50. van der Maarel SM, Tawil R, Tapscott SJ. 2011. Facioscapulohumeral muscular dystrophy and DUX4: breaking the silence. Trends Mol Med 17:252-258.
51. Vanderplanck C, Ansseau E, Charron S, Stricwant N, Tassin A, Laoudj-Chenivesse D, Wilton SD, Coppée F, Belayew A. 2011. The FSHD atrophic myotube phenotype is caused by DUX4 expression. PLoS One 6:e26820.
52. van Overveld PG, Lemmers RJ, Sandkuijl LA, Enthoven L, Winokur ST, Bakels F, Padberg GW, van Ommen G-JB, Frants RR, van der Maarel SM. 2003. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet 35:315-317.
53. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schübeler D. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37:853-862.
54. Winokur ST, Bengtsson U, Feddersen J, Mathews KD, Weif-fenbach B, Bailey H, Markovich RP, Murray JC, Wasmuth JJ, Altherr MR. 1994. The DNA rearrangement associated with facioscapulohumeral muscular dystrophy involves a heterochromatin-associated repetitive element: implications for a role of chromatin structure in the pathogenesis of the disease. Chromosome Res 2:225-234.
55. Winokur ST, Bengtsson U, Vargas JC, Wasmuth JJ, Altherr MR, Weiffenbach B, Jacobsen SJ. 1996. The evolutionary distribution and structural organization of the homeoboxs-containing repeat D4Z4 indicates a functional role for the ancestral copy in the FSHD region. Hum Mol Genet 5:1567-1575.
56. Xia J, Han L, Zhao Z. 2012. Investigating the relationship of DNA methylation with mutation rate and allele frequency in the human genome. BMC Genomics 13:S7.
57. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187-191.
58. Zeng W, de Greef JC, Chen Y-Y, Chien R, Kong X, Gregson HC, Winokur ST, Pyle A, Robertson KD, Schmiesing JA, Kimonis VE, Balog J, et al. 2009. 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.
59. Zhang Y, Forner J, Fournet S, Jeanpierre M. 2001. Improved characterization of FSHD mutations. Ann Genet 44:105-110.