Two novel DXZ4-associated long noncoding RNAs show developmental changes in expression coincident with heterochromatin formation at the human (Homo sapiens) macrosatellite repeat

Chromosome Research

Volumn 23, Issue 4, 2015, Pages 733-752

  Figueroa, Debbie M ^a,b   Darrow, Emily M ^a   Chadwick, Brian P ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

DXZ4; Euchromatin and heterochromatin; Human embryonic stem cells; Long noncoding RNA; Macrosatellite; X chromosome inactivation

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; DXZ4 PROTEIN; HISTONE H3; LONG UNTRANSLATED RNA; PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; HETEROCHROMATIN; SATELLITE DNA;

ARTICLE; CHROMATIN; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; DIFFERENTIATION; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GENE EXPRESSION; HETEROCHROMATIN; HUMAN; HUMAN CELL; MALE; PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; RNA TRANSCRIPTION; TANDEM REPEAT; X CHROMOSOME; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL MAPPING; CYTOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; HUMAN EMBRYONIC STEM CELL; METABOLISM; REPRODUCIBILITY; TRANSFORMED CELL LINE; X CHROMOSOME INACTIVATION;

CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, X; DNA METHYLATION; DNA, SATELLITE; FEMALE; GENE EXPRESSION; HETEROCHROMATIN; HUMAN EMBRYONIC STEM CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; RNA, LONG NONCODING; X CHROMOSOME INACTIVATION;

EID: 84949085429     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-015-9479-3     Document Type: Article

References (62)

1. Awaya T, Kato T, Mizuno Y et al (2012) Selective development of myogenic mesenchymal cells from human embryonic and induced pluripotent stem cells. PLoS One 7(12):e51638. doi:10.1371/journal.pone.0051638
2. Booth MJ, Branco MR, Ficz G et al (2012) Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336(6083):934–937. doi:10.1126/science.1220671
3. Branco MR, Ficz G, Reik W (2012) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13(1):7–13. doi:10.1038/nrg3080
4. Brockdorff N, Ashworth A, Kay GF et al (1992) The product of the mouse Xist gene is a 15kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71:515–526
5. Brown CJ, Hendrich BD, Rupert JL et al (1992) The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71:527–542
6. Cabianca DS, Casa V, Bodega B et al (2012) A long ncRNA links copy number variation to a Polycomb/Trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149(4):819–831. doi:10.1016/j.cell.2012.03.035
7. Cadet J, Wagner JR (2014) TET enzymatic oxidation of 5-methylcytosine, 5-hydroxymethylcytosine and 5-formylcytosine. Mutat Res Genet Toxicol Environ Mutagen 764–765:18–35. doi:10.1016/j.mrgentox.2013.09.001
8. Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14(2):155–164. doi:10.1016/j.gde.2004.02.001
9. Cao R, Wang L, Wang H et al (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298(5595):1039–1043
10. Castel SE, Martienssen RA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14(2):100–112. doi:10.1038/nrg3355
11. Chadwick BP (2008) DXZ4 chromatin adopts an opposing conformation to that of the surrounding chromosome and acquires a novel inactive X-specific role involving CTCF and antisense transcripts. Genome Res 18(8):1259–1269
12. Chadwick BP, Willard HF (2002) Cell cycle-dependent localization of macroH2A in chromatin of the inactive X chromosome. J Cell Biol 157(7):1113–1123
13. Chadwick BP, Willard HF (2003a) Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. Semin Cell Dev Biol 14:359–367
14. Chadwick BP, Willard HF (2003b) Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome. Hum Mol Genet 12(17):2167–2178
15. Cheng YH, Wong EW, Cheng CY (2011) Cancer/testis (CT) antigens, carcinogenesis and spermatogenesis. Spermatogenesis 1(3):209–220. doi:10.4161/spmg.1.3.179902156-5554-1-3-5
16. Chetty S, Pagliuca FW, Honore C, Kweudjeu A, Rezania A, Melton DA (2013) A simple tool to improve pluripotent stem cell differentiation. Nat Methods 10(6):553–556. doi:10.1038/nmeth.2442
17. Chopra P, Papale LA, White AT et al (2014) Array-based assay detects genome-wide 5-mC and 5-hmC in the brains of humans, non-human primates, and mice. BMC Genomics 15:131. doi:10.1186/1471-2164-15-131
18. Consortium EP, Bernstein BE, Birney E (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489(7414):57–74. doi:10.1038/nature11247
19. Deidda G, Cacurri S, Grisanti P, Vigneti E, Piazzo N, Felicetti L (1995) 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(3):155–167
20. Ficz G, Branco MR, Seisenberger S et al (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473(7347):398–402. doi:10.1038/nature10008
21. Gendrel AV, Heard E (2014) Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu Rev Cell Dev Biol. doi:10.1146/annurev-cellbio-101512-122415
22. Geng LN, Yao Z, Snider L et al (2012) DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 22:1–14. doi:10.1016/j.devcel.2011.11.013
23. Giacalone J, Friedes J, Francke U (1992) A novel GC-rich human macrosatellite VNTR in Xq24 is differentially methylated on active and inactive X chromosomes. Nat Genet 1(2):137–143
24. Globisch D, Munzel M, Muller M et al (2010) Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 5(12):e15367. doi:10.1371/journal.pone.0015367
25. Hacisuleyman E, Goff LA, Trapnell C et al (2014) Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat Struc Mol Biol 21(2):198–206
26. Hasson D, Alonso A, Cheung F et al (2011) Formation of novel CENP-A domains on tandem repetitive DNA and across chromosome breakpoints on human chromosome 8q21 neocentromeres. Chromosoma 120(6):621–632. doi:10.1007/s00412-011-0337-6
27. Horakova AH, Calabrese JM, McLaughlin CR, Tremblay DC, Magnuson T, Chadwick BP (2012a) The mouse DXZ4 homolog retains Ctcf binding and proximity to Pls3 despite substantial organizational differences compared to the primate macrosatellite. Genome Biol 13(8):R70. doi:10.1186/gb-2012-13-8-r70
28. Horakova AH, Moseley SC, McLaughlin CR, Tremblay DC, Chadwick BP (2012b) The macrosatellite DXZ4 mediates CTCF-dependent long-range intrachromosomal interactions on the human inactive X chromosome. Hum Mol Genet. doi:10.1093/hmg/dds270
29. Jeon Y, Sarma K, Lee JT (2012) New and xisting regulatory mechanisms of X chromosome inactivation. Curr Opin Genet Dev 22(2):62–71. doi:10.1016/j.gde.2012.02.007
30. Lemmers RJ, de Kievit P, Sandkuijl L et al (2002) Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere. Nat Genet 32(2):235–236. doi:10.1038/ng999ng999
31. Lemmers RJ, van der Vliet PJ, Klooster R et al (2010) A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329:1650–1653. doi:10.1126/science.1189044
32. Lessing D, Anguera MC, Lee JT (2013) X chromosome inactivation and epigenetic responses to cellular reprogramming. Annu Rev Genomics Hum Genet 14:85–110. doi:10.1146/annurev-genom-091212-153530
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitiatve PCR and the 2-ΔΔCT method. Methods 25(4):402–408, ISSN 1046-2023
34. Lobanenkov VV, Nicolas RH, Adler VV et al (1990) A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5′-flanking sequence of the chicken c-myc gene. Oncogene 5(12):1743–1753
35. Lyon MF (2002) X-chromosome inactivation and human genetic disease. Acta Paediatr Suppl 91(439):107–112
36. Mahmood A, Harkness L, Schroder HD, Abdallah BM, Kassem M (2010) Enhanced differentiation of human embryonic stem cells to mesenchymal progenitors by inhibition of TGF-beta/activin/nodal signaling using SB-431542. J Bone Min Res: Off J Am Soc Bone Min Res 25(6):1216–1233. doi:10.1002/jbmr.34
37. McLaughlin CR, Chadwick BP (2011) Characterization of DXZ4 conservation in primates implies important functional roles for CTCF binding, array expression and tandem repeat organization on the X chromosome. Genome Biol 12:R37
38. Minkovsky A, Patel S, Plath K (2012) Concise review: pluripotency and the transcriptional inactivation of the female Mammalian X chromosome. Stem Cells 30(1):48–54. doi:10.1002/stem.755
39. Moseley SC, Rizkallah R, Tremblay DC, Anderson BR, Hurt MM, Chadwick BP (2012) YY1 associates with the macrosatellite DXZ4 on the inactive X chromosome and binds with CTCF to a hypomethylated form in some male carcinomas. Nucleic Acids Res 40(4):1596–1608. doi:10.1093/nar/gkr964
40. Okada T, Gondo Y, Goto J, Kanazawa I, Hadano S, Ikeda JE (2002) Unstable transmission of the RS447 human megasatellite tandem repetitive sequence that contains the USP17 deubiquitinating enzyme gene. Hum Genet 110(4):302–313
41. Ottaviani A, Rival-Gervier S, Boussouar A et al (2009) The D4Z4 macrosatellite repeat acts as a CTCF and A-type lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet 5(2):e1000394
42. Parkhomchuk D, Borodina T, Amstislavskiy V et al (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37(18):e123. doi:10.1093/nar/gkp596
43. Plath K, Fang J, Mlynarczyk-Evans SK et al (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300(5616):131–135
44. Pohlers M, Calabrese JM, Magnuson T (2014) Small RNA expression from the human macrosatellite DXZ4. G3. doi:10.1534/g3.114.012260
45. Rao SSP, Huntley MH, Durand NC et al (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1–16
46. Santos-Rosa H, Schneider R, Bannister AJ et al (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419(6905):407–411
47. Schaap M, Lemmers RJ, Maassen R et al (2013) Genome-wide analysis of macrosatellite repeat copy number variation in worldwide populations: evidence for differences and commonalities in size distributions and size restrictions. BMC Genomics 14:143. doi:10.1186/1471-2164-14-143
48. Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T (2004) Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6(1):73–77
49. Stroud H, Feng S, Morey Kinney S, Pradhan S, Jacobsen SE (2011) 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 12(6):R54. doi:10.1186/gb-2011-12-6-r54
50. Szulwach KE, Li X, Li Y et al (2011a) Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet 7(6):e1002154. doi:10.1371/journal.pgen.1002154PGENETICS-D-11-00676
51. Szulwach KE, Li X, Li Y et al (2011b) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14(12):1607–1616. doi:10.1038/nn.2959
52. Teller K, Illner D, Thamm S et al (2011) A top-down analysis of Xa- and Xi-territories reveals differences of higher order structure at >/= 20 Mb genomic length scales. Nucleus 2(5):465–477. doi:10.4161/nucl.2.5.17862
53. Tremblay DC, Alexander G Jr, Moseley S, Chadwick BP (2010) Expression, tandem repeat copy number variation and stability of four macrosatellite arrays in the human genome. BMC Genomics 11:632
54. Tremblay DC, Moseley S, Chadwick BP (2011) Variation in array size, monomer composition and expression of the macrosatellite DXZ4. PLoS ONE 6(4):e18969. doi:10.1371/journal.pone.0018969
55. van Deutekom JC, Wijmenga C, van Tienhoven EA et al (1993) FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum Mol Genet 2(12):2037–2042
56. van Overveld PG, Lemmers RJ, Sandkuijl LA et al (2003) Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet 35(4):315–317
57. Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W (2013) CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res 41(6):e74. doi:10.1093/nar/gkt006
58. Warburton PE, Hasson D, Guillem F, Lescale C, Jin X, Abrusan G (2008) Analysis of the largest tandemly repeated DNA families in the human genome. BMC Genomics 9:533
59. Wijmenga C, Hewitt JE, Sandkuijl LA et al (1992) Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 2(1):26–30
60. Yang F, Deng X, Berletch JB et al (2015) The lncRNA Firre anchors the inactive X chromsoome to the nucleolus by binding CTCF and maintains H3K27me3 methylation. Gen Biol 16:52. doi:10.1186/s13059-015-0618-0
61. Yu M, Hon GC, Szulwach KE et al (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149(6):1368–1380. doi:10.1016/j.cell.2012.04.027
62. Zeng W, de Greef JC, Chen YY et al (2009) Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 5(7):e1000559. doi:10.1371/journal.pgen.1000559