Loss of WSTF results in spontaneous fluctuations of heterochromatin formation and resolution, combined with substantial changes to gene expression

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Culver Cochran, Ashley E ^a   Chadwick, Brian P ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; HETEROCHROMATIN PROTEIN 1; HISTONE H3; LYSINE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WILLIAMS SYNDROME TRANSCRIPTION FACTOR; ZINC FINGER NUCLEASE; BAZ1B PROTEIN, HUMAN; HETEROCHROMATIN; HISTONE;

ARTICLE; BAZ1B GENE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHROMATIN; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DENSE BODY; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE INACTIVATION; GENE ISOLATION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HAPLOINSUFFICIENCY; HETEROCHROMATIN; HINGE REGION; HOMEOSTASIS; HUMAN; HUMAN CELL; METHYLATION; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN FUNCTION; WILLIAMS BEUREN SYNDROME; X CHROMOSOME INACTIVATION; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEFICIENCY; GENETICS; METABOLISM; PROMOTER REGION; X CHROMOSOME;

BASE SEQUENCE; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMES, HUMAN, X; GENE KNOCKOUT TECHNIQUES; HAPLOINSUFFICIENCY; HETEROCHROMATIN; HISTONES; HUMANS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; WILLIAMS SYNDROME;

EID: 84886377769     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-740     Document Type: Article

References (86)

1. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373.
2. Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 2013, 152:1308-1323.
3. Chadwick BP, Willard HF. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc Natl Acad Sci U S A 2004, 101:17450-17455.
4. Boggs BA, Cheung P, Heard E, Spector DL, Chinault AC, Allis CD. Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat Genet 2002, 30:73-76.
5. Peters AH, Mermoud JE, O'Carroll D, Pagani M, Schweizer D, Brockdorff N, Jenuwein T. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat Genet 2002, 30:77-80.
6. Chadwick BP, Willard HF. Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome. Hum Mol Genet 2003, 12:2167-2178.
7. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. Role of histone H3 lysine 27 methylation in X inactivation. Science 2003, 300:131-135.
8. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, Peters AH, Jenuwein T, Otte AP, Brockdorff N. Establishment of histone h3 methylation on the inactive x chromosome requires transient recruitment of eed-enx1 polycomb group complexes. Dev Cell 2003, 4:481-495.
9. Chadwick BP, Willard HF. Histone H2A variants and the inactive X chromosome: identification of a second macroH2A variant. Hum Mol Genet 2001, 10:1101-1103.
10. Costanzi C, Pehrson JR. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 1998, 393:599-601.
11. Costanzi C, Pehrson JR. MacroH2A2, a new member of the MacroH2A core histone family. J Biol Chem 2001, 276:21776-21784.
12. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 1992, 71:515-526.
13. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF. 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 1992, 71:527-542.
14. Clemson CM, McNeil JA, Willard HF, Lawrence JB. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 1996, 132:1-17.
15. Culver-Cochran AE, Chadwick BP. The WSTF-ISWI chromatin remodeling complex transiently associates with the human inactive X chromosome during late S-phase prior to BRCA1 and gamma-H2AX. PLoS One 2012, 7:e50023.
16. Bozhenok L, Wade PA, Varga-Weisz P. WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. EMBO J 2002, 21:2231-2241.
17. Poot RA, Bozhenok L, van den Berg DL, Hawkes N, Varga-Weisz PD. Chromatin remodeling by WSTF-ISWI at the replication site: opening a window of opportunity for epigenetic inheritance?. Cell Cycle 2005, 4:543-546.
18. Poot RA, Bozhenok L, van den Berg DL, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz PD. The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol 2004, 6:1236-1244.
19. Lu X, Meng X, Morris CA, Keating MT. A novel human gene, WSTF, is deleted in Williams syndrome. Genomics 1998, 54:241-249.
20. Cavellan E, Asp P, Percipalle P, Farrants AK. The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J Biol Chem 2006, 281:16264-16271.
21. Xiao A, Li H, Shechter D, Ahn SH, Fabrizio LA, Erdjument-Bromage H, Ishibe-Murakami S, Wang B, Tempst P, Hofmann K, et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 2009, 457:57.
22. Percipalle P, Fomproix N, Cavellan E, Voit R, Reimer G, Kruger T, Thyberg J, Scheer U, Grummt I, Farrants AK. The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep 2006, 7:525-530.
23. Cook PJ, Ju BG, Telese F, Wang X, Glass CK, Rosenfeld MG. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 2009, 458:591-596.
24. Stucki M. Histone H2A.X Tyr142 phosphorylation: a novel sWItCH for apoptosis?. DNA Repair (Amst) 2009, 8:873-876.
25. Stromme P, Bjornstad PG, Ramstad K. Prevalence estimation of Williams syndrome. J Child Neurol 2002, 17:269-271.
26. Perez Jurado LA, Peoples R, Kaplan P, Hamel BC, Francke U. Molecular definition of the chromosome 7 deletion in Williams syndrome and parent-of-origin effects on growth. Am J Hum Genet 1996, 59:781-792.
27. Valero MC, de Luis O, Cruces J, Perez Jurado LA. Fine-scale comparative mapping of the human 7q11.23 region and the orthologous region on mouse chromosome 5G: the low-copy repeats that flank the Williams-Beuren syndrome deletion arose at breakpoint sites of an evolutionary inversion(s). Genomics 2000, 69:1-13.
28. Bayes M, Magano LF, Rivera N, Flores R, Perez Jurado LA. Mutational mechanisms of Williams-Beuren syndrome deletions. Am J Hum Genet 2003, 73:131-151.
29. DeSilva U, Elnitski L, Idol JR, Doyle JL, Gan W, Thomas JW, Schwartz S, Dietrich NL, Beckstrom-Sternberg SM, McDowell JC, et al. Generation and comparative analysis of approximately 3.3 Mb of mouse genomic sequence orthologous to the region of human chromosome 7q11.23 implicated in Williams syndrome. Genome Res 2002, 12:3-15.
30. Merla G, Ucla C, Guipponi M, Reymond A. Identification of additional transcripts in the Williams-Beuren syndrome critical region. Hum Genet 2002, 110:429-438.
31. Peoples RJ, Cisco MJ, Kaplan P, Francke U. Identification of the WBSCR9 gene, encoding a novel transcriptional regulator, in the Williams-Beuren syndrome deletion at 7q11.23. Cytogenet Cell Genet 1998, 82:238-246.
32. Bellugi U, Bihrle A, Jernigan T, Trauner D, Doherty S. Neuropsychological, neurological, and neuroanatomical profile of Williams syndrome. Am J Med Genet Suppl 1990, 6:115-125.
33. Burn J. Williams syndrome. J Med Genet 1986, 23:389-395.
34. Morris CA, Demsey SA, Leonard CO, Dilts C, Blackburn BL. Natural history of Williams syndrome: physical characteristics. J Pediatr 1988, 113:318-326.
35. Cus R, Maurus D, Kuhl M. Cloning and developmental expression of WSTF during Xenopus laevis embryogenesis. Gene Expr Patterns 2006, 6:340-346.
36. Yoshimura K, Kitagawa H, Fujiki R, Tanabe M, Takezawa S, Takada I, Yamaoka I, Yonezawa M, Kondo T, Furutani Y, et al. Distinct function of 2 chromatin remodeling complexes that share a common subunit, Williams syndrome transcription factor (WSTF). Proc Natl Acad Sci U S A 2009, 106:9280-9285.
37. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
38. Carroll D. Genome engineering with zinc-finger nucleases. Genetics 2011, 188:773-782.
39. Topaloglu O, Hurley PJ, Yildirim O, Civin CI, Bunz F. Improved methods for the generation of human gene knockout and knockin cell lines. Nucleic Acids Res 2005, 33:e158.
40. Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 2010, 79:181-211.
41. Barr ML, Bertram EG. A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 1949, 163:676-677.
42. Casas-Delucchi CS, Brero A, Rahn HP, Solovei I, Wutz A, Cremer T, Leonhardt H, Cardoso MC. Histone acetylation controls the inactive X chromosome replication dynamics. Nat Commun 2011, 2:222.
43. Chadwick BP, Willard HF. Cell cycle-dependent localization of macroH2A in chromatin of the inactive X chromosome. J Cell Biol 2002, 157:1113-1123.
44. Jeppesen P, Turner BM. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 1993, 74:281-289.
45. Chadwick BP, Lane TF. BRCA1 associates with the inactive X chromosome in late S-phase, coupled with transient H2AX phosphorylation. Chromosoma 2005, 114:432-439.
46. Ito T, Levenstein ME, Fyodorov DV, Kutach AK, Kobayashi R, Kadonaga JT. ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev 1999, 13:1529-1539.
47. Strohner R, Nemeth A, Jansa P, Hofmann-Rohrer U, Santoro R, Langst G, Grummt I. NoRC-a novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J 2001, 20:4892-4900.
48. Tsukiyama T, Daniel C, Tamkun J, Wu C. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 1995, 83:1021-1026.
49. Varga-Weisz PD, Wilm M, Bonte E, Dumas K, Mann M, Becker PB. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 1997, 388:598-602.
50. Guenatri M, Bailly D, Maison C, Almouzni G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 2004, 166:493-505.
51. Narita M, Narita M, Krizhanovsky V, Nunez S, Chicas A, Hearn SA, Myers MP, Lowe SW. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006, 126:503-514.
52. Saunders WS, Chue C, Goebl M, Craig C, Clark RF, Powers JA, Eissenberg JC, Elgin SC, Rothfield NF, Earnshaw WC. Molecular cloning of a human homologue of Drosophila heterochromatin protein HP1 using anti-centromere autoantibodies with anti-chromo specificity. J Cell Sci 1993, 104:573-582.
53. Singh PB, Miller JR, Pearce J, Kothary R, Burton RD, Paro R, James TC, Gaunt SJ. A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucleic Acids Res 1991, 19:789-794.
54. Ye Q, Worman HJ. Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J Biol Chem 1996, 271:14653-14656.
55. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001, 410:120-124.
56. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, Eissenberg JC, Allis D, Khorasanizadeh S. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J 2001, 20:5232-5241.
57. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001, 410:116-120.
58. Nozawa RS, Nagao K, Igami KT, Shibata S, Shirai N, Nozaki N, Sado T, Kimura H, Obuse C. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struct Mol Biol 2013, 20:566-573.
59. Minc E, Allory Y, Worman HJ, Courvalin J-C, Buendia B. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 1999, 108:220-234.
60. Earnshaw WC, Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 1985, 91:313-321.
61. Warburton PE, Cooke CA, Bourassa S, Vafa O, Sullivan BA, Stetten G, Gimelli G, Warburton D, Tyler-Smith C, Sullivan KF, et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol 1997, 7:901-904.
62. Barnett C, Krebs JE. WSTF does it all: a multifunctional protein in transcription, repair, and replication. Biochem Cell Biol 2011, 89:12-23.
63. Lallemand-Breitenbach V, de The H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010, 2:a000661.
64. Nishitani H, Taraviras S, Lygerou Z, Nishimoto T. The human licensing factor for DNA replication Cdt1 accumulates in G1 and is destabilized after initiation of S-phase. J Biol Chem 2001, 276:44905-44911.
65. Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A. Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 2000, 290:2309-2312.
66. Celis JE, Celis A. Cell cycle-dependent variations in the distribution of the nuclear protein cyclin proliferating cell nuclear antigen in cultured cells: subdivision of S phase. Proc Natl Acad Sci U S A 1985, 82:3262-3266.
67. Leonhardt H, Rahn HP, Weinzierl P, Sporbert A, Cremer T, Zink D, Cardoso MC. Dynamics of DNA replication factories in living cells. J Cell Biol 2000, 149:271-280.
68. Hendzel MJ, Wei Y, Mancini MA, Hooser AV, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD. Mitosis-specific phosphorylation of histone H3 intiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997, 106:348-360.
69. El-Amraoui A, Petit C. Cadherins as targets for genetic diseases. Cold Spring Harb Perspect Biol 2010, 2:a003095.
70. Dallosso AR, Hancock AL, Szemes M, Moorwood K, Chilukamarri L, Tsai HH, Sarkar A, Barasch J, Vuononvirta R, Jones C, et al. Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Genet 2009, 5:e1000745.
71. Dallosso AR, Oster B, Greenhough A, Thorsen K, Curry TJ, Owen C, Hancock AL, Szemes M, Paraskeva C, Frank M, et al. Long-range epigenetic silencing of chromosome 5q31 protocadherins is involved in early and late stages of colorectal tumorigenesis through modulation of oncogenic pathways. Oncogene 2012, 31:4409-4419.
72. Wang J, Mager J, Chen Y, Schneider E, Cross JC, Nagy A, Magnuson T. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 2001, 28:371-375.
73. Kalantry S, Millis KC, Yee D, Otte AP, Panning B, Magnuson T. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat Cell Biol 2006, 8:195-202.
74. Mise N, Sado T, Tada M, Takada S, Takagi N. Activation of the inactive X chromosome induced by cell fusion between a murine EC and female somatic cell accompanies reproducible changes in the methylation pattern of the Xist gene. Exp Cell Res 1996, 223:193-202.
75. Sado T, Tada T, Takagi N. Mosaic methylation of Xist gene before chromosome inactivation in undifferentiated female mouse embryonic stem and embryonic germ cells. Dev Dyn 1996, 205:421-434.
76. Takagi N. De novo X-chromosome inactivation in somatic hybrid cells between the XO mouse embryonal carcinoma cell and XY rat lymphocyte. Exp Cell Res 1983, 145:397-404.
77. Takagi N. Variable X chromosome inactivation patterns in near-tetraploid murine EC x somatic cell hybrid cells differentiated in vitro. Genetica 1993, 88:107-117.
78. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
79. van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton GJ, Ariyurek Y, den Dunnen JT, Lamond AI. High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell 2010, 21:3735-3748.
80. Zhang LF, Huynh KD, Lee JT. Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing. Cell 2007, 129:693-706.
81. Chadwick BP, Willard HF. A novel chromatin protein, distantly related to histone H2A, is largely excluded from the inactive X chromosome. J Cell Biol 2001, 152:375-384.
82. Harlow E, Lane D. Using Antibodies: A Laboratory Manual 1999, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
83. McLaughlin CR, Chadwick BP. 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 2011, 12:R37.
84. Grimes BR, Babcock J, Rudd MK, Chadwick B, Willard HF. Assembly and characterization of heterochromatin and euchromatin on human artificial chromosomes. Genome Biol 2004, 5:R89.
85. Alekseev OM, Bencic DC, Richardson RT, Widgren EE, O'Rand MG. Overexpression of the Linker histone-binding protein tNASP affects progression through the cell cycle. J Biol Chem 2003, 278:8846-8852.
86. Chadwick BP. 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 2008, 18:1259-1269.