The ATTCT repeats of spinocerebellar ataxia type 10 display strong nucleosome assembly which is enhanced by repeat interruptions

Gene

Volumn 434, Issue 1-2, 2009, Pages 29-34

  Hagerman, Katharine A ^a,b   Ruan, Haihe ^c   Edamura, Kerrie Nichol ^b   Matsuura, Tohru ^d   Pearson, Christopher E ^a,b   Wang, Yuh Hwa ^e  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c The State University of New Jersey   (United States)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Histone acetylation; Nucleosome formation; Pentanucleotide; Repeat purity; SCA10

Indexed keywords

CELL PROTEIN; HISTONE; NUCLEIC ACID BINDING PROTEIN; NUCLEOSOME ASSEMBLY PROTEIN 1; SPINOCEREBELLAR ATAXIA TYPE 10; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; GENETIC STABILITY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOSOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINOCEREBELLAR DEGENERATION;

ACETYLATION; BASE SEQUENCE; CHROMOSOME POSITIONING; GENOME, HUMAN; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NUCLEOSOMES; REPETITIVE SEQUENCES, NUCLEIC ACID; SPINOCEREBELLAR ATAXIAS;

EID: 60649116036     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gene.2008.12.011     Document Type: Article

References (56)

1. Aggarwal B.D., and Calvi B.R. Chromatin regulates origin activity in Drosophila follicle cells. Nature 430 (2004) 372-376
2. Bradbury E.M. Reversible histone modifications and the chromosome cell cycle. Bioessays 14 (1992) 9-16
3. Cho D.H., Thienes C.P., Mahoney S.E., Analau E., Filippova G.N., and Tapscott S.J. Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol. Cell 20 (2005) 483-489
4. Cleary J.D., and Pearson C.E. The contribution of cis-elements to disease-associated repeat instability: clinical and experimental evidence. Cytogenet. Genome Res. 100 (2003) 25-55
5. Eichler E.E., et al. Length of uninterrupted CGG repeats determines instability in the FMR1 gene. Nat. Genet. 8 (1994) 88-94
6. Fujii-Nakata T., Ishimi Y., Okuda A., and Kikuchi A. Functional analysis of nucleosome assembly protein, NAP-1. The negatively charged COOH-terminal region is not necessary for the intrinsic assembly activity. J. Biol. Chem. 267 (1992) 20980-20986
7. Gabellini D., Green M.R., and Tupler R. Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110 (2002) 339-348
8. Gemmen G.J., Sim R., Haushalter K.A., Ke P.C., Kadonaga J.T., and Smith D.E. Forced unraveling of nucleosomes assembled on heterogeneous DNA using core histones, NAP-1, and ACF. J. Mol. Biol. 351 (2005) 89-99
9. Godde J.S., Kass S.U., Hirst M.C., and Wolffe A.P. Nucleosome assembly on methylated CGG triplet repeats in the fragile X mental retardation gene 1 promoter. J. Biol. Chem. 271 (1996) 24325-24328
10. Grewal R.P., et al. Clinical features and ATTCT repeat expansion in spinocerebellar ataxia type 10. Arch. Neurol. 59 (2002) 1285-1290
11. Grewal R.P., et al. Clinical and genetic analysis of a distinct autosomal dominant spinocerebellar ataxia. Neurology 51 (1998) 1423-1426
12. Handa V., Yeh H.J., McPhie P., and Usdin K. The AUUCU repeats responsible for spinocerebellar ataxia type 10 form unusual RNA hairpins. J. Biol. Chem. 280 (2005) 29340-29345
13. Hsu Y.Y., and Wang Y.H. Human fragile site FRA16B DNA excludes nucleosomes in the presence of distamycin. J. Biol. Chem. 277 (2002) 17315-17319
14. Ito T., Bulger M., Kobayashi R., and Kadonaga J.T. Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16 (1996) 3112-3124
15. Kemp M.G., Ghosh M., Liu G., and Leffak M. The histone deacetylase inhibitor trichostatin A alters the pattern of DNA replication origin activity in human cells. Nucleic Acids Res. 33 (2005) 325-336
16. Kowalski D., Natale D.A., and Eddy M.J. Stable DNA unwinding, not "breathing," accounts for single-strand-specific nuclease hypersensitivity of specific A+T-rich sequences. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 9464-9468
17. Kunst C.B., and Warren S.T. Cryptic and polar variation of the fragile X repeat could result in predisposing normal alleles. Cell 77 (1994) 853-861
18. Leeflang E.P., and Arnheim N. A novel repeat structure at the myotonic dystrophy locus in a 37 repeat allele with unexpectedly high stability. Hum. Mol. Genet. 4 (1995) 135-136
19. Libby R.T., et al. CTCF cis-regulates trinucleotide repeat instability in an epigenetic manner: a novel basis for mutational hot spot determination. PLoS Genet. 4 11 (2008) e1000257
20. Lin X., and Ashizawa T. Recent progress in spinocerebellar ataxia type-10 (SCA10). Cerebellum 4 (2005) 37-42
21. Liu G., Bissler J.J., Sinden R.R., and Leffak M. Unstable spinocerebellar ataxia type 10 (ATTCT)*(AGAAT) repeats are associated with aberrant replication at the ATX10 locus and replication origin-dependent expansion at an ectopic site in human cells. Mol. Cell. Biol. 27 (2007) 7828-7838
22. Lowary P.T., and Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. Sequence-dependent DNA structure: dinucleotide conformational maps. J. Mol. Biol. 276 (1998) 19-42
23. Loyola A., LeRoy G., Wang Y.H., and Reinberg D. Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. Genes Dev. 15 (2001) 2837-2851
24. Luger K., Rechsteiner T.J., and Richmond T.J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119 (1999) 1-16
25. Matsuura T., Achari M., Khajavi M., Bachinski L.L., Zoghbi H.Y., and Ashizawa T. Mapping of the gene for a novel spinocerebellar ataxia with pure cerebellar signs and epilepsy. Ann. Neurol. 45 (1999) 407-411
26. Matsuura T., et al. Somatic and germline instability of the ATTCT repeat in spinocerebellar ataxia type 10. Am. J. Hum. Genet. 74 (2004) 1216-1224
27. Matsuura T., et al. Interruptions in the expanded ATTCT repeat of spinocerebellar ataxia type 10: repeat purity as a disease modifier?. Am. J. Hum. Genet. 78 (2006) 125-129
28. Matsuura T., et al. Large expansion of the ATTCT pentanucleotide repeat in spinocerebellar ataxia type 10. Nat. Genet. 26 (2000) 191-194
29. Mulvihill D.J., Edamura K.N., Hagerman K.A., Pearson C.E., and Wang Y.H. Effect of CAT or AGG interruptions and CpG methylation on nucleosome assembly upon trinucleotide repeats on spinocerebellar ataxia, type 1 and fragile X syndrome. J. Biol. Chem. 280 (2005) 4498-4503
30. Norton V.G., Imai B.S., Yau P., and Bradbury E.M. Histone acetylation reduces nucleosome core particle linking number change. Cell 57 (1989) 449-457
31. Orphanides G. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92 (1998) 105-116
32. Packer M.J., Dauncey M.P., and Hunter C.A. Sequence-dependent DNA structure: dinucleotide conformational maps. J. Mol. Biol. 295 (2000) 71-83
33. Pavri R., et al. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125 (2006) 703-717
34. Pearson C.E., et al. Interruptions in the triplet repeats of SCA1 and FRAXA reduce the propensity and complexity of slipped strand DNA (S-DNA) formation. Biochemistry 37 (1998) 2701-2708
35. Pearson C.E., Nichol Edamura K., and Cleary J.D. Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet. 6 (2005) 729-742
36. Potaman V.N., et al. Unpaired structures in SCA10 (ATTCT)n.(AGAAT)n repeats. J. Mol. Biol. 326 (2003) 1095-1111
37. Ranum L.P., and Cooper T.A. RNA-mediated neuromuscular disorders. Annu. Rev. Neurosci. 29 (2006) 259-277
38. Rasmussen A., et al. Clinical and genetic analysis of four Mexican families with spinocerebellar ataxia type 10. Ann. Neurol. 50 (2001) 234-239
39. Saveliev A., Everett C., Sharpe T., Webster Z., and Festenstein R. DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 422 (2003) 909-913
40. Shrader T.E., and Crother D.M. Artificial nucleosome positioning sequences. Proc. Natl. Acad. Sci. U. S. A. 86 (1990) 7418-7422
41. Slean M.M., Panigrahi G.B., Ranum L.P., and Pearson C.E. Mutagenic roles of DNA "repair" proteins in antibody diversity and disease-associated trinucleotide repeat instability. DNA Repair (Amst) 7 (2008) 1135-1154
42. Tassone F., et al. Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA 13 (2007) 555-562
43. Tassone F., Hagerman R.J., Chamberlain W.D., and Hagerman P.J. Transcription of the FMR1 gene in individuals with fragile X syndrome. Am. J. Med. Genet. 97 (2000) 195-203
44. Thomsen B., Bendixen C., and Westergaard O. Histone hyperacetylation is accompanied by changes in DNA topology in vivo. Eur. J. Biochem. 201 (1991) 107-111
45. Tolstorukov M.Y., Colasanti A.V., McCandlish D.M., Olson W.K., and Zhurkin V.B. A novel roll-and slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. J. Mol. Biol. 371 (2007) 725-738
46. Trojer P., et al. L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129 (2007) 915-928
47. Wakamiya M., et al. The role of ataxin 10 in the pathogenesis of spinocerebellar ataxia type 10. Neurology 67 (2006) 607-613
48. Wang Y.H., Amirhaeri S., Kang S., Wells R.D., and Griffith J.D. Preferential nucleosome assembly at DNA triplet repeats from the myotonic dystrophy gene. Science 265 (1994) 669-671
49. Wang Y.H., Gellibolian R., Shimizu M., Wells R.D., and Griffith J. Long CCG triplet repeat blocks exclude nucleosomes: a possible mechanism for the nature of fragile sites in chromosomes. J. Mol. Biol. 263 (1996) 511-516
50. Wang Y.H., and Griffith J. Expanded CTG triplet blocks from the myotonic dystrophy gene create the strongest known natural nucleosome positioning elements. Genomics 25 (1995) 570-573
51. Wang Y.H., and Griffith J. Methylation of expanded CCG triplet repeat DNA from fragile X syndrome patients enhances nucleosome exclusion. J. Biol. Chem. 271 (1996) 22937-22940
52. Wang Y.H. Chromatin structure of repeating CTG/CAG and CGG/CCG sequences in human disease. Front Biosci. 12 (2007) 4731-4741
53. Waragai M., Nagamitsu S., Xu W., Li Y.J., Lin X., and Ashizawa T. Ataxin 10 induces neuritogenesis via interaction with G-protein beta2 subunit. J. Neurosci. Res. 83 (2006) 1170-1178
54. Yau P., Thorne A.W., Imai B.S., Matthews H.R., and Bradbury E.M. Thermal denaturation studies of acetylated nucleosomes and oligonucleosomes. Eur. J. Biochem. 129 (1982) 281-288
55. Zhong N., Yang W., Dobkin C., and Brown W.T. Fragile X gene instability: anchoring AGGs and linked microsatellites. Am. J. Hum. Genet. 57 (1995) 351-361
56. Zhou J., et al. Cell cycle regulation of chromatin at an origin of DNA replication. EMBO J. 24 (2005) 1406-1417