Unusual structures are present in DNA fragments containing super-long huntingtin CAG repeats

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Duzdevich, Daniel ^a   Li, Jinliang ^b   Whang, Jhoon ^b   Takahashi, Hirohide ^c   Takeyasu, Kunio ^c   Dryden, David T F ^d   Morton, A Jennifer ^a   Edwardson, J Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Laragen Inc   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; GENOMIC DNA; GUANINE; HUNTINGTIN; NUCLEASE; PROTEIN ECOP151; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG; DNA; DNA MODIFICATION METHYLASE ECOP15I; HD PROTEIN, HUMAN; NERVE PROTEIN; NUCLEAR PROTEIN; SINGLE STRANDED DNA; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC);

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DNA CLEAVAGE; DNA FRAGMENTATION; DNA HAIRPIN; DNA REPLICATION; DNA STRUCTURE; MOUSE; NONHUMAN; RESTRICTION MAPPING; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; TRINUCLEOTIDE REPEAT; ANIMAL; ATOMIC FORCE MICROSCOPY; CHEMISTRY; CONFORMATION; EXON; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; HUMAN; HUNTINGTON CHOREA; INVERTED REPEAT; METABOLISM; MUTATION; POLYMERASE CHAIN REACTION;

VIGNA RADIATA VAR. RADIATA;

ANIMALS; DNA; DNA, SINGLE-STRANDED; EXONS; GENE EXPRESSION REGULATION; GENOTYPE; HUMANS; HUNTINGTON DISEASE; INVERTED REPEAT SEQUENCES; MICE; MICROSCOPY, ATOMIC FORCE; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; POLYMERASE CHAIN REACTION; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC); TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEATS;

EID: 79951833466     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017119     Document Type: Article

References (53)

1. Orr HT, Zoghbi HY, (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
2. López Castel A, Cleary JD, Pearson CE, (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat Rev Mol Cell Biol 11: 165-170.
3. Wexler NS, Lorimer J, Porter J, Gomez F, Moskowitz C, et al. (2004) Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc Natl Acad Sci USA 101: 3498-3503.
4. Li JL, Hayden MR, Warby SC, Durr A, Morrison PJ, et al. (2006) Genome-wide significance for a modifier of age at neurological onset in Huntington's disease at 6q23-24: the HD MAPS study. BMC Med Genet 7: 71.
5. Andresen JM, Gayán J, Djousse L, Roberts S, Brocklebank D, et al. (2007) The relationship between CAG repeat length and age of onset differs for Huntington's disease patients with juvenile onset or adult onset. Ann Hum Genet 71: 295-301.
6. Telenius H, Kremer B, Goldberg YP, Theilmann J, Andrew SE, et al. (1994) Somatic and gonadal mosaicism of the Huntington disease gene CAG repeat in brain and sperm. Nat Genet 6: 409-414.
7. Aronin N, Chase K, Young C, Sapp E, Schwarz C, et al. (1995) CAG expansion affects the expression of mutant Huntingtin in Huntington's disease brain. Neuron 15: 1193-1201.
8. Kono Y, Agawa Y, Watanabe Y, Ohama E, Nanba E, et al. (1999) Analysis of the CAG repeat number in a patient with Huntington's disease. Intern Med 38: 407-411.
9. Kennedy L, Evans E, Chen CM, Craven L, Detloff PJ, et al. (2003) Dramatic tissue-specific mutation length increases are an early molecular event in Huntington disease pathogenesis. Hum Mol Genet 12: 3359-3367.
10. Shelbourne PF, Keller-McGandy C, Bi WL, Yoon SR, Dubeau L, et al. (2007) Triplet repeat mutation length gains correlate with cell-type specific vulnerability in Huntington disease brain. Hum Mol Genet 16: 1133-1142.
11. Mangiarini L, Sathasivam K, Mahal A, Mott R, Seller M, et al. (1997) Instability of highly expanded CAG repeats in mice transgenic for the Huntington's disease mutation. Nat Genet 15: 197-200.
12. Wheeler VC, Auerbach W, White JK, Srinidhi J, Auerbach A, et al. (1999) Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum Mol Genet 8: 115-122.
13. Kennedy L, Shelbourne PF, (2000) Dramatic mutation instability in HD mouse striatum: does polyglutamine load contribute to cell-specific vulnerability in Huntington's disease? Hum Mol Genet 9: 2539-2544.
14. Wheeler VC, Lebel LA, Vrbanac V, Teed A, te Riele H, et al. (2003) Mismatch repair gene Msh2 modifies the timing of early disease in Hdh(Q111) striatum. Hum Mol Genet 12: 272-281.
15. Gonitel R, Moffitt H, Sathasivam K, Woodman B, Detloff PJ, et al. (2008) DNA instability in postmitotic neurons. Proc Natl Acad Sci USA 105: 3467-3472.
16. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, et al. (1996) Exon 1 of the HD gene with an expended CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87: 493-506.
17. Morton AJ, Glynn D, Leavens W, Zheng Z, Faull RL, et al. (2009) Paradoxical delay in the onset of disease caused by super-long CAG repeat expansions in R6/2 mice. Neurobiol Dis 33: 331-341.
18. Dragatsis I, Goldowitz D, Del Mar N, Deng YP, Meade CA, et al. (2009) CAG repeat lengths ≥335 attenuate the phenotype in the R6/2 Huntington's disease transgenic mouse. Neurobiol Dis 33: 315-330.
19. Dixon KT, Cearley JA, Hunter JM, Detloff PJ, (2004) Mouse Huntington's disease homolog mRNA levels: variation and allele effects. Gene Expr 11: 221-231.
20. Sinden R, Potaman VN, Oussatcheva EA, Pearson CE, Lyubchenko, YL, et al. (2002) Triplet repeat DNA structures and human genetic disease: dynamic mutations from dynamic DNA. J Biosci 27: 53-65.
21. Pearson CE, Sinden RR, (1996) Alternative structures in duplex DNA formed within the trinucleotide repeats of the myotonic dystrophy and fragile X loci. Biochemistry 35: 5041-5053.
22. Pearson CE, Wang Y-H, Griffith JD, Sinden RR, (1998) Structural analysis of slipped-strand DNA (S-DNA) formed in (CTG)n•(CAG)n repeats from the myotonic dystrophy locus. Nucleic Acids Res 26: 816-823.
23. Pearson CE, Tam M, Wang Y-H, Montgomery SE, Dar AC, et al. (2002) Slipped-strand DNAs formed by long (CAG)•(CAG) repeats: slipped-out repeats and slip-out junctions. Nucleic Acids Res 30: 4534-4547.
24. Crampton N, Roes S, Dryden DTF, Rao DN, Edwardson JM, et al. (2007) DNA looping and translocation provide an optimal cleavage mechanism for the type III restriction enzymes. EMBO J 26: 3815-3825.
25. Neaves KJ, Cooper LP, White JH, Carnally SM, Dryden DTF, et al. (2009) Atomic force microscopy of the EcoKI type I DNA restriction enzyme bound to DNA shows enzyme dimerisation and DNA looping. Nucleic Acids Res 37: 2053-2063.
26. Neaves KJ, Huppert JL, Henderson RM, Edwardson JM, (2009) Direct visualization of G-quadruplexes in DNA using atomic force microscopy. Nucleic Acids Res 37: 6269-6275.
27. Duquette ML, Handa P, Vincent JA, Taylor AF, Maizels N, (2007) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Devel 18: 1618-1629.
28. Potaman VN, Oussatcheva EA, Lyubchenko YL, Shlyakhtenko LS, Bidichandani SI, et al. (2004) Length-dependent structure formation in Friedreich ataxia (GAA)n•(TTC)n repeats at neutral pH. Nucleic Acids Res 32: 1224-1131.
29. Morton AJ, Lagan MA, Skepper JN, Dunnett SB, (2000) Progressive formation of inclusions in the striatum and hippocampus of mice transgenic for the human Huntington's disease mutation. J Neurocytol 29: 679-702.
30. Wheeler VC, Auerbach W, White JK, Srinidhi J, Auerbach A, et al. (1999) Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum Mol Genet 8: 115-122.
31. Milunsky JM, Maher TA, Loose BA, Darras BT, Ito M, et al. (2003) XL PCR for the detection of large trinucleotide expansions in juvenile Huntington's disease. Clin Genet 64: 70-73.
32. Nørremølle A, Hasholt L, Petersen CB, Eiberg H, Hasselbalch SG, et al. (2004) Mosaicism of the CAG repeat sequence in the Huntington disease gene in a pair of monozygotic twins. Am J Med Genet 130A: 154-159.
33. Mutter GL, Boynton KA, (1995) PCR bias in amplification of androgen receptor alleles, a trinucleotide repeat marker used in clonality studies. Nucleic Acids Res 23: 1411-1418.
34. Poirier J, Ohshima K, Pandolfo M, (1999) Heteroduplexes may confuse the interpretation of PCR-based molecular tests for the Friedreich ataxia GAA triplet repeat. Hum Mut 13: 328-330.
35. Hamon L, Pastré D, Dupaigne P, Le Breton C, Le Cam E, et al. (2007) High-resolution AFM imaging of a single-stranded DNA-binding (SSB) protein-DNA complexes. Nucleic Acids Res 35: e58.
36. Carnally SM, Johannessen M, Henderson RM, Jackson MB, Edwardson JM, (2010) Demonstration of a direct interaction between σ-1 receptors and acid-sensing ion channels. Biophys J 98: 1182-1191.
37. Meisel A, Bickel TA, Krüger DH, Schroeder C, (1992) Type-III restriction enzymes need 2 inversely oriented sites for DNA cleavage. Nature 355: 467-469.
38. Meisel A, Mackeldanz P, Bickel TA, Krüger DH, Schroeder C, (1995) Type-III restriction endonucleases translocate DNA in a reaction driven by recognition site-specific ATP hydrolysis. EMBO J 14: 2958-2966.
39. Möncke-Buchner E, Reich S, Mücke M, Reuter M, Messer W, et al. (2002) Counting CAG repeats in the Huntington's disease gene by restriction endonuclease EcoP15I cleavage. Nucleic Acids Res 30: e83.
40. Kienberger F, Kada G, Mueller H, Hinterdorfer P, (2005) Single molecule studies of antibody-antigen interaction strength versus intra-molecular antigen stability. J Mol Biol 347: 597-606.
41. Allen S, Davies J, Dawkes AC, Davies MC, Edwards JC, et al. (1996) In situ observation of streptavidin-biotin binding on an immunoassay well surface using an atomic force microscope. FEBS Lett 390: 161-164.
42. Baldi P, Brunak S, Chauvin Y, Pedersen AG, (1999) Structural basis for triplet repeat disorders: a computational analysis. Bioinformatics 15: 918-929.
43. Chastain PD, Sinden RR, (1998) CTG repeats associated with human genetic disease are inherently flexible. J Mol Biol 275: 405-411.
44. Atwal RS, Xia J, Pinchev D, Taylor J, Epand RM, et al. (2007) Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity. Hum Mol Genet 16: 2600-2615.
45. Peters MF, Nucifora FC Jr, Kushi J, Seaman HC, Cooper JK, et al. (1999) Nuclear targeting of mutant Huntingtin increases toxicity. Mol Cell Neurosci 14: 121-128.
46. Schilling G, Savonenko AV, Klevytska A, Morton JL, Tucker SM, et al. (2004) Nuclear-targeting of mutant huntingtin fragments produces Huntington's disease-like phenotypes in transgenic mice. Hum Mol Genet 13: 1599-1610.
47. Benn CL, Landles C, Li H, Strand AD, Woodman B, et al. (2005) Contribution of nuclear and extranuclear polyQ to neurological phenotypes in mouse models of Huntington's disease. Hum Mol Gen: 14: 3065-3078.
48. Bochtler M, Szczepanowski RH, Tamulaitis G, Grazulis S, Czapinska H, et al. (2006) Nucleotide flips determine the specificity of the Ecl18kI restriction endonuclease. EMBO J 25: 2219-2229.
49. Janscak P, MacWilliams MP, Sandmeier U, Nagaraja V, Bickle TA, (1999) DNA translocation blockage, a general mechanism of cleavage site selection by type I restriction enzymes. EMBO J 18: 2638-2647.
50. Reddy YVR, Rao DN, (2000) Binding of EcoP15I DNA methyltransferase to DNA reveals a large structural distortion within the recognition sequence. J Mol Biol 298: 597-610.
51. Pearson CE, Nichol Edamura K, Cleary JD, (2005) Repeat instability: mechanisms of dynamic mutations. Nat Rev Genet 6: 729-742.
52. Kovtun IV, McMurray CT, (2008) Features of trinucleotide repeat instability in vivo. Cell Res 18: 198-213.
53. Wang YH, (2007) Chromatin structure of repeating CTG/CAG and CGG/CCG sequences in human disease. Front Biosci 12: 4731-4741.