Non-B DNA structure-induced genetic instability and evolution

Cellular and Molecular Life Sciences

Volumn 67, Issue 1, 2010, Pages 43-62

  Zhao, Junhua ^a   Bacolla, Albino ^a   Wang, Guliang ^a   Vasquez, Karen M ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Evolutionary change; Gene regulation; Genomic instability; Non B DNA structures; Repetitive sequences

Indexed keywords

CRUCIFORM DNA; DNA; DNA B; DNA PRIMASE; DNA Z; ORIGIN RECOGNITION COMPLEX;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; CROSS LINKING; DNA HELIX; DNA MODIFICATION; DNA REPLICATION; DNA SEQUENCE; DNA STRAND; DNA STRAND BREAKAGE; DNA STRUCTURE; ESCHERICHIA COLI; GENE; GENE CONTROL; GENE DELETION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC STABILITY; GENETIC TRANSCRIPTION; GENOME; HUMAN; HUMAN GENOME; INVERTED REPEAT; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE REPEAT; REVIEW; Y CHROMOSOME; YEAST;

CHROMOSOMES, HUMAN, Y; DNA; DNA REPAIR; DNA, CRUCIFORM; EVOLUTION, MOLECULAR; GENOMIC INSTABILITY; HUMANS; NUCLEIC ACID CONFORMATION;

EUKARYOTA; PROKARYOTA;

EID: 73749085274     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0131-2     Document Type: Review

References (164)

1. JD Watson FH Crick 1953 Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid Nature 171 737 738 1:CAS:528:DyaG2cXivVGktA%3D%3D 13054692
2. SM Mirkin 2008 Discovery of alternative DNA structures: a heroic decade (1979-1989) Front Biosci 13 1064 1071 1:CAS:528:DC%2BD1cXhs1Churc%3D 17981612
3. G Felsenfeld DR Davies A Rich 1957 Formation of a three-stranded polynucleotide molecule J Am Chem Soc 79 2023 2024 1:CAS:528: DyaG2sXms12ruw%3D%3D
4. AH Wang GJ Quigley FJ Kolpak JL Crawford JH van Boom G van der Marel A Rich 1979 Molecular structure of a left-handed double helical DNA fragment at atomic resolution Nature 282 680 686 1:CAS:528:DyaL3cXhsF2is7k%3D 514347
5. DM Lilley 1980 The inverted repeat as a recognizable structural feature in supercoiled DNA molecules Proc Natl Acad Sci USA 77 6468 6472 1:CAS:528:DyaL3MXis1eitA%3D%3D 6256738
6. N Panayotatos RD Wells 1981 Cruciform structures in supercoiled DNA Nature 289 466 470 1:CAS:528:DyaL3MXhvVOjuro%3D 7464915
7. VI Lyamichev IG Panyutin MD Frank-Kamenetskii 1983 Evidence of cruciform structures in superhelical DNA provided by two-dimensional gel electrophoresis FEBS Lett 153 298 302 1:CAS:528:DyaL3sXhslGjtL0%3D 6352326
8. D Sen W Gilbert 1988 Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis Nature 334 364 366 1:CAS:528:DyaL1cXls1GrsLk%3D 3393228
9. A Bacolla RD Wells 2004 Non-B DNA conformations, genomic rearrangements, and human disease J Biol Chem 279 47411 47414 1:CAS:528:DC%2BD2cXptl2gt7Y%3D 15326170
10. A Bacolla A Jaworski JE Larson JP Jakupciak N Chuzhanova SS Abeysinghe CD O'Connell DN Cooper RD Wells 2004 Breakpoints of gross deletions coincide with non-B DNA conformations Proc Natl Acad Sci USA 101 14162 14167 1:CAS:528:DC%2BD2cXosVylsb4%3D 15377784
11. G Wang KM Vasquez 2006 Non-B DNA structure-induced genetic instability Mutat Res 598 103 119 1:CAS:528:DC%2BD28XlsFGkt7s%3D 16516932
12. G Wang KM Vasquez 2004 Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells Proc Natl Acad Sci USA 101 13448 13453 1:CAS:528:DC%2BD2cXnvFeiur0%3D 15342911
13. BW Glickman LS Ripley 1984 Structural intermediates of deletion mutagenesis: a role for palindromic DNA Proc Natl Acad Sci USA 81 512 516 1:CAS:528:DyaL2cXhtlemtbk%3D 6582506
14. HT Orr HY Zoghbi 2007 Trinucleotide repeat disorders Annu Rev Neurosci 30 575 621 1:CAS:528:DC%2BD2sXptFKnu70%3D 17417937
15. SM Mirkin 2007 Expandable DNA repeats and human disease Nature 447 932 940 1:CAS:528:DC%2BD2sXms12jsrc%3D 17581576
16. RS Lahue DL Slater 2003 DNA repair and trinucleotide repeat instability Front Biosci 8 s653 s665 1:CAS:528:DC%2BD3sXjvVChurc%3D 12700078
17. RD Wells R Dere ML Hebert M Napierala LS Son 2005 Advances in mechanisms of genetic instability related to hereditary neurological diseases Nucleic Acids Res 33 3785 3798 1:CAS:528:DC%2BD2MXmsV2hsLc%3D 16006624
18. G Wang LA Christensen KM Vasquez 2006 Z-DNA-forming sequences generate large-scale deletions in mammalian cells Proc Natl Acad Sci USA 103 2677 2682 1:CAS:528:DC%2BD28XksF2rtr8%3D 16473937
19. M Adachi Y Tsujimoto 1990 Potential Z-DNA elements surround the breakpoints of chromosome translocation within the 5-flanking region of bcl-2 gene Oncogene 5 1653 1657 1:CAS:528:DyaK3MXls1KktA%3D%3D 2176281
20. SC Raghavan MR Lieber 2004 Chromosomal translocations and non-B DNA structures in the human genome Cell Cycle 3 762 768 1:CAS:528: DC%2BD2MXmtVCmsg%3D%3D 15254430
21. SC Raghavan P Chastain JS Lee BG Hegde S Houston R Langen CL Hsieh IS Haworth MR Lieber 2005 Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation J Biol Chem 280 22749 22760 1:CAS:528:DC%2BD2MXltVyhtr4%3D 15840562
22. SC Raghavan MR Lieber 2006 DNA structures at chromosomal translocation sites Bioessays 28 480 494 1:CAS:528:DC%2BD28XkvVyjs7g%3D 16615081
23. G Wang S Carbajal J Vijg J DiGiovanni KM Vasquez 2008 DNA structure-induced genomic instability in vivo J Natl Cancer Inst 100 1815 1817 1:CAS:528:DC%2BD1MXhtVGksQ%3D%3D 19066276
24. T Kato H Inagaki K Yamada H Kogo T Ohye H Kowa K Nagaoka M Taniguchi BS Emanuel H Kurahashi 2006 Genetic variation affects de novo translocation frequency Science 311 971 1:CAS:528:DC%2BD28Xhs1WisLc%3D 16484486
25. H Inagaki T Ohye H Kogo T Kato H Bolor M Taniguchi TH Shaikh BS Emanuel H Kurahashi 2009 Chromosomal instability mediated by non-B DNA: cruciform conformation and not DNA sequence is responsible for recurrent translocation in humans Genome Res 19 191 198 1:CAS:528:DC%2BD1MXhvVSjurY%3D 18997000
26. BS Emanuel 2008 Molecular mechanisms and diagnosis of chromosome 22q11.2 rearrangements Dev Disabil Res Rev 14 11 18 18636632
27. H Kurahashi H Inagaki T Ohye H Kogo T Kato BS Emanuel 2006 Palindrome-mediated chromosomal translocations in humans DNA Repair (Amst) 5 1136 1145 1:CAS:528:DC%2BD28XptFSrtrs%3D
28. AL Gotter TH Shaikh ML Budarf CH Rhodes BS Emanuel 2004 A palindrome-mediated mechanism distinguishes translocations involving LCR-B of chromosome 22q11.2 Hum Mol Genet 13 103 115 1:CAS:528:DC%2BD3sXhtVSjsrfE 14613967
29. A Bacolla RD Wells 2009 Non-B DNA conformations as determinants of mutagenesis and human disease Mol Carcinog 48 273 285 1:CAS:528: DC%2BD1MXksVKku78%3D 19306308
30. GR Smith 2008 Meeting DNA palindromes head-to-head Genes Dev 22 2612 2620 1:CAS:528:DC%2BD1cXht1ClsbrL 18832065
31. J Watson FA Hays PS Ho 2004 Definitions and analysis of DNA Holliday junction geometry Nucleic Acids Res 32 3017 3027 1:CAS:528:DC%2BD2cXltVWls7g%3D 15173384
32. RR Sinden DE Pettijohn 1984 Cruciform transitions in DNA J Biol Chem 259 6593 6600 1:CAS:528:DyaL2cXktF2hsbg%3D 6373762
33. EA Oussatcheva J Pavlicek OF Sankey RR Sinden YL Lyubchenko VN Potaman 2004 Influence of global DNA topology on cruciform formation in supercoiled DNA J Mol Biol 338 735 743 1:CAS:528:DC%2BD2cXjtFOhu7o%3D 15099741
34. DK Nag TD Petes 1991 Seven-base-pair inverted repeats in DNA form stable hairpins in vivo in Saccharomyces cerevisiae Genetics 129 669 673 1:CAS:528:DyaK38XhtVSntrw%3D 1752412
35. ES Lander LM Linton B Birren C Nusbaum MC Zody J Baldwin K Devon K Dewar M Doyle W FitzHugh R Funke D Gage K Harris A Heaford J Howland L Kann J Lehoczky R LeVine P McEwan K McKernan J Meldrim JP Mesirov C Miranda W Morris J Naylor C Raymond M Rosetti R Santos A Sheridan C Sougnez N Stange-Thomann N Stojanovic A Subramanian D Wyman J Rogers J Sulston R Ainscough S Beck D Bentley J Burton C Clee N Carter A Coulson R Deadman P Deloukas A Dunham I Dunham R Durbin L French D Grafham S Gregory T Hubbard S Humphray A Hunt M Jones C Lloyd A McMurray L Matthews S Mercer S Milne JC Mullikin A Mungall R Plumb M Ross R Shownkeen S Sims RH Waterston RK Wilson LW Hillier JD McPherson MA Marra ER Mardis LA Fulton AT Chinwalla KH Pepin WR Gish SL Chissoe MC Wendl KD Delehaunty TL Miner A Delehaunty JB Kramer LL Cook RS Fulton DL Johnson PJ Minx SW Clifton T Hawkins E Branscomb P Predki P Richardson S Wenning T Slezak N Doggett JF Cheng A Olsen S Lucas C Elkin E Uberbacher M Frazier RA Gibbs DM Muzny SE Scherer JB Bouck EJ Sodergren KC Worley CM Rives JH Gorrell ML Metzker SL Naylor RS Kucherlapati DL Nelson GM Weinstock Y Sakaki A Fujiyama M Hattori T Yada A Toyoda T Itoh C Kawagoe H Watanabe Y Totoki T Taylor J Weissenbach R Heilig W Saurin F Artiguenave P Brottier T Bruls E Pelletier C Robert P Wincker DR Smith L Doucette-Stamm M Rubenfield K Weinstock HM Lee J Dubois A Rosenthal M Platzer G Nyakatura S Taudien A Rump H Yang J Yu J Wang G Huang J Gu L Hood L Rowen A Madan S Qin RW Davis NA Federspiel AP Abola MJ Proctor RM Myers J Schmutz M Dickson J Grimwood DR Cox MV Olson R Kaul C Raymond N Shimizu K Kawasaki S Minoshima GA Evans M Athanasiou R Schultz BA Roe F Chen H Pan J Ramser H Lehrach R Reinhardt WR McCombie M de la Bastide N Dedhia H Blocker K Hornischer G Nordsiek R Agarwala L Aravind JA Bailey A Bateman S Batzoglou E Birney P Bork DG Brown CB Burge L Cerutti HC Chen D Church M Clamp RR Copley T Doerks SR Eddy EE Eichler TS Furey J Galagan JG Gilbert C Harmon Y Hayashizaki D Haussler H Hermjakob K Hokamp W Jang LS Johnson TA Jones S Kasif A Kaspryzk S Kennedy WJ Kent P Kitts EV Koonin I Korf D Kulp D Lancet TM Lowe A McLysaght T Mikkelsen JV Moran N Mulder VJ Pollara CP Ponting G Schuler J Schultz G Slater AF Smit E Stupka J Szustakowski D Thierry-Mieg J Thierry-Mieg L Wagner J Wallis R Wheeler A Williams YI Wolf KH Wolfe SP Yang RF Yeh F Collins MS Guyer J Peterson A Felsenfeld KA Wetterstrand A Patrinos MJ Morgan P de Jong JJ Catanese K Osoegawa H Shizuya S Choi YJ Chen 2001 Initial sequencing and analysis of the human genome Nature 409 860 921 1:CAS:528:DC%2BD3MXhsFCjtLc%3D 11237011
36. SC Harvey 1983 DNA structural dynamics: longitudinal breathing as a possible mechanism for the B in equilibrium Z transition Nucleic Acids Res 11 4867 4878 1:CAS:528:DyaL3sXltVWju7w%3D 6878036
37. n DNA sequences from right- to left-handed helical structure by salt, Co(III), or negative supercoiling Proc Natl Acad Sci USA 79 4560 4564 1:CAS:528:DyaL38XlsVSns70%3D 6956879
38. CK Singleton J Klysik SM Stirdivant RD Wells 1982 Left-handed Z-DNA is induced by supercoiling in physiological ionic conditions Nature 299 312 316 1:CAS:528:DyaL3sXkvVyltg%3D%3D 6287292
39. SC Ha K Lowenhaupt A Rich YG Kim KK Kim 2005 Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases Nature 437 1183 1186 1:CAS:528:DC%2BD2MXhtFahtL%2FE 16237447
40. H Htun JE Dahlberg 1988 Single strands, triple strands, and kinks in H-DNA Science 241 1791 1796 1:CAS:528:DyaL1MXjtFCi 3175620
41. RD Wells 1988 Unusual DNA structures J Biol Chem 263 1095 1098 1:CAS:528:DyaL1cXht1Kktr8%3D 3275663
42. A Jain G Wang KM Vasquez 2008 DNA triple helices: biological consequences and therapeutic potential Biochimie 90 1117 1130 1:CAS:528:DC%2BD1cXptVWltrc%3D 18331847
43. A Majumdar DJ Patel 2002 Identifying hydrogen bond alignments in multistranded DNA architectures by NMR Acc Chem Res 35 1 11 1:CAS:528: DC%2BD3MXptFyisr8%3D 11790083
44. RR Sinden MJ Pytlos-Sinden VN Potaman 2007 Slipped strand DNA structures Front Biosci 12 4788 4799 1:CAS:528:DC%2BD2sXosF2rur4%3D 17569609
45. SH Chou KH Chin AH Wang 2003 Unusual DNA duplex and hairpin motifs Nucleic Acids Res 31 2461 2474 1:CAS:528:DC%2BD3sXjslWhtbc%3D 12736295
46. G Wang J Zhao KM Vasquez 2009 Methods to determine DNA structural alterations and genetic instability Methods 48 54 62 1:CAS:528: DC%2BD1MXmsVCltbY%3D 19245837
47. CE Pearson EE Eichler D Lorenzetti SF Kramer HY Zoghbi DL Nelson RR Sinden 1998 Interruptions in the triplet repeats of SCA1 and FRAXA reduce the propensity and complexity of slipped strand DNA (S-DNA) formation Biochemistry 37 2701 2708 1:CAS:528:DyaK1cXotFGqsw%3D%3D 9485421
48. CT Caskey A Pizzuti YH Fu RG Fenwick Jr DL Nelson 1992 Triplet repeat mutations in human disease Science 256 784 789 1:CAS:528:DyaK38XktVGitL8%3D 1589758
49. CS Benton R de Silva SL Rutledge S Bohlega T Ashizawa HY Zoghbi 1998 Molecular and clinical studies in SCA-7 define a broad clinical spectrum and the infantile phenotype Neurology 51 1081 1086 1:STN:280:DyaK1cvlt1OqsQ%3D%3D 9781533
50. E Palecek 1991 Local supercoil-stabilized DNA structures Crit Rev Biochem Mol Biol 26 151 226 1:CAS:528:DyaK3MXlsFehs74%3D 1914495
51. GP Schroth PS Ho 1995 Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA Nucleic Acids Res 23 1977 1983 1:CAS:528: DyaK2MXms1eksbg%3D 7596826
52. EM Lafer A Moller A Nordheim BD Stollar A Rich 1981 Antibodies specific for left-handed Z-DNA Proc Natl Acad Sci USA 78 3546 3550 1:CAS:528: DyaL3MXkslyhtL0%3D 6943554
53. A Nordheim ML Pardue EM Lafer A Moller BD Stollar A Rich 1981 Antibodies to left-handed Z-DNA bind to interband regions of Drosophila polytene chromosomes Nature 294 417 422 1:CAS:528:DyaL38Xhtlyhs7s%3D 6796893
54. A Nordheim EM Lafer LJ Peck JC Wang BD Stollar A Rich 1982 Negatively supercoiled plasmids contain left-handed Z-DNA segments as detected by specific antibody binding Cell 31 309 318 1:CAS:528:DyaL3sXivFyrsg%3D%3D 7159926
55. EM Lafer R Sousa R Ali A Rich BD Stollar 1986 The effect of anti-Z-DNA antibodies on the B-DNA-Z-DNA equilibrium J Biol Chem 261 6438 6443 1:CAS:528:DyaL28XktVaqsbg%3D 3700399
56. YM Agazie JS Lee GD Burkholder 1994 Characterization of a new monoclonal antibody to triplex DNA and immunofluorescent staining of mammalian chromosomes J Biol Chem 269 7019 7023 1:CAS:528:DyaK2cXjtF2qur0%3D 7509814
57. JS Lee GD Burkholder LJ Latimer BL Haug RP Braun 1987 A monoclonal antibody to triplex DNA binds to eucaryotic chromosomes Nucleic Acids Res 15 1047 1061 1:CAS:528:DyaL2sXhslCgsr8%3D 2434928
58. YM Agazie GD Burkholder JS Lee 1996 Triplex DNA in the nucleus: direct binding of triplex-specific antibodies and their effect on transcription, replication and cell growth Biochem J 316 Pt 2 461 466 1:CAS:528: DyaK28XjvVahtrs%3D 8687388
59. M Ohno T Fukagawa JS Lee T Ikemura 2002 Triplex-forming DNAs in the human interphase nucleus visualized in situ by polypurine/polypyrimidine DNA probes and antitriplex antibodies Chromosoma 111 201 213 1:CAS:528:DC%2BD38XntlOmtbo%3D 12355210
60. JC Brown BA Brown 2nd Y Li CC Hardin 1998 Construction and characterization of a quadruplex DNA selective single-chain autoantibody from a viable motheaten mouse hybridoma with homology to telomeric DNA binding proteins Biochemistry 37 16338 16348 1:CAS:528:DyaK1cXmvFCitrs%3D 9819226
61. BA Brown 2nd Y Li JC Brown CC Hardin JF Roberts SC Pelsue LD Shultz 1998 Isolation and characterization of a monoclonal anti-quadruplex DNA antibody from autoimmune "viable motheaten" mice Biochemistry 37 16325 16337 1:CAS:528:DyaK1cXmvFCitr0%3D 9819225
62. C Schaffitzel I Berger J Postberg J Hanes HJ Lipps A Pluckthun 2001 In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei Proc Natl Acad Sci USA 98 8572 8577 1:CAS:528:DC%2BD3MXls1Witr4%3D 11438689
63. L Frappier GB Price RG Martin M Zannis-Hadjopoulos 1989 Characterization of the binding specificity of two anticruciform DNA monoclonal antibodies J Biol Chem 264 334 341 1:CAS:528:DyaL1MXltlWhsQ%3D%3D 2462559
64. Sinden RR (1994) Cruciform structures in DNA and triplex DNA in DNA structure and function. Academic, San Diego, pp 160-164 (see also pp 241-242)
65. SC Raghavan A Tsai CL Hsieh MR Lieber 2006 Analysis of non-B DNA structure at chromosomal sites in the mammalian genome Methods Enzymol 409 301 316 1:CAS:528:DC%2BD2sXmt1Ghsro%3D 16793408
66. R Cox SM Mirkin 1997 Characteristic enrichment of DNA repeats in different genomes Proc Natl Acad Sci USA 94 5237 5242 1:STN:280: DyaK2s3ovFOmsg%3D%3D 9144221
67. S Repping H Skaletsky J Lange S Silber F Van Der Veen RD Oates DC Page S Rozen 2002 Recombination between palindromes P5 and P1 on the human Y chromosome causes massive deletions and spermatogenic failure Am J Hum Genet 71 906 922 12297986
68. KS Lobachev A Rattray V Narayanan 2007 Hairpin- and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells Front Biosci 12 4208 4220 1:CAS:528:DC%2BD2sXms1KlsL4%3D 17485368
69. PE Warburton J Giordano F Cheung Y Gelfand G Benson 2004 Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes Genome Res 14 1861 1869 1:CAS:528:DC%2BD2cXotl2hurY%3D 15466286
70. P Khuu M Sandor J DeYoung PS Ho 2007 Phylogenomic analysis of the emergence of GC-rich transcription elements Proc Natl Acad Sci USA 104 16528 16533 1:CAS:528:DC%2BD2sXht1WhtbnO 17925442
71. A Nordheim A Rich 1983 Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequences Nature 303 674 679 1:CAS:528:DyaL3sXksV2isrY%3D 6304535
72. DB Oh YG Kim A Rich 2002 Z-DNA-binding proteins can act as potent effectors of gene expression in vivo Proc Natl Acad Sci USA 99 16666 16671 1:CAS:528:DC%2BD3sXhvV2jtw%3D%3D 12486233
73. B Wong S Chen JA Kwon A Rich 2007 Characterization of Z-DNA as a nucleosome-boundary element in yeast Saccharomyces cerevisiae Proc Natl Acad Sci USA 104 2229 2234 1:CAS:528:DC%2BD2sXisVWrsbw%3D 17284586
74. A Bacolla JR Collins B Gold N Chuzhanova M Yi RM Stephens S Stefanov A Olsh JP Jakupciak M Dean RA Lempicki DN Cooper RD Wells 2006 Long homopurine*homopyrimidine sequences are characteristic of genes expressed in brain and the pseudoautosomal region Nucleic Acids Res 34 2663 2675 1:CAS:528:DC%2BD28XmsVeiuro%3D 16714445
75. AK Todd M Johnston S Neidle 2005 Highly prevalent putative quadruplex sequence motifs in human DNA Nucleic Acids Res 33 2901 2907 1:CAS:528: DC%2BD2MXkvVSgsrw%3D 15914666 (Pubitemid 41511229)
76. JL Huppert S Balasubramanian 2005 Prevalence of quadruplexes in the human genome Nucleic Acids Res 33 2908 2916 1:CAS:528:DC%2BD2MXkvVSgsL0%3D 15914667
77. WI Sundquist A Klug 1989 Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops Nature 342 825 829 1:CAS:528:DyaK3cXpsVSqtg%3D%3D 2601741
78. JR Williamson MK Raghuraman TR Cech 1989 Monovalent cation-induced structure of telomeric DNA: the G-quartet model Cell 59 871 880 1:CAS:528:DyaK3cXhtFCgsLo%3D 2590943
79. n strand Nucleic Acids Res 17 8257 8271 1:CAS:528:DyaK3cXjt1amsw%3D%3D 2554253
80. JL Huppert S Balasubramanian 2007 G-quadruplexes in promoters throughout the human genome Nucleic Acids Res 35 406 413 1:CAS:528:DC%2BD2sXhtlOls74%3D 17169996
81. Z Du Y Zhao N Li 2008 Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription Genome Res 18 233 241 1:CAS:528:DC%2BD1cXhvVSrsbs%3D 18096746
82. Z Du P Kong Y Gao N Li 2007 Enrichment of G4 DNA motif in transcriptional regulatory region of chicken genome Biochem Biophys Res Commun 354 1067 1070 1:CAS:528:DC%2BD2sXhs1SnsLs%3D 17275786
83. JL Huppert A Bugaut S Kumari S Balasubramanian 2008 G-quadruplexes: the beginning and end of UTRs Nucleic Acids Res 36 6260 6268 1:CAS:528: DC%2BD1cXhtlGgs7zP 18832370
84. D Sen W Gilbert 1990 A sodium-potassium switch in the formation of four-stranded G4-DNA Nature 344 410 414 1:CAS:528:DyaK3cXitlWnsL4%3D 2320109
85. RK Moyzis DC Torney J Meyne JM Buckingham JR Wu C Burks KM Sirotkin WB Goad 1989 The distribution of interspersed repetitive DNA sequences in the human genome Genomics 4 273 289 1:CAS:528:DyaL1MXktVWrtLY%3D 2714792
86. RL Stallings DC Torney CE Hildebrand JL Longmire LL Deaven JH Jett NA Doggett RK Moyzis 1990 Physical mapping of human chromosomes by repetitive sequence fingerprinting Proc Natl Acad Sci USA 87 6218 6222 1:CAS:528: DyaK3cXlsVKksrk%3D 2385591
87. TG Krontiris 1995 Minisatellites and human disease Science 269 1682 1683 1:CAS:528:DyaK2MXot1aisbg%3D 7569893
88. A Bacolla M Wojciechowska B Kosmider JE Larson RD Wells 2006 The involvement of non-B DNA structures in gross chromosomal rearrangements DNA Repair (Amst) 5 1161 1170 1:CAS:528:DC%2BD28XptFSrtrk%3D
89. A Bacolla JE Larson JR Collins J Li A Milosavljevic PD Stenson DN Cooper RD Wells 2008 Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties Genome Res 18 1545 1553 1:CAS:528:DC%2BD1cXht1elu77K 18687880
90. International Human Genome Sequencing Consortium 2004 Finishing the euchromatic sequence of the human genome Nature 431 931 945
91. EE Eichler RA Clark X She 2004 An assessment of the sequence gaps: unfinished business in a finished human genome Nat Rev Genet 5 345 354 1:CAS:528:DC%2BD2cXjsl2iu7w%3D 15143317
92. S Repping SK van Daalen LG Brown CM Korver J Lange JD Marszalek T Pyntikova F van der Veen H Skaletsky DC Page S Rozen 2006 High mutation rates have driven extensive structural polymorphism among human Y chromosomes Nat Genet 38 463 467 1:CAS:528:DC%2BD28XivFSht7s%3D 16501575
93. W Huang da BT Sherman RA Lempicki 2009 Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res 37 1 13 19033363
94. T Walsh JM McClellan SE McCarthy AM Addington SB Pierce GM Cooper AS Nord M Kusenda D Malhotra A Bhandari SM Stray CF Rippey P Roccanova V Makarov B Lakshmi RL Findling L Sikich T Stromberg B Merriman N Gogtay P Butler K Eckstrand L Noory P Gochman R Long Z Chen S Davis C Baker EE Eichler PS Meltzer SF Nelson AB Singleton MK Lee JL Rapoport MC King J Sebat 2008 Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia Science 320 539 543 1:CAS:528:DC%2BD1cXkvFGkt7s%3D 18369103
95. G Venkatasubramanian 2009 Triplex DNA, human evolution and schizophrenia Acta Neuropsychiatr 21 100 101
96. MM Alba R Guigo 2004 Comparative analysis of amino acid repeats in rodents and humans Genome Res 14 549 554 1:CAS:528:DC%2BD2cXjt1yjsbk%3D 15059995
97. NG Faux SP Bottomley AM Lesk JA Irving JR Morrison MG de la Banda JC Whisstock 2005 Functional insights from the distribution and role of homopeptide repeat-containing proteins Genome Res 15 537 551 1:CAS:528:DC%2BD2MXjsVahtbg%3D 15805494
98. D Schaafsma SS Roscioni H Meurs M Schmidt 2008 Monomeric G-proteins as signal transducers in airway physiology and pathophysiology Cell Signal 20 1705 1714 1:CAS:528:DC%2BD1cXhtVejt7%2FK 18538541
99. K Burridge K Wennerberg 2004 Rho and Rac take center stage Cell 116 167 179 1:CAS:528:DC%2BD2cXhtValsrs%3D 14744429
100. Y Zhao Z Du N Li 2007 Extensive selection for the enrichment of G4 DNA motifs in transcriptional regulatory regions of warm blooded animals FEBS Lett 581 1951 1956 1:CAS:528:DC%2BD2sXkvFGltbo%3D 17462634
101. P Rawal VB Kummarasetti J Ravindran N Kumar K Halder R Sharma M Mukerji SK Das S Chowdhury 2006 Genome-wide prediction of G4 DNA as regulatory motifs: role in Escherichia coli global regulation Genome Res 16 644 655 1:CAS:528:DC%2BD28XkslCgs78%3D 16651665
102. Y Qin LH Hurley 2008 Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions Biochimie 90 1149 1171 1:CAS:528:DC%2BD1cXptVWlt7s%3D 18355457
103. A Siddiqui-Jain CL Grand DJ Bearss LH Hurley 2002 Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription Proc Natl Acad Sci USA 99 11593 11598 1:CAS:528:DC%2BD38XntFWqsL4%3D 12195017
104. LH Hurley DD Von Hoff A Siddiqui-Jain D Yang 2006 Drug targeting of the c-MYC promoter to repress gene expression via a G-quadruplex silencer element Semin Oncol 33 498 512 1:CAS:528:DC%2BD28XpsVersbY%3D 16890804
105. RJ Aitken JA Marshall Graves 2002 The future of sex Nature 415 963 1:CAS:528:DC%2BD38Xhsl2ltL8%3D 11875544
106. S Rozen H Skaletsky JD Marszalek PJ Minx HS Cordum RH Waterston RK Wilson DC Page 2003 Abundant gene conversion between arms of palindromes in human and ape Y chromosomes Nature 423 873 876 1:CAS:528:DC%2BD3sXks1KmtbY%3D 12815433
107. BK Bhowmick Y Satta N Takahata 2007 The origin and evolution of human ampliconic gene families and ampliconic structure Genome Res 17 441 450 1:CAS:528:DC%2BD2sXktFGnsbo%3D 17185645
108. JF Hughes H Skaletsky T Pyntikova PJ Minx T Graves S Rozen RK Wilson DC Page 2005 Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee Nature 437 100 103 16136134
109. J Kolb NA Chuzhanova J Hogel KM Vasquez DN Cooper A Bacolla H Kehrer-Sawatzki 2009 Cruciform-forming inverted repeats appear to have mediated many of the microinversions that distinguish the human and chimpanzee genomes Chromosome Res 7 469 483
110. FO Losch A Bredenbeck VM Hollstein P Walden P Wrede 2007 Evidence for a large double-cruciform DNA structure on the X chromosome of human and chimpanzee Hum Genet 122 337 343 1:CAS:528:DC%2BD2sXhtFyqsrrI 17638018
111. Kurahashi H, Inagaki H, Kato T, Hosoba E, Kogo H, Ohye T, Tsutsumi M, Bolor H, Tong M, Emanuel BS (2009) Impaired DNA replication prompts deletions within palindromic sequences, but does not induce translocations in human cells. Hum Mol Genet 18:3397-3406
112. RR Sinden O Bat PR Kramer 1999 Psoralen cross-linking as probe of torsional tension and topological domain size in vivo Methods 17 112 124 1:CAS:528:DyaK1MXhvVagtL8%3D 10075890
113. CE Pearson K Nichol Edamura JD Cleary 2005 Repeat instability: mechanisms of dynamic mutations Nat Rev Genet 6 729 742 1:CAS:528:DC%2BD2MXhtVGru77P 16205713
114. EV Mirkin SM Mirkin 2007 Replication fork stalling at natural impediments Microbiol Mol Biol Rev 71 13 35 1:CAS:528:DC%2BD2sXksleqsLg%3D 17347517
115. G Wang KM Vasquez 2009 Models for chromosomal replication-independent non-B DNA structure-induced genetic instability Mol Carcinog 48 286 298 1:CAS:528:DC%2BD1MXksVKku7w%3D 19123200
116. CH Freudenreich 2007 Chromosome fragility: molecular mechanisms and cellular consequences Front Biosci 12 4911 4924 1:CAS:528:DC%2BD2sXosF2qsr4%3D 17569619
117. NS Collins S Bhattacharyya RS Lahue 2007 Rev1 enhances CAG•CTG repeat stability in Saccharomyces cerevisiae DNA Repair (Amst) 6 38 44 1:CAS:528:DC%2BD2sXhsFGktQ%3D%3D
118. I Voineagu V Narayanan KS Lobachev SM Mirkin 2008 Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins Proc Natl Acad Sci USA 105 9936 9941 1:CAS:528:DC%2BD1cXptFGitbg%3D 18632578
119. H Zhang CH Freudenreich 2007 An AT-rich sequence in human common fragile site FRA16D causes fork stalling and chromosome breakage in S. cerevisiae Mol Cell 27 367 379 17679088
120. BS Balakumaran CH Freudenreich VA Zakian 2000 CGG/CCG repeats exhibit orientation-dependent instability and orientation-independent fragility in Saccharomyces cerevisiae Hum Mol Genet 9 93 100 1:CAS:528:DC%2BD3cXmt1eqsw%3D%3D 10587583
121. GB Panigrahi JD Cleary CE Pearson 2002 In vitro (CTG)*(CAG) expansions and deletions by human cell extracts J Biol Chem 277 13926 13934 1:CAS:528:DC%2BD38XjsFWnsbY%3D 11832482
122. S Kang A Jaworski K Ohshima RD Wells 1995 Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E. coli Nat Genet 10 213 218 1:CAS:528:DyaK2MXmtFCqt7s%3D 7663518
123. CH Freudenreich JB Stavenhagen VA Zakian 1997 Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome Mol Cell Biol 17 2090 2098 1:CAS:528:DyaK2sXhvFOhsr4%3D 9121457
124. HM Kim V Narayanan PA Mieczkowski TD Petes MM Krasilnikova SM Mirkin KS Lobachev 2008 Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair EMBO J 27 2896 2906 1:CAS:528:DC%2BD1cXhtlaltL7P 18833189
125. ML Hebert LA Spitz RD Wells 2004 DNA double-strand breaks induce deletion of CTG•CAG repeats in an orientation-dependent manner in Escherichia coli J Mol Biol 336 655 672 1:CAS:528:DC%2BD2cXptFSnsg%3D%3D 15095979
126. M Mitas 1997 Trinucleotide repeats associated with human disease Nucleic Acids Res 25 2245 2254 1:CAS:528:DyaK2sXkt12ltLk%3D 9171073
127. CE Pearson M Tam YH Wang SE Montgomery AC Dar JD Cleary K Nichol 2002 Slipped-strand DNAs formed by long (CAG)*(CTG) repeats: slipped-out repeats and slip-out junctions Nucleic Acids Res 30 4534 4547 1:CAS:528:DC%2BD38Xot1Cju7Y%3D 12384601
128. IV Kovtun CT McMurray 2008 Features of trinucleotide repeat instability in vivo Cell Res 18 198 213 1:CAS:528:DC%2BD1cXitl2qtQ%3D%3D 18166978
129. n-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition Nat Struct Mol Biol 12 663 670 1:CAS:528:DC%2BD2MXmvVOhs70%3D 16025128
130. K Manley TL Shirley L Flaherty A Messer 1999 Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice Nat Genet 23 471 473 1:CAS:528:DyaK1MXnvFOkuro%3D 10581038
131. Y Lin V Dion JH Wilson 2006 Transcription promotes contraction of CAG repeat tracts in human cells Nat Struct Mol Biol 13 179 180 1:CAS:528: DC%2BD28XhtFajsLs%3D 16388310
132. I Voineagu CF Surka AA Shishkin MM Krasilnikova SM Mirkin 2009 Replisome stalling and stabilization at CGG repeats, which are responsible for chromosomal fragility Nat Struct Mol Biol 16 226 228 1:CAS:528:DC%2BD1MXktVehsA%3D%3D 19136957
133. KS Lobachev JE Stenger OG Kozyreva J Jurka DA Gordenin MA Resnick 2000 Inverted Alu repeats unstable in yeast are excluded from the human genome EMBO J 19 3822 3830 1:CAS:528:DC%2BD3cXmtlegsLk%3D 10899135
134. C Spiro R Pelletier ML Rolfsmeier MJ Dixon RS Lahue G Gupta MS Park X Chen SV Mariappan CT McMurray 1999 Inhibition of FEN-1 processing by DNA secondary structure at trinucleotide repeats Mol Cell 4 1079 1085 1:CAS:528:DC%2BD3cXislaqtA%3D%3D 10635332
135. EW Refsland DM Livingston 2005 Interactions among DNA ligase I, the flap endonuclease and proliferating cell nuclear antigen in the expansion and contraction of CAG repeat tracts in yeast Genetics 171 923 934 1:CAS:528:DC%2BD28Xjs1KlsA%3D%3D 16079237
136. S Bhattacharyya RS Lahue 2005 Srs2 helicase of Saccharomyces cerevisiae selectively unwinds triplet repeat DNA J Biol Chem 280 33311 33317 1:CAS:528:DC%2BD2MXhtVensLzJ 16085654
137. A Kerrest RP Anand R Sundararajan R Bermejo G Liberi B Dujon CH Freudenreich GF Richard 2009 SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination Nat Struct Mol Biol 16 159 167 1:CAS:528:DC%2BD1MXktVartg%3D%3D 19136956
138. DL Daee T Mertz RS Lahue 2007 Postreplication repair inhibits CAG•CTG repeat expansions in Saccharomyces cerevisiae Mol Cell Biol 27 102 110 1:CAS:528:DC%2BD2sXjs1Kl 17060452
139. SE Moe JG Sorbo T Holen 2008 Huntingtin triplet-repeat locus is stable under long-term Fen1 knockdown in human cells J Neurosci Methods 171 233 238 1:CAS:528:DC%2BD1cXmtVajsbk%3D 18466979
140. n repeat in a knock-in mouse model for DM1 FEBS Lett 580 5208 5214 16978612
141. SS Chong AE McCall J Cota SH Subramony HT Orr MR Hughes HY Zoghbi 1995 Gametic and somatic tissue-specific heterogeneity of the expanded SCA1 CAG repeat in spinocerebellar ataxia type 1 Nat Genet 10 344 350 1:CAS:528:DyaK2MXms1Kjur0%3D 7670474
142. H Telenius B Kremer YP Goldberg J Theilmann SE Andrew J Zeisler S Adam C Greenberg EJ Ives LA Clarke, et al. 1994 Somatic and gonadal mosaicism of the Huntington disease gene CAG repeat in brain and sperm Nat Genet 6 409 414 1:CAS:528:DyaK2cXjt1SksL4%3D 8054984
143. IV Kovtun CT McMurray 2001 Trinucleotide expansion in haploid germ cells by gap repair Nat Genet 27 407 411 1:CAS:528:DC%2BD3MXjtFShsL4%3D 11279522
144. KM Trujillo P Sung 2001 DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex J Biol Chem 276 35458 35464 1:CAS:528:DC%2BD3MXntFahsro%3D 11454871
145. DK Nag M Fasullo Z Dong A Tronnes 2005 Inverted repeat-stimulated sister-chromatid exchange events are RAD1-independent but reduced in a msh2 mutant Nucleic Acids Res 33 5243 5249 1:CAS:528:DC%2BD2MXhtVKhsr3E 16166656
146. DT Kirkpatrick TD Petes 1997 Repair of DNA loops involves DNA-mismatch and nucleotide-excision repair proteins Nature 387 929 931 1:CAS:528: DyaK2sXkt1Kgsro%3D 9202128
147. P Parniewski A Bacolla A Jaworski RD Wells 1999 Nucleotide excision repair affects the stability of long transcribed (CTG*CAG) tracts in an orientation-dependent manner in Escherichia coli Nucleic Acids Res 27 616 623 1:CAS:528:DyaK1MXhtVKmt7w%3D 9862988
148. R Pelletier BT Farrell JJ Miret RS Lahue 2005 Mechanistic features of CAG*CTG repeat contractions in cultured cells revealed by a novel genetic assay Nucleic Acids Res 33 5667 5676 1:CAS:528:DC%2BD2MXhtFWltrjN 16199754
149. GB Panigrahi R Lau SE Montgomery MR Leonard CE Pearson 2005 Slipped (CTG)*(CAG) repeats can be correctly repaired, escape repair or undergo error-prone repair Nat Struct Mol Biol 12 654 662 1:CAS:528:DC%2BD2MXmvVOiu7c%3D 16025129
150. C Savouret C Garcia-Cordier J Megret H te Riele C Junien G Gourdon 2004
151. G Wang KM Vasquez 2007 Z-DNA, an active element in the genome Front Biosci 12 4424 4438 1:CAS:528:DC%2BD2sXms1KlsbY%3D 17485386
152. Zhao J, Jain A, Iyer RR, Modrich PL, Vasquez KM (2009). Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks. Nucleic Acids Res 37:4420-4429
153. ML Rolfsmeier MJ Dixon RS Lahue 2000 Mismatch repair blocks expansions of interrupted trinucleotide repeats in yeast Mol Cell 6 1501 1507 1:CAS:528:DC%2BD3MXlvFansg%3D%3D 11163222
154. C Savouret E Brisson J Essers R Kanaar A Pastink H te Riele C Junien G Gourdon 2003 CTG repeat instability and size variation timing in DNA repair-deficient mice EMBO J 22 2264 2273 1:CAS:528:DC%2BD3sXjsVKmurY%3D 12727892
155. ML Hebert RD Wells 2005 Roles of double-strand breaks, nicks and gaps in stimulating deletions of CTG•CAG repeats by intramolecular DNA repair J Mol Biol 353 961 979 1:CAS:528:DC%2BD2MXhtFKms7bF 16213518
156. n sequence results in frequent deletion of the triplet-repeat sequence Nucleic Acids Res 36 489 500 1:CAS:528:DC%2BD1cXhs1Wqt7o%3D 18045804
157. JL Marcadier CE Pearson 2003 Fidelity of primate cell repair of a double-strand break within a (CTG)•(CAG) tract. Effect of slipped DNA structures J Biol Chem 278 33848 33856 1:CAS:528:DC%2BD3sXmvVCrtb4%3D 12807901
158. B Downing R Morgan K VanHulle A Deem A Malkova 2008 Large inverted repeats in the vicinity of a single double-strand break strongly affect repair in yeast diploids lacking Rad51 Mutat Res 645 9 18 1:CAS:528:DC%2BD1cXht1egtLvK 18755201
159. K VanHulle FJ Lemoine V Narayanan B Downing K Hull C McCullough M Bellinger K Lobachev TD Petes A Malkova 2007 Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements Mol Cell Biol 27 2601 2614 1:CAS:528:DC%2BD2sXjs1ajsb4%3D 17242181
160. JP Jakupciak RD Wells 2000 Gene conversion (recombination) mediates expansions of CTG•CAG repeats J Biol Chem 275 40003 40013 1:CAS:528:DC%2BD3MXhsFehug%3D%3D 11005819
161. L Tartier V Michalik M Spotheim-Maurizot AR Rahmouni R Sabattier M Charlier 1994 Radiolytic signature of Z-DNA Nucleic Acids Res 22 5565 5570 1:CAS:528:DyaK2MXjtlGisL4%3D 7838708
162. DT Ribeiro C Madzak A Sarasin P Di Mascio H Sies CF Menck 1992 Singlet oxygen induced DNA damage and mutagenicity in a single-stranded SV40-based shuttle vector Photochem Photobiol 55 39 45 1:CAS:528:DyaK38XhtVSkurw%3D 1318549
163. C Lagravere B Malfoy M Leng J Laval 1984 Ring-opened alkylated guanine is not repaired in Z-DNA Nature 310 798 800 1:CAS:528:DyaL2cXlvVKrsro%3D 6382026
164. S Boiteux R Costa de Oliveira J Laval 1985 The Escherichia coli O6-methylguanine-DNA methyltransferase does not repair promutagenic O6-methylguanine residues when present in Z-DNA J Biol Chem 260 8711 8715 1:CAS:528:DyaL2MXkvVegsrk%3D 3894348