Long homopurine•homopyrimidine sequences are characteristic of genes expressed in brain and the pseudoautosomal region

Nucleic Acids Research

Volumn 34, Issue 9, 2006, Pages 2663-2675

  Bacolla, Albino ^e   Collins, Jack R ^a   Gold, Bert ^a   Chuzhanova, Nadia ^b   Yi, Ming ^a   Stephens, Robert M ^a   Stefanov, Stefan ^a   Olsh, Adam ^a   Jakupciak, John P ^c   Dean, Michael ^a   Lempicki, Richard A ^d   Cooper, David N ^b   Wells, Robert D ^e  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^d SAIC FREDERICK INC   (United States)

^e TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENE PRODUCT; PURINE; PYRIMIDINE; PROTEIN; PURINE DERIVATIVE; PYRIMIDINE DERIVATIVE; TRIPLEX DNA;

ARTICLE; BASE PAIRING; BRAIN REGION; CELL MEMBRANE; CHIMPANZEE; DEVELOPMENTAL BIOLOGY; DNA REPAIR; EVOLUTION; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE MAPPING; GENE MUTATION; GENE REARRANGEMENT; GENE REPLICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC RECOMBINATION; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; INHIBITION KINETICS; INTRON; MENTAL DISEASE; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCHIZOPHRENIA; SEX CHROMOSOME; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; ANIMAL; BRAIN; CHEMISTRY; GENETICS; GENOME; METABOLISM; MOLECULAR EVOLUTION; PAN TROGLODYTES; TISSUE DISTRIBUTION;

PAN; PAN TROGLODYTES;

ANIMALS; BRAIN; DNA; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENOME, HUMAN; HUMANS; PAN TROGLODYTES; PROTEINS; PURINES; PYRIMIDINES; REPETITIVE SEQUENCES, NUCLEIC ACID; SEX CHROMOSOMES; TISSUE DISTRIBUTION;

EID: 33646902184     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl354     Document Type: Article

References (78)

1. Sinden,R.R. (1994) DNA Structure and Function. Academic Press, San Diego, CA.
2. Wells,R.D., Dere,R., Hebert,M.L., Napierala,M. and Son,L.S. (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res., 33, 3785-3798.
3. Mirkin,S.M. and Frank-Kamenetskii,M.D. (1994) H-DNA and related structures. Annu. Rev. Biophys. Biomol. Struct., 23, 541-576.
4. RTch,A. and Zhang,S. (2003) Timeline: Z-DNA: the long road to biological function. Nature Rev. Genet., 4, 566-572.
5. Neidle,S. and Parkinson,G.N. (2003) The structure of telomeric DNA. Curr. Opin. Struct. Biol., 13, 275-283.
6. Soyfer,V.N. and Potaman,V.N. (1996) Triple-Helical Nucleic Acids. Springer-Verlag, New York.
7. Hurley,L.H. (2002) DNA and its associated processes as targets for cancer therapy. Nature Rev. Cancer, 2, 188-200.
8. Bacolla,A. and Wells,R.D. (2004) Non-B DNA conformations, genomic rearrangements, and human disease. J. Biol. Chem., 279, 47411-47414.
9. Bacolla,A., Jaworski,A., Larson,J.E., Jakupciak,J.P., Chuzhanova,N., Abeysinghe,S.S., O'Connell,C.D., Cooper,D.N. and Wells,R.D. (2004) Breakpoints of gross deletions coincide with non-B DNA conformations. Proc. Natl Acad. Sci. USA, 101, 14162-14167.
10. Wojciechowska,M., Bacolla,A., Larson,J.E. and Wells,R.D. (2005) The myotonic dystrophy type 1 triplet repeat sequence induces gross deletions and inversions. J. Biol. Chem., 280, 941-952.
11. Kuroda-Kawaguchi,T., Skaletsky,H., Brown,L.G., Minx,P.J., Cordum,H.S., Waterston,R.H., Wilson,R.K., Silber,S., Oates,R., Rozen,S. et al. (2001) The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nature Genet., 29, 279-286.
12. Repping,S., Skaletsky,H., Lange,J., Silber,S., Van Der Veen,F., Oates,R.D., Page,D.C. and Rozen,S. (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.
13. Gotter,A.L., Shaikh,T.H., Budarf,M.L., Rhodes,C.H. and Emanuel,B.S. (2004) A palindrome-mediated mechanism distinguishes translocations involving LCR-B of chromosome 22q11.2. Hum. Mol. Genet., 13, 103-115.
14. Abeysinghe,S.S., Chuzhanova,N., Krawczak,M., Ball,E.V. and Cooper,D.N. (2003) Translocation and gross deletion breakpoints in human inherited disease and cancer I: Nucleotide composition and recombination-associated motifs. Hum. Mutat., 22, 229-244.
15. Chuzhanova,N., Abeysinghe,S.S., Krawczak,M. and Cooper,D.N. (2003) Translocation and gross deletion breakpoints in human inherited disease and cancer II: Potential involvement of repetitive sequence elements in secondary structure formation between DNA ends. Hum. Mutat., 22, 245-251.
16. Kato,T., Inagaki,H., Yamada,K., Kogo,H., Ohye,T., Kowa,H., Nagaoka,K., Taniguchi,M., Emanuel,B.S. and Kurahashi,H. (2006) Genetic variation affects de novo translocation frequency. Science, 311, 971.
17. Wells,R.D., Collier,D.A., Hanvey,J.C., Shimizu,M. and Wohlrab,F. (1988) The chemistry and biology of unusual DNA structures adopted by oligopurine.oligopyrimidine sequences. FASEB J., 2, 2939-2949.
18. Frank-Kamenetskii,M.D. and Mirkin,S.M. (1995) Triplex DNA structures. Annu. Rev. Biochem., 64, 65-95.
19. Chan,P.P. and Glazer,P.M. (1997) Triplex DNA: Fundamentals, advances, and potential applications for gene therapy. J. Mol. Med., 75, 267-282.
20. Inman,R.B. (1964) Transitions of DNA Homopolymers. J. Mol. Biol., 9, 624-637.
21. Wells,R.D. and Larson,J.E. (1972) Buoyant density studies on natural and synthetic deoxyribonucleic acids in neutral and alkaline solutions. J. Biol. Chem., 247, 3405-3409.
22. Jaishree,T.N. and Wang,A.H. (1993) NMR studies of pH-dependent conformational polymorphism of alternating (C-T)n sequences. Nucleic Acids Res., 21, 3839-3844.
23. Morgan,A.R. and Wells,R.D. (1968) Specificity of the three-stranded complex formation between double-stranded DNA and single-stranded RNA containing repeating nucleotide sequences. J. Mol. Biol., 37, 63-80.
24. Krasilnikov,A.S., Panyutin,I.G., Samadashwily,G.M., Cox,R., Lazurkin,Y.S. and Mirkin,S.M. (1997) Mechanisms of triplex-caused polymerization arrest. Nucleic Acids Res., 25, 1339-1346.
25. Patel,H.P., Lu,L., Blaszak,R.T. and Bissler,J.J. (2004) PKD1 intron 21: triplex DNA formation and effect on replication. Nucleic Acids Res., 32, 1460-1468.
26. Ohshima,K., Montermini,L., Wells,R.D. and Pandolfo,M. (1998) Inhibitory effects of expanded GAA• TTC triplet repeats from intron I of the Friedreich ataxia gene on transcription and replication in vivo. J. Biol. Chem., 275, 14588-14595.
27. Kohwi,Y. and Panchenko,Y. (1993) Transcription-dependent recombination induced by triple-helix formation. Genes Dev., 7, 1766-1778.
28. Faruqi,A.F., Datta,H.J., Carroll,D., Seidman,M.M. and Glazer,P.M. (2000) Triple-helix formation induces recombination in mammalian cells via a nucleotide excision repair-dependent pathway. Mol. Cell. Biol., 20, 990-1000.
29. Luo,Z., Macris,M.A., Faruqi,A.F. and Glazer,P.M. (2000) High-frequency intrachromosomal gene conversion induced by triplex-forming oligonucleotides microinjected into mouse cells. Proc. Natl Acad. Sci. USA, 97, 9003-9008.
30. Vasquez,K.M., Narayanan,L. and Glazer,P.M. (2000) Specific mutations induced by triplex-forming oligonucleotides in mice. Science, 290, 530-533.
31. Wang,G. and Vasquez,K.M. (2004) Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. Proc. Natl Acad. Sci. USA, 101, 13448-13453.
32. Bacolla,A., Jaworski,A., Connors,T.D. and Wells,R.D. (2001) PKD1 unusual DNA conformations are recognized by nucleotide excision repair. J. Biol. Chem., 276, 18597-18604.
33. Pandolfo,M. and Koenig,M. (1998) Freidreich's Ataxia. In Wells,R.D. and Warren,S.T. (eds), Genetic Instabilities and Hereditary Neurological Diseases. Academic Press, San Diego, CA, pp. 373-398.
34. Vetcher,A.A., Napierala,M., Iyer,R.R., Chastain,P.D., Griffith,J.D. and Wells,R.D. (2002) Sticky DNA, a long GAA.GAA.TTC triplex that is formed intramolecularly, in the sequence of intron 1 of the frataxin gene. J. Biol. Chem., 277, 39217-39227.
35. Raghavan,S.C., Chastain,P., Lee,J.S., Hegde,B.G., Houston,S., Langen,R., Hsieh,C.L., Haworth,I.S. and Lieber,M.R. (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.
36. Raghavan,S.C. and Lieber,M.R. (2004) Chromosomal translocations and non-B DNA structures in the human genome. Cell Cycle, 3, 762-768.
37. Raghavan,S.C., Swanson,P.C., Wu,X., Hsieh,C.L. and Lieber,M.R. (2004) A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Nature, 428, 88-93.
38. Knauert,M.P., Lloyd,J.A., Rogers,F.A., Datta,H.J., Bennett,M.L., Weeks,D.L. and Glazer,P.M. (2005) Distance and affinity dependence of triplex-induced recombination. Biochemistry, 44, 3856-3864.
39. Hoffman-Liebermann,B., Liebermann,D., Troutt,A., Kedes,L.H. and Cohen,S.N. (1986) Human homologs of TU transposon sequences: Polypurine/ polypyrimidine sequence elements that can alter DNA conformation in vitro and in vivo. Mol. Cell. Biol., 6, 3632-3642.
40. Christophe,D., Cabrer,B., Bacolla,A., Targovnik,H., Pohl,V. and Vassart,G. (1985) An unusually long poly(purine)-poly(pyrimidine) sequence is located upstream from the human thyroglobulin gene. Nucleic Acids Res., 13, 5127-5144.
41. Behe,M.J. (1987) The DNA sequence of the human beta-globin region is strongly biased in favor of long strings of contiguous purine or pyrimidine residues. Biochemistry, 26, 7870-7875.
42. Schroth,G.P. and Ho,P.S. (1995) Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA. Nucleic Acids Res., 23, 1977-1983.
43. Ussery,D., Soumpasis,D.M., Brunak,S., Staerfeldt,H.H., Worning,P. and Krogh,A. (2002) Bias of purine stretches in sequenced chromosomes. Comput. Chem., 26, 531-541.
44. Warburton,P.E., Giordano,J., Cheung,F., Gelfand,Y. and Benson,G. (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.
45. Collins,J.R., Stephens,R.M., Gold,B., Long,B., Dean,M. and Burt,S.K. (2003) An exhaustive DNA micro-satellite map of the human genome using high performance computing. Genomics, 82, 10-19.
46. Ming,Y., Horton,D., Cohen,J.C., Hobbs,H.H. and Stephens,R.M. (2006) WholePathwayScope: A comprehensive pathway-based analysis tool for high-throughput data. BMC Bioinformatics, 7, 30.
47. Karlin,S. and Macken,C. (1991) Some statistical problems in the assessment of inhomogenesis of DNA sequence data. J. Am. Statist. Assoc., 86, 27-35.
48. Gusev,V.D., Nemytikova,L.A. and Chuzhanova,N.A. (1999) On the complexity measures of genetic sequences. Bioinformatics, 15, 994-999.
49. Van Raay,T.J., Burn,T.C., Connors,T.D., Petri,L.R., Germino,G.G., Klinger,K.W. and Landes,G.M. (1996) A 2.5 kb polypyrimidine tract in the PKD1 gene contains at least 23 H-DNA-forming sequences. Microb. Comp. Genomics, 1, 317-327.
50. Vasquez,K.M., Wang,G., Havre,P.A. and Glazer,P.M. (1999) Chromosomal mutations induced by triplex-forming oligonicleotides in mammalian cells. Nucleic Acids Res., 27, 1176-1181.
51. Wang,G., Seidman,M.M. and Glazer,P.M. (1996) Mutagenesis in mammalian cells induced by triple helix formation and transcription-coupled repair. Science, 271, 802-805.
52. Filatov,D.A. and Gerrard,D.T. (2003) High mutation rates in human and ape pseudoautosomal genes. Gene, 317, 67-77.
53. Perry,J., Palmer,S., Gabriel,A. and Ashworth,A. (2001) A short pseudoautosomal region in laboratory mice. Genome Res., 11, 1826-1832.
54. Napierala,M., Dere,R., Vetcher,A. and Wells,R.D. (2004) Structure-dependent recombination hot spot activity of GAA.TTC sequences from intron 1 of the Friedreich's ataxia gene. J. Biol. Chem., 279, 6444-6454.
55. Sakamoto,N., Chastain,P.D., Parniewski,P., Ohshima,K., Pandolfo,M., Griffith,J.D. and Wells,R.D. (1999) Sticky DNA: Self-association properties of long GAAaTTC repeats in R R Y triplex structures from Friedreich's ataxia. Molecular Cell, 3, 465-475.
56. Subramanian,S., Mishra,R.K. and Singh,L. (2003) Genome-wide analysis of microsatellite repeats in humans: Their abundance and density in specific genomic regions. Genome Biol., 4, R13.
57. Sandstrom,K., Warmlander,S., Graslund,A. and Leijon,M. (2002) A-tract DNA disfavours triplex formation. J. Mol. Biol., 315, 737-748.
58. Roberts,R.W. and Crothers,D.M. (1996) Prediction of the stability of DNA triplexes. Proc. Natl Acad. Sci. USA, 93, 4320-4325.
59. James,P.L., Brown,T. and Fox,K.R. (2003) Thermodynamic and kinetic stability of intermolecular triple helices containing different proportions of C+*GC and T*AT triplets. Nucleic Acids Res., 31, 5598-5606.
60. Mikkelsen,T.S., Hillier,L.W., Eichler,E.E., Zody,M.C., Jaffe,D.B., Yang,S.-P., Enard,W., Hellmann,I., Lindblad-Toh,K., Altheide,T.K. et al. (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature, 437, 69-87.
61. Linardopoulou,E.V., Williams,E.M., Fan,Y., Friedman,C., Young,J.M. and Trask,B.J. (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature, 437, 94-100.
62. Chiaromonte,F., Yang,S., Elnitski,L., Yap,V.B., Miller,W. and Hardison,R.C. (2001) Association between divergence and interspersed repeats in mammalian noncoding genomic DNA. Proc. Natl Acad. Sci. USA, 98, 14503-14508.
63. Meservy,J.L., Sargent,R.G., Iyer,R.R., Chan,F., McKenzie,G.J., Wells,R.D. and Wilson,J.H. (2003) Long CTG tracts from the myotonic dystrophy gene induce deletions and rearrangements during recombination at the APRT locus in CHO cells. Mol. Cell. Biol., 23, 3152-3162.
64. Kong,A., Gudbjartsson,D.F., Sainz,J., Jonsdottir,G.M., Gudjonsson,S.A., Richardsson,B., Sigurdardottir,S., Barnard,J., Hallbeck,B., Masson,G. et al. (2002) A high-resolution recombination map of the human genome. Nature Genet., 31, 241-247.
65. Jensen-Seaman,M.I., Furey,T.S., Payseur,B.A., Lu,Y., Roskin,K.M., Chen,C.F., Thomas,M.A., Haussler,D. and Jacob,H.J. (2004) Comparative recombination rates in the rat, mouse, and human genomes. Genome Res., 14, 528-538.
66. Hellmann,I., Prufer,K., Ji,H., Zody,M.C., Paabo,S. and Ptak,S.E. (2005) Why do human diversity levels vary at a megabase scale? Genome Res., 15, 1222-1231.
67. Myers,S., Bottolo,L., Freeman,C., McVean,G. and Donnelly,P. (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science, 310, 321-324.
68. Wells,R.D. and Warren,S.T. (1998) Genetic Instabilities and Hereditary Neurological Diseases. Academic Press, San Diego, CA.
69. Kehrer-Sawatzki,H., Sandig,C., Chuzhanova,N., Goidts,V., Szamalek,J.M., Tanzer,S., Muller,S., Platzer,M., Cooper,D.N. and Hameister,H. (2005) Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes). Hum. Mutat., 25, 45-55.
70. Szamalek,J.M., Goidts,V., Chuzhanova,N., Hameister,H., Cooper,D.N. and Kehrer-Sawatzki,H. (2005) Molecular characterisation of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Hum. Genet., 117, 168-176.
71. Khaitovich,P., Hellmann,I., Enard,W., Nowick,K., Leinweber,M., Franz,H., Weiss,G., Lachmann,M. and Paabo,S. (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science, 309, 1850-1854.
72. Preuss,T.M., Caceres,M., Oldham,M.C. and Geschwind,D.H. (2004) Human brain evolution: Insights from microarrays. Nature Rev. Genet., 5, 850-860.
73. Uddin,M., Wildman,D.E., Liu,G., Xu,W., Johnson,R.M., Hof,P.R., Kapatos,G., Grossman,L.I. and Goodman,M. (2004) Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc. Natl Acad. Sci. USA, 101, 2957-2962.
74. Carninci,P., Kasukawa,T., Katayama,S., Gough,J., Frith,M.C., Maeda,N., Oyama,R., Ravasi,T., Lenhard,B., Wells,C. et al. (2005) The transcriptional landscape of the mammalian genome. Science, 309, 1559-1563.
75. Katayama,S., Tomaru,Y., Kasukawa,T., Waki,K., Nakanishi,M., Nakamura,M., Nishida,H., Yap,C.C., Suzuki,M., Kawai,J. et al. (2005) Antisense transcription in the mammalian transcriptome. Science, 309, 1564-1566.
76. Fabregat,I., Koch,K.S., Aoki,T., Atkinson,A.E., Dang,H., Amosova,O., Fresco,J.R., Schildkraut,C.L. and Leffert,H.L. (2001) Functional pleiotropy of an intramolecular triplex-forming fragment from the 3′-UTR of the rat Pigr gene. Physiol. Genomics, 5, 53-65.
77. Harrison,P.J. and Weinberger,D.R. (2005) Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence. Mol. Psychiatry, 10, 40-68.
78. Lewis,D.A., Hashimoto,T. and Volk,D.W. (2005) Cortical inhibitory neurons and schizophrenia. Nature Rev. Neurosci., 6, 312-324.