Non-B DNA conformations as determinants of mutagenesis and human disease

Molecular Carcinogenesis

Volumn 48, Issue 4, 2009, Pages 273-285

  Bacolla, Albino ^a   Wells, Robert D ^a  

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

Author keywords

Cruciforms; DNA repair; DNA structure; Microsatellites; ROS signaling

Indexed keywords

AMINO ACID; CRUCIFORM DNA; DNA Z; GUANINE QUADRUPLEX; PURINE; PYRIMIDINE; REACTIVE OXYGEN METABOLITE; REPETITIVE DNA; DNA;

ALLELE; CANCER SUSCEPTIBILITY; CHROMOSOME; DEGENERATIVE DISEASE; DNA BINDING MOTIF; DNA CONFORMATION; DNA RECOMBINATION; DNA REPAIR; DNA SEQUENCE; DNA STRUCTURE; DNA SYNTHESIS; GENE; GENE REARRANGEMENT; GENE TARGETING; GENETIC ASSOCIATION; GENETIC DISORDER; GENOME; HUMAN; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; TUMOR GENE; CONFORMATION; GENERAL ASPECTS OF DISEASE; GENETICS;

VERTEBRATA;

DISEASE; DNA; HUMANS; MUTAGENESIS; NUCLEIC ACID CONFORMATION;

EID: 65249186097     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20507     Document Type: Review

References (97)

1. Heidelberger C. Chemical carcinogenesis. Annu Rev Bio Chem 1975;44: 79-121.
2. Wells RD. Non-B DNA conformations, mutagenesis and disease. Trends Biochem Sci 2007;32: 271-278.
3. Wang G, Vasquez KM. Non-B DNA structure-induced genetic instability. Mutat Res 2006;598: 103-119.
4. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998;396: 643-649.
5. Wells RD, Ashizawa T, editors. Genetic instabilities and neurological diseases. 2nd edition. San Diego: Elsevier/ Academic Press; 2006. 766 p.
6. Wells RD, Dere R, Hebert ML, Napierala M, Son LS. Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res 2005;33: 3785-3798.
7. Gatchel JR, Zoghbi HY. Diseases of unstable repeat expansion: Mechanisms and common principles. Nat Rev Genet 2005;6: 743-755.
8. Lin Y, Hubert L, Jr., Wilson JH. Transcription destabilizes triplet repeats. Mol Carcinog this issue.
9. Duker NJ. Chromosome breakage syndromes and cancer. AmJ Med Genet 2002;115: 125-129.
10. Lupski JR, Stankiewicz P, editors. Genomic disorders: The genomic basis of disease. Totowa, NJ: Humana Press; 2006.426 p.]
11. Wells RD. Reflections: Discovery of the role of non-B DNA structures in mutagenesis and human diseases. J Biol Chem (in press).
12. Sinden RR. DNA structure and function. San Diego, California: Academic Press; 1994.
13. Bowater RP, Wells RD. The intrinsically unstable life of DNA triplet repeats associated with human hereditary disorders. Progr Nucleic Acid Res Mol Biol 2000;66: 159-202.
14. Wells RD. DNA triplexes and Friedreich ataxia. FASEB J 2008;22: 1625-1634.
15. Jakupciak JP, Wells RD. Genetic instabilities of triplet repeat sequencesbyrecombination. Life 2000;50: 355-359.
16. Wang G, Vasquez KM. Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. Proc Natl Acad Sci USA 2004;101: 13448-13453.
17. Bacolla A, Jaworski A, Larson JE, et al. Breakpoints of gross deletions coincide with non-B DNA conformations. Proc Natl Acad Sci USA 2004;101: 14162-14167.
18. Raghavan SC, Swanson PC, Wu X, Hsieh CL, Lieber MR. A non-B-DNA structure at the Bc/-2 major breakpoint region is cleaved by the RAG complex. Nature 2004;428: 88-93.
19. Wang G, Christensen LA, Vasquez KM. Z-DNA-forming sequences generate large-scale deletions in mammalian cells. Proc Natl Acad Sci USA 2006;103: 2677-2682.
20. Bacolla A, Wojciechowska M, Kosmider B, Larson JE, Wells RD. The involvement of non-B DNA structures in gross chromosomal rearrangements. DNA Repair 2006;5: 1161-1170.
21. Bacolla A, Wells RD. Non-B DNA conformations, genomic rearrangements, and human disease. J Biol Chem 2004;279: 47411-47414.
22. Bacolla A, Wells RD. Non-B DNA and chromosomal rearrangements. In: Lupski JR, Stankiewicz P, editors. Genomic disorders: The genomic basis of disease. Totowa, NJ: Humana Press; 2006. p 89-99.
23. Sharan SK, Kuznetsov SG. Resolving RAD51C function in late stages of homologous recombination. Cell Div 2007;2: 15.
24. Inagaki K, Ma C, Storm TA, Kay MA, Nakai H. The role of DNA-PKcsand artemis in opening viral DNA hairpin termini in various tissues in mice. J Virol 2007;81: 11304-11321.
25. Ma Y, Schwarz K, Lieber MR. The artemis: DNA-PKcs endo- nuclease cleaves DNA loops, flaps, and gaps. DNA Repair 2005;4: 845-851.
26. Bacolla A, Collins JR, Gold B, et al. Long homopurine homopyrimidine sequences are characteristic of genes expressed in brain and the pseudoautosomal region. Nucleic Acids Res 2006;34: 2663-2675.
27. Du Z, Zhao Y, Li N. Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription. Genome Res 2008; 18: 233-241.
28. Huppert JL, Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 2007;35: 406-413.
29. Wojciechowska M, Napierala M, Larson JE, Wells RD. Non-B DNA conformations formed by long repeating tracts of DM1, DM2 and FRDA genes, not the sequences per se, promote mutagenesis in flanking regions. J Biol Chem 2006;281: 24531-24543.
30. SamadashwilyGM, Raca G, Mirkin SM. Trinucleotide repeats affect DNA replication in vivo. Nat Genet 1997;17: 298-304.
31. Raghavan SC, Chastain P, Lee JS, et al. Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. J Biol Chem 2005;280: 22749-22760.
32. Bacolla A, Jaworski A, Connors TD, Wells RD. PKD1 unusual DNA conformations are recognized by nucleotide excision repair. J Biol Chem 2001;276: 18597-18604.
33. Freudenreich CH, Stavenhagen JB, Zakian VA. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol Cell Biol 1997;17: 2090-2098.
34. Gotter AL, ShaikhTH, Budarf ML, Rhodes CH, Emanuel BS. A palindrome-mediated mechanism distinguishes translocations involving LCR-B of chromosome 22q11.2. Hum Mol Genet 2004;13: 103-115.
35. Kato T, Inagaki H, Yamada K, et al. Genetic variation affects de novo translocation frequency. Science (New York, NY) 2006;311: 971.
36. Rooney SM, Moore PD. Antiparallel, intramolecular triplex DNA stimulates homologous recombination in human cells. Proc Natl Acad Sci USA 1995;92: 2141-2144.
37. Mulvihill DJ, Nichol Edamura K, Hagerman KA, Pearson CE, Wang YH. 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 2005;280: 4498-4503.
38. Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature 2001;409: 860-921.
39. Fondon JW, III, Garner HR. Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci USA 2004;101: 18058-18063.
40. Riancho JA, Zarrabeitia MT, Valero C, et al. Aromatase gene and osteoporosis: Relationship of ten polymorphic loci with bone mineral density. Bone 2005;36: 917-925.
41. Bacolla A, Larson JE, Collins JR, et al. Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties. Genome Res 2008;18: 1545-1553.
42. Clark RM, Bhaskar SS, Miyahara M, Dalgliesh GL, Bidichandani SI. Expansion of GAA trinucleotide repeats in mammals. Genomics 2006;87: 57-67.
43. Xu L, Chow J, Bonacum J, et al. Microsatellite instability at AAAG repeat sequences in respiratory tract cancers. Int J Cancer 2001;91: 200-204.
44. Danaee H, Nelson HH, Karagas MR, et al. Microsatellite instability at tetranucleotide repeats in skin and bladder cancer. Oncogene 2002;21: 4894-4899.
45. Mirkin SM. Expandable DNA repeats and human disease. Nature 2007;447: 932-940.
46. Orr HT, Zoghbi HY. Trinucleotide repeat disorders. Annu Rev Neurosci 2007;30: 575-621.
47. Yang W. Poor base stacking at DNA lesions may initiate recognition by many repair proteins. DNA Repair 2006; 5: 654-666.
48. Huntley MA, Clark AG. Evolutionary analysis of amino acid repeats across the genomes of 12 Drosophila species. Mol Biol Evol 2007;24: 2598-2609.
49. Karlin S, Brocchieri L, Bergman A, Mrazek J, Gentles AJ. Amino acid runs in eukaryotic proteomes and disease associations. Proc Natl Acad Sci USA 2002;99: 333-338.
50. Faux NG, Bottomley SP, Lesk AM, et al. Functional insights from the distribution and role of homopeptide repeat- containing proteins. Genome Res 2005;15: 537-551.
51. Subramanian S, Madgula VM, George R, et al. MRD: A microsatellite repeats database for prokaryotic and eukaryotic genomes. Genome Biol 2002;3: Preprint 0011.
52. Alba MM, Guigo R. Comparative analysis of amino acid repeats in rodents and humans. Genome Res 2004;14: 549-554.
53. Zalba G, Fortuno A, Orbe J, et al. Phagocytic NADPH oxidase- dependent superoxide production stimulates matrix metal- loproteinase-9: Implications for human atherosclerosis. Arterioscler ThrombVasc Biol 2007;27: 587-593.
54. Yu F, Sabeti PC, Hardenbol P, et al. Positive selection of a pre- expansion CAG repeat of the human SCA2 gene. PLoS Genet 2005;1:e41.
55. Mularoni L, Veitia RA, Alba MM. Highly constrained proteins contain an unexpectedly large number of aminoacid tandem repeats. Genomics 2007;89: 316-325.
56. Haberman Y, Amariglio N, Rechavi G, Eisenberg E. Trinucleotide repeats are prevalent among cancer-related genes. Trends Genet 2008;24: 14-18.
57. Chuzhanova N, Abeysinghe SS, Krawczak M, Cooper DN. 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 2003;22: 245-251.
58. Brandt B, Meyer-Staeckling S, Schmidt H, Agelopoulos K, Buerger H. Mechanisms of egfr gene transcription modulation: Relationship to cancer risk and therapyresponse. Clin Cancer Res 2006;12: 7252-7260.
59. HolgateST, Lackie P, Wilson S, Roche W, Davies D. Bronchial epithelium as a key regulator of airway allergen sensitization and remodeling in asthma. Am J Respir Crit Care Med 2000;162: S113-S117.
60. Nomura M, Shigematsu H, Li L, et al. Polymorphisms, mutations, and amplification of the EGFR gene in non-small cell lung cancers. PLoS Med 2007;4: 125.
61. Etienne-Grimaldi MC, Pereira S, Magne N, et al. Analysis of the dinucleotide repeat polymorphism in the epidermal growth factor receptor (EGFR) gene in head and neck cancer patients. Ann Oncol 2005;16: 934-941.
62. Zhang W, Weissfeld JL, Romkes M, Land SR, Grandis JR, Siegfried JM. Association of the EGFR intron 1 CA repeat length with lung cancer risk. Mol Carcinog 2007;46: 372-380.
63. Dubey S, Stephenson P, Levy DE, et al. EGFR dinucleotide repeat polymorphism as a prognostic indicator in non-small cell lung cancer. J Thorac Oncol 2006;1: 406-412.
64. Sueoka-Aragane N, Imai K, Komiya K, et al. Exon 19 of EGFR mutation in relation to the CA-repeat polymorphism in intron 1. Cancer Sci 2008;99: 1180-1187.
65. Ichihara S, Toyooka S, Fujiwara Y, et al. The impact of epidermal growth factor receptor gene status on gefitinib- treated Japanese patients with non-small-cell lung cancer. Int J Cancer 2007;120: 1239-1247.
66. Han SW, Jeon YK, Lee KH, et al. Intron 1 CA dinucleotide repeat polymorphism and mutations of epidermal growth factor receptor and gefitinib responsiveness in non-small-cell lung cancer. Pharmacogenet Genomics 2007;17: 313-319.
67. Buerger H, Packeisen J, Boecker A, et al. Allelic length of a CA dinucleotide repeat in the egfr gene correlates with the frequency of amplifications of this sequence-First results of an inter-ethnic breast cancer study. J Pathol 2004;203: 545-550.
68. Reeves SG, Rich D, Meldrum CJ, et al. IGF1 is a modifier of disease risk in hereditary non-polyposis colorectal cancer. Int J Cancer 2008;123: 1339-1343.
69. Cleveland RJ, Gammon MD, Edmiston SN, et al. IGF1 CA repeat polymorphisms, lifestyle factors and breast cancer risk in the Long Island Breast Cancer Study Project. Carcino-genesis 2006;27: 758-765.
70. Zecevic M, Amos CI, Gu X, et al. IGF1 gene polymorphism and risk for hereditary nonpolyposis colorectal cancer. J Natl Cancer Inst 2006;98: 139-143.
71. McIntyre MH, Kantoff PW, Stampfer MJ, et al. Prostate cancer risk and ESR1 TA, ESR2 CA repeat polymorphisms. Cancer Epidemiol Biomarkers Prev 2007;16: 2233-2236.
72. Boyapati SM, Shu XO, Ruan ZX, et al. Polymorphisms in ER- alpha gene interact with estrogen receptor status in breast cancer survival. Clin Cancer Res 2005;11: 1093-1098
73. Cai Q, Gao YT, Wen W, et al. Association of breast cancer risk with a GT dinucleotide repeat polymorphism upstream of the estrogen receptor-alpha gene. Cancer Res 2003;63: 5727-5730.
74. Kikuchi A, Yamaya M, Suzuki S, et al. Association of susceptibility to the development of lung adenocarcinoma with the heme oxygenase-1 gene promoter polymorphism. Hum Genet 2005;116: 354-360.
75. Lo SS, Lin SC, Wu CW, et al. Heme oxygenase-1 gene promoter polymorphism is associated with risk of gastric adenocarcinoma and lymphovascular tumor invasion. Ann Surg Oncol 2007;14: 2250-2256.
76. Hong CC, Ambrosone CB, Ahn J, et al. Genetic variability in iron-related oxidative stress pathways (Nrf2, NQ01, NOS3, and HO-1), iron intake, and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 2007;16: 1784-1794.
77. Koukourakis MI, Papazoglou D, Giatromanolaki A, et al. C2028T polymorphism in exon 12 and dinucleotide repeat polymorphism in intron 13 of the HIF-1alpha gene define HIF- 1alpha protein expression in non-small cell lung cancer. Lung Cancer (Amsterdam, Netherlands) 2006;53: 257-262.
78. Wang J, Evans JP, Ogura H, La Mar GN, Ortiz de Montellano PR. Alteration of the regiospecificity of human heme oxygenase-1 by unseating of the heme but not disruption of the distal hydrogen bonding network. Biochemistry2006;45: 61-73.
79. Liu Y, Ortiz de Montellano PR. Reaction intermediates and single turnover rate constants for the oxidation of heme by human heme oxygenase-1. J Biol Chem 2000;275: 5297-5307.
80. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med 2008;86: 267-279.
81. Meng D, Shi X, Jiang BH, Fang J. Insulin-like growth factor-I (IGF-I) induces epidermal growth factor receptor trans- activation and cell proliferation through reactive oxygen species. Free Radic Biol Med 2007;42: 1651-1660.
82. Giannoni E, Buricchi F, Grimaldi G, et al. Redox regulation of anoikis: Reactive oxygen species as essential mediators of cell survival. Cell Death Differ 2008;15: 867-878.
83. Astermark J, Oldenburg J, Pavlova A, Berntorp E, Lefvert AK. Polymorphisms in the IL10 but not in the IL1beta and IL4 genes are associated with inhibitor development in patients with hemophilia A. Blood 2006;107: 3167-3172.
84. Cochery-Nouvellon E, Vitry F, Cornillet-Lefebvre P, Hezard N, Gillot L, Nguyen P. Interleukin-10 promoter polymorphism and venous thrombosis: A case-control study. Thromb Haemost 2006;96: 24-28.
85. Murray PJ. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr Opin Pharmacol 2006;6: 379-386.
86. Li K, Dai D, Yao L, et al. Association between the macrophage inflammatory protein-l alpha gene polymorphism and Alzheimer's disease in the Chinese population. Neurosci Lett 2008;433: 125-128.
87. TexereauJ, MarulloS, Hubert D,et al. Nitric oxide synthase 1 as a potential modifier gene of decline in lung function in patients with cystic fibrosis. Thorax 2004;59: 156-158.
88. Bayele HK, Peyssonnaux C, Giatromanolaki A, et al. HIF-1 regulates heritable variation and allele expression pheno- types of the macrophage immune response gene SLC11A1 from a Z-DNA forming microsatellite. Blood 2007;110: 3039-3048.
89. Kodama D, Saito M, Matsumoto W, et al. Longer dinucleotide repeat polymorphism in matrix metalloproteinase-9 (MMP-9) gene promoter which correlates with higher HTLV-I Tax mediated transcriptional activity influences the risk of HTLV-I associated myelopathy/tropical spastic paraparesis (HAM/TSP). J Neuroimmunol 2004;156: 188-194.
90. Shin MH, Moon YJ, Seo JE, Lee Y, Kim KH, Chung JH. Reactive oxygen species produced by NADPH oxidase, xanthine oxidase, and mitochondrial electron transport system mediate heat shock-induced MMP-1 and MMP-9 expression. Free Radic Biol Med 2008;44: 635-645.
91. Uhlemann AC, Szlezak NA, Vonthein R, et al. DNA phasing by TA dinucleotide microsatellite length determines in vitro and in vivo expression of the gp91phox subunit of NADPH oxidase and mediates protection against severe malaria. J Infect Dis 2004;189: 2227-2234.
92. Nichenametla SN, Ellison I, Calcagnotto A, Lazarus P, Muscat JE, Richie JP, Jr. Functional significance of the GAG trinucleotide-repeat polymorphism in the gene for the catalytic subunit of gamma-glutamylcysteine ligase. Free Radic Biol Med 2008;45: 645-650.
93. Tanaka H, Cao Y, Bergstrom DA, Kooperberg C, Tapscott SJ, Yao MC. Intrastrand annealing leads to the formation of a large DNA palindrome and determines the boundaries of genomic amplification in human cancer. Mol Cell Biol 2007; 27:1993-
94. Neiman PE, Elsaesser K, Loring G, Kimmel R. Myconcogene- induced genomic instability: DNA palindromes in bursal lymphomagenesis. PLoS Genet 2008;4: e1000132.
95. Piriyapongsa J, Jordan IK. A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS ONE 2007;2:e203.
96. Wright BE, Schmidt KH, Davis N, Hunt AT, Minnick MF, II. Correlations between secondary structure stability and mutation frequency during somatic hypermutation. Mol Immunol 2008;45: 3600-3608.
97. Gangwal K, Sankar S, Hollenhorst PC, et al. Microsatellitesas EWS/FLI response elements in Ewing's sarcoma. Proc Natl Acad Sci USA 2008;105: 10149-10154.