Base excision repair of chemotherapeutically-induced alkylated DNA damage predominantly causes contractions of expanded GAA repeats associated with Friedreich's ataxia

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Lai, Yanhao ^a,b   Beaver, Jill M ^b   Lorente, Karla ^b   Melo, Jonathan ^b   Ramjagsingh, Shyama ^b   Agoulnik, Irina U ^c   Zhang, Zunzhen ^a   Liu, Yuan ^b  

^a SICHUAN UNIVERSITY   (China)

^b FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA DIRECTED DNA POLYMERASE BETA; DNA FRAGMENT; FLAP ENDONUCLEASE 1; SINGLE STRANDED DNA; TEMOZOLOMIDE; UNCLASSIFIED DRUG; ALKYLATING AGENT; DACARBAZINE;

ARTICLE; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA DAMAGE; DNA STRAND BREAKAGE; DNA STRUCTURE; DNA SYNTHESIS; DNA TEMPLATE; EXCISION REPAIR; FRIEDREICH ATAXIA; GAA REPEAT; GEL ELECTROPHORESIS; GENE DELETION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRON; PROTEIN CLEAVAGE; ALKYLATION; ANALOGS AND DERIVATIVES; CONFORMATION; DNA REPAIR; DNA REPLICATION; DRUG EFFECTS; GENETICS; SINGLE STRANDED DNA BREAK; TRINUCLEOTIDE REPEAT; TUMOR CELL LINE;

ALKYLATION; ANTINEOPLASTIC AGENTS, ALKYLATING; CELL LINE, TUMOR; DACARBAZINE; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; FRIEDREICH ATAXIA; GENOMIC INSTABILITY; HUMANS; INTRONS; NUCLEIC ACID CONFORMATION; SEQUENCE DELETION; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84898606082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093464     Document Type: Article

References (79)

1. Santos R, Lefevre S, Sliwa D, Seguin A, Camadro JM, et al. (2010) Friedreich ataxia: molecular mechanisms, redox considerations, and therapeutic opportunities. Antioxid Redox Signal 13: 651-690.
2. Bradley JL, Blake JC, Chamberlain S, Thomas PK, Cooper JM, et al. (2000) Clinical, biochemical and molecular genetic correlatio (Pubitemid 30052751)
3. Schulz JB, Boesch S, Burk K, Durr A, Giunti P, et al. (2009) Diagnosis and treatment of Friedreich ataxia: a European perspective. Nat Rev Neurol 5: 222-234.
4. Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M, et al. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271: 1423-1427. (Pubitemid 26089479)
5. Pastore A, Puccio H (2013) Frataxin: a protein in search for a function. J Neurochem 126 Suppl 1: 43-52.
6. Zouari M, Feki M, Ben Hamida C, Larnaout A, Turki I, et al. (1998) Electrophysiology and nerve biopsy: comparative study in Friedreich's ataxia and Friedreich's ataxia phenotype with vitamin E deficiency. Neuromuscul Disord 8: 416-425. (Pubitemid 28388943)
7. Filla A, De Michele G, Cavalcanti F, Pianese L, Monticelli A, et al. (1996) The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia. Am J Hum Genet 59: 554-560. (Pubitemid 26269033)
8. Sharma R, De Biase I, Gomez M, Delatycki MB, Ashizawa T, et al. (2004) Friedreich ataxia in carriers of unstable borderline GAA triplet-repeat alleles. Ann Neurol 56: 898-901. (Pubitemid 39578458)
9. Pianese L, Turano M, Lo Casale MS, De Biase I, Giacchetti M, et al. (2004) Real time PCR quantification of frataxin mRNA in the peripheral blood leucocytes of Friedreich ataxia patients and carriers. J Neurol Neurosurg Psychiatry 75: 1061-1063. (Pubitemid 38869629)
10. Durr A, Cossee M, Agid Y, Campuzano V, Mignard C, et al. (1996) Clinical and genetic abnormalities in patients with Friedreich's ataxia. N Engl J Med 335: 1169-1175. (Pubitemid 26339770)
11. Monros E, Molto MD, Martinez F, Canizares J, Blanca J, et al. (1997) Phenotype correlation and intergenerational dynamics of the Friedreich ataxia GAA trinucleotide repeat. Am J Hum Genet 61: 101-110. (Pubitemid 27323329)
12. Grabczyk E, Usdin K (2000) The GAA*TTC triplet repeat expanded in Friedreich's ataxia impedes transcription elongation by T7 RNA polymerase in a length and supercoil dependent manner. Nucleic Acids Res 28: 2815-2822. (Pubitemid 30488540)
13. Grabczyk E, Usdin K (2000) Alleviating transcript insufficiency caused by Friedreich's ataxia triplet repeats. Nucleic Acids Res 28: 4930-4937. (Pubitemid 32014263)
14. Mariappan SV, Catasti P, Silks LA 3rd, Bradbury EM, Gupta G (1999) The high-resolution structure of the triplex formed by the GAA/TTC triplet repeat associated with Friedreich's ataxia. J Mol Biol 285: 2035-2052. (Pubitemid 29078169)
15. Jain A, Rajeswari MR, Ahmed F (2002) Formation and thermodynamic stability of intermolecular (R*R*Y) DNA triplex in GAA/TTC repeats associated with Freidreich's ataxia. J Biomol Struct Dyn 19: 691-699. (Pubitemid 34242146)
16. Sakamoto N, Chastain PD, Parniewski P, Ohshima K, Pandolfo M, et al. (1999) Sticky DNA: self-association properties of long GAA.TTC repeats in R.R.Y triplex structures from Friedreich's ataxia. Mol Cell 3: 465-475. (Pubitemid 29292603)
17. Sakamoto N, Ohshima K, Montermini L, Pandolfo M, Wells RD (2001) Sticky DNA, a self-associated complex formed at long GAA*TTC repeats in intron 1 of the frataxin gene, inhibits transcription. J Biol Chem 276: 27171-27177.
18. Grabczyk E, Mancuso M, Sammarco MC (2007) A persistent RNA.DNA hybrid formed by transcription of the Friedreich ataxia triplet repeat in live bacteria, and by T7 RNAP in vitro. Nucleic Acids Res 35: 5351-5359. (Pubitemid 47423909)
19. Festenstein R, Tolaini M, Corbella P, Mamalaki C, Parrington J, et al. (1996) Locus control region function and heterochromatin-induced position effect variegation. Science 271: 1123-1125. (Pubitemid 26075227)
20. Saveliev A, Everett C, Sharpe T, Webster Z, Festenstein R (2003) DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 422: 909-913. (Pubitemid 36520045)
21. Greene E, Mahishi L, Entezam A, Kumari D, Usdin K (2007) Repeat-induced epigenetic changes in intron 1 of the frataxin gene and its consequences in Friedreich ataxia. Nucleic Acids Res 35: 3383-3390. (Pubitemid 47073601)
22. Al-Mahdawi S, Pinto RM, Ismail O, Varshney D, Lymperi S, et al. (2008) The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum Mol Genet 17: 735-746. (Pubitemid 351292262)
23. Castaldo I, Pinelli M, Monticelli A, Acquaviva F, Giacchetti M, et al. (2008) DNA methylation in intron 1 of the frataxin gene is related to GAA repeat length and age of onset in Friedreich ataxia patients. J Med Genet 45: 808-812.
24. Evans-Galea MV, Carrodus N, Rowley SM, Corben LA, Tai G, et al. (2012) FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann Neurol 71: 487-497.
25. Herman D, Jenssen K, Burnett R, Soragni E, Perlman SL, et al. (2006) Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nat Chem Biol 2: 551-558. (Pubitemid 44413238)
26. Soragni E, Herman D, Dent SY, Gottesfeld JM, Wells RD, et al. (2008) Long intronic GAA*TTC repeats induce epigenetic changes and reporter gene silencing in a molecular model of Friedreich ataxia. Nucleic Acids Res 36: 6056-6065.
27. De Biase I, Chutake YK, Rindler PM, Bidichandani SI (2009) Epigenetic silencing in Friedreich ataxia is associated with depletion of CTCF (CCCTCbinding factor) and antisense transcription. PLoS One 4: e7914.
28. Punga T, Buhler M (2010) Long intronic GAA repeats causing Friedreich ataxia impede transcription elongation. EMBO Mol Med 2: 120-129.
29. Kang S, Ohshima K, Shimizu M, Amirhaeri S, Wells RD (1995) Pausing of DNA synthesis in vitro at specific loci in CTG and CGG triplet repeats from human hereditary disease genes. J Biol Chem 270: 27014-27021.
30. Oussatcheva EA, Hashem VI, Zou Y, Sinden RR, Potaman VN (2001) Involvement of the nucleotide excision repair protein UvrA in instability of CAG*CTG repeat sequences in Escherichia coli. J Biol Chem 276: 30878-30884.
31. Jakupciak JP, Wells RD (2000) Genetic instabilities of triplet repeat sequences by recombination. IUBMB Life 50: 355-359. (Pubitemid 32285197)
32. Ohshima K, Montermini L, Wells RD, 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 273: 14588-14595. (Pubitemid 28319183)
33. Krasilnikova MM, Mirkin SM (2004) Replication stalling at Friedreich's ataxia (GAA)n repeats in vivo. Mol Cell Biol 24: 2286-2295. (Pubitemid 38325985)
34. Chandok GS, Patel MP, Mirkin SM, Krasilnikova MM (2012) Effects of Friedreich's ataxia GAA repeats on DNA replication in mammalian cells. Nucleic Acids Res 40: 3964-3974.
35. Shah KA, Shishkin AA, Voineagu I, Pavlov YI, Shcherbakova PV, et al. (2012) Role of DNA polymerases in repeat-mediated genome instability. Cell Rep 2: 1088-1095.
36. Follonier C, Oehler J, Herrador R, Lopes M (2013) Friedreich's ataxiaassociated GAA repeats induce replication-fork reversal and unusual molecular junctions. Nat Struct Mol Biol 20: 486-494.
37. Pollard LM, Bourn RL, Bidichandani SI (2008) Repair of DNA double-strand breaks within the (GAA*TTC)n sequence results in frequent deletion of the triplet-repeat sequence. Nucleic Acids Res 36: 489-500. (Pubitemid 351250440)
38. Kim HM, Narayanan V, Mieczkowski PA, Petes TD, Krasilnikova MM, et al. (2008) Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair. EMBO J 27: 2896-2906.
39. Tang W, Dominska M, Gawel M, Greenwell PW, Petes TD (2013) Genomic deletions and point mutations induced in Saccharomyces cerevisiae by the trinucleotide repeats (GAA.TTC) associated with Friedreich's ataxia. DNA Repair (Amst) 12: 10-17.
40. De Biase I, Rasmussen A, Endres D, Al-Mahdawi S, Monticelli A, et al. (2007) Progressive GAA expansions in dorsal root ganglia of Friedreich's ataxia patients. Ann Neurol 61: 55-60. (Pubitemid 46214244)
41. Bourn RL, De Biase I, Pinto RM, Sandi C, Al-Mahdawi S, et al. (2012) Pms2 suppresses large expansions of the (GAA.TTC)n sequence in neuronal tissues. PLoS One 7: e47085.
42. Halabi A, Ditch S, Wang J, Grabczyk E (2012) DNA mismatch repair complex MutSbeta promotes GAA.TTC repeat expansion in human cells. J Biol Chem 287: 29958-29967.
43. Du J, Campau E, Soragni E, Ku S, Puckett JW, et al. (2012) Role of mismatch repair enzymes in GAA.TTC triplet-repeat expansion in Friedreich ataxia induced pluripotent stem cells. J Biol Chem 287: 29861-29872.
44. Hick A, Wattenhofer-Donze M, Chintawar S, Tropel P, Simard JP, et al. (2013) Neurons and cardiomyocytes derived from induced pluripotent stem cells as a model for mitochondrial defects in Friedreich's ataxia. Dis Model Mech 6: 608-621.
45. Ku S, Soragni E, Campau E, Thomas EA, Altun G, et al. (2010) Friedreich's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability. Cell Stem Cell 7: 631-637.
46. Richardson TE, Kelly HN, Yu AE, Simpkins JW (2013) Therapeutic strategies in Friedreich's ataxia. Brain Res 1514: 91-97.
47. Gottesfeld JM, Rusche JR, Pandolfo M (2013) Increasing frataxin gene expression with histone deacetylase inhibitors as a therapeutic approach for Friedreich's ataxia. J Neurochem 126 Suppl 1: 147-154.
48. De Michele G, Cavalcanti F, Criscuolo C, Pianese L, Monticelli A, et al. (1998) Parental gender, age at birth and expansion length influence GAA repeat intergenerational instability in the 625 gene: pedigree studies and analysis of sperm from patients with Friedreich's ataxia. Hum Mol Genet 7: 1901-1906. (Pubitemid 28499421)
49. Sharma R, Bhatti S, Gomez M, Clark RM, Murray C, et al. (2002) The GAA triplet-repeat sequence in Friedreich ataxia shows a high level of somatic instability in vivo, with a significant predilection for large contractions. Hum Mol Genet 11: 2175-2187. (Pubitemid 34994006)
50. Hashem VI, Sinden RR (2002) Chemotherapeutically induced deletion of expanded triplet repeats. Mutat Res 508: 107-119.
51. Hashem VI, Pytlos MJ, Klysik EA, Tsuji K, Khajavi M, et al. (2004) Chemotherapeutic deletion of CTG repeats in lymphoblast cells from DM1 patients. Nucleic Acids Res 32: 6334-6346. (Pubitemid 40202092)
52. Lai Y, Xu M, Zhang Z, Liu Y (2013) Instability of CTG repeats is governed by the position of a DNA base lesion through base excision repair. PLoS One 8: e56960.
53. Kovtun IV, Liu Y, Bjoras M, Klungland A, Wilson SH, et al. (2007) OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 447: 447-452. (Pubitemid 46816735)
54. Entezam A, Lokanga AR, Le W, Hoffman G, Usdin K (2010) Potassium bromate, a potent DNA oxidizing agent, exacerbates germline repeat expansion in a fragile X premutation mouse model. Hum Mutat 31: 611-616.
55. Liu Y, Wilson SH (2012) DNA base excision repair: a mechanism of trinucleotide repeat expansion. Trends Biochem Sci 37: 162-172.
56. Liu Y, Prasad R, Beard WA, Hou EW, Horton JK, et al. (2009) Coordination between polymerase beta and FEN1 can modulate CAG repeat expansion. J Biol Chem 284: 28352-28366.
57. Xu M, Gabison J, Liu Y (2013) Trinucleotide repeat deletion via a unique hairpin bypass by DNA polymerase beta and alternate flap cleavage by flap endonuclease 1. Nucleic Acids Res 41: 1684-1697.
58. Calabrese V, Lodi R, Tonon C, D'Agata V, Sapienza M, et al. (2005) Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J Neurol Sci 233: 145-162. (Pubitemid 40812334)
59. Armstrong JS, Khdour O, Hecht SM (2010) Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question. FASEB J 24: 2152-2163.
60. Mrugala MM, Chamberlain MC (2008) Mechanisms of disease: temozolomide and glioblastoma-look to the future. Nat Clin Pract Oncol 5: 476-486.
61. Tang JB, Svilar D, Trivedi RN, Wang XH, Goellner EM, et al. (2011) Nmethylpurine DNA glycosylase and DNA polymerase beta modulate BER inhibitor potentiation of glioma cells to temozolomide. Neuro Oncol 13: 471-486.
62. Wood RD, Mitchell M, Sgouros J, Lindahl T (2001) Human DNA repair genes. Science 291: 1284-1289. (Pubitemid 32173086)
63. Sobol RW, Wilson SH (2001) Mammalian DNA beta-polymerase in base excision repair of alkylation damage. Proc Natl Acad Sci U S A 68: 57-74. (Pubitemid 33804653)
64. Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW (2005) The role of base excision repair in the sensitivity and resistance to temozolomidemediated cell death. Cancer Res 65: 6394-6400. (Pubitemid 40994427)
65. Liu Y, Beard WA, Shock DD, Prasad R, Hou EW, et al. (2005) DNA polymerase beta and flap endonuclease 1 enzymatic specificities sustain DNA synthesis for long patch base excision repair. J Biol Chem 280: 3665-3674. (Pubitemid 40223834)
66. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175: 184-191.
67. Olive PL, Banath JP, Durand RE (1990) Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the "comet" assay. Radiat Res 122: 86-94. (Pubitemid 20130057)
68. Olive PL, Banath JP (1995) Sizing highly fragmented DNA in individual apoptotic cells using the comet assay and a DNA crosslinking agent. Exp Cell Res 221: 19-26.
69. Biade S, Sobol RW, Wilson SH, Matsumoto Y (1998) Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA. J Biol Chem 273: 898-902. (Pubitemid 28049182)
70. Emond M, Lepage G, Vanasse M, Pandolfo M (2000) Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology 55: 1752-1753.
71. Schulz JB, Dehmer T, Schols L, Mende H, Hardt C, et al. (2000) Oxidative stress in patients with Friedreich ataxia. Neurology 55: 1719-1721.
72. Wells RD, Dere R, Hebert ML, Napierala M, Son LS (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res 33: 3785-3798. (Pubitemid 41418548)
73. Mirkin SM (2007) Expandable DNA repeats and human disease. Nature 447: 932-940. (Pubitemid 46975760)
74. Friedman HS, Kerby T, Calvert H (2000) Temozolomide and treatment of malignant glioma. Clin Cancer Res 6: 2585-2597. (Pubitemid 30482092)
75. Dinnes J, Cave C, Huang S, Milne R (2002) A rapid and systematic review of the effectiveness of temozolomide for the treatment of recurrent malignant glioma. Br J Cancer 86: 501-505. (Pubitemid 34185082)
76. Ditch S, Sammarco MC, Banerjee A, Grabczyk E (2009) Progressive GAA.TTC repeat expansion in human cell lines. PLoS Genet 5: e1000704.
77. Davies PA, Gray G (2002) Long-range PCR. Methods Mol Biol 187: 51-55.
78. De Biase I, Rasmussen A, Monticelli A, Al-Mahdawi S, Pook M, et al. (2007) Somatic instability of the expanded GAA triplet-repeat sequence in Friedreich ataxia progresses throughout life. Genomics 90: 1-5. (Pubitemid 46891744)
79. Wells RD (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem Sci 32: 271-278. (Pubitemid 46874927)