A single strand that links multiple neuropathologies in human disease

Brain

Volumn 136, Issue 1, 2013, Pages 14-27

  Reynolds, John J ^a   Stewart, Grant S ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

ataxia oculomotor apraxia; DNA single strand break repair; microcephaly; neurodegeneration; spinocerebellar ataxia

Indexed keywords

APRAXIA; ATAXIA; ATAXIA OCULOMOTOR APRAXIA 1; ATAXIA OCULOMOTOR APRAXIA 2; DEVELOPMENTAL DISORDER; DNA REPAIR; GENE MUTATION; HUMAN; INTRACTABLE EPILEPSY; MICROCEPHALY; NERVE DEGENERATION; NEUROPATHOLOGY; PRIORITY JOURNAL; REVIEW; SINGLE STRANDED DNA BREAK; SPINOCEREBELLAR ATAXIA WITH AXONAL NEUROPATHY 1;

EID: 84873326535     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws310     Document Type: Review

References (149)

1. Ahel I, Rass U, El-Khamisy SF, Katyal S, Clements PM, McKinnon PJ, et al. The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 2006; 443: 713-16.
2. Airoldi G, Guidarelli A, Cantoni O, Panzeri C, Vantaggiato C, Bonato S, et al. Characterization of two novel SETX mutations in AOA2 patients reveals aspects of the pathophysiological role of senataxin. Neurogenetics 2010; 11: 91-100.
3. Anheim M, Monga B, Fleury M, Charles P, Barbot C, Salih M, et al. Ataxia with oculomotor apraxia type 2: clinical, biological and genotype/phenotype correlation study of a cohort of 90 patients. Brain 2009; 132 (Pt 10): 2688-98.
4. Anheim M, Tranchant C, Koenig M. The autosomal recessive cerebellar ataxias. N Engl J Med 2012; 366: 636-46.
5. Armstrong J S, Khdour O, Hecht SM. Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question. FASEB J 2010; 24: 2152-63.
6. Arning L, Schols L, Cin H, Souquet M, Epplen JT, Timmann D. Identification and characterisation of a large senataxin (SETX) gene duplication in ataxia with ocular apraxia type 2 (AOA2). Neurogenetics 2008; 9: 295-9.
7. Avemann K, Knippers R, Koller T, Sogo JM. Camptothecin, a specific inhibitor of type I DNA topoisomerase, induces DNA breakage at replication forks. Mol Cell Biol 1988; 8: 3026-34.
8. Barzilai A. The contribution of the DNA damage response to neuronal viability. Antioxid Redox Signal 2007; 9: 211-18.
9. Becherel OJ, Jakob B, Cherry AL, Gueven N, Fusser M, Kijas AW, et al. CK2 phosphorylation-dependent interaction between aprataxin and MDC1 in the DNA damage response. Nucleic Acids Res 2010; 38: 1489-503.
10. Bendixen C, Thomsen B, Alsner J, Westergaard O. Camptothecin-stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry 1990; 29: 5613-19.
11. Bernstein NK, Williams RS, Rakovszky ML, Cui D, Green R, Karimi-Busheri F, et al. The molecular architecture of the mammalian DNA repair enzyme, polynucleotide kinase. Mol Cell 2005; 17: 657-70.
12. Brooks PJ, Cheng TF, Cooper L. Do all of the neurologic diseases in patients with DNA repair gene mutations result from the accumulation of DNA damage? DNA Repair (Amst) 2008; 7: 834-48.
13. Cadet J, Douki T, Gasparutto D, Ravanat JL. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat Res 2003; 531: 5-23.
14. Caldecott KW. Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays 2001; 23: 447-55.
15. Caldecott KW. XRCC1 and DNA strand break repair. DNA Repair (Amst) 2003; 2: 955-69.
16. Caldecott KW. Single-strand break repair and genetic disease. Nat Rev Genet 2008; 9: 619-31.
17. Caldecott KW, Aoufouchi S, Johnson P, Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res 1996; 24: 4387-94.
18. Campalans A, Marsin S, Nakabeppu, O'Connor TR, Boiteux S, Radicella JP. XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair. DNA Repair (Amst) 2005; 4: 826-35.
19. Carmichael J, Woods C. Genetic defects of human brain development. Curr Neurol Neurosci Rep 2006; 6: 437-46.
20. Castellotti B, Mariotti C, Rimoldi M, Fancellu R, Plumari M, Caimi S, et al. Ataxia with oculomotor apraxia type1 (AOA1): novel and recurrent aprataxin mutations, coenzyme Q10 analyses, and clinical findings in Italian patients. Neurogenetics 2011; 12: 193-201.
21. Chen L, Lee HM, Greeley GH Jr, Englander EW. Accumulation of oxidatively generated DNA damage in the brain: a mechanism of neurotoxicity. Free Radic Biol Med 2007; 42: 385-93.
22. Chen YZ, Bennett CL, Huynh HM, Blair IP, Puls I, Irobi J, et al. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am J Hum Genet 2004; 74: 1128-35.
23. Chen YZ, Hashemi SH, Anderson SK, Huang Y, Moreira MC, Lynch DR, et al. Senataxin, the yeast Sen1p orthologue: characterization of a unique protein in which recessive mutations cause ataxia and dominant mutations cause motor neuron disease. Neurobiol Dis 2006; 23: 97-108.
24. Chiang SC, Carroll J, El-Khamisy SF. TDP1 serine 81 promotes interaction with DNA ligase IIIalpha and facilitates cell survival following DNA damage. Cell Cycle 2010; 9: 588-95.
25. Clements PM, Breslin C, Deeks ED, Byrd PJ, Ju L, Bieganowski P, et al. The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4. DNA Repair (Amst) 2004; 3: 1493-502.
26. Cox J, Jackson AP, Bond J, Woods CG. What primary microcephaly can tell us about brain growth. Trends Mol Med 2006; 12: 358-66.
27. Crimella C, Cantoni O, Guidarelli A, Vantaggiato C, Martinuzzi A, Fiorani M, et al. A novel nonsense mutation in the APTX gene associated with delayed DNA single-strand break removal fails to enhance sensitivity to different genotoxic agents. Hum Mutat 2011; 32: E2118-33.
28. Criscuolo C, Chessa L, Di Giandomenico S, Mancini P, Sacca F, Grieco GS, et al. Ataxia with oculomotor apraxia type 2: a clinical, pathologic, and genetic study. Neurology 2006; 66: 1207-10.
29. Custer SK, Garden GA, Gill N, Rueb U, Libby RT, Schultz C, et al. Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nat Neurosci 2006; 9: 1302-11.
30. Daley JM, Wilson TE, Ramotar D. Genetic interactions between HNT3/Aprataxin and RAD27/FEN1 suggest parallel pathways for 5' end processing during base excision repair. DNA Repair (Amst) 2010; 9: 690-9.
31. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 1999; 342 (Pt 2): 249-68.
32. Das BB, Antony S, Gupta S, Dexheimer TS, Redon CE, Garfield S, et al. Optimal function of the DNA repair enzyme TDP1 requires its phos-phorylation by ATM and/or DNA-PK. EMBO J 2009; 28: 3667-80.
33. Das BB, Dexheimer TS, Maddali K, Pommier Y. Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria. Proc Natl Acad Sci USA 2010; 107: 19790-5.
34. Date H, Onodera O, Tanaka H, Iwabuchi K, Uekawa K, Igarashi S, et al. Early-onset ataxia with ocular motor apraxia and hypoalbuminemia is caused by mutations in a new HIT superfamily gene. Nat Genet 2001; 29: 184-8.
35. De Amicis A, Piane M, Ferrari F, Fanciulli M, Delia D, Chessa L. Role of senataxin in DNA damage and telomeric stability. DNA Repair (Amst) 2011; 10: 199-209.
36. de Graaf-Peters VB, Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when? Early Hum Dev 2006; 82: 257-66.
37. de Planell-Saguer M, Schroeder DG, Rodicio MC, Cox GA, Mourelatos Z. Biochemical and genetic evidence for a role of IGHMBP2 in the trans-lational machinery. Hum Mol Genet 2009; 18: 2115-26.
38. Deckbar D, Birraux J, Krempler A, Tchouandong L, Beucher A, Walker S, et al. Chromosome breakage after G2 checkpoint release. J Cell Biol 2007; 176: 749-55.
39. Dianov G, Price A, Lindahl T. Generation of single-nucleotide repair patches following excision of uracil residues from DNA. Mol Cell Biol 1992; 12: 1605-12.
40. DiGiuseppe JA, Dresler SL. Bleomycin-induced DNA repair synthesis in permeable human fibroblasts: mediation of long-patch and short-patch repair by distinct DNA polymerases. Biochemistry 1989; 28: 9515-20.
41. El-Khamisy SF, Caldecott KW. TDP1-dependent DNA single-strand break repair and neurodegeneration. Mutagenesis 2006; 21: 219-24.
42. El-Khamisy SF, Hartsuiker E, Caldecott KW. TDP1 facilitates repair of ionizing radiation-induced DNA single-strand breaks. DNA Repair (Amst) 2007; 6: 1485-95.
43. El-Khamisy SF, Katyal S, Patel P, Ju L, McKinnon PJ, Caldecott KW. Synergistic decrease of DNA single-strand break repair rates in mouse neural cells lacking both Tdp1 and aprataxin. DNA Repair (Amst) 2009; 8: 760-6.
44. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res 2003; 31: 5526-33.
45. El-Khamisy SF, Saifi GM, Weinfeld M, Johansson F, Helleday T, Lupski JR, et al. Defective DNA single-strand break repair in spinocer-ebellar ataxia with axonal neuropathy-1. Nature 2005; 434: 108-13.
46. Ellenberger T, Tomkinson AE. Eukaryotic DNA ligases: structural and functional insights. Annu Rev Biochem 2008; 77: 313-38.
47. Evans MD, Griffiths HR, Lunec J. Reactive oxygen species and their cyto-toxic mechanisms. In: Chipman JK. Mechanisms of cell toxicity. Vol. 20. London: JAI Press Inc.; 1997. p. 25-73.
48. Finkel JS, Chinchilla K, Ursic D, Culbertson MR. Sen1p performs two genetically separable functions in transcription and processing of U5 small nuclear RNA in Saccharomyces cerevisiae. Genetics 2010; 184: 107-18.
49. Flangas AL, Bowman RE. Differential metabolism of RNA in neuronal-enriched and glial-enriched fractions of rat cerebrum. J Neurochem 1970; 17: 1237-45.
50. Frosina G, Fortini P, Rossi O, Carrozzino F, Raspaglio G, Cox LS, et al. Two pathways for base excision repair in mammalian cells. J Biol Chem 1996; 271: 9573-8.
51. Gatz SA, Ju L, Gruber R, Hoffmann E, Carr AM, Wang ZQ, et al. Requirement for DNA ligase IV during embryonic neuronal development. J Neurosci 2011; 31: 10088-100.
52. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res 1989; 17: 4713-30.
53. Grohmann K, Schuelke M, Diers A, Hoffmann K, Lucke B, Adams C, et al. Mutations in the gene encoding immunoglobulin mu-binding protein 2 cause spinal muscular atrophy with respiratory distress type 1. Nat Genet 2001; 29: 75-7.
54. Gueven N, Becherel OJ, Kijas AW, Chen P, Howe O, Rudolph JH, et al. Aprataxin, a novel protein that protects against genotoxic stress. Hum Mol Genet 2004; 13: 1081-93.
55. Gueven N, Chen P, Nakamura J, Becherel OJ, Kijas AW, GrattanSmith P, et al. A subgroup of spinocerebellar ataxias defective in DNA damage responses. Neuroscience 2007; 145: 1418-25.
56. Harris JL, Jakob B, Taucher-Scholz G, Dianov GL, Becherel OJ, Lavin MF. Aprataxin, poly-ADP ribose polymerase 1 (PARP-1) and apurinic endo-nuclease 1 (APE1) function together to protect the genome against oxidative damage. Hum Mol Genet 2009; 18: 4102-17.
57. Hindle JV. Ageing, neurodegeneration and Parkinson's disease. Age Ageing 2010; 39: 156-161.
58. Hirano M, Yamamoto A, Mori T, Lan L, Iwamoto TA, Aoki M, et al. DNA single-strand break repair is impaired in aprataxin-related ataxia. Ann Neurol 2007; 61: 162-74.
59. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411: 366-74.
60. Hoshino K, Kameyama Y. Developmental-stage-dependent radiosensitiv-ity of neural cells in the ventricular zone of telencephalon in mouse and rat fetuses. Teratology 1988; 37: 257-62.
61. Hoshino K, Kameyama Y, Inouye M. Split-dose effect of X-irradiation on the induction of cell death in the fetal mouse brain. J Radiat Res 1991; 32: 23-27.
62. Hung CW, Chen YC, Hsieh WL, Chiou SH, Kao CL. Ageing and neurodegenerative diseases. Ageing Res Rev 2010; 9 (Suppl 1): S36-46.
63. Iida T, Furuta A, Nishioka K, Nakabeppu Y, Iwaki T. Expression of 8-oxoguanine DNA glycosylase is reduced and associated with neuro-fibrillary tangles in Alzheimer's disease brain. Acta Neuropathol 2002; 103: 20-25.
64. Inamdar KV, Pouliot JJ, Zhou T, Lees-Miller SP, Rasouli-Nia A, Povirk LF. Conversion of phosphoglycolate to phosphate termini on 3' overhangs of DNA double strand breaks by the human tyrosyl-DNA phospho-diesterase hTdp1. J Biol Chem 2002; 277: 27162-8.
65. Interthal H, Chen HJ, Kehl-Fie TE, Zotzmann J, Leppard JB, Champoux JJ. SCAN1 mutant Tdp1 accumulates the enzyme-DNA intermediate and causes camptothecin hypersensitivity. EMBO J 2005; 24: 2224-33.
66. Interthal H, Pouliot JJ, Champoux JJ. The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proc Natl Acad Sci USA 2001; 98: 12009-14.
67. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461: 1071-1078.
68. Jakob B, Rudolph JH, Gueven N, Lavin MF, Taucher-Scholz G. Live cell imaging of heavy-ion-induced radiation responses by beamline microscopy. Radiat Res 2005; 163: 681-90.
69. Jeppesen DK, Bohr VA, Stevnsner T. DNA repair deficiency in neurode-generation. Prog Neurobiol 2011; 94: 166-200.
70. Karimi-Busheri F, Rasouli-Nia A, Allalunis-Turner J, Weinfeld M. Human polynucleotide kinase participates in repair of DNA double-strand breaks by nonhomologous end joining but not homologous recombination. Cancer Res 2007; 67: 6619-25.
71. Katyal S, el-Khamisy SF, Russell HR, Li Y, Ju L, Caldecott KW, et al. TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J 2007; 26: 4720-31.
72. Kim HD, Choe J, Seo YS. The sen1(+) gene of Schizosaccharomyces pombe, a homologue of budding yeast SEN1, encodes an RNA and DNA helicase. Biochemistry 1999; 38: 14697-710.
73. Kim K, Biade S, Matsumoto Y. Involvement of flap endonuclease 1 in base excision DNA repair. J Biol Chem 1998; 273: 8842-8.
74. Kim MY, Zhang T, Kraus WL. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD + into a nuclear signal. Genes Dev 2005; 19: 1951-67.
75. Klungland A, Lindahl T. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J 1997; 16: 3341-8.
76. Koch CA, Agyei R, Galicia S, Metalnikov P, O'Donnell P, Starostine A, et al. Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. EMBO J 2004; 23: 3874-85.
77. Kouzminova EA, Kuzminov A. Fragmentation of replicating chromosomes triggered by uracil in DNA. J Mol Biol 2006; 35520-33.
78. Kroeger PE, Rowe TC. Interaction of topoisomerase 1 with the transcribed region of the Drosophila HSP 70 heat shock gene. Nucleic Acids Res 1989; 17: 8495-509.
79. Kuzminov A. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci USA 2001; 98: 8241-6.
80. Lagercrantz H, Hanson MA, Ment LR, Peebles DM. The newborn brain: neuroscience and clinical applications. New York, NY: Cambridge University Press; 2010.
81. Le Ber I, Bouslam N, Rivaud-Pechoux S, Guimaraes J, Benomar A, Chamayou C, et al. Frequency and phenotypic spectrum of ataxia with oculomotor apraxia 2: a clinical and genetic study in 18 patients. Brain 2004; 127 (Pt 4): 759-67.
82. Le Ber I, Moreira MC, Rivaud-Pechoux S, Chamayou C, Ochsner F, Kuntzer T, et al. Cerebellar ataxia with oculomotor apraxia type 1: clinical and genetic studies. Brain 2003; 126 (Pt 12): 2761-72.
83. Lebedeva NA, Rechkunova NI, El-Khamisy SF, Lavrik OI. Tyrosyl-DNA phosphodiesterase 1 initiates repair of apurinic/apyrimidinic sites. Biochimie 2012; 94: 1749-53.
84. Lee Y, Katyal S, Li Y, El-Khamisy SF, Russell HR, Caldecott KW, et al. The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nat Neurosci 2009; 12: 973-80.
85. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362: 709-15.
86. Loizou JI, El-Khamisy SF, Zlatanou A, Moore DJ, Chan DW, Qin J, et al. The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell 2004; 117: 17-28.
87. Lovell MA, Xie C, Markesbery WR. Decreased base excision repair and increased helicase activity in Alzheimer's disease brain. Brain Res 2000; 855: 116-23.
88. Lu M, Mani RS, Karimi-Busheri F, Fanta M, Wang H, Litchfeld DW, et al. Independent mechanisms of stimulation of polynucleotide kinase/phosphatase by phosphorylated and non-phosphorylated XRCC1. Nucleic Acids Res 2010; 38: 510-21.
89. Luo H, Chan DW, Yang T, Rodriguez M, Chen BP, Leng M, et al. A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol Cell Biol 2004; 24: 8356-65.
90. Mani RS, Fanta M, Karimi-Busheri F, Silver E, Virgen CA, Caldecott KW, et al. XRCC1 stimulates polynucleotide kinase by enhancing its damage discrimination and displacement from DNA repair intermediates. J Biol Chem 2007; 282: 28004-13.
91. Marsin S, Vidal AE, Sossou M, Menissier-de Murcia J, Le Page F, Boiteux S, et al. Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1. J Biol Chem 2003; 278: 44068-74.
92. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G. XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 1998; 18: 3563-71.
93. McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet 2007; 8: 37-55.
94. Medghalchi SM, Frischmeyer PA, Mendell JT, Kelly AG, Lawler AM, Dietz HC. Rent1, a trans-effector of nonsense-mediated mRNA decay, is essential for mammalian embryonic viability. Hum Mol Genet 2001; 10: 99-105.
95. Mendell JT, Rhys CM, Dietz HC. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 2002; 298: 419-22.
96. Mochida GH, Walsh CA. Molecular genetics of human microcephaly. Curr Opin Neurol 2001; 14: 151-6.
97. Moreira MC, Barbot C, Tachi N, Kozuka N, Uchida E, Gibson T, et al. The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin. Nat Genet 2001; 29: 189-93.
98. Moreira MC, Klur S, Watanabe M, Nemeth AH, Le Ber I, Moniz JC, et al. Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat Genet 2004; 36: 225-7.
99. Mosesso P, Piane M, Palitti F, Pepe G, Penna S, Chessa L. The novel human gene aprataxin is directly involved in DNA single-strand-break repair. Cell Mol Life Sci 2005; 62: 485-91.
100. Nicholas AK, Swanson EA, Cox JJ, Karbani G, Malik S, Springell K, et al. The molecular landscape of ASPM mutations in primary microcephaly. J Med Genet 2009; 46: 249-53.
101. O'Connor TR, Laval J. Physical association of the 2, 6-diamino-4-hydroxy- 5N-formamidopyrimidine-DNA glycosylase of Escherichia coli and an activity nicking DNA at apurinic/apyrimidinic sites. Proc Natl Acad Sci USA 1989; 86: 5222-6.
102. O'Driscoll M, Cerosaletti KM, Girard PM, Dai Y, Stumm M, Kysela B, et al. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol Cell 2001; 8: 1175-85.
103. O'Driscoll M, Jeggo PA. The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders. DNA Repair (Amst) 2008; 7: 1039-50.
104. Pommier Y, Redon C, Rao VA, Seiler JA, Sordet O, Takemura H, et al. Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat Res 2003; 532: 173-203.
105. Pourquier P, Pilon AA, Kohlhagen G, Mazumder A, Sharma A, Pommier Y. Trapping of mammalian topoisomerase I and recombinations induced by damaged DNA containing nicks or gaps. Importance of DNA end phosphorylation and camptothecin effects. J Biol Chem 1997; 272: 26441-7.
106. Rasmussen TP, Culbertson MR. The putative nucleic acid helicase Sen1p is required for formation and stability of termini and for maximal rates of synthesis and levels of accumulation of small nucleolar RNAs in Saccharomyces cerevisiae. Mol Cell Biol 1998; 18: 6885-96.
107. Rass U, Ahel I, West SC. Actions of aprataxin in multiple DNA repair pathways. J Biol Chem 2007; 282: 9469-74.
108. Rass U, Ahel I, West SC. Molecular mechanism of DNA deadenylation by the neurological disease protein aprataxin. J Biol Chem 2008; 283: 33994-4001.
109. Reynolds JJ, El-Khamisy SF, Katyal S, Clements P, McKinnon PJ, Caldecott KW. Defective DNA ligation during short-patch single-strand break repair in ataxia oculomotor apraxia 1. Mol Cell Biol 2009; 29: 1354-62.
110. Reynolds JJ, Walker AK, Gilmore EC, Walsh CA, Caldecott KW. Impact of PNKP mutations associated with microcephaly, seizures and developmental delay on enzyme activity and DNA strand break repair. Nucleic Acids Res 2012; 40: 6608-19.
111. Robertson AB, Klungland A, Rognes T, Leiros I. DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci 2009; 66: 981-93.
112. Roca J. The mechanisms of DNA topoisomerases. Trends Biochem Sci 1995; 20: 156-60.
113. Ryan AJ, Squires S, Strutt HL, Johnson RT. Camptothecin cytotoxicity in mammalian cells is associated with the induction of persistent double strand breaks in replicating DNA. Nucleic Acids Res 1991; 19: 3295-300.
114. Sacho EJ, Maizels N. DNA repair factor MRE11/RAD50 cleaves 3'-phosphotyrosyl bonds and resects DNA to repair damage caused by topoisomerase 1 poisons. J Biol Chem 2011; 286: 44945-51.
115. Sarkander HI, Uthoff CG. Comparison of the number of RNA initiation sites in rat brain fractions enriched in neuronal or glial nuclei. FEBS Lett 1976; 72: 53-6.
116. Sarnat HB, Flores-Sarnat L. Integrative classification of morphology and molecular genetics in central nervous system malformations. Am J Med Genet A 2004; 126A: 386-92.
117. Schols L, Arning L, Schule R, Epplen JT, Timmann D. "Pseudodominant inheritance" of ataxia with ocular apraxia type 2 (AOA2). J Neurol 2008; 255: 495-501.
118. Segal-Raz H, Mass G, Baranes-Bachar K, Lerenthal Y, Wang SY, Chung YM, et al. ATM-mediated phosphorylation of polynucleotide kinase/phosphatase is required for effective DNA double-strand break repair. EMBO Rep 2011; 12: 713-19.
119. Sekijima Y, Ohara S, Nakagawa S, Tabata K, Yoshida K, Ishigame H, et al. Hereditary motor and sensory neuropathy associated with cere-bellar atrophy (HMSNCA): clinical and neuropathological features of a Japanese family. J Neurol Sci 1998; 158: 30-7.
120. Shao C, Xiong S, Li GM, Gu L, Mao G, Markesbery WR, et al. Altered 8-oxoguanine glycosylase in mild cognitive impairment and late-stage Alzheimer's disease brain. Free Radic Biol Med 2008; 45: 813-19.
121. Shen J, Gilmore EC, Marshall CA, Haddadin M, Reynolds JJ, Eyaid W, et al. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat Genet 2010; 42: 245-49.
122. Shuman S. Vaccinia virus DNA ligase: specificity, fidelity, and inhibition. Biochemistry 1995; 34: 16138-47.
123. Skourti-Stathaki K, Proudfoot NJ, Gromak N. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol Cell 2011; 42: 794-805.
124. Sriskanda V, Shuman S. Specificity and fidelity of strand joining by Chlorella virus DNA ligase. Nucleic Acids Res 1998; 26: 3536-41.
125. Sugawara M, Wada C, Okawa S, Kobayashi M, Sageshima M, Imota T, et al. Purkinje cell loss in the cerebellar flocculus in patients with ataxia with ocular motor apraxia type 1/early-onset ataxia with ocular motor apraxia and hypoalbuminemia. Eur Neurol 2008; 59: 18-23.
126. Suraweera A, Becherel OJ, Chen P, Rundle N, Woods R, Nakamura J, et al. Senataxin, defective in ataxia oculomotor apraxia type 2, is involved in the defense against oxidative DNA damage. J Cell Biol 2007; 177: 969-79.
127. Suraweera A, Lim Y, Woods R, Birrell GW, Nasim T, Becherel OJ, et al. Functional role for senataxin, defective in ataxia oculomotor apraxia type 2, in transcriptional regulation. Hum Mol Genet 2009; 18: 3384-96.
128. Sykora P, Croteau DL, Bohr VA, Wilson DM 3rd. Aprataxin localizes to mitochondria and preserves mitochondrial function. Proc Natl Acad Sci USA 2011; 108: 7437-42.
129. Takahashi T, Tada M, Igarashi S, Koyama A, Date H, Yokoseki A, et al. Aprataxin, causative gene product for EAOH/AOA1, repairs DNA single-strand breaks with damaged 3'-phosphate and 3'-phosphogly-colate ends. Nucleic Acids Res 2007; 35: 3797-809.
130. Takashima H, Boerkoel CF, John J, Saifi GM, Salih MA, Armstrong D, et al. Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat Genet 2002; 32: 267-72.
131. Taylor AM, Byrd PJ. Molecular pathology of ataxia telangiectasia. J Clin Pathol 2005; 58: 1009-15.
132. Tazir M, Ali-Pacha L, M'Zahem A, Delaunoy JP, Fritsch M, Nouioua S, et al. Ataxia with oculomotor apraxia type 2: a clinical and genetic study of 19 patients. J Neurol Sci 2009; 278: 77-81.
133. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, Thompson LH, et al. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 1999; 208: 513-29.
134. Tebbs RS, Thompson LH, Cleaver JE. Rescue of Xrcc1 knockout mouse embryo lethality by transgene-complementation. DNA Repair (Amst) 2003; 2: 1405-17.
135. Thornton GK, Woods CG. Primary microcephaly: do all roads lead to Rome? Trends Genet 2009; 25: 501-10.
136. Ursic D, Chinchilla K, Finkel JS, Culbertson MR. Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic Acids Res 2004; 32: 2441-52.
137. Ursic D, Himmel KL, Gurley KA, Webb F, Culbertson MR. The yeast SEN1 gene is required for the processing of diverse RNA classes. Nucleic Acids Res 1997; 25: 4778-85.
138. Walton C, Interthal H, Hirano R, Salih MA, Takashima H, Boerkoel CF. Spinocerebellar ataxia with axonal neuropathy. Adv Exp Med Biol 2010; 685: 75-83.
139. Wang JC. Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 2002; 3: 430-40.
140. Wang W, Czaplinski K, Rao Y, Peltz SW. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J 2001; 20: 880-90.
141. Ward J. Nature of lesions formed by ionising radiation. In: JA N. DNA damage and repair. Vol. 2: DNA repair in higher eukaryotes. Totowa, NJ: Human Press Inc.; 1998. p. 65-84.
142. Ward JF, Evans JW, Limoli CL, Calabro-Jones PM. Radiation and hydrogen peroxide induced free radical damage to DNA. Br J Cancer Suppl 1987; 8: 105-112.
143. Weissman L, de Souza-Pinto NC, Stevnsner T, Bohr VA. DNA repair, mitochondria, and neurodegeneration. Neuroscience 2007; 145: 1318-29.
144. Whitehouse CJ, Taylor RM, Thistlethwaite A, Zhang H, Karimi-Busheri F, Lasko DD, et al. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 2001; 104: 107-17.
145. Wu J, Liu LF. Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res 1997; 25: 4181-6.
146. Yang SW, Burgin AB Jr, Huizenga BN, Robertson CA, Yao KC, Nash HA. A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc Natl Acad Sci USA 1996; 93: 11534-9.
147. Yokoseki A, Ishihara T, Koyama A, Shiga A, Yamada M, Suzuki C, et al. Genotype-phenotype correlations in early onset ataxia with ocular motor apraxia and hypoalbuminaemia. Brain 2011; 134 (Pt 5): 1387-99.
148. Zhou T, Lee JW, Tatavarthi H, Lupski JR, Valerie K, Povirk LF. Deficiency in 3'-phosphoglycolate processing in human cells with a hereditary mutation in tyrosyl-DNA phosphodiesterase (TDP1). Nucleic Acids Res 2005; 33: 289-297.
149. Zhou W, Doetsch PW. Transcription bypass or blockage at single-strand breaks on the DNA template strand: effect of different 3' and 5' flanking groups on the T7 RNA polymerase elongation complex. Biochemistry 1994; 33: 14926-34.