DNA strand break repair and neurodegeneration

DNA Repair

Volumn 12, Issue 8, 2013, Pages 558-567

  Rulten, Stuart L ^a   Caldecott, Keith W ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Ataxia; Development; DNA damage; DNA repair; Microcephaly; Neurodegeneration

Indexed keywords

ATM PROTEIN; ATR PROTEIN;

APRAXIA; ARTICLE; ATAXIA; ATAXIA TELANGIECTASIA; BRAIN DEVELOPMENT; CELL PROLIFERATION; CEREBELLAR ATAXIA; CLINICAL FEATURE; COCKAYNE SYNDROME; DNA END JOINING REPAIR; DNA REPAIR; DNA STRAND BREAKAGE; EMBRYO DEATH; HUMAN; MICROCEPHALY; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; PRIORITY JOURNAL; SECKEL SYNDROME; SEIZURE; SINGLE STRANDED DNA BREAK; SPINOCEREBELLAR DEGENERATION; XERODERMA PIGMENTOSUM;

ATAXIA; DEVELOPMENT; DNA DAMAGE; DNA REPAIR; MICROCEPHALY; NEURODEGENERATION;

ANIMALS; BRAIN; CEREBELLAR ATAXIA; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA REPAIR-DEFICIENCY DISORDERS; HUMANS; MUTATION; NEUROGENESIS; NEURONS;

MUS MUSCULUS;

EID: 84880596255     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.04.008     Document Type: Article

References (156)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
2. Mitchell J.R., Hoeijmakers J.H., Niedernhofer L.J. Divide and conquer: nucleotide excision repair battles cancer and ageing. Curr. Opin. Cell Biol. 2003, 15:232-240.
3. Rouse J., Jackson S.P. Interfaces between the detection, signaling, and repair of DNA damage. Science 2002, 297:547-551.
4. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411:366-374.
5. O'Driscoll M., Jeggo P.A. The role of double-strand break repair-insights from human genetics. Nat. Rev. Genet. 2006, 7:45-54.
6. McKinnon P.J., Caldecott K.W. DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet. 2007, 8:37-55.
7. Hoeijmakers J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 2009, 361:1475-1485.
8. Morris L.G., Veeriah S., Chan T.A. Genetic determinants at the interface of cancer and neurodegenerative disease. Oncogene 2010, 29:3453-3464.
9. Sidman R.L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973, 62:1-35.
10. Zecevic N., Hu F., Jakovcevski I. Interneurons in the developing human neocortex. Dev. Neurobiol. 2011, 71:18-33.
11. Letinic K., Zoncu R., Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 2002, 417:645-649.
12. LaMonica B.E., Lui J.H., Wang X., Kriegstein A.R. OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr Opin Neurobiol 2012, 22:747-753.
13. Sanai N., Nguyen T., Ihrie R.A., Mirzadeh Z., Tsai H.H., Wong M., Gupta N., Berger M.S., Huang E., Garcia-Verdugo J.M., Rowitch D.H., Alvarez-Buylla A. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 2011, 478:382-386.
14. Bayatti N., Moss J.A., Sun L., Ambrose P., Ward J.F., Lindsay S., Clowry G.J. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb. Cortex 2008, 18:1536-1548.
15. Zecevic N., Chen Y., Filipovic R. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J. Comp. Neurol. 2005, 491:109-122.
16. Jackson S.P. Sensing and repairing DNA double-strand breaks. Carcinogenesis 2002, 23:687-696.
17. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 2010, 79:181-211.
18. Weterings E., Chen D.J. The endless tale of non-homologous end-joining. Cell Res. 2008, 18:114-124.
19. Moynahan M.E., Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 2010, 11:196-207.
20. Mao Z., Bozzella M., Seluanov A., Gorbunova V. DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle 2008, 7:2902-2906.
21. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., Takeda S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 2006, 5:1021-1029.
22. Orii K.E., Lee Y., Kondo N., McKinnon P.J. Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc. Natl. Acad. Sci. USA 2006, 103:10017-10022.
23. Alter B.P., Rosenberg P.S., Brody L.C. Clinical and molecular features associated with biallelic mutations in FANCD1/BRCA2. J. Med. Genet. 2007, 44:1-9.
24. Fattah K.R., Ruis B.L., Hendrickson E.A. Mutations to Ku reveal differences in human somatic cell lines. DNA Repair (Amst.) 2008, 7:762-774.
25. Li G., Nelsen C., Hendrickson E.A. Ku86 is essential in human somatic cells. Proc. Natl. Acad. Sci. USA 2002, 99:832-837.
26. Buck D., Malivert L., de Chasseval R., Barraud A., Fondaneche M.C., Sanal O., Plebani A., Stephan J.L., Hufnagel M., le Deist F., Fischer A., Durandy A., de Villartay J.P., Revy P. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006, 124:287-299.
27. O'Driscoll M., Cerosaletti K.M., Girard P.M., Dai Y., Stumm M., Kysela B., Hirsch B., Gennery A., Palmer S.E., Seidel J., Gatti R.A., Varon R., Oettinger M.A., Neitzel H., Jeggo P.A., Concannon P. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 2001, 8:1175-1185.
28. van der Burg M., Ijspeert H., Verkaik N.S., Turul T., Wiegant W.W., Morotomi-Yano K., Mari P.O., Tezcan I., Chen D.J., Zdzienicka M.Z., van Dongen J.J., van Gent D.C. A DNA-PKcs mutation in a radiosensitive T-B-SCID patient inhibits Artemis activation and nonhomologous end-joining. J. Clin. Invest. 2009, 119:91-98.
29. Nussenzweig A., Chen C., da Costa Soares V., Sanchez M., Sokol K., Nussenzweig M.C., Li G.C. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 1996, 382:551-555.
30. Ouyang H., Nussenzweig A., Kurimasa A., Soares V.C., Li X., Cordon-Cardo C., Li W., Cheong N., Nussenzweig M., Iliakis G., Chen D.J., Li G.C. Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination in vivo. J. Exp. Med. 1997, 186:921-929.
31. Barnes D.E., Stamp G., Rosewell I., Denzel A., Lindahl T. Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 1998, 8:1395-1398.
32. Frank K.M., Sekiguchi J.M., Seidl K.J., Swat W., Rathbun G.A., Cheng H.L., Davidson L., Kangaloo L., Alt F.W. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 1998, 396:173-177.
33. Gao Y., Sun Y., Frank K.M., Dikkes P., Fujiwara Y., Seidl K.J., Sekiguchi J.M., Rathbun G.A., Swat W., Wang J., Bronson R.T., Malynn B.A., Bryans M., Zhu C., Chaudhuri J., Davidson L., Ferrini R., Stamato T., Orkin S.H., Greenberg M.E., Alt F.W. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 1998, 95:891-902.
34. Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 2001, 11:71-77.
35. Durocher D., Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 2001, 13:225-231.
36. Shechter D., Costanzo V., Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 2004, 6:648-655.
37. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
38. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Ferguson D.O., Zhu C., Manis J.P., Horner J., DePinho R.A., Alt F.W. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 2000, 5:993-1002.
39. Gatz S.A., Ju L., Gruber R., Hoffmann E., Carr A.M., Wang Z.Q., Liu C., Jeggo P.A. Requirement for DNA ligase IV during embryonic neuronal development. J. Neurosci. 2011, 31:10088-10100.
40. Lee Y., Chong M.J., McKinnon P.J. Ataxia telangiectasia mutated-dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status. J. Neurosci. 2001, 21:6687-6693.
41. Taylor A.M., Byrd P.J. Molecular pathology of ataxia telangiectasia. J. Clin. Pathol. 2005, 58:1009-1015.
42. Lakin N.D., Weber P., Stankovic T., Rottinghaus S.T., Taylor A.M., Jackson S.P. Analysis of the ATM protein in wild-type and ataxia telangiectasia cells. Oncogene 1996, 13:2707-2716.
43. Frappart P.O., McKinnon P.J. Ataxia-telangiectasia and related diseases. Neuromolecular Med. 2006, 8:495-511.
44. Vinters H.V., Gatti R.A., Rakic P. Sequence of cellular events in cerebellar ontogeny relevant to expression of neuronal abnormalities in ataxia-telangiectasia. Kroc Found. Ser. 1985, 19:233-255.
45. Paula-Barbosa M.M., Ruela C., Tavares M.A., Pontes C., Saraiva A., Cruz C. Cerebellar cortex ultrastructure in ataxia-telangiectasia. Ann. Neurol. 1983, 13:297-302.
46. Verhagen M.M., Martin J.J., van Deuren M., Ceuterick-de Groote C., Weemaes C.M., Kremer B.H., Taylor M.A., Willemsen M.A., Lammens M. Neuropathology in classical and variant ataxia-telangiectasia. Neuropathology 2012, 32:234-244.
47. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., Shiloh Y., Crawley J.N., Ried T., Tagle D., Wynshaw-Boris A. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
48. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 1996, 10:2411-2422.
49. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300:1542-1548.
50. Sleeth K.M., Sorensen C.S., Issaeva N., Dziegielewski J., Bartek J., Helleday T. RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J. Mol. Biol. 2007, 373:38-47.
51. Syljuasen R.G., Sorensen C.S., Hansen L.T., Fugger K., Lundin C., Johansson F., Helleday T., Sehested M., Lukas J., Bartek J. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol. Cell. Biol. 2005, 25:3553-3562.
52. Goodship J., Gill H., Carter J., Jackson A., Splitt M., Wright M. Autozygosity mapping of a Seckel syndrome locus to chromosome 3q22.1-q24. Am. J. Hum. Genet. 2000, 67:498-503.
53. O'Driscoll M., Ruiz-Perez V.L., Woods C.G., Jeggo P.A., Goodship J.A. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 2003, 33:497-501.
54. Brown E.J., Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000, 14:397-402.
55. de Klein A., Muijtjens M., van Os R., Verhoeven Y., Smit B., Carr A.M., Lehmann A.R., Hoeijmakers J.H. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 2000, 10:479-482.
56. Murga M., Bunting S., Montana M.F., Soria R., Mulero F., Canamero M., Lee Y., McKinnon P.J., Nussenzweig A., Fernandez-Capetillo O. A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging. Nat. Genet. 2009, 41:891-898.
57. Lee Y., Shull E.R., Frappart P.O., Katyal S., Enriquez-Rios V., Zhao J., Russell H.R., Brown E.J., McKinnon P.J. ATR maintains select progenitors during nervous system development. EMBO J. 2012, 31:1177-1189.
58. Alderton G.K., Galbiati L., Griffith E., Surinya K.H., Neitzel H., Jackson A.P., Jeggo P.A., O'Driscoll M. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 2006, 8:725-733.
59. Griffith E., Walker S., Martin C.A., Vagnarelli P., Stiff T., Vernay B., Al Sanna N., Saggar A., Hamel B., Earnshaw W.C., Jeggo P.A., Jackson A.P., O'Driscoll M. Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat. Genet. 2008, 40:232-236.
60. Gruber R., Zhou Z., Sukchev M., Joerss T., Frappart P.O., Wang Z.Q. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 2011, 13:1325-1334.
61. Delaval B., Doxsey S.J. Pericentrin in cellular function and disease. J. Cell Biol. 2010, 188:181-190.
62. Moreno-Herrero F., de Jager M., Dekker N.H., Kanaar R., Wyman C., Dekker C. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 2005, 437:440-443.
63. Stiff T., Reis C., Alderton G.K., Woodbine L., O'Driscoll M., Jeggo P.A. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 2005, 24:199-208.
64. Uziel T., Lerenthal Y., Moyal L., Andegeko Y., Mittelman L., Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 2003, 22:5612-5621.
65. Williams R.S., Tainer J.A. A nanomachine for making ends meet: MRN is a flexing scaffold for the repair of DNA double-strand breaks. Mol. Cell 2005, 19:724-726.
66. Paull T.T., Gellert M. The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1998, 1:969-979.
67. Resnick I.B., Kondratenko I., Pashanov E., Maschan A.A., Karachunsky A., Togoev O., Timakov A., Polyakov A., Tverskaya S., Evgrafov O., Roumiantsev A.G. 657del5 mutation in the gene for Nijmegen breakage syndrome (NBS1) in a cohort of Russian children with lymphoid tissue malignancies and controls. Am. J. Med. Genet. A 2003, 120A:174-179.
68. Varon R., Vissinga C., Platzer M., Cerosaletti K.M., Chrzanowska K.H., Saar K., Beckmann G., Seemanova E., Cooper P.R., Nowak N.J., Stumm M., Weemaes C.M., Gatti R.A., Wilson R.K., Digweed M., Rosenthal A., Sperling K., Concannon P., Reis A. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 1998, 93:467-476.
69. Stewart G.S., Maser R.S., Stankovic T., Bressan D.A., Kaplan M.I., Jaspers N.G., Raams A., Byrd P.J., Petrini J.H., Taylor A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 1999, 99:577-587.
70. Waltes R., Kalb R., Gatei M., Kijas A.W., Stumm M., Sobeck A., Wieland B., Varon R., Lerenthal Y., Lavin M.F., Schindler D., Dork T. Human RAD50 deficiency in a Nijmegen breakage syndrome-like disorder. Am. J. Hum. Genet. 2009, 84:605-616.
71. Barbi G., Scheres J.M., Schindler D., Taalman R.D., Rodens K., Mehnert K., Muller M., Seyschab H. Chromosome instability and X-ray hypersensitivity in a microcephalic and growth-retarded child. Am. J. Med. Genet. 1991, 40:44-50.
72. Matsuura S., Tauchi H., Nakamura A., Kondo N., Sakamoto S., Endo S., Smeets D., Solder B., Belohradsky B.H., Der Kaloustian V.M., Oshimura M., Isomura M., Nakamura Y., Komatsu K. Positional cloning of the gene for Nijmegen breakage syndrome. Nat. Genet. 1998, 19:179-181.
73. Zhu J., Petersen S., Tessarollo L., Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 2001, 11:105-109.
74. Luo G., Yao M.S., Bender C.F., Mills M., Bladl A.R., Bradley A., Petrini J.H. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 1999, 96:7376-7381.
75. Buis J., Wu Y., Deng Y., Leddon J., Westfield G., Eckersdorff M., Sekiguchi J.M., Chang S., Ferguson D.O. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 2008, 135:85-96.
76. Williams B.R., Mirzoeva O.K., Morgan W.F., Lin J., Dunnick W., Petrini J.H. A murine model of Nijmegen breakage syndrome. Curr. Biol. 2002, 12:648-653.
77. Theunissen J.W., Kaplan M.I., Hunt P.A., Williams B.R., Ferguson D.O., Alt F.W., Petrini J.H. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol. Cell 2003, 12:1511-1523.
78. Shull E.R., Lee Y., Nakane H., Stracker T.H., Zhao J., Russell H.R., Petrini J.H., McKinnon P.J. Differential DNA damage signaling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 2009, 23:171-180.
79. McKinnon P.J. ATM and the molecular pathogenesis of ataxia telangiectasia. Annu. Rev. Pathol. 2012, 7:303-321.
80. Lehmann A.R. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 2003, 85:1101-1111.
81. Schumacher B. Transcription-blocking DNA damage in aging: a mechanism for hormesis. Bioessays 2009, 31:1347-1356.
82. Kuzminov A. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl. Acad. Sci. USA 2001, 98:8241-8246.
83. de Boer J., Hoeijmakers J.H. Nucleotide excision repair and human syndromes. Carcinogenesis 2000, 21:453-460.
84. Thorslund T., von Kobbe C., Harrigan J.A., Indig F.E., Christiansen M., Stevnsner T., Bohr V.A. Cooperation of the Cockayne syndrome group B protein and poly(ADP-ribose) polymerase 1 in the response to oxidative stress. Mol. Cell. Biol. 2005, 25:7625-7636.
85. Osterod M., Larsen E., Le Page F., Hengstler J.G., Van Der Horst G.T., Boiteux S., Klungland A., Epe B. A global DNA repair mechanism involving the Cockayne syndrome B (CSB) gene product can prevent the in vivo accumulation of endogenous oxidative DNA base damage. Oncogene 2002, 21:8232-8239.
86. Sugasawa K., Ng J.M., Masutani C., Iwai S., van der Spek P.J., Eker A.P., Hanaoka F., Bootsma D., Hoeijmakers J.H. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 1998, 2:223-232.
87. Bootsma D., Hoeijmakers J.H. The genetic basis of xeroderma pigmentosum. Ann. Genet. 1991, 34:143-150.
88. Bohr V.A., Smith C.A., Okumoto D.S., Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 1985, 40:359-369.
89. Mellon I., Spivak G., Hanawalt P.C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 1987, 51:241-249.
90. Mu D., Sancar A. Model for XPC-independent transcription-coupled repair of pyrimidine dimers in humans. J. Biol. Chem. 1997, 272:7570-7573.
91. Licht C.L., Stevnsner T., Bohr V.A. Cockayne syndrome group B cellular and biochemical functions. Am. J. Hum. Genet. 2003, 73:1217-1239.
92. Ogi T., Lehmann A.R. The Y-family DNA polymerase kappa (pol kappa) functions in mammalian nucleotide-excision repair. Nat. Cell Biol. 2006, 8:640-642.
93. Nance M.A., Berry S.A. Cockayne syndrome: review of 140 cases. Am. J. Med. Genet. 1992, 42:68-84.
94. Stefanini M., Lagomarsini P., Arlett C.F., Marinoni S., Borrone C., Crovato F., Trevisan G., Cordone G., Nuzzo F. Xeroderma pigmentosum (complementation group D) mutation is present in patients affected by trichothiodystrophy with photosensitivity. Hum. Genet. 1986, 74:107-112.
95. Weeda G., Hutter A.W., Groenier K.H., Schuling J. The workload of trainees in general practice. Med. Educ. 1997, 31:138-143.
96. Henning K.A., Li L., Iyer N., McDaniel L.D., Reagan M.S., Legerski R., Schultz R.A., Stefanini M., Lehmann A.R., Mayne L.V., Friedberg E.C. The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 1995, 82:555-564.
97. Mallery D.L., Tanganelli B., Colella S., Steingrimsdottir H., van Gool A.J., Troelstra C., Stefanini M., Lehmann A.R. Molecular analysis of mutations in the CSB (ERCC6) gene in patients with Cockayne syndrome. Am. J. Hum. Genet. 1998, 62:77-85.
98. de Vries A., van Oostrom C.T., Hofhuis F.M., Dortant P.M., Berg R.J., de Gruijl F.R., Wester P.W., van Kreijl C.F., Capel P.J., van Steeg H., et al. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 1995, 377:169-173.
99. Nakane H., Takeuchi S., Yuba S., Saijo M., Nakatsu Y., Murai H., Nakatsuru Y., Ishikawa T., Hirota S., Kitamura Y., et al. High incidence of ultraviolet-B-or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature 1995, 377:165-168.
100. van der Horst G.T., van Steeg H., Berg R.J., van Gool A.J., de Wit J., Weeda G., Morreau H., Beems R.B., van Kreijl C.F., de Gruijl F.R., Bootsma D., Hoeijmakers J.H. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 1997, 89:425-435.
101. de Boer J., van Steeg H., Berg R.J., Garssen J., de Wit J., van Oostrum C.T., Beems R.B., van der Horst G.T., van Kreijl C.F., de Gruijl F.R., Bootsma D., Hoeijmakers J.H., Weeda G. Mouse model for the DNA repair/basal transcription disorder trichothiodystrophy reveals cancer predisposition. Cancer Res. 1999, 59:3489-3494.
102. Revet I., Feeney L., Tang A.A., Huang E.J., Cleaver J.E. Dysmyelination not demyelination causes neurological symptoms in preweaned mice in a murine model of Cockayne syndrome. Proc. Natl. Acad. Sci. USA 2012, 109:4627-4632.
103. Murai M., Enokido Y., Inamura N., Yoshino M., Nakatsu Y., van der Horst G.T., Hoeijmakers J.H., Tanaka K., Hatanaka H. Early postnatal ataxia and abnormal cerebellar development in mice lacking Xeroderma pigmentosum Group A and Cockayne syndrome Group B DNA repair genes. Proc. Natl. Acad. Sci. USA 2001, 98:13379-13384.
104. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 2008, 9:619-631.
105. Jeggo P.A., Tesmer J., Chen D.J. Genetic analysis of ionising radiation sensitive mutants of cultured mammalian cell lines. Mutat. Res. 1991, 254:125-133.
106. Cantoni O., Murray D., Meyn R.E. Induction and repair of DNA single-strand breaks in EM9 mutant CHO cells treated with hydrogen peroxide. Chem. Biol. Interact. 1987, 63:29-38.
107. Okano S., Lan L., Caldecott K.W., Mori T., Yasui A. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell. Biol. 2003, 23:3974-3981.
108. El-Khamisy S.F., Masutani M., Suzuki H., Caldecott K.W. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res. 2003, 31:5526-5533.
109. Breslin C., Caldecott K.W. DNA 3'-phosphatase activity is critical for rapid global rates of single-strand break repair following oxidative stress. Mol. Cell. Biol. 2009, 29:4653-4662.
110. Loizou J.I., El-Khamisy S.F., Zlatanou A., Moore D.J., Chan D.W., Qin J., Sarno S., Meggio F., Pinna L.A., Caldecott K.W. The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell 2004, 117:17-28.
111. Caldecott K.W. Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair (Amst.) 2007, 6:443-453.
112. Gao Y., Katyal S., Lee Y., Zhao J., Rehg J.E., Russell H.R., McKinnon P.J. DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 2011, 471:240-244.
113. Puebla-Osorio N., Lacey D.B., Alt F.W., Zhu C. Early embryonic lethality due to targeted inactivation of DNA ligase III. Mol. Cell. Biol. 2006, 26:3935-3941.
114. Tebbs R.S., Flannery M.L., Meneses J.J., Hartmann A., Tucker J.D., Thompson L.H., Cleaver J.E., Pedersen R.A. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol. 1999, 208:513-529.
115. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol. 1994, 14:68-76.
116. Lakshmipathy U., Campbell C. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res. 2000, 28:3880-3886.
117. Lee Y., Katyal S., Li Y., El-Khamisy S.F., Russell H.R., Caldecott K.W., McKinnon P.J. The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nat. Neurosci. 2009, 12:973-980.
118. Date H., Onodera O., Tanaka H., Iwabuchi K., Uekawa K., Igarashi S., Koike R., Hiroi T., Yuasa T., Awaya Y., Sakai T., Takahashi T., Nagatomo H., Sekijima Y., Kawachi I., Takiyama Y., Nishizawa M., Fukuhara N., Saito K., Sugano S., Tsuji S. Early-onset ataxia with ocular motor apraxia and hypoalbuminemia is caused by mutations in a new HIT superfamily gene. Nat. Genet. 2001, 29:184-188.
119. Moreira M.C., Barbot C., Tachi N., Kozuka N., Uchida E., Gibson T., Mendonca P., Costa M., Barros J., Yanagisawa T., Watanabe M., Ikeda Y., Aoki M., Nagata T., Coutinho P., Sequeiros J., Koenig M. The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin. Nat. Genet. 2001, 29:189-193.
120. Ahel I., Rass U., El-Khamisy S.F., Katyal S., Clements P.M., McKinnon P.J., Caldecott K.W., West S.C. The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 2006, 443:713-716.
121. Clements P.M., Breslin C., Deeks E.D., Byrd P.J., Ju L., Bieganowski P., Brenner C., Moreira M.C., Taylor A.M., Caldecott K.W. 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, 3:1493-1502.
122. Reynolds J.J., El-Khamisy S.F., Katyal S., Clements P., McKinnon P.J., Caldecott K.W. Defective DNA ligation during short-patch single-strand break repair in ataxia oculomotor apraxia 1. Mol. Cell. Biol. 2009, 29:1354-1362.
123. Gueven N., Becherel O.J., Kijas A.W., Chen P., Howe O., Rudolph J.H., Gatti R., Date H., Onodera O., Taucher-Scholz G., Lavin M.F. Aprataxin, a novel protein that protects against genotoxic stress. Hum. Mol. Genet. 2004, 13:1081-1093.
124. El-Khamisy S.F., Katyal S., Patel P., Ju L., McKinnon P.J., Caldecott K.W. Synergistic decrease of DNA single-strand break repair rates in mouse neural cells lacking both Tdp1 and aprataxin. DNA Repair (Amst.) 2009, 8:760-766.
125. El-Khamisy S.F., Saifi G.M., Weinfeld M., Johansson F., Helleday T., Lupski J.R., Caldecott K.W. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 2005, 434:108-113.
126. Takashima H., Boerkoel C.F., John J., Saifi G.M., Salih M.A., Armstrong D., Mao Y., Quiocho F.A., Roa B.B., Nakagawa M., Stockton D.W., Lupski J.R. Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat. Genet. 2002, 32:267-272.
127. Nilsen L., Forstrom R.J., Bjoras M., Alseth I. AP endonuclease independent repair of abasic sites in Schizosaccharomyces pombe. Nucleic Acids Res. 2012, 40:2000-2009.
128. Zhou T., Akopiants K., Mohapatra S., Lin P.S., Valerie K., Ramsden D.A., Lees-Miller S.P., Povirk L.F. Tyrosyl-DNA phosphodiesterase and the repair of 3'-phosphoglycolate-terminated DNA double-strand breaks. DNA Repair (Amst.) 2009, 8:901-911.
129. Murai J., Huang S.Y., Das B.B., Dexheimer T.S., Takeda S., Pommier Y. Tyrosyl-DNA phosphodiesterase 1 (TDP1) repairs DNA damage induced by topoisomerases I and II and base alkylation in vertebrate cells. J. Biol. Chem. 2012, 287:12848-12857.
130. Katyal S., el-Khamisy S.F., Russell H.R., Li Y., Ju L., Caldecott K.W., McKinnon P.J. TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J. 2007, 26:4720-4731.
131. Cortes Ledesma F., El Khamisy S.F., Zuma M.C., Osborn K., Caldecott K.W. A human 5'-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 2009, 461:674-678.
132. Koch C.A., Agyei R., Galicia S., Metalnikov P., O'Donnell P., Starostine A., Weinfeld M., Durocher D. Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. EMBO J. 2004, 23:3874-3885.
133. Whitehouse C.J., Taylor R.M., Thistlethwaite A., Zhang H., Karimi-Busheri F., Lasko D.D., Weinfeld M., Caldecott K.W. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 2001, 104:107-117.
134. Chappell C., Hanakahi L.A., Karimi-Busheri F., Weinfeld M., West S.C. Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J. 2002, 21:2827-2832.
135. Jilani A., Ramotar D., Slack C., Ong C., Yang X.M., Scherer S.W., Lasko D.D. Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3'-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J. Biol. Chem. 1999, 274:24176-24186.
136. Reynolds J.J., Walker A.K., Gilmore E.C., Walsh C.A., Caldecott K.W. Impact of PNKP mutations associated with microcephaly, seizures and developmental delay on enzyme activity and DNA strand break repair. Nucleic Acids Res 2012, 40:6608-6619.
137. Shen J., Gilmore E.C., Marshall C.A., Haddadin M., Reynolds J.J., Eyaid W., Bodell A., Barry B., Gleason D., Allen K., Ganesh V.S., Chang B.S., Grix A., Hill R.S., Topcu M., Caldecott K.W., Barkovich A.J., Walsh C.A. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 2010, 42:245-249.
138. Bendixen C., Thomsen B., Alsner J., Westergaard O. Camptothecin-stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry 1990, 29:5613-5619.
139. Zhou W., Doetsch P.W. Effects of abasic sites and DNA single-strand breaks on prokaryotic RNA polymerases. Proc. Natl. Acad. Sci. USA 1993, 90:6601-6605.
140. Kathe S.D., Shen G.P., Wallace S.S. Single-stranded breaks in DNA but not oxidative DNA base damages block transcriptional elongation by RNA polymerase II in HeLa cell nuclear extracts. J. Biol. Chem. 2004, 279:18511-18520.
141. Donahue B.A., Fuchs R.P., Reines D., Hanawalt P.C. Effects of aminofluorene and acetylaminofluorene DNA adducts on transcriptional elongation by RNA polymerase II. J. Biol. Chem. 1996, 271:10588-10594.
142. Mayne L.V., Lehmann A.R. Failure of RNA synthesis to recover after UV irradiation: an early defect in cells from individuals with Cockayne's syndrome and xeroderma pigmentosum. Cancer Res. 1982, 42:1473-1478.
143. Le Ber I., Bouslam N., Rivaud-Pechoux S., Guimaraes J., Benomar A., Chamayou C., Goizet C., Moreira M.C., Klur S., Yahyaoui M., Agid Y., Koenig M., Stevanin G., Brice A., Durr A. Frequency and phenotypic spectrum of ataxia with oculomotor apraxia 2: a clinical and genetic study in 18 patients. Brain 2004, 127:759-767.
144. Moreira M.C., Klur S., Watanabe M., Nemeth A.H., Le Ber I., Moniz J.C., Tranchant C., Aubourg P., Tazir M., Schols L., Pandolfo M., Schulz J.B., Pouget J., Calvas P., Shizuka-Ikeda M., Shoji M., Tanaka M., Izatt L., Shaw C.E., M'Zahem A., Dunne E., Bomont P., Benhassine T., Bouslam N., Stevanin G., Brice A., Guimaraes J., Mendonca P., Barbot C., Coutinho P., Sequeiros J., Durr A., Warter J.M., Koenig M. Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat. Genet. 2004, 36:225-227.
145. Yuce O., West S.C. Senataxin, defective in the neurodegenerative disorder ataxia with oculomotor apraxia 2, lies at the interface of transcription and the DNA damage response. Mol Cell Biol 2013, 33:406-417.
146. Skourti-Stathaki K., Proudfoot N.J., Gromak N. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell 2011, 42:794-805.
147. Mischo H.E., Gomez-Gonzalez B., Grzechnik P., Rondon A.G., Wei W., Steinmetz L., Aguilera A., Proudfoot N.J. Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 2011, 41:21-32.
148. Ljungman M., Zhang F. Blockage of RNA polymerase as a possible trigger for U.V. light-induced apoptosis. Oncogene 1996, 13:823-831.
149. Ljungman M., Zhang F., Chen F., Rainbow A.J., McKay B.C. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene 1999, 18:583-592.
150. Vrouwe M.G., Pines A., Overmeer R.M., Hanada K., Mullenders L.H. UV-induced photolesions elicit ATR-kinase-dependent signaling in non-cycling cells through nucleotide excision repair-dependent and -independent pathways. J. Cell Sci. 2011, 124:435-446.
151. Derheimer F.A., O'Hagan H.M., Krueger H.M., Hanasoge S., Paulsen M.T., Ljungman M. RPA and ATR link transcriptional stress to p53. Proc. Natl. Acad. Sci. USA 2007, 104:12778-12783.
152. Yu S.W., Andrabi S.A., Wang H., Kim N.S., Poirier G.G., Dawson T.M., Dawson V.L. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc. Natl. Acad. Sci. USA 2006, 103:18314-18319.
153. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002, 297:259-263.
154. Alano C.C., Garnier P., Ying W., Higashi Y., Kauppinen T.M., Swanson R.A. NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J. Neurosci. 2010, 30:2967-2978.
155. Eliasson M.J., Sampei K., Mandir A.S., Hurn P.D., Traystman R.J., Bao J., Pieper A., Wang Z.Q., Dawson T.M., Snyder S.H., Dawson V.L. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 1997, 3:1089-1095.
156. Virag L., Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev. 2002, 54:375-429.