Maintaining genome stability in the nervous system

Nature Neuroscience

Volumn 16, Issue 11, 2013, Pages 1523-1529

  Mckinnon, Peter J ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE RAD3; DNA DIRECTED DNA POLYMERASE GAMMA; DOUBLE STRANDED DNA; MITOCHONDRIAL DNA; PROTEIN P53; RAD50 PROTEIN; REPLICATION FACTOR A; SINGLE STRANDED DNA; XRCC1 PROTEIN;

APOPTOSIS; ATAXIA TELANGIECTASIA; BRAIN FUNCTION; CELL CYCLE; DISEASE PREDISPOSITION; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; EXCISION REPAIR; GENE MUTATION; GENOME; GENOMIC INSTABILITY; MICROCEPHALY; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NEUROLOGIC DISEASE; NIJMEGEN BREAKAGE SYNDROME; PRIORITY JOURNAL; REVIEW; SECKEL SYNDROME; SEIZURE; SPINOCEREBELLAR DEGENERATION;

ANIMALS; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HUMANS; NERVOUS SYSTEM; NERVOUS SYSTEM DISEASES;

EID: 84886867688     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3537     Document Type: Review

References (100)

1. Barres, B.A. The mystery and magic of glia: A perspective on their roles in health and disease. Neuron 60, 430-440 (2008
2. Ge, W.P., Miyawaki, A., Gage, F.H., Jan, Y.N. & Jan, L.Y. Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484, 376-380 (2012
3. Suberbielle, E. et al. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-beta. Nat. Neurosci. 16, 613-621 (2013
4. Lu, T. et al. Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891 (2004
5. McKinnon, P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 10, 100-112 (2009
6. Caldecott, K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 9, 619-631 (2008
7. Chapman, J.R., Taylor, M.R. & Boulton, S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510 (2012
8. Deans, A.J. & West, S.C. DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480 (2011
9. Kee, Y. & D'Andrea, A.D. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev. 24, 1680-1694 (2010
10. Lieber, M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211 (2010
11. Jiricny, J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 7, 335-346 (2006
12. Kamileri, I., Karakasilioti, I. & Garinis, G.A. Nucleotide excision repair: New tricks with old bricks. Trends Genet. 28, 566-573 (2012
13. Garinis, G.A., van der Horst, G.T., Vijg, J. & Hoeijmakers, J.H. DNA damage and ageing: New-Age ideas for an age-old problem. Nat. Cell Biol. 10, 1241-1247 (2008
14. O'Driscoll, M. et al. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 8, 1175-1185 (2001
15. Woodbine, L. et al. PRKDC mutations in a SCID patient with profound neurological abnormalities. J. Clin. Invest. 123, 2969-2980 (2013
16. Anttinen, A. et al. Neurological symptoms and natural course of xeroderma pigmentosum. Brain 131, 1979-1989 (2008
17. Borgesius, N.Z. et al. Accelerated age-related cognitive decline and neurodegeneration, caused by deficient DNA repair. J. Neurosci. 31, 12543-12553 (2011
18. Compe, E. & Egly, J.M. TFIIH: When transcription met DNA repair. Nat. Rev. Mol. Cell Biol. 13, 343-354 (2012
19. Jackson, S.P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071-1078 (2009
20. 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. 8, 1395-1398 (1998
21. Deans, B., Griffin, C.S., Maconochie, M. & Thacker, J. Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J. 19, 6675-6685 (2000
22. Gao, Y. et al. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95, 891-902 (1998
23. Shull, E.R. et al. Differential DNA damage signaling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 23, 171-180 (2009
24. Frappart, P.O. et al. An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat. Med. 11, 538-544 (2005
25. Sugo, N., Aratani, Y., Nagashima, Y., Kubota, Y. & Koyama, H. Neonatal lethality with abnormal neurogenesis in mice deficient in DNA polymerase beta. EMBO J. 19, 1397-1404 (2000
26. Lee, Y. et al. Neurogenesis requires TopBP1 to prevent catastrophic replicative DNA damage in early progenitors. Nat. Neurosci. 15, 819-826 (2012
27. Herzog, K.H., Chong, M.J., Kapsetaki, M., Morgan, J.I. & McKinnon, P.J. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280, 1089-1091 (1998
28. Nijhawan, D., Honarpour, N. & Wang, X. Apoptosis in neural development and disease. Annu. Rev. Neurosci. 23, 73-87 (2000
29. Yoshida, H. et al. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739-750 (1998
30. Shull, E.R. et al. Differential DNA damage signaling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 23, 171-180 (2009
31. Lee, Y. et al. ATR maintains select progenitors during nervous system development. EMBO J. 31, 1177-1189 (2012
32. Shiloh, Y. & Ziv, Y. The ATM protein kinase: Regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 14, 197-210 (2013
33. Stracker, T.H. & Petrini, J.H. The MRE11 complex: Starting from the ends. Nat. Rev. Mol. Cell Biol. 12, 90-103 (2011
34. McKinnon, P.J. ATM and the molecular pathogenesis of ataxia telangiectasia. Annu. Rev. Pathol. 7, 303-321 (2012
35. Taylor, A.M., Groom, A. & Byrd, P.J. Ataxia-Telangiectasia-like disorder (ATLD)-its clinical presentation and molecular basis. DNA Repair (Amst.) 3, 1219-1225 (2004
36. Stewart, G.S. et al. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-Telangiectasia-like disorder. Cell 99, 577-587 (1999
37. Carney, J.P. et al. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double-strand break repair to the cellular DNA damage response. Cell 93, 477-486 (1998
38. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007
39. Cimprich, K.A. & Cortez, D. ATR: An essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627 (2008
40. O'Driscoll, M., Dobyns, W.B., van Hagen, J.M. & Jeggo, P.A. Cellular and clinical impact of haploinsufficiency for genes involved in ATR signaling. Am. J. Hum. Genet. 81, 77-86 (2007
41. 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. 33, 497-501 (2003
42. Kumagai, A., Lee, J., Yoo, H.Y. & Dunphy, W.G. TopBP1 activates the ATR-ATRIP complex. Cell 124, 943-955 (2006
43. 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 103, 10017-10022 (2006
44. Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011
45. Caviness, V.S. Jr., Nowakowski, R.S. & Bhide, P.G. Neocortical neurogenesis: Morphogenetic gradients and beyond. Trends Neurosci. 32, 443-450 (2009
46. Dehay, C. & Kennedy, H. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8, 438-450 (2007
47. Götz, M. & Huttner, W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788 (2005
48. Kishi, Y., Fujii, Y., Hirabayashi, Y. & Gotoh, Y. HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat. Neurosci. 15, 1127-1133 (2012
49. Catez, F. et al. Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol. Cell. Biol. 24, 4321-4328 (2004
50. Zhao, K., Kas, E., Gonzalez, E. & Laemmli, U.K. SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J. 12, 3237-3247 (1993
51. Ikura, T. et al. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102, 463-473 (2000
52. Murga, M. et al. Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol. 178, 1101-1108 (2007
53. Murr, R. et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8, 91-99 (2006
54. Sulli, G., Di Micco, R. & d'Adda di Fagagna, F. Crosstalk between chromatin state and DNA damage response in cellular senescence and cancer. Nat. Rev. Cancer 12, 709-720 (2012
55. Sun, Y. et al. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11, 1376-1382 (2009
56. Soria, G., Polo, S.E. & Almouzni, G. Prime, repair, restore: The active role of chromatin in the DNA damage response. Mol. Cell 46, 722-734 (2012
57. Mellén, M., Ayata, P., Dewell, S., Kriaucionis, S. & Heintz, N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 151, 1417-1430 (2012
58. Baker, S.A. et al. An AT-hook domain in MeCP2 determines the clinical course of Rett syndrome and related disorders. Cell 152, 984-996 (2013
59. Skene, P.J. et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 37, 457-468 (2010
60. Ronan, J.L., Wu, W. & Crabtree, G.R. From neural development to cognition: Unexpected roles for chromatin. Nat. Rev. Genet. 14, 347-359 (2013
61. Aguilera, A. & Garcia-Muse, T. R loops: From transcription byproducts to threats to genome stability. Mol. Cell 46, 115-124 (2012
62. Hanawalt, P.C. & Spivak, G. Transcription-coupled DNA repair: Two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 9, 958-970 (2008
63. Li, X. & Manley, J.L. Cotranscriptional processes and their influence on genome stability. Genes Dev. 20, 1838-1847 (2006
64. Saxowsky, T.T. & Doetsch, P.W. RNA polymerase encounters with DNA damage: Transcription-coupled repair or transcriptional mutagenesis? Chem. Rev. 106, 474-488 (2006
65. Latella, L., Lukas, J., Simone, C., Puri, P.L. & Bartek, J. Differentiation-induced radioresistance in muscle cells. Mol. Cell Biol. 24, 6350-6361 (2004
66. Fortini, P., Ferretti, C. & Dogliotti, E. The response to DNA damage during differentiation: Pathways and consequences. Mutat. Res. 743-744, 160-168 (2013
67. Barzilai, A. The contribution of the DNA damage response to neuronal viability. Antioxid. Redox Signal. 9, 211-218 (2007
68. Du, F. et al. Tightly coupled brain activity and cerebral ATP metabolic rate. Proc. Natl. Acad. Sci. USA 105, 6409-6414 (2008
69. Karanjawala, Z.E., Murphy, N., Hinton, D.R., Hsieh, C.L. & Lieber, M.R. Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol. 12, 397-402 (2002
70. Ju, B.G. et al. A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312, 1798-1802 (2006
71. Ming, G.L. & Song, H. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 70, 687-702 (2011
72. Zhao, C., Deng, W. & Gage, F.H. Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660 (2008
73. Spalding, K.L. et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1219-1227 (2013
74. Shen, J. et al. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 42, 245-249 (2010
75. Date, H. et al. Early-onset ataxia with ocular motor apraxia and hypoalbuminemia is caused by mutations in a new HIT superfamily gene. Nat. Genet. 29, 184-188 (2001
76. Moreira, M.C. et al. The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin. Nat. Genet. 29, 189-193 (2001
77. Takashima, H. et al. Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat. Genet. 32, 267-272 (2002
78. Ahel, I. et al. The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 443, 713-716 (2006
79. Weinfeld, M., Mani, R.S., Abdou, I., Aceytuno, R.D. & Glover, J.N. Tidying up loose ends: The role of polynucleotide kinase/phosphatase in DNA strand break repair. Trends Biochem. Sci. 36, 262-271 (2011
80. 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. 40, 6608-6619 (2012
81. 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. 29, 4653-4662 (2009
82. O'Driscoll, M. & Jeggo, P.A. The role of double-strand break repair-insights from human genetics. Nat. Rev. Genet. 7, 45-54 (2006
83. Klingseisen, A. & Jackson, A.P. Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev. 25, 2011-2024 (2011
84. Thornton, G.K. & Woods, C.G. Primary microcephaly: Do all roads lead to Rome? Trends Genet. 25, 501-510 (2009
85. Griffith, E. et al. Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat. Genet. 40, 232-236 (2008
86. Gruber, R. et al. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 13, 1325-1334 (2011
87. Higginbotham, H.R. & Gleeson, J.G. The centrosome in neuronal development. Trends Neurosci. 30, 276-283 (2007
88. Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955 (2009
89. Alderton, G.K. et al. Regulation of mitotic entry by microcephalin and its overlap with ATR signaling. Nat. Cell Biol. 8, 725-733 (2006
90. Shimada, M. & Komatsu, K. Emerging connection between centrosome and DNA repair machinery. J. Radiat. Res. (Tokyo) 50, 295-301 (2009
91. Tibelius, A. et al. Microcephalin and pericentrin regulate mitotic entry via centrosome-Associated Chk1. J. Cell Biol. 185, 1149-1157 (2009
92. Kalay, E. et al. CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat. Genet. 43, 23-26 (2011
93. DiMauro, S. & Schon, E.A. Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 31, 91-123 (2008
94. Copeland, W.C. Inherited mitochondrial diseases of DNA replication. Annu. Rev. Med. 59, 131-146 (2008
95. de Souza-Pinto, N.C., Wilson, D.M. III, Stevnsner, T.V. & Bohr, V.A. Mitochondrial DNA, base excision repair and neurodegeneration. DNA Repair (Amst.) 7, 1098-1109 (2008
96. Sykora, P., Croteau, D.L., Bohr, V.A. & Wilson, D.M. III. Aprataxin localizes to mitochondria and preserves mitochondrial function. Proc. Natl. Acad. Sci. USA 108, 7437-7442 (2011
97. Gao, Y. et al. DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 471, 240-244 (2011
98. Chen, H. et al. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141, 280-289 (2010
99. Huang, E. et al. The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death. Nat. Cell Biol. 12, 563-571 (2010
100. Nouspikel, T. & Hanawalt, P.C. When parsimony backfires: Neglecting DNA repair may doom neurons in Alzheimer's disease. Bioessays 25, 168-173 (2003