Aberrant topoisomerase-1 DNA lesions are pathogenic in neurodegenerative genome instability syndromes - Nature Neuroscience
- ️McKinnon, Peter J
- ️Sun May 04 2014
McKinnon, P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 10, 100–112 (2009).
Jackson, S.P. & Bartek, J. The DNA-damage response in human biology and disease. Nature 461, 1071–1078 (2009).
O'Driscoll, M. & Jeggo, P.A. The role of double-strand break repair—insights from human genetics. Nat. Rev. Genet. 7, 45–54 (2006).
McKinnon, P.J. Maintaining genome stability in the nervous system. Nat. Neurosci. 16, 1523–1529 (2013).
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).
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).
Lu, T. et al. Gene regulation and DNA damage in the ageing human brain. Nature 429, 883–891 (2004).
Lavin, M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signaling and cancer. Nat. Rev. Mol. Cell Biol. 9, 759–769 (2008).
Lee, Y. & McKinnon, P.J. Responding to DNA double strand breaks in the nervous system. Neuroscience 145, 1365–1374 (2007).
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).
Stracker, T.H. & Petrini, J.H. The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol. 12, 90–103 (2011).
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).
Takai, H. et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21, 5195–5205 (2002).
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).
Caldecott, K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 9, 619–631 (2008).
McKinnon, P.J. ATM and the molecular pathogenesis of ataxia telangiectasia. Annu. Rev. Pathol. 7, 303–321 (2012).
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).
Ahel, I. et al. The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 443, 713–716 (2006).
El-Khamisy, S.F. et al. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434, 108–113 (2005).
Alagoz, M., Chiang, S.C., Sharma, A. & El-Khamisy, S.F. ATM deficiency results in accumulation of DNA–topoisomerase I covalent intermediates in neural cells. PLoS ONE 8, e58239 (2013).
Lin, C.P., Ban, Y., Lyu, Y.L., Desai, S.D. & Liu, L.F. A ubiquitin-proteasome pathway for the repair of topoisomerase I–DNA covalent complexes. J. Biol. Chem. 283, 21074–21083 (2008).
Sordet, O. et al. Ataxia telangiectasia mutated activation by transcription- and topoisomerase I–induced DNA double-strand breaks. EMBO Rep. 10, 887–893 (2009).
Pommier, Y. et al. Repair of topoisomerase I–mediated DNA damage. Prog. Nucleic Acid Res. Mol. Biol. 81, 179–229 (2006).
Wang, J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430–440 (2002).
Wu, H.Y. & Liu, L.F. DNA looping alters local DNA conformation during transcription. J. Mol. Biol. 219, 615–622 (1991).
Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6, 789–802 (2006).
Katyal, S. et al. TDP1 facilitates chromosomal single-strand break repair in neurons and is neuroprotective in vivo. EMBO J. 26, 4720–4731 (2007).
Nitiss, J.L., Soans, E., Rogojina, A., Seth, A. & Mishina, M. Topoisomerase Assays (John Wiley & Sons, 2012).
Subramanian, D., Rosenstein, B.S. & Muller, M.T. Ultraviolet-induced DNA damage stimulates topoisomerase I–DNA complex formation in vivo: possible relationship with DNA repair. Cancer Res. 58, 976–984 (1998).
Heideker, J., Prudden, J., Perry, J.J., Tainer, J.A. & Boddy, M.N. SUMO-targeted ubiquitin ligase, Rad60, and Nse2 SUMO ligase suppress spontaneous Top1-mediated DNA damage and genome instability. PLoS Genet. 7, e1001320 (2011).
Hsiang, Y.H., Hertzberg, R., Hecht, S. & Liu, L.F. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem. 260, 14873–14878 (1985).
Sakasai, R., Teraoka, H., Takagi, M. & Tibbetts, R.S. Transcription-dependent activation of ataxia telangiectasia mutated prevents DNA-dependent protein kinase–mediated cell death in response to topoisomerase I poison. J. Biol. Chem. 285, 15201–15208 (2010).
Chiang, S.C., Carroll, J. & El-Khamisy, S.F. TDP1 serine 81 promotes interaction with DNA ligase IIIalpha and facilitates cell survival following DNA damage. Cell Cycle 9, 588–595 (2010).
Das, B.B. et al. Optimal function of the DNA repair enzyme TDP1 requires its phosphorylation by ATM and/or DNA-PK. EMBO J. 28, 3667–3680 (2009).
Hickson, I. et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152–9159 (2004).
Lin, C.P., Ban, Y., Lyu, Y.L. & Liu, L.F. Proteasome-dependent processing of topoisomerase I–DNA adducts into DNA double strand breaks at arrested replication forks. J. Biol. Chem. 284, 28084–28092 (2009).
Mao, Y., Sun, M., Desai, S.D. & Liu, L.F. SUMO-1 conjugation to topoisomerase I: a possible repair response to topoisomerase-mediated DNA damage. Proc. Natl. Acad. Sci. USA 97, 4046–4051 (2000).
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).
Lee, Y. et al. ATR maintains select progenitors during nervous system development. EMBO J. 31, 1177–1189 (2012).
Lee, Y. et al. The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nat. Neurosci. 12, 973–980 (2009).
Pourquier, P. et al. 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. 272, 26441–26447 (1997).
Pourquier, P. et al. Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I. J. Biol. Chem. 272, 7792–7796 (1997).
Beal, M.F. Oxidatively modified proteins in aging and disease. Free Radic. Biol. Med. 32, 797–803 (2002).
Palmeri, S. et al. Clinical course of two Italian siblings with ataxia-telangiectasia-like disorder. Cerebellum 12, 596–599 (2013).
Vos, S.M., Tretter, E.M., Schmidt, B.H. & Berger, J.M. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 12, 827–841 (2011).
Iossifov, I. et al. De novo gene disruptions in children on the autistic spectrum. Neuron 74, 285–299 (2012).
Neale, B.M. et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 485, 242–245 (2012).
King, I.F. et al. Topoisomerases facilitate transcription of long genes linked to autism. Nature 501, 58–62 (2013).
Stoll, G. et al. Deletion of TOP3beta, a component of FMRP-containing mRNPs, contributes to neurodevelopmental disorders. Nat. Neurosci. 16, 1228–1237 (2013).
Xu, D. et al. Top3beta is an RNA topoisomerase that works with fragile X syndrome protein to promote synapse formation. Nat. Neurosci. 16, 1238–1247 (2013).