Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Emerging Perspectives on DNA Double-strand Breaks in Neurodegenerative Diseases

Author(s): Ling-Shuang Zhu, Ding-Qi Wang, Ke Cui, Dan Liu and Ling-Qiang Zhu*

Volume 17, Issue 12, 2019

Page: [1146 - 1157] Pages: 12

DOI: 10.2174/1570159X17666190726115623

Price: $65

Open Access Journals Promotions 2
Abstract

DNA double-strand breaks (DSBs) are common events that were recognized as one of the most toxic lesions in eukaryotic cells. DSBs are widely involved in many physiological processes such as V(D)J recombination, meiotic recombination, DNA replication and transcription. Deregulation of DSBs has been reported in multiple diseases in human beings, such as the neurodegenerative diseases, with which the underlying mechanisms are needed to be illustrated. Here, we reviewed the recent insights into the dysfunction of DSB formation and repair, contributing to the pathogenesis of neurodegenerative disorders including Alzheimer’s disease (AD), amyotrophic lateral sclerosis (ALS), Huntington’s disease (HD) and ataxia telangiectasia (A-T).

Keywords: DNA double-strand breaks, histone modifications, apoptosis, neurodegenerative diseases, alzheimer’s disease, huntington’s disease, amyotrophic lateral sclerosis.

Graphical Abstract
[1]
Papamichos-Chronakis, M.; Peterson, C.L. Chromatin and the genome integrity network. Nat. Rev. Genet., 2013, 14(1), 62-75.
[http://dx.doi.org/10.1038/nrg3345] [PMID: 23247436]
[2]
Jackson, S.P.; Bartek, J. The DNA-damage response in human biology and disease. Nature, 2009, 461(7267), 1071-1078.
[http://dx.doi.org/10.1038/nature08467] [PMID: 19847258]
[3]
Akematsu, T.; Fukuda, Y.; Garg, J.; Fillingham, J.S.; Pearlman, R.E.; Loidl, J. Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require Topoisomerase II and Spo11. eLife, 2017, 6, 6.
[http://dx.doi.org/10.7554/eLife.26176] [PMID: 28621664]
[4]
Khan, F.A.; Ali, S.O. Physiological roles of DNA double-strand breaks. J. Nucleic Acids, 2017, 20176439169
[http://dx.doi.org/10.1155/2017/6439169] [PMID: 29181194]
[5]
Taleei, R.; Girard, P.M.; Nikjoo, H. DSB repair model for mammalian cells in early S and G1 phases of the cell cycle: Application to damage induced by ionizing radiation of different quality. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2015, 779, 5-14.
[http://dx.doi.org/10.1016/j.mrgentox.2015.01.007] [PMID: 25813721]
[6]
Shiloh, Y.; Ziv, Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol., 2013, 14(4), 197-210.
[http://dx.doi.org/10.1038/nrm3546]
[7]
Falck, J.; Coates, J.; Jackson, S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature, 2005, 434(7033), 605-611.
[http://dx.doi.org/10.1038/nature03442] [PMID: 15758953]
[8]
Brettschneider, J.; Del Tredici, K.; Lee, V.M.; Trojanowski, J.Q. Spreading of pathology in neurodegenerative diseases: a focus on human studies. Nat. Rev. Neurosci., 2015, 16(2), 109-120.
[http://dx.doi.org/10.1038/nrn3887] [PMID: 25588378]
[9]
Lee, V.M.; Goedert, M.; Trojanowski, J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci., 2001, 24, 1121-1159.
[http://dx.doi.org/10.1146/annurev.neuro.24.1.1121] [PMID: 11520930]
[10]
Thoreen, C.C.; Sabatini, D.M. Huntingtin aggregates ask to be eaten. Nat. Genet., 2004, 36(6), 553-554.
[http://dx.doi.org/10.1038/ng0604-553] [PMID: 15167929]
[11]
Neumann, M.; Sampathu, D.M.; Kwong, L.K.; Truax, A.C.; Micsenyi, M.C.; Chou, T.T.; Bruce, J.; Schuck, T.; Grossman, M.; Clark, C.M.; McCluskey, L.F.; Miller, B.L.; Masliah, E.; Mackenzie, I.R.; Feldman, H.; Feiden, W.; Kretzschmar, H.A.; Trojanowski, J.Q.; Lee, V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 2006, 314(5796), 130-133.
[http://dx.doi.org/10.1126/science.1134108] [PMID: 17023659]
[12]
Ghavami, S.; Shojaei, S.; Yeganeh, B.; Ande, S.R.; Jangamreddy, J.R.; Mehrpour, M.; Christoffersson, J.; Chaabane, W.; Moghadam, A.R.; Kashani, H.H.; Hashemi, M.; Owji, A.A.; Łos, M.J. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog. Neurobiol., 2014, 112, 24-49.
[http://dx.doi.org/10.1016/j.pneurobio.2013.10.004] [PMID: 24211851]
[13]
Khanna, K.K.; Jackson, S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet., 2001, 27(3), 247-254.
[http://dx.doi.org/10.1038/85798] [PMID: 11242102]
[14]
Rouse, J.; Jackson, S.P. Interfaces between the detection, signaling, and repair of DNA damage. Science, 2002, 297(5581), 547-551.
[http://dx.doi.org/10.1126/science.1074740] [PMID: 12142523]
[15]
Harrison, J.C.; Haber, J.E. Surviving the breakup: The DNA damage checkpoint. Annu. Rev. Genet., 2006, 40, 209-235.
[http://dx.doi.org/10.1146/annurev.genet.40.051206.105231] [PMID: 16805667]
[16]
Panier, S.; Durocher, D. Push back to respond better: Regulatory inhibition of the DNA double-strand break response. Nat. Rev. Mol. Cell Biol., 2013, 14(10), 661-672.
[http://dx.doi.org/10.1038/nrm3659] [PMID: 24002223]
[17]
Blackford, A.N.; Jackson, S.P. ATM, ATR, and DNA-PK: The trinity at the heart of the DNA damage response. Mol. Cell, 2017, 66(6), 801-817.
[http://dx.doi.org/10.1016/j.molcel.2017.05.015] [PMID: 28622525]
[18]
Brown, K.D.; Ziv, Y.; Sadanandan, S.N.; Chessa, L.; Collins, F.S.; Shiloh, Y.; Tagle, D.A. The ataxia-telangiectasia gene product, a constitutively expressed nuclear protein that is not up-regulated following genome damage. Proc. Natl. Acad. Sci. USA, 1997, 94(5), 1840-1845.
[http://dx.doi.org/10.1073/pnas.94.5.1840] [PMID: 9050866]
[19]
Andegeko, Y.; Moyal, L.; Mittelman, L.; Tsarfaty, I.; Shiloh, Y.; Rotman, G. Nuclear retention of ATM at sites of DNA double strand breaks. J. Biol. Chem., 2001, 276(41), 38224-38230.
[PMID: 11454856]
[20]
Lee, J.H.; Paull, T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science, 2004, 304(5667), 93-96.
[http://dx.doi.org/10.1126/science.1091496] [PMID: 15064416]
[21]
Lee, J.H.; Paull, T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 2005, 308(5721), 551-554.
[http://dx.doi.org/10.1126/science.1108297] [PMID: 15790808]
[22]
Kinner, A.; Wu, W.; Staudt, C.; Iliakis, G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res., 2008, 36(17), 5678-5694.
[http://dx.doi.org/10.1093/nar/gkn550] [PMID: 18772227]
[23]
Kanaar, R.; Hoeijmakers, J.H.; van Gent, D.C. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol., 1998, 8(12), 483-489.
[http://dx.doi.org/10.1016/S0962-8924(98)01383-X] [PMID: 9861670]
[24]
Dupré, A.; Boyer-Chatenet, L.; Gautier, J. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol., 2006, 13(5), 451-457.
[http://dx.doi.org/10.1038/nsmb1090] [PMID: 16622404]
[25]
Yun, M.H.; Hiom, K. Understanding the functions of BRCA1 in the DNA-damage response. Biochem. Soc. Trans., 2009, 37(Pt 3), 597-604.
[http://dx.doi.org/10.1042/BST0370597] [PMID: 19442256]
[26]
Lee, J.H.; Goodarzi, A.A.; Jeggo, P.A.; Paull, T.T. 53BP1 promotes ATM activity through direct interactions with the MRN complex. EMBO J., 2010, 29(3), 574-585.
[http://dx.doi.org/10.1038/emboj.2009.372] [PMID: 20010693]
[27]
Tang, J.; Cho, N.W.; Cui, G.; Manion, E.M.; Shanbhag, N.M.; Botuyan, M.V.; Mer, G.; Greenberg, R.A. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat. Struct. Mol. Biol., 2013, 20(3), 317-325.
[http://dx.doi.org/10.1038/nsmb.2499] [PMID: 23377543]
[28]
Hustedt, N.; Durocher, D. The control of DNA repair by the cell cycle. Nat. Cell Biol., 2016, 19(1), 1-9.
[http://dx.doi.org/10.1038/ncb3452] [PMID: 28008184]
[29]
Reinhardt, H.C.; Yaffe, M.B. Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol., 2013, 14(9), 563-580.
[http://dx.doi.org/10.1038/nrm3640] [PMID: 23969844]
[30]
Lee, Y.; McKinnon, P.J. Responding to DNA double strand breaks in the nervous system. Neuroscience, 2007, 145(4), 1365-1374.
[http://dx.doi.org/10.1016/j.neuroscience.2006.07.026] [PMID: 16934412]
[31]
Chapman, J.R.; Taylor, M.R.; Boulton, S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell, 2012, 47(4), 497-510.
[http://dx.doi.org/10.1016/j.molcel.2012.07.029] [PMID: 22920291]
[32]
Williams, G.J.; Hammel, M.; Radhakrishnan, S.K.; Ramsden, D.; Lees-Miller, S.P.; Tainer, J.A. Structural insights into NHEJ: Building up an integrated picture of the dynamic DSB repair super complex, one component and interaction at a time. DNA Repair (Amst.), 2014, 17, 110-120.
[http://dx.doi.org/10.1016/j.dnarep.2014.02.009] [PMID: 24656613]
[33]
Sibanda, B.L.; Chirgadze, D.Y.; Ascher, D.B.; Blundell, T.L. DNA-PKcs structure suggests an allosteric mechanism modulating DNA double-strand break repair. Science, 2017, 355(6324), 520-524.
[http://dx.doi.org/10.1126/science.aak9654] [PMID: 28154079]
[34]
Bakkenist, C.J.; Kastan, M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 2003, 421(6922), 499-506.
[http://dx.doi.org/10.1038/nature01368] [PMID: 12556884]
[35]
Bannister, L.A.; Schimenti, J.C. Homologous recombinational repair proteins in mouse meiosis. Cytogenet. Genome Res., 2004, 107(3-4), 191-200.
[http://dx.doi.org/10.1159/000080597] [PMID: 15467364]
[36]
Borges, H.L.; Linden, R.; Wang, J.Y. DNA damage-induced cell death: lessons from the central nervous system. Cell Res., 2008, 18(1), 17-26.
[http://dx.doi.org/10.1038/cr.2007.110] [PMID: 18087290]
[37]
Fielder, E.; von Zglinicki, T.; Jurk, D. The DNA damage response in neurons: Die by apoptosis or survive in a senescence-like state? J. Alzheimers Dis., 2017, 60(s1), S107-S131.
[http://dx.doi.org/10.3233/JAD-161221] [PMID: 28436392]
[38]
Sinha, P.; Köttgen, E.; Westermeier, R.; Righetti, P.G. Immobilized pH 2.5-11 gradients for two-dimensional electrophoresis. Electrophoresis, 1992, 13(4), 210-214.
[http://dx.doi.org/10.1002/elps.1150130143] [PMID: 1628600]
[39]
Gomes, N.P.; Bjerke, G.; Llorente, B.; Szostek, S.A.; Emerson, B.M.; Espinosa, J.M. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev., 2006, 20(5), 601-612.
[http://dx.doi.org/10.1101/gad.1398206] [PMID: 16510875]
[40]
Liu, K.; Luo, Y.; Lin, F.T.; Lin, W.C. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev., 2004, 18(6), 673-686.
[http://dx.doi.org/10.1101/gad.1180204] [PMID: 15075294]
[41]
Radi, E.; Formichi, P.; Battisti, C.; Federico, A. Apoptosis and oxidative stress in neurodegenerative diseases. J. Alzheimers Dis., 2014, 42(Suppl. 3), S125-S152.
[http://dx.doi.org/10.3233/JAD-132738] [PMID: 25056458]
[42]
Chi, H.; Chang, H.Y.; Sang, T.K. Neuronal cell death mechanisms in major neurodegenerative diseases. Int. J. Mol. Sci., 2018, 19(10)E3082
[http://dx.doi.org/10.3390/ijms19103082] [PMID: 30304824]
[43]
Fernandez-Capetillo, O.; Mahadevaiah, S.K.; Celeste, A.; Romanienko, P.J.; Camerini-Otero, R.D.; Bonner, W.M.; Manova, K.; Burgoyne, P.; Nussenzweig, A. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell, 2003, 4(4), 497-508.
[http://dx.doi.org/10.1016/S1534-5807(03)00093-5] [PMID: 12689589]
[44]
Fernandez-Capetillo, O.; Lee, A.; Nussenzweig, M.; Nussenzweig, A. H2AX: the histone guardian of the genome. DNA Repair (Amst.), 2004, 3(8-9), 959-967.
[http://dx.doi.org/10.1016/j.dnarep.2004.03.024] [PMID: 15279782]
[45]
Marti, T.M.; Hefner, E.; Feeney, L.; Natale, V.; Cleaver, J.E. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. USA, 2006, 103(26), 9891-9896.
[http://dx.doi.org/10.1073/pnas.0603779103] [PMID: 16788066]
[46]
Lu, C.; Zhu, F.; Cho, Y.Y.; Tang, F.; Zykova, T.; Ma, W.Y.; Bode, A.M.; Dong, Z. Cell apoptosis: requirement of H2AX in DNA ladder formation, but not for the activation of caspase-3. Mol. Cell, 2006, 23(1), 121-132.
[http://dx.doi.org/10.1016/j.molcel.2006.05.023] [PMID: 16818236]
[47]
de Feraudy, S.; Revet, I.; Bezrookove, V.; Feeney, L.; Cleaver, J.E. A minority of foci or pan-nuclear apoptotic staining of gammaH2AX in the S phase after UV damage contain DNA double-strand breaks. Proc. Natl. Acad. Sci. USA, 2010, 107(15), 6870-6875.
[http://dx.doi.org/10.1073/pnas.1002175107] [PMID: 20351298]
[48]
Lemay, M.; Wood, K.A. Detection of DNA damage and identification of UV-induced photoproducts using the CometAssay kit. Biotechniques, 1999, 27(4), 846-851.
[http://dx.doi.org/10.2144/99274pf01] [PMID: 10524327]
[49]
Park, P.J. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet., 2009, 10(10), 669-680.
[http://dx.doi.org/10.1038/nrg2641] [PMID: 19736561]
[50]
Chiarle, R.; Zhang, Y.; Frock, R.L.; Lewis, S.M.; Molinie, B.; Ho, Y.J.; Myers, D.R.; Choi, V.W.; Compagno, M.; Malkin, D.J.; Neuberg, D.; Monti, S.; Giallourakis, C.C.; Gostissa, M.; Alt, F.W. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell, 2011, 147(1), 107-119.
[http://dx.doi.org/10.1016/j.cell.2011.07.049] [PMID: 21962511]
[51]
Frock, R.L.; Hu, J.; Meyers, R.M.; Ho, Y.J.; Kii, E.; Alt, F.W. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat. Biotechnol., 2015, 33(2), 179-186.
[http://dx.doi.org/10.1038/nbt.3101] [PMID: 25503383]
[52]
Canela, A.; Sridharan, S.; Sciascia, N.; Tubbs, A.; Meltzer, P.; Sleckman, B.P.; Nussenzweig, A. DNA breaks and end resection measured genome-wide by end sequencinG. Mol. Cell, 2016, 63(5), 898-911.
[http://dx.doi.org/10.1016/j.molcel.2016.06.034] [PMID: 27477910]
[53]
Scheltens, P.; Blennow, K.; Breteler, M.M.; de Strooper, B.; Frisoni, G.B.; Salloway, S.; Van der Flier, W.M. Alzheimer’s disease. Lancet, 2016, 388(10043), 505-517.
[http://dx.doi.org/10.1016/S0140-6736(15)01124-1] [PMID: 26921134]
[54]
Blennow, K.; de Leon, M.J.; Zetterberg, H. Alzheimer’s disease. Lancet, 2006, 368(9533), 387-403.
[http://dx.doi.org/10.1016/S0140-6736(06)69113-7] [PMID: 16876668]
[55]
Sherrington, R.; Rogaev, E.I.; Liang, Y.; Rogaeva, E.A.; Levesque, G.; Ikeda, M.; Chi, H.; Lin, C.; Li, G.; Holman, K.; Tsuda, T.; Mar, L.; Foncin, J.F.; Bruni, A.C.; Montesi, M.P.; Sorbi, S.; Rainero, I.; Pinessi, L.; Nee, L.; Chumakov, I.; Pollen, D.; Brookes, A.; Sanseau, P.; Polinsky, R.J.; Wasco, W.; Da Silva, H.A.; Haines, J.L.; Perkicak-Vance, M.A.; Tanzi, R.E.; Roses, A.D.; Fraser, P.E.; Rommens, J.M.; St George-Hyslop, P.H. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer’s disease. Nature, 1995, 375(6534), 754-760.
[http://dx.doi.org/10.1038/375754a0] [PMID: 7596406]
[56]
Goate, A.; Chartier-Harlin, M.C.; Mullan, M.; Brown, J.; Crawford, F.; Fidani, L.; Giuffra, L.; Haynes, A.; Irving, N.; James, L. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature, 1991, 349(6311), 704-706.
[http://dx.doi.org/10.1038/349704a0] [PMID: 1671712]
[57]
Raber, J.; Huang, Y.; Ashford, J.W. ApoE genotype accounts for the vast majority of AD risk and AD pathology. Neurobiol. Aging, 2004, 25(5), 641-650.
[http://dx.doi.org/10.1016/j.neurobiolaging.2003.12.023] [PMID: 15172743]
[58]
De Strooper, B.; Karran, E. The cellular phase of alzheimer’s disease. Cell, 2016, 164(4), 603-615.
[http://dx.doi.org/10.1016/j.cell.2015.12.056] [PMID: 26871627]
[59]
Suberbielle, E.; Sanchez, P.E.; Kravitz, A.V.; Wang, X.; Ho, K.; Eilertson, K.; Devidze, N.; Kreitzer, A.C.; Mucke, L. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci., 2013, 16(5), 613-621.
[http://dx.doi.org/10.1038/nn.3356] [PMID: 23525040]
[60]
Frost, B.; Hemberg, M.; Lewis, J.; Feany, M.B. Tau promotes neurodegeneration through global chromatin relaxation. Nat. Neurosci., 2014, 17(3), 357-366.
[http://dx.doi.org/10.1038/nn.3639] [PMID: 24464041]
[61]
Madabhushi, R.; Gao, F.; Pfenning, A.R.; Pan, L.; Yamakawa, S.; Seo, J.; Rueda, R.; Phan, T.X.; Yamakawa, H.; Pao, P.C.; Stott, R.T.; Gjoneska, E.; Nott, A.; Cho, S.; Kellis, M.; Tsai, L.H. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell, 2015, 161(7), 1592-1605.
[http://dx.doi.org/10.1016/j.cell.2015.05.032] [PMID: 26052046]
[62]
Li, S.; Hong, S.; Shepardson, N.E.; Walsh, D.M.; Shankar, G.M.; Selkoe, D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron, 2009, 62(6), 788-801.
[http://dx.doi.org/10.1016/j.neuron.2009.05.012] [PMID: 19555648]
[63]
Li, S.; Jin, M.; Koeglsperger, T.; Shepardson, N.E.; Shankar, G.M.; Selkoe, D.J. Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci., 2011, 31(18), 6627-6638.
[http://dx.doi.org/10.1523/JNEUROSCI.0203-11.2011] [PMID: 21543591]
[64]
Wang, Z.C.; Zhao, J.; Li, S. Dysregulation of synaptic and extrasynaptic N-methyl-D-aspartate receptors induced by amyloid-β. Neurosci. Bull., 2013, 29(6), 752-760.
[http://dx.doi.org/10.1007/s12264-013-1383-2] [PMID: 24136243]
[65]
Suberbielle, E.; Djukic, B.; Evans, M.; Kim, D.H.; Taneja, P.; Wang, X.; Finucane, M.; Knox, J.; Ho, K.; Devidze, N.; Masliah, E.; Mucke, L. DNA repair factor BRCA1 depletion occurs in Alzheimer brains and impairs cognitive function in mice. Nat. Commun., 2015, 6, 8897.
[http://dx.doi.org/10.1038/ncomms9897] [PMID: 26615780]
[66]
Huen, M.S.; Sy, S.M.; Chen, J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat. Rev. Mol. Cell Biol., 2010, 11(2), 138-148.
[http://dx.doi.org/10.1038/nrm2831] [PMID: 20029420]
[67]
Thompson, L.H. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat. Res., 2012, 751(2), 158-246.
[http://dx.doi.org/10.1016/j.mrrev.2012.06.002] [PMID: 22743550]
[68]
Day, J.J.; Sweatt, J.D. Epigenetic mechanisms in cognition. Neuron, 2011, 70(5), 813-829.
[http://dx.doi.org/10.1016/j.neuron.2011.05.019] [PMID: 21658577]
[69]
Gräff, J.; Kim, D.; Dobbin, M.M.; Tsai, L.H. Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol. Rev., 2011, 91(2), 603-649.
[http://dx.doi.org/10.1152/physrev.00012.2010] [PMID: 21527733]
[70]
Jiang, G.; Plo, I.; Wang, T.; Rahman, M.; Cho, J.H.; Yang, E.; Lopez, B.S.; Xia, F. BRCA1-Ku80 protein interaction enhances end-joining fidelity of chromosomal double-strand breaks in the G1 phase of the cell cycle. J. Biol. Chem., 2013, 288(13), 8966-8976.
[http://dx.doi.org/10.1074/jbc.M112.412650] [PMID: 23344954]
[71]
Dohrn, L.; Salles, D.; Siehler, S.Y.; Kaufmann, J.; Wiesmüller, L. BRCA1-mediated repression of mutagenic end-joining of DNA double-strand breaks requires complex formation with BACH1. Biochem. J., 2012, 441(3), 919-926.
[http://dx.doi.org/10.1042/BJ20110314] [PMID: 22032289]
[72]
Wang, H.C.; Chou, W.C.; Shieh, S.Y.; Shen, C.Y. Ataxia telangiectasia mutated and checkpoint kinase 2 regulate BRCA1 to promote the fidelity of DNA end-joining. Cancer Res., 2006, 66(3), 1391-1400.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-3270] [PMID: 16452194]
[73]
DuBoff, B.; Götz, J.; Feany, M.B. Tau promotes neurodegeneration via DRP1 mislocalization in vivo. Neuron, 2012, 75(4), 618-632.
[http://dx.doi.org/10.1016/j.neuron.2012.06.026] [PMID: 22920254]
[74]
Ozata, D.M.; Gainetdinov, I.; Zoch, A.; O’Carroll, D.; Zamore, P.D. PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet., 2019, 20(2), 89-108.
[http://dx.doi.org/10.1038/s41576-018-0073-3] [PMID: 30446728]
[75]
Cooper-Knock, J.; Kirby, J.; Ferraiuolo, L.; Heath, P.R.; Rattray, M.; Shaw, P.J. Gene expression profiling in human neurodegenerative disease. Nat. Rev. Neurol., 2012, 8(9), 518-530.
[http://dx.doi.org/10.1038/nrneurol.2012.156] [PMID: 22890216]
[76]
Lopes, J.P.; Oliveira, C.R.; Agostinho, P. Cdk5 acts as a mediator of neuronal cell cycle re-entry triggered by amyloid-beta and prion peptides. Cell Cycle, 2009, 8(1), 97-104.
[http://dx.doi.org/10.4161/cc.8.1.7506] [PMID: 19158499]
[77]
Neve, R.L.; McPhie, D.L. The cell cycle as a therapeutic target for Alzheimer’s disease. Pharmacol. Ther., 2006, 111(1), 99-113.
[http://dx.doi.org/10.1016/j.pharmthera.2005.09.005] [PMID: 16274748]
[78]
Zhang, J.; Herrup, K. Cdk5 and the non-catalytic arrest of the neuronal cell cycle. Cell Cycle, 2008, 7(22), 3487-3490.
[http://dx.doi.org/10.4161/cc.7.22.7045] [PMID: 19001851]
[79]
Zhang, J.; Cicero, S.A.; Wang, L.; Romito-Digiacomo, R.R.; Yang, Y.; Herrup, K. Nuclear localization of Cdk5 is a key determinant in the postmitotic state of neurons. Proc. Natl. Acad. Sci. USA, 2008, 105(25), 8772-8777.
[http://dx.doi.org/10.1073/pnas.0711355105] [PMID: 18550843]
[80]
Zhang, J.; Li, H.; Herrup, K. Cdk5 nuclear localization is p27-dependent in nerve cells: implications for cell cycle suppression and caspase-3 activation. J. Biol. Chem., 2010, 285(18), 14052-14061.
[http://dx.doi.org/10.1074/jbc.M109.068262] [PMID: 20189989]
[81]
Tang, X.; Wang, X.; Gong, X.; Tong, M.; Park, D.; Xia, Z.; Mao, Z. Cyclin-dependent kinase 5 mediates neurotoxin-induced degradation of the transcription factor myocyte enhancer factor 2. J. Neurosci., 2005, 25(19), 4823-4834.
[http://dx.doi.org/10.1523/JNEUROSCI.1331-05.2005] [PMID: 15888658]
[82]
Gong, X.; Tang, X.; Wiedmann, M.; Wang, X.; Peng, J.; Zheng, D.; Blair, L.A.; Marshall, J.; Mao, Z. Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron, 2003, 38(1), 33-46.
[http://dx.doi.org/10.1016/S0896-6273(03)00191-0] [PMID: 12691662]
[83]
Patrick, G.N.; Zukerberg, L.; Nikolic, M.; de la Monte, S.; Dikkes, P.; Tsai, L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature, 1999, 402(6762), 615-622.
[http://dx.doi.org/10.1038/45159] [PMID: 10604467]
[84]
Lee, M.S.; Kwon, Y.T.; Li, M.; Peng, J.; Friedlander, R.M.; Tsai, L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature, 2000, 405(6784), 360-364.
[http://dx.doi.org/10.1038/35012636] [PMID: 10830966]
[85]
Cruz, J.C.; Tseng, H.C.; Goldman, J.A.; Shih, H.; Tsai, L.H. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron, 2003, 40(3), 471-483.
[http://dx.doi.org/10.1016/S0896-6273(03)00627-5] [PMID: 14642273]
[86]
Taylor, J.P.; Brown, R.H., Jr; Cleveland, D.W. Decoding ALS: from genes to mechanism. Nature, 2016, 539(7628), 197-206.
[http://dx.doi.org/10.1038/nature20413] [PMID: 27830784]
[87]
Mackenzie, I.R.; Bigio, E.H.; Ince, P.G.; Geser, F.; Neumann, M.; Cairns, N.J.; Kwong, L.K.; Forman, M.S.; Ravits, J.; Stewart, H.; Eisen, A.; McClusky, L.; Kretzschmar, H.A.; Monoranu, C.M.; Highley, J.R.; Kirby, J.; Siddique, T.; Shaw, P.J.; Lee, V.M.; Trojanowski, J.Q. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann. Neurol., 2007, 61(5), 427-434.
[http://dx.doi.org/10.1002/ana.21147] [PMID: 17469116]
[88]
Yu, Z.; Fan, D.; Gui, B.; Shi, L.; Xuan, C.; Shan, L.; Wang, Q.; Shang, Y.; Wang, Y. Neurodegeneration-associated TDP-43 interacts with fragile X mental retardation protein (FMRP)/Staufen (STAU1) and regulates SIRT1 expression in neuronal cells. J. Biol. Chem., 2012, 287(27), 22560-22572.
[http://dx.doi.org/10.1074/jbc.M112.357582] [PMID: 22584570]
[89]
Hill, S.J.; Mordes, D.A.; Cameron, L.A.; Neuberg, D.S.; Landini, S.; Eggan, K.; Livingston, D.M. Two familial ALS proteins function in prevention/repair of transcription-associated DNA damage. Proc. Natl. Acad. Sci. USA, 2016, 113(48), E7701-E7709.
[http://dx.doi.org/10.1073/pnas.1611673113] [PMID: 27849576]
[90]
Mitra, J.; Guerrero, E.N.; Hegde, P.M.; Liachko, N.F.; Wang, H.; Vasquez, V.; Gao, J.; Pandey, A.; Taylor, J.P.; Kraemer, B.C.; Wu, P.; Boldogh, I.; Garruto, R.M.; Mitra, S.; Rao, K.S.; Hegde, M.L. Motor neuron disease-associated loss of nuclear TDP-43 is linked to DNA double-strand break repair defects. Proc. Natl. Acad. Sci. USA, 2019. 201818415
[http://dx.doi.org/10.1073/pnas.1818415116] [PMID: 30770445]
[91]
Ripps, M.E.; Huntley, G.W.; Hof, P.R.; Morrison, J.H.; Gordon, J.W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA, 1995, 92(3), 689-693.
[http://dx.doi.org/10.1073/pnas.92.3.689] [PMID: 7846037]
[92]
Kunst, C.B.; Messer, L.; Gordon, J.; Haines, J.; Patterson, D. Genetic mapping of a mouse modifier gene that can prevent ALS onset. Genomics, 2000, 70(2), 181-189.
[http://dx.doi.org/10.1006/geno.2000.6379] [PMID: 11112346]
[93]
Andersen, P.M.; Nilsson, P.; Keränen, M.L.; Forsgren, L.; Hägglund, J.; Karlsborg, M.; Ronnevi, L.O.; Gredal, O.; Marklund, S.L. Phenotypic heterogeneity in motor neuron disease patients with CuZn-superoxide dismutase mutations in Scandinavia. Brain, 1997, 120(Pt 10), 1723-1737.
[http://dx.doi.org/10.1093/brain/120.10.1723] [PMID: 9365366]
[94]
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., 2002, 12(5), 397-402.
[http://dx.doi.org/10.1016/S0960-9822(02)00684-X] [PMID: 11882291]
[95]
Karanjawala, Z.E.; Hsieh, C.L.; Lieber, M.R. Overexpression of Cu/Zn superoxide dismutase is lethal for mice lacking double-strand break repair. DNA Repair (Amst.), 2003, 2(3), 285-294.
[http://dx.doi.org/10.1016/S1568-7864(02)00218-5] [PMID: 12547391]
[96]
Tyebji, S.; Hannan, A.J. Synaptopathic mechanisms of neurodegeneration and dementia: Insights from Huntington’s disease. Prog. Neurobiol., 2017, 153, 18-45.
[http://dx.doi.org/10.1016/j.pneurobio.2017.03.008] [PMID: 28377290]
[97]
Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 2006, 443(7113), 787-795.
[http://dx.doi.org/10.1038/nature05292] [PMID: 17051205]
[98]
Sancar, A.; Lindsey-Boltz, L.A.; Unsal-Kaçmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem., 2004, 73, 39-85.
[http://dx.doi.org/10.1146/annurev.biochem.73.011303.073723] [PMID: 15189136]
[99]
Enokido, Y.; Tamura, T.; Ito, H.; Arumughan, A.; Komuro, A.; Shiwaku, H.; Sone, M.; Foulle, R.; Sawada, H.; Ishiguro, H.; Ono, T.; Murata, M.; Kanazawa, I.; Tomilin, N.; Tagawa, K.; Wanker, E.E.; Okazawa, H. Mutant huntingtin impairs Ku70-mediated DNA repair. J. Cell Biol., 2010, 189(3), 425-443.
[http://dx.doi.org/10.1083/jcb.200905138] [PMID: 20439996]
[100]
Tamura, T.; Sone, M.; Iwatsubo, T.; Tagawa, K.; Wanker, E.E.; Okazawa, H. Ku70 alleviates neurodegeneration in Drosophila models of Huntington’s disease. PLoS One, 2011, 6(11) e27408
[http://dx.doi.org/10.1371/journal.pone.0027408] [PMID: 22096569]
[101]
Gatei, M.; Scott, S.P.; Filippovitch, I.; Soronika, N.; Lavin, M.F.; Weber, B.; Khanna, K.K. Role for ATM in DNA damage-induced phosphorylation of BRCA1. Cancer Res., 2000, 60(12), 3299-3304.
[PMID: 10866324]
[102]
Jeon, G.S.; Kim, K.Y.; Hwang, Y.J.; Jung, M.K.; An, S.; Ouchi, M.; Ouchi, T.; Kowall, N.; Lee, J.; Ryu, H. Deregulation of BRCA1 leads to impaired spatiotemporal dynamics of γ-H2AX and DNA damage responses in Huntington’s disease. Mol. Neurobiol., 2012, 45(3), 550-563.
[http://dx.doi.org/10.1007/s12035-012-8274-9] [PMID: 22580959]
[103]
Lavin, M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol., 2008, 9(10), 759-769.
[http://dx.doi.org/10.1038/nrm2514] [PMID: 18813293]
[104]
Tóth, K.F.; Knoch, T.A.; Wachsmuth, M.; Frank-Stöhr, M.; Stöhr, M.; Bacher, C.P.; Müller, G.; Rippe, K. Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin. J. Cell Sci., 2004, 117(Pt 18), 4277-4287.
[http://dx.doi.org/10.1242/jcs.01293] [PMID: 15292402]
[105]
Meschini, R.; Morucci, E.; Berni, A.; Lopez-Martinez, W.; Palitti, F. Role of chromatin structure modulation by the histone deacetylase inhibitor trichostatin A on the radio-sensitivity of ataxia telangiectasia. Mutat. Res., 2015, 777, 52-59.
[http://dx.doi.org/10.1016/j.mrfmmm.2015.04.009] [PMID: 25942615]
[106]
Goodarzi, A.A.; Noon, A.T.; Jeggo, P.A. The impact of heterochromatin on DSB repair. Biochem. Soc. Trans., 2009, 37(Pt 3), 569-576.
[http://dx.doi.org/10.1042/BST0370569] [PMID: 19442252]
[107]
Goodarzi, A.A.; Jeggo, P.; Lobrich, M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst.), 2010, 9(12), 1273-1282.
[http://dx.doi.org/10.1016/j.dnarep.2010.09.013] [PMID: 21036673]
[108]
White, R.R.; Vijg, J. Do DNA double-strand breaks drive aging? Mol. Cell, 2016, 63(5), 729-738.
[http://dx.doi.org/10.1016/j.molcel.2016.08.004] [PMID: 27588601]
[109]
Vyjayanti, V.N.; Rao, K.S. DNA double strand break repair in brain: Reduced NHEJ activity in aging rat neurons. Neurosci. Lett., 2006, 393(1), 18-22.
[http://dx.doi.org/10.1016/j.neulet.2005.09.053] [PMID: 16226837]
[110]
Brochier, C.; Langley, B. Chromatin modifications associated with DNA double-strand breaks repair as potential targets for neurological diseases. Neurotherapeutics, 2013, 10(4), 817-830.
[http://dx.doi.org/10.1007/s13311-013-0210-9] [PMID: 24072514]
[111]
Cheung, I.; Shulha, H.P.; Jiang, Y.; Matevossian, A.; Wang, J.; Weng, Z.; Akbarian, S. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc. Natl. Acad. Sci. USA, 2010, 107(19), 8824-8829.
[http://dx.doi.org/10.1073/pnas.1001702107] [PMID: 20421462]
[112]
Seiler, D.M.; Rouquette, J.; Schmid, V.J.; Strickfaden, H.; Ottmann, C.; Drexler, G.A.; Mazurek, B.; Greubel, C.; Hable, V.; Dollinger, G.; Cremer, T.; Friedl, A.A. Double-strand break-induced transcriptional silencing is associated with loss of tri-methylation at H3K4. Chromosome Res., 2011, 19(7), 883-899.
[http://dx.doi.org/10.1007/s10577-011-9244-1] [PMID: 21987186]
[113]
Ma, Z.; Wang, H.; Cai, Y.; Wang, H.; Niu, K.; Wu, X.; Ma, H.; Yang, Y.; Tong, W.; Liu, F.; Liu, Z.; Zhang, Y.; Liu, R.; Zhu, Z.J.; Liu, N. Epigenetic drift of H3K27me3 in aging links glycolysis to healthy longevity in Drosophila. eLife, 2018, 7, 7.
[http://dx.doi.org/10.7554/eLife.35368] [PMID: 29809154]
[114]
Lee, M.H.; Siddoway, B.; Kaeser, G.E.; Segota, I.; Rivera, R.; Romanow, W.J.; Liu, C.S.; Park, C.; Kennedy, G.; Long, T.; Chun, J. Somatic APP gene recombination in Alzheimer’s disease and normal neurons. Nature, 2018, 563(7733), 639-645.
[http://dx.doi.org/10.1038/s41586-018-0718-6] [PMID: 30464338]
[115]
Friedberg, E.C.; Meira, L.B. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst.), 2006, 5(2), 189-209.
[http://dx.doi.org/10.1016/j.dnarep.2005.09.009] [PMID: 16290067]
[116]
Rondeau, S.; Vacher, S.; De Koning, L.; Briaux, A.; Schnitzler, A.; Chemlali, W.; Callens, C.; Lidereau, R.; Bièche, I. ATM has a major role in the double-strand break repair pathway dysregulation in sporadic breast carcinomas and is an independent prognostic marker at both mRNA and protein levels. Br. J. Cancer, 2015, 112(6), 1059-1066.
[http://dx.doi.org/10.1038/bjc.2015.60] [PMID: 25742469]
[117]
Su, Y.; Deng, M.F.; Xiong, W.; Xie, A.J.; Guo, J.; Liang, Z.H.; Hu, B.; Chen, J.G.; Zhu, X.; Man, H.Y.; Lu, Y.; Liu, D.; Tang, B.; Zhu, L.Q. MicroRNA-26a/death-associated protein kinase 1 signaling induces synucleinopathy and dopaminergic neuron degeneration in parkinson’s disease. Biol. Psychiatry, 2019, 85(9), 769-781.
[PMID: 30718039]
[118]
Liu, D.; Tang, H.; Li, X.Y.; Deng, M.F.; Wei, N.; Wang, X.; Zhou, Y.F.; Wang, D.Q.; Fu, P.; Wang, J.Z.; Hébert, S.S.; Chen, J.G.; Lu, Y.; Zhu, L.Q. Targeting the HDAC2/HNF-4A/miR-101b/AMPK Pathway Rescues Tauopathy and Dendritic Abnormalities in Alzheimer’s Disease. Mol. Ther., 2017, 25(3), 752-764.
[http://dx.doi.org/10.1016/j.ymthe.2017.01.018] [PMID: 28202389]
[119]
Smirnov, D.A.; Cheung, V.G. ATM gene mutations result in both recessive and dominant expression phenotypes of genes and microRNAs. Am. J. Hum. Genet., 2008, 83(2), 243-253.
[http://dx.doi.org/10.1016/j.ajhg.2008.07.003] [PMID: 18674748]
[120]
Tang, H.; Ma, M.; Wu, Y.; Deng, M.F.; Hu, F.; Almansoub, H.A.M.M.; Huang, H.Z.; Wang, D.Q.; Zhou, L.T.; Wei, N.; Man, H.; Lu, Y.; Liu, D.; Zhu, L.Q. Activation of MT2 receptor ameliorates dendritic abnormalities in Alzheimer’s disease via C/EBPα/miR-125b pathway. Aging Cell, 2019, 18(2) e12902
[http://dx.doi.org/10.1111/acel.12902] [PMID: 30706990]
[121]
Frappart, P.O.; McKinnon, P.J. Mouse models of DNA double-strand break repair and neurological disease. DNA Repair (Amst.), 2008, 7(7), 1051-1060.
[http://dx.doi.org/10.1016/j.dnarep.2008.03.007] [PMID: 18458002]
[122]
Edwin Shackelford, R.; Manuszak, R.P.; Heard, S.C.; Link, C.J.; Wang, S. Pharmacological manipulation of ataxia-telangiectasia kinase activity as a treatment for Parkinson’s disease. Med. Hypotheses, 2005, 64(4), 736-741.
[http://dx.doi.org/10.1016/j.mehy.2004.08.029] [PMID: 15694690]
[123]
Sharma, N.K.; Lebedeva, M.; Thomas, T.; Kovalenko, O.A.; Stumpf, J.D.; Shadel, G.S.; Santos, J.H. Intrinsic mitochondrial DNA repair defects in Ataxia Telangiectasia. DNA Repair (Amst.), 2014, 13, 22-31.
[http://dx.doi.org/10.1016/j.dnarep.2013.11.002] [PMID: 24342190]
[124]
Copani, A.; Guccione, S.; Giurato, L.; Caraci, F.; Calafiore, M.; Sortino, M.A.; Nicoletti, F. The cell cycle molecules behind neurodegeneration in Alzheimer’s disease: Perspectives for drug development. Curr. Med. Chem., 2008, 15(24), 2420-2432.
[http://dx.doi.org/10.2174/092986708785909030] [PMID: 18855671]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy