Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Potential Roles for G-Quadruplexes in Mitochondria

Author(s): Micol Falabella, Rafael J. Fernandez, F. Brad Johnson and Brett A. Kaufman*

Volume 26, Issue 16, 2019

Page: [2918 - 2932] Pages: 15

DOI: 10.2174/0929867325666180228165527

Price: $65

Abstract

Some DNA or RNA sequences rich in guanine (G) nucleotides can adopt noncanonical conformations known as G-quadruplexes (G4). In the nuclear genome, G4 motifs have been associated with genome instability and gene expression defects, but they are increasingly recognized to be regulatory structures. Recent studies have revealed that G4 structures can form in the mitochondrial genome (mtDNA) and potential G4 forming sequences are associated with the origin of mtDNA deletions. However, little is known about the regulatory role of G4 structures in mitochondria. In this short review, we will explore the potential for G4 structures to regulate mitochondrial function, based on evidence from the nucleus.

Keywords: G-quadruplexes, mtDNA, mitochondrial gene expression, mitochondrial genome instability, mtDNA deletions, mtDNA depletion, G4 ligand.

[1]
Burge, S.; Parkinson, G.N.; Hazel, P.; Todd, A.K.; Neidle, S. Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 2005, 34(19), 5402-5415. [http://dx.doi.org/10.1093/nar/gkl655]. [PMID: 17012276].
[2]
Sen, D.; Gilbert, W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature, 1988, 334(6180), 364-366. [http://dx.doi.org/10.1038/334364a0]. [PMID: 3393228].
[3]
Sen, D.; Gilbert, W. A sodium-potassium switch in the formation of four-stranded G4-DNA. Nature, 1990, 344(6265), 410-414. [http://dx.doi.org/10.1038/344410a0]. [PMID: 2320109].
[4]
Hazel, P.; Parkinson, G.N.; Neidle, S. Topology variation and loop structural homology in crystal and simulated structures of a bimolecular DNA quadruplex. J. Am. Chem. Soc., 2006, 128(16), 5480-5487. [http://dx.doi.org/10.1021/ja058577+]. [PMID: 16620121].
[5]
Karsisiotis, A.I.; Hessari, N.M.; Novellino, E.; Spada, G.P.; Randazzo, A.; Webba da Silva, M. Topological characterization of nucleic acid G-quadruplexes by UV absorption and circular dichroism. Angew. Chem. Int. Ed. Engl., 2011, 50(45), 10645-10648. [http://dx.doi.org/10.1002/anie.201105193]. [PMID: 21928459].
[6]
Lane, A.N.; Chaires, J.B.; Gray, R.D.; Trent, J.O. Stability and kinetics of G-quadruplex structures. Nucleic Acids Res., 2008, 36(17), 5482-5515. [http://dx.doi.org/10.1093/nar/gkn517]. [PMID: 18718931].
[7]
Harkness, R.W. V; Mittermaier, A.K. G-quadruplex dynamics. Biochim. Biophys. Acta. Proteins Proteomics, 2017, 1865(11 Pt B), 1544-1554. [http://dx.doi.org/10.1016/j.bbapap.2017.06.012]. [PMID: 28642152].
[8]
Huppert, J.L.; Balasubramanian, S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 2005, 33(9), 2908-2916. [http://dx.doi.org/10.1093/nar/gki609]. [PMID: 15914667].
[9]
Bedrat, A.; Lacroix, L.; Mergny, J.L. Re-evaluation of G-quadruplex propensity with G4 Hunter. Nucleic Acids Res., 2016, 44(4), 1746-1759. [http://dx.doi.org/10.1093/nar/gkw006]. [PMID: 26792894].
[10]
Kwok, C.K.; Merrick, C.J. G-Quadruplexes: Prediction, characterization, and biological application. Trends Biotechnol., 2017, 35(10), 997-1013. [http://dx.doi.org/10.1016/j.tibtech.2017.06.012]. [PMID: 28755976].
[11]
Todd, A.K.; Johnston, M.; Neidle, S. Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 2005, 33(9), 2901-2907. [http://dx.doi.org/10.1093/nar/gki553]. [PMID: 15914666].
[12]
Garg, R.; Aggarwal, J.; Thakkar, B. Genome-wide discovery of G-quadruplex forming sequences and their functional relevance in plants. Sci. Rep., 2016, 6(1), 28211. [http://dx.doi.org/10.1038/srep28211]. [PMID: 27324275].
[13]
Paeschke, K.; Capra, J.A.; Zakian, V.A. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell, 2011, 145(5), 678-691. [http://dx.doi.org/10.1016/j.cell.2011.04.015]. [PMID: 21620135].
[14]
Rawal, P.; Kummarasetti, V.B.; Ravindran, J.; Kumar, N.; Halder, K.; Sharma, R.; Mukerji, M.; Das, S.K.; Chowdhury, S. Genome-wide prediction of G4 DNA as regulatory motifs: role in Escherichia coli global regulation. Genome Res., 2006, 16(5), 644-655. [http://dx.doi.org/10.1101/gr.4508806]. [PMID: 16651665].
[15]
Capra, J.A.; Paeschke, K.; Singh, M.; Zakian, V.A. G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae. PLOS Comput. Biol., 2010, 6(7)e1000861 [http://dx.doi.org/10.1371/journal.pcbi.1000861]. [PMID: 20676380].
[16]
Biffi, G.; Tannahill, D.; McCafferty, J.; Balasubramanian, S. Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 2013, 5(3), 182-186. [http://dx.doi.org/10.1038/nchem.1548]. [PMID: 23422559].
[17]
Henderson, A.; Wu, Y.; Huang, Y.C.; Chavez, E.A.; Platt, J.; Johnson, F.B.; Brosh, R.M., Jr; Sen, D.; Lansdorp, P.M. Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res., 2014, 42(2), 860-869. [http://dx.doi.org/10.1093/nar/gkt957]. [PMID: 24163102].
[18]
Wanrooij, P.H.; Uhler, J.P.; Simonsson, T.; Falkenberg, M.; Gustafsson, C.M. G-quadruplex structures in RNA stimulate mitochondrial transcription termination and primer formation. Proc. Natl. Acad. Sci. USA, 2010, 107(37), 16072-16077. [http://dx.doi.org/10.1073/pnas.1006026107]. [PMID: 20798345].
[19]
Agaronyan, K.; Morozov, Y.I.; Anikin, M.; Temiakov, D. Mitochondrial biology. Replication-transcription switch in human mitochondria. Science, 2015, 347(6221), 548-551. [http://dx.doi.org/10.1126/science.aaa0986]. [PMID: 25635099].
[20]
Dong, D.W.; Pereira, F.; Barrett, S.P.; Kolesar, J.E.; Cao, K.; Damas, J.; Yatsunyk, L.A.; Johnson, F.B.; Kaufman, B.A. Association of G-quadruplex forming sequences with human mtDNA deletion breakpoints. BMC Genomics, 2014, 15(1), 677. [http://dx.doi.org/10.1186/1471-2164-15-677]. [PMID: 25124333].
[21]
Bharti, S.K.; Sommers, J.A.; Zhou, J.; Kaplan, D.L.; Spelbrink, J.N.; Mergny, J-L.; Brosh, R.M. Jr DNA sequences proximal to human mitochondrial DNA deletion breakpoints prevalent in human disease form G-quadruplexes, a class of DNA structures inefficiently unwound by the mitochondrial replicative Twinkle helicase. J. Biol. Chem., 2014, 289(43), 29975-29993. [http://dx.doi.org/10.1074/jbc.M114.567073]. [PMID: 25193669].
[22]
Oliveira, P.H.; da Silva, C.L.; Cabral, J.M. An appraisal of human mitochondrial DNA instability: New insights into the role of non-canonical DNA structures and sequence motifs. PLoS One, 2013, 8(3)e59907 [http://dx.doi.org/10.1371/journal.pone.0059907]. [PMID: 23555828].
[23]
Han, H.; Hurley, L.H.; Salazar, M. A DNA polymerase stop assay for G-quadruplex-interactive compounds. Nucleic Acids Res., 1999, 27(2), 537-542. [http://dx.doi.org/10.1093/nar/27.2.537]. [PMID: 9862977].
[24]
Fernando, H.; Rodriguez, R.; Balasubramanian, S. Europe PMC funders group selective recognition of a DNA G-quadruplex by an engineered antibody, 2009, 47(36), 9365-9371.
[25]
Chambers, V.S.; Marsico, G.; Boutell, J.M.; Di Antonio, M.; Smith, G.P.; Balasubramanian, S. High-throughput sequencing of DNA G-quadruplex structures in the human genome. Nat. Biotechnol., 2015, 33(8), 877-881. [http://dx.doi.org/10.1038/nbt.3295]. [PMID: 26192317].
[26]
Hänsel-Hertsch, R.; Beraldi, D.; Lensing, S.V.; Marsico, G.; Zyner, K.; Parry, A.; Di Antonio, M.; Pike, J.; Kimura, H.; Narita, M.; Tannahill, D.; Balasubramanian, S. G-quadruplex structures mark human regulatory chromatin. Nat. Genet., 2016, 48(10), 1267-1272. [http://dx.doi.org/10.1038/ng.3662]. [PMID: 27618450].
[27]
Liu, H.Y.; Zhao, Q.; Zhang, T.P.; Wu, Y.; Xiong, Y.X.; Wang, S.K.; Ge, Y.L.; He, J.H.; Lv, P.; Ou, T.M.; Tan, J.H.; Li, D.; Gu, L.Q.; Ren, J.; Zhao, Y.; Huang, Z.S. Conformation Selective antibody enables genome profiling and leads to discovery of parallel G-quadruplex in human telomeres. Cell Chem. Biol., 2016, 23(10), 1261-1270. [http://dx.doi.org/10.1016/j.chembiol.2016.08.013]. [PMID: 27693060].
[28]
Kim, N.W.; Piatyszek, M.A.; Prowse, K.R.; Harley, C.B.; West, M.D.; Ho, P.L.; Coviello, G.M.; Wright, W.E.; Weinrich, S.L.; Shay, J.W. Specific association of human telomerase activity with immortal cells and cancer. Science, 1994, 266(5193), 2011-2015. [http://dx.doi.org/10.1126/science.7605428]. [PMID: 7605428].
[29]
Henderson, E.; Hardin, C.C.; Walk, S.K.; Tinoco, I., Jr; Blackburn, E.H. Telomeric DNA oligonucleotides form novel intramolecular structures containing guanine-guanine base pairs. Cell, 1987, 51(6), 899-908. [http://dx.doi.org/10.1016/0092-8674(87)90577-0]. [PMID: 3690664].
[30]
Wolfe, A.L.; Singh, K.; Zhong, Y.; Drewe, P.; Rajasekhar, V.K.; Sanghvi, V.R.; Mavrakis, K.J.; Jiang, M.; Roderick, J.E.; Van Der Meulen, J. Rudimentary G-Quadruplex-Based Telomere Capping in Saccharomyces cerevisiae. Nucleic Acids Res., 2009, 18(4), 764-767.
[31]
Francisco, A.P.; Paulo, A. Oncogene expression modulation in cancer cell lines by DNA G-quadruplex-interactive small molecules. Curr. Med. Chem., 2017, 24(42), 4873-4904. [PMID: 27573064].
[32]
Vy Thi Le, T.; Han, S.; Chae, J.; Park, H-J. G-quadruplex binding ligands: from naturally occurring to rationally designed molecules. Curr. Pharm. Des., 2012, 18(14), 1948-1972. [http://dx.doi.org/10.2174/138161212799958431]. [PMID: 22376113].
[33]
Neidle, S. Human telomeric G-quadruplex: the current status of telomeric G-quadruplexes as therapeutic targets in human cancer. FEBS J., 2010, 277(5), 1118-1125. [http://dx.doi.org/10.1111/j.1742-4658.2009.07463.x]. [PMID: 19951354].
[34]
Riou, J.F.; Guittat, L.; Mailliet, P.; Laoui, A.; Renou, E.; Petitgenet, O.; Mégnin-Chanet, F.; Hélène, C.; Mergny, J.L. Cell senescence and telomere shortening induced by a new series of specific G-quadruplex DNA ligands. Proc. Natl. Acad. Sci. USA, 2002, 99(5), 2672-2677. [http://dx.doi.org/10.1073/pnas.052698099]. [PMID: 11854467].
[35]
Burger, A.M.; Dai, F.; Schultes, C.M.; Reszka, A.P.; Moore, M.J.; Double, J.A.; Neidle, S. The G-quadruplex-interactive molecule BRACO-19 inhibits tumor growth, consistent with telomere targeting and interference with telomerase function. Cancer Res., 2005, 65(4), 1489-1496. [http://dx.doi.org/10.1158/0008-5472.CAN-04-2910]. [PMID: 15735037].
[36]
Müller, S.; Sanders, D.A.; Di Antonio, M.; Matsis, S.; Riou, J-F.; Rodriguez, R.; Balasubramanian, S. Pyridostatin analogues promote telomere dysfunction and long-term growth inhibition in human cancer cells. Org. Biomol. Chem., 2012, 10(32), 6537-6546. [http://dx.doi.org/10.1039/c2ob25830g]. [PMID: 22790277].
[37]
Qi, H.; Lin, C-P.; Fu, X.; Wood, L.M.; Liu, A.A.; Tsai, Y.C.; Chen, Y.; Barbieri, C.M.; Pilch, D.S.; Liu, L.F. G-quadruplexes induce apoptosis in tumor cells. Cancer Res., 2006, 66(24), 11808-11816. [http://dx.doi.org/10.1158/0008-5472.CAN-06-1225]. [PMID: 17178877].
[38]
Moye, A.L.; Porter, K.C.; Cohen, S.B.; Phan, T.; Zyner, K.G.; Sasaki, N.; Lovrecz, G.O.; Beck, J.L.; Bryan, T.M. Telomeric G-quadruplexes are a substrate and site of localization for human telomerase. Nat. Commun., 2015, 6, 7643. [http://dx.doi.org/10.1038/ncomms8643]. [PMID: 26158869].
[39]
Oganesian, L.; Moon, I.K.; Bryan, T.M.; Jarstfer, M.B. Extension of G-quadruplex DNA by ciliate telomerase. EMBO J., 2006, 25(5), 1148-1159. [http://dx.doi.org/10.1038/sj.emboj.7601006]. [PMID: 16511573].
[40]
Huppert, J.L.; Balasubramanian, S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 2007, 35(2), 406-413. [http://dx.doi.org/10.1093/nar/gkl1057]. [PMID: 17169996].
[41]
Hershman, S.G.; Chen, Q.; Lee, J.Y.; Kozak, M.L.; Yue, P.; Wang, L-S.; Johnson, F.B. Genomic distribution and functional analyses of potential G-quadruplex-forming sequences in Saccharomyces cerevisiae. Nucleic Acids Res., 2008, 36(1), 144-156. [http://dx.doi.org/10.1093/nar/gkm986]. [PMID: 17999996].
[42]
Halder, R.; Riou, J-F.; Teulade-Fichou, M-P.; Frickey, T.; Hartig, J.S. Bisquinolinium compounds induce quadruplex-specific transcriptome changes in HeLa S3 cell lines. BMC Res. Notes, 2012, 5, 138. [http://dx.doi.org/10.1186/1756-0500-5-138]. [PMID: 22414013].
[43]
Tang, W.; Robles, A.I.; Beyer, R.P.; Gray, L.T.; Nguyen, G.H.; Oshima, J.; Maizels, N.; Harris, C.C.; Monnat, R.J., Jr The Werner syndrome RECQ helicase targets G4 DNA in human cells to modulate transcription. Hum. Mol. Genet., 2016, 25(10), 2060-2069. [http://dx.doi.org/10.1093/hmg/ddw079]. [PMID: 26984941].
[44]
Nguyen, G.H.; Tang, W.; Robles, A.I.; Beyer, R.P.; Gray, L.T.; Welsh, J.A.; Schetter, A.J.; Kumamoto, K.; Wang, X.W.; Hickson, I.D.; Maizels, N.; Monnat, R.J., Jr; Harris, C.C. Regulation of gene expression by the BLM helicase correlates with the presence of G-quadruplex DNA motifs. Proc. Natl. Acad. Sci. USA, 2014, 111(27), 9905-9910. [http://dx.doi.org/10.1073/pnas.1404807111]. [PMID: 24958861].
[45]
Johnson, J.E.; Cao, K.; Ryvkin, P.; Wang, L.S.; Johnson, F.B. Altered gene expression in the Werner and Bloom syndromes is associated with sequences having G-quadruplex forming potential. Nucleic Acids Res., 2010, 38(4), 1114-1122. [http://dx.doi.org/10.1093/nar/gkp1103]. [PMID: 19966276].
[46]
Eddy, J.; Maizels, N. Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res., 2006, 34(14), 3887-3896. [http://dx.doi.org/10.1093/nar/gkl529]. [PMID: 16914419].
[47]
Phan, A.T.; Modi, Y.S.; Patel, D.J. Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J. Am. Chem. Soc., 2004, 126(28), 8710-8716. [http://dx.doi.org/10.1021/ja048805k]. [PMID: 15250723].
[48]
Siddiqui-Jain, A.; Grand, C.L.; Bearss, D.J.; Hurley, L.H. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl. Acad. Sci. USA, 2002, 99(18), 11593-11598. [http://dx.doi.org/10.1073/pnas.182256799]. [PMID: 12195017].
[49]
Sun, D.; Liu, W-J.; Guo, K.; Rusche, J.J.; Ebbinghaus, S.; Gokhale, V.; Hurley, L.H. The proximal promoter region of the human vascular endothelial growth factor gene has a G-quadruplex structure that can be targeted by G-quadruplex-interactive agents. Mol. Cancer Ther., 2008, 7(4), 880-889. [http://dx.doi.org/10.1158/1535-7163.MCT-07-2119]. [PMID: 18413801].
[50]
Rankin, S.; Reszka, A.P.; Huppert, J.; Zloh, M.; Parkinson, G.N.; Todd, A.K.; Ladame, S.; Balasubramanian, S.; Neidle, S. Putative DNA quadruplex formation within the human c-kit oncogene. J. Am. Chem. Soc., 2005, 127(30), 10584-10589. [http://dx.doi.org/10.1021/ja050823u]. [PMID: 16045346].
[51]
Cogoi, S.; Xodo, L.E. G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription. Nucleic Acids Res., 2006, 34(9), 2536-2549. [http://dx.doi.org/10.1093/nar/gkl286]. [PMID: 16687659].
[52]
Palumbo, S.L.; Ebbinghaus, S.W.; Hurley, L.H. Formation of a unique end-to-end stacked pair of G-quadruplexes in the hTERT core promoter with implications for inhibition of telomerase by G-quadruplex-interactive ligands. J. Am. Chem. Soc., 2009, 131(31), 10878-10891. [http://dx.doi.org/10.1021/ja902281d]. [PMID: 19601575].
[53]
Dexheimer, T.S.; Sun, D.; Hurley, L.H. Deconvoluting the structural and drug-recognition complexity of the G-quadruplex-forming region upstream of the bcl-2 P1 promoter. J. Am. Chem. Soc., 2006, 128(16), 5404-5415. [http://dx.doi.org/10.1021/ja0563861]. [PMID: 16620112].
[54]
Cogoi, S.; Rapozzi, V.; Cauci, S.; Xodo, L.E. Critical role of hnRNP A1 in activating KRAS transcription in pancreatic cancer cells: A molecular mechanism involving G4 DNA. Biochim. Biophys. Acta, Gen. Subj., 2017, 1861(5 Pt B), 1389-1398. [http://dx.doi.org/10.1016/j.bbagen.2016.11.031]. [PMID: 27888145].
[55]
Lopergolo, A.; Perrone, R.; Tortoreto, M.; Doria, F.; Beretta, G.L.; Zuco, V.; Freccero, M.; Borrello, M.G.; Lanzi, C.; Richter, S.N.; Zaffaroni, N.; Folini, M. Targeting of RET oncogene by naphthalene diimide-mediated gene promoter G-quadruplex stabilization exerts anti-tumor activity in oncogene-addicted human medullary thyroid cancer. Oncotarget, 2016, 7(31), 49649-49663. [http://dx.doi.org/10.18632/oncotarget.10105]. [PMID: 27351133].
[56]
Wu, P.; Ma, D.L.; Leung, C.H.; Yan, S.C.; Zhu, N.; Abagyan, R.; Che, C.M. Stabilization of G-quadruplex DNA with platinum(II) Schiff base complexes: luminescent probe and down-regulation of c-myc oncogene expression. Chemistry, 2009, 15(47), 13008-13021. [http://dx.doi.org/10.1002/chem.200901943]. [PMID: 19876976].
[57]
Murat, P.; Gormally, M. V; Sanders, D.; Di Antonio, M.; Balasubramanian, S. Light-mediated in cell downregulation of G-Quadruplex-containing genes using a photo-caged ligand (ESI). Chem. Commun. (Camb), 2013, 49(Scheme 1). , 8453-8455.
[58]
Halder, K.; Halder, R.; Chowdhury, S. Genome-wide analysis predicts DNA structural motifs as nucleosome exclusion signals. Mol. Biosyst., 2009, 5(12), 1703-1712. [http://dx.doi.org/10.1039/b905132e]. [PMID: 19587895].
[59]
Song, J.; Perreault, J-P.; Topisirovic, I.; Richard, S. RNA G-quadruplexes and their potential regulatory roles in translation. Translation (Austin), 2016, 4(2)e1244031 [http://dx.doi.org/10.1080/21690731.2016.1244031]. [PMID: 28090421].
[60]
Guo, J. U.; Bartel, D. P. RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria. Science (80-. ), 2016, 353(6306)
[61]
Besnard, E.; Babled, A.; Lapasset, L.; Milhavet, O.; Parrinello, H.; Dantec, C.; Marin, J-M.; Lemaitre, J-M. Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat. Struct. Mol. Biol., 2012, 19(8), 837-844. [http://dx.doi.org/10.1038/nsmb.2339]. [PMID: 22751019].
[62]
Bochman, M.L.; Paeschke, K.; Zakian, V.A. DNA secondary structures: Stability and function of G-quadruplex structures. Nat. Rev. Genet., 2012, 13(11), 770-780. [http://dx.doi.org/10.1038/nrg3296]. [PMID: 23032257].
[63]
Langley, A.R.; Gräf, S.; Smith, J.C.; Krude, T. Genome-wide identification and characterisation of human DNA replication origins by initiation site sequencing (ini-seq). Nucleic Acids Res., 2016, 44(21), 10230-10247. [PMID: 27587586].
[64]
Cayrou, C.; Coulombe, P.; Vigneron, A.; Stanojcic, S.; Ganier, O.; Peiffer, I.; Rivals, E.; Puy, A.; Laurent-Chabalier, S.; Desprat, R.; Méchali, M. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res., 2011, 21(9), 1438-1449. [http://dx.doi.org/10.1101/gr.121830.111]. [PMID: 21750104].
[65]
Valton, A.L.; Hassan-Zadeh, V.; Lema, I.; Boggetto, N.; Alberti, P.; Saintomé, C.; Riou, J.F.; Prioleau, M.N. G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBO J., 2014, 33(7), 732-746. [http://dx.doi.org/10.1002/embj.201387506]. [PMID: 24521668].
[66]
Lopes, J.; Piazza, A.; Bermejo, R.; Kriegsman, B.; Colosio, A.; Teulade-Fichou, M-P.; Foiani, M.; Nicolas, A. G-quadruplex-induced instability during leading-strand replication. EMBO J., 2011, 30(19), 4033-4046. [http://dx.doi.org/10.1038/emboj.2011.316]. [PMID: 21873979].
[67]
Piazza, A.; Boulé, J-B.; Lopes, J.; Mingo, K.; Largy, E.; Teulade-Fichou, M-P.; Nicolas, A. Genetic instability triggered by G-quadruplex interacting Phen-DC compounds in Saccharomyces cerevisiae. Nucleic Acids Res., 2010, 38(13), 4337-4348. [http://dx.doi.org/10.1093/nar/gkq136]. [PMID: 20223771].
[68]
Rodriguez, R.; Miller, K.M.; Forment, J.V.; Bradshaw, C.R.; Nikan, M.; Britton, S.; Oelschlaegel, T.; Xhemalce, B.; Balasubramanian, S.; Jackson, S.P. Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat. Chem. Biol., 2012, 8(3), 301-310. [http://dx.doi.org/10.1038/nchembio.780]. [PMID: 22306580].
[69]
De, S.; Michor, F. DNA secondary structures and epigenetic determinants of cancer genome evolution. Nat. Struct. Mol. Biol., 2011, 18(8), 950-955. [http://dx.doi.org/10.1038/nsmb.2089]. [PMID: 21725294].
[70]
Zimmer, J.; Tacconi, E.M.; Folio, C.; Badie, S.; Porru, M.; Klare, K.; Tumiati, M.; Markkanen, E.; Halder, S.; Ryan, A.; Jackson, S.P.; Ramadan, K.; Kuznetsov, S.G.; Biroccio, A.; Sale, J.E.; Tarsounas, M. Targeting BRCA1 and BRCA2 deficiencies with G-quadruplex-interacting compounds. Mol. Cell, 2016, 61(3), 449-460. [http://dx.doi.org/10.1016/j.molcel.2015.12.004]. [PMID: 26748828].
[71]
van Wietmarschen, N.; Merzouk, S.; Halsema, N.; Spierings, D.C.; Guryev, V.; Lansdorp, P.M. BLM helicase suppresses recombination at G-quadruplex motifs in transcribed genes. Nat. Commun., 2018, 9(1), 271. [http://dx.doi.org/10.1038/s41467-017-02760-1]. [PMID: 29348659].
[72]
Anderson, S.; Bankier, A.T.; Barrell, B.G.; de Bruijn, M.H.; Coulson, A.R.; Drouin, J.; Eperon, I.C.; Nierlich, D.P.; Roe, B.A.; Sanger, F.; Schreier, P.H.; Smith, A.J.; Staden, R.; Young, I.G. Sequence and organization of the human mitochondrial genome. Nature, 1981, 290(5806), 457-465. [http://dx.doi.org/10.1038/290457a0]. [PMID: 7219534].
[73]
Kang, E.; Wu, J.; Gutierrez, N.M.; Koski, A.; Tippner-Hedges, R.; Agaronyan, K.; Platero-Luengo, A.; Martinez-Redondo, P.; Ma, H.; Lee, Y.; Hayama, T.; Van Dyken, C.; Wang, X.; Luo, S.; Ahmed, R.; Li, Y.; Ji, D.; Kayali, R.; Cinnioglu, C.; Olson, S.; Jensen, J.; Battaglia, D.; Lee, D.; Wu, D.; Huang, T.; Wolf, D.P.; Temiakov, D.; Belmonte, J.C.; Amato, P.; Mitalipov, S. Mitochondrial replacement in human oocytes carrying pathogenic mitochondrial DNA mutations. Nature, 2016, 540(7632), 270-275. [http://dx.doi.org/10.1038/nature20592]. [PMID: 27919073].
[74]
Kukat, C.; Wurm, C.A.; Spåhr, H.; Falkenberg, M.; Larsson, N-G.; Jakobs, S. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc. Natl. Acad. Sci. USA, 2011, 108(33), 13534-13539. [http://dx.doi.org/10.1073/pnas.1109263108]. [PMID: 21808029].
[75]
Alexeyev, M.; Shokolenko, I.; Wilson, G.; LeDoux, S. The maintenance of mitochondrial DNA integrity--critical analysis and update. Cold Spring Harb. Perspect. Biol., 2013, 5(5)a012641 [http://dx.doi.org/10.1101/cshperspect.a012641]. [PMID: 23637283].
[76]
Yakes, F.M.; Van Houten, B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA, 1997, 94(2), 514-519. [http://dx.doi.org/10.1073/pnas.94.2.514]. [PMID: 9012815].
[77]
Safdar, A.; Annis, S.; Kraytsberg, Y.; Laverack, C.; Saleem, A.; Popadin, K.; Woods, D.C.; Tilly, J.L.; Khrapko, K. Amelioration of premature aging in mtDNA mutator mouse by exercise: the interplay of oxidative stress, PGC-1α, p53, and DNA damage. A hypothesis. Curr. Opin. Genet. Dev., 2016, 38, 127-132. [http://dx.doi.org/10.1016/j.gde.2016.06.011]. [PMID: 27497229].
[78]
Valente, W.J.; Ericson, N.G.; Long, A.S.; White, P.A.; Marchetti, F.; Bielas, J.H. Mitochondrial DNA exhibits resistance to induced point and deletion mutations. Nucleic Acids Res., 2016, 44(18), 8513-8524. [http://dx.doi.org/10.1093/nar/gkw716]. [PMID: 27550180].
[79]
Szczepanowska, K.; Trifunovic, A. Origins of mtDNA mutations in ageing. Essays Biochem., 2017, 61(3), 325-337. [http://dx.doi.org/10.1042/EBC20160090]. [PMID: 28698307].
[80]
Kauppila, T.E.; Kauppila, J.H.; Larsson, N-G. Mammalian mitochondria and aging: An update. Cell Metab., 2017, 25(1), 57-71. [http://dx.doi.org/10.1016/j.cmet.2016.09.017]. [PMID: 28094012].
[81]
McKinney, E.A.; Oliveira, M.T. Replicating animal mitochondrial DNA. Genet. Mol. Biol., 2013, 36(3), 308. [3h1t5tp.. [http://dx.doi.org/10.1590/S1415-47572013000300002]. [PMID: 24130435].
[82]
Shadel, G.S.; Clayton, D.A. Mitochondrial DNA maintenance in vertebrates. Annu. Rev. Biochem., 1997, 66(1), 409-435. [http://dx.doi.org/10.1146/annurev.biochem.66.1.409]. [PMID: 9242913].
[83]
Eoff, R.L.; Raney, K.D. A catch and release program for single-stranded DNA. J. Biol. Chem., 2017, 292(31), 13085-13086. [http://dx.doi.org/10.1074/jbc.H117.791392]. [PMID: 28778884].
[84]
Yamada, T.; Akiyama, H.; McGeer, P.L. Complement-activated oligodendroglia: a new pathogenic entity identified by immunostaining with antibodies to human complement proteins C3d and C4d. Neurosci. Lett., 1990, 112(2-3), 161-166. [http://dx.doi.org/10.1016/0304-3940(90)90196-G]. [PMID: 2359515].
[85]
Reyes, A.; Gissi, C.; Pesole, G.; Saccone, C. Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Mol. Biol. Evol., 1998, 15(8), 957-966. [http://dx.doi.org/10.1093/oxfordjournals.molbev.a026011]. [PMID: 9718723].
[86]
Kaasik, A.; Safiulina, D.; Zharkovsky, A.; Veksler, V. Regulation of mitochondrial matrix volume. Am. J. Physiol. Cell Physiol., 2007, 292(1), C157-C163. [http://dx.doi.org/10.1152/ajpcell.00272.2006]. [PMID: 16870828].
[87]
Clayton, D.A. Transcription and replication of animal mitochondrial DNAs. Int. Rev. Cytol., 1992, 141, 217-232. [http://dx.doi.org/10.1016/S0074-7696(08)62067-7]. [PMID: 1452432].
[88]
Wanrooij, P.H.; Uhler, J.P.; Shi, Y.; Westerlund, F.; Falkenberg, M.; Gustafsson, C.M. A hybrid G-quadruplex structure formed between RNA and DNA explains the extraordinary stability of the mitochondrial R-loop. Nucleic Acids Res., 2012, 40(20), 10334-10344. [http://dx.doi.org/10.1093/nar/gks802]. [PMID: 22965135].
[89]
Zheng, K.W.; Wu, R.Y.; He, Y.D.; Xiao, S.; Zhang, J.Y.; Liu, J.Q.; Hao, Y.H.; Tan, Z. A competitive formation of DNA:RNA hybrid G-quadruplex is responsible to the mitochondrial transcription termination at the DNA replication priming site. Nucleic Acids Res., 2014, 42(16), 10832-10844. [http://dx.doi.org/10.1093/nar/gku764]. [PMID: 25140009].
[90]
Lyonnais, S.; Tarrés-Solé, A.; Rubio-Cosials, A.; Cuppari, A.; Brito, R.; Jaumot, J.; Gargallo, R.; Vilaseca, M.; Silva, C.; Granzhan, A.; Teulade-Fichou, M.P.; Eritja, R.; Solà, M. The human mitochondrial transcription factor A is a versatile G-quadruplex binding protein. Sci. Rep., 2017, 7, 43992. [http://dx.doi.org/10.1038/srep43992]. [PMID: 28276514].
[91]
Agaronyan, K.; Morozov, Y.I.; Anikin, M.; Temiakov, D. Mitochondrial biology. Replication-transcription switch in human mitochondria. Science, 2015, 347(6221), 548-551. [http://dx.doi.org/10.1126/science.aaa0986]. [PMID: 25635099].
[92]
Boulé, J-B.; Zakian, V.A. Roles of Pif1-like helicases in the maintenance of genomic stability. Nucleic Acids Res., 2006, 34(15), 4147-4153. [http://dx.doi.org/10.1093/nar/gkl561]. [PMID: 16935874].
[93]
Futami, K.; Shimamoto, A.; Furuichi, Y. Mitochondrial and nuclear localization of human Pif1 helicase. Biol. Pharm. Bull., 2007, 30(9), 1685-1692. [http://dx.doi.org/10.1248/bpb.30.1685]. [PMID: 17827721].
[94]
Mendoza, O.; Bourdoncle, A.; Boulé, J.B.; Brosh, R.M., Jr; Mergny, J.L. G-quadruplexes and helicases. Nucleic Acids Res., 2016, 44(5), 1989-2006. [http://dx.doi.org/10.1093/nar/gkw079]. [PMID: 26883636].
[95]
Paeschke, K.; Bochman, M.L.; Garcia, P.D.; Cejka, P.; Friedman, K.L.; Kowalczykowski, S.C.; Zakian, V.A. Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature, 2013, 497(7450), 458-462. [http://dx.doi.org/10.1038/nature12149]. [PMID: 23657261].
[96]
Sabouri, N. The functions of the multi-tasking Pfh1Pif1 helicase. Curr. Genet., 2017, 63(4), 621-626. [http://dx.doi.org/10.1007/s00294-016-0675-2]. [PMID: 28054200].
[97]
O’Rourke, T.W.; Doudican, N.A.; Mackereth, M.D.; Doetsch, P.W.; Shadel, G.S. Mitochondrial dysfunction due to oxidative mitochondrial DNA damage is reduced through cooperative actions of diverse proteins. Mol. Cell. Biol., 2002, 22(12), 4086-4093. [http://dx.doi.org/10.1128/MCB.22.12.4086-4093.2002]. [PMID: 12024022].
[98]
Ribeyre, C.; Lopes, J.; Boulé, J.B.; Piazza, A.; Guédin, A.; Zakian, V.A.; Mergny, J.L.; Nicolas, A. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet., 2009, 5(5)e1000475 [http://dx.doi.org/10.1371/journal.pgen.1000475]. [PMID: 19424434].
[99]
Paeschke, K.; Capra, J.A.; Zakian, V.A. DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell, 2011, 145(5), 678-691. [http://dx.doi.org/10.1016/j.cell.2011.04.015]. [PMID: 21620135].
[100]
Snow, B.E.; Mateyak, M.; Paderova, J.; Wakeham, A.; Iorio, C.; Zakian, V.; Squire, J.; Harrington, L. Murine Pif1 interacts with telomerase and is dispensable for telomere function in vivo. Mol. Cell. Biol., 2007, 27(3), 1017-1026. [http://dx.doi.org/10.1128/MCB.01866-06]. [PMID: 17130244].
[101]
Bannwarth, S.; Berg-Alonso, L.; Augé, G.; Fragaki, K.; Kolesar, J.E.; Lespinasse, F.; Lacas-Gervais, S.; Burel-Vandenbos, F.; Villa, E.; Belmonte, F.; Michiels, J.F.; Ricci, J.E.; Gherardi, R.; Harrington, L.; Kaufman, B.A.; Paquis-Flucklinger, V. Inactivation of Pif1 helicase causes a mitochondrial myopathy in mice. Mitochondrion, 2016, 30, 126-137. [http://dx.doi.org/10.1016/j.mito.2016.02.005]. [PMID: 26923168].
[102]
Croteau, D.L.; Rossi, M.L.; Canugovi, C.; Tian, J.; Sykora, P.; Ramamoorthy, M.; Wang, Z.M.; Singh, D.K.; Akbari, M.; Kasiviswanathan, R.; Copeland, W.C.; Bohr, V.A. RECQL4 localizes to mitochondria and preserves mitochondrial DNA integrity. Aging Cell, 2012, 11(3), 456-466. [http://dx.doi.org/10.1111/j.1474-9726.2012.00803.x]. [PMID: 22296597].
[103]
Lyonnais, S.; Tarrés-Solé, A.; Rubio-Cosials, A.; Cuppari, A.; Brito, R.; Jaumot, J.; Gargallo, R.; Vilaseca, M.; Silva, C.; Granzhan, A.; Teulade-Fichou, M.P.; Eritja, R.; Solà, M. The human mitochondrial transcription factor A is a versatile G-quadruplex binding protein. Sci. Rep., 2017, 7, 43992. [http://dx.doi.org/10.1038/srep43992]. [PMID: 28276514].
[104]
Ohno, T.; Umeda, S.; Hamasaki, N.; Kang, D. Binding of human mitochondrial transcription factor A, an HMG box protein, to a four-way DNA junction. Biochem. Biophys. Res. Commun., 2000, 271(2), 492-498. [http://dx.doi.org/10.1006/bbrc.2000.2656]. [PMID: 10799324].
[105]
Antonicka, H.; Sasarman, F.; Nishimura, T.; Paupe, V.; Shoubridge, E.A. The mitochondrial RNA-binding protein GRSF1 localizes to RNA granules and is required for posttranscriptional mitochondrial gene expression. Cell Metab., 2013, 17(3), 386-398. [http://dx.doi.org/10.1016/j.cmet.2013.02.006]. [PMID: 23473033].
[106]
Emerman, A.B.; Zhang, Z-R.; Chakrabarti, O.; Hegde, R.S. LRPPRC and SLIRP Interact in a Ribonucleoprotein Complex That Regulates Posttranscriptional Gene Expression in Mitochondria. Mol. Biol. Cell, 2010, 21(24), 4325-4337. [http://dx.doi.org/10.1091/mbc.e10-09-0742]. [PMID: 20980618].
[107]
Williams, P.; Li, L.; Dong, X.; Wang, Y. Identification of SLIRP as a G quadruplex-binding protein. J. Am. Chem. Soc., 2017, 139(36), 12426-12429. [http://dx.doi.org/10.1021/jacs.7b07563]. [PMID: 28859475].
[108]
Huang, W-C.; Tseng, T-Y.; Chen, Y-T.; Chang, C-C.; Wang, Z-F.; Wang, C-L.; Hsu, T-N.; Li, P-T.; Chen, C-T.; Lin, J-J.; Lou, P.J.; Chang, T.C. Direct evidence of mitochondrial G-quadruplex DNA by using fluorescent anti-cancer agents. Nucleic Acids Res., 2015, 43(21), 10102-10113. [PMID: 26487635].
[109]
Li, C-P.; Huang, J-H.; Chang, A-C.; Hung, Y-M.; Lin, C-H.; Chao, Y.; Lee, S-D.; Whang-Peng, J.; Huang, T-S. A G-quadruplex ligand 3,3′-diethyloxadicarbocyanine iodide induces mitochondrion-mediated apoptosis but not decrease of telomerase activity in nasopharyngeal carcinoma NPC-TW01 cells. Pharm. Res., 2004, 21(1), 93-100. [http://dx.doi.org/10.1023/B:PHAM.0000012166.44521.1f]. [PMID: 14984262].
[110]
Zhuang, X-Y.; Yao, Y-G. Mitochondrial dysfunction and nuclear-mitochondrial shuttling of TERT are involved in cell proliferation arrest induced by G-quadruplex ligands. FEBS Lett., 2013, 587(11), 1656-1662. [http://dx.doi.org/10.1016/j.febslet.2013.04.010]. [PMID: 23603390].

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