Non-canonical DNA structures in the human ribosomal DNA
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
37750997
DOI
10.1007/s00418-023-02233-1
PII: 10.1007/s00418-023-02233-1
Knihovny.cz E-zdroje
- Klíčová slova
- DNA quadruplexes, Non-canonical DNA, R-loops, rDNA,
- MeSH
- G-kvadruplexy * MeSH
- konformace nukleové kyseliny MeSH
- lidé MeSH
- ribozomální DNA genetika MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- ribozomální DNA MeSH
Non-canonical structures (NCS) refer to the various forms of DNA that differ from the B-conformation described by Watson and Crick. It has been found that these structures are usual components of the genome, actively participating in its essential functions. The present review is focused on the nine kinds of NCS appearing or likely to appear in human ribosomal DNA (rDNA): supercoiling structures, R-loops, G-quadruplexes, i-motifs, DNA triplexes, cruciform structures, DNA bubbles, and A and Z DNA conformations. We discuss the conditions of their generation, including their sequence specificity, distribution within the locus, dynamics, and beneficial and detrimental role in the cell.
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Abou Assi H, Garavis M, Gonzalez C, Damha MJ (2018) i-Motif DNA: structural features and significance to cell biology. Nucleic Acids Res 46(16):8038–8056. https://doi.org/10.1093/nar/gky735 PubMed DOI PMC
Abraham KJ, Khosraviani N, Chan JNY, Gorthi A, Samman A, Zhao DRY, Wang ML, Bokros M, Vidya E, Ostrowski LA, Oshidari R, Pietrobon V, Patel PS, Algouneh A, Singhania R, Liu YP, Yerlici VT, De Carvalho DD, Ohh M, Dickson BC, Hakem R, Greenblatt JF, Lee SP, Bishop AJR, Mekhail K (2020) Nucleolar RNA polymerase II drives ribosome biogenesis. Nature 585(7824):298. https://doi.org/10.1038/s41586-020-2497-0 PubMed DOI PMC
Aguilera A, Garcia-Muse T (2012) R loops: from transcription byproducts to threats to genome stability. Mol Cell 46(2):115–124. https://doi.org/10.1016/j.molcel.2012.04.009 PubMed DOI
Albert B, Leger-Silvestre I, Normand C, Ostermaier MK, Perez-Fernandez J, Panov KI, Zomerdijk JCBM, Schultz P, Gadal O (2011) RNA polymerase I-specific subunits promote polymerase clustering to enhance the rRNA gene transcription cycle. J Cell Biol 192(2):277–293. https://doi.org/10.1083/jcb.201006040 PubMed DOI PMC
Alexandrov BS, Gelev V, Yoo SW, Alexandrov LB, Fukuyo Y, Bishop AR, Rasmussen KO, Usheva A (2010) DNA dynamics play a role as a basal transcription factor in the positioning and regulation of gene transcription initiation. Nucleic Acids Res 38(6):1790–1795. https://doi.org/10.1093/nar/gkp1084 PubMed DOI
Alexandrov BS, Fukuyo Y, Lange M, Horikoshi N, Gelev V, Rasmussen KO, Bishop AR, Usheva A (2012) DNA breathing dynamics distinguish binding from nonbinding consensus sites for transcription factor YY1 in cells. Nucleic Acids Res 40(20):10116–10123. https://doi.org/10.1093/nar/gks758 PubMed DOI PMC
Allison DF, Wang GG (2019) R-loops: formation, function, and relevance to cell stress. Cell Stress 3(2):38–46. https://doi.org/10.15698/cst2019.02.175 PubMed DOI PMC
Altan-Bonnet G, Libchaber A, Krichevsky O (2003) Bubble dynamics in double-stranded DNA. Phys Rev Lett. https://doi.org/10.1103/PhysRevLEtt.90.138101 PubMed DOI
Amon JD, Koshland D (2016) RNase H enables efficient repair of R-loop induced DNA damage. Elife. https://doi.org/10.7554/eLife.20533 PubMed DOI PMC
Athanasiadis A (2012) Zalpha-domains: At the intersection between RNA editing and innate immunity. Semin Cell Dev Biol 23(3):275–280. https://doi.org/10.1016/j.semcdb.2011.11.001 PubMed DOI
Audas TE, Jacob MD, Lee S (2012) The nucleolar detention pathway A cellular strategy for regulating molecular networks. Cell Cycle 11(11):2059–2062. https://doi.org/10.4161/cc.20140 PubMed DOI PMC
Bag S, Burman MD, Bhowmik S (2023) Structural insights and shedding light on preferential interactions of dietary flavonoids with G-quadruplex DNA structures: a new horizon. Heliyon. https://doi.org/10.1016/j.heliyon.2023.e13959 PubMed DOI PMC
Bancaud A, Huet S, Daigle N, Mozziconacci J, Beaudouin J, Ellenberg J (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. Embo J 28(24):3785–3798. https://doi.org/10.1038/emboj.2009.340 PubMed DOI PMC
Banerjee A, Sobell HM (1983) Presence of nonlinear excitations in DNA-structure and their relationship to DNA premelting and to drug intercalation. J Biomol Struct Dyn 1(1):253–262. https://doi.org/10.1080/07391102.1983.10507438 PubMed DOI
Baranello L, Levens D, Kouzine F (2018) DNA Supercoiling(omics). In: Lavelle C, Victor J-M (eds) Nuclear Architecture and Dynamics, vol 2. Academic Press, Boston
Bassett A, Cooper S, Wu CY, Travers A (2009) The folding and unfolding of eukaryotic chromatin. Curr Opin Genet Dev 19(2):159–165. https://doi.org/10.1016/j.gde.2009.02.010 PubMed DOI
Bazett-Jones DP, Leblanc B, Herfort M, Moss T (1994) Short-range DNA looping by the xenopus hmg-box transcription factor. Xubf Science 264(5162):1134–1137. https://doi.org/10.1126/science.8178172 PubMed DOI
Belotserkovskii BP, Mirkin SM, Hanawalt PC (2013) DNA sequences that interfere with transcription: implications for genome function and stability. Chem Rev 113(11):8620–8637. https://doi.org/10.1021/cr400078y PubMed DOI
Ben-Shem A, Jenner L, Yusupova G, Yusupov M (2010) Crystal structure of the eukaryotic ribosome. Science 330(6008):1203–1209. https://doi.org/10.1126/science.1194294 PubMed DOI
Bhaysar-Jog YP, Van Dornshuld E, Brooks TA, Tschumper GS, Wadkins RM (2014) Epigenetic modification, dehydration, and molecular crowding effects on the thermodynamics of i-motif structure formation from C-Rich DNA. Biochemistry 53(10):1586–1594. https://doi.org/10.1021/bi401523b DOI
Bierhoff H, Schmitz K, Maass F, Ye J, Grummt I (2010) Noncoding transcripts in sense and antisense orientation regulate the epigenetic state of ribosomal RNA genes. Cold Spring Harb Symp Quant Biol 75:357–364. https://doi.org/10.1101/sqb.2010.75.060 PubMed DOI
Bierhoff H, Postepska-Igielska A, Grummt I (2014) Noisy silence Non-coding RNA and heterochromatin formation at repetitive elements. Epigenetics 9(1):53–61. https://doi.org/10.4161/epi.26485 PubMed DOI
Brazda V, Laister RC, Jagelska EB, Arrowsmith C (2011) Cruciform structures are a common DNA feature important for regulating biological processes. Bmc Mol Biol. https://doi.org/10.1186/1471-2199-12-33 PubMed DOI PMC
Brazda V, Bartas M, Lysek J, Coufal J, Fojta M (2020) Global analysis of inverted repeat sequences in human gene promoters reveals their non-random distribution and association with specific biological pathways. Genomics 112(4):2772–2777. https://doi.org/10.1016/j.ygeno.2020.03.014 PubMed DOI
Brooks TA, Kendrick S, Hurley L (2010) Making sense of G-quadruplex and i-motif functions in oncogene promoters. Febs J 277(17):3459–3469. https://doi.org/10.1111/j.1742-4658.2010.07759.x PubMed DOI PMC
Byrd AK, Zybailov BL, Maddukuri L, Gao J, Marecki JC, Jaiswal M, Bell MR, Griffin WC, Reed MR, Chib S, Mackintosh SG, MacNicol AM, Baldini G, Eoff RL, Raney KD (2016) Evidence that G-quadruplex DNA accumulates in the cytoplasm and participates in stress granule assembly in response to oxidative stress. J Biol Chem 291(34):18041–18057. https://doi.org/10.1074/jbc.M116.718478 PubMed DOI PMC
Caburet S, Conti C, Schurra C, Lebofsky R, Edelstein SJ, Bensimon A (2005) Human ribosomal RNA gene arrays display a broad range of palindromic structures. Genome Res 15(8):1079–1085. https://doi.org/10.1101/gr.3970105 PubMed DOI PMC
Caudron-Herger M, Pankert T, Seiler J, Németh A, Voit R, Grummt I, Rippe K (2015) Alu element-containing RNAs maintain nucleolar structure and function. Embo J 34(22):2758–2774. https://doi.org/10.15252/embj.201591458 PubMed DOI PMC
Cer RZ, Bruce KH, Mudunuri US, Yi M, Volfovsky N, Luke BT, Bacolla A, Collins JR, Stephens RM (2011) Non-B DB: a database of predicted non-B DNA-forming motifs in mammalian genomes. Nucleic Acids Res 39:D383–D391. https://doi.org/10.1093/nar/gkq1170 PubMed DOI
Cerna A, Cuadrado A, Jouve N, Diaz de la Espina SM, De la Torre C (2004) Z-DNA, a new in situ marker for transcription. Eur J Histochem 48(1):49–56 PubMed
Cerritelli SM, Crouch RJ (2009) Ribonuclease H: the enzymes in eukaryotes. Febs J 276(6):1494–1505. https://doi.org/10.1111/j.1742-4658.2009.06908.x PubMed DOI
Chambers VS, Marsico G, Boutell JM, Di Antonio M, Smith GP, Balasubramanian S (2015) High-throughput sequencing of DNA G-quadruplex structures in the human genome. Nat Biotechnol 33(8):877–881. https://doi.org/10.1038/nbt.3295 PubMed DOI
Champ PC, Maurice S, Vargason JM, Camp T, Ho PS (2004) Distributions of Z-DNA and nuclear factor I in human chromosome 22: a model for coupled transcriptional regulation. Nucleic Acids Res 32(22):6501–6510. https://doi.org/10.1093/nar/gkh988 PubMed DOI PMC
Chan PP, Glazer PM (1997) Triplex DNA: fundamentals, advances, and potential applications for gene therapy. J Mol Med (berl) 75(4):267–282. https://doi.org/10.1007/s001090050112 PubMed DOI
Chaudhuri J, Basu U, Zarrin A, Yan C, Franco S, Perlot T, Vuong B, Wang J, Phan RT, Datta A, Manis J, Alt FW (2007) Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 94:157–214. https://doi.org/10.1016/S0065-2776(06)94006-1 PubMed DOI
Chiarella S, De Cola A, Scaglione GL, Carletti E, Graziano V, Barcaroli D, Lo Sterzo C, Di Matteo A, Di Ilio C, Falini B, Arcovito A, De Laurenzi V, Federici L (2013) Nucleophosmin mutations alter its nucleolar localization by impairing G-quadruplex binding at ribosomal DNA. Nucleic Acids Res 41(5):3228–3239. https://doi.org/10.1093/nar/gkt001 PubMed DOI PMC
Chmurciakova N, Smirnov E, Kurfurst J, Liska F, Cmarko D (2022) Variability of human rDNA and transcription activity of the ribosomal genes. Int J Mol Sci 23(23):15195. https://doi.org/10.3390/ijms232315195 PubMed DOI PMC
Choi J, Majima T (2011) Conformational changes of non-B DNA. Chem Soc Rev 40(12):5893–5909. https://doi.org/10.1039/c1cs15153c PubMed DOI
Choi CH, Kalosakas G, Rasmussen KO, Hiromura M, Bishop AR, Usheva A (2004) DNA dynamically directs its own transcription initiation. Nucleic Acids Res 32(4):1584–1590. https://doi.org/10.1093/nar/gkh335 PubMed DOI PMC
Costantino L, Koshland D (2018) Genome-wide map of R-Loop-induced damage reveals how a subset of R-loops contributes to genomic instability. Mol Cell 71(4):487. https://doi.org/10.1016/j.molcel.2018.06.037 PubMed DOI PMC
Cozzarelli NR, Boles TC, White JH (1990) Primer on the Topology and geometry of DNA supercoiling. In: Cozzarelli NR, Wang JC (eds) DNA Topology and its Biological Effects, vol 20. Cold Spring Harbor Laboratory Press, NY, pp 139–184
Cui JJ, Waltman P, Le VH, Lewis EA (2013) The effect of molecular crowding on the stability of human c-MYC promoter sequence I-motif at neutral pH. Molecules 18(10):12751–12767. https://doi.org/10.3390/molecules181012751 PubMed DOI PMC
Cui YX, Kong DM, Ghimire C, Xu CX, Mao HB (2016) Mutually exclusive formation of G-quadruplex and i-motif Is a general phenomenon governed by steric hindrance in duplex DNA. Biochemistry 55(15):2291–2299. https://doi.org/10.1021/acs.biochem.6b00016 PubMed DOI
D’Alessandro G, Whelan DR, Howard SM, Vitelli V, Renaudin X, Adamowicz M, Iannelli F, Jones-Weinert CW, Lee M, Matti V, Lee WTC, Morten MJ, Venkitaraman AR, Cejka P, Rothenberg E, di Fagagna FD (2018) BRCA2 controls DNA:RNA hybrid level at DSBs by mediating RNase H2 recruitment. Nat Commun. https://doi.org/10.1038/s41467-018-07799-2 PubMed DOI PMC
Datta A, Pollock KJ, Kormuth KA, Brosh RM (2021) G-Quadruplex assembly by ribosomal DNA: emerging roles in disease pathogenesis and cancer biology. Cytogenet Genome Res 161(6–7):285–296. https://doi.org/10.1159/000516394 PubMed DOI
De Magis A, Manzo SG, Russo M, Marinello J, Morigi R, Sordet O, Capranico G (2019) DNA damage and genome instability by G-quadruplex ligands are mediated by R loops in human cancer cells. P Natl Acad Sci USA 116(3):816–825. https://doi.org/10.1073/pnas.1810409116 DOI
Denissov S, Lessard F, Mayer C, Stefanovsky V, van Driel M, Grummt I, Moss T, Stunnenberg HG (2011) A model for the topology of active ribosomal RNA genes. Embo Rep 12(3):231–237. https://doi.org/10.1038/embor.2011.8 PubMed DOI PMC
Dornberger U, Leijon M, Fritzsche H (1999) High base pair opening rates in tracts of GC base pairs. J Biol Chem 274(11):6957–6962. https://doi.org/10.1074/jbc.274.11.6957 PubMed DOI
Drew HR, Weeks JR, Travers AA (1985) Negative supercoiling induces spontaneous unwinding of a bacterial promoter. Embo J 4(4):1025–1032. https://doi.org/10.1002/j.1460-2075.1985.tb03734.x PubMed DOI PMC
Drolet M (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59(3):723–730. https://doi.org/10.1111/j.1365-2958.2005.05006.x PubMed DOI
Drosopoulos WC, Kosiyatrakul ST, Schildkraut CL (2015) BLM helicase facilitates telomere replication during leading strand synthesis of telomeres. J Cell Biol 210(2):191–208. https://doi.org/10.1083/jcb.201410061 PubMed DOI PMC
Drygin D, Siddiqui-Jain A, O’Brien S, Schwaebe M, Lin A, Bliesath J, Ho CB, Proffitt C, Trent K, Whitten JP, Lim JKC, Von Hoff D, Anderes K, Rice WG (2009) Anticancer activity of CX-3543: A Direct inhibitor of rRNA biogenesis. Cancer Res 69(19):7653–7661. https://doi.org/10.1158/0008-5472.Can-09-1304 PubMed DOI
Duardo RC, Guerra F, Pepe S, Capranico G (2023) Non-B DNA structures as a booster of genome instability. Biochimie. https://doi.org/10.1016/j.biochi.2023.07.002 PubMed DOI
Fei JY, Ha T (2013) Watching DNA breath one molecule at a time. P Natl Acad Sci USA 110(43):17173–17174. https://doi.org/10.1073/pnas.1316493110 DOI
Firulli AB, Maibenco DC, Kinniburgh AJ (1994) Triplex forming ability of a C-Myc promoter element predicts promoter strength. Arch Biochem Biophys 310(1):236–242. https://doi.org/10.1006/abbi.1994.1162 PubMed DOI
Fleming AM, Ding Y, Rogers RA, Zhu J, Zhu J, Burton AD, Carlisle CB, Burrows CJ (2017) 4n–1 Is a “Sweet Spot” in DNA i-Motif Folding of 2 ’-deoxycytidine homopolymers. J Am Chem Soc 139(13):4682–4689. https://doi.org/10.1021/jacs.6b10117 PubMed DOI
Fogg JM, Randall GL, Pettitt BM, Sumners DL, Harris SA, Zechiedrich L (2012) Bullied no more: when and how DNA shoves proteins around. Q Rev Biophys 45(3):257–299. https://doi.org/10.1017/S0033583512000054 PubMed DOI PMC
Fogg JM, Judge AK, Stricker E, Chan HL, Zechiedrich L (2021) Supercoiling and looping promote DNA base accessibility and coordination among distant sites. Nat Commun. https://doi.org/10.1038/s41467-021-25936-2 PubMed DOI PMC
Foloppe N, MacKerell AD (1999) Intrinsic conformational properties of deoxyribonucleosides: implicated role for cytosine in the equilibrium among the A, B, and Z forms of DNA. Biophys J 76(6):3206–3218. https://doi.org/10.1016/S0006-3495(99)77472-2 PubMed DOI PMC
Frank-Kamenetskii MD, Mirkin SM (1995) Triplex DNA structures. Annu Rev Biochem 64:65–95. https://doi.org/10.1146/annurev.bi.64.070195.000433 PubMed DOI
Freund AM, Bichara M, Fuchs RPP (1989) Z-DNA-forming sequences are spontaneous deletion hot spots. P Natl Acad Sci USA 86(19):7465–7469. https://doi.org/10.1073/pnas.86.19.7465 DOI
Gaddis SS, Wu Q, Thames HD, Digiovanni J, Walborg EF, MacLeod MC, Vasquez KM (2006) A web-based search engine for triplex-forming oligonucleotide target sequences. Oligonucleotides 16(2):196–201. https://doi.org/10.1089/oli.2006.16.196 PubMed DOI
Garner MM, Felsenfeld G (1987) Effect of Z-DNA on Nucleosome Placement. J Mol Biol 196(3):581–590. https://doi.org/10.1016/0022-2836(87)90034-9 PubMed DOI
Gehring K, Leroy JL, Gueron M (1993) A tetrameric DNA-structure with protonated cytosine. Cytosine Base-Pairs Nature 363(6429):561–565. https://doi.org/10.1038/363561a0 PubMed DOI
Glaser RL, Thomas GH, Siegfried E, Elgin SCR, Lis JT (1990) Optimal heat-induced expression of the drosophila Hsp26 gene requires a promoter sequence containing (Ct)N(Ga)N repeats. J Mol Biol 211(4):751–761. https://doi.org/10.1016/0022-2836(90)90075-W PubMed DOI
Grabczyk E, Fishman MC (1995) A long purine-pyrimidine homopolymer acts as a transcriptional diode. J Biol Chem 270(4):1791–1797. https://doi.org/10.1074/jbc.270.4.1791 PubMed DOI
Groh M, Gromak N (2014) Out of balance: R-loops in human disease. Plos Genet. https://doi.org/10.1371/journal.pgen.1004630 PubMed DOI PMC
Gupta A, Kulkarni M, Mukherjee A (2021) Accurate prediction of B-form/A-form DNA conformation propensity from primary sequence: a machine learning and free energy handshake. Patterns 2(9):100329. https://doi.org/10.1016/j.patter.2021.100329 PubMed DOI PMC
Ha SC, Lowenhaupt K, Rich A, Kim YG, Kim KK (2005) Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature 437(7062):1183–1186. https://doi.org/10.1038/nature04088 PubMed DOI
Hall AC, Ostrowski LA, Pietrobon V, Mekhail K (2017) Repetitive DNA loci and their modulation by the non-canonical nucleic acid structures R-loops and G-quadruplexes. Nucleus 8(2):162–181. https://doi.org/10.1080/19491034.2017.1292193 PubMed DOI PMC
Hanakahi LA, Sun H, Maizels N (1999) High affinity interactions of nucleolin with G-G-paired rDNA. J Biol Chem 274(22):15908–15912. https://doi.org/10.1074/jbc.274.22.15908 PubMed DOI
Hancock R (2004) Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol Cell 96(8):595–601. https://doi.org/10.1016/j.biolcel.2004.05.003 PubMed DOI
Hansel-Hertsch R, Spiegel J, Marsico G, Tannahill D, Balasubramanian S (2018) Genome-wide mapping of endogenous G-quadruplex DNA structures by chromatin immunoprecipitation and high-throughput sequencing. Nat Protoc 13(3):551–564. https://doi.org/10.1038/nprot.2017.150 PubMed DOI
Hao Q, Prasanth KV (2022) Regulatory roles of nucleolus organizer region-derived long non-coding RNAs. Mamm Genome 33(2):402–411. https://doi.org/10.1007/s00335-021-09906-z PubMed DOI
Herbert A (2019) Z-DNA and Z-RNA in human disease. Commun Biol 2:7. https://doi.org/10.1038/s42003-018-0237-x PubMed DOI PMC
Hershman SG, Chen Q, Lee JY, Kozak ML, Yue P, Wang LS, Johnson FB (2008) Genomic distribution and functional analyses of potential G-quadruplex-forming sequences in Saccharomyces cerevisiae. Nucleic Acids Res 36(1):144–156. https://doi.org/10.1093/nar/gkm986 PubMed DOI
Hoshina S, Yura K, Teranishi H, Kiyasu N, Tominaga A, Kadoma H, Nakatsuka A, Kunichika T, Obuse C, Waga S (2013) Human origin recognition complex binds preferentially to G-quadruplex-preferable RNA and single-stranded DNA. J Biol Chem 288(42):30161–30171. https://doi.org/10.1074/jbc.M113.492504 PubMed DOI PMC
Hu Y, Cecconello A, Idili A, Ricci F, Willner I (2017) Triplex DNA nanostructures: from basic properties to applications. Angew Chem Int Ed Engl 56(48):15210–15233. https://doi.org/10.1002/anie.201701868 PubMed DOI
Huppert JL, Balasubramanian S (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 35(2):406–413. https://doi.org/10.1093/nar/gkl1057 PubMed DOI
Indig FE, Rybanska I, Karmakar P, Devulapalli C, Fu HQ, Carrier F, Bohr VA (2012) Nucleolin inhibits G4 oligonucleotide unwinding by werner helicase. PLoS ONE 7(6):325229. https://doi.org/10.1371/journal.pone.0035229 DOI
Jain A, Wang G, Vasquez KM (2008) DNA triple helices: biological consequences and therapeutic potential. Biochimie 90(8):1117–1130. https://doi.org/10.1016/j.biochi.2008.02.011 PubMed DOI PMC
James PL, Brown T, Fox KR (2003) Thermodynamic and kinetic stability of intermolecular triple helices containing different proportions of C+*GC and T*AT triplets. Nucleic Acids Res 31(19):5598–5606. https://doi.org/10.1093/nar/gkg782 PubMed DOI PMC
Jose D, Weitzel SE, von Hippel PH (2012) Breathing fluctuations in position-specific DNA base pairs are involved in regulating helicase movement into the replication fork. P Natl Acad Sci USA 109(36):14428–14433. https://doi.org/10.1073/pnas.1212929109 DOI
Kaulage MH, Bhattacharya S, Muniyappa K (2018) Structural characterization of i-Motif structure in the human Acetyl-CoA carboxylase1 gene promoters and their role in the regulation of gene expression. ChemBioChem 19(10):1078–1087. https://doi.org/10.1002/cbic.201800021 PubMed DOI
Kaushik M, Kaushik S, Roy K, Singh A, Mahendru S, Kumar M, Chaudhary S, Ahmed S, Kukreti S (2016) A bouquet of DNA structures: emerging diversity. Biochem Biophys Rep 5:388–395. https://doi.org/10.1016/j.bbrep.2016.01.013 PubMed DOI PMC
Kendrick S, Akiyama Y, Hecht SM, Hurley LH (2009) The i-motif in the bcl-2 P1 promoter forms an unexpectedly stable structure with a unique 8:5:7 loop folding pattern. J Am Chem Soc 131(48):17667–17676. https://doi.org/10.1021/ja9076292 PubMed DOI PMC
Kim JH, Dilthey AT, Nagaraja R, Lee HS, Koren S, Dudekula D, Wood Iii WH, Piao Y, Ogurtsov AY, Utani K, Noskov VN, Shabalina SA, Schlessinger D, Phillippy AM, Larionov V (2018a) Variation in human chromosome 21 ribosomal RNA genes characterized by TAR cloning and long-read sequencing. Nucleic Acids Res 46(13):6712–6725. https://doi.org/10.1093/nar/gky442 PubMed DOI PMC
Kim SH, Ganji M, Kim E, van der Torre J, Abbondanzieri E, Dekker C (2018b) DNA sequence encodes the position of DNA supercoils. Elife. https://doi.org/10.7554/eLife.36557 PubMed DOI PMC
Kobayashi T (2014) Ribosomal RNA gene repeats, their stability and cellular senescence. P Jpn Acad B-Phys 90(4):119–129. https://doi.org/10.2183/pjab.90.119 DOI
Kouzine F, Wojtowicz D, Baranello L, Yamane A, Nelson S, Resch W, Kieffer-Kwon KR, Benham CJ, Casellas R, Przytycka TM, Levens D (2017) Permanganate/S1 nuclease footprinting reveals non-B DNA structures with regulatory potential across a mammalian genome. Cell Syst 4(3):344–356. https://doi.org/10.1016/j.cels.2017.01.013 PubMed DOI PMC
Krall JB, Nichols PJ, Henen MA, Vicens Q, Vogeli B (2023) Structure and formation of Z-DNA and Z-RNA. Molecules 28(2):843. https://doi.org/10.3390/molecules28020843 PubMed DOI PMC
Kulkarni M, Mukherjee A (2017) Understanding B-DNA to A-DNA transition in the right-handed DNA helix: Perspective from a local to global transition. Prog Biophys Mol Bio 128:63–73. https://doi.org/10.1016/j.pbiomolbio.2017.05.009 DOI
Lafer EM, Valle RPC, Moller A, Nordheim A, Schur PH, Rich A, Stollar BD (1983) Z-DNA-specific antibodies in human systemic Lupus-erythematosus. J Clin Invest 71(2):314–321. https://doi.org/10.1172/Jci110771 PubMed DOI PMC
Lankas F, Lavery R, Maddocks JH (2006) Kinking occurs during molecular dynamics simulations of small DNA minicircles. Structure 14(10):1527–1534. https://doi.org/10.1016/j.str.2006.08.004 PubMed DOI
Lee KS, Bumbaca D, Kosman J, Setlow P, Jedrzejas MJ (2008) Structure of a protein-DNA complex essential for DNA protection in spores of bacillus species. P Natl Acad Sci USA 105(8):2806–2811. https://doi.org/10.1073/pnas.0708244105 DOI
Lee M, Kim SH, Hong SC (2010) Minute negative superhelicity is sufficient to induce the B-Z transition in the presence of low tension. P Natl Acad Sci USA 107(11):4985–4990. https://doi.org/10.1073/pnas.0911528107 DOI
Levens D (2008) How the c-myc promoter works and why it sometimes does not. JNCI Monographs 2008(39):41–43. https://doi.org/10.1093/jncimonographs/lgn004 DOI
Li Z, Hann SR (2013) Nucleophosmin is essential for c-Myc nucleolar localization and c-Myc-mediated rDNA transcription. Oncogene 32(15):1988–1994. https://doi.org/10.1038/onc.2012.227 PubMed DOI
Lilley DMJ, White MF (2001) The junction-resolving enzymes. Nat Rev Mol Cell Bio 2(6):433–443. https://doi.org/10.1038/35073057 DOI
Liu LF, Wang JC (1987) Supercoiling of the DNA-template during transcription. P Natl Acad Sci USA 84(20):7024–7027. https://doi.org/10.1073/pnas.84.20.7024 DOI
Lu XJ, Shakked Z, Olson WK (2000) A-form conformational motifs in ligand-bound DNA structures. J Mol Biol 300(4):819–840. https://doi.org/10.1006/jmbi.2000.3690 PubMed DOI
Makova KD, Weissensteiner MH (2023) Noncanonical DNA structures are drivers of genome evolution. Trends Genet 39(2):109–124. https://doi.org/10.1016/j.tig.2022.11.005 PubMed DOI
Maldonado R, Filarsky M, Grummt I, Langst G (2018) Purine- and pyrimidine-triple-helix-forming oligonucleotides recognize qualitatively different target sites at the ribosomal DNA locus. RNA 24(3):371–380. https://doi.org/10.1261/rna.063800.117 PubMed DOI PMC
Malig M, Hartono SR, Giafaglione JM, Sanz LA, Chedin F (2020) Ultra-deep coverage single-molecule R-loop footprinting reveals principles of R-loop formation. J Mol Biol 432(7):2271–2288. https://doi.org/10.1016/j.jmb.2020.02.014 PubMed DOI PMC
Manzo SG, Hartono SR, Sanz LA, Marinello J, De Biasi S, Cossarizza A, Capranico G, Chedin F (2018) DNA topoisomerase I differentially modulates R-loops across the human genome. Genome Biol. https://doi.org/10.1186/s13059-018-1478-1 PubMed DOI PMC
Marchena-Cruz E, Camino LP, Bhandari J, Silva S, Marqueta-Gracia JJ, Amdeen SA, Guillen-Mendoza C, Garcia-Rubio ML, Calderon-Montano JM, Xue X, Luna R, Aguilera A (2023) DDX47, MeCP2, and other functionally heterogeneous factors protect cells from harmful R loops. Cell Rep 42(3):112148. https://doi.org/10.1016/j.celrep.2023.112148 PubMed DOI PMC
Marinello J, Bertoncini S, Aloisi I, Cristini A, Tagliazucchi GM, Forcato M, Sordet O, Capranico G (2016) Dynamic effects of topoisomerase I Inhibition on R-Loops and short transcripts at active promoters. PLoS ONE 11(1):147053. https://doi.org/10.1371/journal.pone.0147053 DOI
Matson JP, Zou L (2020) A genome-wide and cotranscriptional suppressor of R loops. Genes Dev 34(13–14):863–864. https://doi.org/10.1101/gad.339861.120 PubMed DOI PMC
Matthews AJ, Zheng S, DiMenna LJ, Chaudhuri J (2014) Regulation of immunoglobulin class-switch recombination: choreography of noncoding transcription, targeted DNA deamination, and long-range DNA repair. Adv Immunol 122:1–57. https://doi.org/10.1016/B978-0-12-800267-4.00001-8 PubMed DOI PMC
Matyasek R, Kuderova A, Kutilkova E, Kucera M, Kovarik A (2019) Intragenomic heterogeneity of intergenic ribosomal DNA spacers in Cucurbita moschata is determined by DNA minisatellites with variable potential to form non-canonical DNA conformations. DNA Res 26(3):273–286. https://doi.org/10.1093/dnares/dsz008 PubMed DOI PMC
Mayer C, Schmitz KM, Li JW, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22(3):351–361. https://doi.org/10.1016/j.molcel.2006.03.028 PubMed DOI
Mayer C, Neubert M, Grummt I (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. Embo Rep 9(8):774–780. https://doi.org/10.1038/embor.2008.109 PubMed DOI PMC
Mikheikin AL, Lushnikov AY, Lyubchenko YL (2006) Effect of DNA supercoiling on the geometry of holliday junctions. Biochemistry 45(43):12998–13006. https://doi.org/10.1021/bi061002k PubMed DOI
Miller OL, Beatty BR (1969) Visualization of nucleolar genes. Science 164(3882):955. https://doi.org/10.1126/science.164.3882.955 PubMed DOI
Mir B, Serrano I, Buitrago D, Orozco M, Escaja N, Gonzalez C (2017) Prevalent sequences in the human genome can form mini i-Motif structures at physiological pH. J Am Chem Soc 139(40):13985–13988. https://doi.org/10.1021/jacs.7b07383 PubMed DOI
Mirkin SM (2007) Expandable DNA repeats and human disease. Nature 447(7147):932–940. https://doi.org/10.1038/nature05977 PubMed DOI
Mukundan VT, Phan AT (2013) Bulges in G-quadruplexes: broadening the definition of G-Quadruplex-forming sequences. J Am Chem Soc 135(13):5017–5028. https://doi.org/10.1021/ja310251r PubMed DOI
Nadel J, Athanasiadou R, Lemetre C, Wijetunga NA, Broin PO, Sato H, Zhang ZD, Jeddeloh J, Montagna C, Golden A, Seoighe C, Greally JM (2015) RNA:DNA hybrids in the human genome have distinctive nucleotide characteristics, chromatin composition, and transcriptional relationships. Epigenet Chromatin. https://doi.org/10.1186/s13072-015-0040-6 DOI
Neil AJ, Liang MU, Khristich AN, Shah KA, Mirkin SM (2018) RNA-DNA hybrids promote the expansion of Friedreich’s ataxia (GAA)(n) repeats via break-induced replication. Nucleic Acids Res 46(7):3487–3497. https://doi.org/10.1093/nar/gky099 PubMed DOI PMC
Nemeth A, Langst G (2011) Genome organization in and around the nucleolus. Trends Genet 27(4):149–156. https://doi.org/10.1016/j.tig.2011.01.002 PubMed DOI
Niehrs C, Luke B (2020) Regulatory R-loops as facilitators of gene expression and genome stability. Nat Rev Mol Cell Bio 21(3):167–178. https://doi.org/10.1038/s41580-019-0206-3 DOI
Nurk S, Koren S, Rhie A, Rautiainen M, Bzikadze AV, Mikheenko A, Vollger MR, Altemose N, Uralsky L, Gershman A, Aganezov S, Hoyt SJ, Diekhans M, Logsdon GA, Alonge M, Antonarakis SE, Borchers M, Bouffard GG, Brooks SY, Caldas GV, Chen NC, Cheng HY, Chin CS, Chow W, de Lima LG, Dishuck PC, Durbin R, Dvorkina T, Fiddes IT, Formenti G, Fulton RS, Fungtammasan A, Garrison E, Grady PGS, Graves-Lindsay TA, Hall IM, Hansen NF, Hartley GA, Haukness M, Howe K, Hunkapiller MW, Jain C, Jain M, Jarvis ED, Kerpedjiev P, Kirsche M, Kolmogorov M, Korlach J, Kremitzki M, Li H, Maduro VV, Marschall T, McCartney AM, McDaniel J, Miller DE, Mullikin JC, Myers EW, Olson ND, Paten B, Peluso P, Pevzner PA, Porubsky D, Potapova T, Rogaev EI, Rosenfeld JA, Salzberg SL, Schneider VA, Sedlazeck FJ, Shafin K, Shew CJ, Shumate A, Sims Y, Smit AFA, Soto DC, Sovic I, Storer JM, Streets A, Sullivan BA, Thibaud-Nissen F, Torrance J, Wagner J, Walenz BP, Wenger A, Wood JMD, Xiao CL, Yan SM, Young AC, Zarate S, Surti U, McCoy RC, Dennis MY, Alexandrov IA, Gerton JL, O’Neill RJ, Timp W, Zook JM, Schatz MC, Eichler EE, Miga KH, Phillippy AM (2022) The complete sequence of a human genome. Science 376(6588):44–53. https://doi.org/10.1126/science.abj6987 PubMed DOI PMC
Palecek E (1991) Local supercoil-stabilized DNA structures. Crit Rev Biochem Mol 26(2):151–226. https://doi.org/10.3109/10409239109081126 DOI
Palumbo SL, Ebbinghaus SW, Hurley LH (2009) 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 131(31):10878–10891. https://doi.org/10.1021/ja902281d PubMed DOI PMC
Pearson CE, Zorbas H, Price GB, ZannisHadjopoulos M (1996) Inverted repeats, stem-loops, and cruciforms: significance for initiation of DNA replication. J Cell Bioch 63(1):1–22 DOI
Peyrard M, Cuesta-Lopez S, James G (2009) Nonlinear analysis of the dynamics of DNA breathing. J Biol Phys 35(1):73–89. https://doi.org/10.1007/s10867-009-9127-2 PubMed DOI PMC
Pirogov SA, Gvozdev VA, Klenov MS (2019) Long Noncoding RNAs and Stress Response in the Nucleolus. Cells. https://doi.org/10.3390/cells807066 PubMed DOI PMC
Prohofsky EW (1988) Solitons hiding in DNA and their possible significance in Rna-transcription. Phys Rev A 38(3):1538–1541. https://doi.org/10.1103/PhysRevA.38.1538 DOI
Puget N, Miller KM, Legube G (2019) Non-canonical DNA/RNA structures during transcription-coupled double-strand break repair: roadblocks or Bona fide repair intermediates? DNA Repair 81:102661. https://doi.org/10.1016/j.dnarep.2019.102661 PubMed DOI PMC
Ravichandran S, Subramani VK, Kim KK (2019) Z-DNA in the genome: from structure to disease. Biophys Rev 11(3):383–387. https://doi.org/10.1007/s12551-019-00534-1 PubMed DOI PMC
Reaban ME, Lebowitz J, Griffin JA (1994) Transcription induces the formation of a stable RNA DNA hybrid in the immunoglobulin alpha switch region. J Biol Chem 269(34):21850–21857 PubMed DOI
Rich A, Zhang S (2003) Timeline: Z-DNA: the long road to biological function. Nat Rev Genet 4(7):566–572. https://doi.org/10.1038/nrg1115 PubMed DOI
Salvi JS, Chan JN, Szafranski K, Liu TT, Wu JD, Olsen JB, Khanam N, Poon BP, Emili A, Mekhail K (2014) Roles for Pbp1 and caloric restriction in genome and lifespan maintenance via suppression of RNA-DNA hybrids. Dev Cell 30(2):177–191. https://doi.org/10.1016/j.devcel.2014.05.013 PubMed DOI
Sanchez-Martin V, Schneider DA, Ortiz-Gonzalez M, Soriano-Lerma A, Linde-Rodriguez A, Perez-Carrasco V, Gutierrez-Fernandez J, Cuadros M, Gonzalez C, Soriano M, Garcia-Salcedo JA (2021) Targeting ribosomal G-quadruplexes with naphthalene-diimides as RNA polymerase I inhibitors for colorectal cancer treatment. Cell Chem Biol 28(11):1590. https://doi.org/10.1016/j.chembiol.2021.05.021 PubMed DOI
Sander EE, Grummt I (1997) Oligomerization of the transcription termination factor TTF-I: Implications for the structural organization of ribosomal transcription units. Nucleic Acids Res 25(6):1142–1147. https://doi.org/10.1093/nar/25.6.1142 PubMed DOI PMC
Santoro R, Schmitz KM, Sandoval J, Grummt I (2010) Intergenic transcripts originating from a subclass of ribosomal DNA repeats silence ribosomal RNA genes in trans. Embo Rep 11(1):52–58. https://doi.org/10.1038/embor.2009.254 PubMed DOI
Savic N, Bar D, Leone S, Frommel SC, Weber FA, Vollenweider E, Ferrari E, Ziegler U, Kaech A, Shakhova O, Cinelli P, Santoro R (2014) lncRNA maturation to initiate heterochromatin formation in the nucleolus is required for exit from pluripotency in ESCs. Cell Stem Cell 15(6):720–734. https://doi.org/10.1016/j.stem.2014.10.005 PubMed DOI
Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Gene Dev 24(20):2264–2269. https://doi.org/10.1101/gad.590910 PubMed DOI PMC
Schroth GP, Ho PS (1995) Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA. Nucleic Acids Res 23(11):1977–1983. https://doi.org/10.1093/nar/23.11.1977 PubMed DOI PMC
Schroth GP, Chou PJ, Ho PS (1992) Mapping Z-DNA in the human genome - computer-aided mapping reveals a nonrandom distribution of potential Z-DNA-forming sequences in human genes. J Biol Chem 267(17):11846–11855 PubMed DOI
Schvartzman JB, Stasiak A (2004) A topological view of the replicon. Embo Rep 5(3):256–261. https://doi.org/10.1038/sj.embor.7400101 PubMed DOI PMC
Sengupta P, Bose D, Chatterjee S (2021) The molecular tete-a-tete between G-Quadruplexes and the i-motif in the human genome. ChemBioChem 22(9):1517–1537. https://doi.org/10.1002/cbic.202000703 PubMed DOI
Shaw PJ, McKeown PC (2011) The Structure of rDNA Chromatin. In: Olson MOJ (ed) The Nucleolus. Springer, New York, New York NY
Simonsson T, Pecinka P, Kubista M (1998) DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res 26(5):1167–1172. https://doi.org/10.1093/nar/26.5.1167 PubMed DOI PMC
Skourti-Stathaki K, Proudfoot NJ, Gromak N (2011) Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol Cell 42(6):794–805. https://doi.org/10.1016/j.molcel.2011.04.026 PubMed DOI PMC
Smirnov E, Chmurciakova N, Cmarko D (2021a) Human rDNA and cancer. Cells 10(12):3452. https://doi.org/10.3390/cells10123452 PubMed DOI PMC
Smirnov E, Chmurciakova N, Liska F, Bazantova P, Cmarko D (2021b) Variability of human rDNA. Cells 10(2):196. https://doi.org/10.3390/cells10020196 PubMed DOI PMC
Spiegel J, Cuesta SM, Adhikari S, Hansel-Hertsch R, Tannahill D, Balasubramanian S (2021) G-quadruplexes are transcription factor binding hubs in human chromatin. Genome Biol. https://doi.org/10.1186/s13059-021-02324-z PubMed DOI PMC
Stefanovsky VY, Bazett-Jones DP, Pelletier G, Moss T (1996) The DNA supercoiling architecture induced by the transcription factor xUBF requires three of its five HMG-boxes. Nucleic Acids Res 24(16):3208–3215. https://doi.org/10.1093/nar/24.16.3208 PubMed DOI PMC
Stefanovsky VY, Pelletier G, Bazett-Jones DP, Crane-Robinson C, Moss T (2001) DNA looping in the RNA polymerase I enhancesome is the result of non-cooperative in-phase bending by two UBF molecules. Nucleic Acids Res 29(15):3241–3247. https://doi.org/10.1093/nar/29.15.3241 PubMed DOI PMC
Stolz R, Sulthana S, Hartono SR, Malig M, Benham CJ, Chedin F (2019) Interplay between DNA sequence and negative superhelicity drives R-loop structures. P Natl Acad Sci USA 116(13):6260–6269. https://doi.org/10.1073/pnas.1819476116 DOI
Subramani VK, Ravichandran S, Bansal V, Kim KK (2019) Chemical-induced formation of BZ-junction with base extrusion. Biochem Bioph Res Co 508(4):1215–1220. https://doi.org/10.1016/j.bbrc.2018.12.045 DOI
Sun D, Hurley LH (2009) The importance of negative superhelicity in inducing the formation of G-quadruplex and i-Motif structures in the c-Myc promoter: implications for drug targeting and control of gene expression. J Med Chem 52(9):2863–2874. https://doi.org/10.1021/jm900055s PubMed DOI PMC
Sutherland C, Cui YX, Mao HB, Hurley LH (2016) A Mechanosensor mechanism controls the G-quadruplex/i-Motif molecular switch in the MYC promoter NHE III1. J Am Chem Soc 138(42):14138–14151. https://doi.org/10.1021/jacs.6b09196 PubMed DOI
Takahashi S, Brazier JA, Sugimoto N (2017) Topological impact of noncanonical DNA structures on Klenow fragment of DNA polymerase. P Natl Acad Sci USA 114(36):9605–9610. https://doi.org/10.1073/pnas.1704258114 DOI
Todd AK, Johnston M, Neidle S (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res 33(9):2901–2907. https://doi.org/10.1093/nar/gki553 PubMed DOI PMC
Trantirek L, Stefl R, Vorlickova M, Koca J, Sklenar V, Kypr J (2000) An A-type double helix of DNA having B-type puckering of the deoxyribose rings. J Mol Biol 297(4):907–922. https://doi.org/10.1006/jmbi.2000.3592 PubMed DOI
Travers A, Muskhelishvili G (2007) A common topology for bacterial and eukaryotic transcription initiation? Embo Rep 8(2):147–151. https://doi.org/10.1038/sj.embor.7400898 PubMed DOI PMC
Ussery DW (2002) DNA Structure: A, B and Z-DNA Helix Families. In: Wiley J (ed) Encyclopedia of life sciences. John Wiley & Sons. USA
van Holde K, Zlatanova J (1994) Unusual DNA structures, chromatin and transcription. BioEssays 16(1):59–68. https://doi.org/10.1002/bies.950160110 PubMed DOI
van Erp TS, Cuesta-Lopez S, Peyrard M (2006) Bubbles and denaturation in DNA. Eur Phys J E 20(4):421–434. https://doi.org/10.1140/epje/i2006-10032-2 PubMed DOI
Varizhuk A, Ischenko D, Tsvetkov V, Novikov R, Kulemin N, Kaluzhny D, Vlasenok M, Naumov V, Smirnov I, Pozmogova G (2017) The expanding repertoire of G4 DNA structures. Biochimie 135:54–62. https://doi.org/10.1016/j.biochi.2017.01.003 PubMed DOI
Varshney D, Spiegel J, Zyner K, Tannahill D, Balasubramanian S (2020) The regulation and functions of DNA and RNA G-quadruplexes. Nat Rev Mol Cell Biol 21(8):459–474. https://doi.org/10.1038/s41580-020-0236-x PubMed DOI PMC
von Hippel PH, Johnson NP, Marcus AH (2013) Fifty years of DNA “breathing”: Reflections on old and new approaches. Biopolymers 99(12):923–954. https://doi.org/10.1002/bip.22347 DOI
Vydzhak O, Luke B, Schindler N (2020) Non-coding RNAs at the Eukaryotic rDNA Locus: RNA-DNA Hybrids and Beyond. J Mol Biol 432(15):4287–4304. https://doi.org/10.1016/j.jmb.2020.05.011 PubMed DOI
Wahba L, Gore SK, Koshland D (2013) The homologous recombination machinery modulates the formation of RNA-DNA hybrids and associated chromosome instability. Elife. https://doi.org/10.7554/eLife.00505 PubMed DOI PMC
Wang GL, Vasquez KM (2004) Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. P Natl Acad Sci USA 101(37):13448–13453. https://doi.org/10.1073/pnas.0405116101 DOI
Wang GL, Vasquez KM (2023) Dynamic alternative DNA structures in biology and disease. Nat Rev Genet 24(4):211–234. https://doi.org/10.1038/s41576-022-00539-9 PubMed DOI
Wang AHJ, Quigley GJ, Kolpak FJ, Crawford JL, Vanboom JH, Vandermarel G, Rich A (1979) Molecular-structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282(5740):680–686. https://doi.org/10.1038/282680a0 PubMed DOI
Wang GL, Christensen LA, Vasquez KM (2006) Z-DNA-forming sequences generate large-scale deletions in mammalian cells. P Natl Acad Sci USA 103(8):2677–2682. https://doi.org/10.1073/pnas.0511084103 DOI
Wang ML, Bokros M, Theodoridis PR, Lee S (2019) Nucleolar Sequestration: remodeling nucleoli into amyloid bodies. Front Genet. https://doi.org/10.3389/fgene.2019.01179 PubMed DOI PMC
Waszkiewicz R, Ranasinghe M, Fogg JM, Catanese DJC, Ekiel-Jezewska ML, Lisicki M, Demeler B, Zechiedrich L, Szymczak P (2023) DNA supercoiling-induced shapes alter minicircle hydrodynamic properties. Nucleic Acids Res 51(8):4027–4042. https://doi.org/10.1093/nar/gkad183 PubMed DOI PMC
Whitley DC, Runfola V, Cary P, Nazlamova L, Guille M, Scarlett G (2014) APTE: identification of indirect read-out A-DNA promoter elements in genomes. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-15-288 PubMed DOI PMC
Widom J (1984) DNA bending and kinking. Nature 309(5966):312–313. https://doi.org/10.1038/309312a0 PubMed DOI
Wittig B, Wölfl S, Dorbic T, Vahrson W, Rich A (1992) Transcription of human c-myc in permeabilized nuclei is associated with formation of Z-DNA in three discrete regions of the gene. EMBO J 11(12):4653–4663. https://doi.org/10.1002/j.1460-2075.1992.tb05567.x PubMed DOI PMC
Wolfl S, Wittig B, Rich A (1995) Identification of transcriptionally induced Z-DNA segments in the human c-myc gene. Bba-Gene Struct Expr 1264(3):294–302. https://doi.org/10.1016/0167-4781(95)00155-7 DOI
Wolfl S, Martinez C, Rich A, Majzoub JA (1996) Transcription of the human corticotropin-releasing hormone gene in NPLC cells is correlated with Z-DNA formation. P Natl Acad Sci USA 93(8):3664–3668. https://doi.org/10.1073/pnas.93.8.3664 DOI
Wright EP, Huppert JL, Waller ZAE (2017) Identification of multiple genomic DNA sequences which form i-motif structures at neutral pH (vol 45, pg 2951, 2017). Nucleic Acids Res. https://doi.org/10.1093/nar/gkx1178 PubMed DOI PMC
Xu H, Di Antonio M, McKinney S, Mathew V, Ho B, O’Neil NJ, Dos Santos N, Silvester J, Wei V, Garcia J, Kabeer F, Lai D, Soriano P, Banath J, Chiu DS, Yap D, Le DD, Ye FB, Zhang AN, Thu K, Soong J, Lin SC, Tsai AHC, Osako T, Algara T, Saunders DN, Wong J, Xian J, Bally MB, Brenton JD, Brown GW, Shah SP, Cescon D, Mak TW, Caldas C, Stirling PC, Hieter P, Balasubramanian S, Aparicio S (2017) CX-5461 is a DNA G-quadruplex stabilizer with selective lethality in BRCA1/2 deficient tumours. Nat Commun. https://doi.org/10.1038/ncomms14432 PubMed DOI PMC
Yamamoto Y, Miura O, Ohyama T (2021) Cruciform formable sequences within Pou5f1 enhancer are indispensable for mouse ES cell integrity. Int J Mol Sci. https://doi.org/10.3390/ijms22073399 PubMed DOI PMC
Yu KF, Chedin F, Hsieh CL, Wilson TE, Lieber MR (2003) R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat Immunol 4(5):442–451. https://doi.org/10.1038/ni919 PubMed DOI
Yu F, Shen XY, Fan L, Yu ZC (2015) Analysis of histone modifications at human ribosomal DNA in liver cancer cell. Sci Rep-Uk. https://doi.org/10.1038/srep18100 DOI
Zentner GE, Saiakhova A, Manaenkov P, Adams MD, Scacheri PC (2011) Integrative genomic analysis of human ribosomal DNA. Nucleic Acids Res 39(12):4949–4960. https://doi.org/10.1093/nar/gkq1326 PubMed DOI PMC
Zeraati M, Langley DB, Schofield P, Moye AL, Rouet R, Hughes WE, Bryan TM, Dinger ME, Christ D (2018) I-motif DNA structures are formed in the nuclei of human cells. Nat Chem 10(6):631–637. https://doi.org/10.1038/s41557-018-0046-3 PubMed DOI
Zhang XO, Gingeras TR, Weng ZP (2019) Genome-wide analysis of polymerase III-transcribed Alu elements suggests cell-type-specific enhancer function. Genome Res 29(9):1402–1414. https://doi.org/10.1101/gr.249789.119 PubMed DOI PMC
Zhao ZL, Senturk N, Song CL, Grummt I (2018) lncRNA PAPAS tethered to the rDNA enhancer recruits hypophosphorylated CHD4/NuRD to repress rRNA synthesis at elevated temperatures. Gene Dev 32(11–12):836–848. https://doi.org/10.1101/gad.311688.118 PubMed DOI PMC
Zhou H, Wang YP, Wang Q, Li L, Hu Y, Wu YQ, Gautam M, Li LJ (2021) R-loops mediate transcription-associated formation of human rDNA secondary constrictions. J Cell Biochem 122(10):1517–1533. https://doi.org/10.1002/jcb.30074 PubMed DOI