The importance of unusual DNA structures in the regulation of basic cellular processes is an emerging field of research. Amongst local non-B DNA structures, G-quadruplexes (G4s) have gained in popularity during the last decade, and their presence and functional relevance at the DNA and RNA level has been demonstrated in a number of viral, bacterial, and eukaryotic genomes, including humans. Here, we performed the first systematic search of G4-forming sequences in all archaeal genomes available in the NCBI database. In this article, we investigate the presence and locations of G-quadruplex forming sequences using the G4Hunter algorithm. G-quadruplex-prone sequences were identified in all archaeal species, with highly significant differences in frequency, from 0.037 to 15.31 potential quadruplex sequences per kb. While G4 forming sequences were extremely abundant in Hadesarchaea archeon (strikingly, more than 50% of the Hadesarchaea archaeon isolate WYZ-LMO6 genome is a potential part of a G4-motif), they were very rare in the Parvarchaeota phylum. The presence of G-quadruplex forming sequences does not follow a random distribution with an over-representation in non-coding RNA, suggesting possible roles for ncRNA regulation. These data illustrate the unique and non-random localization of G-quadruplexes in Archaea.

Department of Biology and Ecology Institute of Environmental Technologies Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic

Faculty of Chemistry Brno University of Technology Purkyňova 464 118 612 00 Brno Czech Republic

Faculty of Mechanical Engineering Brno University of Technology Technicka 2896 2 616 69 Brno Czech Republic

Institut Curie CNRS UMR9187 INSERM U1196 Universite Paris Saclay 91400 Orsay France

Institut de Biologie Intégrative de la Cellule CNRS Université Paris Saclay CEDEX 91198 Gif sur Yvette France

Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 612 65 Brno Czech Republic

Laboratoire d'Optique et Biosciences Ecole Polytechnique CNRS INSERM Institut Polytechnique de Paris 91128 Palaiseau France

Mendel University in Brno Zemědělská 1 613 00 Brno Czech Republic

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Woese C.R., Fox G.E. Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc. Natl. Sci. Acad. USA. 1977;74:5088–5090. doi: 10.1073/pnas.74.11.5088. PubMed DOI PMC

Olsen G.J., Woese C.R. Archaeal genomics: An overview. Cell. 1997;89:991–994. doi: 10.1016/S0092-8674(00)80284-6. PubMed DOI

Forterre P. Archaea: What can we learn from their sequences? Curr. Opin. Genet. Dev. 1997;7:764–770. doi: 10.1016/S0959-437X(97)80038-X. PubMed DOI

Grüber G., Manimekalai M.S.S., Mayer F., Müller V. ATP synthases from archaea: The beauty of a molecular motor. Biochim. Biophys. Acta. 2014;1837:940–952. doi: 10.1016/j.bbabio.2014.03.004. PubMed DOI

Bolhuis A. The archaeal Sec-dependent protein translocation pathway. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2004;359:919–927. doi: 10.1098/rstb.2003.1461. PubMed DOI PMC

Samson R.Y., Dobro M.J., Jensen G.J., Bell S.D. The Structure, Function and Roles of the Archaeal ESCRT Apparatus. Subcell. Biochem. 2017;84:357–377. doi: 10.1007/978-3-319-53047-5_12. PubMed DOI

Spang A., Eme L., Saw J.H., Caceres E.F., Zaremba-Niedzwiedzka K., Lombard J., Guy L., Ettema T.J.G. Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet. 2018;14:e1007080. doi: 10.1371/journal.pgen.1007080. PubMed DOI PMC

Da Cunha V., Gaia M., Nasir A., Forterre P. Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genet. 2018;14:e1007215. doi: 10.1371/journal.pgen.1007215. PubMed DOI PMC

Adam P.S., Borrel G., Brochier-Armanet C., Gribaldo S. The growing tree of Archaea: New perspectives on their diversity, evolution and ecology. ISME J. 2017;11:2407. doi: 10.1038/ismej.2017.122. PubMed DOI PMC

Spang A., Caceres E.F., Ettema T.J.G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017;357 doi: 10.1126/science.aaf3883. PubMed DOI

Pennisi E. Survey of archaea in the body reveals other microbial guests. Science. 2017;358:983. doi: 10.1126/science.358.6366.983. PubMed DOI

Chaudhary P.P., Conway P.L., Schlundt J. Methanogens in humans: Potentially beneficial or harmful for health. Appl. Microbiol. Biotechnol. 2018;102:3095–3104. doi: 10.1007/s00253-018-8871-2. PubMed DOI

Vuillemin A., Wankel S.D., Coskun Ö.K., Magritsch T., Vargas S., Estes E.R., Spivack A.J., Smith D.C., Pockalny R., Murray R.W. Archaea dominate oxic subseafloor communities over multimillion-year time scales. Sci. Adv. 2019;5:eaaw4108. doi: 10.1126/sciadv.aaw4108. PubMed DOI PMC

Jain S., Caforio A., Driessen A.J.M. Biosynthesis of archaeal membrane ether lipids. Front. Microbiol. 2014;5:641. doi: 10.3389/fmicb.2014.00641. PubMed DOI PMC

Nobu M.K., Narihiro T., Kuroda K., Mei R., Liu W.-T. Chasing the elusive Euryarchaeota class WSA2: Genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J. 2016;10:2478–2487. doi: 10.1038/ismej.2016.33. PubMed DOI PMC

Aouad M., Borrel G., Brochier-Armanet C., Gribaldo S. Evolutionary placement of Methanonatronarchaeia. Nat. Microbiol. 2019;4:558–559. doi: 10.1038/s41564-019-0359-z. PubMed DOI

Forterre P. The universal tree of life: An update. Front. Microbiol. 2015;6 doi: 10.3389/fmicb.2015.00717. PubMed DOI PMC

Dombrowski N., Lee J.-H., Williams T.A., Offre P., Spang A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol. Lett. 2019;366:fnz008. doi: 10.1093/femsle/fnz008. PubMed DOI PMC

Gaia M., Forterre P. The Tree of Life. In: Rampelotto P.H., editor. Molecular Mechanisms of Microbial Evolution (Grand Challenges in Biology and Biotechnology) Springer; New York, NY, USA: 2018.

Sun Z.-Y., Wang X.-N., Cheng S.-Q., Su X.-X., Ou T.-M. Developing Novel G-Quadruplex Ligands: From Interaction with Nucleic Acids to Interfering with Nucleic Acid–Protein Interaction. Molecules. 2019;24:396. doi: 10.3390/molecules24030396. PubMed DOI PMC

Harkness R.W., Mittermaier A.K. G-quadruplex dynamics. BBA Proteins Proteomics. 2017;1865:1544–1554. doi: 10.1016/j.bbapap.2017.06.012. PubMed DOI

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;99:11593–11598. doi: 10.1073/pnas.182256799. PubMed DOI PMC

Lee S.C., Zhang J., Strom J., Yang D., Dinh T.N., Kappeler K., Chen Q.M. G-Quadruplex in the NRF2 mRNA 5′ Untranslated Region Regulates De Novo NRF2 Protein Translation under Oxidative Stress. Mol. Cell. Biol. 2016;37 doi: 10.1128/MCB.00122-16. PubMed DOI PMC

Crenshaw E., Leung B.P., Kwok C.K., Sharoni M., Olson K., Sebastian N.P., Ansaloni S., Schweitzer-Stenner R., Akins M.R., Bevilacqua P.C., et al. Amyloid Precursor Protein Translation is Regulated by a 3′UTR Guanine Quadruplex. PLoS ONE. 2015;10 doi: 10.1371/journal.pone.0143160. PubMed DOI PMC

Gage H.L., Merrick C.J. Conserved associations between G-quadruplex-forming DNA motifs and virulence gene families in malaria parasites. BMC Genomics. 2020;21:236. doi: 10.1186/s12864-020-6625-x. PubMed DOI PMC

Gazanion E., Lacroix L., Alberti P., Gurung P., Wein S., Cheng M., Mergny J., Gomes A., Lopez-Rubio J. Genome wide distribution of G-quadruplexes and their impact on gene expression in malaria parasites. PLoS Genetics. 2020 doi: 10.1371/journal.pgen.1008917. PubMed DOI PMC

Cahoon L.A., Seifert H.S. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science. 2009;325:764–767. doi: 10.1126/science.1175653. PubMed DOI PMC

Thakur R.S., Desingu A., Basavaraju S., Subramanya S., Rao D.N., Nagaraju G. Mycobacterium tuberculosis DinG is a structure-specific helicase that unwinds G4 DNA implications for targeting g4 dna as a novel therapeutic approach. J. Biol. 2014;289:25112–25136. PubMed PMC

Mishra S.K., Shankar U., Jain N., Sikri K., Tyagi J.S., Sharma T.K., Mergny J.-L., Kumar A. Characterization of G-Quadruplex Motifs in espB, espK, and cyp51 Genes of Mycobacterium tuberculosis as Potential Drug Targets. Mol. Ther. Nucleic. Acids. 2019;16:698–706. doi: 10.1016/j.omtn.2019.04.022. PubMed DOI PMC

Brazda V., Haronikova L., Liao J.C., Fojta M. DNA and RNA Quadruplex-Binding Proteins. Int. J. Mol. Sci. 2014;15:17493–17517. doi: 10.3390/ijms151017493. PubMed DOI PMC

Brázda V., Červeň J., Bartas M., Mikysková N., Coufal J., Pečinka P. The Amino Acid Composition of Quadruplex Binding Proteins Reveals a Shared Motif and Predicts New Potential Quadruplex Interactors. Molecules. 2018;23:2341. doi: 10.3390/molecules23092341. PubMed DOI PMC

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:e1000475. doi: 10.1371/journal.pgen.1000475. PubMed DOI PMC

Bartas M., Čutová M., Brázda V., Kaura P., Šťastný J., Kolomazník J., Coufal J., Goswami P., Červeň J., Pečinka P. The Presence and Localization of G-Quadruplex Forming Sequences in the Domain of Bacteria. Molecules. 2019;24:1711. doi: 10.3390/molecules24091711. PubMed DOI PMC

Marguet E., Forterre P. DNA stability at temperatures typical for hyperthermophiles. Nucleic Acids Res. 1994;22:1681–1686. doi: 10.1093/nar/22.9.1681. PubMed DOI PMC

Ding Y., Fleming A.M., Burrows C.J. Case studies on potential G-quadruplex-forming sequences from the bacterial orders Deinococcales and Thermales derived from a survey of published genomes. Sci. Rep. 2018 doi: 10.1038/s41598-018-33944-4. PubMed DOI PMC

Kota S., Dhamodharan V., Pradeepkumar P.I., Misra H.S. G-quadruplex forming structural motifs in the genome of Deinococcus radiodurans and their regulatory roles in promoter functions. Appl. Microbiol. Biotechnol. 2015;99:9761–9769. doi: 10.1007/s00253-015-6808-6. PubMed DOI

Mishra S., Chaudhary R., Singh S., Kota S., Misra H.S. Guanine Quadruplex DNA Regulates Gamma Radiation Response of Genome Functions in the Radioresistant Bacterium Deinococcus radiodurans. J. Bacteriol. 2019;201 doi: 10.1128/JB.00154-19. PubMed DOI PMC

Todd A.K., Johnston M., Neidle S. Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res. 2005;33:2901–2907. doi: 10.1093/nar/gki553. PubMed DOI PMC

Huppert J.L., Balasubramanian S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res. 2005;33:2908–2916. doi: 10.1093/nar/gki609. PubMed DOI PMC

Eddy J., Maizels N. Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res. 2006;34:3887–3896. doi: 10.1093/nar/gkl529. PubMed DOI PMC

Bedrat A., Lacroix L., Mergny J.L. Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016 doi: 10.1093/nar/gkw006. PubMed DOI PMC

Brázda V., Kolomazník J., Lýsek J., Bartas M., Fojta M., Šťastný J., Mergny J.-L. G4Hunter web application: A web server for G-quadruplex prediction. Bioinformatics. 2019;35:3493–3495. doi: 10.1093/bioinformatics/btz087. PubMed DOI PMC

Finan T.M. The divided bacterial genome: Structure, function, and evolution. Microbiol. Mol. Biol. Rev. 2017;81:e00019-17. PubMed PMC

Yadav V.K., Abraham J.K., Mani P., Kulshrestha R., Chowdhury S. QuadBase: Genome-wide database of G4 DNA-occurrence and conservation in human, chimpanzee, mouse and rat promoters and 146 microbes. Nucleic Acids Res. 2008;36:D381–D385. doi: 10.1093/nar/gkm781. PubMed DOI PMC

Waller Z.A., Pinchbeck B.J., Buguth B.S., Meadows T.G., Richardson D.J., Gates A.J. Control of bacterial nitrate assimilation by stabilization of G-quadruplex DNA. Chem. Commun. 2016;52:13511–13514. doi: 10.1039/C6CC06057A. PubMed DOI PMC

Rawal P., Kummarasetti V.B.R., 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;16:644–655. doi: 10.1101/gr.4508806. PubMed DOI PMC

Brázda V., Lýsek J., Bartas M., Fojta M. Complex Analyses of Short Inverted Repeats in All Sequenced Chloroplast DNAs. BioMed Res. Int. 2018;2018:1097018. doi: 10.1155/2018/1097018. PubMed DOI PMC

Čechová J., Lýsek J., Bartas M., Brázda V. Complex analyses of inverted repeats in mitochondrial genomes revealed their importance and variability. Bioinformatics. 2018;34:1081–1085. doi: 10.1093/bioinformatics/btx729. PubMed DOI PMC

Cahoon L.A., Seifert H.S. Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae. PLoS Pathog. 2013;9:e1003074. doi: 10.1371/journal.ppat.1003074. PubMed DOI PMC

Neidle S. The structures of quadruplex nucleic acids and their drug complexes. Curr. Opin. Struct. Biol. 2009;19:239–250. doi: 10.1016/j.sbi.2009.04.001. PubMed DOI

Dhapola P., Chowdhury S. QuadBase2: Web server for multiplexed guanine quadruplex mining and visualization. Nucleic Acids Res. 2016;44:W277–W283. doi: 10.1093/nar/gkw425. PubMed DOI PMC

Sayers E.W., Agarwala R., Bolton E.E., Brister J.R., Canese K., Clark K., Connor R., Fiorini N., Funk K., Hefferon T., et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2019;47:D23–D28. doi: 10.1093/nar/gky1069. PubMed DOI PMC

Brázda V., Kolomazník J., Lỳsek J., Hároníková L., Coufal J., Št’astnỳ J. Palindrome analyser—A new web-based server for predicting and evaluating inverted repeats in nucleotide sequences. Biochem. Biophys. Res. Commun. 2016;478:1739–1745. doi: 10.1016/j.bbrc.2016.09.015. PubMed DOI

Computational Tools—Pandas 0.25.1 Documentation. [(accessed on 16 October 2019)]; Available online: https://pandas.pydata.org/pandas-docs/stable/user_guide/computation.html.

Suzuki R., Shimodaira H. Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006;22:1540–1542. doi: 10.1093/bioinformatics/btl117. PubMed DOI

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Grant C.E., Bailey T.L., Noble W.S. FIMO: Scanning for occurrences of a given motif. Bioinformatics. 2011;27:1017–1018. doi: 10.1093/bioinformatics/btr064. PubMed DOI PMC

Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J., Li W.W., Noble W.S. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–W208. doi: 10.1093/nar/gkp335. PubMed DOI PMC

Gertz E.M., Yu Y.-K., Agarwala R., Schäffer A.A., Altschul S.F. Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST. BMC Biol. 2006;4:41. doi: 10.1186/1741-7007-4-41. PubMed DOI PMC

Wernersson R. Virtual Ribosome—A comprehensive DNA translation tool with support for integration of sequence feature annotation. Nucleic Acids Res. 2006;34:W385–W388. doi: 10.1093/nar/gkl252. PubMed DOI PMC

Artimo P., Jonnalagedda M., Arnold K., Baratin D., Csardi G., De Castro E., Duvaud S., Flegel V., Fortier A., Gasteiger E. ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 2012;40:W597–W603. doi: 10.1093/nar/gks400. PubMed DOI PMC

Marchler-Bauer A., Derbyshire M.K., Gonzales N.R., Lu S., Chitsaz F., Geer L.Y., Geer R.C., He J., Gwadz M., Hurwitz D.I., et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–D226. doi: 10.1093/nar/gku1221. PubMed DOI PMC

Čutová M., Manta J., Porubiaková O., Kaura P., Šťastný J., Jagelská E.B., Goswami P., Bartas M., Brázda V. Divergent distributions of inverted repeats and G-quadruplex forming sequences in Saccharomyces cerevisiae. Genomics. 2020;112:1897–1901. doi: 10.1016/j.ygeno.2019.11.002. PubMed DOI

Guo J.U., Bartel D.P. RNA G-quadruplexes are globally unfolded in eukaryotic cells and depleted in bacteria. Science. 2016;353 doi: 10.1126/science.aaf5371. PubMed DOI PMC

Galtier N., Tourasse N., Gouy M. A nonhyperthermophilic common ancestor to extant life forms. Science. 1999;283:220–221. doi: 10.1126/science.283.5399.220. PubMed DOI

Klein R.J., Misulovin Z., Eddy S.R. Noncoding RNA genes identified in AT-rich hyperthermophiles. Proc. Natl. Sci. Acad. USA. 2002;99:7542–7547. doi: 10.1073/pnas.112063799. PubMed DOI PMC

Lyons S.M., Gudanis D., Coyne S.M., Gdaniec Z., Ivanov P. Identification of functional tetramolecular RNA G-quadruplexes derived from transfer RNAs. Nat. Commun. 2017;8:1127. doi: 10.1038/s41467-017-01278-w. PubMed DOI PMC

Gebetsberger J., Zywicki M., Künzi A., Polacek N. tRNA-derived fragments target the ribosome and function as regulatory non-coding RNA in Haloferax volcanii. Archaea. 2012;2012:260909. doi: 10.1155/2012/260909. PubMed DOI PMC

Magnus M., Kappel K., Das R., Bujnicki J.M. RNA 3D structure prediction guided by independent folding of homologous sequences. BMC Bioinf. 2019;20:512. doi: 10.1186/s12859-019-3120-y. PubMed DOI PMC

Kamura T., Katsuda Y., Kitamura Y., Ihara T. G-quadruplexes in mRNA: A key structure for biological function. Biochem. Biophys. Res. Commun. 2020 doi: 10.1016/j.bbrc.2020.02.168. PubMed DOI

Qu Z., Adelson D.L. Evolutionary conservation and functional roles of ncRNA. Front. Genet. 2012;3 doi: 10.3389/fgene.2012.00205. PubMed DOI PMC

Buddeweg A., Daume M., Randau L., Schmitz R.A. Noncoding RNAs in Archaea: Genome-Wide Identification and Functional Classification. Meth. Enzymol. 2018;612:413–442. doi: 10.1016/bs.mie.2018.08.003. PubMed DOI

Luo H., Gao F. DoriC 10.0: An updated database of replication origins in prokaryotic genomes including chromosomes and plasmids. Nucleic Acids Res. 2019;47:D74–D77. doi: 10.1093/nar/gky1014. PubMed DOI PMC

Cossu M., Da Cunha V., Toffano-Nioche C., Forterre P., Oberto J. Comparative genomics reveals conserved positioning of essential genomic clusters in highly rearranged Thermococcales chromosomes. Biochimie. 2015;118:313–321. doi: 10.1016/j.biochi.2015.07.008. PubMed DOI PMC

Matsunaga F., Forterre P., Ishino Y., Myllykallio H. In vivo interactions of archaeal Cdc6/Orc1 and minichromosome maintenance proteins with the replication origin. Proc. Natl. Acad. Sci. USA. 2001;98:11152–11157. doi: 10.1073/pnas.191387498. PubMed DOI PMC

Dueber E.C., Costa A., Corn J.E., Bell S.D., Berger J.M. Molecular determinants of origin discrimination by Orc1 initiators in archaea. Nucleic Acids Res. 2011;39:3621–3631. doi: 10.1093/nar/gkq1308. PubMed DOI PMC

Norais C., Hawkins M., Hartman A.L., Eisen J.A., Myllykallio H., Allers T. Genetic and physical mapping of DNA replication origins in Haloferax volcanii. PLoS Genet. 2007;3:e77. doi: 10.1371/journal.pgen.0030077. PubMed DOI PMC

Wu Z., Liu J., Yang H., Liu H., Xiang H. Multiple replication origins with diverse control mechanisms in Haloarcula hispanica. Nucleic Acids Res. 2013;42:2282–2294. doi: 10.1093/nar/gkt1214. PubMed DOI PMC

Zhuang X., Tang J., Hao Y., Tan Z. Fast detection of quadruplex structure in DNA by the intrinsic fluorescence of a single-stranded DNA binding protein. J. Mol. Recognit. 2007;20:386–391. doi: 10.1002/jmr.847. PubMed DOI

Mendoza O., Bourdoncle A., Boulé J.-B., Brosh R.M., Mergny J.-L. G-quadruplexes and helicases. Nucleic Acids Res. 2016;44:1989–2006. doi: 10.1093/nar/gkw079. PubMed DOI PMC

Beaume N., Pathak R., Yadav V.K., Kota S., Misra H.S., Gautam H.K., Chowdhury S. Genome-wide study predicts promoter-G4 DNA motifs regulate selective functions in bacteria: Radioresistance of D. radiodurans involves G4 DNA-mediated regulation. Nucleic Acids Res. 2013;41:76–89. doi: 10.1093/nar/gks1071. PubMed DOI PMC

Gehring K., Leroy J.-L., Guéron M. A tetrameric DNA structure with protonated cytosine-cytosine base pairs. Nature. 1993;363:561–565. doi: 10.1038/363561a0. PubMed DOI

Barrett T., Clark K., Gevorgyan R., Gorelenkov V., Gribov E., Karsch-Mizrachi I., Kimelman M., Pruitt K.D., Resenchuk S., Tatusova T., et al. BioProject and BioSample databases at NCBI: Facilitating capture and organization of metadata. Nucleic Acids Res. 2012;40:D57–D63. doi: 10.1093/nar/gkr1163. PubMed DOI PMC

Bartas M., Brázda V., Karlický V., Červeň J., Pečinka P. Bioinformatics analyses and in vitro evidence for five and six stacked G-quadruplex forming sequences. Biochimie. 2018;150:70–75. doi: 10.1016/j.biochi.2018.05.002. PubMed DOI

Risitano A., Fox K.R. Stability of Intramolecular DNA Quadruplexes: Comparison with DNA Duplexes. Biochemistry. 2003;42:6507–6513. doi: 10.1021/bi026997v. PubMed DOI

Couturier M., Gadelle D., Forterre P., Nadal M., Garnier F. The reverse gyrase TopR1 is responsible for the homeostatic control of DNA supercoiling in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol. Microbiol. 2020;113:356–368. doi: 10.1111/mmi.14424. PubMed DOI

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;33:877. doi: 10.1038/nbt.3295. PubMed DOI

Hänsel-Hertsch R., Spiegel J., Marsico G., Tannahill D., Balasubramanian S. Genome-wide mapping of endogenous G-quadruplex DNA structures by chromatin immunoprecipitation and high-throughput sequencing. Nat. Protoc. 2018;13:551. doi: 10.1038/nprot.2017.150. PubMed DOI

Hänsel-Hertsch R., Di Antonio M., Balasubramanian S. DNA G-quadruplexes in the human genome: Detection, functions and therapeutic potential. Nat. Rev. Mol. Cell. Biol. 2017;18:279. doi: 10.1038/nrm.2017.3. PubMed DOI

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