G-quadruplex propensity in H. neanderthalensis, H. sapiens and Denisovans mitochondrial genomes
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
38817800
PubMed Central
PMC11137754
DOI
10.1093/nargab/lqae060
PII: lqae060
Knihovny.cz E-zdroje
- Publikační typ
- časopisecké články MeSH
Current methods of processing archaeological samples combined with advances in sequencing methods lead to disclosure of a large part of H. neanderthalensis and Denisovans genetic information. It is hardly surprising that the genome variability between modern humans, Denisovans and H. neanderthalensis is relatively limited. Genomic studies may provide insight on the metabolism of extinct human species or lineages. Detailed analysis of G-quadruplex sequences in H. neanderthalensis and Denisovans mitochondrial DNA showed us interesting features. Relatively similar patterns in mitochondrial DNA are found compared to modern humans, with one notable exception for H. neanderthalensis. An interesting difference between H. neanderthalensis and H. sapiens corresponds to a motif found in the D-loop region of mtDNA, which is responsible for mitochondrial DNA replication. This area is directly responsible for the number of mitochondria and consequently for the efficient energy metabolism of cell. H. neanderthalensis harbor a long uninterrupted run of guanines in this region, which may cause problems for replication, in contrast with H. sapiens, for which this run is generally shorter and interrupted. One may propose that the predominant H. sapiens motif provided a selective advantage for modern humans regarding mtDNA replication and function.
Zobrazit více v PubMed
Harvati K., Gunz P., Grigorescu D. Cioclovina (Romania): affinities of an early modern European. J. Hum. Evol. 2007; 53:732–746. PubMed
Soficaru A., Doboş A., Trinkaus E. Early modern humans from the Peştera Muierii, Baia de Fier, Romania. Proc. Natl. Acad. Sci. USA. 2006; 103:17196–17201. PubMed PMC
Prüfer K., de Filippo C., Grote S., Mafessoni F., Korlević P., Hajdinjak M., Vernot B., Skov L., Hsieh P., Peyrégne S. et al. . A high-coverage Neandertal genome from Vindija Cave in Croatia. Science. 2017; 358:655–658. PubMed PMC
Prüfer K., Racimo F., Patterson N., Jay F., Sankararaman S., Sawyer S., Heinze A., Renaud G., Sudmant P.H., de Filippo C. et al. . The complete genome sequence of a Neanderthal from the Altai Mountains. Nature. 2014; 505:43–49. PubMed PMC
Green R.E., Malaspinas A.-S., Krause J., Briggs A.W., Johnson P.L.F., Uhler C., Meyer M., Good J.M., Maricic T., Stenzel U. et al. . A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell. 2008; 134:416–426. PubMed PMC
Serre D., Langaney A., Chech M., Teschler-Nicola M., Paunovic M., Mennecier P., Hofreiter M., Possnert G., Pääbo S. No evidence of Neandertal mtDNA contribution to early modern humans. PLoS Biol. 2004; 2:e57. PubMed PMC
Briggs A.W., Good J.M., Green R.E., Krause J., Maricic T., Stenzel U., Lalueza-Fox C., Rudan P., Brajković D., Kućan Ž. et al. . Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science. 2009; 325:318–321. PubMed
Mafessoni F., Grote S., De Filippo C., Slon V., Kolobova K.A., Viola B., Markin S.V., Chintalapati M., Peyrégne S., Skov L. et al. . A high-coverage Neandertal genome from Chagyrskaya Cave. Proc. Natl. Acad. Sci. USA. 2020; 117:15132–15136. PubMed PMC
Hajdinjak M., Fu Q., Hübner A., Petr M., Mafessoni F., Grote S., Skoglund P., Narasimham V., Rougier H., Crevecoeur I. et al. . Reconstructing the genetic history of late Neanderthals. Nature. 2018; 555:652–656. PubMed PMC
Wall J.D., Yang M.A., Jay F., Kim S.K., Durand E.Y., Stevison L.S., Gignoux C., Woerner A., Hammer M.F., Slatkin M. Higher levels of Neanderthal ancestry in East Asians than in Europeans. Genetics. 2013; 194:199–209. PubMed PMC
Sankararaman S., Mallick S., Dannemann M., Prüfer K., Kelso J., Pääbo S., Patterson N., Reich D. The genomic landscape of Neanderthal ancestry in present-day humans. Nature. 2014; 507:354–357. PubMed PMC
Reich D., Green R.E., Kircher M., Krause J., Patterson N., Durand E.Y., Viola B., Briggs A.W., Stenzel U., Johnson P.L.F. et al. . Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature. 2010; 468:1053–1060. PubMed PMC
Fu Q., Li H., Moorjani P., Jay F., Slepchenko S.M., Bondarev A.A., Johnson P.L.F., Aximu-Petri A., Prüfer K., De Filippo C. et al. . Genome sequence of a 45,000-year-old modern human from western Siberia. Nature. 2014; 514:445–449. PubMed PMC
Reilly P.F., Tjahjadi A., Miller S.L., Akey J.M., Tucci S. The contribution of Neanderthal introgression to modern human traits. Curr. Biol. 2022; 32:R970–R983. PubMed PMC
Deschamps M., Laval G., Fagny M., Itan Y., Abel L., Casanova J.-L., Patin E., Quintana-Murci L. Genomic signatures of selective pressures and introgression from archaic hominins at human innate immunity genes. Am. Hum. Genet. 2016; 98:5–21. PubMed PMC
Enard D., Petrov D.A. Evidence that RNA viruses drove adaptive introgression between Neanderthals and modern humans. Cell. 2018; 175:360–371. PubMed PMC
Zhang X., Witt K.E., Bañuelos M.M., Ko A., Yuan K., Xu S., Nielsen R., Huerta-Sanchez E. The history and evolution of the Denisovan- EPAS1 haplotype in Tibetans. Proc. Natl. Acad. Sci. U.S.A. 2021; 118:e2020803118. PubMed PMC
International Human Genome Sequencing Consortium, Whitehead Institute for Biomedical Research, Center for Genome Research Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K. et al. . Initial sequencing and analysis of the human genome. Nature. 2001; 409:860–921. PubMed
Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A. et al. . The sequence of the human genome. Science. 2001; 291:1304–1351. PubMed
Nurk S., Koren S., Rhie A., Rautiainen M., Bzikadze A.V., Mikheenko A., Vollger M.R., Altemose N., Uralsky L., Gershman A. et al. . The complete sequence of a human genome. Science. 2022; 376:44–53. PubMed PMC
Kerner G., Patin E., Quintana-Murci L. New insights into human immunity from ancient genomics. Curr. Opin. Immunol. 2021; 72:116–125. PubMed PMC
Mergny J.-L., Sen D. DNA quadruple helices in nanotechnology. Chem. Rev. 2019; 119:6290–6325. PubMed
Wong A., Wu G. Selective binding of monovalent cations to the stacking G-quartet structure formed by guanosine 5‘-monophosphate: a solid-state NMR study. J. Am. Chem. Soc. 2003; 125:13895–13905. PubMed
Harkness R.W., Mittermaier A.K. G-quadruplex dynamics. Biochim. Biophys. Acta (BBA) - Proteins Proteomics. 2017; 1865:1544–1554. PubMed
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. PubMed PMC
Bohálová N., Mergny J.-L., Brázda V. Novel G-quadruplex prone sequences emerge in the complete assembly of the human X chromosome. Biochimie. 2021; 191:87–90. PubMed
Brázda V., Luo Y., Bartas M., Kaura P., Porubiaková O., Šťastný J., Pečinka P., Verga D., Da Cunha V., Takahashi T.S. et al. . G-quadruplexes in the archaea domain. Biomolecules. 2020; 10:1349. PubMed PMC
Chashchina G.V., Shchyolkina A.K., Kolosov S.V., Beniaminov A.D., Kaluzhny D.N. Recurrent potential G-quadruplex sequences in archaeal genomes. Front. Microbiol. 2021; 12:647851. PubMed PMC
Cueny R.R., McMillan S.D., Keck J.L. G-quadruplexes in bacteria: insights into the regulatory roles and interacting proteins of non-canonical nucleic acid structures. Crit. Rev. Biochem. Mol. Biol. 2022; 57:539–561. PubMed PMC
Dobrovolná M., Bohálová N., Peška V., Wang J., Luo Y., Bartas M., Volná A., Mergny J.-L., Brázda V. The newly sequenced genome of Pisum sativum is replete with potential G-quadruplex-forming sequences—implications for evolution and biological regulation. Int. J. Mol. Sci. 2022; 23:8482. PubMed PMC
Griffin B.D., Bass H.W. Plant G-quadruplex (G4) motifs in DNA and RNA; abundant, intriguing sequences of unknown function. Plant Sci. 2018; 269:143–147. PubMed
Huppert J.L. Prevalence of quadruplexes in the human genome. Nucleic Acids Res. 2005; 33:2908–2916. PubMed PMC
Zhang Z.-H., Qian S.H., Wei D., Chen Z.-X. In vivo dynamics and regulation of DNA G-quadruplex structures in mammals. Cell Biosci. 2023; 13:117. PubMed PMC
Rhodes D., Lipps H.J. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 2015; 43:8627–8637. PubMed PMC
Galli S., Melidis L., Flynn S.M., Varshney D., Simeone A., Spiegel J., Madden S.K., Tannahill D., Balasubramanian S. DNA G-quadruplex recognition in vitro and in live cells by a structure-specific manobody. J. Am. Chem. Soc. 2022; 144:23096–23103. PubMed PMC
Jansson L.I., Hentschel J., Parks J.W., Chang T.R., Lu C., Baral R., Bagshaw C.R., Stone M.D. Telomere DNA G-quadruplex folding within actively extending human telomerase. Proc. Natl. Acad. Sci. U.S.A. 2019; 116:9350–9359. PubMed PMC
Raguseo F., Chowdhury S., Minard A., Di Antonio M. Chemical-biology approaches to probe DNA and RNA G-quadruplex structures in the genome. Chem. Commun. 2020; 56:1317–1324. PubMed
Brázda V., Bohálová N., Bowater R.P. New telomere to telomere assembly of human chromosome 8 reveals a previous underestimation of G-quadruplex forming sequences and inverted repeats. Gene. 2022; 810:146058. PubMed
Kang Y., Wei C. A stilbene derivative as dual-channel fluorescent probe for mitochondrial G-quadruplex DNA in living cells. Spectrochim. Acta Part A. 2022; 278:121316. PubMed
Varshney D., Spiegel J., Zyner K., Tannahill D., Balasubramanian S. The regulation and functions of DNA and RNA G-quadruplexes. Nat. Rev. Mol. Cell Biol. 2020; 21:459–474. PubMed PMC
Bedrat A., Lacroix L., Mergny J.-L. Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016; 44:1746–1759. PubMed PMC
Doimo M., Chaudhari N., Abrahamsson S., L’Hôte V., Nguyen T.V.H., Berner A., Ndi M., Abrahamsson A., Das R.N., Aasumets K. et al. . Enhanced mitochondrial G-quadruplex formation impedes replication fork progression leading to mtDNA loss in human cells. Nucleic Acids Res. 2023; 51:7392–7408. PubMed PMC
Bohálová N., Dobrovolná M., Brázda V., Bidula S. Conservation and over-representation of G-quadruplex sequences in regulatory regions of mitochondrial DNA across distinct taxonomic sub-groups. Biochimie. 2022; 194:28–34. PubMed
Cavalcante G.C., Magalhães L., Ribeiro-dos-Santos Â., Vidal A.F. Mitochondrial epigenetics: non-coding RNAs as a novel layer of complexity. Int. J. Mol. Sci. 2020; 21:1838. PubMed PMC
Liu C.-C., Fang T.-J., Ou T.-T., Wu C.-C., Li R.-N., Lin Y.-C., Lin C.-H., Tsai W.-C., Liu H.-W., Yen J.-H. Global DNA methylation, DNMT1, and MBD2 in patients with rheumatoid arthritis. Immunol. Lett. 2011; 135:96–99. PubMed
Guo X., Jing C., Li L., Zhang L., Shi Y., Wang J., Liu J., Li C. Down-regulation of VEZT gene expression in human gastric cancer involves promoter methylation and miR-43c. Biochem. Biophys. Res. Commun. 2011; 404:622–627. PubMed
Zhang J., Zhang J., Lai R., Peng C., Guo Z., Wang C. Risk-associated single nucleotide polymorphisms of mitochondrial D-loop mediate imbalance of cytokines and redox in rheumatoid arthritis. Int. J of Rheum. Dis. 2023; 26:124–131. PubMed
Zhao Y., Peng C., Lai R., Zhang J., Zhang X., Guo Z. The SNPs of mitochondrial DNA displacement loop region and mitochondrial DNA copy number associated with risk of polymyositis and dermatomyositis. Sci. Rep. 2022; 12:5903. PubMed PMC
Zhao Y., Peng C., Zhang J., Lai R., Zhang X., Guo Z. Mitochondrial displacement loop region SNPs modify Sjögren's syndrome development by regulating cytokines expression in female patients. Front. Genet. 2022; 13:847521. PubMed PMC
Mposhi A., Liang L., Mennega K.P., Yildiz D., Kampert C., Hof I.H., Jellema P.G., De Koning T.J., Faber K.N., Ruiters M.H.J. et al. . The mitochondrial epigenome: an unexplored avenue to explain unexplained myopathies?. Int. J. Mol. Sci. 2022; 23:2197. PubMed PMC
Lai R., Zhang X., Qiao K., Gao X., Li S., Zhang R., Qi Y., Peng C. Identification of sequence polymorphisms in the mitochondrial deoxyribonucleic acid displacement-loop region as risk factors for systemic lupus erythematosus. Arch. Rheumatol. 2021; 36:375–380. PubMed PMC
Stoccoro A., Smith A.R., Baldacci F., Del Gamba C., Lo Gerfo A., Ceravolo R., Lunnon K., Migliore L., Coppedè F. Mitochondrial D-loop region methylation and copy number in peripheral blood DNA of Parkinson's disease patients. Genes. 2021; 12:720. PubMed PMC
Yang H. Correlation between increased ND2 expression and demethylated displacement loop of mtDNA in colorectal cancer. Mol. Med. Rep. 2012; 6:125–130. PubMed
Nicholls T.J., Minczuk M. In D-loop: 40years of mitochondrial 7S DNA. Exp. Gerontol. 2014; 56:175–181. PubMed
Esnault C., Magat T., Zine El Aabidine A., Garcia-Oliver E., Cucchiarini A., Bouchouika S., Lleres D., Goerke L., Luo Y., Verga D. et al. . G4access identifies G-quadruplexes and their associations with open chromatin and imprinting control regions. Nat. Genet. 2023; 55:1359–1369. PubMed
Okonechnikov K., Golosova O., Fursov M.the UGENE team Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012; 28:1166–1167. PubMed
Crooks G.E., Hon G., Chandonia J.-M., Brenner S.E. WebLogo: a sequence logo generator: Figure 1. Genome Res. 2004; 14:1188–1190. PubMed PMC
Luo Y., Granzhan A., Marquevielle J., Cucchiarini A., Lacroix L., Amrane S., Verga D., Mergny J.-L. Guidelines for G-quadruplexes: I. In vitro characterization. Biochimie. 2022; 214:5–23. PubMed
Renaud De La Faverie A., Guédin A., Bedrat A., Yatsunyk L.A., Mergny J.-L Thioflavin T as a fluorescence light-up probe for G4 formation. Nucleic Acids Res. 2014; 42:e65. PubMed PMC
Zhang Z., Schwartz S., Wagner L., Miller W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 2000; 7:203–214. PubMed
Sengar A., Heddi B., Phan A.T. Formation of G-quadruplexes in poly-G sequences: structure of a propeller-type parallel-stranded G-quadruplex formed by a G 15 stretch. Biochemistry. 2014; 53:7718–7723. PubMed
Behar D.M., van Oven M., Rosset S., Metspalu M., Loogväli E.-L., Silva N.M., Kivisild T., Torroni A., Villems R. A “Copernican” reassessment of the human mitochondrial DNA tree from its root. Am. Hum. Genet. 2012; 90:675–684. PubMed PMC
Luo Y., Granzhan A., Verga D., Mergny J. FRET-MC: a fluorescence melting competition assay for studying G4 structures in vitro. Biopolymers. 2021; 112:e23415. PubMed
Mergny J.-L. Thermal difference spectra: a specific signature for nucleic acid structures. Nucleic Acids Res. 2005; 33:e138. PubMed PMC
Chu I.-T., Wu C.-C., Chang T.-C. G-quadruplex formation by single-base mutation or deletion of mitochondrial DNA sequences. Biochim. Biophys. Acta. 2019; 1863:418–425. PubMed
Sahayasheela V.J., Yu Z., Hidaka T., Pandian G.N., Sugiyama H. Mitochondria and G-quadruplex evolution: an intertwined relationship. Trends Genet. 2023; 39:15–30. PubMed PMC
Butler T.J., Estep K.N., Sommers J.A., Maul R.W., Moore A.Z., Bandinelli S., Cucca F., Tuke M.A., Wood A.R., Bharti S.K. et al. . Mitochondrial genetic variation is enriched in G-quadruplex regions that stall DNA synthesis in vitro. Hum. Mol. Genet. 2020; 29:1292–1309. PubMed PMC
Bharti S.K., Sommers J.A., Zhou J., Kaplan D.L., Spelbrink J.N., Mergny J.-L., Brosh R.M. 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; 289:29975–29993. PubMed PMC
Sullivan E.D., Longley M.J., Copeland W.C. Polymerase γ efficiently replicates through many natural template barriers but stalls at the HSP1 quadruplex. J. Biol. Chem. 2020; 295:17802–17815. PubMed PMC
Falabella M., Kolesar J.E., Wallace C., De Jesus D., Sun L., Taguchi Y.V., Wang C., Wang T., Xiang I.M., Alder J.K. et al. . G-quadruplex dynamics contribute to regulation of mitochondrial gene expression. Sci. Rep. 2019; 9:5605. PubMed PMC
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; 40:10334–10344. PubMed PMC
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. U.S.A. 2010; 107:16072–16077. PubMed PMC
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. et al. . Direct evidence of mitochondrial G-quadruplex DNA by using fluorescent anti-cancer agents. Nucleic Acids Res. 2015; 43:10102–10113. PubMed PMC
Falabella M., Fernandez R.J., Johnson F.B., Kaufman B.A. Potential roles for G-quadruplexes in mitochondria. CMC. 2019; 26:2918–2932. PubMed PMC
Liou C.-W., Lin T.-K., Huang F.-M., Chen T.-L., Lee C.-F., Chuang Y.-C., Tan T.-Y., Chang K.-C., Wei Y.-H. Association of the mitochondrial DNA 16189 T to C variant with lacunar cerebral infarction: evidence from a hospital-based case-control study. Ann. N. Y. Acad. Sci. 2004; 1011:317–324. PubMed
Pandey R., Mehrotra D., Mahdi A.A., Sarin R., Kowtal P. Additional cytosine inside mitochondrial C-tract D-loop as a progression risk factor in oral precancer cases. J. Oral Biol. Craniof. Res. 2014; 4:3–7. PubMed PMC
Ha P.K., Tong B.C., Westra W.H., Sanchez-Cespedes M., Parrella P., Zahurak M., Sidransky D., Califano J.A. Mitochondrial C-tract alteration in premalignant lesions of the head and neck: a marker for progression and clonal proliferation. Clin. Cancer Res. 2002; 8:2260–2265. PubMed
Tang D., Zhou X., Zhou K., Li X., Zhao L., Liu F., Zheng F., Liu S. [Association of mitochondrial DNA variation with type 2 diabetes mellitus]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi. 2005; 22:636–640. PubMed
Liou C.-W., Lin T.-K., Chen J.-B., Tiao M.-M., Weng S.-W., Chen S.-D., Chuang Y.-C., Chuang J.-H., Wang P.-W. Association between a common mitochondrial DNA D-loop polycytosine variant and alteration of mitochondrial copy number in human peripheral blood cells. J. Med. Genet. 2010; 47:723–728. PubMed
Agaronyan K., Morozov Y.I., Anikin M., Temiakov D. Mitochondrial biology. Replication-transcription switch in human mitochondria. Science. 2015; 347:548–551. PubMed PMC