Quadruplex DNA in long terminal repeats in maize LTR retrotransposons inhibits the expression of a reporter gene in yeast

. 2018 Mar 06 ; 19 (1) : 184. [epub] 20180306

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29510672

Grantová podpora
18-00258S Grantová Agentura České Republiky - International
FIT-S-17-3964 Vysoké Učení Technické v Brně - International

Odkazy

PubMed 29510672
PubMed Central PMC5838962
DOI 10.1186/s12864-018-4563-7
PII: 10.1186/s12864-018-4563-7
Knihovny.cz E-zdroje

BACKGROUND: Many studies have shown that guanine-rich DNA sequences form quadruplex structures (G4) in vitro but there is scarce evidence of guanine quadruplexes in vivo. The majority of potential quadruplex-forming sequences (PQS) are located in transposable elements (TEs), especially close to promoters within long terminal repeats of plant LTR retrotransposons. RESULTS: In order to test the potential effect of G4s on retrotransposon expression, we cloned the long terminal repeats of selected maize LTR retrotransposons upstream of the lacZ reporter gene and measured its transcription and translation in yeast. We found that G4s had an inhibitory effect on translation in vivo since "mutants" (where guanines were replaced by adenines in PQS) showed higher expression levels than wild-types. In parallel, we confirmed by circular dichroism measurements that the selected sequences can indeed adopt G4 conformation in vitro. Analysis of RNA-Seq of polyA RNA in maize seedlings grown in the presence of a G4-stabilizing ligand (NMM) showed both inhibitory as well as stimulatory effects on the transcription of LTR retrotransposons. CONCLUSIONS: Our results demonstrate that quadruplex DNA located within long terminal repeats of LTR retrotransposons can be formed in vivo and that it plays a regulatory role in the LTR retrotransposon life-cycle, thus also affecting genome dynamics.

Zobrazit více v PubMed

Kwok CK, Merrick CJ. G-Quadruplexes: prediction, characterization, and biological application. Trends Biotechnol. 2017;35:997–1013. doi: 10.1016/j.tibtech.2017.06.012. PubMed DOI

Vorlíčková M, Kejnovská I, Sagi J, Renčiuk D, Bednářová K, Motlová J, et al. Circular dichroism and guanine quadruplexes. Methods. 2012;57:64–75. doi: 10.1016/j.ymeth.2012.03.011. PubMed DOI

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

Lam EYN, Beraldi D, Tannahill D, Balasubramanian S. G-quadruplex structures are stable and detectable in human genomic DNA. Nat Commun. 2013;4:1796. doi: 10.1038/ncomms2792. PubMed DOI PMC

Andorf CM, Kopylov M, Dobbs D, Koch KE, Stroupe ME, Lawrence CJ, et al. G-Quadruplex (G4) motifs in the maize (Zea mays L.) genome are enriched at specific locations in thousands of genes coupled to energy status, hypoxia, low sugar, and nutrient deprivation. J Genet Genomics. 2014;41:627–647. doi: 10.1016/j.jgg.2014.10.004. PubMed DOI

Rhodes D, Lipps HJ. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 2015;43:8627–8637. doi: 10.1093/nar/gkv862. PubMed DOI PMC

Fay MM, Lyons SM, Ivanov P. RNA G-Quadruplexes in biology: principles and molecular mechanisms. J Mol Biol. 2017;429:2127–2147. doi: 10.1016/j.jmb.2017.05.017. PubMed DOI PMC

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

Li Q, Xiang JF, Yang QF, Sun HX, Guan AJ, Tang YL. G4LDB: a database for discovering and studying G-quadruplex ligands. Nucleic Acids Res. 2013;41:1115–1123. doi: 10.1093/nar/gks1101. PubMed DOI PMC

Biffi G, Di Antonio M, Tannahill D, Balasubramanian S. Visualization and selective chemical targeting of RNA G-quadruplex structures in the cytoplasm of human cells. Nat Chem. 2014;6:75–80. doi: 10.1038/nchem.1805. PubMed DOI PMC

Lexa M, Kejnovský E, Šteflová P, Konvalinová H, Vorlíčková M, Vyskot B. Quadruplex-forming sequences occupy discrete regions inside plant LTR retrotransposons. Nucleic Acids Res. 2014;42:968–978. doi: 10.1093/nar/gkt893. PubMed DOI PMC

Lexa M, Steflova P, Martinek T, Vorlickova M, Vyskot B, Kejnovsky E. Guanine quadruplexes are formed by specific regions of human transposable elements. BMC Genomics. 2014;15:1032. doi: 10.1186/1471-2164-15-1032. PubMed DOI PMC

Sahakyan AB, Murat P, Mayer C, Balasubramanian S. G-quadruplex structures within the 3′ UTR of LINE-1 elements stimulate retrotransposition. Nat Struct Mol Biol. 2017;24:243–247. doi: 10.1038/nsmb.3367. PubMed DOI

D’Antonio L, Bagga P. Proceedings of the 2004 IEEE computational systems bioinformatics conference. 2004. Computational methods for predicting intra-molecular G-quadruplexes in nucleotide sequences; pp. 590–591.

Hon J, Martínek T, Zendulka J, Lexa M. pqsfinder: an exhaustive and imperfection-tolerant search tool for potential quadruplex-forming sequences in R. Bioinformatics. 2017;33:3373–3379. doi: 10.1093/bioinformatics/btx413. PubMed DOI

Bedrat A, Lacroix L, Mergny JL. Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016;44:1746–1759. doi: 10.1093/nar/gkw006. PubMed DOI PMC

Garant JM, Perreault JP, Scott MS. Motif independent identification of potential RNA G-quadruplexes by G4RNA screener. Bioinformatics. 2017;33:3532–3537. doi: 10.1093/bioinformatics/btx498. PubMed DOI PMC

Sahakyan AB, Chambers VS, Marsico G, Santner T, D'Antonio M, Balasubramanian S. Machine learning model for sequence-driven DNA G-quadruplex formation. Sci Rep. 2017; 10.1038/s41598-017-14017-4. PubMed PMC

Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods. 2015;12:115–121. doi: 10.1038/nmeth.3252. PubMed DOI PMC

Chambers VS, Marsico G, Boutell JM, Di Antonio M, Smith GP, Balasubramanian S. High-throughput sequencing of DNA G-quadruplex structures in the human genome. Nat Biotechnol. 2015;33:877–881. doi: 10.1038/nbt.3295. PubMed DOI

Xu Z, Wang H. LTR-FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007;35:265–268. doi: 10.1093/nar/gkm286. PubMed DOI PMC

Gish W, States DJ. Identification of protein coding regions by database similarity search. Nat Genet. 1993;3:266–272. doi: 10.1038/ng0393-266. PubMed DOI

Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, et al. The gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. 2011;39:D70–D74. doi: 10.1093/nar/gkq1061. PubMed DOI PMC

Mumberg D, Müller R, Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene. 1995;156:119–122. doi: 10.1016/0378-1119(95)00037-7. PubMed DOI

Collart MA, Oliviero S. Current protocol in molecular biology. United States: Wiley; 1993. Preparation of yeast RNA. PubMed

Shahmuradov IA, Umarov RK, Solovyev VV. TSSPlant: a new tool for prediction of plant Pol II promoters. Nucleic Acids Res. 2017;45:e65. PubMed PMC

Reid PH, York ET. Effect of nutrient deficiencies on growth and fruiting characteristics of peanuts in sand cultures1. Agron J. 1958;50:63–67. doi: 10.2134/agronj1958.00021962005000020002x. DOI

Andrews S. FastQC a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 20 Oct 2017.

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. doi: 10.1093/bioinformatics/bts635. PubMed DOI PMC

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–930. doi: 10.1093/bioinformatics/btt656. PubMed DOI

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

Schurch NJ, Schofield P, Gierliński M, Cole C, Sherstnev A, Singh V, et al. Erratum: how many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA. 2016;22:839–851. doi: 10.1261/rna.053959.115. PubMed DOI PMC

Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. doi: 10.1093/bioinformatics/btq033. PubMed DOI PMC

Kumari S, Bugaut A, Huppert JL, Balasubramanian S. An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation. Nat Chem Biol. 2007;3:218–221. doi: 10.1038/nchembio864. PubMed DOI PMC

Arora A, Dutkiewicz M, Scaria V, Hariharan M, Maiti S, Kurreck J. Inhibition of translation in living eukaryotic cells by an RNA G-quadruplex motif. RNA. 2008;14:1290–1296. doi: 10.1261/rna.1001708. PubMed DOI PMC

Smestad JA, Maher LJ. Relationships between putative G-quadruplex-forming sequences, RecQ helicases, and transcription. BMC Med Genet. 2015;16:91. doi: 10.1186/s12881-015-0236-4. PubMed DOI PMC

Lyonnais S, Gorelick RJ, Mergny JL, Le Cam E, Mirambeau G. G-quartets direct assembly of HIV-1 nucleocapsid protein along single-stranded DNA. Nucleic Acids Res. 2003;31:5754–5763. doi: 10.1093/nar/gkg716. PubMed DOI PMC

Piekna-Przybylska D, Sharma G, Bambara RA. Mechanism of HIV-1 RNA dimerization in the central region of the genome and significance for viral evolution. J Biol Chem. 2013;288:24140–24150. doi: 10.1074/jbc.M113.477265. PubMed DOI PMC

Shen W, Gorelick RJ, Bambara RA. HIV-1 nucleocapsid protein increases strand transfer recombination by promoting dimeric G-quartet formation. J Biol Chem. 2011;286:29838–29847. doi: 10.1074/jbc.M111.262352. PubMed DOI PMC

Marquet R, Christophe PJ, Skripkin E, Ehresmann C, Ehresmann B. Dimerization of human immunodeficiency virus type 1 RNA involves sequences located upstream of the splice donor site. Nucleic Acids Res. 1994;22:145–151. doi: 10.1093/nar/22.2.145. PubMed DOI PMC

Sundquist WI, Heaphy S. Evidence for interstrand quadruplex formation in the dimerization of human immunodeficiency virus 1 genomic RNA. Proc Natl Acad Sci U S A. 1993;90:3393–3397. doi: 10.1073/pnas.90.8.3393. PubMed DOI PMC

Morris MJ, Negishi Y, Pazsint C, Schonhoft JD, Basu S. An RNA G-quadruplex is essential for cap-independent translation initiation in human VEGF IRES. J Am Chem Soc. 2010;132:17831–17839. doi: 10.1021/ja106287x. PubMed DOI

Miyoshi D, Karimata H, Sugimoto N. Hydration regulates thermodynamics of G-quadruplex formation under molecular crowding conditions. J Am Chem Soc. 2006;128:7957–7963. doi: 10.1021/ja061267m. PubMed DOI

Lacerda R, Menezes J, Romão L. More than just scanning: the importance of cap-independent mRNA translation initiation for cellular stress response and cancer. Cell Mol Life Sci. 2017;74:1659–1680. doi: 10.1007/s00018-016-2428-2. PubMed DOI PMC

Kejnovsky E, Lexa M. Quadruplex-forming DNA sequences spread by retrotransposons may serve as genome regulators. Mob Genet Elements. 2014;4:e28084. doi: 10.4161/mge.28084. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...