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Research Paper

R1 retrotransposons in the nucleolar organizers of Drosophila melanogaster are transcribed by RNA polymerase I upon heat shock

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Pages 273-285 | Received 18 Jan 2018, Accepted 23 Jul 2018, Published online: 21 Aug 2018

References

  • Long EO, Dawid IB. Alternative pathways in the processing of ribosomal RNA precursor in Drosophila melanogaster. J Mol Biol. 1980;138(4):873–878. PMID:6774101
  • Turowski TW, Tollervey D. Cotranscriptional events in eukaryotic ribosome synthesis. WIREs RNA. 2015;6(1):129–139. PMID:25176256
  • Perez-Gonzalez CE, Eickbush TH. Rates of R1 and R2 retrotransposition and elimination from the rDNA locus of Drosophila melanogaster. Genetics. 2002;162(2):799–811. PMID:12399390
  • Eickbush TH. R2 and related site-specific non-long terminal repeat retrotransposons. mobile DNA II. Washington (DC): American Society of Microbiology; 2002. DOI:10.1128/9781555817954.ch34.
  • Stage DE, Eickbush TH. Origin of nascent lineages and the mechanisms used to prime second-strand DNA synthesis in the R1 and R2 retrotransposons of Drosophila. Genome Biol. 2009;10:R49.
  • Long EO, Dawid IB. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 1979;18(4):1185–1196. PMID:117903
  • Ye J, Eickbush TH. Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol. 2006;26(23):8781–8790. PMID: 17000772
  • Eickbush DG, Eickbush TH. R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript. Mol Cell Biol. 2010;30(13):3142–3150. PMID:20421411
  • He F, James A, Raje H, et al. Deletion of Drosophila Nopp140 induces subcellular ribosomopathies. Chromosoma. 2015;124(2):191–208. PMID:25384888
  • Chen H, Zheng X, Xiao D, et al. Age-associated de-repression of retrotransposons in the Drosophila fat body, its potential cause and consequence. Aging Cell. 2016;15(3):542–552. PMID:27072046
  • Lavie L, Maldener E, Brouha B, et al. The human L1 promoter: variable transcription initiation sites and a major impact of upstream flanking sequence on promoter activity. Genome Res. 2004;14(11):2253–2260. PMID:15520289
  • Cavrak VV, Lettner N, Jamge S, et al. How a retrotransposon exploits the plant’s heat stress response for its activation. PLoS Genet. 2014;10(1):e1004115. PMID:24497839
  • Ikeda K, Nakayashiki H, Takagi M, et al. Heat shock, copper sulfate and oxidative stress activate the retrotransposon MAGGY resident in the plant pathogenic fungus Magnaporthe grisea. Mol Genet Genomics. 2001;266(2):318–325. PMID:11683275
  • Strand DJ, McDonald JF. Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res. 1985;13(12):4401–4410. PMID:2409535
  • Gilmour DS, Lis JT. In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol Cell Biol. 1985;5(8):2009–2018. PMID:3018544
  • Svensson MJ, Larsson J. Thioredoxin-2 affects lifespan and oxidative stress in Drosophila. Hereditas. 2007;144(1):25–32. PMID:17567437
  • He F, DiMario PJ. Drosophila delta-1-pyrroline-5-carboxylate dehydrogenase (P5CDh) is required for proline breakdown and mitochondrial integrity - Establishing a fly model for human type II hyperprolinemia. Mitochondrion. 2011;11:397–404. PMID:21168532
  • Perry RP, Kelley DE. Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J Cell Physiol. 1970;76(2):127–139. PMID: 55000970
  • Chen HK, Pai CY, Huang JY, et al. Human Nopp140, which interacts with RNA polymerase I: implications for rRNA gene transcription and nucleolar structural organization. Mol Cell Biol. 1999;19(12):8536–8546. PMID 10567578
  • Shcherbik N, Wang M, Lapik YR, et al. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 2010;11(2):106–111. PMID:20062005
  • Allmang C, Mitchell P, Petfalski E, et al. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 2000;28(8):1684–1691. PMID:10734186
  • Mizrokhi LJ, Georgieva SG, Ilyin YV. Jockey, a mobile Drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell. 1988;54(5):685–691. PMID:2842063
  • Heras SR, Thomas MC, García-Canadas M, et al. L1Tc non-LTR retrotransposons from Trypanosoma cruzi contain a functional viral-like self-cleaving 2A sequence in frame with the active proteins they encode. Cell Mol Life Sci. 2006;63(12):1449–1460. PMID:16767356
  • Ostertag EM, Kazazian HH Jr. Biology of mammalian L1 retrotransposons. Annu Rev Genet. 2001;35:501–538. PMID:11700292
  • Dawid IB, Botchan P. Sequences homologous to ribosomal insertions occur in the Drosophila genome outside the nucleolus organizer. Proc Natl Acad Sci USA. 1977;74:4233–4237. PMID:412186
  • Kidd SJ, Glover DM. A DNA segment from D. melanogaster which contains five tandemly repeated units homologous to the major rDNA insertion. Cell. 1980;19:103–119. PMID:6244098
  • Roiha H, Miller JR, Woods LC, et al. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature. 1981;290:749–753. PMID:6783966
  • Browne MJ, Read CA, Roiha H, et al. Site specific insertion of a type I rDNA element into a unique sequence in the Drosophila melanogaster genome. Nucleic Acids Res. 1984;12:9111–9122. PMID:6096818
  • Glover DM, Hogness DS. A novel arrangement of the 18S and 28S sequences in a repeating unit of Drosophila melanogaster rDNA. Cell. 1977;10:167–176. PMID:402220
  • Hendrix DA, Hong J-W, Zeitlinger J, et al. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc Natl Acad Sci. 2008;105(22):7762–7767. PMID:18505835
  • Akerfelt M, Morimoto RI, Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol. 2010;11(8):545–555. PMID:20628411
  • Duarte FM, Fuda NJ, Mahat DB, et al. Transcription factors GAF and HSF act at distinct regulatory steps to modulate stress-induced gene activation. Genes Dev. 2016;30(15):1731–1746. PMID:27492368
  • Mahat DB, Kwak H, Booth GT, et al. Base-pair-resolution genome-wide mapping of active RNA polymerases using precision nuclear run-on (PRO-seq). Nat Protoc. 2016;11(8):1455–1476. PMID:27442863
  • Bouche G, Raynal F, Amalric F, et al. Unusual processing of nucleolar RNA synthesized during a heat shock in CHO cells. Mol Biol Rep. 1981;7:253–258. PMID:7290092
  • Ghoshal K, Jacob ST. Heat shock selectively inhibits ribosomal RNA gene transcription and down-regulates E1BF/Ku in mouse lymphosarcoma cells. Biochem J. 1996;317:689–695. PMID:8760351
  • Zhao Z, Dammert MA, Hoppe S, et al. Heat shock represses rRNA synthesis by inactivation of TIF-IA and lncRNA-dependent changes in nucleosome positioning. Nucleic Acids Res. 2016;44(17):8144–8152. PMID:27257073
  • Ellgaard EG, Clever U. RNA metabolism during puff induction in Drosophila melanogaster. Chromosoma. 1971;36(1):60–78. PMID:5003534
  • Lengyel JA, Ransom LJ, Graham ML, et al. Transcription and metabolism of RNA from the Drosophila melanogaster heat shock puff site 93D. Chromosoma. 1980;80(3):237–252. PMID:6160021
  • Bell J, Neilson L, Pelligrini M. Effect of heat shock on ribosomal synthesis in Drosophila melanogaster. Mol Cell Biol. 1988;8(1):91–95. PMID:3122028
  • Bonner JJ, Kerby RL. RNA polymerase II transcribes all of the heat shock induced genes of Drosophila melanogaster. Chromosoma. 1982;85(1):93–108. PMID:6807638
  • Mahat DB, Salamanca HH, Duarte FM, et al. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell. 2016;62(1):63–78. PMID:27052732
  • Perisic O, Xiao H, Lis JT. Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell. 1989;59(5):797–806. PMID:2590940
  • Amin J, Ananthan J, Voellmy R. Key features of heat shock regulatory elements. Mol Cell Biol. 1988;8(9):3761–3769. PMID:3146692
  • O’Brien T, Wilkins RC, Giardina C, et al. Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev. 1995;9(9):1098–1110. PMID:7744251
  • Winer J, Jung CK, Shackel I, et al. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem. 1999;270(1):41–49. PMID:10328763
  • Afgan E, Baker D, van den Beek M, et al. The galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res. 2016;44(W1):W3–W10. PMID:27137889
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. PMID:22388286
  • Robinson JT, Thorvaldsdottir H, Winckler W, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29(1):24–26. PMID:21221095

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