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Structure of an RNA polymerase II-RNA inhibitor complex elucidates transcription regulation by noncoding RNAs.

Kettenberger H, Eisenführ A, Brueckner F, Theis M, Famulok M, Cramer P
Nat Struct Mol Biol 13 44-8 (2006)
Cited: 49 times
EuropePMC logo PMID: 16341226

Abstract

The noncoding RNA B2 and the RNA aptamer FC bind RNA polymerase (Pol) II and inhibit messenger RNA transcription initiation, but not elongation. We report the crystal structure of FC(*), the central part of FC RNA, bound to Pol II. FC(*) RNA forms a double stem-loop structure in the Pol II active center cleft. B2 RNA may bind similarly, as it competes with FC(*) RNA for Pol II interaction. Both RNA inhibitors apparently prevent the downstream DNA duplex and the template single strand from entering the cleft after DNA melting and thus interfere with open-complex formation. Elongation is not inhibited, as nucleic acids prebound in the cleft would exclude the RNA inhibitors. The structure also indicates that A-form RNA could interact with Pol II similarly to a B-form DNA promoter, as suggested for the bacterial transcription inhibitor 6S RNA.

Reviews - 2b63 mentioned but not cited (1)

  1. Structural Biology for the Molecular Insight between Aptamers and Target Proteins. Zhang N, Chen Z, Liu D, Jiang H, Zhang ZK, Lu A, Zhang BT, Yu Y, Zhang G. Int J Mol Sci 22 4093 (2021)

Articles - 2b63 mentioned but not cited (4)

  1. Molecular architecture of the human Mediator-RNA polymerase II-TFIIF assembly. Bernecky C, Grob P, Ebmeier CC, Nogales E, Taatjes DJ. PLoS Biol 9 e1000603 (2011)
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  4. Characterization of known protein complexes using k-connectivity and other topological measures. Gallagher SR, Goldberg DS. F1000Res 2 172 (2013)


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  2. B2 RNA and Alu RNA repress transcription by disrupting contacts between RNA polymerase II and promoter DNA within assembled complexes. Yakovchuk P, Goodrich JA, Kugel JF. Proc Natl Acad Sci U S A 106 5569-5574 (2009)
  3. Fluorescence-activated cell sorting for aptamer SELEX with cell mixtures. Mayer G, Ahmed MS, Dolf A, Endl E, Knolle PA, Famulok M. Nat Protoc 5 1993-2004 (2010)
  4. Molecular basis of RNA-dependent RNA polymerase II activity. Lehmann E, Brueckner F, Cramer P. Nature 450 445-449 (2007)
  5. An allosteric path to transcription termination. Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E. Mol Cell 28 991-1001 (2007)
  6. Characterization of the structure, function, and mechanism of B2 RNA, an ncRNA repressor of RNA polymerase II transcription. Espinoza CA, Goodrich JA, Kugel JF. RNA 13 583-596 (2007)
  7. Structural biology of RNA polymerase III: subcomplex C17/25 X-ray structure and 11 subunit enzyme model. Jasiak AJ, Armache KJ, Martens B, Jansen RP, Cramer P. Mol Cell 23 71-81 (2006)
  8. Real-time footprinting of DNA in the first kinetically significant intermediate in open complex formation by Escherichia coli RNA polymerase. Davis CA, Bingman CA, Landick R, Record MT, Saecker RM. Proc Natl Acad Sci U S A 104 7833-7838 (2007)
  9. Iwr1 directs RNA polymerase II nuclear import. Czeko E, Seizl M, Augsberger C, Mielke T, Cramer P. Mol Cell 42 261-266 (2011)
  10. 6S RNA binding to Esigma(70) requires a positively charged surface of sigma(70) region 4.2. Klocko AD, Wassarman KM. Mol Microbiol 73 152-164 (2009)
  11. Selection and application of ssDNA aptamers to detect active TB from sputum samples. Rotherham LS, Maserumule C, Dheda K, Theron J, Khati M. PLoS One 7 e46862 (2012)
  12. Function and assembly of a chromatin-associated RNase P that is required for efficient transcription by RNA polymerase I. Reiner R, Krasnov-Yoeli N, Dehtiar Y, Jarrous N. PLoS One 3 e4072 (2008)
  13. Inhibition of hepatitis C virus (HCV) RNA polymerase by DNA aptamers: mechanism of inhibition of in vitro RNA synthesis and effect on HCV-infected cells. Bellecave P, Cazenave C, Rumi J, Staedel C, Cosnefroy O, Andreola ML, Ventura M, Tarrago-Litvak L, Astier-Gin T. Antimicrob Agents Chemother 52 2097-2110 (2008)
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  15. The non-coding B2 RNA binds to the DNA cleft and active-site region of RNA polymerase II. Ponicsan SL, Houel S, Old WM, Ahn NG, Goodrich JA, Kugel JF. J Mol Biol 425 3625-3638 (2013)
  16. Inhibition of BACE1 Activity by a DNA Aptamer in an Alzheimer's Disease Cell Model. Liang H, Shi Y, Kou Z, Peng Y, Chen W, Li X, Li S, Wang Y, Wang F, Zhang X. PLoS One 10 e0140733 (2015)
  17. B2 SINE retrotransposon causes polymorphic expression of mouse 5-aminolevulinic acid synthase 1 gene. Chernova T, Higginson FM, Davies R, Smith AG. Biochem Biophys Res Commun 377 515-520 (2008)
  18. An RNA-based transcription activator derived from an inhibitory aptamer. Wang S, Shepard JR, Shi H. Nucleic Acids Res 38 2378-2386 (2010)
  19. RNA-aptamers that modulate the RhoGEF activity of Tiam1. Niebel B, Wosnitza CI, Famulok M. Bioorg Med Chem 21 6239-6246 (2013)
  20. Non-Coding RNAs As Transcriptional Regulators In Eukaryotes. Burenina OY, Oretskaya TS, Kubareva EA. Acta Naturae 9 13-25 (2017)
  21. RNAs nonspecifically inhibit RNA polymerase II by preventing binding to the DNA template. Pai DA, Kaplan CD, Kweon HK, Murakami K, Andrews PC, Engelke DR. RNA 20 644-655 (2014)
  22. Mechanistic Dissection of RNA-Binding Proteins in Regulated Gene Expression at Chromatin Levels. Chen JY, Lim DH, Fu XD. Cold Spring Harb Symp Quant Biol 84 55-66 (2019)
  23. RNA polymerase II-binding aptamers in human ACRO1 satellites disrupt transcription in cis. Boots JL, von Pelchrzim F, Weiss A, Zimmermann B, Friesacher T, Radtke M, Żywicki M, Chen D, Matylla-Kulińska K, Zagrovic B, Schroeder R. Transcription 11 217-229 (2020)
  24. News Merging the RNA and DNA worlds. Artsimovitch I, Vassylyev DG. Nat Struct Mol Biol 14 1122-1123 (2007)
  25. Nascent RNA signaling to yeast RNA Pol II during transcription elongation. Klopf E, Moes M, Amman F, Zimmermann B, von Pelchrzim F, Wagner C, Schroeder R. PLoS One 13 e0194438 (2018)
  26. Altered stoichiometry of an evolved RNA aptamer. Ohuchi S, Suess B. RNA 24 480-485 (2018)


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