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Crystal structure and nucleotide binding of the Thermus thermophilus RNA helicase Hera N-terminal domain.

Rudolph MG, Heissmann R, Wittmann JG, Klostermeier D
J Mol Biol 361 731-43 (2006)
Related entries: 2gxq, 2gxu

Cited: 28 times
EuropePMC logo PMID: 16890241

Abstract

DEAD box RNA helicases use the energy of ATP hydrolysis to unwind double-stranded RNA regions or to disrupt RNA/protein complexes. A minimal RNA helicase comprises nine conserved motifs distributed over two RecA-like domains. The N-terminal domain contains all motifs involved in nucleotide binding, namely the Q-motif, the DEAD box, and the P-loop, as well as the SAT motif, which has been implicated in the coordination of ATP hydrolysis and RNA unwinding. We present here the crystal structure of the N-terminal domain of the Thermus thermophilus RNA helicase Hera in complex with adenosine monophosphate (AMP). Upon binding of AMP the P-loop adopts a partially collapsed or half-open conformation that is still connected to the DEAD box motif, and the DEAD box in turn is linked to the SAT motif via hydrogen bonds. This network of interactions communicates changes in the P-loop conformation to distant parts of the helicase. The affinity of AMP is comparable to that of ADP and ATP, substantiating that the binding energy from additional phosphate moieties is directly converted into conformational changes of the entire helicase. Importantly, the N-terminal Hera domain forms a dimer in the crystal similar to that seen in another thermophilic prokaryote. It is possible that this mode of dimerization represents the prototypic architecture in RNA helicases of thermophilic origin.

Reviews citing this publication (5)

  1. RNA helicase proteins as chaperones and remodelers. Jarmoskaite I, Russell R. Annu Rev Biochem 83 697-725 (2014)
  2. DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Putnam AA, Jankowsky E. Biochim Biophys Acta 1829 884-893 (2013)
  3. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Hilbert M, Karow AR, Klostermeier D. Biol Chem 390 1237-1250 (2009)
  4. How RNA unfolds and refolds. Li PT, Vieregg J, Tinoco I. Annu Rev Biochem 77 77-100 (2008)
  5. Modular peptide binding: from a comparison of natural binders to designed armadillo repeat proteins. Reichen C, Hansen S, Plückthun A. J Struct Biol 185 147-162 (2014)

Articles citing this publication (23)

  1. Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Theissen B, Karow AR, Köhler J, Gubaev A, Klostermeier D. Proc Natl Acad Sci U S A 105 548-553 (2008)
  2. Crystal structure of conserved domains 1 and 2 of the human DEAD-box helicase DDX3X in complex with the mononucleotide AMP. Högbom M, Collins R, van den Berg S, Jenvert RM, Karlberg T, Kotenyova T, Flores A, Karlsson Hedestam GB, Schiavone LH. J Mol Biol 372 150-159 (2007)
  3. Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM. Nature 490 121-125 (2012)
  4. Invariant U2 snRNA nucleotides form a stem loop to recognize the intron early in splicing. Perriman R, Ares M. Mol Cell 38 416-427 (2010)
  5. Division of Labor in an Oligomer of the DEAD-Box RNA Helicase Ded1p. Putnam AA, Gao Z, Liu F, Jia H, Yang Q, Jankowsky E. Mol Cell 59 541-552 (2015)
  6. A novel dimerization motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility. Klostermeier D, Rudolph MG. Nucleic Acids Res 37 421-430 (2009)
  7. Solution and crystal structures of mRNA exporter Dbp5p and its interaction with nucleotides. Fan JS, Cheng Z, Zhang J, Noble C, Zhou Z, Song H, Yang D. J Mol Biol 388 1-10 (2009)
  8. The putative RNase P motif in the DEAD box helicase Hera is dispensable for efficient interaction with RNA and helicase activity. Linden MH, Hartmann RK, Klostermeier D. Nucleic Acids Res 36 5800-5811 (2008)
  9. Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase. Mallam AL, Sidote DJ, Lambowitz AM. Elife 3 e04630 (2014)
  10. DEAD-box RNA helicase domains exhibit a continuum between complete functional independence and high thermodynamic coupling in nucleotide and RNA duplex recognition. Samatanga B, Klostermeier D. Nucleic Acids Res 42 10644-10654 (2014)
  11. Mutational analysis of Mycobacterium UvrD1 identifies functional groups required for ATP hydrolysis, DNA unwinding, and chemomechanical coupling. Sinha KM, Glickman MS, Shuman S. Biochemistry 48 4019-4030 (2009)
  12. Crystal structure of human RNA helicase A (DHX9): structural basis for unselective nucleotide base binding in a DEAD-box variant protein. Schütz P, Wahlberg E, Karlberg T, Hammarström M, Collins R, Flores A, Schüler H. J Mol Biol 400 768-782 (2010)
  13. AMP sensing by DEAD-box RNA helicases. Putnam AA, Jankowsky E. J Mol Biol 425 3839-3845 (2013)
  14. Structural and functional analysis of the RNA helicase Prp43 from the thermophilic eukaryote Chaetomium thermophilum. Tauchert MJ, Fourmann JB, Christian H, Lührmann R, Ficner R. Acta Crystallogr F Struct Biol Commun 72 112-120 (2016)
  15. Recognition of two distinct elements in the RNA substrate by the RNA-binding domain of the T. thermophilus DEAD box helicase Hera. Steimer L, Wurm JP, Linden MH, Rudolph MG, Wöhnert J, Klostermeier D. Nucleic Acids Res 41 6259-6272 (2013)
  16. High-throughput genetic identification of functionally important regions of the yeast DEAD-box protein Mss116p. Mohr G, Del Campo M, Turner KG, Gilman B, Wolf RZ, Lambowitz AM. J Mol Biol 413 952-972 (2011)
  17. The Thermus thermophilus DEAD box helicase Hera contains a modified RNA recognition motif domain loosely connected to the helicase core. Rudolph MG, Klostermeier D. RNA 15 1993-2001 (2009)
  18. The Q Motif Is Involved in DNA Binding but Not ATP Binding in ChlR1 Helicase. Ding H, Guo M, Vidhyasagar V, Talwar T, Wu Y. PLoS One 10 e0140755 (2015)
  19. Changing nucleotide specificity of the DEAD-box helicase Hera abrogates communication between the Q-motif and the P-loop. Strohmeier J, Hertel I, Diederichsen U, Rudolph MG, Klostermeier D. Biol Chem 392 357-369 (2011)
  20. eIF4A1-dependent mRNAs employ purine-rich 5'UTR sequences to activate localised eIF4A1-unwinding through eIF4A1-multimerisation to facilitate translation. Schmidt T, Dabrowska A, Waldron JA, Hodge K, Koulouras G, Gabrielsen M, Munro J, Tack DC, Harris G, McGhee E, Scott D, Carlin LM, Huang D, Le Quesne J, Zanivan S, Wilczynska A, Bushell M. Nucleic Acids Res 51 1859-1879 (2023)
  21. Deciphering the molecular basis for nucleotide selection by the West Nile virus RNA helicase. Despins S, Issur M, Bougie I, Bisaillon M. Nucleic Acids Res 38 5493-5506 (2010)
  22. Crystallization and preliminary characterization of the Thermus thermophilus RNA helicase Hera C-terminal domain. Rudolph MG, Wittmann JG, Klostermeier D. Acta Crystallogr Sect F Struct Biol Cryst Commun 65 248-252 (2009)
  23. The Thermus thermophilus DEAD-box protein Hera is a general RNA binding protein and plays a key role in tRNA metabolism. Donsbach P, Yee BA, Sanchez-Hevia D, Berenguer J, Aigner S, Yeo GW, Klostermeier D. RNA 26 1557-1574 (2020)


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