Functional visualization of viral molecular motor by hydrogen-deuterium exchange reveals transient states

Nature Structural and Molecular Biology

Volumn 12, Issue 5, 2005, Pages 460-466

  Lísal, Jiří ^a   Lam, TuKiet T ^b,c   Kainov, Denis E ^a   Emmett, Mark R ^b   Marshall, Alan G ^b   Tuma, Roman ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b FLORIDA STATE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEUTERIUM; DOUBLE STRANDED RNA; HELICASE; MOLECULAR MOTOR; VIRUS PROTEIN; RNA;

ARTICLE; BACTERIOPHAGE; BINDING SITE; DEUTERIUM HYDROGEN EXCHANGE; ENERGY; KINETICS; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; RNA BINDING; SPECTROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; GENETICS; METABOLISM; MUTATION; NUCLEAR MAGNETIC RESONANCE; PROTEIN QUATERNARY STRUCTURE;

BACTERIOPHAGE PHI-8;

ADENOSINE TRIPHOSPHATE; BINDING SITES; DEUTERIUM EXCHANGE MEASUREMENT; KINETICS; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, QUATERNARY; RNA; VIRAL PROTEINS;

EID: 20444463552     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb927     Document Type: Article

References (38)

1. Keller, D. & Bustamante, C. The mechanochemistry of molecular motors. Biophys. J. 78,541-556 (2000).
2. Delagoutte, E. & von Hippel, P.H. Helicase mechanisms and the coupling of helicases within macromolecular machines. Part I: structures and properties of isolated helicases. Quart. Rev. Biophys. 35,431-478 (2002).
3. Moore, S.D. & Prevelige, P.E. Jr. DNA packaging: a new class of molecular motors. Curr. Biol. 12, R96-R98 (2002).
4. Mancini, E.J. et al. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 118, 743-755 (2004).
5. Kainov, D.E. et al. RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J. Biol. Chem. 278,48084-48091 (2003).
6. Singleton, M.R., Sawaya, M.R., Ellenberger, T. & Wigley, D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101, 589-600 (2000).
7. Patel, S.S. & Picha, K.M. Structure and function of hexameric helicases. Annu. Rev. Biochem. 69,651-697 (2000).
8. Skordalakes, E. & Berger, J.M. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114, 135-146 (2003).
9. Gai, D., Zhao, R., Li, D., Finkielstein, C.V. & Chen, X.S. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119, 47-60 (2004).
10. Hoofnagle, A.N., Resing, K.A. & Ahn, N.G. Protein analysis by hydrogen exchange mass spectrometry. Annu. Rev. Biophys. Biomol. Struct. 32,1-25 (2003).
11. Englander, S.W., Sosnick, T.R., Englander, J.J. & Mayne, L. Mechanisms and uses of hydrogen exchange. Curr. Opin. Struct. Biol. 6, 18-23 (1996).
12. Hoofnagle, A.N., Resing, K.A., Goldsmith, E.J. & Ahn, N.G. Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl. Acad. Sci. USA 98,956-961 (2001).
13. Lanman, J. et al. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11, 676-677 (2004).
14. Marshall, A.G., Hendrickson, C.L. & Jackson, G.S. Fourier transform ion cyclotron resonance mass spectrometry: a primer. Mass Spectrom. Rev. 17, 1-35 (1998).
15. Wang, F. et al. Fourier transform ion cyclotron resonance mass spectrometric detection of small Ca(2+)-induced conformational changes in the regulatory domain of human cardiac troponin C. J. Am. Soc. Mass Spectrom. 10, 703-710 (1999).
16. Lisal, J., Kainov, D.E., Bamford, D.H., Thomas, G.J. Jr. & Tuma, R. Enzymatic mechanism of RNA translocation in double-stranded RNA bacteriophages. J. Biol. Chem. 279,1343-1350 (2004).
17. Milne, J.S., Mayne, L., Roder, H., Wand, A.J. & Englander, S.W. Determinants of protein hydrogen exchange studied in equine cytochrome c. Protein Sci. 7, 739-745 (1998).
18. Englander, J.J. et al. Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry. Proc. Natl. Acad. Sci. USA 100, 7057-7062 (2003).
19. Picha, K.M., Ahnert, P. & Patel, S.S. DNA binding in the central channel of bacteriophage T7 helicase-primase is a multistep process. Nucleotide hydrolysis is not required. Biochemistry 39,6401-6409 (2000).
20. Zhang, Z., Post, C.B. & Smith, D.L. Amide hydrogen exchange determined by mass spectrometry: application to rabbit muscle aldolase. Biochemistry 35,779-791 (1996).
21. Frilander, M. & Bamford, D.H. In vitro packaging of the single-stranded RNA genomic precursors of the segmented double-stranded RNA bacteriophage φ6: the three segments modulate each other's packaging efficiency. J. Mol. Biol. 246,418-428 (1995).
22. Kim, D.E. & Patel, S.S. The kinetic pathway of RNA binding to the Escherichia coli transcription termination factor Rho. J. Biol. Chem. 276,13902-13910 (2001).
23. Ahnert, P., Picha, K.M. & Patel, S.S. A ring-opening mechanism for DNA binding in the central channel of the T7 helicase-primase protein. EMBO J. 19, 3418-3427 (2000).
24. Davey, M.J., Jeruzalmi, D., Kuriyan, J. & O'Donnell, M. Motors and switches: AAA+ machines within the replisome. Nat. Rev. Mol. Cell Biol. 3, 826-835 (2002).
25. Mindich, L. Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage φ6. Microbiol. Mol. Biol. Rev. 63,149-160 (1999).
26. Kainov, D.E., Lisal, J., Bamford, D.H. & Tuma, R. Packaging motor from double-stranded RNA bacteriophage φ12 acts as an obligatory passive conduit during transcription. Nucleic Acids Res. 32, 3515-3521 (2004).
27. Juuti, J.T., Bamford, D.H., Tuma, R. & Thomas, G.J., Jr. Structure and NTPase activity of the RNA-translocating protein (P4) of bacteriophage φ6. J. Mol. Biol. 279,347-359 (1998).
28. Wooll, J.O., Wrabl, J.O. & Hilser, V.J. Ensemble modulation as an origin of denaturant-independent hydrogen exchange in proteins. J. Mol. Biol. 301,247-256 (2000).
29. Hilser, V.J. & Freire, E. Structure-based calculation of the equilibrium folding pathway of proteins. Correlation with hydrogen exchange protection factors. J. Mol. Biol. 262, 756-772 (1996).
30. Hilser, V.J. Modeling the native state ensemble. Methods Mol. Biol. 168, 93-116 (2001).
31. Kainov, D.E., Butcher, S.J., Bamford, D.H. & Tuma, R. Conserved intermediates on the assembly pathway of double-stranded RNA bacteriophages. J. Mol. Biol. 328,791-804 (2003).
32. Lam, T.T. et al. Mapping of protein:protein contact surfaces by hydrogen/deuterium exchange, followed by on-line high-performance liquid chromatography-electrospray ionization Fourier-transform ion-cyclotron-resonance mass analysis. J. Chromatogr. A 982, 85-95 (2002).
33. Emmett, M.R. & Caprioli, R.M. Micro-electrospray mass spectrometry: ultra-high-sensitivity analysis of peptides and proteins. J. Am. Soc. Mass Spectrom. 5, 605-613 (1994).
34. Emmett, M.R., White, F.M., Hendrickson, C.L., Shi, S.D.-H. & Marshall, A.G. Application of micro-electrospray liquid chromatographic techniques to FT-ICR MS to enable high-sensitivity biological analysis. J. Am. Soc. Mass Spectrom. 9, 333-340 (1998).
35. Senko, M.W., Hendrickson, C.L., Emmett, M.R., Shi, S.D.-H. & Marshall, A.G. External accumulation of ions for enhanced electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. J. Am. Soc. Mass Spectrom. 8, 970-976 (1997).
36. Zhang, Z., Li, W., Logan, T.M., Li, M. & Marshall, A.G. Human recombinant [C22A] FK506-binding protein amide hydrogen exchange rates from mass spectrometry match and extend those from NMR. Protein Sci. 6, 2203-2217 (1997).
37. Huang, C.C., Couch, G.S., Pettersen, E.F. & Ferrin, T.E. Chimera: an extensible molecular modeling application constructed using standard components. Pac. Symp. Biocomput. 1, 724-725 (1996).
38. Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (1994).