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Simulating activity of the bacterial ribosome

Published online by Cambridge University Press:  10 May 2010

Joanna Trylska
Joanna Trylska*
Affiliation:
Interdisciplinary Centre for Mathematical and Computational Modelling, University of Warsaw, Warsaw, Poland
*
*Author for correspondence: J. Trylska, Interdisciplinary Centre for Mathematical and Computational Modelling, University of Warsaw, Zwirki i Wigury 93, 02-089Warsaw, Poland. Tel.: 48-22-5540-843; Fax: 48-22-5540-801; Email: joanna@icm.edu.pl
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Abstract

Computational modeling studies that investigate activity of the bacterial ribosome were reviewed. Computational approaches became possible with the availability of three-dimensional atomic resolution structures of the ribosomal subunits. However, due to the enormous size of the system, theoretical efforts to study the ribosome are few and challenging. For example, to extend the simulation timescales to biologically relevant ones, often, reduced models that require tedious parameterizations need to be applied. To that end, modeling of the ribosome focused on its internal dynamics, electrostatic properties, inhibition by antibiotics, polypeptide folding in the ribosome tunnel and assembly mechanisms driving the formation of the small ribosomal subunit.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 42 , Issue 4 , November 2009 , pp. 301 - 316
Copyright
Copyright © Cambridge University Press 2010

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References

9. References

Aleksandrov, A. & Simonson, T. (2008). Molecular dynamics simulations of the 30S ribosomal subunit reveal a preferred tetracycline binding site. Journal of the American Chemical Society 130, 1114–1115.Google Scholar
Baker, N. A. (2004). Poisson–Boltzmann methods for biomolecular electrostatics. Numerical Computer Methods, Pt D 383, 94–118.Google Scholar
Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. (2001). Electrostatics of nanosystems: application to microtubules and the ribosome. Proceedings of the National Academy of Sciences USA 98, 10037–10041.Google Scholar
Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. (2000). The complete atomic structure of the large ribosomal subunit at 2·4 angstrom resolution. Science 289, 905–920.Google Scholar
Bashan, A. & Yonath, A. (2008). Correlating ribosome function with high-resolution structures. Trends in Microbiology 16, 326–335.Google Scholar
Bernstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, E. F., Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). Protein Data Bank – Computer-based archival file for macromolecular structures. Journal of Molecular Biology 112, 535–542.Google Scholar
Borovinskaya, M. A., Shoji, S., Fredrick, K. & Cate, J. H. D. (2008). Structural basis for hygromycin B inhibition of protein biosynthesis. RNA 14, 1590–1599.Google Scholar
Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T. & Ramakrishnan, V. (2000). Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407, 340–348.Google Scholar
Chacon, P., Tama, F. & Wriggers, W. (2003). Mega-Dalton biomolecular motion captured from electron microscopy reconstructions. Journal of Molecular Biology 326, 485–492.CrossRefGoogle ScholarPubMed
Dlugosz, M. & Trylska, J. (2009). Aminoglycoside association pathways with the 30S ribosomal subunit. Journal of Physical Chemistry B 113, 7322–7330.Google Scholar
Elcock, A. H. (2006). Molecular Simulations of cotranslational protein folding: fragment stabilities, folding cooperativity, and trapping in the ribosome. Plos Computational Biology 2, 824–841.CrossRefGoogle ScholarPubMed
Frank, J. (2003). Electron microscopy of functional ribosome complexes. Biopolymers 68, 223–233.Google Scholar
Frank, J. & Agrawal, R. K. (2000). A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318–322.Google Scholar
Gabashvili, I. S., Agrawal, R. K., Grassucci, R., Squires, C. L., Dahlberg, A. E. & Frank, J. (1999). Major rearrangements in the 70S ribosomal 3D structure caused by a conformational switch in 16S ribosomal RNA. EMBO Journal 18, 6501–6507.Google Scholar
Gavrilova, L. P., Kostiashkina, O. E., Koteliansky, V. E., Rutkevitch, N. M. & Spirin, A. S. (1976). Factor-free (non-enzymic) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. Journal of Molecular Biology 101, 537–552.Google Scholar
Go, N. (1983). Theoretical-studies of protein folding. Annual Review of Biophysics and Bioengineering 12, 183–210.Google Scholar
Hamacher, K., Trylska, J. & McCammon, J. A. (2006). Dependency map of proteins in the small ribosomal subunit. Plos Computational Biology 2, 80–87.Google Scholar
Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F. & Yonath, A. (2001). High resolution structure of the large ribosomal subunit from a mesophilic Eubacterium. Cell 107, 679–688.CrossRefGoogle ScholarPubMed
Held, W. A., Ballou, B., Mizushim, S. & Nomura, M. (1974). Assembly mapping of 30 S ribosomal-proteins from Escherichia coli – further studies. Journal of Biological Chemistry 249, 3103–3111.Google Scholar
Hermann, T. (2005). Drugs targeting the ribosome. Current Opinion in Structural Biology 15, 355–366.Google Scholar
Honig, B. & Nicholls, A. (1995). Classical electrostatics in biology and chemistry. Science 268, 1144–1149.CrossRefGoogle ScholarPubMed
Humphrey, W., Dalke, A. & Schulten, K. (1996). VMD: visual molecular dynamics. Journal of Molecular Graphics 14, 33–38.Google Scholar
Ishida, H. & Hayward, S. (2008). Path of nascent polypeptide in exit tunnel revealed by molecular dynamics simulation of ribosome. Biophysical Journal 95, 5962–5973.Google Scholar
Jenni, S. & Ban, N. (2003). The chemistry of protein synthesis and voyage through the ribosomal tunnel. Current Opinion in Structural Biology 13, 212–219.Google Scholar
Kirmizialtin, S., Ganesan, V. & Makarov, D. E. (2004). Translocation of a beta-hairpin-forming peptide through a cylindrical tunnel. Journal of Chemical Physics 121, 10268–10277.Google Scholar
Klein, D. J., Moore, P. B. & Steitz, T. A. (2004). The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. Journal of Molecular Biology 340, 141–177.Google Scholar
Korostelev, A., Ermolenko, D. N. & Noller, H. F. (2008). Structural dynamics of the ribosome. Current Opinion in Chemical Biology 12, 674–683.Google Scholar
Kurkcuoglu, O., Doruker, P., Sen, T. Z., Kloczkowski, A. & Jernigan, R. L. (2008). The ribosome structure controls and directs mRNA entry, translocation and exit dynamics. Physical Biology 5, 46005.Google Scholar
Kurkcuoglu, O., Kurkcuoglu, Z., Doruker, P. & Jernigan, R. L. (2009). Collective dynamics of the ribosomal tunnel revealed by elastic network modeling. Proteins 75, 837–845.Google Scholar
Liljas, A. (2004). Structural Aspects of Protein Synthesis. Singapore: World Scientific Publishing Co. Pte. Ltd.Google Scholar
Lu, J. L. & Deutsch, C. (2005). Folding zones inside the ribosomal exit tunnel. Nature Structural & Molecular Biology 12, 1123–1129.Google Scholar
Ma, C. S., Baker, N. A., Joseph, S. & Mccammon, J. A. (2002). Binding of aminoglycoside antibiotics to the small ribosomal subunit: a continuum electrostatics investigation. Journal of the American Chemical Society 124, 1438–1442.Google Scholar
Malhotra, A., Tan, R. K. Z. & Harvey, S. C. (1994). Modeling large RNAs and ribonucleoprotein-particles using molecular mechanics techniques. Biophysical Journal 66, 1777–1795.Google Scholar
Meroueh, S. O. & Mobashery, S. (2007). Conformational transition in the aminoacyl t-RNA site of the bacterial ribosome both in the presence and absence of an aminoglycoside antibiotic. Chemical Biology & Drug Design 69, 291–297.Google Scholar
Mitra, K., Schaffitzel, C., Fabiola, F., Chapman, M. S., Ban, N. & Frank, J. (2006). Elongation arrest by SecM via a cascade of ribosomal RNA rearrangements. Molecular Cell 22, 533–543.Google Scholar
Munro, J. B., Vaiana, A., Sanbonmatsu, K. Y. & Blanchard, S. C. (2008). A new view of protein synthesis: mapping the free energy landscape of the ribosome using single-molecule FRET. Biopolymers 89, 565–577.Google Scholar
Nakatogawa, H. & Ito, K. (2002). The ribosomal exit tunnel functions as a discriminating gate. Cell 108, 629–636.Google Scholar
Poehlsgaard, J. & Douthwaite, S. (2005). The bacterial ribosome as a target for antibiotics. Nature Reviews Microbiology 3, 870–881.Google Scholar
Powers, T., Daubresse, G. & Noller, H. F. (1993). Dynamics of in-vitro assembly of 16-S ribosomal-RNA into 30-S ribosomal-subunits. Journal of Molecular Biology 232, 362–374.Google Scholar
Qin, S. B. & Zhou, H. X. (2009). Dissection of the high rate constant for the binding of a ribotoxin to the ribosome. Proceedings of the National Academy of Sciences USA 106, 6974–6979.Google Scholar
Qizhi Cui, R. Z-K. Tan, Harvey, S. C. & Case, D. A. (2006). Low-resolution molecular dynamics simulations of the 30S ribosomal subunit. Multiscale Modeling and Simulation 5, 1248–1263.Google Scholar
Reblova, K., Lankas, F., Razga, F., Krasovska, M. V., Koca, J. & Sponer, J. (2006). Structure, dynamics, and elasticity of free 16S rRNA helix 44 studied by molecular dynamics simulations. Biopolymers 82, 504–520.Google Scholar
Rodnina, M. V., Beringer, M. & Wintermeyer, W. (2006). Mechanism of peptide bond formation on the ribosome. Quarterly Reviews of Biophysics 39, 203–225.Google Scholar
Romanowska, J., Setny, P. & Trylska, J. (2008). Molecular dynamics study of the ribosomal A-site. Journal of Physical Chemistry B 112, 15227–15243.Google Scholar
Sanbonmatsu, K. Y. (2006). Energy landscape of the ribosomal decoding center. Biochimie 88, 1053–1059.Google Scholar
Sanbonmatsu, K. Y., Joseph, S. & Tung, C. S. (2005). Simulating movement of tRNA into the ribosome during decoding. Proceedings of the National Academy of Sciences USA 102, 15854–15859.Google Scholar
Sanbonmatsu, K. Y. & Tung, C. S. (2007). High performance computing in biology: multimillion atom simulations of nanoscale systems. Journal of Structural Biology 157, 470–480.Google Scholar
Schlick, T. (2002). Molecular Modeling and Simulation, Springer-Verlag.Google Scholar
Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F. & Yonath, A. (2000). Structure of functionally activated small ribosomal subunit at 3·3 angstrom resolution. Cell 102, 615–623.Google Scholar
Southworth, D. R., Brunelle, J. L. & Green, R. (2002). EFG-independent translocation of the mRNA: tRNA complex is promoted by modification of the ribosome with thiol-specific reagents. Journal of Molecular Biology 324, 611–623.Google Scholar
Stagg, S. M., Mears, J. A. & Harvey, S. C. (2003). A structural model for the assembly of the 30 S subunit of the ribosome. Journal of Molecular Biology 328, 49–61.Google Scholar
Talkington, M. W. T., Siuzdak, G. & Williamson, J. R. (2005). An assembly landscape for the 30S ribosomal subunit. Nature 438, 628–632.Google Scholar
Tama, F., Valle, M., Frank, J. & Brooks, C. L. (2003). Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy. Proceedings of the National Academy of Sciences USA 100, 9319–9323.Google Scholar
Tenson, T. & Ehrenberg, M. (2002). Regulatory nascent peptides in the ribosomal tunnel. Cell 108, 591–594.Google Scholar
Trylska, J., Konecny, R., Tama, F., Brooks, C. L. & McCammon, J. A. (2004). Ribosome motions modulate electrostatic properties. Biopolymers 74, 423–431.Google Scholar
Trylska, J., McCammon, J. A. & Brooks, C. L. (2005a). Exploring assembly energetics of the 30S ribosomal subunit using an implicit solvent approach. Journal of the American Chemical Society 127, 11125–11133.Google Scholar
Trylska, J., Tozzini, V. & McCammon, J. A. (2005b). Exploring global motions and correlations in the ribosome. Biophysical Journal 89, 1455–1463.Google Scholar
Tung, C. S. & Sanbonmatsu, K. Y. (2004). Atomic model of the Thermus thermophilus 70S ribosome developed in silico. Biophysical Journal 87, 2714–2722.Google Scholar
Vaiana, A. C. & Sanbonmatsu, K. Y. (2009). Stochastic gating and drug-ribosome interactions. Journal of Molecular Biology 386, 648–661.Google Scholar
Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M. & Frank, J. (2003). Locking and unlocking of ribosomal motions. Cell 114, 123–134.CrossRefGoogle ScholarPubMed
Voss, N. R., Gerstein, M., Steitz, T. A. & Moore, P. B. (2006). The geometry of the ribosomal polypeptide exit tunnel. Journal of Molecular Biology 360, 893–906.CrossRefGoogle ScholarPubMed
Wang, Y. M., Rader, A. J., Bahar, I. & Jernigan, R. L. (2004). Global ribosome motions revealed with elastic network model. Journal of Structural Biology 147, 302–314.Google Scholar
Williamson, J. R. (2008). Biophysical studies of bacterial ribosome assembly. Current Opinion in Structural Biology 18, 299–304.Google Scholar
Wilson, D. N. & Nierhaus, K. H. (2003). The ribosome through the looking glass. Angewandte Chemie-International Edition 42, 3464–3486.Google Scholar
Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T. & Ramakrishnan, V. (2000). Structure of the 30S ribosomal subunit. Nature 407, 327–339.Google Scholar
Yan, A. M., Wang, Y. M., Kloczkowski, A. & Jernigan, R. L. (2008). Effects of protein subunits removal on the computed motions of partial 30S structures of the ribosome. Journal of Chemical Theory and Computation 4, 1757–1767.Google Scholar
Yang, G., Trylska, J., Tor, Y. & McCammon, J. A. (2006). Binding of aminoglycosidic antibiotics to the oligonucleotide A-site model and 30S ribosomal subunit: Poisson–Boltzmann model, thermal denaturation, and fluorescence studies. Journal of Medicinal Chemistry 49, 5478–5490.Google Scholar
Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H. D. & Noller, H. F. (2001). Crystal structure of the ribosome at 5·5 angstrom resolution. Science 292, 883–896.Google Scholar
Ziv, G., Haran, G. & Thirumalai, D. (2005). Ribosome exit tunnel can entropically stabilize alpha-helices. Proceedings of the National Academy of Sciences USA 102, 18956–18961.Google Scholar