ABC  Vol.5 No.2 , April 2015
Structural Implications of Universal Complementarities in Translation—High Accuracy at the Decoding Site
Author(s) Kozo Nagano*
ABSTRACT
X-ray structures of transfer RNAs (tRNAs) bound to the whole ribosome do not fully explain the mechanism of translation. The cause of the failure seems to come mainly from a high Mg2+ ion concentration compared to that in the living cells. There exists a wide range of nucleotide sequence conservation in tRNA and ribosomal RNAs (rRNAs) of small and large subunits as well as sequence complementarities, that seems to explain how high accuracy in translation can be achieved at the decoding site. Conformational transition between U33-folded and U33-extended forms of anticodon loops of tRNAs and G-C pair formation and disruption between C1399 and G1504 of 16S rRNA, etc. play the central role in explaining why E-site tRNA can automatically be expelled when an aminoacyl-tRNA at the A site turns out to be cognate.

Cite this paper
Nagano, K. (2015) Structural Implications of Universal Complementarities in Translation—High Accuracy at the Decoding Site. Advances in Biological Chemistry, 5, 151-167. doi: 10.4236/abc.2015.52012.
References
[1]   Yusupov, M.M., et al. (2001) Crystal Structure of the Ribosome at 5.5 A Resolution. Science, 292, 883-896.
http://dx.doi.org/10.1126/science.1060089

[2]   Korosterev, A., Trakhanov, S., Laurberg, M. and Noller, H.F. (2006) Crystal Structure of a 70S Ribosome-tRNA Complex Reveals Functional Interactions and Rearrangements. Cell, 126, 1065-1077.
http://dx.doi.org/10.1016/j.cell.2006.08.032

[3]   Sergiev, P.V., et al. (2005) Function of the Ribosomal E-Site: A Mutagenesis Study. Nucleic Acids Research, 33, 6048-6056.
http://dx.doi.org/10.1093/nar/gki910

[4]   Gutell, R.R. (1993) The Simplicity behind the Elucidation of Complex Structure in Ribosomal RNA. In: Nierhaus, K.H., Franceschi, F., Subramanian, A.R., Erdmann, V.A. and Wittmann-Liebold, B., Eds., The Translational Apparatus, Structure, Function, Regulation, Evolution, Plenum Press, New York, 477-488.

[5]   Brimacombe, R. (1995) The Structure of Ribosomal RNA: A Three-Dimensional Jigsaw Puzzle. European Journal of Biochemistry, 230, 365-383.
http://dx.doi.org/10.1111/j.1432-1033.1995.0365h.x

[6]   Selmer, M., et al. (2006) Structure of the 70S Ribosome Complexed with mRNA and tRNA. Science, 313, 1935-1942.
http://dx.doi.org/10.1126/science.1131127

[7]   Yusupova, G., Jenner, L., Rees, B., Moras, D. and Yusupov, M. (2006) Structural Basis for Messenger RNA Movement on the Ribosome. Nature, 444, 391-394.
http://dx.doi.org/10.1038/nature05281

[8]   Frank, J. and Agrawal, R.K. (2000) A Ratchet-Like Intersubunit Reorganization of the Ribosome during Translocation. Nature, 406, 318-322.
http://dx.doi.org/10.1038/35018597

[9]   Agirrezabala, X., Lei, J., Brunelle, J.L., Ortiz-Meoz, R.F., Green, R. and Frank, J. (2008) Visualization of the Hybrid State of tRNA Binding Promoted by Spontaneous Ratcheting of the Ribosome. Molecular Cell, 32, 190-197.
http://dx.doi.org/10.1016/j.molcel.2008.10.001

[10]   Kim, H.D., Puglisi, J. and Chu, S. (2007) Fluctuations of tRNAs between Classical and Hybrid States. Biophysical Journal, 104, 13661-13665.

[11]   Munro, J.B., Altman, R.B., O’Connor, N. and Blanchard, S.C. (2007) Identification of Two Distinct Hybrid State Intermediates on the Ribosome. Molecular Cell, 25, 505-517.
http://dx.doi.org/10.1016/j.molcel.2007.01.022

[12]   Cornish, P.V., Ermolenko, D.N., Noller, H.F. and Ha, T. (2008) Spontaneous Intersubunit Rotation in Single Ribosomes. Molecular Cell, 30, 578-588.
http://dx.doi.org/10.1016/j.molcel.2008.05.004

[13]   Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M. and Frank, J. (2003) Locking and Unlocking of Ribosomal Motions. Cell, 114, 123-134.
http://dx.doi.org/10.1016/S0092-8674(03)00476-8

[14]   Nagano, K. and Nagano, N. (2007) Mechanism of Translation Based on Intersubunit Complementarities of Ribosomal RNAs and tRNAs. Journal of Theoretical Biology, 245, 644-668.
http://dx.doi.org/10.1016/j.jtbi.2006.11.004

[15]   Lotfield, R.B. and Vanderjagt, D. (1972) The Frequency of Errors in Protein Biosynthesis. Biochemical Journal, 128, 1353-1356.

[16]   Hopfield, J.J. (1974) Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity. Proceedings of the National Academy of Sciences of the United States of America, 71, 4135-4139. http://dx.doi.org/10.1073/pnas.71.10.4135

[17]   Szer, W. and Ochoa, S. (1964) Complexing Ability and Coding Properties of Synthetic Polynucleotides. Journal of Molecular Biology, 8, 823-834.
http://dx.doi.org/10.1016/S0022-2836(64)80163-7

[18]   Thompson, R.C., Dix, D.B., Gerson, R.B. and Karim, A.M. (1981) Effect of Mg2+ Concentration, Polyamines, Streptomycin, and Mutations in Ribosomal Proteins on the Accuracy of the Two-Step Selection of Aminoacyl-tRNAs in Protein Biosynthesis. Journal of Biological Chemistry, 256, 6676-6681.

[19]   Moazed, D. and Noller, H.F. (1974) Interaction of Antibiotics with Functional Sites in 16S Ribosomal RNA. Nature, 327, 389-394.
http://dx.doi.org/10.1038/327389a0

[20]   Egebjerg, J., Larsen, N. and Garrett, R.A. (1990) Structural Map of 23S rRNA. In: Hill, E.E., Dahlberg, A., Garrett, R.A., Moore, P.B., Schlesinger, D. and Warner, J.R., Eds., The Ribosome Structure, Function and Evolution, American Society for Microbiology, Washington DC, 168-179.

[21]   Carter, A.P., Clemons, W.M., Brodersen, D.E., Morgan-Warren, R.J., Wimberly, B.T. and Ramakrishnan, V. (2000) Functional Insights from the Structure of the 30S Ribosomal Subunit and Its Interactions with Antibiotics. Nature, 407, 340-348.
http://dx.doi.org/10.1038/35030019

[22]   Bollen, B., Davies, J., Ozaki, M. and Mizushima, S. (1969) Ribosomal Protein Conferring Sensitivity to the Antibiotic Spectinomycin in Escherichia coli. Science, 165, 85-86.
http://dx.doi.org/10.1126/science.165.3888.85

[23]   Sigmund, C.D., Ettayebi, M. and Morgan, E.A. (1984) Antibiotic Resistance Mutations in 16S and 23S Ribosomal RNA Genes of Escherichia coli. Nucleic Acids Research, 12, 4653-4663.
http://dx.doi.org/10.1093/nar/12.11.4653

[24]   Garcia-Ortega, L., Alvarez-Garcia, E., Gavilanes, J.G., Martinez-del-Pozo, A. and Joseph, S. (2010) Cleavage of the Sarcin-Ricin Loop of 23S rRNA Differentially Affects EF-G and EF-Tu Binding. Nucleic Acids Research, 38, 4108-4119.
http://dx.doi.org/10.1093/nar/gkq151

[25]   Horan, L.H. and Noller, H.F. (2007) Intersubunit Movement Is Required for Ribosomal Translocation. Proceedings of the National Academy of Sciences of the United States of America, 104, 4881-4885.
http://dx.doi.org/10.1073/pnas.0700762104

[26]   Holbrook, S.R., Sussman, J.L., Warrant, R.W. and Kim, S.H. (1978) Crystal Structure of Yeast Phenylalanine Transfer RNA II. Structural Features and Functional Implications. Journal of Molecular Biology, 123, 631-660.

[27]   Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. and Yusupova, G. (2012) A New Understanding of the Decoding Principle on the Ribosome. Nature, 484, 256-259.
http://dx.doi.org/10.1038/nature10913

[28]   Prince, J.B., Taylor, B.H., Thurlow, D.L., Ofengand, J. and Zimmermann, R.A. (1982) Covalent Crosslinking of tRNA1Val to 16S RNA at the Ribosomal P Site: Identification of Crosslinked Residues. Proceedings of the National Academy of Sciences of the United States of America, 79, 5450-5454.
http://dx.doi.org/10.1073/pnas.79.18.5450

[29]   Sprinzl, M., Wagner, T., Lorenz, S. and Erdmann, V.A. (1976) Regions of tRNA Important for Binding to the Ribosomal A and P Sites. Biochemistry, 15, 3031-3039.
http://dx.doi.org/10.1021/bi00659a015

[30]   Spahn, C.M. and Nierhaus, K.H. (1998) Models of the Elongation Cycle: An Evaluation. Biological Chemistry, 379, 753-772.

[31]   Nagano, K. and Nagano, N. (1997) Transfer RNA Docking Pair Model in the Ribosomal Pre- and Post-Translocational States. Nucleic Acids Research, 25, 1254-1264.
http://dx.doi.org/10.1093/nar/25.6.1254

[32]   Ogle, J.M., Brodersen, D.E., Clemons Jr., W.M., Tarry, M.J., Carter, A.P. and Ramakrishnan, V. (2001) Recognition of Cognate Transfer RNA by the 30S Ribosomal Subunit. Science, 292, 897-902.
http://dx.doi.org/10.1126/science.1060612

[33]   Fredrick, K. and Noller, H.F. (2003) Catalysis of Ribosomal Translocation by Sparsomycin. Science, 300, 1159-1162. http://dx.doi.org/10.1126/science.1084571

[34]   Peske, F., Savelsbergh, A., Katunin, V.I., Rodnina, M.V. and Wintermeyer, W. (2004) Conformational Changes of the Small Ribosomal Subunit during Elongation Factor G-Dependent tRNA-mRNA Translocation. Journal of Molecular Biology, 343, 1183-1194.
http://dx.doi.org/10.1016/j.jmb.2004.08.097

[35]   Feinberg, J.S. and Joseph, S. (2001) Identification of Molecular Interactions between P-Site tRNA and the Ribosome Essential for Translocation. Proceedings of the National Academy of Sciences of the United States of America, 98, 11120-11125.
http://dx.doi.org/10.1073/pnas.211184098

[36]   Schmeing, T.M., Voorhees, R.M., Kelley, A.C., Gao, Y.G., Murphy IV, F.V., Weir, J.R. and Ramakrishnan, V. (2009) The Crystal Structure of the Ribosome Bound to EF-Tu and Aminoacyl-tRNA. Science, 326, 688-694.
http://dx.doi.org/10.1126/science.1179700

[37]   Schmeing, T.M., Voorhees, R.M., Kelley, A.C. and Ramakrishnan, V. (2011) How Mutations in tRNA Distant from the Anticodon Affect the Fidelity of Decoding. Nature Structural & Molecular Biology, 18, 432-436.
http://dx.doi.org/10.1038/nsmb.2003

[38]   AEvarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., al-Karadaghi, S., et al. (1994) Three Dimensional Structure of the Ribosomal Translocase: Elongation Factor G from Thermus thermophilus. EMBO Journal, 13, 3669-3677.

[39]   Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C. and Ramakrishnan, V. (2009) The Structure of the Ribosome with Elongation Factor G Trapped in the Posttranslocational State. Science, 326, 694-699.
http://dx.doi.org/10.1126/science.1179709

[40]   Kisselev, L.L. and Buckingham, R.H. (2000) Translational Termination Comes of Age. Trends in Biochemical Sciences, 25, 561-566.
http://dx.doi.org/10.1016/S0968-0004(00)01669-8

[41]   Ito, K., Uno, M. and Nakamura, Y. (2000) A Tripeptide “Anticodon” Deciphers Stop in Messenger RNA. Nature, 403, 680-684.

[42]   Rawat, U.B., Zavialov, A.V., Sengupta, J., Valle, M., Grassucci, R.A., Linde, J., et al. (2003) A Cryo-Electron Microscopic Study of Ribosome-Bound Termination Factor RF2. Nature, 421, 87-90.
http://dx.doi.org/10.1038/nature01224

[43]   Klaholz, B.P., Pape, T., Zavialov, A.V., Myasnikov, A.G., Orlova, E.V., Vestergaard, B., et al. (2003) Structure of the Escherichia coli Ribosomal Termination Complex with Release Factor 2. Nature, 421, 90-94.
http://dx.doi.org/10.1038/nature01225

[44]   Song, H., Mugnier, P., Das, A.K., Webb, H.M., Evans, D.R., Tuite, M.F., et al. (2000) The Crystal Structure of Human Eukaryotic Release Factor eRF1-Mechanism of Stop Codon Recognition and Peptidyl-tRNA Hydrolysis. Cell, 100, 311-321.
http://dx.doi.org/10.1016/S0092-8674(00)80667-4

[45]   Osawa, S., Jukes, T.H., Watanabe, K. and Muto, A. (1992) Recent Evidence for Evolution of the Genetic Code. Microbiological Reviews, 56, 229-264.

[46]   Nierhaus, K.H. (1990) The Allosteric Three-Site Model for the Ribosomal Elongation Cycle: Features and Future. Biochemistry, 29, 4997-5008.
http://dx.doi.org/10.1021/bi00473a001

[47]   Di Giacco, V., Marquez, Y., Qin, Y., Pech, M., Triana-Alonso, F.J., Wilson, D.N. and Nierhaus, K.H. (2011) Shine-Dalgarno Interaction Prevents Incorporation of Noncognate Amino Acids at Codon Following the AUG. Proceedings of the National Academy of Sciences of the United States of America, 108, 16980-16985.

[48]   Geigenmüller, U. and Nierhaus, K.H. (1990) Significance of the Third tRNA Binding Site, the E-Site, on E. coli Ribosomes for the Accuracy of Translation: An Occupied E-Site Prevents the Binding of Non-Cognate Amino-acyl-tRNA to the A-Site. EMBO Journal, 9, 4527-4533.

[49]   Schilling-Bartetzko, S., Bartetzko, A. and Nierhaus, K.H. (1992) Kinetic and Thermodynamic Parameters for tRNA Binding to the Ribosome and for the Translocation Reaction. Journal of Biological Chemistry, 267, 4703-4712.

[50]   Nierhaus, K.H. (2006) Decoding Errors and the Involvement of the E-Site. Biochimie, 88, 1013-1019.
http://dx.doi.org/10.1016/j.biochi.2006.02.009

[51]   Semenkov, Y.P., Rodnina, M.V. and Wintermeyer, W. (1996) The “Allosteric Three-Site Model” of Elongation Cannot Be Confirmed in a Well-Defined Ribosome System from Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 93, 12183-12188.
http://dx.doi.org/10.1073/pnas.93.22.12183

[52]   Uemura, S., Aitken, C.E., Korlach, J., Flusberg, B.A., Turner, S.W. and Puglisi, J.D. (2010) Real-Time tRNA Transit on Single Translating Ribosomes at Codon Resolution. Nature, 464, 1012-1017.
http://dx.doi.org/10.1038/nature08925

[53]   Chen, C., Stevens, B., Kaur, J., Smilansky, Z., Cooperman, B.S. and Goldman, Y.E. (2011) Allosteric vs. Spontaneous Exit-Site (E-Site) tRNA Dissociation Early in Protein Synthesis. Proceedings of the National Academy of Sciences of the United States of America, 108, 16980-16985.
http://dx.doi.org/10.1073/pnas.1106999108

[54]   Petropoulos, A.D. and Green, R. (2012) Further in Vitro Exploration Fails to Support the Allosteric Three-Site Model. Journal of Biological Chemistry, 287, 11642-11648.
http://dx.doi.org/10.1074/jbc.C111.330068

[55]   Liao, P.Y., Gupta, P., Petrov, A.N., Dinman, J.D. and Lee, K.H. (2008) A New Kinetic Model Reveals the Synergistic Effect of E-, P- and A-Sites on +1 Ribosomal Frameshifting. Nucleic Acids Research, 36, 2619-2629.
http://dx.doi.org/10.1093/nar/gkn100

[56]   Sundararajan, A., Michaud, W.A., Qian, Q., Stahl, G. and Farabaugh, P.J. (1999) Near-Cognate Peptidyl-tRNAs Promote +1 Programmed Translational Frameshifting in Yeast. Molecular Cell, 4, 1005-1015.
http://dx.doi.org/10.1016/S1097-2765(00)80229-4

[57]   Bartetzko, A. and Nierhaus, K.H. (1988) Mg2+/NH4+/Polyamine System for Polyuridine-Dependent Polyphenylalanine Synthesis with Near in Vivo Characteristics. Methods in Enzymology, 164, 650-658.
http://dx.doi.org/10.1016/S0076-6879(88)64075-4

[58]   Bernstein, H.J. (2000) Recent Changes of RasMol, Recombining the Variants. Trends in Biochemical Sciences, 25, 453-455.
http://dx.doi.org/10.1016/S0968-0004(00)01606-6

 
 
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