Experimental and computational analysis of translation products in apomyoglobin expression

Journal of Molecular Biology

Volumn 357, Issue 4, 2006, Pages 1121-1143

  Jungbauer, Lisa M ^a   Bakke, Courtney K ^a   Cavagnero, Silvia ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cell free expression; E. coli; Elongation; Incomplete translation; Kinetics

Indexed keywords

APOMYOGLOBIN; POLYPEPTIDE;

ALGORITHM; AMINOACYLATION; ANALYSIS; ARTICLE; AUTORADIOGRAPHY; BLOTTING; CODON USAGE; DATA ANALYSIS; ESCHERICHIA COLI; EXPERIMENTATION; KINETICS; MASS SPECTROMETRY; MATHEMATICAL COMPUTING; MODEL; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RESIDUE ANALYSIS; RNA TRANSLATION;

ESCHERICHIA COLI;

EID: 33644818408     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.012     Document Type: Article

References (103)

1. W.J. Netzer, and F.U. Hartl Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms Trends Biochem. Sci. 23 1998 68 73
2. A.N. Fedorov, and T.O. Baldwin Protein folding and assembly in a cell-free expression system Methods Enzymol. 290 1998 1 17
3. C.O. Gualerzi, and C.L. Pon Initiation of mRNA translation in prokaryotes Biochemistry 29 1990 5881 5889
4. M. Jaquet, and A. Kepes Initiation, elongation and inactivation of lac messenger rna in Escherichia coli studied by measurement of its beta-galactosidase synthesising capacity in vivo J. Mol. Biol. 60 1971 453 472
5. C.L. Pon, and C.O. Gualerzi Mechanism of protein biosynthesis in prokaryotic cells: effect of initiation factor if1 on the initial rate of 30S initiation complex formation FEBS Letters 175 1984 203 207
6. J. Tomsic, L.A. Vitali, T. Daviter, A. Savelsbergh, R. Spurio, and P. Striebeck Late events of translation initiation in bacteria: a kinetic analysis EMBO J. 19 2000 2127 2136
7. M. Kozak Initiation of translation in prokaryotes and eukaryotes Gene 234 1999 187 208
8. W. Wintermeyer, F. Peske, M. Beringer, K.B. Gromadski, A. Savelsbergh, and M.V. Rodnina Mechanisms of elongation on the ribosome: dynamics of a macromolecular machine Biochem. Soc. Trans. 32 2004 733 737
9. K.B. Gromadski, H.-J. Wieden, and M.V. Rodnina Kinetic mechanism of elongation factor Ts-catalyzed nucleotide exchange in elongation factor Tu Biochemistry 41 2002 162 169
10. T. Pape, W. Wintermeyer, and M. Rodnina Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the a site of the E. coli ribosome EMBO J. 17 1998 7490 7497
11. A. Savelsbergh, V.I. Katunin, D. Mohr, F. Peske, M.V. Rodnina, and W. Wintermeyer An elongation factor G-induced ribosome rearrangement precedes tRNA-mRNA translocation Mol. Cell. 11 2003 1517 1523
12. Y.P. Semenkov, M.V. Rodnina, and W. Wintermeyer Energetic contribution of trna hybrid state formation to translocation catalysis on the ribosome Nature Struct. Biol. 7 2000 1027 1031
13. M.V. Rodnina, H. Stark, A. Savelsbergh, H.-J. Wieden, D. Mohr, and N.B. Matassova GTPase mechanisms and functions of translation factors on the ribosome Biol. Chem. 381 2000 377 387
14. K.B. Gromadski, and M.V. Rodnina Kinetic determinants of high-fidelity tRNA discrimination on the ribosome Mol. Cell. 13 2004 191 200
15. T. Pape, W. Wintermeyer, and M. Rodnina Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome EMBO J. 18 1999 3800 3807
16. M.V. Rodnina, and W. Wintermeyer Ribosome fidelity: tRNA discrimination, proofreading and induced fit Trends Biochem. Sci. 26 2001 124 130
17. R. Karimi, M.Y. Pavlov, R.H. Buckingham, and M. Ehrenberg Novel roles for classical factors at the interface between translation termination and initiation Mol. Cell. 3 1999 601 609
18. D.V. Freistroffer, M. Kwiatkowski, R.H. Buckingham, and M. Ehrenberg The accuracy of codon recognition by polypeptide release factors Proc. Natl Acad. Sci. USA 97 2000 2046 2051
19. D.V. Freistroffer, M.Y. Pavlov, J. Macdougall, R.H. Buckingham, and M. Ehrenberg Release factor rf3 in E. coli accelerates the dissociation of release factors rf1 and rf2 from the ribosome in a GTP-dependent manner EMBO J. 16 1997 4126 4133
20. S.C. Blanchard, R.L. Gonzales, H.D. Kim, S. Chu, and J.D. Puglisi tRNA selection and kinetic proofreading in translation Nature Struct. Mol. Biol. 11 2004 1008 1014
21. M.A. Sorensen, C.G. Kurland, and S. Pedersen Codon usage determines translation rate in Escherichia coli J. Mol. Biol. 207 1989 365 377
22. M.A. Sorensen, and S. Pedersen Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons gaa and gag are translated with a threefold difference in rate J. Mol. Biol. 222 1991 265 280
23. B. Irwin, J.D. Heck, and G.W. Hatfield Codon pair utilization biases influence translational elongation step times J. Biol. Chem. 270 1995 22801 22806
24. E.G. Shpaer Constraints on codon context in Escherichia coli genes. Their possible role in modulating the efficiency of translation J. Mol. Biol. 188 1986 555 564
25. M. Yarus, and L.S. Folley Sense codons are found in specific contexts J. Mol. Biol. 182 1985 529 540
26. H. Dong, L. Nilsson, and C.G. Kurland Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates J. Mol. Biol. 260 1996 649 663
27. T. Ikemura Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system J. Mol. Biol. 151 1981 389 409
28. C.G. Kurland Codon bias and gene expression FEBS Letters 285 1991 165 169
29. M. Gouy, and C. Gautier Codon usage in bacteria: correlation with gene expressivity Nucl. Acids Res. 10 1982 7055 7074
30. J.F. Kane Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli Curr. Opin. Biotechnol. 6 1995 494 500
31. M.H.D. Smit, and J.V. Duin Control of translation by mrna secondary structure in Escherichia coli J. Mol. Biol. 244 1994 144 150
32. C.R. Wood, M.A. Boss, T.P. Patel, and J.S. Emtage The influence of messenger RNA secondary structure on expression of an immunoglobulin heavy chain in Escherichia coli Nucl. Acids Res. 12 1984 3937 3950
33. H.R. Drew, D. Lewy, J. Conaty, K.N. Rand, P. Hendry, and T. Lockett RNA hairpin loops repress protein synthesis more strongly than hammerhead ribozymes Eur. J. Biochem. 266 1999 260 273
34. W.G. Chaney, and A.J. Morris Nonuniform size distribution of nascent peptides: the effect of messenger RNA structure upon the rate of translation Arch. Biochem. Biophys. 194 1979 283 291
35. P. Somogyi, A.J. Jenner, I. Brierley, and S.C. Inglis Ribosomal pausing during translation of an RNA pseudoknot Mol. Cell. Biol. 13 1993 6931 6940
36. P.C. Jelenc, and C.G. Kurland Nucleoside triphosphate regeneration decreases the frequency of translation errors Proc. Natl Acad. Sci. USA 76 1979 3174 3178
37. I. Pettersson, and C.G. Kurland Ribosomal protein l7/l12 is required for optimal translation Proc. Natl Acad. Sci. USA 77 1980 4007 4010
38. L. Jermutus, L.A. Ryabova, and A. Pluckthun Recent advances in producing and selecting functional proteins by using cell-free translation Curr. Opin. Biotechnol. 9 1998 534 548
39. Ambuel, Y., Oosbree, T. R. V., Mccormick, M. R. & Mierendorf, R. C. (2002). E. coli extract for protein synthesis. In US Patent and Trademark Office, United States.
40. D.-M. Kim, and J.R. Swartz Prolonging cell-free protein synthesis by selective reagent additions Biotechnol. Prog. 16 2000 385 390
41. L. Gerstenfeld, J.C. Beldekas, C. Franzblau, and G.E. Sonenshein Cell-free translation of calf type iii collagen: effect of magnesium on ribosome movement during elongation J. Biol. Chem. 258 1963 12058 12063
42. A.K. Abraham, and A. Pihl Variable rate of polypeptide chain elongation in vitro Eur. J. Biochem. 106 1980 257 262
43. P. Ortoleva, E. Berry, Y. Brun, J. Fan, M. Fontus, and K. Hubbard The karyote physico-chemical genomic, proteomic, metabolic cell modeling system OMICS A Journal of Integr. Biol. 7 2003 269 283
44. M. Tomita Whole-cell simulation: a grand challenge of the 21st century Trends Biotechnol. 19 2001 210
45. S. Lee, and J. Bailey Analysis of growth rate effects on productivity of recombinant Escherichia coli populations using molecular mechanics models Biotech. Bioeng. 79 2002 550 557
46. E.L. Weitzke, and P.J. Ortoleva Simulating cellular dynamics through a coupled transcription, translation, metabolic model Comput. Biol. Chem. 27 2003 469 480
47. M. Gouy, and R. Grantham Polypeptide elongation and tRNA cycling in Escherichia coli: a dynamic approach FEBS Letters 115 1980 151 155
48. L.B. Shaw, R.K.P. Zia, and K.H. Lee Totally asymmetric exclusion process with extended objects: a model for protein synthesis Phys. Rev. E 68 2003 021910 (1-17)
49. X. Xia How optimized is the translational machinery in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae Genetics 149 1998 37 44
50. C. Kurland, and M. Ehrenberg Growth-optimizing accuracy of gene expression Annu. Rev. Biophys. Biophys. Chem. 16 1987 291 317
51. O. Elf, O. Berg, and M. Ehrenberg Conmparison of repressor and transcriptional attenuator systems for control of amino acid biosynthetic operons J. Mol. Biol. 313 2001 941 954
52. F. Jorgensen, and C.G. Kurland Processivity errors of gene expression in Escherichia coli J. Mol. Biol. 215 1990 511 521
53. V. Ramachandiran, G. Kramer, and B. Hardesty Expression of different coding sequences in cell-free bacterial and eukaryotic systems indicates translational pausing on Escherichia coli ribosomes FEBS Letters 482 2000 185 188
54. S. Varenne, J. Buc, R. Lloubes, and C. Lazdunski Translation is a non-uniform process: effect of tRNA availability on the rate of elongation of nascent polypeptide chains J. Mol. Biol. 180 1984 549 576
55. J.L. Manley Synthesis and degradation of termination and premature-termination fragments of beta-galactosidase in vitro and in vivo J. Mol. Biol. 125 1978 407 432
56. C. Kurland, and J. Gallant Errors of heterologous protein expression Curr. Opin. Biotechnol. 7 1996 489 493
57. J. Parker Variations in reading the genetic code D.L. Hatfield B.J. Lee R.M. Pirtle Transfer RNA in Protein Synthesis 1992 CRC Press Boca Raton, FL 191 267
58. J.R. Menninger Peptidyl transfer RNA dissociates during protein synthesis from ribosomes of Escherichia coli J. Biol. Chem. 251 1976 3392 3398
59. M. Dreyfus, and S. Joyce The interplay between translation and mRNA decay in prokaryotes: a discussion on current paradigms J. Lapointe L. Brakier-Gingras Translation Mechanisms 2003 Kluwer Academic/Plenum Publishers New York 165 183
60. B.A. Springer, and S.G. Sligar High-level expression of sperm whale myoglobin in Escherichia coli Proc. Natl Acad. Sci. USA 84 1987 8961 8965
61. G. Kramer, V. Ramachandiran, and B. Hardesty Cotranslational incorporation of chemically modified initiator tRNA Recent Res. Devel. Anal. Biochem. 1 2001 39 48
62. A.E. Johnson, W.R. Woodward, E. Herbert, and J.R. Menninger N-e-acetyllysine transfer ribonucleic acid: a biologically active analogue of aminoacyl transfer ribonucleic acids Biochemistry 15 1976 569 575
63. V. Ramachandiran, C. Willms, G. Kramer, and B. Hardesty Fluorophores at the N-terminus of nascent chloramphenicol acetyltransferase peptides affect translation and movement through the ribosome J. Biol. Chem. 275 2000 1781 1786
64. Nakamura, Y., Gojobori, T. & Ikemura, T. (2000). Codon usage tabulated from international DNA sequence databases; status for the year 2000. Nucl. Acids Res., 28, 292.
65. I. Iost, J. Guillerez, and M. Dreyfus Bacteriophage T7 RNA polymerase travels far ahead of ribosomes in vivo J. Bacteriol. 174 1992 619 622
66. A.A. Komar, T. Lesnik, and C. Reiss Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation FEBS Letters 462 1999 387 391
67. M. Ibba, and D. Soll Aminoacyl-tRNA synthesis Annu. Rev. Biochem. 69 2000 617 650
68. E.A. First Catalysis of tRNA aminoacylation by class i and class ii aminoacyl-tRNA synthetases M. Sinnott Comprehensive Biological Catalysis vol. I 1998 Academic Press Ltd San Diego 573 607
69. T.L. Calderone, R.D. Stevens, and T.G. Oas High-level misincorporation of lysine for arginine at aga codons in a fusion protein expressed in Escherichia coli J. Mol. Biol. 262 1996 311 322
70. Kim, D.-M. & Swartz, J. R. (1999). Prolonging cell-free protein synthesis with a novel ATP regeneration system. Biotechnol. Bioeng. 66, 180-188.
71. T. Kigawa, T. Yabuki, Y. Yoshida, M. Tsutsui, Y. Ito, T. Shibata, and S. Yokoyama Cell-free production and stable-isotope labeling of milligram quantities of proteins FEBS Letters 442 1999 15 19
72. D.-M. Kim, and C.-Y. Choi A semicontinuous prokaryotic coupled transcription/translation system using a dialysis membrane Biotechnol. Prog. 12 1996 645 649
73. A.S. Spirin High-throughput cell-free systems for synthesis of functionally active proteins Trends Biotechnol. 22 2004 538 545
74. M. Grunberg-Manago Messenger RNA stability and its role in control of gene expression in bacteria and phages Annu. Rev. Genet. 33 1999 193 227
75. S. Boycheva, G. Chkodrov, and I. Ivanov Codon pairs in the genome of Escherichia coli Bioinformatics 19 2003 987 998
76. L. Cheng, and E. Goldman Absence of effect of varying thr-leu codon pairs on protein synthesis in a T7 system Biochemistry 40 2001 6102 6106
77. T. Tsalkova, G. Kramer, and B. Hardesty The effect of a hydrophobic N-terminal probe on translational pausing of chloramphenicol acetyl transferase and rhodanese J. Mol. Biol. 286 1999 71 81
78. C.C. Chow, C. Chow, V. Raghunathan, T.J. Huppert, E.B. Kimball, and S. Cavagnero Chain length dependence of apomyoglobin folding: structural evolution from misfolded sheets to native helices Biochemistry 42 2003 7090 7099
79. R.F. Gesteland Unfolding of Escherichia coli ribosomes by removal of magnesium J. Mol. Biol. 18 1966 356 371
80. W.J. Netzer, and F.U. Hartl Recombination of protein domains facilitated by co-translational folding in eukaryotes Nature 388 1997 343 349
81. A.V. Nicola, W. Chen, and A. Helenius Co-translational folding of an alphavirus capsid protein in the cytosol of living cells Nature Cell Biol. 1 1999 341 345
82. S.A. Lesley Preparation and use of E. coli D-30 extracts M.J. Tymms Methods in Molecular Biology: In vitro Transcription and Translation Protocols vol. 37 1995 Humana Press Inc. Totowa 265 278
83. H. Schagger, and G. Vonjagow Tricine-sodium dodecyl sulfate- polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa Anal. Biochem. 166 1987 368 379
84. F.C. Neidhardt F.C. Neidhardt R.C. Iii J. Ingraham E. Lin Jr KL M. Magasanik W. Reznikoff M. Riley M. Schaechter H. Umbarger 2nd edit. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology vol. 1 1996 ASM Press Washington, DC
85. B.J.S. Efiok, and E.E. Eduok Basic Calculations for Chemical and Biological Analysis 2nd edit. 2000 AOAC International Gaithersburg, MD, pp. 200
86. N. Ban, P. Nissen, J. Hansen, P.B. Moore, and T.A. Steitz The complete atomic structure of the large ribosomal subunit at 2.4 angstrom resolution Science 289 2000 905 920
87. A. Spirin Ribosomal RNA P. Siekevitz Cellular Organelles 1999 Kluwer Academic/Plenum Publishers New York, NY
88. V. Ramachandiran, G. Kramer, P.M. Horowitz, and B. Hardesty Single synonymous codon substitution eliminates pausing during chloramphenicol acetyltransferase synthesis on Escherichia coli ribosomes in vitro FEBS Letters 512 2002 209 212
89. P. Mendes Gepasi: a software package for modeling the dynamics, steady states and control of biochemical and other systems Comput. Applic. Biosci. 9 1993 563 571
90. P. Mendes Biochemistry by numbers: simulation of biochemical pathways with gepasi 3 Trends Biochem. Sci. 22 1997 361 363
91. P. Mendes, and D.B. Kell Non-linear optimization of biochemical pathways: applications to metabolic engineering and parameter estimation Bioinformatics 14 1998 869 883
92. L.R. Petzold Automatic selection of methods for solving stiff and nonstiff systems of ordinary differential equations SIAM J. Sci. Stat. Comput. 4 1983 36 148
93. A.C. Hindmarsh Odepack, a systematised collection of ode solvers R.S. Stepleman Scientific Computing 1983 North Holland Amsterdam 55 64
94. F. Hyafil, Y. Jacques, G. Fayat, M. Fromant, P. Dessen, and S. Blanquet Methionyl-tRNA synthetase from Escherichia coli: active stoichiometry and stopped-flow analysis of methionyl adenylate formation Biochemistry 15 1976 3678 3685
95. T. Meinnel, Y. Mechulam, and S. Blanquet Aminoacyl-trna synthetases: occurrence, structure, and function D. Soll U. Rajbhandary tRNA: Structure, Biosynthesis, and Function 1995 American Society for Microbiology Washington, DC 251 292
96. T.S. Papas, and A. Peterkofsky A random sequential mechanism for arginyl transfer ribonucleic acid synthetase of Escherichia coli Biochemistry 11 1972 4602 4608
97. M. Jahn, M.J. Rogers, and D. Soll Anticodon and acceptor stem nucleotides in trna(gln) are major recognition elements for E. coli glutaminl-tRNA synthetase Nature 352 1991 258 260
98. R.K. Airas ATP-induced activation of the aminoacylation of tRNA by the isoleucyl-tRNA synthetase from Escherichia coli Eur. J. Biochem. 176 1988 359 363
99. S.J. Park, Y.-M. Hou, and P. Schimmel A single base pair affects binding and catalytic parameters in the molecular recognition of a transfer RNA Biochemistry 28 1989 2740 2746
100. L.H. Schulman, and H. Pelka The anticodon contains a major element of the identity of arginine transfer RNAs Science 246 1989 1595 1597
101. H. Jakubowski, and E. Goldman Quantities of individual aminoacyl-trna families and their turnover in Escherichia coli J. Bacteriol. 158 1984 769 776
102. C.D. Yegian, G.S. Stent, and E.M. Martin Intracellular condition of Escherichia coli transfer RNA Proc. Natl Acad. Sci. USA 55 1966 839 846
103. G. Zubay In vitro synthesis of proteins in microbial systems Annu. Rev. Genet. 7 1973 267 287