Manipulating the genetic code for membrane protein production: What have we learnt so far?

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 1091-1096

  Nørholm, Morten H H ^a   Light, Sara ^a   Virkki, Minttu T I ^a   Elofsson, Arne ^a   Von Heijne, Gunnar ^a   Daley, Daniel O ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Codon use; Membrane protein engineering; Membrane protein folding; Membrane protein overexpression

Indexed keywords

AMINO ACID; MEMBRANE PROTEIN;

BIOENGINEERING; BIOSYNTHESIS; CODON USAGE; GENE EXPRESSION; GENE SEQUENCE; GENETIC CODE; HETEROLOGOUS EXPRESSION; HOMOLOGOUS EXPRESSION; HUMAN; MEMBRANE BIOLOGY; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; TRANSLATION INITIATION; TRANSLATION REGULATION;

BASE SEQUENCE; CODON; GENETIC CODE; MEMBRANE PROTEINS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; RNA, MESSENGER;

EID: 84857659619     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.08.018     Document Type: Review

References (69)

1. F.H. Crick, L. Barnett, S. Brenner, and R.J. Watts-Tobin General nature of the genetic code for proteins Nature 192 1961 1227 1232
2. M. Gouy, and C. Gautier Codon usage in bacteria: correlation with gene expressivity Nucleic Acids Res. 10 1982 7055 7074
3. T. Ikemura Codon usage and tRNA content in unicellular and multicellular organisms Mol. Biol. Evol. 2 1985 13 34
4. D. Chen, and D.E. Texada Low-usage codons and rare codons of Escherichia coli Gene Ther. Mol. Biol. 10 2006 1 12
5. J.B. Plotkin, and G. Kudla Synonymous but not the same: the causes and consequences of codon bias Nat. Rev. Genet. 12 2011 32 42
6. F. Wright The 'effective number of codons' used in a gene Gene 87 1990 23 29
7. T. Ikemura Measurement of relative amount of E. coli tRNAs: codon choice in E. coli genes is largely constrained by the concentration of anticodons (author's transl) Tanpakushitsu Kakusan Koso 25 1980 668 678
8. 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
9. T. Ikemura Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes J. Mol. Biol. 146 1981 1 21
10. J.L. Bennetzen, and B.D. Hall Codon selection in yeast J. Biol. Chem. 257 1982 3026 3031
11. M. dos Reis, R. Savva, and L. Wernisch Solving the riddle of codon usage preferences: a test for translational selection Nucleic Acids Res. 32 2004 5036 5044
12. P.M. Sharp, and W.H. Li The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications Nucleic Acids Res. 15 1987 1281 1295
13. J. Elf, G.W. Li, and X.S. Xie Probing transcription factor dynamics at the single-molecule level in a living cell Science 316 2007 1191 1194
14. M. Welch, S. Govindarajan, J.E. Ness, A. Villalobos, A. Gurney, J. Minshull, and C. Gustafsson Design parameters to control synthetic gene expression in Escherichia coli PLoS One 4 2009 e7002
15. G. Kudla, A.W. Murray, D. Tollervey, and J.B. Plotkin Coding-sequence determinants of gene expression in Escherichia coli Science 324 2009 255 258
16. M. Marin Folding at the rhythm of the rare codon beat Biotechnol. J. 3 2008 1047 1057
17. C.J. Tsai, Z.E. Sauna, C. Kimchi-Sarfaty, S.V. Ambudkar, M.M. Gottesman, and R. Nussinov Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima J. Mol. Biol. 383 2008 281 291
18. K. Fredrick, and M. Ibba How the sequence of a gene can tune its translation Cell 141 2010 227 229
19. S. Makino, J.N. Qu, K. Uemori, H. Ichikawa, T. Ogura, and H. Matsuzawa A silent mutation in the ftsH gene of Escherichia coli that affects FtsH protein production and colicin tolerance Mol. Gen. Genet. 254 1997 578 583
20. J. Duan, M.S. Wainwright, J.M. Comeron, N. Saitou, A.R. Sanders, J. Gelernter, and P.V. Gejman Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor Hum. Mol. Genet. 12 2003 205 216
21. A. Deana, R. Ehrlich, and C. Reiss Silent mutations in the Escherichia coli ompA leader peptide region strongly affect transcription and translation in vivo Nucleic Acids Res. 26 1998 4778 4782
22. C. Kimchi-Sarfaty, J.M. Oh, I.W. Kim, Z.E. Sauna, A.M. Calcagno, S.V. Ambudkar, and M.M. Gottesman A "silent" polymorphism in the MDR1 gene changes substrate specificity Science 315 2007 525 528
23. T.A. Thanaraj, and P. Argos Ribosome-mediated translational pause and protein domain organization Protein Sci. 5 1996 1594 1612
24. R. Saunders, and C.M. Deane Synonymous codon usage influences the local protein structure observed Nucleic Acids Res. 38 2010 6719 6728
25. G. Zhang, M. Hubalewska, and Z. Ignatova Transient ribosomal attenuation coordinates protein synthesis and co-translational folding Nat. Struct. Mol. Biol. 16 2009 274 280
26. P. Cortazzo, C. Cervenansky, M. Marin, C. Reiss, R. Ehrlich, and A. Deana Silent mutations affect in vivo protein folding in Escherichia coli Biochem. Biophys. Res. Commun. 293 2002 537 541
27. A.A. Komar, T. Lesnik, and C. Reiss Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation FEBS Lett. 462 1999 387 391
28. V. Ramachandiran, G. Kramer, P.M. Horowitz, and B. Hardesty Single synonymous codon substitution eliminates pausing during chloramphenicol acetyl transferase synthesis on Escherichia coli ribosomes in vitro FEBS Lett. 512 2002 209 212
29. T. Hessa, H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, H. Andersson, I. Nilsson, S.H. White, and G. von Heijne Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
30. M.B. Ulmschneider, M.S. Sansom, and A. Di Nola Properties of integral membrane protein structures: derivation of an implicit membrane potential Proteins 59 2005 252 265
31. J. Prilusky, and E. Bibi Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs Proc. Natl. Acad. Sci. U.S.A. 106 2009 6662 6666
32. R.V. Wolfenden, P.M. Cullis, and C.C. Southgate Water, protein folding, and the genetic code Science 206 1979 575 577
33. K. Nevo-Dinur, A. Nussbaum-Shochat, S. Ben-Yehuda, and O. Amster-Choder Translation-independent localization of mRNA in E. coli Science 331 2011 1081 1084
34. K. Lin, S.B. Tan, P.R. Kolatkar, and R.J. Epstein Nonrandom intragenic variations in patterns of codon bias implicate a sequential interplay between transitional genetic drift and functional amino acid selection J. Mol. Evol. 57 2003 538 545
35. F. Kepes The "+ 70 pause": hypothesis of a translational control of membrane protein assembly J. Mol. Biol. 262 1996 77 86
36. P. Dessen, and F. Kepes The PAUSE software for analysis of translational control over protein targeting: application to E. nidulans membrane proteins Gene 244 2000 89 96
37. G.F. Chen, and M. Inouye Suppression of the negative effect of minor arginine codons on gene expression; preferential usage of minor codons within the first 25 codons of the Escherichia coli genes Nucleic Acids Res. 18 1990 1465 1473
38. A. Eyre-Walker, and M. Bulmer Reduced synonymous substitution rate at the start of enterobacterial genes Nucleic Acids Res. 21 1993 4599 4603
39. D.A. Phoenix, and E. Korotkov Evidence of rare codon clusters within Escherichia coli coding regions FEMS Microbiol. Lett. 155 1997 63 66
40. C.M. Stenstrom, H. Jin, L.L. Major, W.P. Tate, and L.A. Isaksson Codon bias at the 3′-side of the initiation codon is correlated with translation initiation efficiency in Escherichia coli Gene 263 2001 273 284
41. T.F.t. Clarke, and P.L. Clark Rare codons cluster PLoS One 3 2008 e3412
42. N.T. Ingolia, S. Ghaemmaghami, J.R. Newman, and J.S. Weissman Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling Science 324 2009 218 223
43. T. Tuller, A. Carmi, K. Vestsigian, S. Navon, Y. Dorfan, J. Zaborske, T. Pan, O. Dahan, I. Furman, and Y. Pilpel An evolutionarily conserved mechanism for controlling the efficiency of protein translation Cell 141 2010 344 354
44. N. Mitarai, K. Sneppen, and S. Pedersen Ribosome collisions and translation efficiency: optimization by codon usage and mRNA destabilization J. Mol. Biol. 382 2008 236 245
45. J. Kim, P.G. Klein, and J.E. Mullet Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction center protein D1 J. Biol. Chem. 266 1991 14931 14938
46. N.E. Stollar, J.K. Kim, and M.J. Hollingsworth Ribosomes pause during the expression of the large ATP synthase gene cluster in spinach chloroplasts Plant Physiol. 105 1994 1167 1177
47. J. Frank, A. Verschoor, Y. Li, J. Zhu, R.K. Lata, M. Radermacher, P. Penczek, R. Grassucci, R.K. Agrawal, and S. Srivastava A model of the translational apparatus based on a three-dimensional reconstruction of the Escherichia coli ribosome Biochem. Cell Biol. 73 1995 757 765
48. S. Bhushan, M. Gartmann, M. Halic, J.P. Armache, A. Jarasch, T. Mielke, O. Berninghausen, D.N. Wilson, and R. Beckmann Alpha-helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel Nat. Struct. Mol. Biol. 17 2010 313 317
49. A. Ujvari, R. Aron, T. Eisenhaure, E. Cheng, H.A. Parag, Y. Smicun, R. Halaban, and D.N. Hebert Translation rate of human tyrosinase determines its N-linked glycosylation level J. Biol. Chem. 276 2001 5924 5931
50. C. Gustafsson, S. Govindarajan, and J. Minshull Codon bias and heterologous protein expression Trends Biotechnol. 22 2004 346 353
51. M. Welch, A. Villalobos, C. Gustafsson, and J. Minshull You're one in a googol: optimizing genes for protein expression J. R. Soc. Interface 6 Suppl 4 2009 S467 S476
52. G. Wu, L. Dress, and S.J. Freeland Optimal encoding rules for synthetic genes: the need for a community effort Mol. Syst. Biol. 3 2007 134
53. E.M. Slimko, and H.A. Lester Codon optimization of Caenorhabditis elegans GluCl ion channel genes for mammalian cells dramatically improves expression levels J. Neurosci. Methods 124 2003 75 81
54. J.L. Baneres, A. Martin, P. Hullot, J.P. Girard, J.C. Rossi, and J. Parello Structure-based analysis of GPCR function: conformational adaptation of both agonist and receptor upon leukotriene B4 binding to recombinant BLT1 J. Mol. Biol. 329 2003 801 814
55. F.F. Hamdan, A. Mousa, and P. Ribeiro Codon optimization improves heterologous expression of a Schistosoma mansoni cDNA in HEK293 cells Parasitol. Res. 88 2002 583 586
56. B. Maertens, A. Spriestersbach, U. von Groll, U. Roth, J. Kubicek, M. Gerrits, M. Graf, M. Liss, D. Daubert, R. Wagner, and F. Schafer Gene optimization mechanisms: a multi-gene study reveals a high success rate of full-length human proteins expressed in Escherichia coli Protein Sci. 19 2010 1312 1326
57. M. Allert, J.C. Cox, and H.W. Hellinga Multifactorial determinants of protein expression in prokaryotic open reading frames J. Mol. Biol. 402 2010 905 918
58. S. Fath, A.P. Bauer, M. Liss, A. Spriestersbach, B. Maertens, P. Hahn, C. Ludwig, F. Schafer, M. Graf, and R. Wagner Multiparameter RNA and codon optimization: a standardized tool to assess and enhance autologous mammalian gene expression PLoS One 6 2011 e17596
59. U. Brinkmann, R.E. Mattes, and P. Buckel High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product Gene 85 1989 109 114
60. 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
61. S.J. Park, S.K. Lee, and B.J. Lee Effect of tandem rare codon substitution and vector-host combinations on the expression of the EBV gp110 C-terminal domain in Escherichia coli Protein Expr. Purif. 24 2002 470 480
62. H. Tegel, S. Tourle, J. Ottosson, and A. Persson Increased levels of recombinant human proteins with the Escherichia coli strain Rosetta(DE3) Protein Expr. Purif. 69 2010 159 167
63. M.F. Alexeyev, and H.H. Winkler Gene synthesis, bacterial expression and purification of the Rickettsia prowazekii ATP/ADP translocase Biochim. Biophys. Acta 1419 1999 299 306
64. S.E. Bane, J.E. Velasquez, and A.S. Robinson Expression and purification of milligram levels of inactive G-protein coupled receptors in E. coli Protein Expr. Purif. 52 2007 348 355
65. D.O. Daley, M. Rapp, E. Granseth, K. Melen, D. Drew, and G. von Heijne Global topology analysis of the Escherichia coli inner membrane proteome Science 308 2005 1321 1323
66. M. Osterberg, H. Kim, J. Warringer, K. Melen, A. Blomberg, and G. von Heijne Phenotypic effects of membrane protein overexpression in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 103 2006 11148 11153
67. o-ATPase subunit a is inhibited by instability of the uncB gene transcript FEBS Lett. 547 2003 97 100
68. A. Bernsel, H. Viklund, J. Falk, E. Lindahl, G. von Heijne, and A. Elofsson Prediction of membrane-protein topology from first principles Proc. Natl. Acad. Sci. U.S.A. 105 2008 7177 7181
69. T. Becker, S. Bhushan, A. Jarasch, J.P. Armache, S. Funes, F. Jossinet, J. Gumbart, T. Mielke, O. Berninghausen, K. Schulten, E. Westhof, R. Gilmore, E.C. Mandon, and R. Beckmann Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome Science 326 2009 1369 1373