Non-standard genetic codes define new concepts for protein engineering

Life

Volumn 5, Issue 4, 2015, Pages 1610-1628

  Bezerra, Ana R ^a   Guimarães, Ana R ^a   Santos, Manuel A S ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Amino acids; Biotechnology; Codon reassignment; Evolution; Genetic code

Indexed keywords

EID: 84947051079     PISSN: None     EISSN: 20751729     Source Type: Journal    
DOI: 10.3390/life5041610     Document Type: Review

References (135)

1. Crick, F.H. The origin of the genetic code. J. Mol. Biol. 1968, 38, 367–379. [CrossRef]
2. Ibba, M.; Soll, D. Aminoacyl-tRNAs: Setting the limits of the genetic code. Genes Dev. 2004, 18, 731–738. [CrossRef][PubMed]
3. Santos, M.; Santos, M.A. Structural and molecular features of non-standard genetic codes. In Codon Evolution: Mechanisms and Models; Cannarozzi, G.M., Schneider, A., Eds.; Oxford University Press: New York, NY, USA, 2012; pp. 258–271.
4. Butler, G.; Rasmussen, M.D.; Lin, M.F.; Santos, M.A.S.; Sakthikumar, S.; Munro, C.A.; Rheinbay, E.; Grabherr, M.; Forche, A.; Reedy, J.L., et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009, 459, 657–662. [CrossRef][PubMed]
5. Sugita, T.; Nakase, T. Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. Syst. Appl. Microbiol. 1999, 22, 79–86. [CrossRef]
6. Hanyu, N.; Kuchino, Y.; Nishimura, S.; Beier, H. Dramatic events in ciliate evolution: Alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in two Tetrahymena tRNAs. EMBO J. 1986, 5, 1307–1311. [PubMed]
7. Yamao, F.; Muto, A.; Kawauchi, Y.; Iwami, M.; Iwagami, S.; Azumi, Y.; Osawa, S. UGA is read as tryptophan in Mycoplasma capricolum. Proc. Natl. Acad. Sci. USA 1985, 82, 2306–2309. [CrossRef][PubMed]
8. Van der Gulik, P.T.; Hoff, W.D. Unassigned codons, nonsense suppression, and anticodon modifications in the evolution of the genetic code. J. Mol. Evol. 2011, 73, 59–69. [CrossRef][PubMed]
9. Allmang, C.; Krol, A. Selenoprotein synthesis: UGA does not end the story. Biochimie 2006, 88, 1561–1571. [CrossRef][PubMed]
10. Yuan, J.; O’Donoghue, P.; Ambrogelly, A.; Gundllapalli, S.; Sherrer, R.L.; Palioura, S.; Simonovic, M.; Soll, D. Distinct genetic code expansion strategies for selenocysteine and pyrrolysine are reflected in different aminoacyl-tRNA formation systems. FEBS Lett. 2010, 584, 342–349. [CrossRef][PubMed]
11. Gaston, M.A.; Zhang, L.; Green-Church, K.B.; Krzycki, J.A. The complete biosynthesis of the genetically encoded amino acid pyrrolysine from lysine. Nature 2011, 471, 647–650. [CrossRef][PubMed]
12. Krzycki, J.A. The direct genetic encoding of pyrrolysine. Curr. Opin. Microbiol. 2005, 8, 706–712. [CrossRef][PubMed]
13. Chin, J.W. Expanding and reprogramming the genetic code of cells and animals. Annu. Rev. Biochem. 2014, 83, 379–408. [CrossRef][PubMed]
14. Li, F.; Zhang, H.; Sun, Y.; Pan, Y.; Zhou, J.; Wang, J. Expanding the genetic code for photoclick chemistry in E. coli, mammalian cells, and A. thaliana. Angew. Chem. Int. Ed. Engl. 2013, 52, 9700–9704. [CrossRef][PubMed]
15. Lin, S.; Zhang, Z.; Xu, H.; Li, L.; Chen, S.; Li, J.; Hao, Z.; Chen, P.R. Site-specific incorporation of photo-cross-linker and bioorthogonal amino acids into enteric bacterial pathogens. J. Am. Chem. Soc. 2011, 133, 20581–20587. [CrossRef][PubMed]
16. Wang, F.; Robbins, S.; Guo, J.; Shen, W.; Schultz, P.G. Genetic incorporation of unnatural amino acids into proteins in Mycobacterium tuberculosis. PLoS ONE 2010, 5, e9354. [CrossRef][PubMed]
17. Greiss, S.; Chin, J.W. Expanding the genetic code of an animal. J. Am. Chem. Soc. 2011, 133, 14196–14199. [CrossRef][PubMed]
18. Teramoto, H.; Kojima, K. Production of Bombyx mori silk fibroin incorporated with unnatural amino acids. Biomacromolecules 2014, 15, 2682–2690. [CrossRef][PubMed]
19. Mukai, T.; Hayashi, A.; Iraha, F.; Sato, A.; Ohtake, K.; Yokoyama, S.; Sakamoto, K. Codon reassignment in the Escherichia coli genetic code. Nucleic Acids Res. 2010, 38, 8188–8195. [CrossRef][PubMed]
20. Bacher, J.M.; Ellington, A.D. Selection and characterization of Escherichia coli variants capable of growth on an otherwise toxic tryptophan analogue. J. Bacteriol. 2001, 183, 5414–5425. [CrossRef][PubMed]
21. Bacher, J.M.; de Crecy-Lagard, V.; Schimmel, P.R. Inhibited cell growth and protein functional changes from an editing-defective tRNA synthetase. Proc. Natl. Acad. Sci. USA 2005, 102, 1697–1701. [CrossRef][PubMed]
22. Turanov, A.A.; Lobanov, A.V.; Fomenko, D.E.; Morrison, H.G.; Sogin, M.L.; Klobutcher, L.A.; Hatfield, D.L.; Gladyshev, V.N. Genetic code supports targeted insertion of two amino acids by one codon. Science 2009, 323, 259–261. [CrossRef][PubMed]
23. Knight, R.D.; Freeland, S.J.; Landweber, L.F. Rewiring the keyboard: Evolvability of the genetic code. Nat. Rev. Genet. 2001, 2, 49–58. [CrossRef][PubMed]
24. Stamburski, C.; Renaudin, J.; Bove, J.M. Mutagenesis of a tryptophan codon from TGG to TGA in the cat gene does not prevent its expression in the helical mollicute Spiroplasma citri. Gene 1992, 110, 133–134. [CrossRef]
25. McCutcheon, J.P.; McDonald, B.R.; Moran, N.A. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet. 2009, 5, e1000565. [CrossRef][PubMed]
26. Wrighton, K.C.; Thomas, B.C.; Sharon, I.; Miller, C.S.; Castelle, C.J.; VerBerkmoes, N.C.; Wilkins, M.J.; Hettich, R.L.; Lipton, M.S.; Williams, K.H., et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 2012, 337, 1661–1665. [CrossRef][PubMed]
27. Campbell, J.H.; O’Donoghue, P.; Campbell, A.G.; Schwientek, P.; Sczyrba, A.; Woyke, T.; Soll, D.; Podar, M. UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc. Natl. Acad. Sci. USA 2013, 110, 5540–5545. [CrossRef][PubMed]
28. Rinke, C.; Schwientek, P.; Sczyrba, A.; Ivanova, N.N.; Anderson, I.J.; Cheng, J.F.; Darling, A.; Malfatti, S.; Swan, B.K.; Gies, E.A., et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 2013, 499, 431–437. [CrossRef][PubMed]
29. Citti, C.; Marechal-Drouard, L.; Saillard, C.; Weil, J.H.; Bove, J.M. Spiroplasma citri UGG and UGA tryptophan codons: Sequence of the two tryptophanyl-tRNAs and organization of the corresponding genes. J. Bacteriol. 1992, 174, 6471–6478. [PubMed]
30. Inagaki, Y.; Bessho, Y.; Osawa, S. Lack of peptide-release activity responding to codon UGA in Mycoplasma capricolum. Nucleic Acids Res. 1993, 21, 1335–1338. [CrossRef][PubMed]
31. Ohama, T.; Inagaki, Y.; Bessho, Y.; Osawa, S. Evolving genetic code. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2008, 84, 58–74. [CrossRef][PubMed]
32. Shackelton, L.A.; Holmes, E.C. The role of alternative genetic codes in viral evolution and emergence. J. Theor. Biol. 2008, 254, 128–134. [CrossRef][PubMed]
33. Ivanova, N.N.; Schwientek, P.; Tripp, H.J.; Rinke, C.; Pati, A.; Huntemann, M.; Visel, A.; Woyke, T.; Kyrpides, N.C.; Rubin, E.M. Stop codon reassignments in the wild. Science 2014, 344, 909–913. [CrossRef][PubMed]
34. Lajoie, M.J.; Rovner, A.J.; Goodman, D.B.; Aerni, H.R.; Haimovich, A.D.; Kuznetsov, G.; Mercer, J.A.; Wang, H.H.; Carr, P.A.; Mosberg, J.A., et al. Genomically recoded organisms expand biological functions. Science 2013, 342, 357–360. [CrossRef][PubMed]
35. Song, H.; Mugnier, P.; Das, A.K.; Webb, H.M.; Evans, D.R.; Tuite, M.F.; Hemmings, B.A.; Barford, D. The crystal structure of human eukaryotic release factor eRF1–mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 2000, 100, 311–321. [CrossRef]
36. Bertram, G.; Bell, H.A.; Ritchie, D.W.; Fullerton, G.; Stansfield, I. Terminating eukaryote translation: Domain 1 of release factor eRF1 functions in stop codon recognition. RNA 2000, 6, 1236–1247. [CrossRef][PubMed]
37. Seit-Nebi, A.; Frolova, L.; Justesen, J.; Kisselev, L. Class-1 translation termination factors: Invariant GGQ minidomain is essential for release activity and ribosome binding but not for stop codon recognition. Nucleic Acids Res. 2001, 29, 3982–3987. [PubMed]
38. Cheng, Z.; Saito, K.; Pisarev, A.V.; Wada, M.; Pisareva, V.P.; Pestova, T.V.; Gajda, M.; Round, A.; Kong, C.; Lim, M., et al. Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev. 2009, 23, 1106–1118. [CrossRef][PubMed]
39. Keeling, P.J.; Doolittle, W.F. A non-canonical genetic code in an early diverging eukaryotic lineage. EMBO J. 1996, 15, 2285–2290. [PubMed]
40. Keeling, P.J.; Leander, B.S. Characterisation of a non-canonical genetic code in the oxymonad Streblomastix strix. J. Mol. Biol. 2003, 326, 1337–1349. [CrossRef]
41. Cocquyt, E.; Gile, G.H.; Leliaert, F.; Verbruggen, H.; Keeling, P.J.; De Clerck, O. Complex phylogenetic distribution of a non-canonical genetic code in green algae. BMC. Evol. Biol. 2010, 10. [CrossRef]
42. Caron, F.; Meyer, E. Does Paramecium primaurelia use a different genetic code in its macronucleus? Nature 1985, 314, 185–188. [CrossRef][PubMed]
43. Horowitz, S.; Gorovsky, M.A. An unusual genetic code in nuclear genes of Tetrahymena. Proc. Natl. Acad. Sci. USA 1985, 82, 2452–2455. [CrossRef][PubMed]
44. Tourancheau, A.B.; Tsao, N.; Klobutcher, L.A.; Pearlman, R.E.; Adoutte, A. Genetic code deviations in the ciliates: Evidence for multiple and independent events. EMBO J. 1995, 14, 3262–3267. [PubMed]
45. Helftenbein, E. Nucleotide sequence of a macronuclear DNA molecule coding for alpha-tubulin from the ciliate Stylonychia lemnae. Special codon usage: TAA is not a translation termination codon. Nucleic Acids Res. 1985, 13, 415–433. [CrossRef][PubMed]
46. Sanchez-Silva, R.; Villalobo, E.; Morin, L.; Torres, A. A new noncanonical nuclear genetic code: Translation of UAA into glutamate. Curr. Biol. 2003, 13, 442–447. [CrossRef]
47. Meyer, F.; Schmidt, H.J.; Plumper, E.; Hasilik, A.; Mersmann, G.; Meyer, H.E.; Engstrom, A.; Heckmann, K. UGA is translated as cysteine in pheromone 3 of Euplotes octocarinatus. Proc. Natl. Acad. Sci. USA 1991, 88, 3758–3761. [CrossRef][PubMed]
48. Lozupone, C.A.; Knight, R.D.; Landweber, L.F. The molecular basis of nuclear genetic code change in ciliates. Curr. Biol. 2001, 11, 65–74. [CrossRef]
49. Grimm, M.; Brunen-Nieweler, C.; Junker, V.; Heckmann, K.; Beier, H. The hypotrichous ciliate Euplotes octocarinatus has only one type of tRNACys with GCA anticodon encoded on a single macronuclear DNA molecule. Nucleic Acids Res. 1998, 26, 4557–4565. [CrossRef][PubMed]
50. Conard, S.E.; Buckley, J.; Dang, M.; Bedwell, G.J.; Carter, R.L.; Khass, M.; Bedwell, D.M. Identification of eRF1 residues that play critical and complementary roles in stop codon recognition. RNA 2012, 18, 1210–1221. [CrossRef][PubMed]
51. Inagaki, Y.; Doolittle, W.F. Class I release factors in ciliates with variant genetic codes. Nucleic Acids Res. 2001, 29, 921–927. [CrossRef][PubMed]
52. Lekomtsev, S.; Kolosov, P.; Bidou, L.; Frolova, L.; Rousset, J.P.; Kisselev, L. Different modes of stop codon restriction by the Stylonychia and Paramecium eRF1 translation termination factors. Proc. Natl. Acad. Sci. USA 2007, 104, 10824–10829. [CrossRef][PubMed]
53. Ito, K.; Frolova, L.; Seit-Nebi, A.; Karamyshev, A.; Kisselev, L.; Nakamura, Y. Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within domain 1. Proc. Natl. Acad. Sci. USA 2002, 99, 8494–8499. [CrossRef][PubMed]
54. Salas-Marco, J.; Fan-Minogue, H.; Kallmeyer, A.K.; Klobutcher, L.A.; Farabaugh, P.J.; Bedwell, D.M. Distinct paths to stop codon reassignment by the variant-code organisms Tetrahymena and Euplotes. Mol. Cell Biol. 2006, 26, 438–447. [CrossRef][PubMed]
55. Kervestin, S.; Frolova, L.; Kisselev, L.; Jean-Jean, O. Stop codon recognition in ciliates: Euplotes release factor does not respond to reassigned UGA codon. EMBO Rep. 2001, 2, 680–684. [CrossRef][PubMed]
56. Blanchet, S.; Rowe, M.; von der, H.T.; Fabret, C.; Demais, S.; Howard, M.J.; Namy, O. New insights into stop codon recognition by eRF1. Nucleic Acids Res. 2015, 43, 3298–3308. [CrossRef][PubMed]
57. Bezerra, A.R.; Simoes, J.; Lee, W.; Rung, J.; Weil, T.; Gut, I.G.; Gut, M.; Bayes, M.; Rizzetto, L.; Cavalieri, D., et al. Reversion of a fungal genetic code alteration links proteome instability with genomic and phenotypic diversification. Proc. Natl. Acad. Sci. USA 2013, 110, 11079–11084. [CrossRef][PubMed]
58. Gomes, A.C.; Miranda, I.; Silva, R.M.; Moura, G.R.; Thomas, B.; Akoulitchev, A.; Santos, M.A. A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol. 2007, 8, R206. [CrossRef][PubMed]
59. Santos, M.A.; Tuite, M.F. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res. 1995, 23, 1481–1486. [CrossRef][PubMed]
60. Santos, M.A.; Keith, G.; Tuite, M.F. Non-standard translational events in Candida albicans mediated by an unusual seryl-tRNA with a 5'-CAG-3' (leucine) anticodon. EMBO J. 1993, 12, 607–616. [PubMed]
61. Santos, M.A.; Perreau, V.M.; Tuite, M.F. Transfer RNA structural change is a key element in the reassignment of the CUG codon in Candida albicans. EMBO J. 1996, 15, 5060–5068. [PubMed]
62. Knight, R.D.; Landweber, L.F.; Yarus, M. How mitochondria redefine the code. J. Mol. Evol. 2001, 53, 299–313. [CrossRef][PubMed]
63. Anderson, S.; Bankier, A.T.; Barrell, B.G.; de Bruijn, M.H.; Coulson, A.R.; Drouin, J.; Eperon, I.C.; Nierlich, D.P.; Roe, B.A.; Sanger, F., et al. Sequence and organization of the human mitochondrial genome. Nature 1981, 290, 457–465. [CrossRef][PubMed]
64. Watanabe, K.; Yokobori, S. tRNA Modification and Genetic Code Variations in Animal Mitochondria. J. Nucleic Acids 2011, 2011, 623095. [CrossRef][PubMed]
65. Jacob, J.E.; Vanholme, B.; Van Leeuwen, T.; Gheysen, G. A unique genetic code change in the mitochondrial genome of the parasitic nematode Radopholus similis. BMC Res. Notes 2009, 2. [CrossRef][PubMed]
66. Lavrov, D.V.; Pett, W.; Voigt, O.; Worheide, G.; Forget, L.; Lang, B.F.; Kayal, E. Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): Six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code. Mol. Biol. Evol. 2013, 30, 865–880. [CrossRef][PubMed]
67. Hayashi-Ishimaru, Y.; Ohama, T.; Kawatsu, Y.; Nakamura, K.; Osawa, S. UAG is a sense codon in several chlorophycean mitochondria. Curr. Genet. 1996, 30, 29–33. [CrossRef][PubMed]
68. Sengupta, S.; Yang, X.; Higgs, P.G. The mechanisms of codon reassignments in mitochondrial genetic codes. J. Mol. Evol. 2007, 64, 662–688. [CrossRef][PubMed]
69. Suzuki, T.; Miyauchi, K.; Suzuki, T.; Yokobori, S.; Shigi, N.; Kondow, A.; Takeuchi, N.; Yamagishi, A.; Watanabe, K. Taurine-containing uridine modifications in tRNA anticodons are required to decipher non-universal genetic codes in ascidian mitochondria. J. Biol. Chem. 2011, 286, 35494–35498. [CrossRef][PubMed]
70. Moriya, J.; Yokogawa, T.; Wakita, K.; Ueda, T.; Nishikawa, K.; Crain, P.F.; Hashizume, T.; Pomerantz, S.C.; McCloskey, J.A.; Kawai, G., et al. A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 1994, 33, 2234–2239. [CrossRef][PubMed]
71. Takemoto, C.; Spremulli, L.L.; Benkowski, L.A.; Ueda, T.; Yokogawa, T.; Watanabe, K. Unconventional decoding of the AUA codon as methionine by mitochondrial tRNAMet with the anticodon f5CAU as revealed with a mitochondrial in vitro translation system. Nucleic Acids Res. 2009, 37, 1616–1627. [CrossRef][PubMed]
72. Telford, M.J.; Herniou, E.A.; Russell, R.B.; Littlewood, D.T. Changes in mitochondrial genetic codes as phylogenetic characters: Two examples from the flatworms. Proc. Natl. Acad. Sci. USA 2000, 97, 11359–11364. [CrossRef][PubMed]
73. Tomita, K.; Ueda, T.; Watanabe, K. The presence of pseudouridine in the anticodon alters the genetic code: A possible mechanism for assignment of the AAA lysine codon as asparagine in echinoderm mitochondria. Nucleic Acids Res. 1999, 27, 1683–1689. [CrossRef][PubMed]
74. Miranda, I.; Silva, R.; Santos, M.A. Evolution of the genetic code in yeasts. Yeast 2006, 23, 203–213. [CrossRef][PubMed]
75. Giege, R.; Sissler, M.; Florentz, C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 1998, 26, 5017–5035. [CrossRef][PubMed]
76. Su, D.; Lieberman, A.; Lang, B.F.; Simonovic, M.; Soll, D.; Ling, J. An unusual tRNAThr derived from tRNAHis reassigns in yeast mitochondria the CUN codons to threonine. Nucleic Acids Res. 2011, 39, 4866–4874. [CrossRef][PubMed]
77. Ling, J.; Daoud, R.; Lajoie, M.J.; Church, G.M.; Soll, D.; Lang, B.F. Natural reassignment of CUU and CUA sense codons to alanine in Ashbya mitochondria. Nucleic Acids Res. 2014, 42, 499–508. [CrossRef][PubMed]
78. Ling, J.; Peterson, K.M.; Simonovic, I.; Cho, C.; Soll, D.; Simonovic, M. Yeast mitochondrial threonyl-tRNA synthetase recognizes tRNA isoacceptors by distinct mechanisms and promotes CUN codon reassignment. Proc. Natl. Acad. Sci. USA 2012, 109, 3281–3286. [CrossRef][PubMed]
79. Haen, K.M.; Lang, B.F.; Pomponi, S.A.; Lavrov, D.V. Glass sponges and bilaterian animals share derived mitochondrial genomic features: A common ancestry or parallel evolution? Mol. Biol. Evol. 2007, 24, 1518–1527. [CrossRef][PubMed]
80. Yokobori, S.; Ueda, T.; Watanabe, K. Codons AGA and AGG are read as glycine in ascidian mitochondria. J. Mol. Evol. 1993, 36, 1–8. [CrossRef][PubMed]
81. Yokobori, S.; Suzuki, T.; Watanabe, K. Genetic code variations in mitochondria: tRNA as a major determinant of genetic code plasticity. J. Mol. Evol. 2001, 53, 314–326. [CrossRef][PubMed]
82. Tomita, K.; Ueda, T.; Ishiwa, S.; Crain, P.F.; McCloskey, J.A.; Watanabe, K. Codon reading patterns in Drosophila melanogaster mitochondria based on their tRNA sequences: A unique wobble rule in animal mitochondria. Nucleic Acids Res. 1999, 27, 4291–4297. [CrossRef][PubMed]
83. Tomita, K.; Ueda, T.; Watanabe, K. 7-Methylguanosine at the anticodon wobble position of squid mitochondrial tRNA(Ser)GCU: Molecular basis for assignment of AGA/AGG codons as serine in invertebrate mitochondria. Biochim. Biophys. Acta 1998, 1399, 78–82. [CrossRef]
84. Watanabe, Y.; Tsurui, H.; Ueda, T.; Furushima, R.; Takamiya, S.; Kita, K.; Nishikawa, K.; Watanabe, K. Primary and higher order structures of nematode (Ascaris suum) mitochondrial tRNAs lacking either the T or D stem. J. Biol. Chem. 1994, 269, 22902–22906. [PubMed]
85. Abascal, F.; Posada, D.; Knight, R.D.; Zardoya, R. Parallel evolution of the genetic code in arthropod mitochondrial genomes. PLoS Biol. 2006, 4, e127. [CrossRef][PubMed]
86. Kuck, U.; Jekosch, K.; Holzamer, P. DNA sequence analysis of the complete mitochondrial genome of the green alga Scenedesmus obliquus: Evidence for UAG being a leucine and UCA being a non-sense codon. Gene 2000, 253, 13–18. [CrossRef]
87. Richter, R.; Rorbach, J.; Pajak, A.; Smith, P.M.; Wessels, H.J.; Huynen, M.A.; Smeitink, J.A.; Lightowlers, R.N.; Chrzanowska-Lightowlers, Z.M. A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J. 2010, 29, 1116–1125. [CrossRef][PubMed]
88. Lind, C.; Sund, J.; Aqvist, J. Codon-reading specificities of mitochondrial release factors and translation termination at non-standard stop codons. Nat. Commun. 2013, 4. [CrossRef][PubMed]
89. Huynen, M.A.; Duarte, I.; Chrzanowska-Lightowlers, Z.M.; Nabuurs, S.B. Nabuurs, Structure based hypothesis of a mitochondrial ribosome rescue mechanism. Biol. Direct 2012, 7. [CrossRef][PubMed]
90. Akabane, S.; Ueda, T.; Nierhaus, K.H.; Takeuchi, N. Ribosome rescue and translation termination at non-standard stop codons by ICT1 in mammalian mitochondria. PLoS Genet. 2014, 10, e1004616. [CrossRef][PubMed]
91. Nozaki, Y.; Matsunaga, N.; Ishizawa, T.; Ueda, T.; Takeuchi, N. HMRF1L is a human mitochondrial translation release factor involved in the decoding of the termination codons UAA and UAG. Genes Cells 2008, 13, 429–438. [CrossRef][PubMed]
92. Bock, A.; Forchhammer, K.; Heider, J.; Leinfelder, W.; Sawers, G.; Veprek, B.; Zinoni, F. Selenocysteine: The 21st amino acid. Mol. Microbiol. 1991, 5, 515–520. [CrossRef][PubMed]
93. Srinivasan, G.; James, C.M.; Krzycki, J.A. Pyrrolysine encoded by UAG in Archaea: Charging of a UAG-decoding specialized tRNA. Science 2002, 296, 1459–1462. [CrossRef][PubMed]
94. Ambrogelly, A.; Palioura, S.; Soll, D. Natural expansion of the genetic code. Nat. Chem. Biol. 2007, 3, 29–35. [CrossRef][PubMed]
95. Blight, S.K.; Larue, R.C.; Mahapatra, A.; Longstaff, D.G.; Chang, E.; Zhao, G.; Kang, P.T.; Green-Church, K.B.; Chan, M.K.; Krzycki, J.A. Direct charging of tRNA(CUA) with pyrrolysine in vitro and in vivo. Nature 2004, 431, 333–335. [CrossRef][PubMed]
96. Koonin, E.V.; Novozhilov, A.S. Origin and evolution of the genetic code: The universal enigma. IUBMB Life 2009, 61, 99–111. [CrossRef][PubMed]
97. Moura, G.R.; Paredes, J.A.; Santos, M.A. Development of the genetic code: Insights from a fungal codon reassignment. FEBS Lett. 2010, 584, 334–341. [CrossRef][PubMed]
98. Link, A.J.; Mock, M.L.; Tirrell, D.A. Non-canonical amino acids in protein engineering. Curr. Opin. Biotechnol. 2003, 14, 603–609. [CrossRef][PubMed]
99. Voloshchuk, N.; Montclare, J.K. Incorporation of unnatural amino acids for synthetic biology. Mol. Biosyst. 2010, 6, 65–80. [CrossRef][PubMed]
100. Yang, W.; Hendrickson, W.A.; Crouch, R.J.; Satow, Y. Structure of ribonuclease H phased at 2 A resolution by MAD analysis of the selenomethionyl protein. Science 1990, 249, 1398–1405. [CrossRef][PubMed]
101. Beatty, K.E.; Xie, F.; Wang, Q.; Tirrell, D.A. Selective dye-labeling of newly synthesized proteins in bacterial cells. J. Am. Chem. Soc. 2005, 127, 14150–14151. [CrossRef][PubMed]
102. Liu, C.C.; Schultz, P.G. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 2010, 79, 413–444. [CrossRef][PubMed]
103. Wang, L.; Schultz, P.G. A general approach for the generation of orthogonal tRNAs. Chem. Biol. 2001, 8, 883–890. [CrossRef]
104. Hoesl, M.G.; Budisa, N. Recent advances in genetic code engineering in Escherichia coli. Curr. Opin. Biotechnol. 2012, 23, 751–757. [CrossRef][PubMed]
105. Johnson, D.B.; Xu, J.; Shen, Z.; Takimoto, J.K.; Schultz, M.D.; Schmitz, R.J.; Xiang, Z.; Ecker, J.R.; Briggs, S.P.; Wang, L. RF1 knockout allows ribosomal incorporation of unnatural amino acids at multiple sites. Nat. Chem. Biol. 2011, 7, 779–786. [CrossRef][PubMed]
106. Mukai, T.; Hoshi, H.; Ohtake, K.; Takahashi, M.; Yamaguchi, A.; Hayashi, A.; Yokoyama, S.; Sakamoto, K. Highly reproductive Escherichia coli cells with no specific assignment to the UAG codon. Sci Rep. 2015, 5. [CrossRef][PubMed]
107. Isaacs, F.J.; Carr, P.A.; Wang, H.H.; Lajoie, M.J.; Sterling, B.; Kraal, L.; Tolonen, A.C.; Gianoulis, T.A.; Goodman, D.B.; Reppas, N.B., et al. Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 2011, 333, 348–353. [CrossRef][PubMed]
108. Rovner, A.J.; Haimovich, A.D.; Katz, S.R.; Li, Z.; Grome, M.W.; Gassaway, B.M.; Amiram, M.; Patel, J.R.; Gallagher, R.R.; Rinehart, J., et al. Recoded organisms engineered to depend on synthetic amino acids. Nature 2015, 518, 89–93. [CrossRef][PubMed]
109. Wang, H.H.; Isaacs, F.J.; Carr, P.A.; Sun, Z.Z.; Xu, G.; Forest, C.R.; Church, G.M. Programming cells by multiplex genome engineering and accelerated evolution. Nature 2009, 460, 894–898. [CrossRef][PubMed]
110. Nakamura, Y.; Ito, K.; Ehrenberg, M. Mimicry grasps reality in translation termination. Cell 2000, 101, 349–352. [CrossRef]
111. Wang, Q.; Wang, L. New methods enabling efficient incorporation of unnatural amino acids in yeast. J. Am. Chem. Soc. 2008, 130, 6066–6067. [CrossRef][PubMed]
112. Cohen, G.N.; Cowie, D.B. Total replacement of methionine by selenomethionine in the proteins of Escherichia coli. C. R. Hebd. Seances Acad. Sci. 1957, 244, 680–683. [PubMed]
113. Link, A.J.; Tirrell, D.A. Reassignment of sense codons in vivo. Methods 2005, 36, 291–298. [CrossRef][PubMed]
114. Wang, P.; Fichera, A.; Kumar, K.; Tirrell, D.A. Alternative translations of a single RNA message: An identity switch of (2S,3R)-4,4,4-trifluorovaline between valine and isoleucine codons. Angew. Chem. Int. Ed. Engl. 2004, 43, 3664–3666. [CrossRef][PubMed]
115. Tang, Y.; Tirrell, D.A. Attenuation of the editing activity of the Escherichia coli leucyl-tRNA synthetase allows incorporation of novel amino acids into proteins in vivo. Biochemistry 2002, 41, 10635–10645. [CrossRef][PubMed]
116. Kwon, I.; Kirshenbaum, K.; Tirrell, D.A. Breaking the degeneracy of the genetic code. J. Am. Chem. Soc. 2003, 125, 7512–7513. [CrossRef][PubMed]
117. Zeng, Y.; Wang, W.; Liu, W.R. Towards reassigning the rare AGG codon in Escherichia coli. ChemBioChem 2014, 15, 1750–1754. [CrossRef][PubMed]
118. Mukai, T.; Yamaguchi, A.; Ohtake, K.; Takahashi, M.; Hayashi, A.; Iraha, F.; Kira, S.; Yanagisawa, T.; Yokoyama, S.; Hoshi, H., et al. Reassignment of a rare sense codon to a non-canonical amino acid in Escherichia coli. Nucleic Acids Res. 2015, 43, 8111–8122. [CrossRef][PubMed]
119. Anderson, J.C.; Wu, N.; Santoro, S.W.; Lakshman, V.; King, D.S.; Schultz, P.G. An expanded genetic code with a functional quadruplet codon. Proc. Natl. Acad. Sci. USA 2004, 101, 7566–7571. [CrossRef][PubMed]
120. Neumann, H.; Wang, K.; Davis, L.; Garcia-Alai, M.; Chin, J.W. Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 2010, 464, 441–444. [CrossRef][PubMed]
121. Wang, K.; Neumann, H.; Peak-Chew, S.Y.; Chin, J.W. Evolved orthogonal ribosomes enhance the efficiency of synthetic genetic code expansion. Nat. Biotechnol. 2007, 25, 770–777. [CrossRef][PubMed]
122. Chen, I.A.; Schindlinger, M. Quadruplet codons: One small step for a ribosome, one giant leap for proteins: an expanded genetic code could address fundamental questions about algorithmic information, biological function, and the origins of life. Bioessays 2010, 32, 650–654. [CrossRef][PubMed]
123. Santos, M.A.; Moura, G.; Massey, S.E.; Tuite, M.F. Driving change: The evolution of alternative genetic codes. Trends Genet. 2004, 20, 95–102. [CrossRef][PubMed]
124. Schultz, D.W.; Yarus, M. On malleability in the genetic code. J. Mol. Evol. 1996, 42, 597–601. [CrossRef][PubMed]
125. Osawa, S.; Jukes, T.H. Codon reassignment (codon capture) in evolution. J. Mol. Evol. 1989, 28, 271–278. [CrossRef][PubMed]
126. Andersson, S.G.; Kurland, C.G. Genomic evolution drives the evolution of the translation system. Biochem. Cell Biol. 1995, 73, 775–787. [CrossRef][PubMed]
127. Osawa, S.; Jukes, T.H.; Watanabe, K.; Muto, A. Recent evidence for evolution of the genetic code. Microbiol. Rev. 1992, 56, 229–264. [PubMed]
128. Osawa, S.; Collins, D.; Ohama, T.; Jukes, T.H.; Watanabe, K. Evolution of the mitochondrial genetic code. III. Reassignment of CUN codons from leucine to threonine during evolution of yeast mitochondria. J. Mol. Evol. 1990, 30, 322–328. [CrossRef][PubMed]
129. Ohama, T.; Suzuki, T.; Mori, M.; Osawa, S.; Ueda, T.; Watanabe, K.; Nakase, T. Non-universal decoding of the leucine codon CUG in several Candida species. Nucleic Acids Res. 1993, 21, 4039–4045. [CrossRef][PubMed]
130. Elstner, M.; Andreoli, C.; Ahting, U.; Tetko, I.; Klopstock, T.; Meitinger, T.; Prokisch, H. MitoP2: An integrative tool for the analysis of the mitochondrial proteome. Mol. Biotechnol. 2008, 40, 306–315. [CrossRef][PubMed]
131. Massey, S.E.; Moura, G.; Beltrao, P.; Almeida, R.; Garey, J.R.; Tuite, M.F.; Santos, M.A. Comparative evolutionary genomics unveils the molecular mechanism of reassignment of the CTG codon in Candida spp. Genome Res. 2003, 13, 544–557. [CrossRef][PubMed]
132. Lu, T.K.; Khalil, A.S.; Collins, J.J. Next-generation synthetic gene networks. Nat. Biotechnol. 2009, 27, 1139–1150. [CrossRef][PubMed]
133. Cho, H.; Daniel, T.; Buechler, Y.J.; Litzinger, D.C.; Maio, Z.; Putnam, A.M.; Kraynov, V.S.; Sim, B.C.; Bussell, S.; Javahishvili, T., et al. Optimized clinical performance of growth hormone with an expanded genetic code. Proc. Natl. Acad. Sci. USA 2011, 108, 9060–9065. [CrossRef][PubMed]
134. Dieterich, D.C.; Link, A.J.; Graumann, J.; Tirrell, D.A.; Schuman, E.M. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc. Natl. Acad. Sci. USA 2006, 103, 9482–9487. [CrossRef][PubMed]
135. Malyshev, D.A.; Dhami, K.; Quach, H.T.; Lavergne, T.; Ordoukhanian, P.; Torkamani, A.; Romesberg, F.E. Efficient and sequence-independent replication of DNA containing a third base pair establishes a functional six-letter genetic alphabet. Proc. Natl. Acad. Sci. USA 2012, 109, 12005–12010. [CrossRef][PubMed]