Coupling genetic code expansion and metabolic engineering for synthetic cells

Current Opinion in Biotechnology

Volumn 48, Issue , 2017, Pages 1-7

  Völler, Jan Stefan ^a   Budisa, Nediljko ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL ENGINEERING; COST EFFECTIVENESS; INDUSTRIAL RESEARCH; METABOLISM;

ACADEMIC RESEARCH; BIO-PRODUCTION; BIOSYNTHETIC PATHWAY; COST-EFFECTIVE SOLUTIONS; IN-SITU PRODUCTION; INDUSTRIAL BIOTECHNOLOGY; NON-CANONICAL AMINO ACIDS; PROTEIN TRANSLATION;

METABOLIC ENGINEERING;

ALPHA AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; BRANCHED CHAIN AMINO ACID; CHLORAMPHENICOL; CYSTEINE; METHIONINE; PYRROLYSINE; TRANSFER RNA; TRYPTOPHAN; UNCLASSIFIED DRUG; AMINO ACID; PEPTIDE; PROTEIN;

AMINO ACID SYNTHESIS; BIOSAFETY; CELL GROWTH; DRUG SYNTHESIS; GENETIC CODE EXPANSION; GENETIC TRANSCRIPTION AND TRANSLATION; METABOLIC ENGINEERING; NONHUMAN; PROTEIN EXPRESSION; REVIEW; ANIMAL; ARTIFICIAL CELL; BIOTECHNOLOGY; GENETIC CODE; GENETIC ENGINEERING; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROCEDURES; TRENDS;

AMINO ACIDS; AMINO ACYL-TRNA SYNTHETASES; ANIMALS; ARTIFICIAL CELLS; BIOTECHNOLOGY; GENETIC CODE; GENETIC ENGINEERING; HUMANS; METABOLIC ENGINEERING; PEPTIDES; PROTEINS;

EID: 85013793402     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2017.02.002     Document Type: Review

References (44)

1. 1• Agostini, F., Völler, J.-S., Koksch, B., Acevedo-Rocha, C.G., Kubyshkin, V., Budisa, N., Xenobiology meets enzymology: exploring the potential of unnatural building blocks in biocatalysis. Angew Chem Int Ed Engl, 2017, 10.1002/anie.201610129 [Epub ahead of print] By thoroughly surveying current literature in both research areas, this review comprehensively summarizes a large body of work on the use of ncAAs to modulate enzyme properties.
2. 2 Salwiczek, M., Nyakatura, E.K., Gerling, Ulla I.M., Ye, S., Koksch, B., Fluorinated amino acids: compatibility with native protein structures and effects on protein–protein interactions. Chem Soc Rev 41 (2012), 2135–2171.
3. 3 Baumann, T., Nickling, J., Bartholomae, M., Buivydas, A., Kuipers, O., Budisa, N., Prospects of in vivo incorporation of noncanonical amino acids for the chemical diversification of antimicrobial peptides. Front Microbiol, 8, 2017, 124.
4. 4 Schmidt, M.J., Summerer, D., Genetic code expansion as a tool to study regulatory processes of transcription. Front Chem, 2, 2014, 7.
5. 5 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, 5, 2015, 9699.
6. 6 Johnson, D.B.F., 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 7 (2011), 779–786.
7. 7 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 342 (2013), 357–360.
8. 8 Bohlke, N., Budisa, N., Sense codon emancipation for proteome-wide incorporation of noncanonical amino acids: rare isoleucine codon AUA as a target for genetic code expansion. FEMS Microbiol Lett 351 (2014), 133–144.
9. 9 Kwon, I., Kirshenbaum, K., Tirrell, D.A., Breaking the degeneracy of the genetic code. J Am Chem Soc 125 (2003), 7512–7513.
10. 10•• Anderhuber, N., Fladischer, P., Gruber-Khadjawi, M., Mairhofer, J., Striedner, G., Wiltschi, B., High-level biosynthesis of norleucine in E. coli for the economic labeling of proteins. J Biotechnol 235 (2016), 100–111 The authors optimize the biosynthetic production of the ncAA norleucine for subsequent incorporation into proteins via SPI with a focus on large-scale bacterial cultures.
11. 11• Chubukov, V., Mukhopadhyay, A., Petzold, C.J., Keasling, J.D., Martín, H.G., Synthetic and systems biology for microbial production of commodity chemicals. NPJ Syst Biol Appl, 2, 2016, 16009 This review comprehensively explains the challenges and options in pathway optimization and up-scaling of bacterial fermentation.
12. 12 Seigler, D.S., (eds.) Plant Secondary Metabolism, 1998, Springer.
13. 13 Piel, J., Natural Products via Enzymatic Reactions. 2010, Springer.
14. 14 Kaur, J., Sharma, R., Directed evolution: an approach to engineer enzymes. Crit Rev Biotechnol 26 (2006), 165–199.
15. 15 Lee, J.W., Kim, T.Y., Jang, Y.-S., Choi, S., Lee, S.Y., Systems metabolic engineering for chemicals and materials. Trends Biotechnol 29 (2011), 370–378.
16. 16• Petzold, C.J., Chan, L.J.G., Nhan, M., Adams, P.D., Analytics for metabolic engineering. Front Bioeng Biotechnol, 3, 2015, 135 This is an excellent review for readers that are interested in analytical methods that can provide important information for metabolic engineering.
17. 17 Mehl, R.A., Anderson, J.C., Santoro, S.W., Wang, L., Martin, A.B., King, D.S., Horn, D.M., Schultz, P.G., Generation of a bacterium with a 21 amino acid genetic code. J Am Chem Soc 125 (2003), 935–939.
18. 18 Masuo, S., Zhou, S., Kaneko, T., Takaya, N., Bacterial fermentation platform for producing artificial aromatic amines. Sci Rep, 6, 2016, 25764.
19. 19 Di Salvo, M.L., Budisa, N., Contestabile, R., PLP-dependent enzymes: a powerful tool for metabolic synthesis of non-canonical amino acids. Beilstein Bozen Symposium on Molecular Engineering and Control, Beilstein Institute, Prien, 2013, 27–66.
20. 20 Maier, T.H., Semisynthetic production of unnatural L-alpha-amino acids by metabolic engineering of the cysteine-biosynthetic pathway. Nat Biotechnol 21 (2003), 422–427.
21. 21•• Exner, M.P., Kuenzl, T., To, T.M.T., Ouyang, Z., Schwagerus, S., Hoesl, M.G., Hackenberger, C.P.R., Lensen, M.C., Panke, S., Budisa, N., Design of S-allylcysteine in situ production and incorporation based on a novel pyrrolysyl-tRNA synthetase variant. ChemBioChem 18 (2017), 85–90 The authors show that the Cys biosynthetic pathway can be used for the generation of a novel ncAA, which they incorporated site-specifically into proteins via a newly identified PylRS mutant. This is an elegant coupling of simple metabolic conversion with GCE.
22. 22 Broos, J., Gabellieri, E., Biemans-Oldehinkel, E., Strambini, G.B., Efficient biosynthetic incorporation of tryptophan and indole analogs in an integral membrane protein. Protein Sci 12 (2003), 1991–2000.
23. 23 Lepthien, S., Hoesl, M.G., Merkel, L., Budisa, N., Azatryptophans endow proteins with intrinsic blue fluorescence. Proc Natl Acad Sci U S A 105 (2008), 16095–16100.
24. 24 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 471 (2011), 647–650.
25. 25 Cellitti, S.E., Ou, W., Chiu, H.-P., Grunewald, J., Jones, D.H., Hao, X., Fan, Q., Quinn, L.L., Ng, K., Anfora, A.T., et al. D-Ornithine coopts pyrrolysine biosynthesis to make and insert pyrroline-carboxy-lysine. Nat Chem Biol 7 (2011), 528–530.
26. 26 Ou, W., Uno, T., Chiu, H.-P., Grunewald, J., Cellitti, S.E., Crossgrove, T., Hao, X., Fan, Q., Quinn, L.L., Patterson, P., et al. Site-specific protein modifications through pyrroline-carboxy-lysine residues. Proc Natl Acad Sci U S A 108 (2011), 10437–10442.
27. 27• Ehrlich, M., Gattner, M.J., Viverge, B., Bretzler, J., Eisen, D., Stadlmeier, M., Vrabel, M., Carell, T., Orchestrating the biosynthesis of an unnatural pyrrolysine amino acid for its direct incorporation into proteins inside living cells. Chemistry 21 (2015), 7701–7704 This work incorporates the Pyl biosynthesis pathway and the wild-type PylRS into E. coli for biosynthesis and subsequent incorporation of an alkyne-bearing Pyl analogue into proteins, offering the possibility to use two different orthogonal click reactions.
28. 28 Welch, M., Phillips, R.S., Enzymatic syntheses of 6-(4H-selenolo3,2-bpyrrolyl)-L-alanine, 4-(6H-selenolo2,3-bpyrrolyl)-L-alanine, and 6-(4H-furo3,2-bpyrrolyl)-L-alanine. Bioorg Med Chem Lett 9 (1999), 637–640.
29. 29 Phillips, R.S., Cohen, L.A., Annby, U., Wensbo, D., Gronowitz, S., Enzymatic synthesis of Thia-L-tryptophans. Bioorg Med Chem Lett 5 (1995), 1133–1134.
30. 30 Goss, R.J.M., Newill, P.L.A., A convenient enzymatic synthesis of L-halotryptophans. Chem Commun (Camb), 2006, 4924–4925.
31. 31• Herger, M., van Roye, P., Romney, D.K., Brinkmann-Chen, S., Buller, A.R., Arnold, F.H., Synthesis of beta-branched tryptophan analogues using an engineered subunit of tryptophan synthase. J Am Chem Soc 138 (2016), 8388–8391 This work uses directed evolution to change an enzyme's reaction preferences towards novel ncAAs.
32. 32 Borrel, G., Gaci, N., Peyret, P., O'Toole, P.W., Gribaldo, S., Brugere, J.-F., Unique characteristics of the pyrrolysine system in the 7th order of methanogens: implications for the evolution of a genetic code expansion cassette. Archaea, 2014, 2014, 374146.
33. 33 Ma, Y., Biava, H., Contestabile, R., Budisa, N., Di Salvo, M.L., Coupling bioorthogonal chemistries with artificial metabolism: intracellular biosynthesis of azidohomoalanine and its incorporation into recombinant proteins. Molecules 19 (2014), 1004–1022.
34. 34 Sycheva, E.V., Yampol'skaya, T.A., Preobrajenskaya, E.S., Novikova, A.E., Matrosov, N.G., Stoynova, N.V., Overproduction of noncanonical amino acids by Escherichia coli cells. Microbiology 76 (2007), 712–718.
35. 35 Brooks, A.N., Turkarslan, S., Beer, K.D., Lo, F.Y., Baliga, N.S., Adaptation of cells to new environments. Wiley Interdiscip Rev Syst Biol Med 3 (2011), 544–561.
36. 36 Lee, Y., Lafontaine Rivera, J.G., Liao, J.C., Ensemble modeling for robustness analysis in engineering non-native metabolic pathways. Metab Eng 25 (2014), 63–71.
37. 37•• Hoesl, M.G., Oehm, S., Durkin, P., Darmon, E., Peil, L., Aerni, H.-R., Rappsilber, J., Rinehart, J., Leach, D., Söll, D., et al. Chemical evolution of a bacterial proteome. Angew Chem Int Ed Engl 54 (2015), 10030–10034 First report on successful and unambiguous adaptation of E. coli to a particular ncAA. Evolved cells are tolerant towards proteome-wide incorporation of this ncAA and are thus able to robustly grow under SPI conditions.
38. 38• Kuthning, A., Durkin, P., Oehm, S., Hoesl, M.G., Budisa, N., Sussmuth, R.D., Towards biocontained cell factories: an evolutionarily adapted Escherichia coli strain produces a new-to-nature bioactive lantibiotic containing thienopyrrole-alanine. Sci Rep, 6, 2016, 33447 Usage of a metabolically engineered strain gained from directed evolution for the production of a novel lantibiotic containing an ncAA that was intracellularly produced by TrpS in the presence of a supplemented indole analogue.
39. 39 Budisa, N., Xenobiology, new-to-nature synthetic cells and genetic firewall. Curr Org Chem 18 (2014), 936–943.
40. 40 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 518 (2015), 89–93.
41. 41 Tack, D.S., Ellefson, J.W., Thyer, R., Wang, B., Gollihar, J., Forster, M.T., Ellington, A.D., Addicting diverse bacteria to a noncanonical amino acid. Nat Chem Biol 12 (2016), 138–140.
42. 42 Mandell, D.J., Lajoie, M.J., Mee, M.T., Takeuchi, R., Kuznetsov, G., Norville, J.E., Gregg, C.J., Stoddard, B.L., Church, G.M., Biocontainment of genetically modified organisms by synthetic protein design. Nature 518 (2015), 55–60.
43. 43 Wong, J.T.-F., Ng, S.-K., Mat, W.-K., Hu, T., Xue, H., Coevolution theory of the genetic code at age forty: pathway to translation and synthetic life. Life (Basel), 6, 2016, 12.
44. 44 Acevedo-Rocha, C., Budisa, N., Xenomicrobiology: a roadmap for genetic code engineering. Microb Biotechnol 9 (2016), 666–676.