Optimized orthogonal translation of unnatural amino acids enables spontaneous protein double-labelling and FRET (original) (raw)

• Zhang, J., Campbell, R. E., Ting, A. Y. & Tsien, R. Y. Creating new fluorescent probes for cell biology. Nature Rev. Mol. Cell Biol. 3, 906–918 (2002).
  CAS Google Scholar
• Kajihara, D. et al. FRET analysis of protein conformational change through position-specific incorporation of fluorescent amino acids. Nature Methods 3, 923–929 (2006).
  CAS PubMed Google Scholar
• Scott, C.P., Abel-Santos, E., Wall, M., Wahnon, D. C. & Benkovic, S. J. Production of cyclic peptides and proteins in vivo. Proc. Natl Acad. Sci. USA 96, 13638–13643 (1999).
  CAS PubMed Google Scholar
• Li, P. & Roller, P. P. Cyclization strategies in peptide derived drug design. Curr. Top. Med. Chem. 2, 325–341 (2002).
  CAS PubMed Google Scholar
• Wang, K., Schmied, W. H. & Chin, J. W. Reprogramming the genetic code: from triplet to quadruplet codes. Angew. Chem. Int. Ed. 51, 2288–2297 (2012).
  CAS Google Scholar
• Davis, L. & Chin, J. W. Designer proteins: applications of genetic code expansion in cell biology. Nature Rev. Mol. Cell Biol. 13, 168–182 (2012).
  CAS Google Scholar
• Chin, J. W. Molecular biology. Reprogramming the genetic code. Science 336, 428–429 (2012).
  CAS PubMed Google Scholar
• Chin, J. W. Expanding and reprogramming the genetic code of cells and animals. Annu. Rev. Biochem. http://dx.doi.org/10.1146/annurev-biochem-060713-035737 (2014).
  Google Scholar
• 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 464, 441–444 (2010).
  CAS PubMed Google Scholar
• Rackham, O. & Chin, J. W. A network of orthogonal ribosome X mRNA pairs. Nature Chem. Biol. 1, 159–166 (2005).
  CAS Google Scholar
• Wang, K., Neumann, H., Peak-Chew, S. Y. & Chin, J. W. Evolved orthogonal ribosomes enhance the efficiency of synthetic genetic code expansion. Nature Biotechnol. 25, 770–777 (2007).
  Google Scholar
• An, W. & Chin, J. W. Synthesis of orthogonal transcription–translation networks. Proc. Natl Acad. Sci. USA 106, 8477–8482 (2009).
  CAS PubMed Google Scholar
• Atkins, J. F. & Bjork, G. R. A gripping tale of ribosomal frameshifting: extragenic suppressors of frameshift mutations spotlight P-site realignment. Microbiol. Mol. Biol. Rev. 73, 178–210 (2009).
  CAS PubMed PubMed Central Google Scholar
• Stahl, G., McCarty, G. P. & Farabaugh, P. J. Ribosome structure: revisiting the connection between translational accuracy and unconventional decoding. Trends Biochem. Sci. 27, 178–183 (2002).
  CAS PubMed Google Scholar
• Wan, W. et al. A facile system for genetic incorporation of two different noncanonical amino acids into one protein in Escherichia coli. Angew. Chem. Int. Ed. 49, 3211–3214 (2010).
  CAS Google Scholar
• Wu, B., Wang, Z., Huang, Y. & Liu, W. R. Catalyst-free and site-specific one-pot dual-labeling of a protein directed by two genetically incorporated noncanonical amino acids. ChemBioChem 13, 1405–1408 (2012).
  CAS PubMed PubMed Central Google Scholar
• Chatterjee, A., Sun, S. B., Furman, J. L., Xiao, H. & Schultz, P. G. A versatile platform for single- and multiple-unnatural amino acid mutagenesis in Escherichia coli. Biochemistry 52, 1828–1837 (2013).
  CAS PubMed Google Scholar
• Ambrogelly, A. et al. Pyrrolysine is not hardwired for cotranslational insertion at UAG codons. Proc. Natl Acad. Sci. USA 104, 3141–3146 (2007).
  CAS PubMed Google Scholar
• Jiang, R. & Krzycki, J. A. PylSn and the homologous N-terminal domain of pyrrolysyl-tRNA synthetase bind the tRNA that is essential for the genetic encoding of pyrrolysine. J. Biol. Chem. 287, 32738–32746 (2012).
  CAS PubMed PubMed Central Google Scholar
• Magliery, T. J., Anderson, J. C. & Schultz, P. G. Expanding the genetic code: selection of efficient suppressors of four-base codons and identification of ‘shifty’ four-base codons with a library approach in Escherichia coli. J. Mol. Biol. 307, 755–769 (2001).
  CAS PubMed Google Scholar
• Niu, W., Schultz, P. G. & Guo, J. An expanded genetic code in mammalian cells with a functional quadruplet codon. ACS Chem. Biol. 8, 1640–1645 (2013).
  CAS PubMed PubMed Central Google Scholar
• Beuning, P. J. & Musier-Forsyth, K. Transfer RNA recognition by aminoacyl-tRNA synthetases. Biopolymers 52, 1–28 (1999).
  CAS PubMed Google Scholar
• Chin, J. W. et al. Addition of _p_-azido-l-phenylalanine to the genetic code of Escherichia coli. J. Am. Chem. Soc. 124, 9026–9027 (2002).
  CAS PubMed Google Scholar
• Yanagisawa, T. et al. Multistep engineering of pyrrolysyl-tRNA synthetase to genetically encode _N_ɛ-(_o_-azidobenzyloxycarbonyl) lysine for site-specific protein modification. Chem. Biol. 15, 1187–1197 (2008).
  CAS PubMed Google Scholar
• Nguyen, D. P. et al. Genetic encoding and labeling of aliphatic azides and alkynes in recombinant proteins via pyrrolysyl-tRNA synthetase/tRNA CUAPair and click chemistry. J. Am. Chem. Soc. 131, 8720–8721 (2009).
  CAS PubMed Google Scholar
• Deiters, A. & Schultz, P. G. In vivo incorporation of an alkyne into proteins in Escherichia coli. Bioorg. Med. Chem. Lett. 15, 1521–1524 (2005).
  CAS PubMed Google Scholar
• Seitchik, J. L. et al. Genetically encoded tetrazine amino acid directs rapid site-specific in vivo bioorthogonal ligation with _trans_-cyclooctenes. J. Am. Chem. Soc. 134, 2898–2901 (2012).
  CAS PubMed PubMed Central Google Scholar
• Chin, J. W., Martin, A. B., King, D. S., Wang, L. & Schultz, P. G. Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc. Natl Acad. Sci. 99, 11020–11024 (2002).
  CAS PubMed Google Scholar
• Sasmal, P. K. et al. Catalytic azide reduction in biological environments. ChemBioChem 13, 1116–1120 (2012).
  CAS PubMed Google Scholar
• Blackman, M. L., Royzen, M. & Fox, J. M. Tetrazine ligation: fast bioconjugation based on inverse-electron-demand Diels–Alder reactivity. J. Am. Chem. Soc. 130, 13518–13519 (2008).
  CAS PubMed PubMed Central Google Scholar
• Devaraj, N. K. & Weissleder, R. Biomedical applications of tetrazine cycloadditions. Acc. Chem. Res. 44, 816–827 (2011).
  CAS PubMed PubMed Central Google Scholar
• Lang, K. & Chin, J. W. Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chem. Rev. http://dx.doi.org/10.1021/cr400355w (2014).
• Lang, K. et al. Genetically encoded norbornene directs site-specific cellular protein labelling via a rapid bioorthogonal reaction. Nature Chem. 4, 298–304 (2012).
  CAS Google Scholar
• Lang, K. et al. Genetic encoding of bicyclononynes and _trans_-cyclooctenes for site-specific protein labeling in vitro and in live mammalian cells via rapid fluorogenic Diels–Alder reactions. J. Am. Chem. Soc. 134, 10317–10320 (2012).
  CAS PubMed PubMed Central Google Scholar
• Plass, T. et al. Amino acids for Diels–Alder reactions in living cells. Angew. Chem. Int. Ed. 51, 4166–4170 (2012).
  CAS Google Scholar
• Borrmann, A. et al. Genetic encoding of a bicyclo[6.1.0]nonyne-charged amino acid enables fast cellular protein imaging by metal-free ligation. ChemBioChem 13, 2094–2099 (2012).
  CAS PubMed Google Scholar
• Balcar, J., Chrisam, G., Huber, F. X. & Sauer, J. Reaktivitaet von Stickstoff-Heterocyclen gegenueber Cyclooctin als Dienophil. Tetrahedron Lett. 24, 1481–1484 (1983).
  CAS Google Scholar
• Thalhammer, F., Wallfahrer, U. & Sauer, J. Reaktivitaet einfacher offenkettiger und cyclischer Dienophile bei Diels–Alder Reaktionen mit inversem Elektronenbedarf. Tetrahedron Lett. 31, 6851–6854 (1990).
  CAS Google Scholar
• Kaya, E. et al. A Genetically encoded norbornene amino acid for the mild and selective modification of proteins in a copper-free click reaction. Angew. Chem. Int. Ed. 51, 4466–4469 (2012).
  CAS Google Scholar
• Lang, K. & Chin, J. W. Bioorthogonal reactions for labeling proteins. ACS Chem. Biol. 9, 16–20 (2014).
  CAS PubMed Google Scholar
• Hellstrand, E. et al. Förster resonance energy transfer studies of calmodulin produced by native protein ligation reveal inter-domain electrostatic repulsion. FEBS J 280, 2675–2687 (2013).
  CAS PubMed Google Scholar
• Wissner, R. F., Batjargal, S., Fadzen, C. M. & Petersson, E. J. Labeling proteins with fluorophore/thioamide Förster resonant energy transfer pairs by combining unnatural amino acid mutagenesis and native chemical ligation. J. Am. Chem. Soc. 135, 6529–6540 (2013).
  CAS PubMed PubMed Central Google Scholar
• Hoeflich, K. P. & Ikura, M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108, 739–742 (2002).
  CAS PubMed Google Scholar
• Carafoli, E. Calcium signaling: a tale for all seasons. Proc. Natl Acad. Sci. USA 99, 1115–1122 (2002).
  CAS PubMed Google Scholar
• Taylor, D. A., Sack, J. S., Maune, J. F., Beckingham, K. & Quiocho, F. A. Structure of a recombinant calmodulin from Drosophila melanogaster refined at 2.2-A resolution. J. Biol. Chem. 266, 21375–21380 (1991).
  CAS PubMed Google Scholar
• Fallon, J. L. & Quiocho, F. A. A closed compact structure of native Ca2+-calmodulin. Structure 11, 1303–1307 (2003).
  CAS PubMed Google Scholar
• Linse, S., Helmersson, A. & Forsen, S. Calcium binding to calmodulin and its globular domains. J. Biol. Chem. 266, 8050–8054 (1991).
  CAS PubMed Google Scholar
• Babu, Y. S. et al. Three-dimensional structure of calmodulin. Nature 315, 37–40 (1985).
  CAS PubMed Google Scholar
• Chou, J. J., Li, S., Klee, C. B. & Bax, A. Solution structure of Ca2+-calmodulin reveals flexible hand-like properties of its domains. Nature Struct. Biol. 8, 990–997 (2001).
  CAS PubMed Google Scholar
• Johnson, C. K. Calmodulin, conformational states, and calcium signaling. A single-molecule perspective. Biochemistry 45, 14233–14246 (2006).
  CAS PubMed PubMed Central Google Scholar
• Wu, G., Gao, Z., Dong, A. & Yu, S. Calcium-induced changes in calmodulin structural dynamics and thermodynamics. Int. J. Biol. Macromol. 50, 1011–1017 (2012).
  CAS PubMed Google Scholar
• Porumb, T. Determination of calcium-binding constants by flow dialysis. Anal. Biochem. 220, 227–237 (1994).
  CAS PubMed Google Scholar
• Haiech, J., Klee, C. B. & Demaille, J. G. Effects of cations on affinity of calmodulin for calcium: ordered binding of calcium ions allows the specific activation of calmodulin-stimulated enzymes. Biochemistry 20, 3890–3897 (1981).
  CAS PubMed Google Scholar
• Stefan, M. I., Edelstein, S. J. & Le Novere, N. An allosteric model of calmodulin explains differential activation of PP2B and CaMKII. Proc. Natl Acad. Sci. USA 105, 10768–10773 (2008).
  CAS PubMed Google Scholar