Labeling proteins on live mammalian cells using click chemistry

Nature Protocols

Volumn 10, Issue 5, 2015, Pages 780-791

  Nikic, Ivana ^a   Kang, Jun Hee ^a   Girona, Gemma Estrada ^a   Aramburu, Iker Valle ^a   Lemke, Edward A ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKENE; ALKYNE; AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; CELL SURFACE PROTEIN; INSULIN RECEPTOR; NONCANONICAL AMINO ACID; UNCLASSIFIED DRUG; ALEXA FLUOR 647; AZIDE; CARBOCYANINE; CYANINE DYE 5; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; PROTEIN; STOP CODON;

AMBER STOP CODON; ARTICLE; CELL LABELING; CLICK CHEMISTRY; CYCLOADDITION; EXPERIMENTAL DESIGN; GENETIC TRANSFECTION; HEK293 CELL LINE; HYDROPHOBICITY; INCUBATION TIME; INTERMETHOD COMPARISON; INTRACELLULAR SIGNALING; LIVE MAMMALIAN CELL; MAMMAL CELL; MOLECULAR CLONING; MOLECULAR DYNAMICS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; STOP CODON; STRAIN PROMOTED ALKYNE AZIDE CYCLOADDITION; STRAIN PROMOTED INVERSE ELECTRON DEMAND DIELS ALDER CYCLOADDITION; STRUCTURE ACTIVITY RELATION; ANIMAL; CHEMISTRY; DEVICES; GENETICS; HUMAN; MAMMAL; METABOLISM; PROCEDURES;

ALNUS; MAMMALIA;

ALKYNES; AMINO ACIDS; AMINO ACYL-TRNA SYNTHETASES; ANIMALS; AZIDES; CARBOCYANINES; CLICK CHEMISTRY; CODON, TERMINATOR; CYCLOADDITION REACTION; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MAMMALS; MUTAGENESIS, SITE-DIRECTED; PROTEINS; RECEPTOR, INSULIN;

EID: 84929484088     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2015.045     Document Type: Article

References (56)

1. Glaeser, J., Nuss, A.M., Berghoff, B.A. & Klug, G. Singlet oxygen stress in microorganisms. Adv. Microb. Physiol. 58, 141-173 (2011).
2. Chudakov, D.M., Matz, M.V., Lukyanov, S. & Lukyanov, K.A. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol. Rev. 90, 1103-1163 (2010).
3. Fernandez-Suarez, M. & Ting, A.Y. Fluorescent probes for super-resolution imaging in living cells. Nat. Rev. Mol. Cell Biol. 9, 929-943 (2008).
4. van de Linde, S., Heilemann, M. & Sauer, M. Live-cell super-resolution imaging with synthetic fluorophores. Annu. Rev. Phys. Chem. 63, 519-540 (2012).
5. Milles, S. & Lemke, E.A. What precision-protein-tuning and nano-resolved single molecule sciences can do for each other. BioEssays 35, 65-74 (2013).
6. Griffin, B.A., Adams, S.R. & Tsien, R.Y. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272 (1998).
7. Adams, S.R. et al. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124, 6063-6076 (2002).
8. Keppler, A. et al. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21, 86-89 (2003).
9. Gautier, A. et al. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15, 128-136 (2008).
10. Los, G.V. & Wood, K. The HaloTag: a novel technology for cell imaging and protein analysis. Methods Mol. Biol. 356, 195-208 (2007).
11. Miller, L.W., Cai, Y., Sheetz, M.P. & Cornish, V.W. In vivo protein labeling with trimethoprim conjugates: a flexible chemical tag. Nat. Methods 2, 255-257 (2005).
12. Uttamapinant, C. et al. A fluorophore ligase for site-specific protein labeling inside living cells. Proc. Natl. Acad. Sci. USA 107, 10914-10919 (2010).
13. Uttamapinant, C. et al. Fast, cell-compatible click chemistry with copper-chelating azides for biomolecular labeling. Angew. Chem. Int. Ed. Engl. 51, 5852-5856 (2012).
14. Wang, L. & Schultz, P.G. Expanding the genetic code. Angew. Chem. Int. Ed. Engl. 44, 34-66 (2004).
15. Liu, C.C. & Schultz, P.G. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79, 413-444 (2010).
16. Lemke, E.A. The exploding genetic code. Chembiochem 15, 1691-1694 (2014).
17. Lang, K. & Chin, J.W. Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. Chem. Rev. 114, 4764-4806 (2014).
18. Wang, J., Xie, J. & Schultz, P.G. A genetically encoded fluorescent amino acid. J. Am. Chem. Soc. 128, 8738-8739 (2006).
19. Jewett, J.C. & Bertozzi, C.R. Cu-free click cycloaddition reactions in chemical biology. Chem. Soc. Rev. 39, 1272-1279 (2010).
20. Agard, N.J., Prescher, J.A. & Bertozzi, C.R. A strain-promoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126, 15046-15047 (2004).
21. Wiessler, M., Waldeck, W., Kliem, C., Pipkorn, R. & Braun, K. The Diels-Alder-reaction with inverse-electron-demand, a very efficient versatile click-reaction concept for proper ligation of variable molecular partners. Int. J. Med. Sci. 7, 19-28 (2009).
22. 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).
23. Kolb, H.C., Finn, M.G. & Sharpless, K.B. Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. Engl. 40, 2004-2021 (2001).
24. Rostovtsev, V.V., Green, L.G., Fokin, V.V. & Sharpless, K.B. A stepwise Huisgen cycloaddition process: copper(I)-catalyzed regioselective 'ligation' of azides and terminal alkynes. Angew. Chem. Int. Ed. Engl. 41, 2596-2599 (2002).
25. Plass, T., Milles, S., Koehler, C., Schultz, C. & Lemke, E.A. Genetically encoded copper-free click chemistry. Angew. Chem. Int. Ed. Engl. 50, 3878-3881 (2011).
26. Plass, T. et al. Amino acids for Diels-Alder reactions in living cells. Angew. Chem. Int. Ed. Engl. 51, 4166-4170 (2012).
27. Elliott, T.S. et al. Proteome labeling and protein identification in specific tissues and at specific developmental stages in an animal. Nat. Biotechnol. 32, 465-472 (2014).
28. Nikic, I. et al. Minimal tags for rapid dual-color live-cell labeling and super-resolution microscopy. Angew. Chem. Int. Ed. Engl. 53, 2245-2249 (2014).
29. Raulf, A. et al. Click chemistry facilitates direct labelling and super-resolution imaging of nucleic acids and proteins. RSC Adv. 4, 30462-30466 (2014).
30. Zhou, P. et al. Multicolor labeling of living-virus particles in live cells. Angew. Chem. Int. Ed. Engl. 51, 670-674 (2012).
31. Milles, S. et al. Click strategies for single-molecule protein fluorescence. J. Am. Chem. Soc. 134, 5187-5195 (2012).
32. Sun, S.B., Schultz, P.G. & Kim, C.H. Therapeutic applications of an expanded genetic code. Chembiochem 15, 1721-1729 (2014).
33. Patterson, D.M., Nazarova, L.A. & Prescher, J.A. Finding the right (bioorthogonal) chemistry. ACS Chem. Biol. 9, 592-605 (2014).
34. Liu, D.S. et al. Diels-Alder cycloaddition for fluorophore targeting to specific proteins inside living cells. J. Am. Chem. Soc. 134, 792-795 (2012).
35. Uttamapinant, C., Sanchez, M.I., Liu, D.S., Yao, J.Z. & Ting, A.Y. Site-specific protein labeling using PRIME and chelation-assisted click chemistry. Nat. Protoc. 8, 1620-1634 (2013).
36. Lee, H.S., Guo, J., Lemke, E.A., Dimla, R.D. & Schultz, P.G. Genetic incorporation of a small, environmentally sensitive, fluorescent probe into proteins in Saccharomyces cerevisiae. J. Am. Chem. Soc. 131, 12921-12923 (2009).
37. Summerer, D. et al. A genetically encoded fluorescent amino acid. Proc. Natl. Acad. Sci. USA 103, 9785-9789 (2006).
38. Herner, A. et al. New generation of bioorthogonally applicable fluorogenic dyes with visible excitations and large stokes shifts. Bioconjug. Chem. 25, 1370-1374 (2014).
39. Herner, A., Nikic, I., Kallay, M., Lemke, E.A. & Kele, P. A new family of bioorthogonally applicable fluorogenic labels. Org. Biomol. Chem. 11, 3297-3306 (2013).
40. Lukinavicius, G. et al. A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat. Chem. 5, 132-139 (2013).
41. Meimetis, L.G., Carlson, J.C., Giedt, R.J., Kohler, R.H. & Weissleder, R. Ultrafluorogenic coumarin-tetrazine probes for real-time biological imaging. Angew. Chem. Int. Ed. Engl. 53, 7531-7534 (2014).
42. 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. Soc. 134, 10317-10320 (2012).
43. 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).
44. Parrish, A.R. et al. Expanding the genetic code of Caenorhabditis elegans using bacterial aminoacyl-tRNA synthetase/tRNA pairs. ACS Chem. Biol. 7, 1292-1302 (2012).
45. Greiss, S. & Chin, J.W. Expanding the genetic code of an animal. J. Am. Chem. Soc. 133, 14196-14199 (2011).
46. Carey, M.F., Peterson, C.L. & Smale, S.T. PCR-mediated site-directed mutagenesis. Cold Spring Harb. Protoc. 2013, 738-742 (2013).
47. Pott, M., Schmidt, M.J. & Summerer, D. Evolved sequence contexts for highly efficient amber suppression with noncanonical amino acids. ACS Chem. Biol. 9, 2815-2822 (2014).
48. Beier, H. & Grimm, M. Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res. 29, 4767-4782 (2001).
49. Phillips-Jones, M.K., Hill, L.S., Atkinson, J. & Martin, R. Context effects on misreading and suppression at UAG codons in human cells. Mol. Cell. Biol. 15, 6593-6600 (1995).
50. Yanagisawa, T. et al. Multistep engineering of pyrrolysyl-tRNA synthetase to genetically encode N(?)-(o-azidobenzyloxycarbonyl) lysine for site-specific protein modification. Chem. Biol. 15, 1187-1197 (2008).
51. Mizuguchi, H., Xu, Z., Ishii-Watabe, A., Uchida, E. & Hayakawa, T. IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol. Ther. 1, 376-382 (2000).
52. Ryan, M.D. & Drew, J. Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J. 13, 928-933 (1994).
53. Lang, K. et al. Genetically encoded norbornene directs site-specific cellular protein labelling via a rapid bioorthogonal reaction. Nat. Chem. 4, 298-304 (2012).
54. Sauer, J., Mielert, A., Lang, D. & Peter, D. Eine studie der Diels-Alder-reaktion, III: umsetzungen von 1.2.4.5-tetrazinen mit olefinen. Zur dtruktur von dihydropyridazinen. Chemische Berichte 98, 1435-1445 (1965).
55. 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. Engl. 51, 4466-4469 (2012).
56. Li, J., Jia, S. & Chen, P.R. Diels-Alder reaction-triggered bioorthogonal protein decaging in living cells. Nat. Chem. Biol. 10, 1003-1005 (2014).