Enzymatic labeling of proteins: Techniques and approaches

Bioconjugate Chemistry

Volumn 24, Issue 8, 2013, Pages 1277-1294

  Rashidian, Mohammad ^a   Dozier, Jonathan K ^a   Distefano, Mark D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL MODIFICATION;

BIOLOGY AND MEDICINE; CHEMICAL BIOLOGY; LABELINGS; LIGASES; NATURALLY OCCURRING; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN IMMOBILIZATION; PROTEIN MODIFICATIONS; REACTIVE FUNCTIONAL GROUPS; SITE-SPECIFIC MODIFICATIONS;

ENZYMES;

BIOTIN LIGASE; LIGASE; LIPOIC ACID LIGASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN N MYRISTOYLTRANSFERASE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; ENZYME; PROTEIN;

ENZYME ASSAY; MYRISTYLATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REVIEW; SIALYLATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROCEDURES; STAINING;

AMINO ACID SEQUENCE; ANIMALS; ENZYMES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; STAINING AND LABELING;

EID: 84883183094     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc400102w     Document Type: Review

References (138)

1. Hackenberger, C. P. R. and Schwarzer, D. (2008) Chemoselective Ligation and Modification Strategies for Peptides and Proteins Angew. Chem., Int. Ed. 47, 10030-10074
2. Rabuka, D. (2010) Chemoenzymatic methods for site-specific protein modification Curr. Opin. Chem. Biol. 14, 790-796
3. Carrico, I. S. (2008) Chemoselective modification of proteins: hitting the target Chem. Soc. Rev. 37, 1423
4. Wong, S. S., Jameson, D. M., and Wong, S. S. (2012) Chemistry of protein and nucleic acid cross-linking and conjugation, Taylor & Francis/CRC Press, Boca Raton.
5. Fontana, A., Spolaore, B., Mero, A., and Veronese, F. M. (2008) Site-specific modification and PEGylation of pharmaceutical proteins mediated by transglutaminase Adv. Drug Delivery Rev. 60, 13-28
6. Junutula, J. R., Raab, H., Clark, S., Bhakta, S., Leipold, D. D., Weir, S., Chen, Y., Simpson, M., Tsai, S. P., Dennis, M. S., Lu, Y., Meng, Y. G., Ng, C., Yang, J., Lee, C. C., Duenas, E., Gorrell, J., Katta, V., Kim, A., McDorman, K., Flagella, K., Venook, R., Ross, S., Spencer, S. D., Lee Wong, W., Lowman, H. B., Vandlen, R., Sliwkowski, M. X., Scheller, R. H., Polakis, P., and Mallet, W. (2008) Site-specific conjugation of a cytotoxic drug to an antibody improves the therapeutic index Nat. Biotechnol. 26, 925-932
7. Gauchet, C., Labadie, G. R., and Poulter, C. D. (2006) Regio- and chemoselective covalent immobilization of proteins through unnatural amino acids J. Am. Chem. Soc. 128, 9274-9275
8. Kochendoerfer, G. G. (2005) Site-specific polymer modification of therapeutic proteins Curr. Opin. Chem. Biol. 9, 555-560
9. Chen, I., Howarth, M., Lin, W., and Ting, A. Y. (2005) Site-specific labeling of cell surface proteins with biophysical probes using biotin ligase Nat. Meth. 2, 99-104
10. Köhn, M. (2009) Immobilization strategies for small molecule, peptide and protein microarrays J. Pept. Sci. 15, 393-397
11. Wong, L. S., Khan, F., and Micklefield, J. (2009) Selective covalent protein immobilization: strategies and applications Chem. Rev. 109, 4025-4053
12. Tiefenbrunn, T. K. and Dawson, P. E. (2010) Chemoselective ligation techniques: Modern applications of time-honored chemistry Biopolymers 94, 95-106
13. Wu, B.-Y., Hou, S.-H., Huang, L., Yin, F., Zhao, Z.-X., Anzai, J.-I., and Chen, Q. (2008) Oriented immobilization of immunoglobulin G onto the cuvette surface of the resonant mirror biosensor through layer-by-layer assembly of multilayer films Mater. Sci. Eng., C 28, 1065-1069
14. Hermanson, G. T. (2008) Bioconjugate techniques, Academic Press, Amsterdam.
15. Dixon, H. B. (1964) Transamination of peptides Biochem. J. 92, 661-666
16. Wu, P. and Brand, L. (1997) N-terminal modification of proteins for fluorescence measurements Meth. Enzymol. 278, 321-330
17. Scheck, R. A., Dedeo, M. T., Iavarone, A. T., and Francis, M. B. (2008) Optimization of a biomimetic transamination reaction J. Am. Chem. Soc. 130, 11762-11770
18. Geoghegan, K. F. and Stroh, J. G. (1992) Site-directed conjugation of nonpeptide groups to peptides and proteins via periodate oxidation of a 2-amino alcohol. Application to modification at N-terminal serine Bioconjugate Chem. 3, 138-146
19. Akgul, C., Moulding, D. A., White, M. R.., and Edwards, S. W. (2000) In vivo localisation and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins FEBS Lett. 478, 72-76
20. Dundr, M., McNally, J. G., Cohen, J., and Misteli, T. (2002) Quantitation of GFP-fusion proteins in single living cells J. Struct. Biol. 140, 92-99
21. Kanda, T., Sullivan, K. F., and Wahl, G. M. (1998) Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells Curr. Biol. 8, 377-385
22. Marguet, D., Spiliotis, E. T., Pentcheva, T., Lebowitz, M., Schneck, J., and Edidin, M. (1999) Lateral diffusion of GFP-tagged H2Ld molecules and of GFP-TAP1 reports on the assembly and retention of these molecules in the endoplasmic reticulum Immunity 11, 231-240
23. Lisenbee, C. S., Karnik, S. K., and Trelease, R. N. (2003) Overexpression and mislocalization of a tail-anchored GFP redefines the identity of peroxisomal ER Traffic 4, 491-501
24. De Graaf, A. J., Kooijman, M., Hennink, W. E., and Mastrobattista, E. (2009) Nonnatural amino acids for site-specific protein conjugation Bioconjugate Chem. 20, 1281-1295
25. Wang, L., Xie, J., and Schultz, P. G. (2006) Expanding the genetic code Annu. Rev. Biophys. Biomol. Struct. 35, 225-249
26. Chen, P. R., Groff, D., Guo, J., Ou, W., Cellitti, S., Geierstanger, B. H., and Schultz, P. G. (2009) A facile system for encoding unnatural amino acids in mammalian cells Angew. Chem., Int. Ed. 48, 4052-4055
27. Guo, J., Melancon, C. E., Lee, H. S., Groff, D., and Schultz, P. G. (2009) Evolution of amber suppressor tRNAs for efficient bacterial production of proteins containing nonnatural amino acids Angew. Chem., Int. Ed. 48, 9148-9151
28. Chatterjee, A., Xiao, H., and Schultz, P. G. (2012) Evolution of multiple, mutually orthogonal prolyl-tRNA synthetase/tRNA pairs for unnatural amino acid mutagenesis in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 109, 14841-14846
29. Huisgen, R., Szeimies, G., and Mobius, L. (1967) Chemische Berichte-Recueil Chem. Ber. 100, 2494
30. Rostovtsev, V. V., Green, L. G., Fokin, V. V., and Sharpless, K. B. (2002) A stepwise huisgen cycloaddition process: copper(I)-catalyzed regioselective "ligation" of azides and terminal alkynes Angew. Chem., Int. Ed. 41, 2596-2599
31. Kolb, H. C., Finn, M. G., and Sharpless, K. B. (2001) Click chemistry: diverse chemical function from a few good reactions Angew. Chem., Int. Ed. 40, 2004-2021
32. Köhn, M. and Breinbauer, R. (2004) The Staudinger ligation-a gift to chemical biology Angew. Chem., Int. Ed. 43, 3106-3116
33. Song, W., Wang, Y., Qu, J., Madden, M. M., and Lin, Q. (2008) A photoinducible 1,3-dipolar cycloaddition reaction for rapid, selective modification of tetrazole-containing proteins Angew. Chem., Int. Ed. 47, 2832-2835
34. Song, W., Wang, Y., Qu, J., and Lin, Q. (2008) Selective functionalization of a genetically encoded alkene-containing protein via "photoclick chemistry" in bacterial cells J. Am. Chem. Soc. 130, 9654-9655
35. De Araújo, A. D., Palomo, J. M., Cramer, J., Seitz, O., Alexandrov, K., and Waldmann, H. (2006) Diels-Alder ligation of peptides and proteins Chem.-Eur. J. 12, 6095-6109
36. De Araújo, A. D., Palomo, J. M., Cramer, J., Köhn, M., Schröder, H., Wacker, R., Niemeyer, C., Alexandrov, K., and Waldmann, H. (2006) Diels-Alder ligation and surface immobilization of proteins Angew. Chem., Int. Ed. 45, 296-301
37. Liu, D. S., Tangpeerachaikul, A., Selvaraj, R., Taylor, M. T., Fox, J. M., and Ting, A. Y. (2012) Diels-Alder cycloaddition for fluorophore targeting to specific proteins inside living cells J. Am. Chem. Soc. 134, 792-795
38. Blackman, M. L., Royzen, M., and Fox, J. M. (2008) Tetrazine ligation: fast bioconjugation based on inverse-electron-demand Diels-Alder reactivity J. Am. Chem. Soc. 130, 13518-13519
39. Schoch, J., Wiessler, M., and Jäschke, A. (2010) Post-synthetic modification of DNA by inverse-electron-demand Diels-Alder reaction J. Am. Chem. Soc. 132, 8846-8847
40. Cordes, E. H. and Jencks, W. P. (1962) Nucleophilic catalysis of semicarbazone formation by anilines J. Am. Chem. Soc. 84, 826-831
41. Dirksen, A., Yegneswaran, S., and Dawson, P. E. (2010) Bisaryl hydrazones as exchangeable biocompatible linkers Angew. Chem., Int. Ed. 2023-2027
42. Rashidian, M., Song, J. M., Pricer, R. E., and Distefano, M. D. (2012) Chemoenzymatic reversible immobilization and labeling of proteins without prior purification J. Am. Chem. Soc. 134, 8455-8467
43. Miller, L. W. and Cornish, V. W. (2005) Selective chemical labeling of proteins in living cells Curr. Opin. Chem. Biol. 9, 56-61
44. Sunbul, M. and Yin, J. (2009) Site specific protein labeling by enzymatic posttranslational modification Org. Biomol. Chem. 7, 3361
45. Roeser, D., Preusser-Kunze, A., Schmidt, B., Gasow, K., Wittmann, J. G., Dierks, T., von Figura, K., and Rudolph, M. G. (2006) A general binding mechanism for all human sulfatases by the formylglycine-generating enzyme Proc. Natl. Acad. Sci. U.S.A. 103, 81-86
46. Rush, J. S. and Bertozzi, C. R. (2008) New aldehyde tag sequences identified by screening formylglycine generating enzymes in vitro and in vivo J. Am. Chem. Soc. 130, 12240-12241
47. Wu, P., Shui, W., Carlson, B. L., Hu, N., Rabuka, D., Lee, J., and Bertozzi, C. R. (2009) Site-specific chemical modification of recombinant proteins produced in mammalian cells by using the genetically encoded aldehyde tag Proc. Natl. Acad. Sci. U.S.A. 106, 3000-3005
48. Rabuka, D., Rush, J. S., deHart, G. W., Wu, P., and Bertozzi, C. R. (2012) Site-specific chemical protein conjugation using genetically encoded aldehyde tags Nat. Protoc. 7, 1052-1067
49. Bertozzi, C. R. and Kiessling, L. L. (2001) Chemical glycobiology Science 291, 2357-2364
50. Angata, T. and Varki, A. (2002) Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective Chem. Rev. 102, 439-469
51. Bork, K., Horstkorte, R., and Weidemann, W. (2009) Increasing the sialylation of therapeutic glycoproteins: the potential of the sialic acid biosynthetic pathway J. Pharm. Sci. 98, 3499-3508
52. Anthony, R. M. and Ravetch, J. V. (2010) A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs J. Clin. Immunol. 30 (Suppl 1) S9-14
53. Yu, H., Chokhawala, H., Karpel, R., Yu, H., Wu, B., Zhang, J., Zhang, Y., Jia, Q., and Chen, X. (2005) A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries J. Am. Chem. Soc. 127, 17618-17619
54. Yu, H., Huang, S., Chokhawala, H., Sun, M., Zheng, H., and Chen, X. (2006) Highly efficient chemoenzymatic synthesis of naturally occurring and non-natural α-2,6-linked sialosides: AP. damsela α-2,6- sialyltransferase with extremely flexible donor-substrate specificity Angew. Chem., Int. Ed. 45, 3938-3944
55. Khedri, Z., Muthana, M. M., Li, Y., Muthana, S. M., Yu, H., Cao, H., and Chen, X. (2012) Probe sialidase substrate specificity using chemoenzymatically synthesized sialosides containing C9-modified sialic acid Chem. Commun. 48, 3357-3359
56. Cane, D. E., Walsh, C. T., and Khosla, C. (1998) Harnessing the biosynthetic code: combinations, permutations, and mutations Science 282, 63-68
57. Marahiel, M. A., Stachelhaus, T., and Mootz, H. D. (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis Chem. Rev. 97, 2651-2674
58. Staunton, J. and Weissman, K. J. (2001) Polyketide biosynthesis: a millennium review Nat. Prod. Rep. 18, 380-416
59. Wakil, S. J., Stoops, J. K., and Joshi, V. C. (1983) Fatty acid synthesis and its regulation Annu. Rev. Biochem. 52, 537-579
60. Walsh, C. T., Gehring, A. M., Weinreb, P. H., Quadri, L. E., and Flugel, R. S. (1997) Post-translational modification of polyketide and nonribosomal peptide synthases Curr. Opin. Chem. Biol. 1, 309-315
61. Yin, J., Liu, F., Li, X., and Walsh, C. T. (2004) Labeling proteins with small molecules by site-specific posttranslational modification J. Am. Chem. Soc. 126, 7754-7755
62. Zhou, Z., Cironi, P., Lin, A. J., Xu, Y., Hrvatin, S., Golan, D. E., Silver, P. A., Walsh, C. T., and Yin, J. (2007) Genetically encoded short peptide tags for orthogonal protein labeling by Sfp and AcpS phosphopantetheinyl transferases ACS Chem. Biol. 2, 337-346
63. Clarke, K. M., Mercer, A. C., La Clair, J. J., and Burkart, M. D. (2005) In vivo reporter labeling of proteins via metabolic delivery of coenzyme A analogues J. Am. Chem. Soc. 127, 11234-11235
64. Worthington, A. S. and Burkart, M. D. (2006) One-pot chemo-enzymatic synthesis of reporter-modified proteins Org. Biomol. Chem. 4, 44
65. Kosa, N. M., Haushalter, R. W., Smith, A. R., and Burkart, M. D. (2012) Reversible labeling of native and fusion-protein motifs Nat. Methods 9, 981-984
66. George, N., Pick, H., Vogel, H., Johnsson, N., and Johnsson, K. (2004) Specific labeling of cell surface proteins with chemically diverse compounds J. Am. Chem. Soc. 126, 8896-8897
67. Cappellaro, C., Baldermann, C., Rachel, R., and Tanner, W. (1994) Mating type-specific cell-cell recognition of Saccharomyces cerevisiae: cell wall attachment and active sites of a- and alpha-agglutinin EMBO J. 13, 4737-4744
68. Yin, J., Straight, P. D., McLoughlin, S. M., Zhou, Z., Lin, A. J., Golan, D. E., Kelleher, N. L., Kolter, R., and Walsh, C. T. (2005) Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase Proc. Natl. Acad. Sci. U.S.A. 102, 15815-15820
69. Wong, L. S., Thirlway, J., and Micklefield, J. (2008) Direct site-selective covalent protein immobilization catalyzed by a phosphopantetheinyl transferase J. Am. Chem. Soc. 130, 12456-12464
70. Vocadlo, D. J., Hang, H. C., Kim, E., Hanover, J. A., and Bertozzi, C. R. (2003) A chemical approach for identifying O-GlcNAc-modified proteins in cells Proc. Natl. Acad. Sci. U.S.A. 100, 9116-9121
71. Saxon, E. and Bertozzi, C. R. (2000) Cell surface engineering by a modified Staudinger reaction Science 287, 2007-2010
72. Khidekel, N., Arndt, S., Lamarre-Vincent, N., Lippert, A., Poulin-Kerstien, K. G., Ramakrishnan, B., Qasba, P. K., and Hsieh-Wilson, L. C. (2003) A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications J. Am. Chem. Soc. 125, 16162-16163
73. Clark, P. M., Dweck, J. F., Mason, D. E., Hart, C. R., Buck, S. B., Peters, E. C., Agnew, B. J., and Hsieh-Wilson, L. C. (2008) Direct in-gel fluorescence detection and cellular imaging of O-GlcNAc-modified proteins J. Am. Chem. Soc. 130, 11576-11577
74. Khidekel, N., Ficarro, S. B., Peters, E. C., and Hsieh-Wilson, L. C. (2004) Exploring the O-GlcNAc proteome: Direct identification of O-GlcNAc-modified proteins from the brain Proc. Natl. Acad. Sci. U.S.A. 101, 13132-13137
75. Khidekel, N., Ficarro, S. B., Clark, P. M., Bryan, M. C., Swaney, D. L., Rexach, J. E., Sun, Y. E., Coon, J. J., Peters, E. C., and Hsieh-Wilson, L. C. (2007) Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics Nat. Chem. Biol. 3, 339-348
76. Mazmanian, S. K., Liu, G., Ton-That, H., and Schneewind, O. (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall Science 285, 760-763
77. Tsukiji, S. and Nagamune, T. (2009) Sortase-mediated ligation: a gift from gram-positive bacteria to protein engineering ChemBioChem 10, 787-798
78. Popp, M. W., Antos, J. M., Grotenbreg, G. M., Spooner, E., and Ploegh, H. L. (2007) Sortagging: a versatile method for protein labeling Nat. Chem. Biol. 3, 707-708
79. Tanaka, T., Yamamoto, T., Tsukiji, S., and Nagamune, T. (2008) Site-specific protein modification on living cells catalyzed by sortase ChemBioChem 9, 802-807
80. Strijbis, K., Spooner, E., and Ploegh, H. L. (2012) Protein ligation in living cells using sortase Traffic 13, 780-789
81. Möhlmann, S., Mahlert, C., Greven, S., Scholz, P., and Harrenga, A. (2011) In vitro sortagging of an antibody Fab fragment: overcoming unproductive reactions of sortase with water and lysine side chains ChemBioChem 12, 1774-1780
82. Popp, M. W., Dougan, S. K., Chuang, T.-Y., Spooner, E., and Ploegh, H. L. (2011) Sortase-catalyzed transformations that improve the properties of cytokines Proc. Natl. Acad. Sci. U.S.A. 108, 3169-3174
83. Antos, J. M., Miller, G. M., Grotenbreg, G. M., and Ploegh, H. L. (2008) Lipid modification of proteins through sortase-catalyzed transpeptidation J. Am. Chem. Soc. 130, 16338-16343
84. Guo, X., Wang, Q., Swarts, B. M., and Guo, Z. (2009) Sortase-catalyzed peptide-glycosylphosphatidylinositol analogue ligation J. Am. Chem. Soc. 131, 9878-9879
85. Wu, Z., Guo, X., and Guo, Z. (2011) Sortase A-catalyzed peptide cyclization for the synthesis of macrocyclic peptides and glycopeptides Chem. Commun. 47, 9218
86. Sinisi, A., Popp, M. W.-L., Antos, J. M., Pansegrau, W., Savino, S., Nissum, M., Rappuoli, R., Ploegh, H. L., and Buti, L. (2012) Development of an influenza virus protein array using sortagging technology Bioconjugate Chem. 23, 1119-1126
87. Witte, M. D., Cragnolini, J. J., Dougan, S. K., Yoder, N. C., Popp, M. W., and Ploegh, H. L. (2012) Preparation of unnatural N-to-N and C-to-C protein fusions Proc. Natl. Acad. Sci. U.S.A. 109, 11993-11998
88. Williamson, D. J., Fascione, M. A., Webb, M. E., and Turnbull, W. B. (2012) Efficient N-terminal labeling of proteins by use of sortase Angew. Chem., Int. Ed. 124, 9511-9514
89. Claessen, J. H. L., Witte, M. D., Yoder, N. C., Zhu, A. Y., Spooner, E., and Ploegh, H. L. (2013) Catch-and-release probes applied to semi-intact cells reveal ubiquitin-specific protease expression in Chlamydia trachomatis infection ChemBioChem 14, 343-352
90. Jeger, S., Zimmermann, K., Blanc, A., Grünberg, J., Honer, M., Hunziker, P., Struthers, H., and Schibli, R. (2010) Site-specific and stoichiometric modification of antibodies by bacterial transglutaminase Angew. Chem., Int. Ed. 49, 9995-9997
91. Mero, A., Spolaore, B., Veronese, F. M., and Fontana, A. (2009) Transglutaminase-mediated PEGylation of proteins: direct identification of the sites of protein modification by mass spectrometry using a novel monodisperse PEG Bioconjugate Chem. 20, 384-389
92. Abe, H., Goto, M., and Kamiya, N. (2011) Protein lipidation catalyzed by microbial transglutaminase Chem.-Eur. J. 17, 14004-14008
93. Tanaka, T., Kamiya, N., and Nagamune, T. (2005) N-terminal glycine-specific protein conjugation catalyzed by microbial transglutaminase FEBS Lett. 579, 2092-2096
94. Tominaga, J., Kamiya, N., Doi, S., Ichinose, H., Maruyama, T., and Goto, M. (2005) Design of a specific peptide tag that affords covalent and site-specific enzyme immobilization catalyzed by microbial transglutaminase Biomacromolecules 6, 2299-2304
95. Lin, C.-W. and Ting, A. Y. (2006) Transglutaminase-catalyzed site-specific conjugation of small-molecule probes to proteins in vitro and on the surface of living cells J. Am. Chem. Soc. 128, 4542-4543
96. Duckworth, B. P., Xu, J., Taton, T. A., Guo, A., and Distefano, M. D. (2006) Site-specific, covalent attachment of proteins to a solid surface Bioconjugate Chem. 17, 967-974
97. Kho, Y. (2004) A tagging-via-substrate technology for detection and proteomics of farnesylated proteins Proc. Natl. Acad. Sci. U.S.A. 101, 12479-12484
98. Duckworth, B. P., Zhang, Z., Hosokawa, A., and Distefano, M. D. (2007) Selective labeling of proteins by using protein farnesyltransferase ChemBioChem 8, 98-105
99. Rashidian, M., Dozier, J. K., Lenevich, S., and Distefano, M. D. (2010) Selective labeling of polypeptides using protein farnesyltransferase via rapid oxime ligation Chem. Commun. 46, 8998-9000
100. Nguyen, U. T. T., Guo, Z., Delon, C., Wu, Y., Deraeve, C., Fränzel, B., Bon, R. S., Blankenfeldt, W., Goody, R. S., Waldmann, H., Wolters, D., and Alexandrov, K. (2009) Analysis of the eukaryotic prenylome by isoprenoid affinity tagging Nat. Chem. Biol. 5, 227-235
101. Subramanian, T., Pais, J. E., Liu, S., Troutman, J. M., Suzuki, Y., Leela Subramanian, K., Fierke, C. A., Andres, D. A., and Spielmann, H. P. (2012) Farnesyl diphosphate analogues with aryl moieties are efficient alternate substrates for protein farnesyltransferase Biochemistry 51, 8307-8319
102. Labadie, G. R., Viswanathan, R., and Poulter, C. D. (2007) Farnesyl diphosphate analogues with ω-bioorthogonal azide and alkyne functional groups for protein farnesyl transferase-catalyzed ligation reactions J. Org. Chem. 72, 9291-9297
103. Weinrich, D., Lin, P.-C., Jonkheijm, P., Nguyen, U. T. T., Schröder, H., Niemeyer, C. M., Alexandrov, K., Goody, R., and Waldmann, H. (2010) Oriented immobilization of farnesylated proteins by the thiol-ene reaction Angew. Chem., Int. Ed. 49, 1252-1257
104. Nguyen, U. T. T., Cramer, J., Gomis, J., Reents, R., Gutierrez-Rodriguez, M., Goody, R. S., Alexandrov, K., and Waldmann, H. (2007) Exploiting the substrate tolerance of farnesyltransferase for site-selective protein derivatization ChemBioChem 8, 408-423
105. Rose, M. W., Xu, J., Kale, T. A., O'Doherty, G., Barany, G., and Distefano, M. D. (2005) Enzymatic incorporation of orthogonally reactive prenylazide groups into peptides using geranylazide diphosphate via protein farnesyltransferase: implications for selective protein labeling Biopolymers 80, 164-171
106. Rose, M. W., Rose, N. D., Boggs, J., Lenevich, S., Xu, J., Barany, G., and Distefano, M. D. (2005) Evaluation of geranylazide and farnesylazide diphosphate for incorporation of prenylazides into a CAAX box-containing peptide using protein farnesyltransferase J. Pept. Res. 65, 529-537
107. Xu, J., DeGraw, A. J., Duckworth, B. P., Lenevich, S., Tann, C.-M., Jenson, E. C., Gruber, S. J., Barany, G., and Distefano, M. D. (2006) Synthesis and reactivity of 6,7-dihydrogeranylazides: reagents for primary azide incorporation into peptides and subsequent Staudinger ligation Chem. Biol. Drug. Des. 68, 85-96
108. Duckworth, B. P., Chen, Y., Wollack, J. W., Sham, Y., Mueller, J. D., Taton, T. A., and Distefano, M. D. (2007) A universal method for the preparation of covalent protein-DNA conjugates for use in creating protein nanostructures Angew. Chem. 119, 8975-8978
109. Khatwani, S. L., Kang, J. S., Mullen, D. G., Hast, M. A., Beese, L. S., Distefano, M. D., and Taton, T. A. (2012) Covalent protein-oligonucleotide conjugates by copper-free click reaction Bioorg. Med. Chem. 20, 4532-4539
110. Speers, A. E. and Cravatt, B. F. (2004) Profiling enzyme activities in vivo using click chemistry methods Chem. Biol. 11, 535-546
111. Hosokawa, A., Wollack, J. W., Zhang, Z., Chen, L., Barany, G., and Distefano, M. D. (2007) Evaluation of an alkyne-containing analogue of farnesyl diphosphate as a dual substrate for protein-prenyltransferases Int. J. Pept. Res. Ther. 13, 345-354
112. Wollack, J. W., Silverman, J. M., Petzold, C. J., Mougous, J. D., and Distefano, M. D. (2009) A minimalist substrate for enzymatic peptide and protein conjugation ChemBioChem 10, 2934-2943
113. Mahmoodi, M. M., Rashidian, M., Dozier, J. K., and Distefano, M. D. (2013) Chemoenzymatic reversible immobilization and labeling of proteins from crude cellular extract Curr. Protoc. Chem. Biol. 89-109
114. Dirksen, A., Hackeng, T. M., and Dawson, P. E. (2006) Nucleophilic catalysis of oxime ligation Angew. Chem., Int. Ed. 45, 7581-7584
115. Rashidian, M., Mahmoodi, M. M., Shah, R., Dozier, J. K., Wagner, C. R., and Distefano, M. D. (2013) A highly efficient catalyst for oxime ligation and hydrazone-oxime exchange suitable for bioconjugation Bioconjugate Chem. 24, 333-342
116. Crisalli, P. and Kool, E. T. (2013) Water-soluble organocatalysts for hydrazone and oxime formation J. Org. Chem. 78, 1184-1189
117. Algar, W. R., Prasuhn, D. E., Stewart, M. H., Jennings, T. L., Blanco-Canosa, J. B., Dawson, P. E., and Medintz, I. L. (2011) The controlled display of biomolecules on nanoparticles: a challenge suited to bioorthogonal chemistry Bioconjugate Chem. 22, 825-858
118. Howarth, M., Takao, K., hayashi, Y., and Ting, A. Y. (2005) Targeting quantum dots to surface proteins in living cells with biotin ligase Proc. Natl. Acad. Sci. U.S.A. 102, 7583-7588
119. Howarth, M., Liu, W., Puthenveetil, S., Zheng, Y., Marshall, L. F., Schmidt, M. M., Wittrup, K. D., Bawendi, M. G., and Ting, A. Y. (2008) Monovalent, reduced-size quantum dots for imaging receptors on living cells Nat. Meth. 5, 397-399
120. Slavoff, S. A., Chen, I., Choi, Y.-A., and Ting, A. Y. (2008) Expanding the substrate tolerance of biotin ligase through exploration of enzymes from diverse species J. Am. Chem. Soc. 130, 1160-1162
121. Fernández-Suárez, M., Chen, T. S., and Ting, A. Y. (2008) Protein-protein interaction detection in vitro and in cells by proximity biotinylation J. Am. Chem. Soc. 130, 9251-9253
122. Sueda, S., Yoneda, S., and Hayashi, H. (2011) Site-specific labeling of proteins by using biotin protein ligase conjugated with fluorophores ChemBioChem 12, 1367-1375
123. Roux, K. J., Kim, D. I., Raida, M., and Burke, B. (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells J. Cell Biol. 196, 801-810
124. Fernández-Suárez, M., Baruah, H., Martínez- Hernández, L., Xie, K. T., Baskin, J. M., Bertozzi, C. R., and Ting, A. Y. (2007) Redirecting lipoic acid ligase for cell surface protein labeling with small-molecule probes Nat. Biotechnol. 25, 1483-1487
125. Cohen, J. D., Thompson, S., and Ting, A. Y. (2011) Structure-guided engineering of a pacific blue fluorophore ligase for specific protein imaging in living cells Biochemistry 50, 8221-8225
126. Uttamapinant, C., White, K. A., Baruah, H., Thompson, S., Fernandez-Suarez, M., Puthenveetil, S., and Ting, A. Y. (2010) From the cover: a fluorophore ligase for site-specific protein labeling inside living cells Proc. Natl. Acad. Sci. U.S.A. 107, 10914-10919
127. Slavoff, S. A., Liu, D. S., Cohen, J. D., and Ting, A. Y. (2011) Imaging protein-protein interactions inside living cells via interaction-dependent fluorophore ligation J. Am. Chem. Soc. 133, 19769-19776
128. Cohen, J. D., Zou, P., and Ting, A. Y. (2012) Site-specific protein modification using lipoic acid ligase and bis-aryl hydrazone formation ChemBioChem 13, 888-894
129. Uttamapinant, C., Tangpeerachaikul, A., Grecian, S., Clarke, S., Singh, U., Slade, P., Gee, K. R., and Ting, A. Y. (2012) Fast, cell-compatible click chemistry with copper-chelating azides for biomolecular labeling Angew. Chem., Int. Ed. 51, 5852-5856
130. Yao, J. Z., Uttamapinant, C., Poloukhtine, A., Baskin, J. M., Codelli, J. A., Sletten, E. M., Bertozzi, C. R., Popik, V. V., and Ting, A. Y. (2012) Fluorophore targeting to cellular proteins via enzyme-mediated azide ligation and strain-promoted cycloaddition J. Am. Chem. Soc. 134, 3720-3728
131. Farazi, T. A., Waksman, G., and Gordon, J. I. (2001) The biology and enzymology of protein N-myristoylation J. Biol. Chem. 276, 39501-39504
132. Towler, D. A., Gordon, J. I., Adams, S. P., and Glaser, L. (1988) The biology and enzymology of eukaryotic protein acylation Annu. Rev. Biochem. 57, 69-99
133. Price, H. P., Menon, M. R., Panethymitaki, C., Goulding, D., McKean, P. G., and Smith, D. F. (2003) Myristoyl-CoA:protein N-myristoyltransferase, an essential enzyme and potential drug target in kinetoplastid parasites J. Biol. Chem. 278, 7206-7214
134. Martinez, A., Traverso, J. A., Valot, B., Ferro, M., Espagne, C., Ephritikhine, G., Zivy, M., Giglione, C., and Meinnel, T. (2008) Extent of N-terminal modifications in cytosolic proteins from eukaryotes Proteomics 8, 2809-2831
135. Wright, M. H., Heal, W. P., Mann, D. J., and Tate, E. W. (2010) Protein myristoylation in health and disease J. Chem. Biol. 3, 19-35
136. Heal, W. P., Wickramasinghe, S. R., Bowyer, P. W., Holder, A. A., Smith, D. F., Leatherbarrow, R. J., and Tate, E. W. (2008) Site-specific N-terminal labelling of proteins in vitro and in vivo using N-myristoyl transferase and bioorthogonal ligation chemistry Chem. Commun. 480
137. Heal, W. P., Wickramasinghe, S. R., Leatherbarrow, R. J., and Tate, E. W. (2008) N-Myristoyl transferase-mediated protein labelling in vivo Org. Biomol. Chem. 6, 2308
138. Heal, W. P., Wright, M. H., Thinon, E., and Tate, E. W. (2012) Multifunctional protein labeling via enzymatic N-terminal tagging and elaboration by click chemistry Nat. Protoc. 7, 105-117