Directed evolution of a probe ligase with activity in the secretory pathway and application to imaging intercellular protein-protein interactions

Biochemistry

Volumn 52, Issue 21, 2013, Pages 3728-3739

  White, Katharine A ^a,b   Zegelbone, Phillip M ^a,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIRECTED EVOLUTION; ENDOPLASMIC RETICULUM; INTRACELLULAR PROTEINS; LABELED PROTEINS; MAMMALIAN CELLS; PEPTIDE RECOGNITION; PROTEIN-PROTEIN INTERACTIONS; SECRETORY PATHWAYS; INTERCELLULAR PROTEINS;

AMINO ACIDS; CELL MEMBRANES; ENZYMES; ESCHERICHIA COLI; IMAGING TECHNIQUES; OPTIMIZATION; PROBES; CELLS; CYTOLOGY; MAMMALS;

PROTEINS;

GREEN FLUORESCENT PROTEIN; LIGASE; LIPOIC ACID LIGASE; NEUREXIN; NEUROLIGIN; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTICLE; CATALYSIS; CELL SURFACE; CHEMICAL LABELING; CONTROLLED STUDY; COVALENT BOND; DIRECTED MOLECULAR EVOLUTION; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERMETHOD COMPARISON; LIPOYLATION; MAMMAL CELL; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SECRETORY PATHWAY; SEQUENCE ANALYSIS; SYNAPSE; YEAST CELL; CELL SELECTION; CLICK CHEMISTRY; MASS SPECTROMETRY; MUTATION RATE;

DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; LIPASE; MOLECULAR PROBES; PROTEIN BINDING; PROTEINS;

ESCHERICHIA COLI; MAMMALIA;

EID: 84878319440     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400268m     Document Type: Article

References (36)

1. Uttamapinant, C., White, K. A., Baruah, H., Thompson, S., Fernandez-Suarez, M., Puthenveetil, S., and Ting, A. Y. (2010) A fluorophore ligase for site-specific protein labeling inside living cells Proc. Natl. Acad. Sci. U.S.A. 107, 10914-10919
2. 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
3. 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
4. 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
5. 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
6. 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
7. Green, D. E., Morris, T. W., Green, J., Cronan, J. E., Jr., and Guest, J. R. (1995) Purification and properties of the lipoate protein ligase of Escherichia coli Biochem. J. 309 (Part 3) 853-862
8. Turner, N. J. (2009) Directed evolution drives the next generation of biocatalysts Nat. Chem. Biol. 5, 567-573
9. Goldsmith, M. and Tawfik, D. S. (2012) Directed enzyme evolution: Beyond the low-hanging fruit Curr. Opin. Struct. Biol. 4, 406-412
10. Turner, N. J. (2003) Directed evolution of enzymes for applied biocatalysis Trends Biotechnol. 21, 474-478
11. Zhang, K., Li, H., Cho, K. M., and Liao, J. C. (2010) Expanding metabolism for total biosynthesis of the nonnatural amino acid l -homoalanine Proc. Natl. Acad. Sci. U.S.A. 107, 6234-6239
12. Atsumi, S. and Liao, J. C. (2008) Directed evolution of Methanococcus jannaschii citramalate synthase for biosynthesis of 1-propanol and 1-butanol by Escherichia coli Appl. Environ. Microbiol. 74, 7802-7808
13. Blagodatski, A. and Katanaev, V. L. (2010) Technologies of directed protein evolution in vivo Cell. Mol. Life Sci. 68, 1207-1214
14. Janda, K. D., Lo, L. C., Lo, C. H., Sim, M. M., Wang, R., Wong, C. H., and Lerner, R. A. (1997) Chemical selection for catalysis in combinatorial antibody libraries Science 275, 945-948
15. Seelig, B. and Szostak, J. W. (2007) Selection and evolution of enzymes from a partially randomized non-catalytic scaffold Nature 448, 828-831
16. Doi, N., Kumadaki, S., Oishi, Y., Matsumura, N., and Yanagawa, H. (2004) In vitro selection of restriction endonucleases by in vitro compartmentalization Nucleic Acids Res. 32, e95
17. Cohen, H. M., Tawfik, D. S., and Griffiths, A. D. (2004) Altering the sequence specificity of HaeIII methyltransferase by directed evolution using in vitro compartmentalization Protein Eng., Des. Sel. 17, 3-11
18. Fernandez-Gacio, A., Uguen, M., and Fastrez, J. (2003) Phage display as a tool for the directed evolution of enzymes Trends Biotechnol. 21, 408-414
19. Leemhuis, H., Stein, V., Griffiths, A. D., and Hollfelder, F. (2005) New genotype-phenotype linkages for directed evolution of functional proteins Curr. Opin. Struct. Biol. 15, 472-478
20. Chen, I., Dorr, B. M., and Liu, D. R. (2011) A general strategy for the evolution of bond-forming enzymes using yeast display Proc. Natl. Acad. Sci. U.S.A. 108, 11399-11404
21. Agresti, J. J., Antipov, E., Abate, A. R., Ahn, K., Rowat, A. C., Baret, J. C., Marquez, M., Klibanov, A. M., Griffiths, A. D., and Weitz, D. A. (2010) Ultrahigh-throughput screening in drop-based microfluidics for directed evolution Proc. Natl. Acad. Sci. U.S.A. 107, 4004-4009
22. Varadarajan, N., Rodriguez, S., Hwang, B. Y., Georgiou, G., and Iverson, B. L. (2008) Highly active and selective endopeptidases with programmed substrate specificities Nat. Chem. Biol. 4, 290-294
23. Colby, D. W., Kellogg, B. A., Graff, C. P., Yeung, Y. A., Swers, J. S., and Wittrup, K. D. (2004) Engineering antibody affinity by yeast surface display Methods Enzymol. 388, 348-358
24. Jones, R. P. and Greenfield, P. F. (1987) Ethanol and the fluidity of the yeast plasma membrane Yeast 3, 223-232
25. Fujiwara, K., Maita, N., Hosaka, H., Okamura-Ikeda, K., Nakagawa, A., and Taniguchi, H. (2010) Global conformational change associated with the two-step reaction catalyzed by Escherichia coli lipoate-protein ligase A J. Biol. Chem. 285, 9971-9980
26. Fujiwara, K., Toma, S., Okamura-Ikeda, K., Motokawa, Y., Nakagawa, A., and Taniguchi, H. (2005) Crystal structure of lipoate-protein ligase A from Escherichia coli. Determination of the lipoic acid-binding site J. Biol. Chem. 280, 33645-33651
27. Scheiffele, P., Fan, J., Choih, J., Fetter, R., and Serafini, T. (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons Cell 101, 657-669
28. Graff, J. M., Stumpo, D. J., and Blackshear, P. J. (1989) Molecular cloning, sequence, and expression of a cDNA encoding the chicken myristoylated alanine-rich C kinase substrate (MARCKS) Mol. Endocrinol. 3, 1903-1906
29. Craig, A. M. and Kang, Y. (2007) Neurexin-neuroligin signaling in synapse development Curr. Opin. Neurobiol. 17, 43-52
30. Chen, S. X., Tari, P. K., She, K., and Haas, K. (2010) Neurexin-neuroligin cell adhesion complexes contribute to synaptotropic dendritogenesis via growth stabilization mechanisms in vivo Neuron 67, 967-983
31. Liu, D. S., Loh, K. H., Lam, S. S., White, K. A., and Ting, A. Y. (2013) Imaging Trans-Cellular Neurexin-Neuroligin Interactions by Enzymatic Probe Ligation PLoS One 8, e52823
32. Yamagata, M. and Sanes, J. R. (2012) Transgenic strategy for identifying synaptic connections in mice by fluorescence complementation (GRASP) Front. Mol. Neurosci. 5, 18
33. Kim, J., Zhao, T., Petralia, R. S., Yu, Y., Peng, H., Myers, E., and Magee, J. C. (2012) mGRASP enables mapping mammalian synaptic connectivity with light microscopy Nat. Methods 9, 96-102
34. Lin, Y., Tsumuraya, T., Wakabayashi, T., Shiraga, S., Fujii, I., Kondo, A., and Ueda, M. (2003) Display of a functional hetero-oligomeric catalytic antibody on the yeast cell surface Appl. Microbiol. Biotechnol. 62, 226-232
35. Gautier, A., Juillerat, A., Heinis, C., Correa, I. R., Jr., Kindermann, M., Beaufils, F., and Johnsson, K. (2008) An engineered protein tag for multiprotein labeling in living cells Chem. Biol. 15, 128-136
36. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: A novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382