Evaluation of genetically encoded chemical tags as orthogonal fluorophore labeling tools for single-molecule fret applications

Journal of Physical Chemistry B

Volumn 119, Issue 22, 2015, Pages 6611-6619

  Ishitsuka, Yuji ^a   Azadfar, Naghmeh ^a   Kobitski, Andrei Yu ^a   Nienhaus, Karin ^a   Johnsson, Nils ^b   Nienhaus, G Ulrich ^a,c,d,e  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF ULM   (Germany)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^d University of Illinois at Urbana Champaign   (United States)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; ENERGY TRANSFER; FLUORESCENCE; FLUOROPHORES; MOLECULES; PEPTIDES; PROTEINS;

CONFORMATIONAL CHANGE; CONFORMATIONAL DYNAMICS; DONOR AND ACCEPTOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROTEIN MOLECULES; SINGLE MOLECULE LEVEL; SINGLE-MOLECULE FRETS; SPECIFIC LOCATION;

CONFORMATIONS;

CALMODULIN; FLUORESCENT DYE; PEPTIDE; POLYPROLINE;

CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROCEDURES; PROTEIN CONFORMATION;

CALMODULIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; PEPTIDES; PROTEIN CONFORMATION;

EID: 84930685249     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b03584     Document Type: Article

References (62)

1. Förster, T. Energiewanderung und Fluoreszenz Naturwissenschaften 1946, 33, 166-175
2. Förster, T. Zwischenmolekulare Energiewanderung und Fluoreszenz Ann. Phys. 1948, 2, 55-75
3. Stryer, L.; Haugland, R. P. Energy Transfer: A Spectroscopic Ruler Proc. Natl. Acad. Sci. U.S.A. 1967, 58, 719-726
4. Ha, T.; Tinnefeld, P. Photophysics of Fluorescent Probes for Single-Molecule Biophysics and Super-Resolution Imaging Annu. Rev. Phys. Chem. 2012, 63, 595-617
5. Joo, C.; Balci, H.; Ishitsuka, Y.; Buranachai, C.; Ha, T. Advances in Single-Molecule Fluorescence Methods for Molecular Biology Annu. Rev. Biochem. 2008, 77, 51-76
6. Li, G. W.; Xie, X. S. Central Dogma at the Single-Molecule Level in Living Cells Nature 2011, 475, 308-315
7. Kuzmenkina, E. V.; Heyes, C. D.; Nienhaus, G. U. Single-Molecule FRET Study of Denaturant Induced Unfolding of RNase H J. Mol. Biol. 2006, 357, 313-324
8. Puljung, M. C.; Zagotta, W. N. Labeling of Specific Cysteines in Proteins Using Reversible Metal Protection Biophys. J. 2011, 100, 2513-2521
9. Kim, J.; Seo, M. H.; Lee, S.; Cho, K.; Yang, A.; Woo, K.; Kim, H. S.; Park, H. S. Simple and Efficient Strategy for Site-Specific Dual Labeling of Proteins for Single-Molecule Fluorescence Resonance Energy Transfer Analysis Anal. Chem. 2013, 85, 1468-1474
10. Liu, C. C.; Schultz, P. G. Adding New Chemistries to the Genetic Code Annu. Rev. Biochem. 2010, 79, 413-444
11. Seo, M. H.; Lee, T. S.; Kim, E.; Cho, Y. L.; Park, H. S.; Yoon, T. Y.; Kim, H. S. Efficient Single-Molecule Fluorescence Resonance Energy Transfer Analysis by Site-Specific Dual-Labeling of Protein Using an Unnatural Amino Acid Anal. Chem. 2011, 83, 8849-8854
12. Wang, L.; Brock, A.; Herberich, B.; Schultz, P. G. Expanding the Genetic Code of Escherichia coli Science 2001, 292, 498-500
13. Uchinomiya, S. H.; Nonaka, H.; Fujishima, S. H.; Tsukiji, S.; Ojida, A.; Hamachi, I. Site-Specific Covalent Labeling of His-Tag Fused Proteins with a Reactive Ni(II)-NTA Probe Chem. Commun. (Cambridge, U.K.) 2009, 5880-5882
14. Carrico, I. S.; Carlson, B. L.; Bertozzi, C. R. Introducing Genetically Encoded Aldehydes into Proteins Nat. Chem. Biol. 2007, 3, 321-322
15. Shi, X.; Jung, Y.; Lin, L. J.; Liu, C.; Wu, C.; Cann, I. K.; Ha, T. Quantitative Fluorescence Labeling of Aldehyde-Tagged Proteins for Single-Molecule Imaging Nat. Methods 2012, 9, 499-503
16. Griffin, B. A.; Adams, S. R.; Tsien, R. Y. Specific Covalent Labeling of Recombinant Protein Molecules inside Live Cells Science 1998, 281, 269-272
17. Jager, M.; Nir, E.; Weiss, S. Site-Specific Labeling of Proteins for Single-Molecule FRET by Combining Chemical and Enzymatic Modification Protein Sci. 2006, 15, 640-646
18. Yano, Y.; Yano, A.; Oishi, S.; Sugimoto, Y.; Tsujimoto, G.; Fujii, N.; Matsuzaki, K. Coiled-Coil Tag-Probe System for Quick Labeling of Membrane Receptors in Living Cell ACS Chem. Biol. 2008, 3, 341-345
19. Muralidharan, V.; Muir, T. W. Protein Ligation: An Enabling Technology for the Biophysical Analysis of Proteins Nat. Methods 2006, 3, 429-438
20. Vila-Perello, M.; Liu, Z.; Shah, N. H.; Willis, J. A.; Idoyaga, J.; Muir, T. W. Streamlined Expressed Protein Ligation Using Split Inteins J. Am. Chem. Soc. 2013, 135, 286-292
21. Parthasarathy, R.; Subramanian, S.; Boder, E. T. Sortase a as a Novel Molecular "Stapler" for Sequence-Specific Protein Conjugation Bioconjugate Chem. 2007, 18, 469-476
22. Popp, M. W.; Antos, J. M.; Grotenbreg, G. M.; Spooner, E.; Ploegh, H. L. Sortagging: A Versatile Method for Protein Labeling Nat. Chem. Biol. 2007, 3, 707-708
23. So, M. K.; Yao, H.; Rao, J. HaloTag Protein-Mediated Specific Labeling of Living Cells with Quantum Dots Biochem. Biophys. Res. Commun. 2008, 374, 419-423
24. Calloway, N. T.; Choob, M.; Sanz, A.; Sheetz, M. P.; Miller, L. W.; Cornish, V. W. Optimized Fluorescent Trimethoprim Derivatives for in Vivo Protein Labeling ChemBioChem 2007, 8, 767-774
25. Miller, L. W.; Cai, Y.; Sheetz, M. P.; Cornish, V. W. In Vivo Protein Labeling with Trimethoprim Conjugates: A Flexible Chemical Tag Nat. Methods 2005, 2, 255-257
26. Gautier, A.; Juillerat, A.; Heinis, C.; Correa, I. R.; Kindermann, M.; Beaufils, F.; Johnsson, K. An Engineered Protein Tag for Multiprotein Labeling in Living Cells Chem. Biol. 2008, 15, 128-136
27. Keppler, A.; Gendreizig, S.; Gronemeyer, T.; Pick, H.; Vogel, H.; Johnsson, K. A General Method for the Covalent Labeling of Fusion Proteins with Small Molecules in Vivo Nat. Biotechnol. 2003, 21, 86-89
28. Klein, T.; Loschberger, A.; Proppert, S.; Wolter, S.; van de Linde, S.; Sauer, M. Live-Cell dStorm with Snap-Tag Fusion Proteins Nat. Methods 2011, 8, 7-9
29. Albizu, L.; Cottet, M.; Kralikova, M.; Stoev, S.; Seyer, R.; Brabet, I.; Roux, T.; Bazin, H.; Bourrier, E.; Lamarque, L. Time-Resolved FRET between GPCR Ligands Reveals Oligomers in Native Tissues Nat. Chem. Biol. 2010, 6, 587-594
30. Bosch, P. J.; Correa, I. R., Jr.; Sonntag, M. H.; Ibach, J.; Brunsveld, L.; Kanger, J. S.; Subramaniam, V. Evaluation of Fluorophores to Label Snap-Tag Fused Proteins for Multicolor Single-Molecule Tracking Microscopy in Live Cells Biophys. J. 2014, 107, 803-814
31. Grimm, J. B.; English, B. P.; Chen, J.; Slaughter, J. P.; Zhang, Z.; Revyakin, A.; Patel, R.; Macklin, J. J.; Normanno, D.; Singer, R. H. A General Method to Improve Fluorophores for Live-Cell and Single-Molecule Microscopy Nat. Methods 2015, 12, 244-250
32. Jones, S. A.; Shim, S. H.; He, J.; Zhuang, X. Fast, Three-Dimensional Super-Resolution Imaging of Live Cells Nat. Methods 2011, 8, 499-508
33. Brun, M. A.; Tan, K.-T.; Nakata, E.; Hinner, M. J.; Johnsson, K. Semisynthetic Fluorescent Sensor Proteins Based on Self-Labeling Protein Tags J. Am. Chem. Soc. 2009, 131, 5873-5884
34. Tyagi, S.; VanDelinder, V.; Banterle, N.; Fuertes, G.; Milles, S.; Agez, M.; Lemke, E. A. Continuous Throughput and Long-Term Observation of Single-Molecule FRET without Immobilization Nat. Methods 2014, 11, 297-350
35. Kampmeier, F.; Ribbert, M.; Nachreiner, T.; Dembski, S.; Beaufils, F.; Brecht, A.; Barth, S. Site-Specific, Covalent Labeling of Recombinant Antibody Fragments Via Fusion to an Engineered Version of 6-O-Alkylguanine DNA Alkyltransferase Bioconjugate Chem. 2009, 20, 1010-1015
36. Gautier, A.; Nakata, E.; Lukinavicius, G.; Tan, K. T.; Johnsson, K. Selective Cross-Linking of Interacting Proteins Using Self-Labeling Tags J. Am. Chem. Soc. 2009, 131, 17954-17962
37. Engin, S.; Fichtner, D.; Wedlich, D.; Fruk, L. Snap-Tag as a Tool for Surface Immobilization Curr. Pharm. Des. 2013, 19, 5443-5448
38. Tyagi, S.; VanDelinder, V.; Banterle, N.; Fuertes, G.; Milles, S.; Agez, M.; Lemke, E. A. Continuous Throughput and Long-Term Observation of Single-Molecule FRET without Immobilization Nat. Methods 2014, 11, 297-300
39. Minderer, M.; Liu, W.; Sumanovski, L. T.; Kugler, S.; Helmchen, F.; Margolis, D. J. Chronic Imaging of Cortical Sensory Map Dynamics Using a Genetically Encoded Calcium Indicator J. Physiol. 2012, 590, 99-107
40. Heyes, C. D.; Kobitski, A. Y.; Amirgoulova, E. V.; Nienhaus, G. U. Biocompatible Surfaces for Specific Tethering of Individual Protein Molecules J. Phys. Chem. B 2004, 108, 13387-13394
41. Kapanidis, A. N.; Lee, N. K.; Laurence, T. A.; Doose, S.; Margeat, E.; Weiss, S. Fluorescence-Aided Molecule Sorting: Analysis of Structure and Interactions by Alternating-Laser Excitation of Single Molecules Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 8936-8941
42. Rasnik, I.; McKinney, S. A.; Ha, T. Nonblinking and Long-Lasting Single-Molecule Fluorescence Imaging Nat. Methods 2006, 3, 891-893
43. Myong, S.; Cui, S.; Cornish, P. V.; Kirchhofer, A.; Gack, M. U.; Jung, J. U.; Hopfner, K. P.; Ha, T. Cytosolic Viral Sensor RIG-I Is a 5′-Triphosphate-Dependent Translocase on Double-Stranded RNA Science 2009, 323, 1070-1074
44. Shi, X.; Lim, J.; Ha, T. Acidification of the Oxygen Scavenging System in Single-Molecule Fluorescence Studies: In Situ Sensing with a Ratiometric Dual-Emission Probe Anal. Chem. 2010, 82, 6132-6138
45. Diao, J.; Ishitsuka, Y.; Lee, H.; Joo, C.; Su, Z.; Syed, S.; Shin, Y. K.; Yoon, T. Y.; Ha, T. A Single Vesicle-Vesicle Fusion Assay for in Vitro Studies of Snares and Accessory Proteins Nat. Protoc. 2012, 7, 921-934
46. Zhou, H. X. A Gaussian-Chain Model for Treating Residual Charge-Charge Interactions in the Unfolded State of Proteins Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 3569-3574
47. Schuler, B.; Lipman, E. A.; Steinbach, P. J.; Kumke, M.; Eaton, W. A. Polyproline and the "Spectroscopic Ruler" Revisited with Single-Molecule Fluorescence Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 2754-2759
48. Schimmel, P. R.; Flory, P. J. Conformational Energy and Configurational Statistics of Poly- l -Proline Proc. Natl. Acad. Sci. U.S.A. 1967, 58, 52-59
49. Best, R. B.; Merchant, K. A.; Gopich, I. V.; Schuler, B.; Bax, A.; Eaton, W. A. Effect of Flexibility and Cis Residues in Single-Molecule FRET Studies of Polyproline Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 18964-18969
50. Watkins, L. P.; Chang, H.; Yang, H. Quantitative Single-Molecule Conformational Distributions: A Case Study with Poly-(l -Proline) J. Phys. Chem. A 2006, 110, 5191-5203
51. Doose, S.; Neuweiler, H.; Barsch, H.; Sauer, M. Probing Polyproline Structure and Dynamics by Photoinduced Electron Transfer Provides Evidence for Deviations from a Regular Polyproline Type II Helix Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 17400-17405
52. Hoefling, M.; Lima, N.; Haenni, D.; Seidel, C. A.; Schuler, B.; Grubmüller, H. Structural Heterogeneity and Quantitative FRET Efficiency Distributions of Polyprolines through a Hybrid Atomistic Simulation and Monte Carlo Approach PLoS One 2011, 6, e19791
53. Schuler, B.; Lipman, E. A.; Eaton, W. A. Probing the Free-Energy Surface for Protein Folding with Single-Molecule Fluorescence Spectroscopy Nature 2002, 419, 743-747
54. Stigler, J.; Ziegler, F.; Gieseke, A.; Gebhardt, J. C.; Rief, M. The Complex Folding Network of Single Calmodulin Molecules Science 2011, 334, 512-516
55. Gao, Y.; Ye, L. H.; Kishi, H.; Okagaki, T.; Samizo, K.; Nakamura, A.; Kohama, K. Myosin Light Chain Kinase as a Multifunctional Regulatory Protein of Smooth Muscle Contraction IUBMB Life 2001, 51, 337-344
56. Blumenthal, D. K.; Takio, K.; Edelman, A. M.; Charbonneau, H.; Titani, K.; Walsh, K. A.; Krebs, E. G. Identification of the Calmodulin-Binding Domain of Skeletal Muscle Myosin Light Chain Kinase Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 3187-3191
57. Junker, J. P.; Ziegler, F.; Rief, M. Ligand-Dependent Equilibrium Fluctuations of Single Calmodulin Molecules Science 2009, 323, 633-637
58. Lakowski, T. M.; Lee, G. M.; Okon, M.; Reid, R. E.; McIntosh, L. P. Calcium-Induced Folding of a Fragment of Calmodulin Composed of EF-Hands 2 and 3 Protein Sci. 2007, 16, 1119-1132
59. Ye, Y.; Lee, H. W.; Yang, W.; Shealy, S.; Yang, J. J. Probing Site-Specific Calmodulin Calcium and Lanthanide Affinity by Grafting J. Am. Chem. Soc. 2005, 127, 3743-3750
60. Hoskins, A. A.; Friedman, L. J.; Gallagher, S. S.; Crawford, D. J.; Anderson, E. G.; Wombacher, R.; Ramirez, N.; Cornish, V. W.; Gelles, J.; Moore, M. J. Ordered and Dynamic Assembly of Single Spliceosomes Science 2011, 331, 1289-1295
61. Jain, A.; Liu, R.; Ramani, B.; Arauz, E.; Ishitsuka, Y.; Ragunathan, K.; Park, J.; Chen, J.; Xiang, Y. K.; Ha, T. Probing Cellular Protein Complexes Using Single-Molecule Pull-Down Nature 2011, 473, 484-488
62. Joo, C.; Fareh, M.; Kim, V. N. Bringing Single-Molecule Spectroscopy to Macromolecular Protein Complexes Trends Biochem. Sci. 2013, 38, 30-37