An experimental study of GFP-based FRET, with application to intrinsically unstructured proteins

Protein Science

Volumn 16, Issue 7, 2007, Pages 1429-1438

  Ohashi, Tomoo ^a   Galiacy, Stephane D ^a   Briscoe, Gina ^a   Erickson, Harold P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

CyPet; FRET; GFP; Persistence length; Unstructured proteins; Worm like chain; YPet

Indexed keywords

ALPHA ADDUCIN; FIBRONECTIN; FIBRONECTIN TYPE 3; FTSZ PROTEIN; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DIMERIZATION; ELECTRON MICROSCOPY; FIELD EMISSION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE; SEDIMENTATION; SIGNAL DETECTION;

ALGORITHMS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 34250885891     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.072845607     Document Type: Article

References (53)

1. Ai, H.W., Henderson, J.N., Remington, S.J., and Campbell, R.E. 2006. Directed evolution of a monomeric, bright, and photostable version of Clavularia cyan fluorescent protein: Structural characterization and applications in fluorescence imaging. Biochem. J. 400: 531-540.
2. Chebotareva, N.A., Kurganov, B.I., and Livanova, N.B. 2004. Biochemical effects of molecular crowding. Biochemistry (Mosc.) 69: 1239-1251.
3. Cota, E., Hamill, S.J., Fowler, S.B., and Clarke, J. 2000. Two proteins with the same structure respond very differently to mutation: The role of plasticity in protein stability. J. Mol. Biol. 302: 713-725.
4. Dedmon, M.M., Patel, C.N., Young, G.B., and Pielak, G.J. 2002. FlgM gains structure in living cells. Proc. Natl. Acad. Sci. 99: 12681-12684.
5. Despa, F., Orgill, D.P., and Lee, R.C. 2005. Molecular crowding effects on protein stability. Ann. N. Y. Acad. Sci. 1066: 54-66.
6. Dietz, H. and Rief, M. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. 101: 16192-16197.
7. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M., and Obradovic, Z. 2002. Intrinsic disorder and protein function. Biochemistry 41: 6573-6582.
8. Dyson, H.J. and Wright, P.E. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6: 197-208.
9. Ellis, R.J. 2001. Macromolecular crowding: An important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 11: 114-119.
10. Erickson, H.P. 2001. The FtsZ protofilament and attachment of ZipA - structural constraints on the FtsZ power stroke. Curr. Opin. Cell Biol. 13: 55-60.
11. Evers, T.H., van Dongen, E.M., Faesen, A.C., Meijer, E.W., and Merkx, M. 2006. Quantitative understanding of the energy transfer between fluorescent proteins connected via flexible peptide linkers. Biochemistry 45: 13183-13192.
12. Flaugh, S.L. and Lumb, K.J. 2001. Effects of macromolecular crowding on the intrinsically disordered proteins c-Fos and p27(Kip1). Biomacromolecules 2: 538-540.
13. Fowler, W.E. and Erickson, H.P. 1979. Trinodular structure of fibrinogen. Confirmation by both shadowing and negative stain electron microscopy. J. Mol. Biol. 134: 241-249.
14. Franks, W.T., Wylie, B.J., Stellfox, S.A., and Rienstra, C.M. 2006. Backbone conformational constraints in a microcrystalline U-15N-labeled protein by 3D dipolar-shift solid-state NMR spectroscopy. J. Am. Chem. Soc. 128: 3154-3155.
15. Heim, R. and Tsien, R.Y. 1996. Engineering green fluorescent protein for improved brightness, longer wavelengths, and fluorescence resonance energy transfer. Curr. Biol. 6: 178-182.
16. Hughes, C.A. and Bennett, V. 1995. Adducin: A physical model with implications for function in assembly of spectrin-actin complexes. J. Biol. Chem. 270: 18990-18996.
17. Lakowicz, J.R. 1999. Principles of fluorescence spectroscopy, 2nd ed. Kluwer Academic, New York.
18. Leahy, D.J., Aukhil, I., and Erickson, H.P. 1996. 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell 84: 155-164.
19. Li, H., Oberhauser, A.F., Redick, S.D., Carrion-Vazquez, M., Erickson, H.P., and Fernandez, J.M. 2001. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. 98: 10682-10686.
20. Liu, Z., Chen, K., Ng, A., Shi, Z., Woody, R.W., and Kallenbach, N.R. 2004. Solvent dependence of PII conformation in model alanine peptides. J. Am. Chem. Soc. 126: 15141-15150.
21. McNulty, B.C., Young, G.B., and Pielak, G.J. 2006. Macromolecular crowding in the Escherichia coli periplasm maintains α-synuclein disorder. J. Mol. Biol. 355: 893-897.
22. McPhie, P., Ni, Y.S., and Minton, A.P. 2006. Macromolecular crowding stabilizes the molten globule form of apomyoglobin with respect to both cold and heat unfolding. J. Mol. Biol. 361: 7-10.
23. Minton, A.P. 2005. Influence of macromolecular crowding upon the stability and state of association of proteins: Predictions and observations. J. Pharm. Sci. 94: 1668-1675.
24. Minton, A.P. and Wilf, J. 1981. Effect of macromolecular crowding upon the structure and function of an enzyme: Glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 20: 4821-4826.
25. Miroux, B. and Walker, J.E. 1996. Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260: 289-298.
26. Mitra, R.D., Silva, C.M., and Youvan, D.C. 1996. Fluorescence resonance energy transfer between blue-emitting and red-shifted excitation derivatives of the green fluorescent protein. Gene 173: 13-17.
27. 2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
28. Mohana-Borges, R., Goto, N.K., Kroon, G.J., Dyson, H.J., and Wright, P.E. 2004. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 340: 1131-1142.
29. Nagai, T., Ibata, K., Park, E.S., Kubota, M., Mikoshiba, K., and Miyawaki, A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20: 87-90.
30. Nguyen, A.W. and Daugherty, P.S. 2005. Evolutionary optimization of fluorescent proteins for intracellular FRET. Nat. Biotechnol. 23: 355-360.
31. Oberhauser, A.F., Marszalek, P.E., Erickson, H.P., and Fernandez, J.M. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393: 181-185.
32. Ohashi, T. and Erickson, H.P. 2004. The disulfide bonding pattern in ficolin multimers. J. Biol. Chem. 279: 6534-6539.
33. Ohashi, T., Hale, C.A., De Boer, P.A., and Erickson, H.P. 2002. Structural evidence that the P/Q domain of ZipA is an unstructured, flexible tether between the membrane and the C-terminal FtsZ-binding domain. J. Bacteriol. 184: 4313-4315.
34. Ormo, M., Cubitt, A.B., Kallio, K., Gross, L.A., Tsien, R.Y., and Remington, S.J. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273: 1392-1395.
35. Patterson, G.H., Piston, D.W., and Barisas, B.G. 2000. Forster distances between green fluorescent protein pairs. Anal. Biochem. 284: 438-440.
36. 2+. Cell Calcium 22: 209-216.
37. Phillips Jr., G.N. 1997. Structure and dynamics of green fluorescent protein. Curr. Opin. Struct. Biol. 7: 821-827.
38. Plaxco, K.W., Spitzfaden, C., Campbell, I.D., and Dobson, C.M. 1997. A comparison of the folding kinetics and thermodynamics of two homologous fibronectin type III modules. J. Mol. Biol. 270: 763-770.
39. Rekas, A., Alattia, J.R., Nagai, T., Miyawaki, A., and Ikura, M. 2002. Crystal structure of venus, a yellow fluorescent protein with improved maturation and reduced environmental sensitivity. J. Biol. Chem. 277: 50573-50578.
40. Rivetti, C., Guthold, M., and Bustamante, C. 1996. Scanning force microscopy of DNA deposited onto mica: Equilibration versus kinetic trapping studied by statistical polymer chain analysis. J. Mol. Biol. 264: 919-932.
41. Schürmann, G., Haspel, J., Grumet, M., and Erickson, H.P. 2001. Cell adhesion molecule L1 in folded (horseshoe) and extended conformations. Mol. Biol. Cell 12: 1765-1773.
42. Shimozono, S., Hosoi, H., Mizuno, H., Fukano, T., Tahara, T., and Miyawaki, A. 2006. Concatenation of cyan and yellow fluorescent proteins for efficient resonance energy transfer. Biochemistry 45: 6267-6271.
43. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27: 527-533.
44. Tsien, R.Y. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67: 509-544.
45. Uversky, V.N. 2002. Natively unfolded proteins: A point where biology waits for physics. Protein Sci. 11: 739-756.
46. Whittington, S.J., Chellgren, B.W., Hermann, V.M., and Creamer, T.P. 2005. Urea promotes polyproline II helix formation: Implications for protein denatured states. Biochemistry 44: 6269-6275.
47. Wu, P. and Brand, L. 1994. Resonance energy transfer: Methods and applications. Anal. Biochem. 218: 1-13.
48. Xu, X., Gerard, A.L., Huang, B.C., Anderson, D.C., Payan, D.G., and Luo, Y. 1998. Detection of programmed cell death using fluorescence energy transfer. Nucleic Acids Res. 26: 2034-2035.
49. Yang, G., Cecconi, C., Baase, W.A., Vetter, I.R., Breyer, W.A., Haack, J.A., Matthews, B.W., Dahlquist, F.W., and Bustamante, C. 2000. Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme. Proc. Natl. Acad. Sci. 97: 139-144.
50. You, X., Nguyen, A.W., Jabaiah, A., Sheff, M.A., Thorn, K.S., and Daugherty, P.S. 2006. Intracellular protein interaction mapping with FRET hybrids. Proc. Natl. Acad. Sci. 103: 18458-18463.
51. Zaccolo, M., De Giorgi, F., Cho, C.Y., Feng, L., Knapp, T., Negulescu, P.A., Taylor, S.S., Tsien, R.Y., and Pozzan, T. 2000. A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat. Cell Biol. 2: 25-29.
52. Zacharias, D.A., Violin, J.D., Newton, A.C., and Tsien, R.Y. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916.
53. Zhou, H.X. 2004. Polymer models of protein stability, folding, and interactions. Biochemistry 43: 2141-2154.