Understanding the folding of GFP using biophysical techniques

Expert Review of Proteomics

Volumn 3, Issue 5, 2006, Pages 545-559

  Jackson, Sophie E ^a   Craggs, Timothy D ^a   Huang, Jie Rong ^a  

^a Chemistry Department   (United Kingdom)

Author keywords

Aggregation; Denatured state; Equilibrium intermediate; Kinetic intermediate; Misfolding; Oligomeric state; Protein folding selection

Indexed keywords

BIOLOGICAL MARKER; GREEN FLUORESCENT PROTEIN;

BIOPHYSICS; BIOSENSOR; CHROMATOPHORE; CYCLIZATION; DIMERIZATION; GENE EXPRESSION; MEDICAL RESEARCH; NONHUMAN; OXIDATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN VARIANT; REVIEW; SCIENTIFIC LITERATURE;

GREEN FLUORESCENT PROTEINS; KINETICS; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING;

EID: 33750612930     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/14789450.3.5.545     Document Type: Review

References (48)

1. Tsien RY. The green fluorescent protein. Ann. Rev. Biochem. 67, 509-544 (1998).
2. Shaner NC, Steinbach PA, Tsien RY. A guide to choosing fluorescent proteins. Nat. Methods 2, 905-916 (2005). • Very useful practical guide to selecting fluorescent proteins for use in a wide range of applications.
3. Zimmer M. Green fluorescent protein (GFP): applications structure, and related photophysical behavior. Chem. Rev. 102, 759-781 (2002).
4. Reid BG, Flynn GC. Chromophore formation in green fluorescent protein. Biochemistry 36, 6786-6791 (1997).
5. Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392-1395 (1996).
6. Yang F, Moss L, Phillips G. The molecular structure of green fluorescent protein. Nat. Biotech. 14, 1246-1251 (1996).
7. Waldo GS, Standish BM, Berendzen J, Terwillger TC. Rapid protein folding assay using green fluorescent protein. Nat. Biotechnol. 17, 691-695 (1999).
8. Baird GS, Zacharias DA, Tsien RY. Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl Acad. Sci. USA 96, 11241-11246 (1999).
9. Topell S, Hennecke J, Glockshuber R. Circularly permuted variants of the green fluorescent protein. FEBS Lett. 457, 283-289 (1999).
10. Topell S, Glockshuber R. Circular permutation of the green fluorescent protein. Methods Mol. Biol. 183, 31-48 (2002).
11. Siemering K. R, Golbik R, Sever R, Haseloff J. Mutations that suppress the thermosensitivity of green fluorescent protein. Current Biol. 6, 1653-1663 (1996).
12. Kimata Y, Iwaki M, Lim CR, Kohno K. A novel mutation which enhances the fluorescence of GFP at high temperatures. Biochem. Biophys. Res. Comm. 232, 69-73 (1997).
13. Crameri A, Whitehorn EA, Tate E, Stemmer WP. C. Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat. Biotech. 14, 315-319 (1996).
14. Battistutta R, Negro A, Zanotti G. Crystal structure and refolding properties of the mutant F99S/M153T/V163A of the Green Fluorescent Protein. Proteins: Struct. Func. Gen. 41, 429-437 (2000). • The structure and folding properties of the widely used cycle 3 variant.
15. Fukuda H, Arai M, Kuwajima K. Folding of green fluorescent protein and the cycle 3 mutant. Biochemistry 39, 12025-12032 (2000).
16. Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotech. 24, 79-88 (2006). •• Describes very recent studies on the selection of a superfolding variant of GFP using a folding interference method for selection.
17. Heim R, Prasher DC, Tsien RY. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl Acad. Sci. USA 91, 12501-12504 (1994).
18. Cubitt AB, Heim R, Adams SR, Boyd AE, Gross LA, Tsien RY. Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci. 20, 448-455 (1995).
19. Wood TI, Barondeau DP, Hitomi C, Kassmann CJ, Tainer JA, Getzoff ED. Defining the role of arginine 96 in Green fluorescent protein fluorophore biosynthesis. Biochemistry 44, 16211-16220 (2005).
20. Sniegowski JA, Phail ME, Wachter RM. Maturation efficiency, trypsin sensitivity, and optical properties of Arg96, Glu222, and Gly67 variants of green fluorescent protein. Biochem. Biophys. Res. Comm. 332, 657-663 (2005).
21. Barondeau DP, Putnam CD, Kassmann CJ, Tainer JA, Getzoff ED. Mechanism and energetics of green fluorescent protein chromophore synthesis revealed by trapped intermediate structures. Proc. Natl Acad. Sci. USA 100, 12111-12116 (2003). •• Here, mutations which substantially slow the rate but not the yield of post-translationally modified protein are used and the structure of the trapped precyclisation intermediate and oxidised post-translational state reported.
22. Rosenow MA, Huffman HA, Phail ME, Wachter RM. The crystal structure of the Y66L variant of green fluorescent protein Supports a cyclization-oxidation- dehydration mechanism for chromophore maturation. Biochemistry 43, 4464-4472 (2004).
23. Zhang L, Patel HN, Lappe JW, Wachter RM. Reaction Progress of Chromophore Biogenesis in Green Fluorescent Protein. J. Am. Chem. Soc. 128, 4766-4772 (2006). •• This study uses the kinetics of hydrogen peroxide evolution during the maturation of GFP in vitro to inform on the mechanism of formation. Under highly aerobic conditions, the dominant pathway is found to involve a cyclisation then oxidation followed by dehydration.
24. Siegbahn PEM, Wirstam M, Zimmer M. Theoretical study of the mechanism of peptide ring formation in green fluorescent protein. Int. J. Quantum Chem. 81, 169-186 (2001).
25. Branchini BR, Nemser AR, Zimmer M. A computational analysis of the unique protein-induced tight turn that results in posttranslational chromophore formation in green fluorescent protein. J. Am. Chem. Soc. 120, 1-6 (1998).
26. Baffour-Awuah NY, Fedeles F, Zimmer M. Structural features responsible for GFPuv and S147P-GFP's improved fluorescence. Chem. Phys. 310, 25-31 (2005).
27. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric gfps into membrane microdomains of live cells. Science 296, 913-916 (2002).
28. Jackson SE. How do small single-domain proteins fold? Fold. Des. 3, 81-91 (1998).
29. Huang J-R, Craggs TD, Christodoulou J, Jackson SE. Stable intermediate states are formed in the equilibrium unfolding of GFP. Protein Science submitted (2006).
30. Merkel JS, Regan L. Modulating Protein Folding rates in vivo and in vitro by side-chain interactions between the parallel strands of green fluorescent protein. J. Biol. Chem. 275, 29200-29206 (2000).
31. Iwai H, Lingel A, Pluckthun A. Cyclic green fluorescent protein produced in vivo using an artificially split PI-PfuI intein from Pyrococcus furiosus. J. Biol. Chem. 276, 16548-16554 (2001).
32. Enoki S, Saeki K, Maki K, Kuwajima K. Acid denaturation and refolding of green fluorescent protein. Biochemistry 43, 14238-14248 (2004). •• This study was the first to report detailed kinetic experiments on the folding of GFP and detect multiple intermediate states and a parallel pathway resulting from proline isomerisation.
33. Enoki S, Maki K, inobe T, Takahashi K et al. The equilibrium unfolding intermediate observed at pH 4 and its relationship with the kinetic folding intermediates in green fluorescent protein. J. Mol. Biol. 361(5), 969-982 (2006).
34. Vrzheshch PV, Akovbian NA, Varfolomeyev SD, Verkhusha VV. Denaturation and partial renaturation of a tightly tetramized DsRed protein under mildly acidic conditions. FEBS Lett. 487, 203-208 (2000).
35. Stepanenko OV, Verkhusha VV, Kazakov VI et al. Comparative studies on the structure and stability of fluorescent proteins EGFP, zFP506, mRFP1, "dimer2", and DsRed1. Biochemistry 43, 14913-14923 (2004).
36. Herberhold H, Marchal S, Lange R, Scheyhing CH, Vogel RF, Winter R. Characterization of the pressure -induced intermediate and unfolded state of red-shifted green fluorescent protein - a static and kinetic FTIR, UV/VIS and fluorescence spectroscopy study. J. Mol. Biol. 330, 1153-1164 (2003).
37. 19F NMR studies of the native and denatured states of green fluorescent protein. J. Am. Chem. Soc. 128, 10729-10737 (2006).
38. Haupt U, Maiti S, Schwille P, Webb WW. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc. Natl Acad. Sci. USA 95, 13573-13578 (1998).
39. Bonsma S, Purchase R, Jezowski S, Gallus J, Konz F, Volke RS. Green and red fluorescent proteins: photo- and thermally induced dynamics probed by site-selective spectroscopy and hole burning. Chem. Phys. Chem. 6, 838-849 (2005).
40. Seifert MH. J, Georgescu J, Ksiazek D et al. Backbone dynamics of green fluorescent protein and the effect of histidine 148 substitution. Biochemistry 42, 2500-2512 (2003).
41. Dietz H, Rief M. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl Acad. Sci. USA 101, 16192-16197 (2004).
42. Dickson RM, Cubitt AB, Tsien RY, Moerner WE. On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388, 355-258 (1997).
43. Schwille P, Kummer S, Heikal AA, Moerner WE, Webb WW. Dynamics of fluorescence fluctuations in green fluorescent protein observed by fluorescence correlation spectroscopy. Proc. Natl Acad. Sci. USA 97, 151-156 (2000).
44. Cannone F, Bologna S, Campanini B, Diaspro A, Bettati S, Mozzarelli A, Chirico G. Tracking unfolding and refolding of single GFPmut2 molecules. Biophys. J. 89, 2033-2045 (2005).
45. White SS, Balasubramanian S, Klenerman D, Ying LM. A Simple nanomixer for single molecule kinetics. Angewante Chem. (2006) (In Press).
46. Heikal AA, Hess ST, Baird GS, Tsien RY, Webb WW. Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: Coral red (dsRed) and yellow (Citrine). Proc. Natl Acad. Sci. USA 97, 11996-12001 (2000).
47. Zhang J, Campbell RE, Ting A, Tsien RY. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Biol. 3, 906-918 (2002).
48. Miyawaki A, Tsien RY. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327 472-500 (2000).