Fluorescence of Alexa Fluor Dye Tracks Protein Folding

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Lindhoud, Simon ^a   Westphal, Adrie H ^a   Visser, Antonie J W G ^a   Borst, Jan Willem ^a   van Mierlo, Carlo P M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXA FLUOR; CYSTEINE; DYE; FLAVODOXIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; AZOTOBACTER VINELANDII; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; NONHUMAN; PROTEIN FOLDING; PROTEIN STRUCTURE; QUANTUM YIELD; STEADY STATE; THERMODYNAMICS; UNFOLDED PROTEIN RESPONSE;

APOPROTEINS; AZOTOBACTER VINELANDII; BACTERIAL PROTEINS; CYSTEINE; FLAVODOXIN; FLUORESCENT DYES; MALEIMIDES; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; TIME FACTORS;

EID: 84867305395     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046838     Document Type: Article

References (41)

1. Anfinsen CB, (1973) Principles that govern the folding of protein chains. Science 181: 223-230.
2. Dill KA, Chan HS, (1997) From Levinthal to pathways to funnels. Nat Struct Mol Biol 4: 10-19.
3. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (1995) Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins Struct Funct Bioinf 21: 167-195.
4. Dinner AR, Sali A, Smith LJ, Dobson CM, Karplus M, (2000) Understanding protein folding via free-energy surfaces from theory and experiment. Trends Biochem Sci 25: 331-339.
5. Ptitsyn OB, (1995) Molten globule and protein folding. Adv Protein Chem 47: 83-229.
6. Arai M, Kuwajima K, (2000) Role of the molten globule state in protein folding. Adv Protein Chem 53: 209-282.
7. Dobson CM, (2003) Protein folding and misfolding. Nature 426: 884-890.
8. Vendruscolo M, Paci E, Dobson CM, Karplus M, (2001) Three key residues form a critical contact network in a protein folding transition state. Nature 409: 641-645.
9. Ohgushi M, Wada A, (1983) 'Molten-globule state': a compact form of globular proteins with mobile side-chains. FEBS Lett 164: 21-24.
10. Eftink MR, (1994) The use of fluorescence methods to monitor unfolding transitions in proteins. Biophys J 66: 482-501.
11. Kuznetsova IM, Turoverov KK, Uversky VN, (2004) Use of the phase diagram method to analyze the protein unfolding-refolding reactions: Fishing out the "invisible" intermediates. Journal of Proteome Research 3: 485-494.
12. Visser NV, Westphal AH, van Hoek A, van Mierlo CP, Visser AJ, et al. (2008) Tryptophan-tryptophan energy migration as a tool to follow apoflavodoxin folding. Biophys J 95: 2462-2469.
13. Laptenok SP, Visser NV, Engel R, Westphal AH, van Hoek A, et al. (2011) A general approach for detecting folding intermediates from steady-state and time-resolved fluorescence of single-tryptophan-containing proteins. Biochemistry 50: 3441-3450.
14. Panchuk-Voloshina N, Haugland RP, Bishop-Stewart J, Bhalgat MK, Millard PJ, et al. (1999) Alexa dyes, a series of new fluorescent dyes that yield exceptionally bright, photostable conjugates. J Histochem Cytochem 47: 1179-1188.
15. Deniz AA, Laurence TA, Beligere GS, Dahan M, Martin AB, et al. (2000) Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc Natl Acad Sci USA 97: 5179-5184.
16. Rhoades E, Cohen M, Schuler B, Haran G, (2004) Two-state folding observed in individual protein molecules. J Am Chem Soc 126: 14686-14687.
17. Schuler B, Lipman EA, Eaton WA, (2002) Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419: 743-747.
18. Deniz AA, Dahan M, Grunwell JR, Ha TJ, Faulhaber AE, et al. (1999) Single-pair fluorescence resonance energy transfer on freely diffusing molecules: Observation of Forster distance dependence and subpopulations. Proc Natl Acad Sci USA 96: 3670-3675.
19. Haas E, Katchalski-Katzir E, Steinberg IZ, (1978) Brownian-Motion of Ends of Oligopeptide Chains in Solution as Estimated by Energy-Transfer between Chain Ends. Biopolymers 17: 11-31.
20. Amir D, Haas E, (1987) Estimation of Intramolecular Distance Distributions in Bovine Pancreatic Trypsin-Inhibitor by Site-Specific Labeling and Nonradiative Excitation Energy-Transfer Measurements. Biochemistry 26: 2162-2175.
21. Förster T, (1948) Zwischenmolekulare Energiewanderung Und Fluoreszenz. Ann Phys 2: 55-75.
22. Stryer L, Haugland RP, (1967) Energy transfer: a spectroscopic ruler. Proc Natl Acad Sci USA 58: 719-726.
23. Engel R, Westphal AH, Huberts DH, Nabuurs SM, Lindhoud S, et al. (2008) Macromolecular crowding compacts unfolded apoflavodoxin and causes severe aggregation of the off-pathway intermediate during apoflavodoxin folding. J Biol Chem 283: 27383-27394.
24. Rhoades E, Gussakovsky E, Haran G, (2003) Watching proteins fold one molecule at a time. Proc Natl Acad Sci USA 100: 3197-3202.
25. Bollen YJ, Sanchéz IE, van Mierlo CP, (2004) Formation of on- and off-pathway intermediates in the folding kinetics of Azotobacter vinelandii apoflavodoxin. Biochemistry 43: 10475-10489.
26. Bollen YJ, Kamphuis MB, van Mierlo CP, (2006) The folding energy landscape of apoflavodoxin is rugged: Hydrogen exchange reveals nonproductive misfolded intermediates. Proc Natl Acad Sci USA 103: 4095-4100.
27. Bollen YJ, Nabuurs SM, van Berkel WJ, van Mierlo CP, (2005) Last in, first out: The role of cofactor binding in flavodoxin folding. J Biol Chem 280: 7836-7844.
28. Steensma E, Heering HA, Hagen WR, Van Mierlo CP, (1996) Redox properties of wild-type, Cys69Ala, and Cys69Ser Azotobacter vinelandii flavodoxin II as measured by cyclic voltammetry and EPR spectroscopy. Eur J Biochem 235: 167-172.
29. Nabuurs SM, Westphal AH, van Mierlo CP, (2008) Extensive formation of off-pathway species during folding of an α-β parallel protein is due to docking of (non)native structure elements in unfolded molecules. J Am Chem Soc 130: 16914-16920.
30. Nabuurs SM, Westphal AH, aan den Toorn M, Lindhoud S, van Mierlo CP, (2009) Topological switching between an α-β parallel protein and a remarkably helical molten globule. J Am Chem Soc 131: 8290-8295.
31. Nabuurs SM, de Kort BJ, Westphal AH, van Mierlo CP, (2009) Non-native hydrophobic interactions detected in unfolded apoflavodoxin by paramagnetic relaxation enhancement. Eur Biophys J 39: 689-698.
32. van Mierlo CP, van Dongen WM, Vergeldt F, van Berkel WJ, Steensma E, (1998) The equilibrium unfolding of Azotobacter vinelandii apoflavodoxin II occurs via a relatively stable folding intermediate. Protein Sci 7: 2331-2344.
33. Borst JW, Hink MA, van Hoek A, Visser AJ, (2005) Effects of refractive index and viscosity on fluorescence and anisotropy decays of enhanced cyan and yellow fluorescent proteins. J Fluoresc 15: 153-160.
34. Nozaki Y (1972) The preparation of guanidine hydrochloride. Methods Enzymol 26.
35. Bollen YJ, van Mierlo CP, (2005) Protein topology affects the appearance of intermediates during the folding of proteins with a flavodoxin-like fold. Biophys Chem 114: 181-189.
36. Lakowicz JR (2006) Principles of fluorescence spectroscopy. New York: Springer Verlag. 954 p.
37. Sillen A, Engelborghs Y, (1998) The correct use of "average" fluorescence parameters. Photochem Photobiol 67: 475-486.
38. Chen H, Ahsan SS, Santiago-Berrios MB, Abruna HD, Webb WW, (2010) Mechanisms of quenching of Alexa fluorophores by natural amino acids. J Am Chem Soc 132: 7244-7245.
39. Choi J, Kim S, Tachikawa T, Fujitsuka M, Majima T, (2011) Unfolding dynamics of cytochrome c revealed by single-molecule and ensemble-averaged spectroscopy. Phys Chem Chem Phys 13: 5651-5658.
40. Zhong DP, Zewail AH, (2001) Femtosecond dynamics of flavoproteins: Charge separation and recombination in riboflavine (vitamin B-2)-binding protein and in glucose oxidase enzyme. Proc Natl Acad Sci USA 98: 11867-11872.
41. Alagaratnam S, van Pouderoyen G, Pijning T, Dijkstra BW, Cavazzini D, et al. (2005) A crystallographic study of Cys69Ala flavodoxin II from Azotobacter vinelandii: structural determinants of redox potential. Protein Sci 14: 2284-2295.