The extremely slow-exchanging core and acid-denatured state of green fluorescent protein

HFSP Journal

Volumn 2, Issue 6, 2008, Pages 378-387

  Huang, Jie rong ^a,b   Danny Hsu, Shang Te ^a   Christodoulou, John ^a,c,d   Jackson, Sophie E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 70349347502     PISSN: 19552068     EISSN: 1955205X     Source Type: Journal    
DOI: 10.2976/1.2976660     Document Type: Article

References (67)

1. Alkaabi, KM, Yafea, A, and Ashraf, SS (2005). "Effect of pH on thermaland chemical-induced denaturation of GFP." Appl. Biochem. Biotechnol. 126, 149-156.
2. Andrews, BT, Schoenfish, AR, Roy, M, Waldo, G, and Jennings, PA (2007). "The rough energy landscape of superfolder GFP is linked to the chromophore." J. Mol. Biol. 373, 476-490.
3. Bai, Y, Milne, JS, Mayne, L, and Englander, SW (1993). "Primary structure effects on peptide group hydrogen exchange." Proteins 17, 75-86.
4. Bai, Y, Milne, JS, Mayne, L, and Englander, SW (1994). "Protein stability parameters measured by hydrogen exchange." Proteins 20, 4-14.
5. Bai, Y, Sosnick, TR, Mayne, L, and Englander, SW (1995). "Protein folding intermediates: native-state hydrogen exchange." Science 269, 192-197.
6. Bhavesh, NS, Juneja, J, Udgaonkar, JB, and Hosur, RV (2004). "Native and nonnative conformational preferences in the urea-unfolded state of barstar." Protein Sci. 13, 3085-3091.
7. Bhavesh, NS, Panchal, SC, Mittal, R, and Hosur, RV (2001). "NMR identification of local structural preferences in HIV-1 protease tethered heterodimer in 6 M guanidine hydrochloride." FEBS Lett. 509, 218-224.
8. Bhavesh, NS, Sinha, R, Mohan, PM, and Hosur, RV (2003). "NMR elucidation of early folding hierarchy in HIV-1 protease." J. Biol. Chem. 278, 19980-19985.
9. Bhutani, N, and Udgaonkar, JB (2003). "Folding subdomains of thioredoxin characterized by native-state hydrogen exchange." Protein Sci. 12, 1719-1731.
10. Bowler, BE (2007). "Thermodynamics of protein denatured states." Mol. Biosyst. 3, 88-99.
11. Chamberlain, AK, Handel, TM, and Marqusee, S (1996). "Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH." Nat. Struct. Biol. 3, 782-787.
12. Chatterjee, A, Mridula, P, Mishra, RK, Mittal, R, and Hosur, RV (2005). "Folding regulates autoprocessing of HIV-1 protease precursor." J. Biol. Chem. 280, 11369-11378.
13. Clarke, J, and Itzhaki, LS (1998). "Hydrogen exchange and protein folding." Curr. Opin. Struct. Biol. 8, 112-118.
14. Clarke, J, Itzhaki, LS, and Fersht, AR (1997). "Hydrogen exchange at equilibrium: a short cut for analysing protein-folding pathways?" Trends Biochem. Sci. 22, 284-287.
15. Connelly, GP, Bai, Y, Jeng, MF, and Englander, SW (1993). "Isotope effects in peptide group hydrogen exchange." Proteins 17, 87-92.
16. Delaglio, F, Grzesiek, S, Vuister, GW, Zhu, G, Pfeifer, J, and Bax, A (1995). "NMRPipe: a multidimensional spectral processing system based on UNIX pipes." J. Biomol. NMR 6, 277-293.
17. Dempsey, CE (2001). "Hydrogen exchange in peptides and proteins using NMR-spectroscopy." Prog. Nucl. Magn. Reson. Spectrosc. 39, 135-170.
18. Dietz, H, and Rief, M (2004). "Exploring the energy landscape of GFP by single-molecule mechanical experiments." Proc. Natl. Acad. Sci. U.S.A. 101, 16192-16197.
19. Dyson, HJ, and Wright, PE (2004). "Unfolded proteins and protein folding studied by NMR." Chem. Rev. (Washington, D.C.) 104, 3607-3622.
20. Englander, SW (2000). "Protein folding intermediates and pathways studied by hydrogen exchange." Annu. Rev. Biophys. Biomol. Struct. 29, 213-238.
21. Englander, SW, and Kallenbach, NR (1983). "Hydrogen-exchange and structural dynamics of proteins and nucleic-acids." Q. Rev. Biophys. 16, 521-655.
22. Englander, SW, Mayne, L, and Krishna, MMG (2007). "Protein folding and misfolding: mechanism and principles." Q. Rev. Biophys. 40, 287-326.
23. Enoki, S, Maki, K, Inobe, T, Takahashi, K, Kamagata, K, Oroguchi, T, Nakatani, H, Tomoyori, K, and Kuwajima, K (2006). "The equilibrium unfolding intermediate observed at pH 4 and its relationship with the kinetic folding intermediates in green fluorescent protein." J. Mol. Biol. 361, 969-982.
24. Enoki, S, Saeki, K, Maki, K, and Kuwajima, K (2004). "Acid denaturation and refolding of green fluorescent protein." Biophys. J. 43, 14238-14248.
25. See EPAPS Document No. E-HJFOA5-2-001807 for supplemental material. This document can be reached through a direct link in the online article's HTML reference Section or via the EPAPS homepage (http://www.aip.org/pubservs/epaps.html).
26. Ferraro, DM, Lazo, ND, and Robertson, AD (2004). "EX1 hydrogen exchange and protein folding." Biophys. J. 43, 587-594.
27. Fukuda, H, Arai, M, and Kuwajima, K (2000). "Folding of green fluorescent protein and the cycle3 mutant." Biophys. J. 39, 12025-12032.
28. Grzesiek, S, and Bax, A (1993). "Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins." J. Biomol. NMR 3, 185-204.
29. Helms, V, Straatsma, TP, and McCammon, JA (1999). "Internal dynamics of green fluorescent protein." J. Phys. Chem. B 103, 3263-3269.
30. Huang, JR, Craggs, TD, Christodoulou, J, and Jackson, SE (2007). "Stable intermediate states and high energy barriers in the unfolding of GFP." J. Mol. Biol. 370, 356-371.
31. Huyghues-Despointes, BM, Scholtz, JM, and Pace, CN (1999). "Protein conformational stabilities can be determined from hydrogen exchange rates." Nat. Struct. Biol. 6, 910-912.
32. Hvidt, A, and Nielsen, SO (1966). "Hydrogen exchange in proteins." Adv. Protein Chem. 21, 287-386.
33. Iimura, S, et al. (2007). "Characterization of the denatured structure of pyrrolidone carboxyl peptidase from a hyperthermophile under nondenaturing conditions: role of the C-terminal alpha-helix of the protein in folding and stability." Biophys. J. 46, 3664-3672.
34. Jackson, SE, Craggs, TD, and Huang, JR (2006). "Understanding the folding of GFP using biophysical techniques." Expert Rev. Proteomics 3, 545-559.
35. Johnson, BA, and Blevins, RA (1994). "NMR view-a computer-program for the visualization and analysis of NMR data." J. Biomol. NMR 4, 603-614.
36. Karplus, M, and McCammon, JA (1981). "The internal dynamics of globular proteins." Crit. Rev. Biochem. 9, 293-349.
37. Khan, F, Kuprov, I, Craggs, TD, Hore, PJ, and Jackson, SE (2006). "(19)F NMR studies of the native and denatured states of green fluorescent protein." J. Am. Chem. Soc. 128, 10729-10737.
38. Klein-Seetharaman, J, et al. (2002). "Long-range interactions within a nonnative protein." Science 295, 1719-1722.
39. Krishna, MM, Hoang, L, Lin, Y, and Englander, SW (2004). "Hydrogen exchange methods to study protein folding." Methods 34, 51-64.
40. Linderstrom-Lang, K (1958). "Deuterium exchange and protein structure." In Symposium of Protein Structure. Neuberger, A (ed.), pp 23-24, Methuen, London.
41. Mayo, SL, and Baldwin, RL (1993). "Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A." Science 262, 873-876.
42. Miller, DW, and Dill, KA (1995). "A statistical mechanical model for hydrogen exchange in globular proteins." Methods 4, 1860-1873.
43. Mohana-Borges, R, Goto, NK, Kroon, GJ, Dyson, HJ, and Wright, PE (2004). "Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings." J. Mol. Biol. 340, 1131-1142.
44. Nakanishi, M, Tsuboi, M, and Ikegami, A (1973). "Fluctuation of the lysozyme structure. II. Effects of temperature and binding of inhibitors." J. Mol. Biol. 75, 673-682.
45. Oliveberg, M, and Fersht, AR (1996). "Thermodynamics of transient conformations in the folding pathway of barnase: reorganization of the folding intermediate at low pH." Biophys. J. 35, 2738-2749.
46. Ormo, M, Cubitt, AB, Kallio, K, Gross, LA, Tsien, RY, and Remington, SJ (1996). "Crystal structure of the Aequorea victoria green fluorescent protein." Science 273, 1392-1395.
47. Otting, G, Liepinsh, E, and Wuthrich, K (1991). "Protein hydration in aqueous solution." Science 254, 974-980.
48. Pace, CN, Laurents, DV, and Erickson, RE (1992). "Urea denaturation of barnase: pH dependence and characterization of the unfolded state." Biophys. J. 31, 2728-2734.
49. Palmer, AG, Cavanagh, J, Wright, PE, and Rance, M (1991). "Sensitivity improvement in proton-detected 2-dimensional heteronuclear correlation NMR-spectroscopy." J. Mater. Res. 93, 151-170.
50. Reid, BG, and Flynn, GC (1997). "Chromophore formation in green fluorescent protein." Biophys. J. 36, 6786-6791.
51. Religa, TL, Markson, JS, Mayor, U, Freund, SM, and Fersht, AR (2005). "Solution structure of a protein denatured state and folding intermediate." Nature (London) 437, 1053-1056.
52. Robic, S, Guzman-Casado, M, Sanchez-Ruiz, JM, and Marqusee, S (2003). "Role of residual structure in the unfolded state of a thermophilic protein." Proc. Natl. Acad. Sci. U.S.A. 100, 11345-11349.
53. Schanda, P, and Brutscher, B (2005). "Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds." J. Am. Chem. Soc. 127, 8014-8015.
54. Schleucher, J, Schwendinger, M, Sattler, M, Schmidt, P, Schedletzky, O, Glaser, SJ, Sorensen, OW, and Griesinger, C (1994). "A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed field gradients." J. Biomol. NMR 4, 301-306.
55. Seifert, MH, Georgescu, J, Ksiazek, D, Smialowski, P, Rehm, T, Steipe, B, and Holak, TA (2003). "Backbone dynamics of green fluorescent protein and the effect of histidine 148 substitution." Biophys. J. 42, 2500-2512.
56. Shortle, D, and Ackerman, MS (2001). "Persistence of native-like topology in a denatured protein in 8 M urea." Science 293, 487-489.
57. Shortle, D, Chan, HS, and Dill, KA (1992). "Modeling the effects of mutations on the denatured states of proteins." Protein Sci. 1, 201-215.
58. Takei, J, Pei, W, Vu, D, and Bai, Y (2002). "Populating partially unfolded forms by hydrogen exchange-directed protein engineering." Biophys. J. 41, 12308-12312.
59. Tsien, RY (1998). "The green fluorescent protein." Annu. Rev. Biochem. 67, 509-544.
60. Wagner, G, and Wuthrich, K (1982). "Amide protein exchange and surface conformation of the basic pancreatic trypsin inhibitor in solution." J. Mol. Biol. 160, 343-361.
61. Wirmer, J, Schlorb, C, Klein-Seetharaman, J, Hirano, R, Ueda, T, Imoto, T, and Schwalbe, H (2004). "Modulation of compactness and longrange interactions of unfolded lysozyme by single point mutations." Angew. Chem., Int. Ed. 43, 5780-5785.
62. Woodward, C, Simon, I, and Tuchsen, E (1982). "Hydrogen exchange and the dynamic structure of proteins." Mol. Cell. Biochem. 48, 135-160.
63. Yan, S, Kennedy, SD, and Koide, S (2002). "Thermodynamic and kinetic exploration of the energy landscape of Borrelia burgdorferi OspA by native-state hydrogen exchange." J. Mol. Biol. 323, 363-375.
64. Yang, F, Moss, LG, and Phillips, GN, Jr. (1996). "The molecular structure of green fluorescent protein." Nat. Biotechnol. 14, 1246-1251.
65. Zhang, X, Xu, Y, Zhang, J, Wu, J, and Shi, Y (2005). "Structural and dynamic characterization of the acid-unfolded state of hUBF HMG box 1 provides clues for the early events in protein folding." Biophys. J. 44, 8117-8125.
66. Zhang, Y-Z, and Roder, H. "SPHERE: a server program for hydrogen exchange rate estimation."
67. Zimmer, M (2002). "Green fluorescent protein (GFP): applications, structure, and related photophysical behavior." Chem. Rev. (Washington, D.C.) 102, 759-781.