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Ultrafast and low barrier motions in the photoreactions of the green fluorescent protein.

van Thor JJ, Georgiev GY, Towrie M, Sage JT
J Biol Chem 280 33652-9 (2005)
Related entries: 1w7t, 1w7u

Cited: 40 times
EuropePMC logo PMID: 16033764

Abstract

Green fluorescent protein (GFP) fluoresces efficiently under blue excitation despite major electrostatic rearrangements resulting from photoionization of the chromophore and neutralization of Glu-222. A competing phototransformation process, which ionizes the chromophore and decarboxylates Glu-222, mimics the electrostatic and structural changes in the fluorescence photocycle. Structural and spectroscopic analysis of the cryogenically stabilized photoproduct at 100 K and a structurally annealed intermediate of the phototransformed protein at 170 K reveals distinct structural relaxations involving protein, chromophore, solvent, and photogenerated CO2. Strong structural changes of the 100 K photoproduct after decarboxylation appear exclusively within 15 angstroms of the chromophore and include the electrostatically driven perturbations of Gln-69, Cys-70, and water molecules in an H-bonding network connecting the chromophore. X-ray crystallography to 1.85 angstroms resolution and static and picosecond time-resolved IR spectroscopy identify structural mechanisms common to phototransformation and to the fluorescence photocycle. In particular, the appearance of a 1697 cm(-1) (+) difference band in both photocycle and phototransformation intermediates is a spectroscopic signature for the structural perturbation of Gln-69. This is taken as evidence for an electrostatically driven dynamic response that is common to both photoreaction pathways. The interactions between the chromophore and the perturbed residues and solvent are decreased or removed in the T203H single and T203H/Q69L double mutants, resulting in a strong reduction of the fluorescence quantum yield. This suggests that the electrostatic response to the transient formation of a buried charge in the wild type is important for the bright fluorescence.

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  1. The fluorescent protein palette: tools for cellular imaging. Day RN, Davidson MW. Chem Soc Rev 38 2887-2921 (2009)
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  1. Direction of actin flow dictates integrin LFA-1 orientation during leukocyte migration. Nordenfelt P, Moore TI, Mehta SB, Kalappurakkal JM, Swaminathan V, Koga N, Lambert TJ, Baker D, Waters JC, Oldenbourg R, Tani T, Mayor S, Waterman CM, Springer TA. Nat Commun 8 2047 (2017)
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  4. Structural evidence for a dehydrated intermediate in green fluorescent protein chromophore biosynthesis. Pletneva NV, Pletnev VZ, Lukyanov KA, Gurskaya NG, Goryacheva EA, Martynov VI, Wlodawer A, Dauter Z, Pletnev S. J Biol Chem 285 15978-15984 (2010)
  5. Balance between ultrafast parallel reactions in the green fluorescent protein has a structural origin. van Thor JJ, Ronayne KL, Towrie M, Sage JT. Biophys J 95 1902-1912 (2008)
  6. The single T65S mutation generates brighter cyan fluorescent proteins with increased photostability and pH insensitivity. Fredj A, Pasquier H, Demachy I, Jonasson G, Levy B, Derrien V, Bousmah Y, Manoussaris G, Wien F, Ridard J, Erard M, Merola F. PLoS One 7 e49149 (2012)
  7. Crystal structure of a novel domain of the motor subunit of the Type I restriction enzyme EcoR124 involved in complex assembly and DNA binding. Grinkevich P, Sinha D, Iermak I, Guzanova A, Weiserova M, Ludwig J, Mesters JR, Ettrich RH. J Biol Chem 293 15043-15054 (2018)
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Reviews citing this publication (4)

  1. Excited state reactions in fluorescent proteins. Meech SR. Chem Soc Rev 38 2922-2934 (2009)
  2. Photoreactions and dynamics of the green fluorescent protein. van Thor JJ. Chem Soc Rev 38 2935-2950 (2009)
  3. Structure, dynamics and optical properties of fluorescent proteins: perspectives for marker development. Nienhaus GU, Wiedenmann J. Chemphyschem 10 1369-1379 (2009)
  4. Photoactivated structural dynamics of fluorescent proteins. Bourgeois D, Regis-Faro A, Adam V. Biochem Soc Trans 40 531-538 (2012)

Articles citing this publication (19)

  1. Improving the photostability of bright monomeric orange and red fluorescent proteins. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Nat Methods 5 545-551 (2008)
  2. Stabilizing role of glutamic acid 222 in the structure of Enhanced Green Fluorescent Protein. Royant A, Noirclerc-Savoye M. J Struct Biol 174 385-390 (2011)
  3. Ultrafast excited-state dynamics in the green fluorescent protein variant S65T/H148D. 2. Unusual photophysical properties. Shi X, Abbyad P, Shu X, Kallio K, Kanchanawong P, Childs W, Remington SJ, Boxer SG. Biochemistry 46 12014-12025 (2007)
  4. The Protein Chaperone ClpX Targets Native and Non-native Aggregated Substrates for Remodeling, Disassembly, and Degradation with ClpP. LaBreck CJ, May S, Viola MG, Conti J, Camberg JL. Front Mol Biosci 4 26 (2017)
  5. Shoot-and-Trap: use of specific x-ray damage to study structural protein dynamics by temperature-controlled cryo-crystallography. Colletier JP, Bourgeois D, Sanson B, Fournier D, Sussman JL, Silman I, Weik M. Proc Natl Acad Sci U S A 105 11742-11747 (2008)
  6. Ground-state proton transfer in the photoswitching reactions of the fluorescent protein Dronpa. Warren MM, Kaucikas M, Fitzpatrick A, Champion P, Sage JT, van Thor JJ. Nat Commun 4 1461 (2013)
  7. The Role of the Tight-Turn, Broken Hydrogen Bonding, Glu222 and Arg96 in the Post-translational Green Fluorescent Protein Chromophore Formation. Lemay NP, Morgan AL, Archer EJ, Dickson LA, Megley CM, Zimmer M. Chem Phys 348 152-160 (2008)
  8. Wide-dynamic-range kinetic investigations of deep proton tunnelling in proteins. Salna B, Benabbas A, Sage JT, van Thor J, Champion PM. Nat Chem 8 874-880 (2016)
  9. Resilience of the iron environment in heme proteins. Leu BM, Zhang Y, Bu L, Straub JE, Zhao J, Sturhahn W, Alp EE, Sage JT. Biophys J 95 5874-5889 (2008)
  10. Structural changes that occur upon photolysis of the Fe(II)(a3)-CO complex in the cytochrome ba(3)-oxidase of Thermus thermophilus: a combined X-ray crystallographic and infrared spectral study demonstrates CO binding to Cu(B). Liu B, Zhang Y, Sage JT, Soltis SM, Doukov T, Chen Y, Stout CD, Fee JA. Biochim Biophys Acta 1817 658-665 (2012)
  11. Ultrafast photoconversion of the green fluorescent protein studied by accumulative femtosecond spectroscopy. Langhojer F, Dimler F, Jung G, Brixner T. Biophys J 96 2763-2770 (2009)
  12. Polarization sensitive ultrafast mid-IR pump probe micro-spectrometer with diffraction limited spatial resolution. Kaucikas M, Barber J, Van Thor JJ. Opt Express 21 8357-8370 (2013)
  13. Charge transfer in green fluorescent protein. van Thor JJ, Sage JT. Photochem Photobiol Sci 5 597-602 (2006)
  14. Thermal effect on Aequorea green fluorescent protein anionic and neutral chromophore forms fluorescence. dos Santos AM. J Fluoresc 22 151-154 (2012)
  15. Efficient photoconversion distorts the fluorescence lifetime of GFP in confocal microscopy: a model kinetic study on mutant Thr203Val. Jung G, Werner M, Schneider M. Chemphyschem 9 1867-1874 (2008)
  16. Optimal atomistic modifications of material surfaces: design of selective nesting sites for biomolecules. Wang B, Král P. Small 3 580-584 (2007)
  17. Dynamical transition in proteins and non-Gaussian behavior of low-frequency modes in self-consistent normal mode analysis. Guo J, Budarz T, Ward JM, Prohofsky EW. Phys Rev E Stat Nonlin Soft Matter Phys 82 041917 (2010)
  18. Theoretical Computer-Aided Mutagenic Study on the Triple Green Fluorescent Protein Mutant S65T/H148D/Y145F. Armengol P, Gelabert R, Moreno M, Lluch JM. Chemphyschem 16 2134-2139 (2015)
  19. Power Density Titration of Reversible Photoisomerization of a Fluorescent Protein Chromophore in the Presence of Thermally Driven Barrier Crossing Shown by Quantitative Millisecond Serial Synchrotron X-ray Crystallography. Baxter JM, Hutchison CDM, Fadini A, Maghlaoui K, Cordon-Preciado V, Morgan RML, Agthe M, Horrell S, Tellkamp F, Mehrabi P, Pfeifer Y, Müller-Werkmeister HM, von Stetten D, Pearson AR, van Thor JJ. J Am Chem Soc (2024)


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