1w7s Citations

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

J. Biol. Chem. 280 33652-9 (2005)
Related entries: 1w7t, 1w7u

Cited: 32 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.

Reviews - 1w7s mentioned but not cited (4)

  1. Beta-barrel scaffold of fluorescent proteins: folding, stability and role in chromophore formation. Stepanenko OV, Stepanenko OV, Kuznetsova IM, Verkhusha VV, Turoverov KK. Int Rev Cell Mol Biol 302 221-278 (2013)
  2. Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Newman RH, Fosbrink MD, Zhang J. Chem. Rev. 111 3614-3666 (2011)
  3. The fluorescent protein palette: tools for cellular imaging. Day RN, Davidson MW. Chem Soc Rev 38 2887-2921 (2009)
  4. Fluorescent proteins as biomarkers and biosensors: throwing color lights on molecular and cellular processes. Stepanenko OV, Verkhusha VV, Kuznetsova IM, Uversky VN, Turoverov KK. Curr. Protein Pept. Sci. 9 338-369 (2008)

Articles - 1w7s mentioned but not cited (7)

  1. 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)
  2. 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)
  3. Anomalous negative fluorescence anisotropy in yellow fluorescent protein (YFP 10C): quantitative analysis of FRET in YFP dimers. Shi X, Basran J, Seward HE, Childs W, Bagshaw CR, Boxer SG. Biochemistry 46 14403-14417 (2007)
  4. 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)
  5. Actin retrograde flow actively aligns and orients ligand-engaged integrins in focal adhesions. Swaminathan V, Kalappurakkal JM, Mehta SB, Nordenfelt P, Moore TI, Koga N, Baker DA, Oldenbourg R, Tani T, Mayor S, Springer TA, Waterman CM. Proc. Natl. Acad. Sci. U.S.A. 114 10648-10653 (2017)
  6. 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)
  7. pHluorin-assisted expression, purification, crystallization and X-ray diffraction data analysis of the C-terminal domain of the HsdR subunit of the Escherichia coli type I restriction-modification system EcoR124I. Grinkevich P, Iermak I, Luedtke NA, Mesters JR, Ettrich R, Ludwig J. Acta Crystallogr F Struct Biol Commun 72 672-676 (2016)


Reviews citing this publication (3)

  1. Photoactivated structural dynamics of fluorescent proteins. Bourgeois D, Regis-Faro A, Adam V. Biochem. Soc. Trans. 40 531-538 (2012)
  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)

Articles citing this publication (18)

  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. 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)
  5. 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)
  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. 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)
  8. 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)
  9. 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)
  10. 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)
  11. Charge transfer in green fluorescent protein. van Thor JJ, Sage JT. Photochem. Photobiol. Sci. 5 597-602 (2006)
  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. 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)
  14. Optimal atomistic modifications of material surfaces: design of selective nesting sites for biomolecules. Wang B, Král P. Small 3 580-584 (2007)
  15. 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)
  16. Thermal effect on Aequorea green fluorescent protein anionic and neutral chromophore forms fluorescence. dos Santos AM. J Fluoresc 22 151-154 (2012)
  17. 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)
  18. 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)