Resonantly enhanced multiphoton ionization spectrum of the neutral green fluorescent protein chromophore

Journal of Physical Chemistry Letters

Volumn 5, Issue 20, 2014, Pages 3588-3592

  Greenwood, Jason B ^a   Miles, Jordan ^a   Camillis, Simone De ^a   Mulholland, Peter ^a   Zhang, Lijuan ^b   Parkes, Michael A ^b   Hailes, Helen C ^b   Fielding, Helen H ^b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

absorption; femtosecond; gas phase; time dependent density functional theory; ultraviolet

Indexed keywords

ABSORPTION; BLUE SHIFT; DENSITY FUNCTIONAL THEORY; ELECTRONIC STRUCTURE; FLUORESCENCE; IONIZATION OF GASES; MULTIPHOTON PROCESSES; PHOTOIONIZATION; PHOTOPHYSICS; PROTEINS;

ELECTRONIC STRUCTURE CALCULATIONS; FEMTOSECONDS; GASPHASE; GREEN FLUORESCENT PROTEIN; MULTIPHOTON IONIZATION SPECTRA; RESONANTLY ENHANCED MULTIPHOTON IONIZATION; TIME DEPENDENT DENSITY FUNCTIONAL THEORY; ULTRAVIOLET;

CHROMOPHORES;

EID: 84908056206     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz5019256     Document Type: Article

References (50)

1. Shimomura, O.; Johnson, F. H.; Saigai, Y. Extraction, Purification and Properties of Aequorin, a Bioluminescent Protein from the Luminous Hydromedusan, Aequorea J. Cell. Comp. Physiol. 1962, 59, 223
2. Griffin, B. A.; Adams, S. R.; Tsien, R. Y. Specific Covalent Labeling of Recombinant Protein Molecules Inside Live Cells Science 1998, 281, 269-272
3. Tsien, R. Y. The Green Fluorescent Protein Annu. Rev. Biochem. 1998, 67, 509-544
4. Chalfie, M.; Tu, Y.; Euskirchen, G.; Ward, W. W.; Prasherf, D. C. Green Fluorescent Protein as a Marker for Gene Expression Science 1994, 263, 802-805
5. Nielsen, S. B.; Lapierre, A.; Andersen, J. U.; Pedersen, U. V.; Tomita, S.; Andersen, L. H. Absorption Spectrum of the Green Fluorescent Protein Chromophore Anion in vacuo Phys. Rev. Lett. 2001, 87, 228102
6. Forbes, M. W.; Nagy1, A. M.; Jockusch, R. A. Photofragmentation of and electron photodetachment from a GFP model chromophore in a quadrupole ion trap Int. J. Mass Spectrom. 2011, 308, 155-166
7. Forbes, M. W.; Jockusch, R. A. Deactivation Pathways of an Isolated Green Fluorescent Protein Model Chromophore Studied by Electronic Action Spectroscopy J. Am. Chem. Soc. 2009, 131, 17038-17039
8. Bochenkova, A. V.; Kloerke, B.; Rahbek, D. B.; Rajput, J.; Toker, Y.; Andersen, L. H. UV Excited-State Photoresponse of Biochromophore Negative Ions Angew. Chem. 2014, 126, 9955-9959
9. Chingin, K.; Balabin, R. M.; Frankevich, V.; Barylyuk, K.; Nieckarz, R.; Sagulenko, P.; Zenobi, R. Absorption of the Green Fluorescent Protein Chromophore Anion in the Gas Phase Studied by a Combination of FTICR Mass Spectrometry with Laser-induced Photodissociation Spectroscopy Int. J. Mass Spectrom. 2011, 306, 241-245
10. Andersen, L. H.; Lapierre, A.; Nielsen, S. B.; Nielsen, I. B.; Pedersen, S. U.; Pedersen, U. V.; Tomita, S. Chromophores of the Green Fluorescent Protein Studied in the Gas Phase Eur. Phys. J. D 2002, 20, 597-600
11. Lincke, K.; Sølling, T.; Andersen, L. H.; Klaerke, B.; Rahbek, D. B.; Rajput, J.; Oehlenschlaeger, C. B.; Petersen, M. A.; Nielsen, M. B. On the Absorption of the Phenolate Chromophore in the Green Fluorescent Protein-Role of Individual Interactions Chem. Commun. 2010, 46, 734-736
12. Mooney, C. R. S.; Horke, D. A.; Chatterley, A. S.; Simperler, A.; Fielding, H. H.; Verlet, J. R. R. Taking the Green Fluorescence out of the Protein: Dynamics of the Isolated GFP Chromophore Anion Chem. Sci. 2013, 4, 921-927
13. West, C. W.; Hudson, A. S.; Cobb, S. L.; Verlet, J. R. R. Autodetachment versus internal conversion from the S1 state of the isolated GFP chromophore anion J. Chem. Phys. 2013, 139, 071104
14. Toker, Y.; Rahbek, D. B.; Klærke, B.; Bochenkova, A. V.; Andersen, L. H. Direct and Indirect Electron Emission from the Green Fluorescent Protein Chromophore Phys. Rev. Lett. 2012, 109, 128101
15. Bochenkova, A. V.; Andersen, L. H. Photo-initiated Dynamics and Spectroscopy of the Deprotonated Green Fluorescent Protein Chromophore. In Photophysics of Ionic Biochromophores; Nielsen, S. B.; Wyer, J. A., Eds.; Springer: Heidelberg, 2013; pp 67-103.
16. Mooney, C. R. S.; Sanz, M. E.; McKay, A. R.; Fitzmaurice, R. J.; Aliev, A. E.; Caddick, S.; Fielding, H. H. Photodetachment Spectra of Deprotonated Fluorescent Protein Chromophore Anions J. Phys. Chem. A 2012, 116, 7943-7949
17. 1ππ∗ State of the GFP Chromophore Anion J. Chem. Phys. 2014, 140, 205103
18. 0 Continuum J. Phys. Chem. Lett. 2014, 5, 2155-2159
19. Bogdanov, A. M.; Mishin, A. S.; Yampolsky, I. V.; Belousov, V. V.; Chudakov, D. M.; Subach, F. V.; Verkhusha, V. V.; Lukyanov, S.; Lukyanov, K. A. Green Fluorescent Proteins are Light-Induced Electron Donors Nat. Chem. Biol. 2009, 5, 459-461
20. Petrone, A.; Caruso, P.; Tenutaab, S.; Rega, N. On the Optical Absorption of the Anionic GFP Chromophore in Vacuum, Solution, and Protein Phys. Chem. Chem. Phys. 2013, 15, 20536-20544
21. Dong, J.; Solntsev, K. M.; Tolbert, L. M. Solvatochromism of the Green Fluorescence Protein Chromophore and Its Derivatives J. Am. Chem. Soc. 2006, 128, 12038-12039
22. Solntsev, K. M.; Poizat, O.; Dong, J.; Rehault, J.; Lou, Y.; Burda, C.; Tolbert, L. M. Meta and Para Effects in the Ultrafast Excited-State Dynamics of the Green Fluorescent Protein Chromophores J. Phys. Chem. B 2008, 112, 2700-2711
23. Mandal, D.; Tahara, T.; Webber, N. M.; Meech, S. R. Ultrafast Fluorescence of the Chromophore of the Green Fluorescent Protein in Alcohol Solutions Chem. Phys. Lett. 2002, 358, 495-501
24. Litvinenko, K. L.; Webber, N. M.; Meech, S. R. Internal Conversion in the Chromophore of the Green Fluorescent Protein: Temperature Dependence and Isoviscosity Analysis J. Phys. Chem. A 2003, 107, 2616-2623
25. Mandal, D.; Tahara, T.; Meech, S. R. Excited-State Dynamics in the Green Fluorescent Protein Chromophore J. Phys. Chem. B 2004, 108, 1102-1108
26. Vengris, M.; van Stokkum, I. H. M.; He, X.; Bell, A. F.; Tonge, P. T.; van Grondelle, R.; Larsen, D. S. Ultrafast Excited and Ground-State Dynamics of the Green Fluorescent Protein Chromophore in Solution J. Phys. Chem. A 2004, 108, 4587-4598
27. Weber, W.; Helms, V.; McCammon, J. A.; Langhoff, P. W. Shedding Light on the Dark and Weakly Fluorescent States of Green Fluorescent Proteins Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 6177-6182
28. Grigorenko, B. L.; Nemukhin, A. V.; Polyakov, I. V.; Morozov, D. I.; Krylov, A. I. First-Principles Characterization of the Energy Landscape and Optical Spectra of Green Fluorescent Protein along the A→I→B Proton Transfer Route J. Am. Chem. Soc. 2013, 135, 11541-11549
29. Grigorenko, B. L.; Nemukhin, A. V.; Morozov, D. I.; Polyakov, I. V.; Bravaya, K. B.; Krylov, A. I. Toward Molecular-Level Characterization of Photoinduced Decarboxylation of the Green Fluorescent Protein: Accessibility of the Charge-Transfer States J. Chem. Theory Comput. 2012, 8, 1912-1920
30. Martin, M. E.; Negri, F.; Olivucci, M. Origin, Nature, and Fate of the Fluorescent State of the Green Fluorescent Protein Chromophore at the CASPT2//CASSCF Resolution J. Am. Chem. Soc. 2004, 126, 5452-5464
31. Lammich, L.; Petersen, M. A.; Nielsen, M. B.; Andersen, L. H. The Gas-Phase Absorption Spectrum of a Neutral GFP Model Chromophore Biophys. J. 2007, 92, 201-207
32. Rajput, J.; Rahbek, D. B.; Andersen, L. H.; Rocha-Rinza, T.; Christiansen, O.; Bravaya, K. B.; Erokhin, a V; Bochenkova, a V; Solntsev, K. M.; Dong, J. Photoabsorption Studies of Neutral Green Fluorescent Protein Model Chromophores in vacuo Phys. Chem. Chem. Phys. 2009, 11, 9996-10002
33. Topol, I.; Collins, J.; Polyakov, I.; Grigorenko, B.; Nemukhin, A. On Photoabsorption of the Neutral Form of the Green Fluorescent Protein Chromophore Biophys. Chem. 2009, 145, 1-6
34. Filippi, C.; Zaccheddu, M.; Buda, F. Absorption Spectrum of the Green Fluorescent Protein Chromophore: A Difficult Case for ab Initio Methods? J. Chem. Theory Comput. 2009, 5, 2074-2087
35. Polyakov, I. V.; Grigorenko, B. L.; Epifanovsky, E. M.; A.I. Krylov Nemukhin, A. V. Potential Energy Landscape of the Electronic States of the GFP Chromophore in Different Protonation Forms: Electronic Transition Energies and Conical Intersections J. Chem. Theory Comput. 2010, 6, 2377-2387
36. Epifanovsky, E.; Polyakov, I.; Grigorenko, B.; Nemukhin, A.; Krylov, A. I. Quantum Chemical Benchmark Studies of the Electronic Properties of the Green Fluorescent Protein Chromophore. 1. Electronically Excited and Ionized States of the Anionic Chromophore in the Gas Phase J. Chem. Theory Comput. 2009, 5, 1895-1906
37. Becke, A. D. Density-Functional Thermochemistry. III. The Role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
38. Lee, C.; Yang, W.; Parr, R. G. Development of the Colle-Salvetti Correlation-Energy Formula into a Functional of the Electron Density Phys. Rev. B 1988, 37, 785-789
39. Vosko, S. H.; Wilk, L.; Nusair, M. Accurate Spin-Dependent Electron Liquid Correlation Energies for Local Spin Density Calculations: A Critical Analysis Can. J. Phys. 1980, 58, 1200-1211
40. Stephens, P. J.; Devlin, F. J.; Chabalowski, C. F.; Frisch, M. J. Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields J. Phys. Chem. 1994, 98, 11623-11627
41. Krishnan, R.; Binkley, J. S.; Seeger, R.; Pople, J. A. Self-Consistent Molecular Orbital Methods. XX. A Basis Set for Correlated Wave Functions J. Chem. Phys. 1980, 72, 650-654
42. Yanai, T.; Tew, D.; Handy, N. C. A New Hybrid Exchange-Correlation Functional Using the Coulomb-Attenuating Method (CAM-B3LYP) Chem. Phys. Lett. 2004, 393, 51-57
43. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A., Gaussian 09, revision A.1; Gaussian, Inc.: Wallingford, CT, 2009.
44. Calvert, C. R.; Belshaw, L.; Duffy, M. J.; Kelly, O.; King, R. B.; Smyth, A. G.; Kelly, T. J.; Costello, J. T.; Timson, D. J.; Bryan, W. A. LIAD-fs Scheme for Studies of Ultrafast Laser Interactions with Gas Phase Biomolecules Phys. Chem. Chem. Phys. 2012, 14, 6289-6297
45. Duffy, M. J.; Kelly, O.; Calvert, C. R.; King, R. B.; Belshaw, L.; Kelly, T. J.; Costello, J. T.; Timson, D. J.; Bryan, W. A.; Kierspel, T. Fragmentation of Neutral Amino Acids and Small Peptides by Intense, Femtosecond Laser Pulses J. Am. Soc. Mass Spectrom. 2013, 24, 1366-1375
46. Calegari, F.; Ayuso, D.; Trabattoni, A.; Belshaw, L.; De Camillis, S.; Anumula, S.; Frassetto, F.; Poletto, L.; Palacios, A.; Decleva, P. Ultrafast Electron Dynamics in Phenylalanine Initiated by Attosecond Pulses. Science 2014, in press.
47. Bravaya, K. B.; Grigorenko, B. L.; Nemukhin, A. V.; Krylov, A. I. Quantum Chemistry Behind Bioimaging: Insights from Ab Initio Studies of Fluorescent Proteins and Their Chromophores Acc. Chem. Res. 2012, 45, 265-275
48. Paige, J. S.; Wu, K. Y.; Jaffrey, S. R. RNA Mimics of Green Fluorescent Protein Science 2011, 333, 642-646
49. Tao, N. J. Electron Transport in Molecular Junctions Nat. Nantechnol. 2006, 1, 174-181
50. Hales, J. M.; Barlow, S.; Kim, H.; Mukhopadhyay, S.; Brédas, J.-L.; Perry, J. W.; Marder, S. R. Design of Organic Chromophores for All-Optical Signal Processing Applications Chem. Mater. 2014, 26, 549-560