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Annual Review of Physical Chemistry

Volume 74, 2023

Photoacid Dynamics in the Green Fluorescent Protein

Abstract

The photoacid dynamics of fluorescent proteins include both electronic excited- and ground-state mechanisms of proton transfer. The associated characteristic timescales of these reactions range over many orders of magnitude, and the tunneling, barrier crossing, and relevant thermodynamics have in certain cases been linked to coherent nuclear motion. We review the literature and summarize the experiments and theory that demonstrate proton tunneling in the electronic ground state of the green fluorescent protein (GFP). We also discuss the excited-state proton-transfer reaction of GFP that takes place on the picosecond timescale. Although this reaction has been investigated using several vibrational spectroscopic methods, the interpretation remains unsettled. We discuss recent advances as well as remaining questions, in particular those related to the vibrational mode couplings that involve low-frequency modulations of chromophore vibrations on the timescale of proton transfer.

Keyword(s): coherence, fluorescence, GFP, green fluorescent protein, proton tunneling, stimulated Raman spectroscopy, ultrafast spectroscopy
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2023-04-24
2024-05-03
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Literature Cited

  1. 1.
    Tsien RY. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509–44
     [Google Scholar]
  2. 2.
    van Thor JJ, Sage JT. 2006. Charge transfer in green fluorescent protein. Photochem. Photobiol. Sci. 5:597–602
     [Google Scholar]
  3. 3.
    van Thor JJ. 2009. Photoreactions and dynamics of the green fluorescent protein. Chem. Soc. Rev. 38:2935–50
     [Google Scholar]
  4. 4.
    Acharya A, Bogdanov AM, Grigorenko BL, Bravaya KB, Nemukhin AV et al. 2017. Photoinduced chemistry in fluorescent proteins: curse or blessing?. Chem. Rev. 117:758–95
     [Google Scholar]
  5. 5.
    Zimmer M. 2002. Green fluorescent protein (GFP): applications, structure, and related photophysical behavior. Chem. Rev. 102:759–81
     [Google Scholar]
  6. 6.
    Meech SR. 2009. Excited state reactions in fluorescent proteins. Chem. Soc. Rev. 38:2922–34
     [Google Scholar]
  7. 7.
    Seward HE, Bagshaw CR. 2009. The photochemistry of fluorescent proteins: implications for their biological applications. Chem. Soc. Rev. 38:2842–51
     [Google Scholar]
  8. 8.
    Zhou XX, Chung HK, Lam AJ, Lin MZ. 2012. Optical control of protein activity by fluorescent protein domains. Science 338:810–14
     [Google Scholar]
  9. 9.
    Wachter RM, Remington SJ. 1999. Sensitivity of the yellow variant of green fluorescent protein to halides and nitrate. Curr. Biol. 9:R628–29
     [Google Scholar]
  10. 10.
    van Thor JJ, Gensch T, Hellingwerf KJ, Johnson LN. 2002. Phototransformation of green fluorescent protein with UV and visible light leads to decarboxylation of glutamate 222. Nat. Struct. Biol. 9:37–41
     [Google Scholar]
  11. 11.
    Wiedenmann J, Ivanchenko S, Oswald F, Schmitt F, Röcker C et al. 2004. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. PNAS 101:15905–10
     [Google Scholar]
  12. 12.
    Fare C, Yuan L, Cordon-Preciado V, Michels JJ, Bearpark MJ et al. 2020. Radical-triggered reaction mechanism of the green-to-red photoconversion of EosFP. J. Phys. Chem. B 124:7765–78
     [Google Scholar]
  13. 13.
    Copeland RA, Chan SI. 1989. Proton translocation in proteins. Annu. Rev. Phys. Chem. 40:671–98
     [Google Scholar]
  14. 14.
    Saraste M. 1999. Oxidative phosphorylation at the fin de siècle. Science 283:1488–93
     [Google Scholar]
  15. 15.
    Luecke H, Richter HT, Lanyi JK. 1998. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science 280:1934–37
     [Google Scholar]
  16. 16.
    DeCoursey TE. 2003. Voltage-gated proton channels and other proton transfer pathways. Physiol. Rev. 83:475–579
     [Google Scholar]
  17. 17.
    Belevich I, Verkhovsky MI, Wikstrom M. 2006. Proton-coupled electron transfer drives the proton pump of cytochrome c oxidase. Nature 440:829–32
     [Google Scholar]
  18. 18.
    Wraight CA. 2006. Chance and design—proton transfer in water, channels and bioenergetic proteins. Biochim. Biophys. Acta Bioenerg. 1757:886–912
     [Google Scholar]
  19. 19.
    Nagle JF, Morowitz HJ. 1978. Molecular mechanisms for proton transport in membranes. PNAS 75:298–302
     [Google Scholar]
  20. 20.
    Kohen A, Cannio R, Bartolucci S, Klinman JP. 1999. Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399:496–99
     [Google Scholar]
  21. 21.
    Masgrau L, Roujeinikova A, Johannissen LO, Hothi P, Basran J et al. 2006. Atomic description of an enzyme reaction dominated by proton tunneling. Science 312:237–41
     [Google Scholar]
  22. 22.
    Bhabha G, Lee J, Ekiert DC, Gam J, Wilson IA et al. 2011. A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332:234–38
     [Google Scholar]
  23. 23.
    Knapp MJ, Rickert K, Klinman JP. 2002. Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124:3865–74
     [Google Scholar]
  24. 24.
    Klinman JP, Kohen A. 2013. Hydrogen tunneling links protein dynamics to enzyme catalysis. Annu. Rev. Biochem. 82:471–96
     [Google Scholar]
  25. 25.
    Garczarek F, Gerwert K. 2006. Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439:109–12
     [Google Scholar]
  26. 26.
    Salna B, Benabbas A, Russo D, Champion PM. 2017. Tunneling kinetics and nonadiabatic proton-coupled electron transfer in proteins: the effect of electric fields and anharmonic donor-acceptor interactions. J. Phys. Chem. B 121:6869–81
     [Google Scholar]
  27. 27.
    Kuznetsov AM, Ulstrup J. 1999. Proton and hydrogen atom tunnelling in hydrolytic and redox enzyme catalysis. Can. J. Chem. 77:1085–96
     [Google Scholar]
  28. 28.
    Hammes-Schiffer S, Stuchebrukhov AA. 2010. Theory of coupled electron and proton transfer reactions. Chem. Rev. 110:6939–60
     [Google Scholar]
  29. 29.
    Antoniou D, Schwartz SD. 1997. Large kinetic isotope effects in enzymatic proton transfer and the role of substrate oscillations. PNAS 94:12360–65
     [Google Scholar]
  30. 30.
    Pu J, Gao J, Truhlar DG. 2006. Multidimensional tunneling, recrossing, and the transmission coefficient for enzymatic reactions. Chem. Rev. 106:3140–69
     [Google Scholar]
  31. 31.
    Cui Q, Karplus M. 2002. Promoting modes and demoting modes in enzyme-catalyzed proton transfer reactions: a study of models and realistic systems. J. Phys. Chem. B 106:7927–47
     [Google Scholar]
  32. 32.
    Kiefer PM, Hynes JT. 2010. Theoretical aspects of tunneling proton transfer reactions in a polar environment. J. Phys. Org. Chem. 23:632–46
     [Google Scholar]
  33. 33.
    Benabbas A, Salna B, Sage JT, Champion PM. 2015. Deep proton tunneling in the electronically adiabatic and non-adiabatic limits: comparison of the quantum and classical treatment of donor-acceptor motion in a protein environment. J. Chem. Phys. 142:114101
     [Google Scholar]
  34. 34.
    Champion PM, Benabbas A 2020. Proton tunneling and proton-coupled electron transfer in biological systems: theory and experimental analysis. Tunneling in Molecules J Kästner, S Kozuch 88–145. Theor. Comput. Chem Ser. No. 18 Cambridge, UK: R. Soc. Chem.
     [Google Scholar]
  35. 35.
    Wikstrom M, Sharma V, Kaila VRI, Hosler JP, Hummer G. 2015. New perspectives on proton pumping in cellular respiration. Chem. Rev. 115:2196–221
     [Google Scholar]
  36. 36.
    Zhu J, Han H, Pawate A, Gennis RB. 2010. Decoupling mutations in the D-channel of the aa3-type cytochrome c oxidase from Rhodobacter sphaeroides suggest that a continuous hydrogen-bonded chain of waters is essential for proton pumping. Biochemistry 49:4476–82
     [Google Scholar]
  37. 37.
    Nagano S, Poulos TL. 2005. Crystallographic study on the dioxygen complex of wild-type and mutant cytochrome P450cam – implications for the dioxygen activation mechanism. J. Biol. Chem. 280:31659–63
     [Google Scholar]
  38. 38.
    Braun-Sand S, Strajbl M, Warshel A. 2004. Studies of proton translocations in biological systems: simulating proton transport in carbonic anhydrase by EVB-based models. Biophys. J. 87:2221–39
     [Google Scholar]
  39. 39.
    Okamura MY, Paddock ML, Graige MS, Feher G. 2000. Proton and electron transfer in bacterial reaction centers. Biochim. Biophys. Acta Bioenerg. 1458:148–63
     [Google Scholar]
  40. 40.
    Okamura MY, Feher G. 1992. Proton-transfer in reaction centers from photosynthetic bacteria. Annu. Rev. Biochem. 61:861–96
     [Google Scholar]
  41. 41.
    Höhner R, Aboukila A, Kunz H-H, Venema K. 2016. Proton gradients and proton-dependent transport processes in the chloroplast. Front. Plant Sci. 7:218
     [Google Scholar]
  42. 42.
    Goyal P, Yang S, Cui Q 2015. Microscopic basis for kinetic gating in cytochrome c oxidase: insights from QM/MM analysis. Chem. Sci. 6:826–41
     [Google Scholar]
  43. 43.
    Salna B, Benabbas A, Sage JT, van Thor J, Champion PM. 2016. Wide-dynamic-range kinetic investigations of deep proton tunnelling in proteins. Nat. Chem. 8:874–80
     [Google Scholar]
  44. 44.
    Kiefer PM, Hynes JT. 2004. Kinetic isotope effects for nonadiabatic proton transfer reactions in a polar environment. 1. Interpretation of tunneling kinetic isotopic effects. J. Phys. Chem. A 108:11793–808
     [Google Scholar]
  45. 45.
    Hammes-Schiffer S, Soudackov AV. 2008. Proton-coupled electron transfer in solution, proteins, and electrochemistry. J. Phys. Chem. B 112:14108–23
     [Google Scholar]
  46. 46.
    Truhlar DG. 2010. Tunneling in enzymatic and nonenzymatic hydrogen transfer reactions. J. Phys. Org. Chem. 23:660–76
     [Google Scholar]
  47. 47.
    Chattoraj M, King BA, Bublitz GU, Boxer SG. 1996. Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. PNAS 93:8362–67
     [Google Scholar]
  48. 48.
    Förster T. 1950. Elektrolytische Dissoziation angeregter Moleküle [Electrolytic dissociation of excited molecules. ]. Z. Elektrochem. Angew. Phys. 54:42–46
     [Google Scholar]
  49. 49.
    Taylor CA, El-Bayoumi MA, Kasha M 1969. Excited-state two-proton tautomerism in hydrogen-bonded N-heterocyclic base pairs. PNAS 63:253
     [Google Scholar]
  50. 50.
    Kennis JTM, Larsen DS, van Stokkum IHM, Vengris M, van Thor JJ, van Grondelle R. 2004. Uncovering the hidden ground state of green fluorescent protein. PNAS 101:17988–93
     [Google Scholar]
  51. 51.
    Yang F, Moss LG, Phillips GN. 1996. The molecular structure of green fluorescent protein. Nat. Biotechnol. 14:1246–51
     [Google Scholar]
  52. 52.
    Scharnagl C, Raupp-Kossmann R, Fischer SF. 1999. Molecular basis for pH sensitivity and proton transfer in green fluorescent protein: protonation and conformational substates from electrostatic calculations. Biophys. J. 77:1839–57
     [Google Scholar]
  53. 53.
    Kasha M. 1986. Proton-transfer spectroscopy: perturbation of the tautomerization potential. J. Chem. Soc. Faraday Trans. 82:2379–92
     [Google Scholar]
  54. 54.
    Stoner-Ma D, Jaye AA, Matousek P, Towrie M, Meech SR, Tonge PJ. 2005. Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy. J. Am. Chem. Soc. 127:2864–65
     [Google Scholar]
  55. 55.
    van Thor JJ, Georgiev GY, Towrie M, Sage JT. 2005. Ultrafast and low barrier motions in the photoreactions of the green fluorescent protein. J. Biol. Chem. 280:33652–59
     [Google Scholar]
  56. 56.
    van Thor JJ, Zanetti G, Ronayne KL, Towrie M. 2005. Structural events in the photocycle of green fluorescent protein. J. Phys. Chem. B 109:16099–108
     [Google Scholar]
  57. 57.
    Di Donato M, van Wilderen L, Van Stokkum IHM, Stuart TC, Kennis JTM et al. 2011. Proton transfer events in GFP. Phys. Chem. Chem. Phys. 13:16295–305
     [Google Scholar]
  58. 58.
    van Thor JJ, Ronayne KL, Towrie M, Sage JT. 2008. Balance between ultrafast parallel reactions in the green fluorescent protein has a structural origin. Biophys. J. 95:1902–12
     [Google Scholar]
  59. 59.
    Stoner-Ma D, Melief EH, Nappa J, Ronayne KL, Tonge PJ, Meech SR. 2006. Proton relay reaction in green fluorescent protein (GFP): polarization-resolved ultrafast vibrational spectroscopy of isotopically edited GFP. J. Phys. Chem. B 110:22009–18
     [Google Scholar]
  60. 60.
    Fang C, Frontiera RR, Tran R, Mathies RA 2009. Mapping GFP structure evolution during proton transfer with femtosecond Raman spectroscopy. Nature 462:200–4
     [Google Scholar]
  61. 61.
    Kukura P, McCamant DW, Mathies RA. 2007. Femtosecond stimulated Raman spectroscopy. Annu. Rev. Phys. Chem. 58:461–88
     [Google Scholar]
  62. 62.
    Schellenberg P, Johnson E, Esposito AP, Reid PJ, Parson WW 2001. Resonance Raman scattering by the green fluorescent protein and an analogue of its chromophore. J. Phys. Chem. B 105:5316–22
     [Google Scholar]
  63. 63.
    Esposito AP, Schellenberg P, Parson WW, Reid PJ. 2001. Vibrational spectroscopy and mode assignments for an analog of the green fluorescent protein chromophore. J. Mol. Struct. 569:25–41
     [Google Scholar]
  64. 64.
    He X, Bell AF, Tonge PJ. 2002. Isotopic labeling and normal-mode analysis of a model green fluorescent protein chromophore. J. Phys. Chem. B 106:6056–66
     [Google Scholar]
  65. 65.
    Fujisawa T, Kuramochi H, Hosoi H, Takeuchi S, Tahara T. 2016. Role of coherent low-frequency motion in excited-state proton transfer of green fluorescent protein studied by time-resolved impulsive stimulated Raman spectroscopy. J. Am. Chem. Soc. 138:3942–45
     [Google Scholar]
  66. 66.
    Kuramochi H, Tahara T. 2021. Tracking ultrafast structural dynamics by time-domain Raman spectroscopy. J. Am. Chem. Soc. 143:9699–717
     [Google Scholar]
  67. 67.
    Fumero G, Schnedermann C, Batignani G, Wende T, Liebel M et al. 2020. Two-dimensional impulsively stimulated resonant Raman spectroscopy of molecular excited states. Phys. Rev. X 10:011051
     [Google Scholar]
  68. 68.
    Winkler K, Lindner JR, Subramaniam V, Jovin TM, Vohringer P. 2002. Ultrafast dynamics in the excited state of green fluorescent protein (wt) studied by frequency-resolved femtosecond pump-probe spectroscopy. Phys. Chem. Chem. Phys. 4:1072–81
     [Google Scholar]
  69. 69.
    Wilson KC, Lyons B, Mehlenbacher R, Sabatini R, McCamant DW. 2009. Two-dimensional femtosecond stimulated Raman spectroscopy: observation of cascading Raman signals in acetonitrile. J. Chem. Phys. 131:214502
     [Google Scholar]
  70. 70.
    Morikis D, Li P, Bangcharoenpaurpong O, Sage JT, Champion PM. 1991. Resonance Raman scattering as a probe of electron-nuclear coupling: applications to heme proteins. J. Phys. Chem. 95:3391–98
     [Google Scholar]
  71. 71.
    Champion PM, Albrecht AC. 1981. On the modeling of absorption band shapes and resonance Raman excitation profiles. Chem. Phys. Lett. 82:410–13
     [Google Scholar]
  72. 72.
    Kumar ATN, Rosca F, Widom A, Champion PM. 2001. Investigations of amplitude and phase excitation profiles in femtosecond coherence spectroscopy. J. Chem. Phys. 114:701–24
     [Google Scholar]
  73. 73.
    Kumar ATN, Rosca F, Widom A, Champion PM. 2001. Investigations of ultrafast nuclear response induced by resonant and nonresonant laser pulses. J. Chem. Phys. 114:6795–815
     [Google Scholar]
  74. 74.
    Kubo M, Gruia F, Benabbas A, Barabanschikov A, Montfort WR et al. 2008. Low-frequency mode activity of heme: femtosecond coherence spectroscopy of iron porphine halides and nitrophorin. J. Am. Chem. Soc. 130:9800–11
     [Google Scholar]
  75. 75.
    Mukamel S, Piryatinski A, Chernyak V. 1999. Two-dimensional Raman echoes: femtosecond view of molecular structure and vibrational coherence. Acc. Chem. Res. 32:145–54
     [Google Scholar]
  76. 76.
    Hamm P, Lim M, Hochstrasser RM. 1998. Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy. J. Phys. Chem. B 102:6123–38
     [Google Scholar]
  77. 77.
    Garg A, Onuchic JN, Ambegaokar V. 1985. Effect of friction on electron transfer in biomolecules. J. Chem. Phys. 83:4491–503
     [Google Scholar]
  78. 78.
    Liang KK, Mebel AM, Lin SH, Hayashi M, Selzle HL et al. 2003. Influence of distortion and Duschinsky effects on Marcus-type theories of electron transfer rate. Phys. Chem. Chem. Phys. 5:4656–65
     [Google Scholar]
  79. 79.
    Sando GM, Spears KG, Hupp JT, Ruhoff PT. 2001. Large electron transfer rate effects from the Duschinsky mixing of vibrations. J. Phys. Chem. A 105:5317–25
     [Google Scholar]
  80. 80.
    Tang J, Lee MT, Lin SH. 2003. Effects of the Duschinsky mode-mixing mechanism on temperature dependence of electron transfer processes. J. Chem. Phys. 119:7188–96
     [Google Scholar]
  81. 81.
    Srajer V, Reinisch L, Champion PM. 1988. Protein fluctuations, distributed coupling, and the binding of ligands to heme proteins. J. Am. Chem. Soc. 110:6656–70
     [Google Scholar]
  82. 82.
    Rosca F, Kumar ATN, Ionascu D, Ye X, Demidov AA et al. 2002. Investigations of anharmonic low-frequency oscillations in heme proteins. J. Phys. Chem. A 106:3540–52
     [Google Scholar]
  83. 83.
    Ionascu D, Rosca F, Gruia F, Yu A, Champion PM. 2006. Optical scanning instrument for ultrafast pump-probe spectroscopy of biomolecules at cryogenic temperatures. Rev. Sci. Instrum. 77:064303
     [Google Scholar]
  84. 84.
    Rosca F, Kumar ATN, Ionascu D, Sjodin T, Demidov AA, Champion PM. 2001. Wavelength selective modulation in femtosecond pump-probe spectroscopy and its application to heme proteins. J. Chem. Phys. 114:10884–98
     [Google Scholar]
  85. 85.
    Salna B. 2017. Proton transport in proteins and the role of quantum tunneling PhD Thesis Northeast. Univ. Boston:
  86. 86.
    Jentzen W, Song XZ, Shelnutt JA. 1997. Structural characterization of synthetic and protein-bound porphyrins in terms of the lowest-frequency normal coordinates of the macrocycle. J. Phys. Chem. B 101:1684–99
     [Google Scholar]
  87. 87.
    Leiderman P, Gepshtein R, Tsimberov I, Huppert D. 2008. Effect of temperature on excited-state proton tunneling in wt-green fluorescent protein. J. Phys. Chem. B 112:1232–39
     [Google Scholar]
  88. 88.
    Yu AC, Ye X, Ionascu D, Cao WX, Champion PM. 2005. Two-color pump-probe laser spectroscopy instrument with picosecond time-resolved electronic delay and extended scan range. Rev. Sci. Instrum. 76:114301–8
     [Google Scholar]
  89. 89.
    Roston D, Islam Z, Kohen A. 2013. Isotope effects as probes for enzyme catalyzed hydrogen-transfer reactions. Molecules 18:5543–67
     [Google Scholar]
  90. 90.
    Nesheim JC, Lipscomb JD. 1996. Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C-H bond cleavage in a reaction cycle intermediate. Biochemistry 35:10240–47
     [Google Scholar]
  91. 91.
    Klinman JP, Offenbacher AR. 2018. Understanding biological hydrogen transfer through the lens of temperature dependent kinetic isotope effects. Acc. Chem. Res. 51:1966–74
     [Google Scholar]
  92. 92.
    Hanoian P, Liu CT, Hammes-Schiffer S, Benkovic S. 2015. Perspectives on electrostatics and conformational motions in enzyme catalysis. Acc. Chem. Res. 48:482–89
     [Google Scholar]
  93. 93.
    Hu S, Soudackov AV, Hammes-Schiffer S, Klinman JP. 2017. Enhanced rigidification within a double mutant of soybean lipoxygenase provides experimental support for vibronically nonadiabatic proton-coupled electron transfer models. ACS Catalysis 7:3569–74
     [Google Scholar]
  94. 94.
    Thompson LM, Lasoroski A, Champion PM, Sage JT, Frisch MJ et al. 2014. Analytical harmonic vibrational frequencies for the green fluorescent protein computed with ONIOM: chromophore mode character and its response to environment. J. Chem. Theory Comput. 10:751–66
     [Google Scholar]
  95. 95.
    Edwards SJ, Soudackov AV, Hammes-Schiffer S. 2009. Analysis of kinetic isotope effects for proton-coupled electron transfer reactions. J. Phys. Chem. A 113:2117–26
     [Google Scholar]
  96. 96.
    Novak A. 1974. Hydrogen bonding in solids. Correlation of spectroscopic and crystallographic data. Struct. Bond. 18:177–216
     [Google Scholar]
  97. 97.
    Ginovska-Pangovska B, Ho MH, Linehan JC, Cheng YH, Dupuis M et al. 2014. Molecular dynamics study of the proposed proton transport pathways in [FeFe]-hydrogenase. Biochim. Biophys. Acta Bioenerg. 1837:131–38
     [Google Scholar]
  98. 98.
    Saito K, Rutherford AW, Ishikita H. 2013. Mechanism of proton-coupled quinone reduction in Photosystem II. PNAS 110:954–59
     [Google Scholar]
  99. 99.
    Pisliakov AV, Sharma PK, Chu ZT, Haranczyk M, Warshel A. 2008. Electrostatic basis for the unidirectionality of the primary proton transfer in cytochrome c oxidase. PNAS 105:7726–31
     [Google Scholar]
  100. 100.
    Xu J, Voth GA. 2005. Computer simulation of explicit proton translocation in cytochrome c oxidase: the D-pathway. PNAS 102:6795–800
     [Google Scholar]
  101. 101.
    Shinobu A, Agmon N. 2017. Proton wire dynamics in the green fluorescent protein. J. Chem. Theory Comput. 13:353–69
     [Google Scholar]
  102. 102.
    Wise F, Rosker M, Millhauser G, Tang C. 1987. Application of linear prediction least-squares fitting to time-resolved optical spectroscopy. IEEE J. Quant. Electron. 23:1116–21
     [Google Scholar]
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Photoacid Dynamics in the Green Fluorescent Protein
Annual Review of Physical Chemistry 74, 123 (2023); https://doi.org/10.1146/annurev-physchem-091422-102619
/content/journals/10.1146/annurev-physchem-091422-102619
/content/journals/10.1146/annurev-physchem-091422-102619
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