Computational studies of the luciferase light-emitting product: Oxyluciferin

Journal of Chemical Theory and Computation

Volumn 7, Issue 4, 2011, Pages 809-817

  Da Silva, Luís Pinto ^a   Esteves Da Silva, Joaquim C G ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79954521515     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct200003u     Document Type: Review

References (89)

1. Marques, S. M.; Esteves da Silva, J. C. G. Firefly bioluminescence. A mechanistic approach of luciferase catalyzed reactions IUBMB Life 2009, 61, 6-17
2. Leita̧o, J. M. M.; Esteves da Silva, J. C. G. Firefly luciferase inhibition J. Photochem. Photobiol. B 2010, 101, 1-8
3. Inouye, S. Firefly luciferase: an adenylate-forming enzyme for multicatalytic functions Cell. Mol. Life Sci. 2010, 67, 387-404
4. Ugarova, N. N. Interactions of firefly luciferase with substracts and their analogues: a study using fluorescence spectroscopy methods Photochem. Photobiol. Sci. 2008, 7, 218-227 (Pubitemid 351248629)
5. Meroni, G.; Rajabi, M.; Santaniello, E. d -luciferin, derivatives and analogues: synthesis and in vitro/in vivo luciferase-catalysed bioluminescence activity ARKIVOC 2009, 265-288
6. Luker, K. E.; Luker, G. D. Applications of bioluminescence imaging to antiviral research and therapy: multiple luciferase enzymes and quantitation Antiviral Res. 2008, 78, 179-187
7. Fan, F.; Wood, K. V. Bioluminescence assays for high-throughput screening Assay Drug Dev. Technol. 2007, 5, 127-136
8. Seliger, H. H.; McElroy, W. D. Spectral emission and quantum yield of firefly bioluminescence Arch. Biochem. Biophys. 1960, 88, 136-141
9. Seliger, H. H.; McElroy, W. D. Colors of firefly bioluminescence - enzyme configuration + species specificity Proc. Natl. Acad. Sci. U.S.A. 1964, 52, 75-81
10. Ando, Y.; Niwa, K.; Yamada, N.; Enomoto, T.; Irie, T.; Kubota, H.; Ohmiya, Y.; Akiyama, H.. Firefly bioluminescence quantum yield and colour change by pH-sensitive green-emission Nat. Photonics 2008, 2, 44-47
11. Fraga, H. Firefly luminescence. A historical perspective and recent developments Photochem. Photobiol. Sci. 2008, 7, 218-227
12. Wood, K. V. The chemical mechanism and evolutionary development of beetle bioluminescence Photochem. Photobiol. 1995, 62, 662-673
13. Hastings, J. W. Chemistries and colors of bioluminescent reactions: A review Gene 1996, 173, 5-11 (Pubitemid 26239673)
14. Seliger, H. H.; Buck, J. B.; Fastie, W. G.; McElroy, W. D. Spectral distribution of firefly light J. Gen. Physiol. 1964, 48, 95-104
15. Lee, R. T.; Denburg, J. L.; McElroy, W. D. Substrate-binding properties of firefly luciferase 0.2. ATP-binding site Arch. Biochem. Biophys. 1970, 141, 38-52
16. Lundovskikh, I.; Dementieva, E.; Ugarova, N. Recombinant firefly luciferase in Escherichia coli - Properties and immobilization Appl. Biochem. Biotechnol. 2000, 88, 127-136
17. Viviani, V. R.; Arnoldi, F. G. C.; Neto, A. J. S.; Oehlmeyer, T. L.; Bechara, E. J. H.; Ohmiya, Y. The structural origin and biological function of pH-sensitivity in firefly luciferases Photochem. Photobiol. Sci. 2008, 7, 159-169 (Pubitemid 351248639)
18. White, E. H.; Rapaport, E.; Seliger, H. H.; Hopkins, T. A. The chemi- and bioluminescence of firefly luciferin: An efficient chemical production of electronically excited states Bioorg. Chem. 1971, 1, 92-122
19. Branchini, B. R.; Murtiashaw, M. H.; Magyar, R. A.; Portier, N. C.; Ruggiero, M. C.; Stroh, J. G. Yellow-green and Red Firefly Bioluminescence from 5, 5-Dimethyloxylucierin J. Am. Chem. Soc. 2002, 124, 2112-2113 (Pubitemid 34267086)
20. McCapra, F.; Gilfoyle, D. J.; Young, D. W.; Church, N. J.; Spencer, P. In Bioluminescence and Chemiluminescence: Fundamental and Applied Aspects; Campbell, A. K.; Kricka, L. J.; Stanley, P. E., Ed.; Wiley: New York, 1994; pp 387 - 391.
21. Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F. AM1: A New General Purpose Quantum Mechanical Molecular Model J. Am. Chem. Soc. 1985, 107, 3902-3909
22. Morton, R. A.; Hopkins, T. A.; Seliger, H. H. Spectroscopic properties of firefly luciferin and related compounds, and approach to product emission Biochemistry 1969, 8, 1598-1607
23. DeLuca, M. Hydrophobic nature of active site of firefly luciferase Biochemistry 1969, 8, 160-166
24. Branchini, B. R.; Southworth, T. L.; Murtiashow, M. H.; Magyar, R. A.; Gonzalez, S. A.; Ruggiero, M. C.; Stroh, J. G. An Alternative Mechanism of Bioluminescence Color Determination in Firefly Luciferase Biochemistry 2004, 43, 7255-7262 (Pubitemid 38745746)
25. Nakatsu, T.; Ichiyama, Y.; Hiratake, J.; Saldanha, A.; Kobashi, N.; Sakata, K.; Kato, H. Structural basis for the spectral difference in luciferase bioluminescence Nature 2006, 440, 372-376
26. Hirano, T.; Hasumi, Y.; Ohtsuka, K.; Maki, S.; Niwa, H.; Yamaji, M.; Hashizume, D. Spectroscopic Studies of the light-Color Modulation Mechanism of Firefly (beetle) Bioluminescence J. Am. Chem. Soc. 2009, 131, 2385-2396
27. Naumov, P.; Ozawa, Y.; Ohkubo, K.; Fukuzumi, S. Structure and Spectroscopy of Oxyluciferin, the Light Emitter of the firefly bioluminescence J. Am. Chem. Soc. 2009, 131, 11590-11605
28. Suzuki, N.; Sato, M.; Okada, K.; Goto, T. Studies of firefly bioluminescence 0.1. Synthesis and spectral properties of firefly oxyluciferin; a possible emitting species in firefly bioluminescence Tetrahedron 1972, 28, 4065-4074
29. White, E. H.; Roswell, D. F. Analogs and derivatives of firefly oxyluciferin, the light emitter in firefly bioluminescence Photochem. Photobiol. 1991, 53, 131-136
30. Leont'eva, O. V.; Vlasova, T. N.; Ugarova, N. N. Dimethyl- and monomethyloxyluciferins as analogs of the product of the bioluminescence reaction catalyzed by firefly luciferase Biochemistry (Moscow) 2006, 71, 51-55 (Pubitemid 43333802)
31. Vlasova, T. N.; Leontieva, O. V.; Ugarova, N. N. Interaction of dimethyl-and monomethyloxyluciferin with recombinant wild-type and mutant firefly luciferases Biochemistry (Moscow) 2006, 71, 555-559 (Pubitemid 43814019)
32. Naumov, P.; Kochunnoonny, M. Spectral-Structural Effects of the Keto-Enol-Enolate and Phenol-Phenolate Equilibria of Oxyluciferin J. Am. Chem. Soc. 2010, 132, 11566-11579
33. White, E. H.; Rapaport, E.; Hopkins, T. A.; Seliger, H. H. Chemi- and bioluminescence of firefly luciferin J. Am. Chem. Soc. 1969, 91, 2178-2180
34. White, E. H.; Steinmetz, M. G.; Miano, J. D.; Wildes, P. D.; Morland, R. Chemi-luminescence and bioluminescence of firefly luciferase J. Am. Chem. Soc. 1980, 102, 3199-3208
35. Jensen, F. In Introduction to Computational Chemistry; Wiley: New York, 1999; p 89.
36. Cramer, C. J. In Essentials of Computational Chemistry. Theories and Models; Wiley: New York, 2002; p 139.
37. Orlova, G.; Goddard, J. D.; Brovko, L. Y. Theoretical Study of the Amazing Firefly Bioluminescence: The Formation and Structures of the Light Emitters J. Am. Chem. Soc. 2003, 125, 6962-6971 (Pubitemid 36682795)
38. Foresman, J. B.; Head-Gordon, J. A.; Frisch, M. J. Towards a systematic molecular-orbital theory for excited-states J. Phys. Chem. 1992, 96, 135-49
39. Becke, A. D. Density-Functional Thermochemistry 0.3. The role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
40. Hehre, W. J.; Ditchfiels, R.; Pople, J. A. Self-Consistent Molecular Orbital Methods. XII: Further Extensions of Gaussian-Type Basis Sets for Use in Molecular Orbital Studies of Organic Molecules J. Chem. Phys. 1972, 56, 2257-2261
41. Branchini, B. R.; Magyar, R. A.; Murtiashaw, M. H.; Anderson, S. M.; Zimmer, M. Site-directed mutagenesis of histidine 245 in firefly luciferase: A proposed model of the active site Biochemistry 1998, 37, 15311-15319 (Pubitemid 28515991)
42. Sandalova, T. P.; Ugarova, N. N. Model of the active site of firefly luciferase Biochemistry (Moscow) 1999, 64, 962-967 (Pubitemid 129580154)
43. Liu, Y.-J.; De Vico, L.; Lindh, R. Ab initio investigation on the chemical origin of the firefly bioluminescence. J Photochem. Photobiol. A 2008, 194, 261-267
44. Gross, E. K. U.; Kohn, W. Time-Dependent Density-Functional Theory Adv. Quantum Chem. 1990, 21, 255-291
45. Casida, M. E. In Recent Advances in Density Functional Methods; Chong, D. P., Ed.; World Scientific: Singapore, 1995;, p 155.
46. Zerner, M. C. In Reviews of Computational Chemistry; Lipkowitz, K. B.; Boyd, D. B., Ed.; VCH: New York, 1991.
47. De Mello, P. C.; Hehenberger, M.; Zernert, M. C. Converging SCF calculations on excited states J. Quantum Chem. 1982, 21, 251-258
48. Burcl, R.; Amos, R. D.; Handy, N. C. Study of excited states of furan and pyrrole by time-dependent density functional theory Chem. Phys. Lett. 2002, 355, 8-18
49. Gross, L. A.; Baird, G. S.; Hoffman, R. C.; Baldridge, K. K.; Tsien, R. Y. The structure of the chromophore within DsRed, a red fluorescent protein from coral Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 11990-11995
50. Ugarova, N. N.; Brovko, L. Y. Protein structure and bioluminescent spectra for firefly bioluminescence Luminescence 2002, 17, 321-330 (Pubitemid 135694429)
51. Ren, A.-M.; Goddard, J. D. Predictions of the electronic absorption and emission spectra of luciferin and oxyluciferins including solvation effects J. Photochem. Photobiol. B 2005, 81, 163-170 (Pubitemid 41722588)
52. Foresman, J. B.; Keith, T. A.; Wiberg, K. B.; Snoonian, J.; Frisch, M. J. Solvent effects 0.5. Influence of cavity shape; truncation of electrostatics; and electron correlation ab initio reaction field calculations J. Phys. Chem. 1996, 100, 16098-16104 (Pubitemid 126799346)
53. Yang, T.; Goddard, J. D. Predictions of the Geometries and Fluorescence Emission Energies of Oxyluciferin J. Phys. Chem. A 2007, 111, 4489-4497 (Pubitemid 46915337)
54. Andersson, K.; Malmqvist, P. A.; Roos, B. O.; Sadlej, A. J.; Wolinski, K. Second-order perturbation theory with a CASSCF reference function J. Phys. Chem. 1990, 94, 5483-5488
55. Andersson, K.; Malmqvist, P. A.; Roos, B. O. Second.order perturbation theory with a complete active space self-consistent field reference function J. Chem. Phys. 1992, 96, 1218-1226
56. Hariharan, P. C.; Pople, J. A. The influence of polarization functions on molecular orbital hydrogenation Theor. Chim. Acta 1973, 28, 213-222
57. Nakatani, N.; Hasegawa, J.-Y.; Nakatsuji, H. Red Light in Chemiluminescence and Yellow-Green Light in Bioluminescence: Color-Tuning Mechanism of Firefly; Photinus pyralis: Studied by the Symmetry-Adapted Cluster-Configuration Interaction Method J. Am. Chem. Soc. 2007, 129, 8756-8765 (Pubitemid 47492063)
58. Nakatsuji, H.; Hirao, K. Cluster expansion of the wavefunction. Symmetry-adapted-cluster expansion; its variational determination; and extension of open-shell orbital theory J. Chem. Phys. 1978, 68, 2053-2066
59. Nakatsuji, H. In Computational Chemistry; Reviews of current Trends; Leszczynski, J., Ed.; World Scientific: Singapore, 1996; p 62.
60. Dreuw, A.; Weisman, J. L.; Head-Gordon, M. Long-range charge-transfer excited states in time-dependent density functional theory require non-local exchange J. Chem. Phys. 2003, 119, 2943-2947
61. Fujimoto, K.; Hayashi, S.; Hasegawa, J.-Y.; Nakatsuji, H. Theoretical Studies on the Color-Tuning Mechanism in Retinal Proteins J. Chem. Theory Comput. 2007, 3, 605-618
62. Barone, V.; Cossi, M.; Tomasi, J. A new definition of cavities for the computation of solvation free energies by the polarizable continuum model J. Chem. Phys. 1997, 107, 3210-3222
63. Li, Z.-W.; Ren, A.-M.; Guo, J.-F.; Yang, T.; Goddard, J. D.; Feng, J.-K. Color-Tuning Mechanism in Firefly Luminescence: Theoretical Studies on Fluorescence of Oxyluciferin in Aqueous Solution Using Time Dependent Density Functional Theory J. Phys. Chem. A 2008, 112, 9796-9800
64. Min, C.-G.; Ren, A.-M.; Guo, J.-F.; Li, Z.-W.; Zou, L.-Y.; Goddard, J. D.; Feng, J.-K. A Time-Dependent Density Functional Theory Investigation on the Origin of Red Chemiluminescence ChemPhysChem 2010, 11, 251-259
65. Cohen, A. J.; Mori-Sánchez; Yang, W. Insights into current limitations of density functional theory Science 2008, 321, 792-794
66. Perdew, J. P.; Wang, Y. Accurate and simple analytic representation of the electron-gas correlation-energy Phys. Rev. B 1992, 45, 13244-13249
67. Klamt, A.; Schuurmann, G. COSMO-A new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient J. Chem. Soc., Perkin Trans 2 1993, 5, 799-805
68. Li, Z.-W.; Min, C.-G.; Ren, A.-M.; Guo, J.-F.; Goddard, J. D.; Feng, J.-K.; Zuo, L. Theoretical Study of the Relationships between Excited State Geometry Changes and Emission Energies of Oxyluciferin Bull. Korean Chem. Soc. 2010, 31, 895-900
69. Conti, E.; Franks, N. P.; Brick, P. Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes Structure 1996, 4, 287-298
70. Nakatani, N.; Hasegawa, J.; Nakatsuji, H. Artificial color tuning of firefly luminescence, Theoretical mutation by tuning electrostatic interactions between protein and luciferin Chem. Phys. Lett. 2009, 469, 191-194
71. Tagami, A.; Ishibashi, N.; Kato, D.-I.; Taguchi, N.; Mochizuki, Y.; Watanabe, H.; Ito, M.; Tanaka, S. Ab initio quantum-chemical study on emission spectra of bioluminescent luciferases by fragment molecular orbital method Chem. Phys. Lett. 2009, 472, 118-123
72. Mochizuki, Y.; Tanaka, K.; Yamashita, K.; Ishikawa, T.; Nakano, T.; Amari, S.; Segawa, K.; Murase, T.; Tokiwa, H.; Sakurai, M. Parallelized integral-direct CIS(D) calculations with multilayer fragment molecular orbital scheme Theor. Chem. Acc. 2007, 117, 541-553
73. Head-Gordon, M.; Rico, R. J.; Oumi, M.; Lee, T. J. A doubles correction to electronic excited states from configuration interaction in the space of single substitutions Chem. Phys. Lett. 1994, 219, 21-29
74. Navizet, I.; Liu, Y.-J.; Xiao, H. Y.; Fang, W. H.; Lindh, R. Color-tuning mechanism of firefly investigated by multi-configurational perturbation method J. Am. Chem. Soc. 2010, 132, 706-712
75. Milne, B. F.; Marques, N. A.; Nogueira, F. Fragment molecular orbital investigation of the role of AMP protonation in firefly luciferase pH-sensitivity Phys. Chem. Chem. Phys. 2010, 12, 14285-14293
76. Dawson, R. M. C.; Elliott, D. C.; Elliott, W. H.; Jones, K. M. Data for Biochemical Research; Oxford University Press: Oxford, England, 1989.
77. Min, C.-G.; Ren, A.-M.; Guo, J.-F.; Goddard, J. D.; Sun, C. C. Theoretical investigation on the origin of yellow-green firefly bioluminescence by time-dependent density functional theory ChemPhysChem 2010, 11, 2199-2204
78. Siegbahn, P. E. M.; Eriksson, L.; Himo, F.; Pavlov, M.. Hydrogen atom transfer in ribonucleotide reductase (RNR) J. Phys. Chem. B 1998, 102, 10622-10629 (Pubitemid 128611896)
79. Siegbahn, P. J. Theoretical study of the substrate mechanism of ribonucleotide reductase J. Am. Chem. Soc. 1998, 120, 8417-8429
80. Blomberg, M. R. A.; Siegbahn, P. E. M.; Babcock, G. T. Modeling electron transfer in biochemistry: A quantum chemical study of charge separation in Rhodobacter sphaeroides and photosystem II J. Am. Chem. Soc. 1998, 120, 8812-8824 (Pubitemid 28442920)
81. Fernandes, P. A.; Ramos, M. J. Theoretical Studies on the Mechanism of Inhibition of Ribonucleotide Reductase by (E)-2′-Fluoromethylene-2′- deoxycitidine-5′-diphosphate J. Am. Chem. Chem. Soc. 2003, 125, 6311-6322 (Pubitemid 36583006)
82. Mao, Y. Dynamics studies of luciferase using elastic network model: how the sequence distribution of luciferase determines its color. Protein Eng., Des. Sel. 2010, DOI: 10.1093/protein/gzq109.
83. Tirion, M. M. Large Amplitude Elastic Motions in Proteins from a Single-Parameter, Atomic Analysis Phys. Rev. Lett. 1996, 77, 1905-1908 (Pubitemid 126625816)
84. Cai, D.; Marques, M. A.; Nogueira, F. Accurate Color Tuning of Firefly Chromophore by Modulation of Local Polarization Electrostatic Fields J. Phys. Chem. B. 2010, 115, 329-332
85. Hohenberg, P.; Kohn, W. Inhomogeneous Electron Gas Phys. Rev. 1964, 136, B864-B871
86. Kohn, W.; Sham, L. J. Self-Consistent Equations Including Exchange and Correlation Effects Phys. Rev. 1965, 140, A1133-A1138
87. Chen, S.-F.; Liu, Y.-J.; Navizet, I.; Ferré, N.; Fang, W.-H.; Lindh, R. Systematic Theoretical Investigation on the Light Emitter of Firefly. J. Chem. Theory Comput. 2011, DOI: 10.1021/ct200045q.
88. Pinto da Silva, L.; Esteves da Silva, J. C. G. Computational Investigation of the effect of pH on the Color of Firefly Bioluminescence by DFT. ChemPhysChem 2011, DOI: 10.1002/cphc.201000980.
89. Adamo, C.; Barone, V. Toward reliable density functional methods without adjustable parameters: The PBE0 model J. Chem. Phys. 1999, 110, 6158-6170