Ultrafast excited-state deactivation of flavins bound to dodecin

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17637-17644

  Staudt, Heike ^a   Oesterhelt, Dieter ^b   Grininger, Martin ^b   Wachtveitl, Josef ^a  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL; BINDING POCKETS; DEPOPULATION MECHANISMS; DODECIN; ELECTRON TRANSFER; PHOTOCHEMICAL PROPERTIES; PHOTOEXCITED STATE; QUATERNARY STRUCTURE; SIDE REACTIONS; TRYPTOPHAN RESIDUES; ULTRA-FAST;

AMINO ACIDS; DEGRADATION; EXCITED STATES; VIRTUAL STORAGE;

COENZYMES;

DODECIN; RIBOFLAVIN; RIBOFLAVIN BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ARTICLE; BINDING SITE; CHEMICAL MODIFICATION; CHEMICAL REACTION; CHEMICAL STRUCTURE; DEGRADATION; ELECTRON TRANSPORT; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; SPECIES DIFFERENCE; ULTRAFAST EXCITED STATE DEACTIVATION;

ARCHAEAL PROTEINS; BACTERIA; BACTERIAL PROTEINS; BINDING SITES; EVOLUTION, MOLECULAR; FLAVIN MONONUCLEOTIDE; HALOBACTERIUM SALINARUM; PROTEIN BINDING; RIBOFLAVIN; SPECIES SPECIFICITY; TRYPTOPHAN;

ARCHAEA; BACTERIA (MICROORGANISMS); HALOBACTERIUM SALINARUM;

EID: 84861204476     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331652     Document Type: Article

References (49)

1. Bieger, B., Essen, L. O., and Oesterhelt, D. (2003) Crystal structure of halophilic dodecin: a novel, dodecameric flavin-binding protein from Halobacterium salinarum. Structure 11, 375-385 (Pubitemid 36419565)
2. Grininger, M., Staudt, H., Johansson, P., Wachtveitl, J., and Oesterhelt, D. (2009) Dodecin is the key player in flavin homeostasis of archaea. J. Biol. Chem. 284, 13068-13076
3. Liu, F., Xiong, J., Kumar, S., Yang, C., Ge, S., Li, S., Xia, N., and Swaminathan, K. (2011) Structural and biophysical characterization of Mycobacterium tuberculosis dodecin Rv1498A. J. Struct. Biol. 175, 31-38
4. Meissner, B., Schleicher, E., Weber, S., and Essen, L. O. (2007) The dodecin from Thermus thermophilus, a bifunctional cofactor storage protein. J. Biol. Chem. 282, 33142-33154 (Pubitemid 350159284)
5. Grininger, M., Zeth, K., and Oesterhelt, D. (2006) Dodecins: a family of lumichrome-binding proteins. J. Mol. Biol. 357, 842-857
6. Grininger, M., Seiler, F., Zeth, K., and Oesterhelt, D. (2006) Dodecin sequesters FAD in closed conformation from the aqueous solution. J. Mol. Biol. 364, 561-566 (Pubitemid 44737821)
7. Vinzenz, X., Grosse, W., Linne, U., Meissner, B., and Essen, L. O. (2011) Chemical engineering of Mycobacterium tuberculosis dodecin hybrids. Chem. Commun. 47, 11071-11073
8. Nissen, M. S., Youn, B., Knowles, B. D., Ballinger, J. W., Jun, S. Y., Belchik, S. M., Xun, L., and Kang, C. (2008) Crystal structures of NADH:FMN oxidoreductase (EmoB) at different stages of catalysis. J. Biol. Chem. 283, 28710-28720
9. Zhong, D., and Zewail, A. H. (2001) Femtosecond dynamics of flavoproteins: charge separation and recombination in riboflavin (vitamin B2)-binding protein and in glucose oxidase enzyme. Proc. Natl. Acad. Sci. U.S.A. 98, 11867-11872 (Pubitemid 32962587)
10. Liu, Z., Tan, C., Guo, X., Kao, Y. T., Li, J., Wang, L., Sancar, A., and Zhong, D. (2011) Dynamics and mechanism of cyclobutane pyrimidine dimer repair byDNAphotolyase. Proc. Natl. Acad. Sci. U.S.A. 108, 14831-14836
11. Gauden, M., van Stokkum, I. H., Key, J. M., Lührs, D. Ch., Van Grondelle, R., Hegemann, P., and Kennis, J. T. (2006) Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor. Proc. Natl. Acad. Sci. U.S.A. 103, 10895-10900 (Pubitemid 44150534)
12. Gauden, M., Grinstead, J. S., Laan, W., van Stokkum, I. H., Avila-Perez, M., Toh, K. C., Boelens, R., Kaptein, R., van Grondelle, R., Hellingwerf, K. J., and Kennis, J. T. (2007) On the role of aromatic side chains in the photoactivation of BLUF domains. Biochemistry 46, 7405-7415 (Pubitemid 46986367)
13. Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L. O., van der Horst, G. T., Batschauer, A., and Ahmad, M. (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu.Rev. Plant Biol. 62, 335-364
14. Tanaka, F., Chosrowjan, H., Taniguchi, S., Mataga, N., Sato, K., Nishina, Y., and Shiga, K. (2007) Donor-acceptor distance-dependence of photoinduced electron-transfer rate in flavoproteins. J. Phys. Chem. B 111, 5694-5699 (Pubitemid 46910830)
15. Nakabayashi, T., Islam, M. S., and Ohta, N. (2010) Fluorescence decay dynamics of flavin adenine dinucleotide in a mixture of alcohol and water in the femtosecond and nanosecond time range. J. Phys. Chem. B 114, 15254-15260
16. Shirdel, J., Penzkofer, A., Prochazka, R., Shen, Z., Strauss, J., and Daub, J. (2007) Absorption and emission spectroscopic characterisation of a pyrene-flavin dyad. Chem. Phys. 331, 427-437
17. Stanley, R. J., and MacFarlane, A. W. (2000) Ultrafast excited state dynamics of oxidized flavins: direct observations of quenching by purines. J. Phys. Chem. A 104, 6899-6906
18. Mataga, N., Chosrowjan, H., Taniguchi, S., Tanaka, F., Kido, N., and Kitamura, M. (2002) Femtosecond fluorescence dynamics of flavoproteins: comparative studies on flavodoxin, its site-directed mutants, and riboflavin-binding protein regarding ultrafast electron transfer in protein nanospaces. J. Phys. Chem. B 106, 8917-8920 (Pubitemid 35382819)
19. Mataga, N., Chosrowjan, H., Shibata, Y., Tanaka, F., Nishina, Y., and Shiga, K. (2000) Dynamics and mechanisms of ultrafast fluorescence quenching reactions of flavin chromophores in protein nanospace. J. Phys. Chem. B 104, 10667-10677 (Pubitemid 32021480)
20. Mataga, N., Chosrowjan, H., Shibata, Y., and Tanaka, F. (1998) Ultrafast fluorescence quenching dynamics of flavin chromophores in protein nanospace. J. Phys. Chem. B 102, 7081-7084 (Pubitemid 128586704)
21. Grajek, H., Gryczynski, I., Bojarski, P., Gryczynski, Z., Bharill, S., and Kulak, L. (2007) Flavin mononucleotide fluorescence intensity decay in concentrated aqueous solutions. Chem. Phys. Lett. 439, 151-156 (Pubitemid 46616827)
22. Glasoe, P. K., and Long, F. A. (1960) Use of glass electrodes to measure acidities in deuterium oxide 1,2. J. Phys. Chem. 64, 188-190
23. Huber, R., Kölenz, M. O., Bamberg, E., Kalmbach, R., Engelhard, M., and Wachtveitl, J. (2005) pH-dependent photoisomerization of retinal in proteorhodopsin. Biochemistry 44, 1800-1806
24. Wilhelm, T., Piel, J., and Riedle, E. (1997) Sub-20-fs pulses tunable across the visible from a blue-pumped single-pass noncollinear parametric converter. Opt. Lett. 22, 1494-1496 (Pubitemid 127604716)
25. Riedle, E., Beutter, M., Lochbrunner, S., Piel, J., Schenkl, S., Sporlein, S., and Zinth, W. (2000) Generation of 10- to 50-fs pulses tunable through all of the visible and the NIR. Appl. Phys. B 71, 457-465
26. Lorenc, M., Ziolek, M., Naskrecki, R., Karolczak, J., Kubicki, J., and Maciejewski, A. (2002) Artifacts in femtosecond transient absorption spectroscopy. Appl. Phys. B 74, 19-27 (Pubitemid 41200780)
27. Ernsting, N. P., Kovalenko, S. A., Senyushkina, T., Saam, J., and Farztdinov, V. (2001) Wave-packet-assisted decomposition of femtosecond transient ultraviolet-visible absorption spectra: application to excited-state intramolecular proton transfer in solution. J. Phys. Chem. A 105, 3443-3453
28. Kovalenko, S. A., Dobryakov, A. L., Ruthmann, J., and Ernsting, N. P. (1999) Femtosecond spectroscopy of condensed phases with chirped supercontinuum probing. Phys. Rev. A 59, 2369-2384
29. van Stokkum, I. H., Larsen, D. S., and van Grondelle, R. (2004) Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82-104 (Pubitemid 38952870)
30. Koziol, J., and Knobloch, E. (1965) The solvent effect on the fluorescence and light absorption of riboflavin and lumiflavin. Biochim. Biophys. Acta 102, 289-300
31. Ghisla, S., Massey, V., Lhoste, J. M., and Mayhew, S. G. (1974) Fluorescence and optical characteristics of reduced flavins and flavoproteins. Biochemistry 13, 589-597
32. Massey, V., and Ganther, H. (1965) On the interpretation of the absorption spectra of flavoproteins with special reference to D-amino acid oxidase. Biochemistry 4, 1161-1173
33. Sun, M., Moore, T. A., and Song, P. S. (1972) Molecular luminescence studies of flavins. I. The excited states of flavins. J. Am. Chem. Soc. 94, 1730-1740
34. Harbury, H. A., and Foley, K. A. (1958) Molecular interaction of isoalloxazine derivatives. Proc. Natl. Acad. Sci. U.S.A. 44, 662-668
35. MacFarlane, A. W., 4th, and Stanley, R. J. (2001) Evidence of powerful substrate electric fields in DNA photolyase: implications for thymidine dimer repair. Biochemistry 40, 15203-15214
36. Weigel, A., Dobryakov, A. L., Veiga, M., and Pérez Lustres, J. L. (2008) Photoinduced processes in riboflavin: superposition of pi pi*-n pi*states by vibronic coupling, transfer of vibrational coherence, and population dynamics under solvent control. J. Phys. Chem. A 112, 12054-12065
37. Heelis, P. F. (1982) The photophysical and photochemical properties of flavins (isoalloxazines). Chem. Soc. Rev. 11, 15-39
38. -radicals in light- and heavy-water solutions: a pulse radiolysis study. J. Phys. Chem. 95, 3639-3643
39. Baldwin, J., Krebs, C., Ley, B. A., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M. (2000) Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 1. Evidence for a transient tryptophan radical. J. Am. Chem. Soc. 122, 12195-12206 (Pubitemid 32062257)
40. Massey, V. (2000) The chemical and biological versatility of riboflavin. Biochem. Soc. Trans. 28, 283-296
41. Massey, V., and Palmer, G. (1966) On the existence of spectrally distinct classes of flavoprotein semiquinones: a new method for the quantitative production of flavoprotein semiquinones. Biochemistry 5, 3181-3189
42. Miura, R. (2001) Versatility and specificity in flavoenzymes: control mechanisms of flavin reactivity. Chem. Rec. 1, 183-194
43. Page, C. C., Moser, C. C., Chen, X., and Dutton, P. L. (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52
44. Grajek, H., Zurkowska, G., and Kuśba, J. (2005) Influence of diffusion on nonradiative energy transfer between FMN molecules in aqueous solutions. J. Photochem. Photobiol. B 80, 145-155 (Pubitemid 40984414)
45. Islam, S. D., Susdorf, T., Penzkofer, A., and Hegemann, P. (2003) Fluorescence quenching of flavin adenine dinucleotide in aqueous solution by pH-dependent isomerisation and photo-induced electron transfer. Chem. Phys. 295, 137-149
46. Weber, G. (1950) Fluorescence of riboflavin and flavin-adenine dinucleotide. Biochem. J. 47, 114-121
47. Chosrowjan, H., Taniguchi, S., Mataga, N., Tanaka, F., and Visser, A. J. W. G. (2003) The stacked flavin adenine dinucleotide conformation in water is fluorescent on picosecond timescale. Chem. Phys. Lett. 378, 354-358
48. Song, P. S. (1968) On the basicity of the excited state of flavins. Photochem. Photobiol. 7, 311-313
49. Katz, A. K., Glusker, J. P., Markham, G. D., and Bock, C. W. (1998) Deprotonation of water in the presence of carboxylate and magnesium ions. J. Phys. Chem. B 102, 6342-6350 (Pubitemid 128611720)