On the involvement of single-bond rotation in the primary photochemistry of photoactive yellow protein

Biophysical Journal

Volumn 101, Issue 5, 2011, Pages 1184-1192

  Stahl, Andreas D ^a   Hospes, Marijke ^b   Singhal, Kushagra ^b   Van Stokkum, Ivo ^a   Van Grondelle, Rienk ^a   Groot, Marie Louise ^a   Hellingwerf, Klaas J ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PHOTOACTIVE YELLOW PROTEIN, BACTERIA; VISUAL PROTEINS AND PIGMENTS;

ARTICLE; CHEMISTRY; HALORHODOSPIRA HALOPHILA; METABOLISM; PH; PHOTOCHEMISTRY; ROTATION; SPECTROSCOPY;

BACTERIAL PROTEINS; HALORHODOSPIRA HALOPHILA; HYDROGEN-ION CONCENTRATION; PHOTOCHEMICAL PROCESSES; PHOTORECEPTORS, MICROBIAL; ROTATION; SPECTRUM ANALYSIS;

EID: 80052442183     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.06.065     Document Type: Article

References (54)

1. M.A. van der Horst, and K.J. Hellingwerf Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families Acc. Chem. Res. 37 2004 13 20
2. T.E. Meyer Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila Biochim. Biophys. Acta 806 1985 175 183
3. W.W. Sprenger, and W.D. Hoff K.J. Hellingwerf The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein J. Bacteriol. 175 1993 3096 3104 (Pubitemid 23148746)
4. K.J. Hellingwerf, J. Hendriks, and T. Gensch Photoactive yellow protein, a new type of photoreceptor protein: will this "yellow lab" bring us where we want to go? J. Phys. Chem. A 107 2003 1082 1094
5. M.A. Cusanovich, and T.E. Meyer Photoactive yellow protein: a prototypic PAS domain sensory protein and development of a common signaling mechanism Biochemistry 42 2003 4759 4770 (Pubitemid 36532027)
6. Y. Imamoto, and M. Kataoka Structure and photoreaction of photoactive yellow protein, a structural prototype of the PAS domain superfamily Photochem. Photobiol. 83 2007 40 49 (Pubitemid 46697222)
7. J.J. Van Beeumen, and B.V. Devreese M.A. Cusanovich Primary structure of a photoactive yellow protein from the phototrophic bacterium Ectothiorhodospira halophila, with evidence for the mass and the binding site of the chromophore Protein Sci. 2 1993 1114 1125 (Pubitemid 23191752)
8. M. Kim, and R.A. Mathies K.J. Hellingwerf Resonance Raman evidence that the thioester-linked 4-hydroxycinnamyl chromophore of photoactive yellow protein is deprotonated Biochemistry 34 1995 12669 12672
9. G.E.O. Borgstahl, D.R. Williams, and E.D. Getzoff 1.4 structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active site, and chromophore Biochemistry 34 1995 6278 6287
10. R. Kort, and H. Vonk K.J. Hellingwerf Evidence for trans-cis isomerization of the p-coumaric acid chromophore as the photochemical basis of the photocycle of photoactive yellow protein FEBS Lett. 382 1996 73 78 (Pubitemid 26092942)
11. S. Yamaguchi, and H. Kamikubo M. Kataoka Low-barrier hydrogen bond in photoactive yellow protein Proc. Natl. Acad. Sci. USA 106 2009 440 444
12. T. Gensch, and C.C. Gradinaru R. van Grondelle The primary photoreaction of photoactive yellow protein (PYP): anisotropy changes and excitation wavelength dependence Chem. Phys. Lett. 356 2002 347 354
13. M.E. van Brederode, and T. Gensch S.E. Braslavsky Photoinduced volume change and energy storage associated with the early transformations of the photoactive yellow protein from Ectothiorhodospira halophila Biophys. J. 68 1995 1101 1109
14. M.L. Groot, and L.J. van Wilderen R. van Grondelle Initial steps of signal generation in photoactive yellow protein revealed with femtosecond mid-infrared spectroscopy Biochemistry 42 2003 10054 10059 (Pubitemid 37052025)
15. 46 donates a proton to the 4-hydroxycinnamate anion chromophore during the photocycle of photoactive yellow protein Biochemistry 35 1996 14671 14678 (Pubitemid 26423797)
16. G. Groenhof, and M.F. Lensink A.E. Mark Signal transduction in the photoactive yellow protein. I. Photon absorption and the isomerization of the chromophore Proteins 48 2002 202 211 (Pubitemid 34743410)
17. G. Groenhof, and L.V. Schäfer M.A. Robb Arginine52 controls the photoisomerization process in photoactive yellow protein J. Am. Chem. Soc. 130 2008 3250 3251 (Pubitemid 351456004)
18. D.S. Larsen, and I.H. van Stokkum R. van Grondelle Incoherent manipulation of the photoactive yellow protein photocycle with dispersed pump-dump-probe spectroscopy Biophys. J. 87 2004 1858 1872 (Pubitemid 39167041)
19. L.J. van Wilderen, and M.A. van der Horst M.L. Groot Ultrafast infrared spectroscopy reveals a key step for successful entry into the photocycle for photoactive yellow protein Proc. Natl. Acad. Sci. USA 103 2006 15050 15055 (Pubitemid 44583162)
20. A. Xie, and L. Kelemen W.D. Hoff Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation Biochemistry 40 2001 1510 1517 (Pubitemid 32144019)
21. M.E. Van Brederode, and W.D. Hoff K.J. Hellingwerf Protein folding thermodynamics applied to the photocycle of the photoactive yellow protein Biophys. J. 71 1996 365 380 (Pubitemid 26227322)
22. T.E. Meyer, and E. Yakali G. Tollin Properties of a water-soluble, yellow protein isolated from a halophilic phototrophic bacterium that has photochemical activity analogous to sensory rhodopsin Biochemistry 26 1987 418 423 (Pubitemid 17022111)
23. W.D. Hoff, and I.H. van Stokkum K.J. Hellingwerf Measurement and global analysis of the absorbance changes in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila Biophys. J. 67 1994 1691 1705 (Pubitemid 24304341)
24. J. Hendriks, I.H.M. van Stokkum, and K.J. Hellingwerf Deuterium isotope effects in the photocycle transitions of the photoactive yellow protein Biophys. J. 84 2003 1180 1191 (Pubitemid 36133439)
25. D. Hoersch, and H. Otto M.P. Heyn Role of a conserved salt bridge between the PAS core and the N-terminal domain in the activation of the photoreceptor photoactive yellow protein Biophys. J. 93 2007 1687 1699 (Pubitemid 47403309)
26. J. Hendriks, and K.J. Hellingwerf pH Dependence of the photoactive yellow protein photocycle recovery reaction reveals a new late photocycle intermediate with a deprotonated chromophore J. Biol. Chem. 284 2009 5277 5288
27. L.L. Premvardhan, and M.A. van der Horst R. van Grondelle Stark spectroscopy on photoactive yellow protein, E46Q, and a nonisomerizing derivative, probes photo-induced charge motion Biophys. J. 84 2003 3226 3239 (Pubitemid 36531770)
28. Z.R. Grabowski, and K. Rotkiewicz W. Baumann Twisted intra-molecular charge-transfer states (TICT) - new class of excited-states with a full charge separation Nouv. J.Chim. 3 1979 443 454
29. Z.R. Grabowski, K. Rotkiewicz, and W. Rettig Structural changes accompanying intramolecular electron transfer: focus on twisted intramolecular charge-transfer states and structures Chem. Rev. 103 2003 3899 4032
30. C. Ko, A.M. Virshup, and T.J. Martinez Electrostatic control of photoisomerization in the photoactive yellow protein chromophore: ab initio multiple spawning dynamics Chem. Phys. Lett. 460 2008 272 277
31. P. Changenet-Barret, and P. Plaza M. Kataoka Role of arginine 52 on the primary photoinduced events in the PYP photocycle Chem. Phys. Lett. 434 2007 320 325 (Pubitemid 46096912)
32. D.S. Larsen, and R. van Grondelle Initial photoinduced dynamics of the photoactive yellow protein ChemPhysChem 6 2005 828 837 (Pubitemid 40669546)
33. M.L. Groot, L.J.G.W. van Wilderen, and M. Di Donato Time-resolved methods in biophysics. 5. Femtosecond time-resolved and dispersed infrared spectroscopy on proteins Photochem. Photobiol. Sci. 6 2007 501 507 (Pubitemid 46717897)
34. J. Hendriks, and W.D. Hoff K.J. Hellingwerf Protonation/deprotonation reactions triggered by photoactivation of photoactive yellow protein from Ectothiorhodospira halophila J. Biol. Chem. 274 1999 17655 17660
35. D.M.F. van Aalten, and A. Haker W. Crielaard Engineering photocycle dynamics. Crystal structures and kinetics of three photoactive yellow protein hinge-bending mutants J. Biol. Chem. 277 2002 6463 6468 (Pubitemid 34968442)
36. R. Kort, and W.D. Hoff K.J. Hellingwerf The xanthopsins: a new family of eubacterial blue-light photoreceptors EMBO J. 15 1996 3209 3218 (Pubitemid 26231926)
37. J. Hendriks, and T. Gensch J.J. van Thor Transient exposure of hydrophobic surface in the photoactive yellow protein monitored with Nile Red Biophys. J. 82 2002 1632 1643 (Pubitemid 34204780)
38. I.H.M. van Stokkum, D.S. Larsen, and R. van Grondelle Global and target analysis of time-resolved spectra Biochim. Biophys. Acta. 1657 2004 82 104 (Pubitemid 38952870)
39. P. Changenet-Barret, and P. Plaza M. Kataoka Structural effects on the ultrafast photoisomerization of photoactive yellow protein. Transient absorption spectroscopy of two point mutants J. Phys. Chem. C 113 2009 11605 11613
40. R.R. Birge, and L.P. Murray K. Nakanishi Two-photon spectroscopy of locked-11-cis-rhodopsin: evidence for a protonated Schiff base in a neutral protein binding site Proc. Natl. Acad. Sci. USA 82 1985 4117 4121 (Pubitemid 15052840)
41. H. Akita Non-bleachable rhodopsins retaining the full natural chromophore J. Am. Chem. Soc. 102 1980 6370 6372
42. K. Inomata, and M.A. Hammam T. Lamparter Sterically locked synthetic bilin derivatives and phytochrome Agp1 from Agrobacterium tumefaciens form photoinsensitive Pr- and Pfr-like adducts J. Biol. Chem. 280 2005 24491 24497 (Pubitemid 40934534)
43. R. Cordfunke, and R. Kort K.J. Hellingwerf Trans/cis (Z/E) photoisomerization of the chromophore of photoactive yellow protein is not a prerequisite for the initiation of the photocycle of this photoreceptor protein Proc. Natl. Acad. Sci. USA 95 1998 7396 7401 (Pubitemid 28293263)
44. M.A. van der Horst, and T.P. Stalcup W.D. Hoff Locked chromophore analogs reveal that photoactive yellow protein regulates biofilm formation in the deep sea bacterium Idiomarina loihiensis J. Am. Chem. Soc. 131 2009 17443 17451
45. M. Sheves, and N. Friedman M. Ottolenghi Primary photochemical event in bacteriorhodopsin: study with artificial pigments Biochemistry 24 1985 1260 1265 (Pubitemid 15096776)
46. B. Borucki, and J.A. Kyndt M.P. Heyn Effect of salt and pH on the activation of photoactive yellow protein and gateway mutants Y98Q and Y98F Biochemistry 44 2005 13650 13663 (Pubitemid 41507446)
47. A.F. Philip, and R.A. Nome W.D. Hoff Spectral tuning in photoactive yellow protein by modulation of the shape of the excited state energy surface Proc. Natl. Acad. Sci. USA 107 2010 5821 5826
48. L. Seidner, and W. Domcke Microscopic modelling of photoisomerization and internal-conversion dynamics Chem. Phys. 186 1994 27 40
49. S. Abbruzzetti, and R. Bizzarri F. Beltram Photoswitching of E222Q GFP mutants: "concerted" mechanism of chromophore isomerization and protonation Photochem. Photobiol. Sci. 9 2010 1307 1319
50. J.M. Berg, J.L. Tymoczko, and L. Stryer Biochemistry 7th ed. 2012 W. H. Freeman New York
51. S. Yeremenko, and I.H. van Stokkum K.J. Hellingwerf Influence of the crystalline state on photoinduced dynamics of photoactive yellow protein studied by ultraviolet-visible transient absorption spectroscopy Biophys. J. 90 2006 4224 4235 (Pubitemid 43846136)
52. U.K. Genick, and G.E. Borgstahl E.D. Getzoff Structure of a protein photocycle intermediate by millisecond time-resolved crystallography Science 275 1997 1471 1475 (Pubitemid 27111294)
53. J. Vreede, and W. Crielaard P.G. Bolhuis Predicting the signaling state of photoactive yellow protein Biophys. J. 88 2005 3525 3535 (Pubitemid 40586601)
54. C. Bernard, and K. Houben N.A. van Nuland The solution structure of a transient photoreceptor intermediate: delta25 photoactive yellow protein Structure 13 2005 953 962 (Pubitemid 40943327)