Direct observation of the structural change of Tyr174 in the primary reaction of sensory Rhodopsin II

Biochemistry

Volumn 50, Issue 15, 2011, Pages 3170-3180

  Mizuno, Misao ^a   Sudo, Yuki ^b,c   Homma, Michio ^b   Mizutani, Yasuhisa ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLUE LIGHT; CONFORMATIONAL CHANGE; DIRECT OBSERVATION; GAIN INSIGHT; INSTRUMENTAL RESPONSE; MONITORING CHANGE; PARTIAL RECOVERY; PHOTOCYCLES; PICOSECOND TIME; PRIMARY REACTION; PROBE PULSE; PROTEIN STRUCTURES; PUMP PULSE; RAMAN BANDS; REAL-TIME OBSERVATION; SENSING MECHANISM; SENSORY RHODOPSIN II (SRII); SPECTRAL CHANGE; STRUCTURAL CHANGE; TIME CONSTANTS; TIME-RESOLVED; TRANSDUCER PROTEINS; TRYPTOPHAN BANDS; TYROSINE RESIDUES; ULTRAVIOLET RESONANCE RAMAN SPECTROSCOPY;

AMINO ACIDS; BACTERIOLOGY; OPHTHALMOLOGY; OPTICAL PUMPING; PROTEINS; RAMAN SPECTROSCOPY; SIGNAL TRANSDUCTION;

CHROMOPHORES;

RHODOPSIN; TRYPTOPHAN; TYROSINE;

ARTICLE; BLEACHING; CHROMATOPHORE; CRYSTALLOGRAPHY; ISOMERIZATION; MUTANT; NONHUMAN; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; RESPONSE TIME; RETINA;

HALOBACTERIACEAE; HALORHODOPSINS; MUTATION; SENSORY RHODOPSINS; SPECTRUM ANALYSIS, RAMAN; TIME FACTORS; TYROSINE; VIBRATION;

EID: 79953847127     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101817y     Document Type: Article

References (77)

1. Suzuki, D., Irieda, H., Homma, M., Kawagishi, I., and Sudo, Y. (2010) Phototactic and Chemotactic Signal Transduction by Transmembrane Receptors and Transducers in Microorganisms Sensors 10, 4010-4039
2. Klare, J., Chizhov, I., and Engelhard, M. (2008) Microbial Rhodopsins: Scaffolds for Ion Pumps, Channels, and Sensors Results Probl. Cell Differ. 45, 73-122
3. Spudich, J. L., Yang, C.-S., Jung, K.-H., and Spudich, E. N. (2000) RETINYLIDENE PROTEINS: Structures and Functions from Archaea to Humans Annu. Rev. Cell Dev. Biol. 16, 365-392 (Pubitemid 32037511)
4. Gordeliy, V. I., Labahn, J., Moukhametzianov, R., Efremov, R., Granzin, J., Schlesinger, R., Buldt, G., Savopol, T., Scheidig, A. J., Klare, J. P., and Engelhard, M. (2002) Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex Nature 419, 484-487
5. Luecke, H., Schobert, B., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Crystal Structure of Sensory Rhodopsin II at 2.4 Angstroms: Insights into Color Tuning and Transducer Interaction Science 293, 1499-1503 (Pubitemid 32801553)
6. Sasaki, J. and Spudich, J. L. (2008) Signal Transfer in Haloarchaeal Sensory Rhodopsin- Transducer Complexes Photochem. Photobiol. 84, 863-868
7. Hein, M., Wegener, A. A., Engelhard, M., and Siebert, F. (2003) Time-Resolved FTIR Studies of Sensory Rhodopsin II (NpSRII) from Natronobacterium pharaonis: Implications for Proton Transport and Receptor Activation Biophys. J. 84, 1208-1217 (Pubitemid 36133442)
8. Ito, M., Sudo, Y., Furutani, Y., Okitsu, T., Wada, A., Homma, M., Spudich, J. L., and Kandori, H. (2008) Steric Constraint in the Primary Photoproduct of Sensory Rhodopsin II Is a Prerequisite for Light-Signal Transfer to HtrII Biochemistry 47, 6208-6215 (Pubitemid 351812833)
9. Kandori, H., Shimono, K., Sudo, Y., Iwamoto, M., Shichida, Y., and Kamo, N. (2001) Structural Changes of pharaonis Phoborhodopsin upon Photoisomerization of the Retinal Chromophore: Infrared Spectral Comparison with Bacteriorhodopsin Biochemistry 40, 9238-9246 (Pubitemid 32730045)
10. Furutani, Y., Kamada, K., Sudo, Y., Shimono, K., Kamo, N., and Kandori, H. (2005) Structural Changes of the Complex between pharaonis Phoborhodopsin and Its Cognate Transducer upon Formation of the M Photointermediate Biochemistry 44, 2909-2915 (Pubitemid 40293665)
11. Moukhametzianov, R., Klare, J. P., Efremov, R., Baeken, C., Göppner, A., Labahn, J., Engelhard, M., Bäldt, G., and Gordeliy, V. I. (2006) Development of the signal in sensory rhodopsin and its transfer to the cognate transducer Nature 440, 115-119 (Pubitemid 43336278)
12. Lutz, I., Sieg, A., Wegener, A. A., Engelhard, M., Boche, I., Otsuka, M., Oesterhelt, D., Wachtveitl, J., and Zinth, W. (2001) Primary reactions of sensory rhodopsins Proc. Natl. Acad. Sci. U.S.A. 98, 962-967 (Pubitemid 32121170)
13. Imamoto, Y., Shichida, Y., Hirayama, J., Tomioka, H., Kamo, N., and Yoshizawa, T. (1992) Nanosecond Laser Photolysis of Phoborhodopsin: from Natronobacterium pharaonis Appearance of KL and L Intermediates in the Photocycle at Room Temperature Photochem. Photobiol. 56, 1129-1134
14. Gross, R., Wolf, M. M. N., Schumann, C., Friedman, N., Sheves, M., Li, L., Engelhard, M., Trentmann, O., Neuhaus, H. E., and Diller, R. (2009) Primary Photoinduced Protein Response in Bacteriorhodopsin and Sensory Rhodopsin II J. Am. Chem. Soc. 131, 14868-14878
15. Harada, I. and Takeuchi, H. (1986) Raman and Ultraviolet Resonance Raman Spectra of Proteins and Related Compounds, in Spectroscopy of Biological Systems (Clark, R. J. H. and Hester, R. E., Eds.), pp 113 - 175, John Wiley & Sons, Chichester.
16. Kitagawa, T. and Hirota, S. (2002) Raman Spectroscopy of Proteins, in Handbook of Vibrational Spectroscopy (Chalmers, J. M. and Griffiths, P. R., Eds.), pp 3426 - 3446, John Wiley & Sons, Chichester.
17. Sato, A., Gao, Y., Kitagawa, T., and Mizutani, Y. (2007) Primary protein response after ligand photodissociation in carbonmonoxy myoglobin Proc. Natl. Sci. Acad. Sci. U.S.A. 104, 9627-9632 (Pubitemid 47175317)
18. Sato, A. and Mizutani, Y. (2005) Picosecond Structural Dynamics of Myoglobin following Photodissociation of Carbon Monoxide As Revealed by Ultraviolet Time-Resolved Resonance Raman Spectroscopy Biochemistry 44, 14709-14714 (Pubitemid 41612250)
19. Mizuno, M., Hamada, N., Tokunaga, F., and Mizutani, Y. (2007) Picosecond Protein Response to the Chromophore Isomerization of Photoactive Yellow Protein: Selective Observation of Tyrosine and Tryptophan Residues by Time-Resolved Ultraviolet Resonance Raman Spectroscopy J. Phys. Chem. B 111, 6293-6296 (Pubitemid 47012629)
20. Fujiwara, A. and Mizutani, Y. (2008) Photoinduced electron transfer in glucose oxidase: a picosecond time-resolved ultraviolet resonance Raman study J. Raman Spectrosc. 39, 1600-1605
21. Mizuno, M., Shibata, M., Yamada, J., Kandori, H., and Mizutani, Y. (2009) Picosecond Time-Resolved Ultraviolet Resonance Raman Spectroscopy of Bacteriorhodopsin: Primary Protein Response to the Photoisomerization of Retinal J. Phys. Chem. B 113, 12121-12128
22. Sudo, Y., Furutani, Y., Kandori, H., and Spudich, J. L. (2006) Functional Importance of the Interhelical Hydrogen Bond between Thr204 and Tyr174 of Sensory Rhodopsin II and Its Alteration during the Signaling Process J. Biol. Chem. 281, 34239-34245 (Pubitemid 46036632)
23. Sudo, Y., Furutani, Y., Shimono, K., Kamo, N., and Kandori, H. (2003) Hydrogen Bonding Alteration of Thr-204 in the Complex between pharaonis Phoborhodopsin and Its Transducer Protein Biochemistry 42, 14166-14172 (Pubitemid 37499413)
24. Kitajima-Ihara, T., Furutani, Y., Suzuki, D., Ihara, K., Kandori, H., Homma, M., and Sudo, Y. (2008) Salinibacter Sensory Rhodopsin J. Biol. Chem. 283, 23533-23541
25. Kaminaka, S. and Mathies, R. A. (1998) High-Throughput Large-Aperture Prism Prefilter for Ultraviolet Resonance Raman Spectroscopy Appl. Spectrosc. 52, 469-473 (Pubitemid 128619558)
26. Sweeney, J. A. and Asher, S. A. (1990) Tryptophan UV Resonance Raman Exsitation Profiles J. Phys. Chem. 94, 4784-4791
27. Doig, S. J., Reid, P. J., and Mathies, R. A. (1991) Picosecond Time-Resolved Resonance Raman Spectroscopy of Bacteriorhodopsins J, K, and KL Intermediates J. Phys. Chem. 95, 6372-6379
28. Herbst, J., Heyne, K., and Diller, R. (2002) Femtosecond Infrared Spectroscopy of Bacteriorhodopsin Chromophore Isomerization Science 297, 822-825 (Pubitemid 34839629)
29. Terentis, A. C., Ujj, L., Abramczyk, H., and Atkinson, G. H. (2005) Primary events in the bacteriorhodopsin photocycle: Tortional vibrational dephasing in the first excited electronic state Chem. Phys. 313, 51-62 (Pubitemid 40501945)
30. Kandori, H., Furutani, Y., Shimono, K., Shichida, Y., and Kamo, N. (2001) Internal Water Molecules of pharaonis Phoborhodopsin Studied by Low-Temperature Infrared Spectroscopy Biochemistry 40, 15693-15698 (Pubitemid 34015197)
31. Hirayama, J., Imamoto, Y., Shichida, Y., Kamo, N., Tomioka, H., and Yoshizawa, T. (1992) Photocycle of phoborhodopsin from haloalkaliphilic bacterium (Natronobacterium pharaonis) studied by low-temperature spectrophotometry Biochemistry 31, 2093-2098
32. Sudo, Y., Furutani, Y., Wada, A., Ito, M., Kamo, N., and Kandori, H. (2005) Steric Constraint in the Primary Photoproduct of an Archaeal Rhodopsin from Regiospecific Perturbation of C-D Stretching Vibration of the Retinyl Chromophore J. Am. Chem. Soc. 127, 16036-16037 (Pubitemid 41689225)
33. Sudo, Y. and Spudich, J. L. (2006) Three strategically placed hydrogen-bonding residues convert a proton pump into a sensory receptor Proc. Natl. Acad. Sci. U.S.A. 103, 16129-16134 (Pubitemid 44715163)
34. He, Y., Krebs, M. P., Fischer, W. B., Khorana, H. G., and Rothschild, K. J. (1993) FTIR Difference Spectroscopy of the Bacteriorhodopsin Mutant Tyr- 185-Phe: Detection of a Stable 0-like Species and Characterization of Its Photocycle at Low Temperature Biochemistry 32, 2282-2290 (Pubitemid 23094890)
35. Wegener, A.-A., Chizhov, I., Engelhard, M., and Steinhoff, H.-J. (2000) Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II J. Mol. Biol. 301, 881-891
36. Wegener, A.-A., Klare, J. P., Engelhard, M., and Steinhoff, H.-J. (2001) Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis EMBO J. 20, 5312-5319 (Pubitemid 32959450)
37. Koch, M. H., Dencher, N. A., Oesterhelt, D., Plöhn, H. J., Rapp, G., and Bäldt, G. (1991) Time-resolved X-ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin EMBO J. 10, 521-526 (Pubitemid 21905504)
38. Subramaniam, S., Gerstein, M., Oesterhelt, D., and Henderson, R. (1993) Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin EMBO J. 12, 1-8 (Pubitemid 23042376)
39. Rothschild, K. J., Braiman, M. S., Mogi, T., Stern, L. J., and Khorana, H. G. (1989) Conserved amino acids in F-helix of bacteriorhodopsin form part of a retinal binding pocket FEBS Lett. 250, 448-452
40. Brack, T. L. and Atkinson, G. H. (1989) Picosecond time-resolved resonance Raman spectrum of the K-590 intermediate in the room temperature bacteriorhodopsin J. Mol. Struct. 214, 289-303
41. Hsieh, C.-L., Nagumo, M., Nicol, M., and El-Sayed, M. A. (1981) Picosecond and Nanosecond Resonance Raman Studies of bancteriorhodopsin. Do Configurational Changes of Retinal Occur in Picoseconds? J. Phys. Chem. 85, 2714-2717
42. Smith, S. O., Lugtenburg, J., and Mathies, R. A. (1985) Determination of Retinal Chromophore Structure in Bacteriorhodopsine with Resonance Raman Spectroscopy J. Membr. Biol. 85, 95-109 (Pubitemid 15036784)
43. 590 intermediate Proc. Natl. Sci. Acad. Sci. U.S.A. 76, 3046-3050 (Pubitemid 9233232)
44. Weidlich, O., Ujj, L., Jäger, F., and Atkinson, G. H. (1997) Nanosecond Retinal Structure Changes in K-590 During the Room-Temperature Bacteriorhodopsin Photocycle: Picosecond Time-Resolved Coherent Anti-Stokes Raman Spectroscopy Biophys. J. 72, 2329-2341 (Pubitemid 27184461)
45. Diller, R., Iannone, M., Cowen, B. R., Maiti, S., Bogomolin, R. A., and Hochstrasser, R. M. (1992) Picosecond Dynamics of Bacteriorhodopsin, Probed by Time-Resoleved Infrared Spectroscopy Biochemistry 31, 5567-5572
46. Diller, R., Maiti, S., Walker, G. C., Cowen, B. R., Pippenger, R., Bogomolin, R. A., and Hochstrasser, R. M. (1995) Femtosecond time-resolved infrared laser study of the J-K transition of bacteriorhodopsin Chem. Phys. Lett. 241, 109-115
47. Dioumaev, A. K. and Braiman, M. S. (1997) Two Bathointermediates of the Bacteriorhodopsin Photocycle, Distinguished by Nanosecond Time-Resoleved FTIR Spectroscopy at Room Temperature J. Phys. Chem. B 101, 1655-1662 (Pubitemid 127628042)
48. Hage, W., Kim, M., Frei, H., and Mathies, R. A. (1996) Protein Dynamics in the Bacteriorhodopsine Photocycle: A Nanosecond Step-Scan FTIR Investigation of the KL to L Transition J. Phys. Chem. 100, 16026-16033 (Pubitemid 126838056)
49. Sasaki, J., Maeda, A., Kato, C., and Hamaguchi, H.-o. (1993) Time-Resolved Infrared Spectral Analysis of the KL-to-L Conversion in the Photocycle of Bacteriorhodopsin Biochemistry 32, 867-871 (Pubitemid 23059368)
50. Weidlich, O. and Siebert, F. (1993) Time-Resolved Step-Scan FT-IR Investigations of the Transition from KL to L in the Bacteriorhodopsin Photocycle: Indentification of Chromophore Twists by Assigning Hydrogen-Out-Of-Plane (HOOP) Bending Vibrations Appl. Spectrosc. 47, 1394-1400
51. Braiman, M. and Mathies, R. (1982) Resonance Raman spectra of bacteriorhodopsins primary photoproduct: Evidence for a distorted 13-cis retinal chromophore Proc. Natl. Sci. Acad. Sci. U.S.A. 79, 403-407
52. Kandori, H., Belenky, M., and Herzfeld, J. (2002) Vibrational Frequency and Dipolar Orientation od the Protonated Schiff Base in bacteriorhodopsin before and after Photoisomerization Biochemistry 41, 6026-6031 (Pubitemid 34498908)
53. Kandori, H., Kinoshita, N., Shichida, Y., and Maeda, A. (1998) Protein Structural Changes in Bacteriorhodopsin upon Photoisomerization As Revealed by Polarized FTIR Spectroscopy J. Phys. Chem. B 102, 7899-7905 (Pubitemid 128576846)
54. Kandori, H., Kinoshita, N., Yamazaki, Y., Maeda, A., Shichida, Y., Needleman, R., Lanyi, J. K., Bizounok, M., Herzfeld, J., Raap, J., and Lugtenburg, J. (1999) Structural Change of Threonine 89 upon Photoisomerization in Bacteriorhodopsin As Reveald by Polarized FTIR Spectroscopy Biochemistry 38, 9676-9683
55. Kandori, H., Kinoshita, N., Yamazaki, Y., Maeda, A., Shichida, Y., Needleman, R., Lanyi, J. K., Bizounok, M., Herzfeld, J., Raap, J., and Lugtenburg, J. (2000) Local and distant protein structural changes on photoisomerization of the retinal in bacteriorhodopsin Proc. Natl. Sci. Acad. Sci. U.S.A. 97, 4643-4648 (Pubitemid 30238611)
56. Kandori, H. and Shichida, Y. (2000) Direct Observation of the Bridged Water Stretching Vibrations Inside a Protein J. Am. Chem. Soc. 122, 11745-11746
57. Kandori, H., Yamazaki, Y., Shichida, Y., Raap, J., Lugtenburg, J., Belenky, M., and Herzfeld, J. (2001) Tight Asp-85-Thr-89 association during the pump switch of bacteriorhodopsin Proc. Natl. Sci. Acad. Sci. U.S.A. 98, 1571-1576 (Pubitemid 32165540)
58. Rothchild, K. J., Roepe, P., and Gillespie, J. (1985) Fourier transform infrared spectroscopic evidence for the existence of two conformations of the bacteriorhodopsin primary photoproduct at low temperature Biochim. Biophys. Acta 808, 140-148 (Pubitemid 15049512)
59. Shibata, M. and Kandori, H. (2005) FTIR Studies of Internal Water Molecules in the Schiff Base Region of Bacteriorhodopsin Biochemistry 44, 7406-7413 (Pubitemid 40695994)
60. Tanimoto, T., Furutani, Y., and Kandori, H. (2003) Structural Changes of Water in the Schiff Base Region of Bacteriorhodopsin: Proposal of a Hydration Switch Model Biochemistry 42, 2300-2306 (Pubitemid 36255204)
61. 2 Intermediates of the Photocycle J. Mol. Biol. 328, 439-450 (Pubitemid 36407586)
62. Schobert, B., Cupp-Vickery, J., Harnak, V., Smith, S. O., and Lanyi, J. K. (2002) Crystallographic Structure of the K intermediate of Bacteriorhodopsin: Conservation of Free Energy after Photoisomerization of the Retinal J. Mol. Biol. 321, 715-726 (Pubitemid 36124806)
63. Hayashi, S., Tajkhorshid, E., Kandori, H., and Schulten, K. (2004) Role of Hydrogen-Bond Network in Energy Storage of Bacteriorhodopsins Light-Driven Proton Pump Revealed by ab initio Normal-Mode Analysis J. Am. Chem. Soc. 126, 10516-10517 (Pubitemid 39129135)
64. Hayashi, S., Tajkhorshid, E., and Schulten, K. (2002) Structural Changes during the Formation of Early Intermediates in the Bacteriorhodopsin Photocycle Biophys. J. 83, 1281-1297 (Pubitemid 34977703)
65. Braiman, M. S., Mogi, T., Stern, L. J., Hackett, N. R., Chao, B. H., Khorana, H. G., and Rothschild, K. J. (1988) Vibrational Spectroscopy of Bacteriorhodopsin Mutants: I. Tyrosine-I85 Protonates and Deprotonates During the Photocycle Proteins: Struct., Funct., Genet. 3, 219-229
66. Rothschild, K. J., Roepe, P., Ahl, P. L., Earnest, T. N., Bogomolni, R. A., Gupta, S. K. D., Mulliken, C. M., and Herzfeld, J. (1986) Evidence for a tyrosine protonation change during the primary phototransition of bacteriorhodopsin at low temperature Proc. Natl. Acad. Sci. U.S.A. 83, 347-351 (Pubitemid 16080010)
67. Asher, S. A., Ludwig, M., and Johnson, C. R. (1986) UV Resonance Raman Excitation Profiles of the Aromatic Amino Acids J. Am. Chem. Soc. 108, 3186-3197
68. Rava, R. P. and Spiro, T. G. (1985) Resonance Enhancement in the Ultraviolet Raman Spectra of Aromatic Amino Acids J. Phys. Chem. 89, 1856-1861
69. Chi, Z. and Asher, S. A. (1998) UV Raman Determination of the Environment and Solvent Exposure of Tyr and Trp Residues J. Phys. Chem. B 102, 9595-9602 (Pubitemid 128611879)
70. Matsuno, M. and Takeuchi, H. (1998) Effects of Hydrogen Bonding and Hydrophobic Interactions on the Ultraviolet Resonance Raman Intensities of Indole Ring Vibrations Bull. Chem. Soc. Jpn. 71, 851-857 (Pubitemid 128499846)
71. Schenkl, S., Mourik, F. v., Zwan, G. v. d., Haacke, S., and Chergui, M. (2005) Probing the Ultrafast Change Translocation of Photoexcited Retinal in Bacteriorhodopsin Science 309, 917-920 (Pubitemid 41099924)
72. Harada, I., Yamaguchi, T., Uchida, K., and Takeuchi, H. (1990) Ultraviolet Resonance Raman Spectra of Bacteriorhodopsin in the Light-Adapted and Dark-Adapted States J. Am. Chem. Soc. 112, 2443-2445 (Pubitemid 20144463)
73. Miura, T., Takeuchi, H., and Harada, I. (1989) Tryptophan Raman Bands Selective to Hydrogen Bonding and Side-Chain Conformation J. Raman Spectrosc. 20, 667-671
74. Ludwig, M. and Asher, S. A. (1988) Ultraviolet ResonanceRaman Excitation Profiles of Tyrosine: Dependence of Raman Cross Sections on Excited-State Intermediates J. Am. Chem. Soc. 110, 1005-1011 (Pubitemid 18058811)
75. Mogi, T., Stern, L. J., Hackett, N. R., and Khorana, H. G. (1987) Bacteriorhodopsin mutants containing single tyrosine to phenylalanine substitutions are all active in proton translocation Proc. Natl. Acad. Sci. U.S.A. 84, 5595-5599
76. Sudo, Y., Furutani, Y., Spudich, J. L., and Kandori, H. (2007) Early Photocycle Structural Changes in a Bacteriorhodopsin Mutant Engineered to Transmit Photosensory Signals J. Biol. Chem. 282, 15550-15558 (Pubitemid 47093300)
77. Amsden, J. J., Kralj, J. M., Bergo, V. B., Spudich, E. N., Spudich, J. L., and Rothschild, K. J. (2008) Different Structural Changes Occur in Blue- and Green-Proteorhodopsins during the Primary Photoreaction Biochemistry 47, 11490-11498