Proton release group of pharaonis phoborhodopsin revealed by ATR-FTIR spectroscopy

Biochemistry

Volumn 48, Issue 7, 2009, Pages 1595-1603

  Kitade, Yuya ^a   Furutani, Yuji ^a   Kamo, Naoki ^b   Kandori, Hideki ^a  

^a NAGOYA INSTITUTE OF TECHNOLOGY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AQUEOUS PHASE; ATR FT-IR; ATR-FT-IR SPECTROSCOPIES; ATTENUATED TOTAL REFLECTIONS; BACTERIORHODOPSIN (BR); C-O STRETCHES; FT-IR SPECTROSCOPIES; LIGHT-INDUCED CHANGES; MICROBIAL RHODOPSINS; MIRROR IMAGES; MOLECULAR MECHANISMS; MUTANT PROTEINS; PHARAONIS; PROTON RELEASE; PROTONATED WATER CLUSTERS; STRUCTURAL CHANGES; TRANSDUCER PROTEINS;

AMINES; AMINO ACIDS; BACTERIOLOGY; BIOCHEMISTRY; CARBOXYLIC ACIDS; LIGHT REFLECTION; ORGANIC ACIDS; PROTONS; RAIN GAGES;

FOURIER TRANSFORM INFRARED SPECTROSCOPY;

CARBOXYLIC ACID; PROTON; HALORHODOPSIN; SENSORY RHODOPSIN; SENSORY RHODOPSIN II PROTEIN, ARCHAEAL;

ARTICLE; DRUG BINDING; INFRARED SPECTROSCOPY; MUTANT; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHODOLOGY;

CRYSTALLOGRAPHY, X-RAY; HALORHODOPSINS; MODELS, MOLECULAR; PROTONS; SENSORY RHODOPSINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

NATRONOMONAS PHARAONIS;

EID: 61749098218     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801984u     Document Type: Article

References (47)

1. Haupts, U., Tittor, J., and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: Progress in understanding the molecules. Annu. ReV. Biophys. Biomol. Struct. 28, 367-399.
2. Lanyi, J. K. (2004) Bacteriorhodopsin. Annu. Rev. Physiol. 66, 665-688.
3. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin. Biochim. Biophys. Acta 1460, 177-191.
4. Kandori, H. (2004) Hydration switch model for the proton transfer in the Schiff base region of bacteriorhodopsin. Biochim. Biophys. Acta 1658, 72-79.
5. 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.
6. Zima'nyi, L., Váró, G., Chang, M., Ni, B., Needleman, R., and Lanyi, J. K. (1992) Pathways of proton release in the bacteriorhodopsin photocycle. Biochemistry 31, 8535-8543.
7. Brown, L. S., Sasaki, J., Kandori, H., Maeda, A., Needleman, R., and Lanyi, L. J. (1995) Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270, 27122-27126.
8. Balashov, S. P., Imasheva, E. S., Ebrey, T. G., Chen, N, Menick, D. R., and Crouch, R. K (1997) Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin. Biochemistry 36, 8671-8676.
9. Dioumaev, A. K, Richter, H.-T., Brown, L. S., Tanio, M., Tuzi, S., Saito, H., Kimura, Y., Needleman, R., and Lanyi, J. K (1998) Existence of a proton transfer chain in bacteriorhodopsin: Participation of Glu-194 in the release of protons to the extracellular surface. Biochemistry 37, 2496-2506.
10. Rammelsberg, R., Huhn, G., Lubben, M., and Gerwert, K (1998) Bacteriorhodopsin's intramolecular proton-release pathway consists of a hydrogen-bonded network. Biochemistry 37, 5001-5009.
11. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 5498-5503.
12. Zscherp, C., Schlesinger, R., and Heberle, J. (2001) Time-resolved FT-IR spectroscopic investigation of the pH-dependent proton transfer reactions in the E194Q mutant of bacteriorhodopsin. Biochem. Biophys. Res. Commun. 283, 57-63.
13. -1 region during the bacteriorhodopsin photocycle. Biophys. J. 87, 2676-2682.
14. Garczarek, F., Brown, L. S., Lanyi, J. K, and Gerwert, K. (2005) Proton binding within a membrane protein by a protonated water cluster. Proc. Natl. Acad. Sci. U.S.A. 102, 3633-3638.
15. Garczarek, F., and Gerwert, K (2005) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439, 109-112.
16. Lorenz-Fonfría, V. A., Furutani, Y., and Kandori, H. (2008) Active internal waters in the bacteriorhodopsin photocycle. A comparative study of the L and M intermediates at room and cryogenic temperatures by infrared spectroscopy. Biochemistry 47, 4071-4081.
17. Krebs, M. P., and Khorana, H. G. (1993) Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175, 1555-1560.
18. Balashov, S. P. (2000) Protonation reactions and their coupling in bacteriorhodopsin. Biochim. Biophys. Acta 1460, 75-94.
19. Dioumaev, A. K, Brown, L. S., Shih, J., Spudich, E. N, Spudich, J. L., and Lanyi, J. K. (2002) Proton transfers in the photochemical reaction cycle of proteorhodopsin. Biochemistry 41, 5348-5358.
20. Waschuk, S. A., Bezerra, A. G., Jr., Shi, L., and Brown, L. S. (2005) Leptosphaeria rhodopsin: Bacteriorhodopsin-like proton pump from a eukaryote. Proc. Natl. Acad. Sci. U.S.A. 102, 6879-6883.
21. Kamo, N, Shimono, K, Iwamoto, M., and Sudo, Y. (2001) Photochemistry and photoinduced proton-transfer by pharaonis phoborhodopsin. Biochemistry (Moscow, Russ. Fed.) 66, 1277-1282.
22. Spudich, J. L., and Luecke, H. (2002) Sensory rhodopsin II: Functional insights from structure. Curr. Opin. Struct. Biol. 12, 540-546.
23. Gordeliy, V. I., Labahn, J., Moukhametzianov, R., Efremov, R., Granzin, J., Schlesinger, R., Büldt, 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.
24. Schmies, G., Lüttenberg, B., Chizhov, I., Engelhard, M., Becker, A., and Bamberg, E. (2000) Sensory rhodopsin II from the haloalkaliphilic natronobacterium pharaonis: light-activated proton transfer reactions. Biophys. J. 78, 967-976.
25. Sudo, Y., Iwamoto, M., Shimono, K, Sumi, M., and Kamo, N. (2001) Photo-induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) is ceased by association with the transducer. Biophys. J. 80, 916-922.
26. Iwamoto, M., Hasegawa, C., Sudo, Y., Shimono, K, Araiso, T, and Kamo, N. (2004) Proton release and uptake of pharaonis phoborhodopsin (sensory rhodopsin II) reconstituted into phospholipids. Biochemistry 43, 3195-3203.
27. 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.
28. Royant, A., Nollert, P., Edman, K, Neutze, R., Landau, E. M., Pebay-Peyroula, E., and Navarro, J. (2001) X-ray structure of sensory rhodopsin II at 2.1 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 98, 10131-10136.
29. 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.
30. Furutani, Y., Iwamoto, M., Shimono, K, Kamo, N, and Kandori, H. (2002) FTIR spectroscopy of the M photointermediate in pharaonis phoborhodopsin. Biophys. J. 83, 3482-3489.
31. Furutani, Y., Sudo, Y., Kamo, N, and Kandori, H. (2003) FTIR spectroscopy of the complex between pharaonis phoborhodopsin and its transducer protein. Biochemistry 42, 4837-4842.
32. 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.
33. Guijarro, J., Engelhard, M., and Siebert, F. (2006) Anion uptake in halorhodopsin from Natromonas pharaonis studied by FTIR spectroscopy: Consequences for the anion transport mechanism. Biochemistry 45, 11578-11588.
34. Iwaki, M., Puustinen, A., Wikström, M., and Rich, P. R. (2003) ATR-FTIR spectroscopy of the Pm and F intermediates of bovine and Paracoccus denitrificans cytochrome c oxidase. Biochemistry 42, 8809-8817.
35. Iwaki, M., Cotton, N. P., Quirk, P. G., Rich, P. R., and Jackson, J. B. (2006) Molecular recognition between protein and nicotinamide dinucleotide in intact, proton-translocating transhydrogenase studied by ATR-FTIR Spectroscopy. J. Am. Chem. Soc. 128, 2621-2629.
36. Jiang, X., Zaitseva, E., Schmidt, M., Siebert, F., Engelhard, M., Schlesinger, R., Ataka, K, Vogel, R., and Heberle, J. (2008) Resolving voltage-dependent structural changes of a membrane photoreceptor by surface-enhanced IR difference spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 105, 12113-12117.
37. Shimono, K, Ikeura, Y., Sudo, Y., Iwamoto, M., and Kamo, N. (2001) Environment around the chromophore in pharaonis phoborhodopsin: Mutation analysis of the retinal binding site. Biochim. Biophys. Acta 1515, 92-100.
38. Tanimoto, T, Shibata, M., Belenky, M., Herzfeld, J., and Kandori, H. (2004) Altered hydrogen bonding of Arg82 during the proton pump cycle of bacteriorhodopsin: A low-temperature polarized FTIR spectroscopic study. Biochemistry 43, 9439-9447.
39. Shimono, K, Kitami, M, Iwamoto, M., and Kamo, N. (2000) Involvement of two groups in reversal of the bathochromic shift of pharaonis phoborhodopsin by chloride at low pH. Biophys. Chem. 87, 225-230.
40. Engelhard, M., Scharf, B., and Siebert, F. (1996) Protonation changes during the photocycle of sensory rhodopsin II from Natronobacterium pharaonis. FEBS Lett. 395, 195-198.
41. Pfefferlé, J. M., Maeda, A., Sasaki, J., and Yoshizawa, T. (1991) Fourier transform infrared study of the N intermediate of bacteriorhodopsin. Biochemistry 30, 6548-6556.
42. Bergo, V., Spudich, E. N., Spudich, J. L., and Rothschild, K. J. (2003) Conformational changes detected in a sensory rhodopsin II-transducer complex. J. Biol. Chem. 278, 36556-36562.
43. Brown, L. S., Needleman, R., and Lanyi, J. K. (1996) Interaction of proton and chloride transfer pathways in recombinant bacteriorhodopsin with chloride transport activity: Implications for the chloride translocation mechanism. Biochemistry 35, 16048-16054.
44. Kötting, C., Kallenbach, A., Suveyzdis, Y., Wittinghofer, A., and Gerwert, K. (2008) The GAP arginine finger movement into the catalytic site of Ras increases the activation entropy. Proc. Natl. Acad. Sci. U.S.A. 105, 6260-6265.
45. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., and Lanyi, J. K. (1999) Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 286, 255-260.
46. Shimono, K., Furutani, Y., Kamo, N., and Kandori, H. (2003) Vibrational modes of the protonated Schiff base in pharaonis phoborhodopsin. Biochemistry 42, 7801-7806.
47. 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.