Crystal Structures of Archaerhodopsin-1 and -2: Common Structural Motif in Archaeal Light-driven Proton Pumps

Journal of Molecular Biology

Volumn 358, Issue 3, 2006, Pages 675-685

  Enami, Nobuo ^a   Yoshimura, Keiko ^a   Murakami, Midori ^a   Okumura, Hideo ^a   Ihara, Kunio ^a   Kouyama, Tsutomu ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b RIKEN HARIMA INSTITUTE   (Japan)

Author keywords

protein crystallization; proton pump; retinal; water translocation; X ray crystallography

Indexed keywords

ARCHAERHODOPSIN 1; ARCHAERHODOPSIN 2; LEUCINE; POLYENE; PROTEIN; PROTON PUMP; SCHIFF BASE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOPLASM; HYDROPHOBICITY; ISOMERIZATION; MEMBRANE POTENTIAL; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN STRUCTURE; RETINA;

ARCHAEA; HALOBACTERIUM SALINARUM; HALORUBRUM;

EID: 33646058552     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.02.032     Document Type: Article

References (48)

1. Oesterhelt D., and Stoeckenius W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233 (1971) 149-152
2. Mukohata Y. Comparative studies on ion pumps of the bacterial rhodopsin family. Biophys. Chem. 50 (1994) 191-201
3. Ihara K., Umemura T., Katagiri I., Kitajima-Ihara T., Sugiyama Y., Kimura Y., and Mukohata Y. Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J. Mol. Biol. 285 (1999) 163-174
4. Blanck A., and Oesterhelt D. The haloopsin gene II. Sequence primary structure of halorhodopsin and comparison with bacteriorhodopsin. EMBO J. 6 (1987) 265-273
5. Blanck A., Oesterhelt D., Ferrando E., Schegk E.S., and Lottspeich F. Primary structure of sensory rhodopsin I, a prokaryotic photoreceptor. EMBO J. 8 (1989) 3963-3971
6. Oesterhelt D. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol. 8 (1998) 489-500
7. Landau E.M., Pebay-Peyroula E., and Neutze R. Structural and mechanistic insight from high resolution structures of archaeal rhodopsins. FEBS Letters 555 (2003) 51-56
8. 550 intermediate contains a C14-C15 s-trans-retinal chromophore. Proc. Natl Acad. Sci. USA 85 (1988) 2156-2160
9. Yan B., Takahashi T., Johnson R., Derguini F., Nakanishi K., and Spudich J.L. All-trans/13-cis isomerization of retinal is required for phototaxis signaling by sensory rhodopsins in Halobacterium halobium. Biophys. J. 57 (1990) 807-814
10. Nishikawa T., Okumura T., and Kouyama T. Crystal structure of the 13-cis isomer of bacteriorhodopsin in the dark-adapted state. J. Mol. Biol. 352 (2005) 319-328
11. Belrhali H., Nollert P., Royant A., Menzel C., Rosenbusch J.P., Landau E.M., and Pebay-Peyroula E. Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution. Proteins: Struct. Funct. Genet. 7 (1999) 909-917
12. Luecke H., Schobert B., Richter H.-T., Cartailler J.-P., and Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291 (1999) 899-911
13. Kolbe M., Besir H., Essen L.O., and Oesterhelt D. Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution. Science 288 (2000) 1390-1396
14. Royant A., Nollert P., Edmani K., Neutze R., Landau E.M., Pebay-Peyroula E., and Navarro J. X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc. Natl Acad. Sci. USA 98 (2001) 10131-10136
15. Luecke H., Schobert B., Lanyi J.K., Spudich E.N., and Spudich J.L. Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction. Science 293 (2001) 1499-1503
16. Edman K., Royant A., Nollert P., Maxwell C.A., Pebay-Peyroula E., Navarro J., et al. Early structural rearrangements in the photocycle of an integral membrane sensory receptor. Structure 10 (2002) 473-482
17. Vogeley L., Sineshchekov O.A., Trivedi V.D., Sasaki J., Spudich J.L., and Luecke H. Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å. Science 306 (2005) 1390-1393
18. Béjà O., Spudich E.N., Spudich J.L., Leclerc M., and DeLong E. Proteorhodopsin phototrophy in the ocean. Nature 411 (2001) 786-789
19. Gärtner W., and Losi A. Crossing the borders: archaeal rhodopsins go bacterial. Trends Microbiol. 11 (2003) 405-407
20. Mukohata Y., Sugiyama Y., Ihara K., and Yoshida M. An Australian Halobacterium contains a novel protein pump retinal protein: archaerhodopsin. Biochem. Biophys. Res. Commun. 151 (1988) 1339-13445
21. Sugiyama Y., Maeda M., Futai M., and Mukohata Y. Isolation of a gene that encodes a new retinal protein, archaerhodopsin, from Halobacterium sp. aus-1. J. Biol. Chem. 264 (1989) 20859-20862
22. Mukohata Y., Ihara K., Uegaki K., Miyashita Y., and Sugiyama Y. Australian halobacteria and their retinal protein ion pumps. Photochem. Photobiol. 54 (1991) 1039-1045
23. Lukashev E.P., Govindjee R., Kono M., Ebrey T.G., Sugiyama Y., and Mukohata Y. pH dependence of the absorption spectra and photochemical transformations of the archaerhodopsins. Photochem., Photobiol. 60 (1994) 69-75
24. Ihara K., Amemiya T., Miyashita Y., and Mukohata Y. Met-145 is a key residue in the dark adaptation of bacteriorhodopsin homologs. Biophys. J. 67 (1994) 1187-1191
25. Kouyama T., Nishikawa T., Tokuhisa T., and Okumura H. Crystal structure of the L intermediate of bacteriorhodopsin: evidence for vertical translocation of a water molecule during the proton pumping cycle. J. Mol. Biol. 335 (2003) 531-546
26. Kouyama T., Yamamoto M., Kamiya N., Iwasaki H., Ueki T., and Sakurai I. Polyhedral assembly of a membrane protein in its three-dimensional crystal. J. Mol. Biol. 236 (1994) 990-994
27. Takeda K., Sato H., Hino T., Kono M., Fukuda K., Sakurai I., et al. A novel three-dimensional crystal of bacteriorhodopsin obtained by successive fusion of the vesicular assemblies. J. Mol. Biol. 283 (1998) 463-474
28. Enami N., Okumura H., and Kouyama T. X-ray crystallographic study of archaerhodopsin. J. Photosci. 9 (2002) 320-322
29. Uegaki K., Sugiyama Y., and Mukohata Y. Archaerhodopsin-2, from Halobacterium sp. aus-2 further reveals essential amino acid residues for light-driven proton pumps. Arch. Biochem. Biophys. 286 (1991) 107-110
30. Okumura H., Murkami M., and Kouyama T. Crystal structures of acid blue and alkaline purple forms of bacteriorhodopsin. J. Mol. Biol. 351 (2005) 481-495
31. Butt H.J., Fendler K., Bamberg E., Tittor J., and Oesterhelt D. Aspartic acids 96 and 85 play a central role in the function of bacteriorhodopsin as a proton pump. EMBO J. 8 (1989) 1657-1663
32. Gerwert K., Souvignier G., and Hess B. Simultaneous monitoring of light-induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy. Proc. Natl Acad. Sci. USA 87 (1990) 9774-9778
33. Szaraz S., Oesterhelt D., and Ormos P. pH-induced structural changes in bacteriorhodopsin studied by Fourier transform infrared spectroscopy. Biophys. J. 67 (1994) 1706-1712
34. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy. Proc. Natl Acad. Sci. USA 96 (1999) 5498-5503
35. Subramaniam S., Gerstein M., Oesterhelt D., and Henderson R. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12 (1993) 1-8
36. Han B.-G., Vonck J., and Glaeser R.M. The bacteriorhodopsin photocycle: direct structural study of two substrates of the M-intermediate. Biophys. J. 67 (1994) 1179-1186
37. Vonck J. A three-dimensional difference map of the N intermediate in the bacteriorhodopsin photocycle: part of the F helix tilts in the M to N transition. Biochemistry 35 (1996) 5870-5878
38. Schobert B., Brown L.S., and Lanyi J.K. Crystallographic structures of the M and N intermediates of bacteriorhodopsin: assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiff base. J. Mol. Biol. 330 (2003) 553-570
39. Takeda K., Matsui Y., Kamiya N., Adachi S., Okumura H., and Kouyama T. Crystal structure of the M intermediate of bacteriorhodopsin: allosteric structural changes mediated by sliding movement of a transmembrane helix. J. Mol. Biol. 341 (2004) 1023-1037
40. Oesterhelt D., and Stoeckenius W. Isolation of the cell membrane of Halobacterium halobium and its fragmentation into red and purple membrane. Methods Enzymol. 31 (1974) 667-678
41. Fukuda K., Ikegami A., Nasuda-Kouyama A., and Kouyama T. Effect of partial delipidation of purple membrane on the photodynamics of bacteriorhodopsin. Biochemistry 29 (1990) 1997-2002
42. Sakai K., Matsui Y., Kouyama T., Shiro Y., and Adachi S. Optical monitoring of freeze-trapped reaction intermediates in protein crystals: a microspectrophotometer for cryogenic protein crystallography. J. Appl. Crystallog. sect D 35 (2002) 270-273
43. Steller I., Bolotovsky B., and Rossmann M.G. An algorithm for automatic indexing of oscillation images using Fourier analysis. J. Appl. Crystallog. sect. D 30 (1997) 1036-1040
44. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
45. Brünger A.T., Adams P.D., Glore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
46. McRee D.E. Practical Protein Crystallography (1993), Academic Press, San Diego
47. Matsui Y., Sakai K., Murakami M., Shiro Y., Adachi S., Okumura H., and Kouyama T. Specific damages induced by X-ray radiation and structural changes in the primary photoreaction of bacteriorhodopsin. J. Mol. Biol. 324 (2002) 469-481
48. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 14-23