Structural Role of Bacterioruberin in the Trimeric Structure of Archaerhodopsin-2

Journal of Molecular Biology

Volumn 375, Issue 5, 2008, Pages 1267-1281

  Yoshimura, Keiko ^a   Kouyama, Tsutomu ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b RIKEN HARIMA INSTITUTE   (Japan)

Author keywords

bacteriorhodopsin; bacterioruberin; membrane protein crystallization; proton pump; retinal

Indexed keywords

ARCHAERHODOPSIN 2; BACTERIAL PROTEIN; PROTEIN BACTERIORUBERIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; PROTON TRANSPORT; STRUCTURE ANALYSIS;

HALORUBRUM;

EID: 37549071095     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.039     Document Type: Article

References (59)

1. Raman P., Cherezova V., and Caffrey M. The Membrane Protein Data Bank. Cell. Mol. Life Sci. 63 (2006) 36-51
2. Seeger M.A., Schiefner A., Eicher T., Verrey F., Diederichs K., and Pos K.M. Structural symmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313 (2006) 1295-1298
3. +-ATPase from Enterococcus hirae. Science 308 (2005) 654-659
4. + conduction and selectivity. Nature 280 (1998) 69-77
5. Eshaghi S., Niegowski D., Kohl A., Molina D.M., Lesley S.A., and Nordlund P. CorA at 2.9 angstrom resolution crystal structure of a divalent metal ion transporter. Science 313 (2006) 354-357
6. Arnold S., and Kadenbach B. Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur. J. Biochem. 249 (1997) 350-354
7. Henderson R., and Unwin P.N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257 (1975) 28-32
8. 1 complex structure. EMBO J. 20 (2001) 6591-6600
9. Jordan P., Fromme P., Witt H.T., Klukas O., Saenger W., and Krauß N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411 (2001) 909-917
10. Cartailler J.-P., and Luecke H. X-ray crystallographic analysis of lipid-protein interactions in the bacteriorhodopsin purple membrane. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 285-310
11. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 302 (2003) 1009-1014
12. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., et al. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428 (2004) 287-292
13. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438 (2005) 1040-1044
14. Pinkett H.W., Lee A.T., Lum P., Locher K.P., and Rees D.C. An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 315 (2007) 373-377
15. Shinzawa-Itoh K., Aoyama H., Muramoto K., Hirohito Terada H., Kurauchi T., Tadehara Y., et al. Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26 (2007) 1713-1725
16. Fyfe P.K., McAuley K.E., Roszak A.W., Isaacs N.W., Cogdell R.J., and Jones M.R. Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. Trends Biochem. Sci. 26 (2001) 106-112
17. Carnara-Artigas A., Brune D., and Allent J.P. Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc. Natl. Acad. Sci. USA 99 (2002) 11055-11060
18. 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
19. 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
20. Lukashev E.P., 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
21. Dundas I.D., and Larsen H. The physiological role of the carotenoid pigments of Halobacterium salinarium. Arch. Microbiol. 44 (1962) 233-239
22. Kushwaha S.C., and Kates M. Effect of nicotine on biosynthesis of C50 carotenoids in Halobacterium cutirubrum. Can. J. Biochem. 54 (1976) 824-829
23. Kushwaha S.C., Kates M., and Stoeckenius W. Comparison of purple membrane from Halobacterium cutirubrum and Halobacterium halobium. Biochim. Biophys. Acta 426 (1976) 703-710
24. Balashov S.P., Imasheva E.S., and Lanyi J.K. Induced chirality of the light-harvesting carotenoid salinixanthin and its interaction with the retinal of xanthorhodopsin. Biochemistry 45 (2006) 10998-11004
25. Enami N., Yoshimura K., Murakami M., Okumura H., Ihara K., and Kouyama T. Crystal structures of archaerhodopsin-1 and -2: common structural motif in archaeal light-driven proton pumps. J. Mol. Biol. 358 (2006) 675-685
26. 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
27. Grigorieff N., Ceska T.A., Downing K.H., Baldwin J.M., and Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259 (1996) 393-421
28. Essen L.-O., Siegert R., Lehmann W.D., and Oesterhelt D. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl. Acad. Sci. USA 95 (1998) 11673-11678
29. Sato H., Takeda K., Tani K., Hino T., Okada T., Nakasako M., et al. Specific lipid-protein interactions in a novel honeycomb lattice structure of bacteriorhodopsin. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 1251-1256
30. Luecke H., Schober 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
31. 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. Protein 7 (1999) 909-917
32. 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
33. Corcelli A., Colella M., Mascolo G., Fanizzi F.P., and Kates M. A novel glycolipid and phospholipid in the purple membrane. Biochemistry 39 (2000) 3318-3326
34. 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
35. Sass H.J., Buldt G., Gessenich R., Hehn D., Neff D., Schlesinger R., et al. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature 406 (2000) 649-653
36. Subramaniam S., Faruqi A.R., Oesterhelt D., and Henderson R. Electron diffraction studies of light-induced conformational changes in the Leu-93 → Ala bacteriorhodopsin mutant. Proc. Natl. Acad. Sci. USA 94 (1997) 1767-1772
37. 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
38. 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
39. Ming M., Wang Y., Wu J., Ma D., Li Q., and Ding J. Triton X-100 can alter the temporal sequence of the light-driven proton pump of archaerhodopsin 4. FEBS Lett. 580 (2007) 6749-6753
40. Sapra K.T., Besir H., Oesterhelt D., and Muller D.J. Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J. Mol. Biol. 355 (2006) 640-650
41. Dencher N.A., and Heyn M.P. Bacteriorhodopsin monomers pump protons. FEBS Lett. 108 (1979) 307-310
42. Heyes C.D., and El-Sayed M.A. The role of the native lipids and lattice structure in bacteriorhodopsin protein conformation and stability as studied by temperature-dependent Fourier transform-infrared spectroscopy. J. Biol. Chem. 277 (2002) 29437-29443
43. Nasuda-Kouyama A., Fukuda K., Iio T., and Kouyama T. Effect of a light-induced pH gradient on purple-to-blue and purple-to-red transitions of bacteriorhodopsin. Biochemistry 29 (1990) 6778-6788
44. Balashov S.P., Imasheva E.S., Boichenko V.A., Antón J., Wang J.M., and Lanyi J.K. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309 (2005) 2061-2064
45. Förster T. Transfer mechanisms of electronic excitation. Discuss. Faraday Soc. 27 (1959) 7-17
46. Boichenko V.A., Wang J.M., Antón J., Lanyi J.K., and Balashov S.P. Functions of carotenoids in xanthorhodopsin and archaerhodopsin, from action spectra of photoinhibition of cell respiration. Biochim. Biophys. Acta 1757 (2006) 1649-1656
47. Sugiyama Y., Maeda M., Futai M., and Mukohata Y. Isolation of a gene that encodes a new retinal protein, archaerhodopsin, from Habobacterium sp. aus-1. J. Biol. Chem. 264 (1989) 20859-20862
48. Okumura H., Noritake S., Enami N., Gotoh T., Sugiyama Y., and Kouyama T. Morphological changes in the higher order structure of archaerhodopsin. 4th International Conference on Biological Physics, Kyoto (2001)
49. El-Sayed W.S., Takaichi S., Saida H., Kamekura M., Abu-Shady M., Seki H., and Kuwabara T. Effects of light and low oxygen tension on pigment biosynthesis in Halobacterium salinarum, revealed by a novel method to quantify both retinal and carotenoids. Plant Cell Physiol. 43 (2002) 379-383
50. Cherezov V., Clogston J., Papiz M.Z., and Caffrey M. Room to move: crystallizing membrane proteins in swollen lipidic mesophases. J. Mol. Biol. 357 (2006) 1605-1618
51. Hino T., Kanamori E., Shen J.-R., and Kouyama T. An icosahedral assembly of the light-harvesting chlorophyll a/b protein complex from pea chloroplast thylakoid membranes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 803-809
52. Oesterhelt D., and Stoeckenius W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233 (1971) 149-152
53. 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. Crystallogr. D 35 (2002) 270-273
54. Steller I., Bolotovsky B., and Rossmann M.G. An algorithm for automatic indexing of oscillation images using Fourier analysis. J. Appl. Crystallogr. D 30 (1997) 1036-1040
55. Collaborative Computing Project Number 4. Programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
56. 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 Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
57. McRee D.E. Practical Protein Crystallography (1993), Academic Press, San Diego, CA
58. Yeates T.O. Detecting and overcoming crystal twinning. Methods Enzymol. 276 (1997) 344-358
59. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025