Crystal Structure of the Light-Driven Chloride Pump Halorhodopsin from Natronomonas pharaonis

Journal of Molecular Biology

Volumn 396, Issue 3, 2010, Pages 564-579

  Kouyama, Tsutomu ^a   Kanada, Soun ^a   Takeguchi, Yuu ^a   Narusawa, Akihiro ^a   Murakami, Midori ^a   Ihara, Kunio ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Bacterioruberin; Chloride ion pump; Halorhodopsin; Proton pump; Retinal

Indexed keywords

CHLORIDE ION; HALORHODOPSIN; SCHIFF BASE; WATER; BACTERIORUBERIN; CAROTENOID; CHLORIDE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM; CHLORIDE TRANSPORT; CRYSTAL STRUCTURE; CYTOPLASM; HYDROGEN BOND; NATRONOMONAS PHARAONIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; BIOLOGICAL MODEL; CHEMISTRY; HALOBACTERIUM; METABOLISM; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ARCHAEA; NATRONOMONAS PHARAONIS;

CAROTENOIDS; CHLORIDES; CRYSTALLOGRAPHY, X-RAY; HALOBACTERIACEAE; HALORHODOPSINS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY;

EID: 77949330298     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.11.061     Document Type: Article

References (64)

1. Mukohata Y., Kaji Y. Light-induced ATP synthesis dependent on halorhodopsin-pH regulation. Arch. Biochem. Biophys. 1981, 208:615-617.
2. Schobert B., Lanyi J.K. Halorhodopsin is a light-driven chloride pump. J. Biol. Chem. 1982, 257:10306-10313.
3. Bivin D.B., Stoeckenius W. Photoactive retinal pigments in haloalkaliphilic bacteria. J. Gen. Microbiol. 1986, 132:2167-2177.
4. Váró G. Analogies between halorhodopsin and bacteriorhodopsin. Biochim. Biophys. Acta 2000, 1460:220-229.
5. Essen L.-O. Halorhodopsin: light-driven ion pumping made simple?. Curr. Opin. Struct. Biol. 2002, 12:516-522.
6. Cisneros D., Oesterhelt D., Müller D.J. Probing origins of molecular interactions stabilizing the membrane proteins halorhodopsin and bacteriorhodopsin. Structure 2005, 13:235-242.
7. Peters F., Herbst J., Tittor J., Oesterhelt D., Dillerd R. Primary reaction dynamics of halorhodopsin, observed by sub-picosecond IR-vibrational spectroscopy. Chem. Phys. 2006, 323:109-116.
8. Gruia A.D., Bondar A.N., Smith J.C., Fischer S. Mechanism of a molecular valve in the halorhodopsin chloride pump. Structure 2006, 13:617-627.
9. Guijarro J., Engelhard M., Siebert F. Anion uptake in halorhodopsin from Natronomonas pharaonis studied by FTIR spectroscopy: consequences for the anion transport mechanism. Biochemistry 2006, 45:11578-11588.
10. Magyari K., Simon V., Váró G. The influence of the halide ions on the photochemical reaction cycle of pharaonis halorhodopsin. J. Photochem. Photobiol., B 2006, 82:16-20.
11. Inoue K., Kubo M, Demura M., Kamo N., Terazima M. Reaction dynamics of halorhodopsin studied by time-resolved diffusion. Biophys. J. 2006, 96:3724-3734.
12. - pump activity. Biophys. J. 2007, 92:2559-2569.
13. Gradinaru V., Thompson K.R., Deisseroth K. eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol. 2008, 36:129-139.
14. Nakamura T., Takeuchi S., Shibata M., Demura M., Kandori H., Tahara T. Ultrafast pump-probe study of the primary photoreaction process in pharaonis halorhodopsin: halide ion dependence and isomerization dynamics. J. Phys. Chem. B 2008, 112:12795-12800.
15. Oesterhelt D. Structure and function of halorhodopsin. Isr. J. Chem. 1995, 35:475-494.
16. Ihara K., Narusawa A., Maruyama K., Takeguchi M., Kouyama T. A halorhodopsin-overproducing mutant isolated from an extremely haloalkaliphilic archaeon Natronomonas pharaonis. FEBS Lett. 2008, 582:2931-2936.
17. Avetisyan A.V., Kaulen A.D., Skulachev V.P., Feniouk BA. Photophosphorylation in alkalophilic halobacterial cells containing halorhodopsin: chloride-ion cycle?. Biochemistry (Moscow) 1998, 63:625-628.
18. Falb M., Pfeiffer F., Palm P., Rodewald K., Hickmann V., Tittor J., Oesterhelt D. Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res. 2005, 15:1336-1343.
19. Blanck A., Oesterhelt D. The halo-opsin gene: II. Sequence, primary structure of halorhodopsin and comparison with bacteriorhodopsin. EMBO J. 1987, 6:265-273.
20. Lanyi J.K., Duschl A., Hatfield G.W., May K., Oesterhelt D. The primary structure of a halorhodopsin from Natronobacterium pharaonis. Structural, functional and evolutionary implications for bacterial rhodopsins and halorhodopsins. J. Biol. Chem. 1990, 265:1253-1260.
21. Scharf B., Engelhard M. Blue halorhodopsin from Natronobacterium pharaonis: wavelength regulation by anions. Biochemistry 1994, 33:6387-6393.
22. Ogurusu T., Maeda A., Sasaki N., Yoshizawa T. Light-induced reaction of halorhodopsin prepared under low salt conditions. J. Biochem. (Tokyo) 1981, 90:1267-1273.
23. Duschl A., Lanyi J.K., Zimányi L. Properties and photochemistry of a halorhodopsin from the haloalkaliphile, Natronobacterium pharaonis. J. Biol. Chem. 1990, 265:1261-1267.
24. Schobert B., Lanyi J.K., Oesterhelt D. Effects of anion binding on the deprotonation reactions of halorhodopsin. J. Biol. Chem. 1986, 261:2690-2696.
25. Hackmann C., Guijarro J., Chizhov I., Engelhard M., Rödig M., Siebert F. Static and time-resolved step-scan Fourier transform infrared investigations of the photoreaction of halorhodopsin from Natronobacterium pharaonis: consequences for models of the anion translocation mechanism. Biophys. J. 2001, 81:394-406.
26. Varo G., Zimanyi L., Fan X., Sun X., Needleman R., Lanyi J.K. Photocycle of halorhodopsin from Halobacterium salinarium. Biophys. J. 1995, 68:2062-2072.
27. Kunji E.R.S., von Gronau S., Oesterhelt D., Henderson R. The three-dimensional structure of halorhodopsin to 5Å by electron crystallography: a new unbending procedure for two-dimensional crystals by using a global reference structure. Proc. Natl Acad. Sci. USA 2000, 97:4637-4642.
28. Kolbe M., Besir H., Essen L.R., Oesterhelt D. Structure of the light-driven chloride pump halorhodopsin at 1.8Å resolution. Science 2000, 288:1390-1396.
29. Gmelin W., Zeth K., Efremov R., Heberle J., Tittor J., Oesterhelt D. The crystal structure of the L1 intermediate of halorhodopsin at 1.9Å resolution. Photochem. Photobiol. 2007, 83:369-377.
30. Rüdiger M., Oesterhelt D. Specific arginine and threonine residues control anion binding and transport in the light-driven chloride pump halorhodopsin. EMBO J. 1997, 16:3813-3821.
31. Zimányi L., Lanyi J.K. Fourier transform Raman study of retinal isomeric composition and equilibration in halorhodopsin. J. Phys. Chem. B 1997, 101:1930-1933.
32. Gerscher S., Mylrajan M., Hildebrandt P., Baron M.H., Muller R., Engelhard M. Chromophore-anion interactions in halorhodopsin from Natronobacterium pharaonis probed by time-resolved resonance Raman spectroscopy. Biochemistry 1997, 36:11012-11020.
33. Yoshimura K., Kouyama T. Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J. Mol. Biol. 2008, 375:1267-1281.
34. 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. 1998, 283:463-474.
35. DeLano Scientific (2006). PyMOL version 0.99. http://pymol.sourceforge.net.
36. Yamamoto M., Hayakawa N., Murakami M., Kouyama T. Crystal structures of different sub-states of bacteriorhodopsin's M intermediate at various pH levels. J. Mol. Biol. 2009, 393:559-573.
37. Sasaki T., Kubo M., Kikukawa T., Kamiya M., Aizawa T., Kawano K., Kamo N. Halorhodopsin from Natronomonas pharaonis forms a trimer even in the presence of a detergent, dodecyl-beta-d-maltoside. Photochem. Photobiol. 2008, 85:130-136.
38. Mukohata Y., Ihara K., Tamura T., Sugiyama Y. Halobacterial rhodopsins. J. Biochem. 1999, 125:649-657.
39. Otomo J. Anion selectivity and pumping mechanism of halorhodopsin. Biophys. Chem. 1995, 56:137-141.
40. Shibata M., Saito Y., Demura M., Kandori H. Deprotonation of Glu234 during the photocycle of Natronomonas pharaonis halorhodopsin. Chem. Phys. Lett. 2006, 432:545-547.
41. Grigorieff N., Ceska T.A., Downing K.H., Baldwin J.M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 1996, 259:393-421.
42. Sato H., Takeda K., Tani K., Hino T., Okada T., Kouyama T., et al. Specific lipid-protein interactions in a novel honeycomb lattice structure of bacteriorhodopsin. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55:1251-1256.
43. Balashov S.P., Imasheva E.S., Boichenko V.A., Antón J., Wang J.M., Lanyi J.K. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 2005, 309:2061-2064.
44. Seki S., Sasabe H., Tomioka H. Voltage-dependent absorbance change of carotenoids in halophilic archaebacteria. Biochim. Biophys. Acta 1996, 1284:79-85.
45. Corcelli A., Lobasso S., Colella M., Trotta M., Guerrieri A., Palmisano A. Role of palmitic acid on the isolation and properties of halorhodopsin. Biochim. Biophys. Acta 1996, 1281:173-181.
46. Shibata M., Muneda N., Sasaki T., Shimono K., Kamo N., Demura M., Kandori H. Hydrogen-bonding alterations of the protonated Schiff base and water molecule in the chloride pump of Natronobacterium pharaonis. Biochemistry 2005, 44:12279-12286.
47. Luecke H., Schobert B., Richter H.-T., Cartailler J.-P., Lanyi J.K. Structural changes in bacteriorhodopsin during ion transport at 2angstrom resolution. Science 1999, 286:255-260.
48. Facciotti M.T., Rouhani S., Burkard F.T., Betancourt F.M., Downing K.H., Rose R.B., et al. Structure of an early intermediate in the M-state phase of the bacteriorhodopsin photocycle. Biophys. J. 2001, 81:3442-3455.
49. Takeda K., Matsui Y., Kamiya N., Adachi S., Okumura H., Kouyama T. Crystal structure of the M intermediate of bacteriorhodopsin: allosteric structural changes mediated by sliding movement of a transmembrane helix. J. Mol. Biol. 2004, 341:1023-1037.
50. Cao Y., Váró G., Chang M., Ni B., Needleman R., Lanyi J.K. Water is required for proton transfer from aspartate-96 to the bacteriorhodopsin Schiff base. Biochemistry 1991, 30:10972-10979.
51. Maeda A., Morgan J.E., Gennis R.B., Ebrey T.G. Water as a cofactor in the unidirectional light-driven proton transfer steps in bacteriorhodopsin. Photochem. Photobiol. 2006, 82:1398-1405.
52. Hayakawa N., Kasahara T., Hasegawa D., Yoshimura K., Murakami M., Kouyama T. Effect of xenon binding to a hydrophobic cavity on the proton pumping cycle in bacteriorhodopsin. J. Mol. Biol. 2008, 384:812-823.
53. Hegemann P., Oesterhelt D., Steiner M. The photocycle of the chloride pump halorhodopsin: I. Azide-catalyzed deprotonation of the chromophore is a side reaction of photocycle intermediates inactivating the pump. EMBO J. 1985, 4:2347-2350.
54. Bamberg E., Tittor J., Oesterhelt D. Light-driven proton or chloride pumping by halorhodopsin. Proc. Natl Acad. Sci. USA 1993, 90:639-643.
55. Váró G., Brown L.S., Needleman R., Lanyi J.K. Proton transport by halorhodopsin. Biochemistry 1996, 35:6604-6611.
56. Sato M., Kubo M., Aizawa T., Kamo N., Kikukawa T., Nitta K., Demura M. Role of putative anion-binding sites in cytoplasmic and extracellular channels of Natronomonas pharaonis halorhodopsin. Biochemistry 2005, 44:4775-4784.
57. Sasaki J., Brown L.S., Chon Y.S., Kandori H., Maeda A., Needleman R., Lanyi J.K. Conversion of bacteriorhodopsin into a chloride ion pump. Science 1995, 269:73-75.
58. Dér A., Szaraz S., Tóth-Boconadi R., Tokaji Z., Keszthelyi L., Stoeckenius W. Alternative translocation of protons and halide ions by bacteriorhodopsin. Proc. Natl Acad. Sci. USA 1991, 88:4751-4755.
59. Kouyama T., Nishikawa T., Tokuhisa T., 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. 2003, 335:531-546.
60. Sakai K., Matsui Y., Kouyama T., Shiro Y., Adachi S. Optical monitoring of freeze-trapped reaction intermediates in protein crystals: a microspectrophotometer for cryogenic protein crystallography. J. Appl. Crystallogr. 2002, 35:270-273.
61. Steller I., Bolotovsky B., Rossmann M.G. An algorithm for automatic indexing of oscillation images using Fourier analysis. J. Appl. Crystallogr. 1997, 30:1036-1040.
62. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
63. Brünger A.T., Adams P.D., Glore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR System (CNS): a new software system for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1998, 54:905-921.
64. McRee D.E. Practical Protein Crystallography 1993, Academic Press, San Diego, CA.