Role of putative anion-binding sites in cytoplasmic and extracellular channels of Natronomonas pharaonis halorhodopsin

Biochemistry

Volumn 44, Issue 12, 2005, Pages 4775-4784

  Sato, Maki ^a   Kubo, Megumi ^a   Aizawa, Tomoyasu ^a   Kamo, Naoki ^a   Kikukawa, Takashi ^a   Nitta, Katsutoshi ^a   Demura, Makoto ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; AMINO ACIDS; ARGON; BONDING; CHLORINE COMPOUNDS; ENZYMES;

ANION BINDING; CYTOPLASMIC (CP) CHANNELS; EXTRACELLULAR (EC) CHANNELS; PHOTOCYCLES;

NEGATIVE IONS;

CHLORIDE CHANNEL; HALORHODOPSIN;

ADSORPTION KINETICS; ARTICLE; BINDING AFFINITY; BINDING SITE; CHLORIDE TRANSPORT; CIRCULAR DICHROISM; CYTOPLASM; ION TRANSPORT; MEMBRANE CHANNEL; MUTATION; NATRONOBACTERIUM PHARAONIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIONS; ARGININE; BINDING SITES; CHLORIDE CHANNELS; CHLORIDES; CIRCULAR DICHROISM; CYTOPLASM; EXTRACELLULAR FLUID; HALORHODOPSINS; LYSINE; MUTAGENESIS, SITE-DIRECTED; NATRONOBACTERIUM; PHOTOLYSIS; SERINE; SPECTROPHOTOMETRY; THREONINE; TITRIMETRY;

EID: 15444378199     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047500f     Document Type: Article

References (56)

1. Matsuno-Yagi, A., and Mukohata, Y. (1980) ATP synthesis linked to light-dependent proton uptake in a rad mutant strain of Halobacterium lacking bacteriorhodopsin, Arch. Biochem. Biophys. 199, 297-303.
2. Mukohata, Y., Ihara, K., Tamura, T., and Sugiyama, Y. (1999) Halobacterial rhodopsins, J. Biochem. 125, 649-657.
3. Oesterhelt, D. (1995) Structure and function of halorhodopsin, Isr. J. Chem. 35, 475-494.
4. Schobert, B., and Lanyi, J. K. (1982) Halorhodopsin is a light-driven chloride pump, J. Biol. Chem. 257, 10306-10313.
5. Váró, G. (2000) Analogies between halorhodopsin and bacteriorhodopsin, Biochim. Biophys. Acta 1460, 220-229.
6. Oesterhelt, D., and Stoeckenius, W. (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium, Nat. New Biol. 233, 149-152.
7. Lanyi, J. K. (2004) Bacteriorhodopsin, Annu. Rev. Physiol. 66, 665-688.
8. Haupts, U., Tittor, J., and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: Progress in understanding the molecule, Annu. Rev. Biophys. Biomol. Struct. 28, 367-399.
9. Booth, P. J., Templer, R. H., Curran, A. R., and Allen, S. J. (2001) Can we identify the forces that drive the folding of integral membrane proteins? Biochem. Soc. Trans. 29, 408-413.
10. Oesterhelt, D., Tittor, J., and Bamberg, E. (1992) A unifying concept for ion translocation by retinal proteins, J. Bioenerg. Biomembr. 24, 181-191.
11. Oesterhelt, D. (1998) The structure and mechanism of the family of retinal proteins from halophilic archaea, Curr. Opin. Struct. Biol. 8, 489-500.
12. Lanyi, J. K. (1997) Mechanism of ion transport across membranes. Bacteriorhodopsin as a prototype for proton pumps, J. Biol. Chem. 272, 31209.
13. Lozier, R. H., Bogomolni, R. A., and Stoeckenius, W. (1975) Bacteriorhodopsin: A light-driven proton pump in Halobacterium halobium, Biophys. J. 15, 955-962.
14. Balashov, S. P., Lu, M., Imasheva, E. S., Govindjee, R., Ebrey, T. G., Othersen, B., Chen, Y., Crouch, R. K., and Menick, D. R. (1999) The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH, Biochemistry 38, 2026-2039.
15. Luecke, H., Schobert, B., Richter, H. C., Cartailler, J. P., and Lanyi, J. K. Structure of bacteriorhodopsin at 1.55 Å resolution, J. Mol. Biol. 291, 899-911.
16. Takeda, K., Matsui, Y., Kamiya, N., Adachi, S., Okumura, H., and Kouyama, T. (2004) Crystal structure of the M intermediate of bacteriorhodopsin: Allosteric structural changes mediated by sliding movement of a transmembrane helix, J. Mol. Biol. 341, 1023-1037.
17. Neutze, R., Pebay-Peyroula, E., Edman, K., Royant, A., Navarro, J., and Landau, E. M. (2002) Bacteriorhodopsin: A high-resolution structural view of vectorial proton transport, Biochim. Biophys. Acta 1565, 144-167.
18. Schobert, B., Brown, L. S., and Lanyi, J. K. (2003) 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, 553-570.
19. Váró, G., Needleman, R., and Lanyi, J. K. (1995) Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. 2. Chloride release and uptake, protein conformation change, and thermodynamics, Biochemistry 34, 14500-14507.
20. Chizhov, I., and Engelhard, M. (2001) Temperature and halide dependence of the photocycle of halorhodopsin from Natronobacterium pharaonis, Biophys. J. 81, 1600-1612.
21. Váró, G., Zimányi, L., Fan, X., Sun, L., Needleman, R., and Lanyi, J. K. (1995) Photocycle of halorhodopsin from Halobacterium salinarium. Biophys. J. 68, 2062-2072.
22. Rüdiger, M., and Oesterhelt, D. (1997) Specific arginine and threonine residues control anion binding and transport in the light-driven chloride pump halorhodopsin, EMBO J. 16, 3813-3821.
23. --dependent photovoltage responses of bacteriorhodopsin: Comparison of the D85T and D85S mutants and wild-type acid purple form, FEBS Lett. 418, 239-242.
24. Paula, S., Tittor, J., and Oesterhelt, D. (2001) Roles of cytoplasmic arginine and threonine in chloride transport by the bacteriorhodopsin mutant D85T, Biophys. J. 80, 2386-2395.
25. Sasaki, J., Brown, L. S., Chon, Y. S., Kandori, H., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Conversion of bacteriorhodopsin into a chloride ion pump, Science 269, 73-75.
26. Kolbe, M., Besir, H., Essen, L. O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution, Science 288, 1390-1396.
27. Essen, L. O. (2002) Halorhodopsin: Light-driven ion pumping made simple? Curr. Opin. Struct. Biol. 12, 516-522.
28. Pebay-Peyroula, E., Rummel, G., Rosenbusch, J. P., and Landau, E. M. (1997) X-ray structure of bacteriorhodopsin at 2.5 Å from microcrystals grown in lipidic cubic phases, Science 277, 1676-1681.
29. 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.
30. Luecke, H., Schobert, B., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Crystal structure of sensory rhodopsin II at 2.4 Å: Insights into color tuning and transducer interaction, Science 293, 1499-1503.
31. Otomo, J. (1996) Influence exercised by histidine-95 on chloride transport and the photocycle in halorhodopsin, Biochemistry 35, 6684-6689.
32. Otomo, J., Tomioka, H., and Sasabe, H. (1992) Properties and the primary structure of a new halorhodopsin from halobacterial strain mex, Biochim. Biophys. Acta 1112, 7-12.
33. Soppa, J., Duschl, J., and Oesterhelt, D. (1993) Bacterioopsin, haloopsin, and sensory opsin I of the halobacterial isolate Halobacterium sp. strain SG1: Three new members of a growing family, J. Bacteriol. 175, 2720-2726.
34. Ihara, K., Umemura, T., Katagiri, I., Kitajima-Ihara, T., Sugiyama, Y., Kimura, Y., and Mukohata, Y. (1999) Evolution of the archaeal rhodopsins: Evolution rate changes by gene duplication and functional differentiation, J. Mol. Biol. 285, 163-174.
35. Bivin, D. B., and Stoeckenius, W. (1986) Photoactive retinal pigments in haloalkaliphilic bacteria, J. Gen. Micrabiol. 132, 2167-2177.
36. Váró, G., Brown, L. S., Sasaki, H., Kandori, H., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. I. The photochemical cycle, Biochemistry 34, 14490-14499.
37. Duschl, A., Lanyi, J. K., and Zimányi, L. (1990) Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis, J. Biol. Chem. 265, 1261-1267.
38. Shimono, K., Iwamoto, M., Sumi, M., and Kamo, N. (1997) Functional expression of pharaonis phoborhodopsin in Escherichia coli, FEBS Lett. 420, 54-56.
39. Hohenfeld, I. P., Wegener, A. A., and Engelhard, M. (1999) Purification of histidine tagged bacteriorhodopsin, pharaonis halorhodopsin and pharaonis sensory rhodopsin II functionally expressed in Escherichia coli, FEBS Lett. 442, 198-202.
40. Sato, M., Kanamori, T., Kamo, N., Demura, M., and Nitta, K. (2002) Stopped-flow analysis on anion binding to blue-form halorhodopsin from Natronobacterium pharaonis: Comparison with the anion-uptake process during the photocycle, Biochemistry 41, 2452-2458.
41. Sato, M., Kikukawa, T., Asairo, T., Okita, H., Shimono, K., Kamo, N., Demura, M., and Nitta, K. (2003) Roles of Ser130 and Thr126 in chloride binding and photocycle of pharaonis halorhodopsin, J. Biochem. 134, 151-158.
42. Scharf, B., and Engelhard, M. (1994) Blue halorhodopsin from Natronobacterium pharaonis: Wavelength regulation by anions, Biochemistry 33, 6387-6393.
43. Takao, K., Kikukawa, T., Araiso, T., and Kamo, N. (1998) Azide accelerates the decay of M-intermediate of pharaonis phoborhodopsin, Biophys. Chem. 73, 145-153.
44. Birge, R. R. (1990) Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin, Biochim. Biophys. Acta 1016, 293-327.
45. Sato, M., Kikukawa, T., Araiso, T., Okita, H., Shimono, K., Kamo, N., Demura, M., and Nitta, K. (2003) Ser-130 of Natronobacterium pharaonis halorhodopsin is important for the chloride binding, Biophys. Chem. 104, 209-216.
46. Hasselbacher, C. A., Spudich, J. L., and Dewey, T. G. (1988) Circular dichroism of halorhodopsin: Comparison with bacteriorhodopsin and sensory rhodopsin I, Biochemistry 27, 2540-2546.
47. Dencher, N. A., and Heyn, M. P. (1982) Preparation and properties of monomeric bacteriorhodopsin, Methods Enzymol. 88, 5-10.
48. Gottschalk, M., Dencher, N. A., and Halle, B. (2001) Microsecond exchange of internal water molecules in bacteriorhodopsin, J. Mol. Biol. 311, 605-621.
49. Ogurusu, T., Maeda, A., and Yoshida, T. (1984) Absorption spectral properties of purified halorhodopsin, J. Biochem. 95, 1073-1082.
50. Subramaniam, S., and Henderson, R. (2000) Molecular mechanism of vectorial proton translocation by bacteriorhodopsin, Nature 406, 653-657.
51. Klare, J. P, Bordignon, E., Engelhard, M., and Steinhoff, H. J. (2004) Sensory rhodopsin II and bacteriorhodopsin: Light activated helix F movement, Photochem. Photobiol. Sci. 3, 543-547.
52. Radzwill, N., Gerwert, K., and Steinhoff, H. J. (2001) Time-resolved detection of transient movement of helices F and G in doubly spin-labeled bacteriorhodopsin, Biophys. J. 80, 2856-2866.
53. Sass, H. J., Buldt, G., Gessenich, R., Hehn, D., Neff, D., Schlesinger, R., Berendzen, J., and Ormos, P. (2000) Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin, Nature 406, 649-653.
54. Vonck, J. (2000) Structure of the bacteriorhodopsin mutant F219L N intermediate revealed by electron crystallography, EMBO J. 19, 2152-2160.
55. Oka, T., Yagi, N., Tokunaga, F., and Kataoka, M. (2002) Time-resolved X-ray diffraction reveals movement of F helix of D96N bacteriorhodopsin during M-MN transition at neutral pH, Biophys. J. 82, 2610-2616.
56. Hackmann, C., Guijarro, J., Chizhov, I., Engelhard, M., Rödig, C., and Siebert, F. (2001) 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. 81, 394-406.