Effect of chloride binding on the thermal trimer-monomer conversion of halorhodopsin in the solubilized system

Biochemistry

Volumn 48, Issue 51, 2009, Pages 12089-12095

  Sasaki, Takanori ^a,b   Aizawa, Tomoyasu ^a   Kamiya, Masakatsu ^a   Kikukawa, Takashi ^a   Kawano, Keiichi ^a   Kamo, Naoki ^c   Demura, Makoto ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b MEIJI UNIVERSITY   (Japan)

^c MATSUYAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE BINDING; DETERGENT CONCENTRATIONS; DISSOCIATION CONSTANT; HALORHODOPSIN; HILL COEFFICIENT; HOMOTRIMERS; INTERMOLECULAR INTERACTIONS; MONOMER CONVERSIONS; PHARAONIS; SLOW COMPONENT; SOLUBILIZED SYSTEM; STRUCTURAL STABILITIES; THERMAL DISSOCIATION; TRIMER DISSOCIATION; TWO-COMPONENT;

ACTIVATION ENERGY; BINDING ENERGY; BLEACHING; CHLORINE COMPOUNDS; CHROMATOGRAPHIC ANALYSIS; CLEANING; CONTROL SURFACES; CONTROL SYSTEM STABILITY; ISOTHERMS; MONOMERS; PUMPS; SIZE EXCLUSION CHROMATOGRAPHY; STABILITY;

DISSOCIATION;

CHLORIDE ION; HALORHODOPSIN; MONOMER;

ARCHAEBACTERIUM; ARTICLE; CHLORIDE PUMP; DISSOCIATION CONSTANT; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; HEAT SENSITIVITY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURFACE PROPERTY;

ARCHAEAL PROTEINS; BINDING SITES; CHLORIDES; HALOBACTERIACEAE; HALORHODOPSINS; HOT TEMPERATURE; KINETICS; PROTEIN BINDING; PROTEIN STABILITY; RECOMBINANT PROTEINS; SOLUBILITY;

NATRONOMONAS PHARAONIS;

EID: 73149094722     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901380c     Document Type: Article

References (40)

1. Lanyi, J. K. (1990) Halorhodopsin, a light-driven electrogenic chloride-transport system. Physiol. Rev. 70, 319-330.
2. Matsuno-Yagi, A., and Mukohata, Y. (1980) ATP synthesis linked to light-dependent proton uptake in a red mutant strain of Halobacterium lacking bacteriorhodopsin. Arch. Biochem. Biophys. 199, 297-303.
3. Váró, G., Brown, L. S., Sasaki, J., Kandori, H., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. 1.The photochemical cycle. Biochemistry 34, 14490-14499.
4. 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.
5. 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.
6. Shimono, K., Iwamoto, M., Sumi, M., and Kamo, N. (1997) Functional expression of pharaonis phoborhodopsin in Escherichia coli. FEBS Lett. 420, 54-56.
7. 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.
8. 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 anionuptake process during the photocycle. Biochemistry 41, 2452-2458.
9. Sato, M., Kubo, M., Aizawa, T., Kamo, N., Kikukawa, T., Nitta, K., and Demura, M. (2005) Role of putative anion-binding sites in cytoplasmic and extracellular channels of Natronomonas pharaonis halorhodopsin. Biochemistry 44, 4775-4784.
10. - Circulation within the Extracellular Channel. Photochem. Photobiol. 83, 293-302.
11. Sato, M., Kikukawa, T., Araiso, 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.
12. 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.
13. Shibata, M., Muneda, N., Sasaki, T., Shimono, K., Kamo, N., Demura, M., and Kandori, H. (2005) Hydrogen-Bonding Alterations of the Protonated Schiff Base and Water Molecule in the Chloride Pump of Natronobacterium pharaonis. Biochemistry 44, 12279-12286.
14. Inoue, K., Kubo, M., Demura, M., Kamo, N., and Terazima, M. (2009) Reaction dynamics of halorhodopsin studied by time-resolved diffusion method. Biophys. J. 96, 3724-3734.
15. Kubo, M., Kikukawa, T., Miyauchi, S., Seki, A., Kamiya, M., Aizawa, T., Kawano, K., Kamo, N., and Demura, M. (2009) Role of Arg123 in light-driven anion pump mechanisms of pharaonis halorhodopsin. Photochem. Photobiol. 85, 547-555.
16. 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.
17. Scharf, B., and Engelhard, M. (1994) Blue halorhodopsin from Natronobacterium pharaonis: Wavelength regulation by anions. Biochemistry 33, 6387-6393.
18. Mevorat-Kaplan, K., Brumfeld, V., Engelhard, M., and Sheves, M.(2006) The protonated Schiff base of halorhodopsin from Natronobacterium pharaonis is hydrolyzed at elevated temperatures. Photochem. Photobiol. 82, 1414-1421.
19. Okuno, D., Asaumi, M., and Muneyuki, E. (2003) Chloride concentration dependency of the electrogenic activity of halorhodopsin. Biochemistry 38, 5422-5429.
20. Kalaidzidis, I. V., and Kalaidzidis, Y. L. (2003) Occupancy of two primary chloride-binding sites in Natronobacterium pharaonis halorhodopsin is a necessary condition for active anion transport. Biochemistry (Moscow, Russ. Fed.) 68, 354-358.
21. Persike, N., Pfeiffer, M., Guckenberger, R., Radmacher, M., and Fritz, M. (2001) Direct observation of different surface structures on high-resolution images of native halorhodopsin. J. Mol. Biol. 310, 773-780.
22. Havelka, W. A., Henderson, R., Heymann, J. A. W., and Oesterhelt, D. (1993) Projection Structure of Halorhodopsin from Halobacterium halobium at 6 Å Resolution Obtained by Electron Cryo-microscopy. J. Mol. Biol. 234, 837-846.
23. Sasaki, T., Kubo, M., Kikukawa, T., Kamiya, M., Aizawa, T., Kawano, K., Kamo, N., and Demura, M. (2009) Halorhodopsin from Natronomonas pharaonis forms a trimer even in the presence of a detergent, dodectyl-β-D- maltoside. Photochem. Photobiol. 85, 130-136.
24. Karnaukhova, E., Vasileiou, C., Wang, A., Berova, N., Nakanishi, K., and Borhan, B. (2006) Circular dichroism of heterochromophoric and partially regenerated purple membrane: Search for exciton coupling. Chirality 18, 72-83.
25. Hasselbacher, C. A., Spudich, J. L., and Dewey, T. G. (1988) Circular dichroism of halorhodopsin: Comparison with bacteriorhodopsin and sensory rhodopsin. Biochemistry 27, 2540-2546.
26. Dencher, N. A., and Heyn, M. P. (1982) Preparation and properties of monomeric bacteriorhodopsin. Methods Enzymol. 88, 5-10.
27. Duschl, A., McCloskey, M. A., and Lanyi, J. K. (1988) Functional reconstitution of halorhodopsin. Properties of halorhodopsin-containing proteoliposomes. J. Biol. Chem. 263, 17016-17022.
28. Sasaki, T., Sonoyama, M., Demura, M., and Mitaku, S. (2005) Photobleaching of bacteriorhodopsin solubilized with Triton X-100. Photochem. Photobiol. 81, 1131-1137.
29. Zhang, F., Wang, L.-P., Brauner, M., Liewald, J. F., Kay, K., Natalie, W., Wood, P. G., Bamberg, E., Nagel, G., Gottschalk, A., and Deisseroth, K. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639.
30. - pump activity. Biophys. J. 92, 2559-2569.
31. Zhang, N., and Li, L. (2004) Effects of common surfactants on protein digestion and MALDI MS analysis of the digested peptides using two-layer sample preparation. Rapid Commun. Mass Spectrom. 18, 889-896.
32. Kubo, M., Sato, M., Aizawa, T., Kojima, C., Kamo, N., Mizuguchi, M., Kawano, K., and Demura, M. (2005) Dissociation and bleaching of chloride-free pharaonis halorhodopsin by octyl-β-glucoside. Biochemistry 44, 12923-12931.
33. Lanyi, J. K., Duschl, A., Váro, G., and Zimányi, L. (1990) Anion binding to the chloride pump, halorhodopsin, and its implications for the transport mechanism. FEBS Lett. 265, 1-6.
34. Gmelin, W., Zeth, K., Efremov, R., Heberle, J., Tittor, J., and Oesterhelt, D. (2007) The crystal structure of the L1 intermediate of halorhodopsin at 1.9 angstroms resolution. Photochem. Photobiol. 83, 369-377.
35. Okumura, H., Murakami, M., and Kouyama, T. (2005) Crystal structures of acid blue and alkaline purple forms of bacteriorhodopsin. J. Mol. Biol. 351, 481-495.
36. Iwamoto, M., Furutani, Y., Sudo, Y., Shimono, K., Kandori, H., and Kamo, N. (2002) Role of Asp193 in chromophore-protein interaction of pharaonis phoborhodopsin (sensory rhodopsin II). Biophys. J. 83, 1130-1135.
37. 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.
38. Ikeura, Y., Shimono, K., Iwamoto, M., Sudo, Y., and Kamo, N. (2003) Arg-72 of pharaonis phoborhodopsin (sensory rhodopsin II) is important for the maintenance of the protein structure in the solubilized states. Photochem. Photobiol. 77, 96-100.
39. Yokoyama, Y., Sonoyama, M., and Mitaku, S. (2004) Inhomogeneous stability of bacteriorhodopsin in purple membrane against photobleaching at high temperature. Proteins 54, 442-454.
40. Mukai, Y., Kamo, N., and Mitaku, S. (1999) Light-induced denaturation of bacteriorhodopsin solubilized by octyl-β-glucoside. Protein Eng. 12, 755-759.