Structural analysis of the phototactic transducer protein HtrII linker region from Natronomonas pharaonis

Biochemistry

Volumn 46, Issue 50, 2007, Pages 14380-14390

  Hayashi, Kokoro ^a   Sudo, Yuki ^b,d   Jee, JunGoo ^a   Mishima, Masaki ^a   Hara, Hideyuki ^c   Kamo, Naoki ^b   Kojima, Chojiro ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c Bruker Corporation   (United States)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

METHYL-ACCEPTING CHEMOTAXIS PROTEINS (MCP); NATRONOMONAS PHARAONIS; PHOTOTAXIS PROTEIN; TRANSMEMBRANE PROTEINS;

BACTERIA; BIOLOGICAL MEMBRANES; MOLECULAR STRUCTURE; PH; SIGNAL TRANSDUCTION;

PROTEINS;

HALOBACTERIAL TRANSDUCER PROTEIN II; HOMODIMER; MEMBRANE PROTEIN; TRYPSIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; CONFORMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; HALOBACTERIACEAE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SENSORY RHODOPSINS;

NATRONOMONAS PHARAONIS;

EID: 37249065137     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701837n     Document Type: Article

References (50)

1. Rudolph, J., Nordmann, B., Storch, K. F., Gruenberg, H., Rodewald, K., and Oesterhelt, D. (1996) A family of halobacterial transducer proteins, FEMS Microbiol. Lett. 139, 161-168.
2. Falke, J. J., and Hazelbauer, G. L. (2001) Transmembrane signaling in bacterial chemoreceptors, Trends Biochem. Sci. 26, 257-265.
3. Rudolph, J., and Oesterhelt, D. (1996) Deletion analysis of the che operon in the archaeon Halobacterium salinarium, J. Mol. Biol. 258, 548-554.
4. Alley, M. R., Maddock, J. R., and Shapiro, L. (1993) Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis, Science 259, 1754-1757.
5. Maddock, J. R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell, Science 259, 1717-1723.
6. Zhang, X. N., Zhu, J., and Spudich, J. L. (1999) The specificity of interaction of archaeal transducers with their cognate sensory rhodopsins is determined by their transmembrane helices, Proc. Natl. Acad. Sci. U.S.A. 96, 857-862.
7. Spudich, J. L., Yang, C. S., Jung, K. H., and Spudich, E. N. (2000) Retinylidene proteins: Structures and functions from archaea to humans, Annu. Rev. Cell Dev. Biol. 16, 365-392.
8. Yan, B., Takahashi, T., Johnson, R., and Spudich, J. L. (1991) Identification of signaling states of a sensory receptor by modulation of lifetimes of stimulus-induced conformations: The case of sensory rhodopsin II, Biochemistry 30, 10686-10692.
9. Klare, J. P., Gordeliy, V. I., Labahn, J., Büldt, G., Steinhoff, H. J., and Engelhard, M. (2004) The archaeal sensory rhodopsin II/transducer complex: A model for transmembrane signal transfer, FEBS Lett. 564, 219-224.
10. Gordeliy, V. I., Labahn, J., Moukhametzianov, R., Efremov, R., Granzin, J., Schlesinger, R., Büldt, G., Savopol, T., Scheidig, A. J., Klare, J. P., and Engelhard, M. (2002) Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex, Nature 419, 484-487.
11. Moukhametzianov, R., Klare, J. P., Efremov, R., Baeken, C., Göppner, A., Labahn, J., Engelhard, M., Büldt, G., and Gordeliy, V. I. (2006) Development of the signal in sensory rhodopsin and its transfer to the cognate transducer, Nature 440, 115-119.
12. Kim, K. K., Yokota, H., and Kim, S. H. (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor, Nature 400, 787-792.
13. Sudo, Y., Okuda, H., Yamabi, M., Fukuzaki, Y., Mishima, M., Kamo, N., and Kojima, C. (2005) Linker region of a halobacterial transducer protein interacts directly with its sensor retinal protein, Biochemistry 44, 6144-6152.
14. Bordignon, E., Klare, J. P., Doebber, M., Wegener, A. A., Martell, S., Engelhard, M., and Steinhoff, H. J. (2005) Structural analysis of a HAMP domain: The linker region of the phototransducer in complex with sensory rhodopsin II, J. Biol. Chem. 280, 38767-38775.
15. Budyak, I. L., Pipich, V., Mironova, O. S., Schlesinger, R., Zaccai, G., and Klein-Seetharaman, J. (2006) Shape and oligomerization state of the cytoplasmic domain of the phototaxis transducer II from Natronobacterium pharaonis, Proc. Natl. Acad. Sci. U.S.A. 103, 15428-15433.
16. Jung, K. H., Spudich, E. N., Trivedi, V. D., and Spudich, J. L. (2001) An archaeal photosignal-transducing module mediates phototaxis in Escherichia coli, J. Bacteriol. 183, 6365-6371.
17. Yang, C. S., and Spudich, J. L. (2001) Light-induced structural changes occur in the transmembrane helices of the Natronobacterium pharaonis HtrII transducer, Biochemistry 40, 14207-14214.
18. Yang, C. S., Sineshchekov, O., Spudich, E. N., and Spudich, J. L. (2004) The cytoplasmic membrane-proximal domain of the HtrII transducer interacts with the E-F loop of photoactivated Natronomonas pharaonis sensory rhodopsin II, J. Biol. Chem. 279, 42970-42976.
19. Umemura, T., Matsumoto, Y., Ohnishi, K., Homma, M., and Kawagishi, I. (2002) Sensing of cytoplasmic pH by bacterial chemoreceptors involves the linker region that connects the membrane-spanning and the signal-modulating helices, J. Biol. Chem. 277, 1593-1598.
20. Appleman, J. A., and Stewart, V. (2003) Mutational analysis of a conserved signal-transducing element: The HAMP linker of the Escherichia coli nitrate sensor NarX, J. Bacteriol. 185, 89-97.
21. Le Moual, H., and Koshland, D. E., Jr. (1996) Molecular Evolution of the C-terminal Cytoplasmic Domain of a Superfamily of Bacterial Receptors Involved in Taxis, J. Mol. Biol. 261, 568-585.
22. Aravind, L., and Ponting, C. P. (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins, FEMS Microbiol. Lett. 176, 111-116.
23. Williams, S. B., and Stewart, V. (1999) Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction, Mol. Microbiol. 33, 1093-1102.
24. Hulko, M., Berndt, F., Gruber, M., Linder, J. U., Truffault, V., Schultz, A., Martin, J., Schultz, J. E., Lupas, A. N., and Coles, M. (2006) The HAMP domain structure implies helix rotation in transmembrane signaling, Cell 126, 929-940.
25. Yao, V. J., and Spudich, J. L. (1992) Primary structure of an archaebacterial transducer, a methyl-accepting protein associated with sensory rhodopsin I, Proc. Natl. Acad. Sci. U.S.A. 89, 11915-11919.
26. Zhang, W., Brooun, A., Mueller, M. M., and Alam, M. (1996) The primary structures of the Archaeon Halobacterium salinarium blue light receptor sensory rhodopsin II and its transducer, a methyl-accepting protein, Proc. Natl. Acad. Sci. U.S.A. 93, 8230-8235.
27. Klare, J. P., Bordignon, E., Doebber, M., Fitter, J., Kriegsmann, J., Chizhov, I., Steinhoff, H. J., and Engelhard, M. (2006) Effects of solubilization on the structure and function of the sensory rhodopsin II/transducer complex, J. Mol. Biol. 356, 1207-1221.
28. Rabenstein, M. D., and Shin, Y. K. (1995) Determination of the distance between two spin labels attached to a macromolecule, Proc. Natl. Acad. Sci. U.S.A. 92, 8239-8243.
29. Altenbach, C., Oh, K. J., Trabanino, R. J., Hideg, K., and Hubbell, W. L. (2001) Estimation of inter-residue distances in spin labeled proteins at physiological temperatures: Experimental strategies and practical limitations, Biochemistry 40, 15471-15482.
30. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Dead-time free measurement of dipole-dipole interactions between electron spins, J. Magn. Reson. 142, 331-340.
31. Sudo, Y., Iwamoto, M., Shimono, K., and Kamo, N. (2001) Pharaonis Phoborhodopsin Binds to its Cognate Truncated Transducer Even in the Presence of a Detergent with a 1:1 Stoichiometry, Photochem. Photobiol. 74, 489-494.
32. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., and Skelton, N. J. (1996) Protein NMR Spectroscopy, Academic Press, San Diego.
33. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293
34. Goddard, T. D., and Kneller, D. G. (1999) SPARKY3, University of California, San Francisco.
35. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
36. Herrmann, T., Güntert, P., and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA, J. Mol. Biol. 319, 209-227.
37. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E. I., DeBolt, S., Ferguson, D., Seibel, G., and Kollman, P. (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules, Comput. Phys. Commun. 91, 1-41.
38. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
39. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55, 29-32.
40. Pfeiffer, M., Rink, T., Gerwert, K., Oesterhelt, D., and Steinhoff, H. J. (1999) Site-directed Spin-labeling Reveals the Orientation of the Amino Acid Side-chains in the E-F Loop of Bacteriorhodopsin, J. Mol. Biol. 287, 163-171.
41. Kandori, H., Shimono, K., Sudo, Y., Iwamoto, M., Shichida, Y., and Kamo, N. (2001) Structural changes of pharaonis phoborhodopsin upon photoisomerization of the retinal chromophore: Infrared spectral comparison with bacteriorhodopsin, Biochemistry 40, 9238-9246.
42. Pannier, M., Veit, S., Schöps, M., Wiesner, U., Jeschke, G., and Spiess, H. W. (2000) Determination of ion cluster sizes and cluster-to-cluster distances in ionomers by four-pulse double electron electron resonance spectroscopy, Macromolecules 33, 7812-7818.
43. Furutani, Y., Kamada, K., Sudo, Y., Shimono, K., Kamo, N., and Kandori, H. (2005) Structural changes of the complex between pharaonis phoborhodopsin and its cognate transducer upon formation of the M photointermediate, Biochemistry 44, 2909-2915.
44. Kishii, R., Falzon, L., Yoshida, T., Kobayashi, H., and Inouye, M. (2007) Structural and functional studies of the HAMP domain of EnvZ, an osmosensing transmembrane histidine kinase in Escherichia coli, J. Biol. Chem. (in press).
45. Hulo, N., Bairoch, A., Bulliard, V., Cerutti, L., De Castro, E., Langendijk-Genevaux, P. S., Pagni, M., and Sigrist, C. J. A. (2006) The PROSITE database, Nucleic Acids Res. 34, D227-D230.
46. Sigrist, C. J. A., Cerutti, L., Hulo, N., Gattiker, A., Falquet, L., Pagni, M., Bairoch, A., and Bucher, P. (2002) PROSITE: A documented database using patterns and profiles as motif descriptors, Briefings Bioinf. 3, 265-274.
47. Gattiker, A., Gasteiger, E., and Bairoch, A. (2002) ScanProsite: A reference implementation of a PROSITE scanning tool, Appl. Bioinf. 1, 107-108.
48. Sigrist, C. J. A., De Castro, E., Langendijk-Genevaux, P. S., Le Saux, V., Bairoch, A., and Hulo, N. (2005) ProRule: A new database containing functional and structural information on PROSITE profiles, Bioinformatics 21, 4060-4066.
49. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol. 234, 779-815.
50. Taniguchi, Y., Ikehara, T., Kamo, N., Yamasaki, H., and Toyoshima, T. (2007) Dynamics of light-induced conformational changes of the phoborhodopsin/transducer complex formed in the n-dodecyl β-D-maltoside micelle, Biochemistry 46, 5349-5357.