Complex Formation and Light Activation in Membrane-Embedded Sensory Rhodopsin II as Seen by Solid-State NMR Spectroscopy

Structure

Volumn 18, Issue 3, 2010, Pages 293-300

  Etzkorn, Manuel ^a   Seidel, Karsten ^a   Li, Lin ^b   Martell, Swetlana ^b   Geyer, Matthias ^b   Engelhard, Martin ^b   Baldus, Marc ^a,c  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

AMINO ACID; RETINAL; RHODOPSIN;

ARCHAEBACTERIUM; ARTICLE; BINDING SITE; CELL MEMBRANE; COMPLEX FORMATION; LIGHT; NATRONOMONAS PHARAONIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLASTICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SOLID STATE; X RAY ANALYSIS;

AMINO ACID SEQUENCE; HALORHODOPSINS; MOLECULAR SEQUENCE DATA; NATRONOBACTERIUM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SENSORY RHODOPSINS; SEQUENCE ALIGNMENT;

NATRONOMONAS PHARAONIS;

EID: 77649091074     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.01.011     Document Type: Article

References (40)

1. Ader C., Schneider R., Hornig S., Velisetty P., Wilson E.M., Lange A., Giller K., Ohmert I., Martin-Eauclaire M.-F., Trauner D., et al. A structural link between inactivation and block of a K+ channel. Nat. Struct. Mol. Biol. 15 (2008) 605-612
2. Ader C., Schneider R., Hornig S., Velisetty P., Vardanyan V., Giller K., Ohmert I., Becker S., Pongs O., and Baldus M. Coupling of activation and inactivation gate in a K+-channel: potassium and ligand sensitivity. EMBO J. 28 (2009) 2825-2834
3. Ahuja S., Hornak V., Yan E.C.Y., Syrett N., Goncalves J.A., Hirshfeld A., Ziliox M., Sakmar T.P., Sheves M., Reeves P.J., et al. Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat. Struct. Mol. Biol. 16 (2009) 168-175
4. Andronesi O.C., Becker S., Seidel K., Heise H., Young H.S., and Baldus M. Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy. J. Am. Chem. Soc. 127 (2005) 12965-12974
5. Bergo V.B., Spudich E.N., Spudich J.L., and Rothschild K.J. Active water in protein-protein communication within the membrane: the case of SRII-HtrII signal relay. Biochemistry 48 (2009) 811-813
6. Bloembergen N. On the interaction of nuclear spins in a crystalline lattice. Physica 15 (1949) 386-426
7. Bordignon E., Klare J.P., Doebber M., Wegener A.A., Martell S., Engelhard M., and Steinhoff H.-J. Structural analysis of a HAMP domain: the linker region of the phototransducer in complex with sensory rhodopsin II. J. Biol. Chem. 280 (2005) 38767-38775
8. Bordignon E., Klare J.P., Holterhues J., Martell S., Krasnaberski A., Engelhard M., and Steinhoff H.-J. Analysis of light-induced conformational changes of Natronomonas pharaonis sensory rhodopsin II by time resolved electron paramagnetic resonance spectroscopy. Photochem. Photobiol. 83 (2007) 263-272
9. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
10. Doebber M., Bordignon E., Klare J.P., Holterhues J., Martell S., Mennes N., Li L., Engelhard M., and Steinhoff H.-J. Salt-driven equilibrium between two conformations in the HAMP domain from Natronomonas pharaonis: the language of signal transfer?. J. Biol. Chem. 283 (2008) 28691-28701
11. Edman K., Royant A., Nollert P., Maxwell C.A., Pebay-Peyroula E., Navarro J., Neutze R., and Landau E.M. Early structural rearrangements in the photocycle of an integral membrane sensory receptor. Structure 10 (2002) 473-482
12. Etzkorn M., Böckmann A., Lange A., and Baldus M. Probing molecular interfaces using 2D magic-angle-spinning NMR on protein mixtures with different uniform labeling. J. Am. Chem. Soc. 126 (2004) 14746-14751
13. Etzkorn M., Martell S., Andronesi O.C., Seidel K., Engelhard M., and Baldus M. Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 46 (2007) 459-462
14. Etzkorn M., Kneuper H., Dunnwald P., Vijayan V., Kramer J., Griesinger C., Becker S., Unden G., and Baldus M. Plasticity of the PAS domain and a potential role for signal transduction in the histidine kinase DcuS. Nat. Struct. Mol. Biol. 15 (2008) 1031-1039
15. Fung B.M., Khitrin A.K., and Ermolaev K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 142 (2000) 97-101
16. Goddard, T.D., and Kneller, D.G. (2008). SPARKY 3. (http://www.cgl.ucsf.edu/home/sparky/).
17. Gordeliy V.I., Labahn J., Moukhametzianov R., Efremov R., Granzin J., Schlesinger R., Buldt G., Savopol T., Scheidig A.J., Klare J.P., and Engelhard M. Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex. Nature 419 (2002) 484-487
18. Hohwy M., Rienstra C.M., Jaroniec C.P., and Griffin R.G. Fivefold symmetric homonuclear dipolar recoupling in rotating solids: application to double quantum spectroscopy. J. Chem. Phys. 110 (1999) 7983-7992
19. Hulko M., Berndt F., Gruber M., Linder J.U., Truffault V., Schultz A., Martin J., Schultz J.E., Lupas A.N., and Coles M. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126 (2006) 929-940
20. Khursigara C.M., Wu X., Zhang P., Lefman J., and Subramaniam S. Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors. Proc. Natl. Acad. Sci. USA 105 (2008) 16555-16560
21. Klare J.P., Gordeliy V.I., Labahn J., Buldt G., Steinhoff H.J., and Engelhard M. The archaeal sensory rhodopsin II/transducer complex: a model for transmembrane signal transfer. FEBS Lett. 564 (2004) 219-224
22. Klare J.P., Bordignon E., Doebber M., Fitter J., Kriegsmann J., Chizhov I., Steinhoff H.J., and Engelhard M. Effects of solubilization on the structure and function of the sensory rhodopsin II/transducer complex. J. Mol. Biol. 356 (2006) 1207-1221
23. Klare J.P., Chizhov I., and Engelhard M. Microbial rhodopsins: scaffolds for ion pumps, channels, and sensors. Results Probl. Cell Differ. 45 (2008) 73-122
24. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., et al. Clustal W and clustal X version 2.0. Bioinformatics 23 (2007) 2947-2948
25. Luca S., Filippov D.V., van Boom J.H., Oschkinat H., de Groot H.J.M., and Baldus M. Secondary chemical shifts in immobilized peptides and proteins: a qualitative basis for structure refinement under magic angle spinning. J. Biomol. NMR 20 (2001) 325-331
26. Luecke H., Schobert B., Lanyi J.K., Spudich E.N., and Spudich J.L. Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction. Science 293 (2001) 1499-1503
27. Mak-Jurkauskas M.L., Bajaj V.S., Hornstein M.K., Belenky M., Griffin R.G., and Herzfeld J. Energy transformations early in the bacteriorhodopsin photocycle revealed by DNP-enhanced solid-state NMR. Proc. Natl. Acad. Sci. USA 105 (2008) 883-888
28. Moukhametzianov R., Klare J.P., Efremov R., Baeken C., Goppner A., Labahn J., Engelhard M., Buldt G., and Gordeliy V.I. Development of the signal in sensory rhodopsin and its transfer to the cognate transducer. Nature 440 (2006) 115-119
29. Neal S., Nip A.M., Zhang H.Y., and Wishart D.S. Rapid and accurate calculation of protein H-1, C-13 and N-15 chemical shifts. J. Biomol. NMR 26 (2003) 215-240
30. Royant A., Nollert P., Edman K., Neutze R., Landau E.M., Pebay-Peyroula E., and Navarro J. X-ray structure of sensory rhodopsin II at 2.1-A resolution. Proc. Natl. Acad. Sci. USA 98 (2001) 10131-10136
31. Sasaki J., and Spudich J.L. Signal transfer in haloarchaeal sensory rhodopsin-transducer complexes. Photochem. Photobiol. 84 (2008) 863-868
32. Sasaki J., Nara T., Spudich E.N., and Spudich J.L. Constitutive activity in chimeras and deletions localize sensory rhodopsin II/HtrII signal relay to the membrane-inserted domain. Mol. Microbiol. 66 (2007) 1321-1330
33. Schneider R., Seidel K., Etzkorn M., Lange A., Becker S., and Baldus M. Probing molecular motion by double-quantum (13C, 13C) solid-state NMR spectroscopy: application to ubiquitin. J. Am. Chem. Soc. 132 (2010) 223-233
34. Seidel K., Lange A., Becker S., Hughes C.E., Heise H., and Baldus M. Protein solid-state NMR resonance assignments from (C-13, C-13) correlation spectroscopy. Phys. Chem. Chem. Phys. 6 (2004) 5090-5093
35. Seidel K., Etzkorn M., Schneider R., Ader C., and Baldus M. Comparative analysis of NMR chemical shift predictions for proteins in the solid phase. Solid State Nucl. Magn. Reson. 35 (2009) 235-242
36. Shaka A.J., Barker P.B., and Freeman R. Computer-optimized decoupling scheme for wideband applications and low-level operation. J. Magn. Reson. 64 (1985) 547-552
37. Sudo Y., and Spudich J.L. Three strategically placed hydrogen-bonding residues convert a proton pump into a sensory receptor. Proc. Natl. Acad. Sci. USA 103 (2006) 16129-16134
38. Sudo Y., Furutani Y., Kandori H., and Spudich J.L. Functional importance of the interhelical hydrogen bond between Thr(204) and Tyr(174) of sensory rhodopsin II and its alteration during the signaling process. J. Biol. Chem. 281 (2006) 34239-34245
39. Wegener A.A., Klare J.P., Engelhard M., and Steinhoff H.J. Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis. EMBO J. 20 (2001) 5312-5319
40. Yang C.-S., Sineshchekov O., Spudich E.N., and Spudich J.L. 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 (2004) 42970-42976