Probing a polar cluster in the retinal binding pocket of bacteriorhodopsin by a chemical design approach

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Simón Vázquez, Rosana ^a,b   Domínguez, Marta ^b   Lórenz Fonfría, Víctor A ^a,c   Álvarez, Susana ^b   Bourdelande, José Luís ^a   de Lera, Ángel R ^b   Padrós, Esteve ^a   Perálvarez Marín, Alex ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF VIGO   (Spain)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; APOPROTEIN; BACTERIORHODOPSIN; HYDROCARBON; METHYL GROUP; RETINAL; RETINOID BINDING PROTEIN; THREONINE;

ARTICLE; CHROMATOPHORE; HYDROGEN BOND; LIGHT HARVESTING SYSTEM; NONHUMAN; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN ENGINEERING; SYNTHESIS; WILD TYPE;

ADAPTATION, OCULAR; ASPARTIC ACID; BACTERIORHODOPSINS; BINDING SITES; BIOCHEMISTRY; BIOLOGICAL TRANSPORT; HALOBACTERIUM SALINARUM; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN DENATURATION; PROTEIN STABILITY; RETINALDEHYDE; TEMPERATURE;

EID: 84864557375     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042447     Document Type: Article

References (42)

1. Ritter E, Przybylski P, Brzezinski B, Bartl F, (2009) Schiff Bases in Biological Systems. Current Organic Chemistry 13: 241-249.
2. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK, (1999) Structure of bacteriorhodopsin at 1.55 A resolution. J Mol Biol 291: 899-911.
3. Salom D, Lodowski DT, Stenkamp RE, Le Trong I, Golczak M, et al. (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci U S A 103: 16123-16128.
4. Lodowski DT, Palczewski K, (2009) Chemokine receptors and other G protein-coupled receptors. Curr Opin HIV AIDS 4: 88-95.
5. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, et al. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318: 1258-1265.
6. Kato HE, Zhang F, Yizhar O, Ramakrishnan C, Nishizawa T, et al. (2012) Crystal structure of the channelrhodopsin light-gated cation channel. Nature.
7. Danon A, Stoeckenius W, (1974) Photophosphorylation in Halobacterium halobium. Proc Natl Acad Sci U S A 71: 1234-1238.
8. Subramaniam S, Henderson R, (2000) Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 406: 653-657.
9. Luecke H, Schobert B, Cartailler JP, Richter HT, Rosengarth A, et al. (2000) Coupling photoisomerization of retinal to directional transport in bacteriorhodopsin. J Mol Biol 300: 1237-1255.
10. Henderson R, Unwin PN, (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257: 28-32.
11. Walz T, Grigorieff N, (1998) Electron Crystallography of Two-Dimensional Crystals of Membrane Proteins. J Struct Biol 121: 142-161.
12. Pebay-Peyroula E, Rummel G, Rosenbusch JP, Landau EM, (1997) X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 277: 1676-1681.
13. Ohno K, Takeuchi Y, Yoshida M, (1977) Effect of light-adaptation on the photoreaction of bacteriorhodopsin from Halobacterium halobium. Biochim Biophys Acta 462: 575-582.
14. Lanyi JK, (2006) Proton transfers in the bacteriorhodopsin photocycle. Biochim Biophys Acta 1757: 1012-1018.
15. Oesterhelt D, Meentzen M, Schuhmann L, (1973) Reversible dissociation of the purple complex in bacteriorhodopsin and identification of 13-cis and all-trans-retinal as its chromophores. Eur J Biochem 40: 453-463.
16. Lazarova T, Querol E, Padros E, (2009) Coupling between the retinal thermal isomerization and the Glu194 residue of bacteriorhodopsin. Photochem Photobiol 85: 617-623.
17. Aharoni A, Ottolenghi M, Sheves M, (2001) Retinal isomerization in bacteriorhodopsin is controlled by specific chromophore-protein interactions. A study with noncovalent artificial pigments. Biochemistry 40: 13310-13319.
18. Balashov SP, Govindjee R, Kono M, Imasheva E, Lukashev E, et al. (1993) Effect of the arginine-82 to alanine mutation in bacteriorhodopsin on dark adaptation, proton release, and the photochemical cycle. Biochemistry 32: 10331-10343.
19. Peralvarez A, Barnadas R, Sabes M, Querol E, Padros E, (2001) Thr90 is a key residue of the bacteriorhodopsin proton pumping mechanism. FEBS Lett 508: 399-402.
20. Peralvarez-Marin A, Marquez M, Bourdelande JL, Querol E, Padros E, (2004) Thr-90 plays a vital role in the structure and function of bacteriorhodopsin. J Biol Chem 279: 16403-16409.
21. Joh NH, Min A, Faham S, Whitelegge JP, Yang D, et al. (2008) Modest stabilization by most hydrogen-bonded side-chain interactions in membrane proteins. Nature 453: 1266-1270.
22. Peralvarez-Marin A, Lorenz-Fonfria VA, Bourdelande JL, Querol E, Kandori H, et al. (2007) Inter-helical hydrogen bonds are essential elements for intra-protein signal transduction: the role of Asp115 in bacteriorhodopsin transport function. J Mol Biol 368: 666-676.
23. Corriu RJP, Masse JP, (1972) Activation of Grignard Reagents by Transition-metal Complexes. A New and Simple Synthesis of trans-Stilbenes and Polyphenyls. J Chem Soc Chem Commun. pp. 144.
24. Tamao K, Sumitani K, Kumada M, (1972) Selective carbon-carbon bond formation by cross-coupling of Grignard reagents with organic halides. Catalysis by nickel-phosphine complexes. Journal of the American Chemical Society 94: 4374-4376.
25. Alvarez R, Iglesias B, de Lera AR, (1999) Stereocontrolled synthesis of retinoids functionalized at C-13 by suzuki coupling reactions. Tetrahedron 55: 13779-13790.
26. Zhang H, Lerro KA, Takekuma S, Baek D-J, Moquin-Pattey C, et al. (1994) Orientation of the Retinal 9-Methyl Group in Bacteriorhodopsin As Studied by Photoaffinity Labeling. Journal of the American Chemical Society 116: 6823-6831.
27. Oesterhelt D, Schuhmann L, (1974) Reconstitution of bacteriorhodopsin. FEBS Lett 44: 262-265.
28. Lopez S, Rodriguez V, Montenegro J, Saa C, Alvarez R, et al. (2005) Synthesis of N-heteroaryl retinals and their artificial bacteriorhodopsins. Chembiochem 6: 2078-2087.
29. Mowery PC, Lozier RH, Chae Q, Tseng YW, Taylor M, et al. (1979) Effect of acid pH on the absorption spectra and photoreactions of bacteriorhodopsin. Biochemistry 18: 4100-4107.
30. Sanz C, Marquez M, Peralvarez A, Elouatik S, Sepulcre F, et al. (2001) Contribution of extracellular Glu residues to the structure and function of bacteriorhodopsin. Presence of specific cation-binding sites. J Biol Chem 276: 40788-40794.
31. Scherrer P, Mathew MK, Sperling W, Stoeckenius W, (1989) Retinal isomer ratio in dark-adapted purple membrane and bacteriorhodopsin monomers. Biochemistry 28: 829-834.
32. Trissl H-W, Gartners W, (1987) Rapid Charge Separation and Bathochromic Absorption Shift of Flash-Excited Bacteriorhodopsins Containing 1 3-Cis or All-Trans Forms of Substituted Retinals. Biochemistry 26: 751-758.
33. Subramaniam S, Greenhalgh DA, Khorana HG, (1992) Aspartic acid 85 in bacteriorhodopsin functions both as proton acceptor and negative counterion to the Schiff base. J Biol Chem 267: 25730-25733.
34. Gärtner W, Oesterhelt D, Vogel J, Maurer R, Schneider S, (1988) Photocycles of Bacteriorhodopsins Containing 13-Alkyl-Substituted Retinals. Biochemistry 27: 6.
35. Gergely C, Ganea C, Varo G, (1994) Combined optical and photoelectric study of the photocycle of 13-cis bacteriorhodopsin. Biophys J 67: 855-861.
36. Brown MF, Heyn MP, Job C, Kim S, Moltke S, et al. (2007) Solid-state 2H NMR spectroscopy of retinal proteins in aligned membranes. Biochim Biophys Acta 1768: 2979-3000.
37. Subramaniam S, Greenhalgh DA, Rath P, Rothschild KJ, Khorana HG, (1991) Replacement of leucine-93 by alanine or threonine slows down the decay of the N and O intermediates in the photocycle of bacteriorhodopsin: implications for proton uptake and 13-cis-retinal-all-trans-retinal reisomerization. Proc Natl Acad Sci U S A 88: 6873-6877.
38. Toth-Boconadi R, Keszthelyi L, Stoeckenius W, (2003) Photoexcitation of the O-intermediate in bacteriorhodopsin mutant L93A. Biophys J 84: 3857-3863.
39. Curran AR, Engelman DM (2003) Sequence motifs, polar interactions and conformational changes in helical membrane proteins Current Opinion in Structural Biology 13.
40. Hiraki K, Hamanaka T, Zheng XG, Shinada T, Kim JM, et al. (2002) Bacteriorhodopsin analog regenerated with 13-desmethyl-13-iodoretinal. Biophys J 83: 3460-3469.
41. Gillespie NB, Ren L, Ramos L, Daniell H, Dews D, et al. (2005) Characterization and photochemistry of 13-desmethyl bacteriorhodopsin. J Phys Chem B 109: 16142-16152.
42. Peralvarez-Marin A, Lorenz-Fonfria VA, Simon-Vazquez R, Gomariz M, Meseguer I, et al. (2008) Influence of proline on the thermostability of the active site and membrane arrangement of transmembrane proteins. Biophys J 95: 4384-4395.