Salt effects on the conformational stability of the visual G-protein-coupled receptor rhodopsin

Biophysical Journal

Volumn 101, Issue 11, 2011, Pages 2798-2806

  Reyes Alcaraz, Arfaxad ^a   Martínez Archundia, Marlet ^a   Ramon, Eva ^a   Garriga, Pere ^a  

^a UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; EYE PROTEIN; INORGANIC SALT; POTASSIUM CHLORIDE; RHODOPSIN; SODIUM CHLORIDE;

ANIMAL; ARTICLE; CATTLE; CHEMISTRY; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; DRUG EFFECT; HYDROLYSIS; KINETICS; METABOLISM; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; TEMPERATURE;

AMMONIUM CHLORIDE; ANIMALS; CALORIMETRY, DIFFERENTIAL SCANNING; CATTLE; CIRCULAR DICHROISM; EYE PROTEINS; HYDROLYSIS; KINETICS; POTASSIUM CHLORIDE; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; RHODOPSIN; SALTS; SODIUM CHLORIDE; TEMPERATURE;

EID: 82955194481     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.09.049     Document Type: Article

References (44)

1. V.M. Unger, and G.F.X. Schertler Low resolution structure of bovine rhodopsin determined by electron cryo-microscopy Biophys. J. 68 1995 1776 1786
2. K. Palczewski, and T. Kumasaka M. Miyano Crystal structure of rhodopsin: a G protein-coupled receptor Science 289 2000 739 745
3. 2-adrenergic G-protein coupled receptor Science 318 2007 1258 1265
4. 1-adrenergic G-protein-coupled receptor Nature 454 2008 486 491
5. 2A adenosine receptor bound to an antagonist Science 322 2008 1211 1217
6. B. Wu, and E.Y.T. Chien R.C. Stevens Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists Science 330 2010 1066 1071
7. C.L. Malin, and H.B. Schiöth Structural diversity of G protein-coupled receptors and significance for drug discovery Natl. Rev. 7 2008 339 357
8. J.S. Landin, M. Katragadda, and A.D. Albert Thermal destabilization of rhodopsin and opsin by proteolytic cleavage in bovine rod outer segment disk membranes Biochemistry 40 2001 11176 11183
9. T.H. Ji, M. Grossmann, and I. Ji G protein-coupled receptors. I. Diversity of receptor-ligand interactions J. Biol. Chem. 273 1998 17299 17302
10. T. Okada, and Y. Fujiyoshi Y. Shichida Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography Proc. Natl. Acad. Sci. USA 99 2002 5982 5987
11. K. Tanuj Sapra, and P.S.-H. Park K. Palczewski Detecting molecular interactions that stabilize native bovine rhodopsin J. Mol. Biol. 358 2006 255 269
12. J. Liu, and M.Y. Liu E.C. Yan Thermal decay of rhodopsin: role of hydrogen bonds in thermal isomerization of 11-cis retinal in the binding site and hydrolysis of protonated Schiff base J. Am. Chem. Soc. 131 2009 8750 8751
13. S.M. Khan, and W. Bolen J.H. McDowell Differential scanning calorimetry of bovine rhodopsin in rod-outer-segment disk membranes Eur. J. Biochem. 200 1991 53 59
14. S. Ahuja, and E. Crocker S.O. Smith Location of the retinal chromophore in the activated state of rhodopsin J. Biol. Chem. 284 2009 10190 10201
15. 2a receptor stability: effects of ligands and disulfide bonds Biochemistry 49 2010 9181 9189
16. O. Soubias, and S.-L. Niu K. Gawrisch Lipid-rhodopsin hydrophobic mismatch alters rhodopsin helical content J. Am. Chem. Soc. 130 2008 12465 12471
17. E. Ramon, and J. Marron P. Garriga Effect of dodecyl maltoside detergent on rhodopsin stability and function Vision Res. 43 2003 3055 3061
18. R. Vogel, and F. Siebert Conformation and stability of α-helical membrane proteins. 2. Influence of pH and salts on stability and unfolding of rhodopsin Biochemistry 41 2002 3536 3545
19. R. Vogel Influence of salts on rhodopsin photoproduct equilibria and protein stability Curr. Opin. Colloid Interface Sci. 9 2004 133 138
20. L.J. del Valle, and E. Ramon P. Garriga Zinc-induced decrease of the thermal stability and regeneration of rhodopsin J. Biol. Chem. 278 2003 4719 4724
21. 2+ in native bovine rhodopsin J. Biol. Chem. 282 2007 11377 11385
22. D. Thévenin, and T. Lazarova Stable interactions between the transmembrane domains of the adenosine A2A receptor Protein Sci. 17 2008 1188 1199
23. K.E. Komolov, and M. Aguil K.W. Koch On-chip photoactivation of heterologously expressed rhodopsin allows kinetic analysis of G-protein signaling by surface plasmon resonance spectroscopy Anal. Bioanal. Chem. 397 2010 2967 2976
24. A. Reyes-Alcaraz, T. Tzanov, and P. Garriga Stabilization of membrane proteins: the case of G-protein coupled receptors Eng. Life Sci. 8 2008 207 217
25. C.P. Schwartz, and J.S. Uejio R.J. Saykally Investigation of protein conformation and interactions with salts via X-ray absorption spectroscopy Proc. Natl. Acad. Sci. USA 107 2010 14008 14013
26. L.M. Pegram, and T. Wendorff M.T. Record Jr. Why Hofmeister effects of many salts favor protein folding but not DNA helix formation Proc. Natl. Acad. Sci. USA 107 2010 7716 7721
27. E. Sedlák, L. Stagg, and P. Wittung-Stafshede Effect of Hofmeister ions on protein thermal stability: roles of ion hydration and peptide groups? Arch. Biochem. Biophys. 479 2008 69 73
28. M. Boström, and D.R. Williams B.W. Ninham Hofmeister effects in membrane biology: the role of ionic dispersion potentials Phys. Rev. E. 68 2003 041902
29. Y. Zhang, and P.S. Cremer Interactions between macromolecules and ions: the Hofmeister series Curr. Opin. Chem. Biol. 10 2006 658 663
30. H.-X. Zhou Interactions of macromolecules with salt ions: an electrostatic theory for the Hofmeister effect Proteins 61 2005 69 78
31. L.M. Gloss, and B.J. Placek The effect of salts on the stability of the H2A-H2B histone dimer Biochemistry 41 2002 14951 14959
32. L. Lavelle, and J.R. Fresco Stabilization of nucleic acid triplexes by high concentrations of sodium and ammonium salts follows the Hofmeister series Biophys. Chem. 105 2003 681 699
33. C.H.I. Ramos, and R.L. Baldwin Sulfate anion stabilization of native ribonuclease A both by anion binding and by the Hofmeister effect Protein Sci. 11 2002 1771 1778
34. D.B. Wright, and D.D. Banks L.M. Gloss The effect of salts on the activity and stability of Escherichia coli and Haloferax volcanii dihydrofolate reductases J. Mol. Biol. 323 2002 327 344
35. S. Shimizu, W.M. McLaren, and N. Matubayasi The Hofmeister series and protein-salt interactions J. Chem. Phys. 124 2006 234905
36. F.F. Davidson, P.C. Loewen, and H.G. Khorana Structure and function in rhodopsin: replacement by alanine of cysteine residues 110 and 187, components of a conserved disulfide bond in rhodopsin, affects the light-activated metarhodopsin II state Proc. Natl. Acad. Sci. USA 91 1994 4029 4033
37. T.E. Creighton Protein Structure: A Practical Approach 1997 Oxford University Press New York
38. J. Liu, and M.Y. Liu E.C. Yan Thermal decay of rhodopsin: role of hydrogen bonds in thermal isomerization of 11-cis retinal in the binding site and hydrolysis of protonated Schiff base J. Am. Chem. Soc. 131 2009 8750 8751
39. L.J. Del Valle, and E. Ramon P. Garriga Specific isomerization of rhodopsin-bound 11-cis-retinal to all-trans-retinal under thermal denaturation Cell. Mol. Life Sci. 60 2003 2532 2537
40. M. Geisler, and T. Pirzer T. Hugel Hydrophobic and Hofmeister effects on the adhesion of spider silk proteins onto solid substrates: an AFM-based single-molecule study Langmuir 24 2008 1350 1355
41. R.L. Baldwin How Hofmeister ion interactions affect protein stability Biophys. J. 71 1996 2056 2063
42. J.M. Broering, and A.S. Bommarius Evaluation of Hofmeister effects on the kinetic stability of proteins J. Phys. Chem. B 109 2005 20612 20619
43. J. Selent, and F. Sanz G. de Fabritiis Induced effects of sodium ions on dopaminergic G-protein coupled receptors PLoS Comput. Biol. 6 2010 e1000884
44. D.L. Farrens, and H.G. Khorana Structure and function in rhodopsin: measurement of the rate of the metarhodopsin II decay by fluorescence spectroscopy J. Biol. Chem. 270 1995 5073 5076