Internal Hydration Increases during Activation of the G-Protein-Coupled Receptor Rhodopsin

Journal of Molecular Biology

Volumn 381, Issue 2, 2008, Pages 478-486

  Grossfield, Alan ^a   Pitman, Michael C ^a   Feller, Scott E ^b   Soubias, Olivier ^c   Gawrisch, Klaus ^c  

^a IBM T J WATSON RESEARCH CENTER   (United States)

^b WABASH COLLEGE   (United States)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

GPCR; hydration; molecular dynamics; NMR

Indexed keywords

RHODOPSIN; WATER;

ARTICLE; HYDRATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIMULATION;

EID: 47049084133     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.05.036     Document Type: Article

References (50)

1. Hubbell W.L., Altenbach C., Hubbell C.M., and Khorana H.G. Rhodopsin structure, dynamics and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking. Adv. Prot. Chem. 63 (2003) 243-290
2. Lefkowitz R.J. Historical review: a brief history and personal retrospective of seven-transmembrane receptors. Trends Pharmacol. Sci. 25 (2004) 413-422
3. Klabunde T., and Hessler G. Drug design strategies for targeting G-protein-coupled receptors. ChemBioChem 3 (2002) 928-944
4. Rasmussen S.G.F., Choi H.-J., Rosenbaum D.M., Kobilka T.S., Thian F.S., Edwards P.C., et al. Crystal structure of the human beta-2 adrenergic G-protein-coupled receptor. Nature (2007)
5. Li J., Edwards P.C., Burghammer M., Villa C., and Schertler G.F. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343 (2004) 1409-1438
6. Okada T. X-ray crystallographic studies for ligand-protein interaction changes in rhodopsin. Biochem. Soc. Trans. 32 (2004) 738-741
7. Okada T., Fujiyoshi Y., Silow M., Navarro J., Landau E.M., and Shichida Y. Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography. Proc. Natl Acad. Sci. USA 99 (2002) 5982-5987
8. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., et al. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000) 739-745
9. Ruprecht J.J., Mielke T., Vogel R., Villa C., and Schertler G.F. Electron crystallography reveals the structure of metarhodopsin I. EMBO J. 23 (2004) 3609-3620
10. Teller D.C., Okada T., Behnke C.A., Palczewski K., and Stenkamp R.E. Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry 40 (2001) 7761-7772
11. Vogel R., Ruprecht J., Villa C., Mielke T., Schertler G.F., and Siebert F. Rhodopsin photoproducts in 2D crystals. J. Mol. Biol. 338 (2004) 597-609
12. Nakamichi H., and Okada T. Local peptide movement in the photoreaction intermediate of rhodopsin. Proc. Natl. Acad. Sci. USA 103 (2006) 12729-12734
13. Salom D., Lodowski D.T., Stenkamp R.E., Le Trong I., Golczak M., Jastrzebska B., et al. Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc. Natl Acad. Sci. USA 103 (2006) 16123-16128
14. Yan E.C., Kazmi M.A., Ganim Z., Hou J.M., Pan D., Chang B.S., et al. Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl Acad. Sci. USA 100 (2003) 9262-9267
15. Ludeke S., Beck M., Yan E.C., Sakmar T.P., Siebert F., and Vogel R. The role of Glu181 in the photoactivation of rhodopsin. J. Mol. Biol. 353 (2005) 345-356
16. Grossfield A., Feller S.E., and Pitman M. A role for direct interactions in the modulation of rhodopsin by omega-3 polyunsaturated lipids. Proc. Natl Acad. Sci. USA 103 (2006) 4888-4893
17. Grossfield A., Feller S.E., and Pitman M.C. Contribution of omega-3 fatty acids to the thermodynamics of membrane protein solvation. J. Phys. Chem. B 110 (2006) 8907-8909
18. Pitman M.C., Grossfield A., Suits F., and Feller S.E. Role of cholesterol and polyunsaturated chains in lipid-protein interactions: molecular dynamics simulation of rhodopsin in a realistic membrane environment. J. Am. Chem. Soc. 127 (2005) 4576-4577
19. Grossfield A., Feller S.E., and Pitman M. Convergence of molecular dynamics simulations of membrane proteins. Proteins: Struct. Funct. Gen. 67 (2006) 31-40
20. Lemaitre V., Yeagle P., and Watts A. Molecular dynamics simulations of retinal in rhodopsin: from the dark-adapted state towards lumirhodopsin. Biochemistry 44 (2005) 15082
21. Rohrig U.F., Guidoni L., Laio A., Frank I., and Rosthlsberger U. A molecular spring for vision. J. Am. Chem. Soc. 126 (2004) 15328-15329
22. Saam J., Tajkhorshid E., Hayashi S., and Shulten K. Molecular dynamics investigation of primary photoinduced events in the activation of rhodopsin. Biophys. J. 83 (2002) 3097-3112
23. Crozier P.S., Stevens M.J., and Woolf T.B. How a small change in retinal leads to G-protein activation: initial events suggested by molecular dynamics calculations. Proteins: Struct. Funct. Genet. 66 (2006) 559-574
24. Martinez-Mayorga K., Pitman M.C., Grossfield A., Feller S.E., and Brown M.F. Retinal counterion switch mechanism in vision evaluated by molecular simulations. J. Am. Chem. Soc. 128 (2006) 16502-16503
25. Epps J., Lewis J.W., Szundi I., and Kliger D.S. Lumi I → Lumi II: the last detergent independent process in rhodopsin photoexcitation. Photochem. Photobiol. 82 (2006) 1436-1441
26. Borhan B., Souto M.L., Imai H., Shichida Y., and Nakanishi K. Movement of retinal along the visual transduction path. Science 288 (2000) 2209-2212
27. Patel A.B., Crocker E., Reeves P.J., Getmanova E.V., Eilers M., Khorana H.G., and Smith S.O. Changes in interhelical hydrogen bonding upon rhodopsin activation. J. Mol. Biol. 347 (2005) 803-812
28. DeLano, W. L. (2000). The PyMOL Molecular Graphics System (Scientific, D., ed), Palo Alto, CA.
29. Crocker E., Eilers M., Ahuja S., Hornak V., Hirshfeld A., Sheves M., and Smith S.O. Location of Trp265 in metarhodopsin II: implications for the activation mechanism of the visual receptor rhodopsin. J. Mol. Biol. 357 (2006) 163-172
30. Altenbach C., Klein-Seetharaman J., Hwa J., Khorana H.G., and Hubbell W.L. Structural features and light-dependent changes in the sequence 59-75 connecting helices I and II in rhodopsin: a site-directed spin-labeling study. Biochemistry 38 (1999) 7945-7949
31. Cai K., Klein-Seetharaman J., Farrens D., Zhang C., Altenbach C., Hubbell W.L., and Khorana H.G. Single-cysteine substitution mutants at amino acid positions 306-321 in rhodopsin, the sequence between the cytoplasmic end of helix VII and the palmitoylation sites: sulfhydryl reactivity and transducin activation reveal a tertiary structure. Biochemistry 38 (1999) 7925-7930
32. Klein-Seetharaman J., Hwa J., Cai K., Altenbach C., Hubbell W.L., and Khorana H.G. Single-cysteine substitution mutants at amino acid positions 55-75, the sequence connecting the cytoplasmic ends of helices I and II in rhodopsin: reactivity of the sulfhydryl groups and their derivatives identifies a tertiary structure that changes upon light-activation. Biochemistry 38 (1999) 7938-7944
33. Allan A.E., and Cooper A. Hydration of retinal and the nature of metarhodopsin II. FEBS Lett. 119 (1980) 238-240
34. Rath P., DeGrip W.J., and Rothschild K.J. Photoactivation of rhodopsin causes an increased hydrogen-deuterium exchange of buried peptide groups. Biophys. J. 74 (1998) 192-198
35. Rafferty C.N., and Shichi H. The involvement of water at the retinal binding site in rhodopsin and early light-induced intramolecular proton transfer. Photochem. Photobiol. 33 (1981) 229-234
36. Mitchell D.C., and Litman B.J. Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation. Biochemistry 38 (1999) 7617-7623
37. Mitchell D.C., and Litman B.J. Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation. J. Biol. Chem. 275 (2000) 5355-5360
38. Soubias O., and Gawrisch K. Probing specific lipid-protein interaction by saturation transfer difference NMR spectroscopy. J. Am. Chem. Soc. 127 (2005) 13110-13111
39. Soubias O., Teague W.E., and Gawrisch K. Evidence for specificity in lipid-rhodopsin interactions. J. Biol. Chem. 44 (2006) 33233-33241
40. Kibelbek J., Mitchell D.C., Beach J.M., and Litman B.J. Functional equivalence of metarhodopsin II and the Gt-activating form of photolyzed bovine rhodopsin. Biochemistry 30 (1991) 6761-6768
41. Martínez-Mayorga K., Pitman M.C., Grossfield A., Feller S.E., and Brown M.F. Retinal counterion switch mechanism in vision evaluated by molecular simulations. J. Am. Chem. Soc. 128 (2006) 16502-16503
42. Fitch B.G., Germain R.S., Mendell M., Pitera J., Pitman M., Rayshubskiy A., et al. Blue Matter, an application framework for molecular simulation on Blue Gene. J. Para. Distrib. Comp. 63 (2003) 759-773
43. Feller S.E., and MacKerell Jr. A.D. An improved empirical potential energy function for molecular simulations of phospholipids. J. Phys. Chem. B 104 (2000) 7510-7515
44. MacKerell Jr. A.D., Bashford D., Bellott M., Dunbrack Jr. R.L., Evanseck J., Field M.J., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
45. Pitman M.C., Suits F., Mackerell Jr. A.D., and Feller S.E. Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol. Biochemistry 43 (2004) 15318-15328
46. Andersen H.C. Rattle: A "Velocity" Version of the Shake Algorithm for Molecular Dynamics Calculations. J. Comput. Phys. 52 (1983) 24-34
47. Swope W.C., Andersen H.C., Berens P.H., and Wilson K.R. A computer simulation method for the calculation of equilibrium constants for the formation of physical clusters of molecules: application to small water clusters. J. Chem. Phys. 76 (1982) 636-649
48. Gara A., Blumrich M.A., Chen D., Chiu G.L.-T., Coteus P., Giampapa M.E., et al. Overview of the Blue Gene/L system architecture. IBM J. Res. Dev. 49 (2005)
49. Fitch, B. G., Rayshubskiy, A., Eleftheriou, M., Ward, T. J. C., Giampapa, M., Zhestkov, Y., et al. (2005). Blue Matter: Strong Scaling of Molecular Dynamics on Blue Gene/L. Research Report RC23688, IBM Research Division, August 2005.
50. Litman B.J. Purification of rhodopsin by concanavalin A affinity chromatography. Methods Enzymol. 81 (1982) 150-153