Rhodopsin activation affects the environment of specific neighboring phospholipids: An FTIR spectroscopic study

Biophysical Journal

Volumn 79, Issue 6, 2000, Pages 3063-3071

  Isele, Jürgen ^a   Sakmar, Thomas P ^b   Siebert, Friedrich ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CARBONYL DERIVATIVE; CARBOXYLIC ACID; G PROTEIN COUPLED RECEPTOR; LIPID; MUTANT PROTEIN; PHOSPHOLIPID; RHODOPSIN;

ARTICLE; CONFORMATIONAL TRANSITION; INFRARED SPECTROSCOPY; LIPID BILAYER; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN LIPID INTERACTION; PROTON TRANSPORT; SIGNAL TRANSDUCTION;

EID: 0033637518     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76541-6     Document Type: Article

References (43)

1. Applebury, M. L., D. M. Zuckerman, A. A. Lamola, and T. M. Jovin. 1974. Rhodopsin: purification and recombination with phospholipids assayed by the metarhodopsin I -> metarhodopsin II transition. Biochemistry. 13:3448-3458.
2. Atwood, P. V., and H. Gutfreund. 1980. The application of pressure relaxation to the study of the equilibrium between metarhodopsin I and II from bovine retinas. FEBS Lett. 119:323-326.
3. Baldwin, P. A., and W. L. Hubbell. 1985. Effects of lipid environment on the light-induced conformational changes of rhodopsin. I. Absence of metarhodopsin II production in dimyristoylphosphatidylcholine recombinant membranes. Biochemistry. 24:2624-2632.
4. Beck, M., T. P. Sakmar, and F. Siebert. 1998a. Spectroscopic evidence for the interaction between transmembrane helices 3 and 5 in rhodopsin. Biochemistry. 37:7630-7639.
5. Beck, M., F. Siebert, and T. P. Sakmar. 1998b. Evidence for the specific interaction of a lipid molecule with rhodopsin which is altered in the transition to the active state metarhodopsin II. FEBS Lett. 436:304-308.
6. 13C=O-labeled phospholipids hydrogen bonding to carbonyl groups. Biochemistry. 27:8239-8249.
7. Davoust, J., A. Bienvenue, P. Fellmann, and P. F. Devaux. 1980. Boundary lipids and protein mobility in rhodopsin-phosphatidylcholine vesicles. Biochim. Biophys. Acta. 596:28-42.
8. Davoust, J., M. Seigneuret, P. Hervé, and P. F. Devaux. 1983. Collision between nitrogen-14 and nitrogen-15 spin-labels. II. Investigation on the specifity of the lipid environment of rhodopsin. Biochemistry. 22: 3146-3151.
9. Delange, F., M. Merkx, P. H. M. Bovee-Geurts, A. M. A. Pistorius, and W. J. DeGrip. 1997. Modulation of the metarhodopsin I/metarhodopsin II equilibrium of bovine rhodopsin by ionic strength: evidence for surface charge effect. Eur. J. Biochem. 243:174-180.
10. Ernst, O. P., C. K. Meyer, E. P. Marin, P. Henklein, W. -Y. Fu, T. P. Sakmar, and K. P. Hofmann. 2000. Mutation of the fourth cytoplasmatic loop of rhodopsin affects binding of transducin and peptides derived from the carboxyl-terminal sequences of transducin α and γ subunits. J. Biol. Chem. 275:1937-1943.
11. Fahmy, K., F. Jäger, M. Beck, T. A. Zvyaga, T. P. Sakmar, and F. Siebert. 1993. Protonation states of membrane-embedded carboxylic acid groups in rhodopsin and metarhodopsin II: a Fourier-transform infrared spectroscopy study of site-directed mutants. Proc. Natl. Acad. Sci. U.S.A. 90:10206-10210.
12. Fahmy, K., T. P. Sakmar, and F. Siebert. 2000. Transducin-dependent protonation of glutamic acid 134 in rhodopsin. Biochemistry. 39: 10607-10612.
13. Farahbakhsh, Z. T., K. Hideg, and W. L. Hubbell. 1993. Photoactivated conformational changes in rhodopsin: a time-resolved spin label study. Science. 262:1416-1419.
14. Farrens, D. L., C. Altenbach, K. Yang, W. L. Hubbell, and H. G. Khorana. 1996. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science. 274:768-770.
15. Felber, S., H. P. Breuer, F. Petruccione, J. Honerkamp, and K. P. Hofmann. 1996. Stochastic simulation of the transducin GTPase cycle. Biophys. J. 71:3051-3063.
16. Ganter, U. M., E. D. Schmid, D. Perez-Sala, R. R. Rando, and F. Siebert. 1989. Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process: a Fourier transform infrared and biochemical investigation. Biochemistry. 28:5954-5962.
17. Gibson, N. J., and M. F. Brown. 1993. Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes. Biochemistry. 32:2438-2454.
18. 9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal. Biochemistry. 37:538-545.
19. Helmreich, E. J. M., and K. P. Hofmann. 1996. Structure and function of proteins in G-protein-coupled signal transfer. Biochim. Biophys. Acta. 1286:285-322.
20. Jäger, F., S. Jäger, O. Kräutle, N. Friedman, M. Sheves, K. P. Hofmann, and F. Siebert. 1994. Interactions of the β-ionone ring with the protein in the visual pigment rhodopsin control the activation mechanism: an FTIR and fluorescence study on artificial vertebrate rhodopsins. Biochemistry. 33:7389-7397.
21. Kamps, K. M. P., W. J. DeGrip, and F. J. M. Daemen. 1982. Use of a density modification technique for isolation of the plasma membrane of rod outer segments. Biochim. Biophys. Acta. 687:296-302.
22. Lamb, T. D. 1994. Stochastic simulation of the activation in the G-protein cascade of phototransduction. Biophys. J. 67:1439-1454.
23. Lamola, A. A., T. Yamane, and A. Zipp. 1974. Effects of detergent and high pressure upon the metarhodopsin I ↔ metarhodopsin II equilibrium. Biochemistry. 13:738-745.
24. Lewis, R. N. A. H., R. N. McElhaney, W. Pohle, and H. H. Mantsch. 1994. Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers: a reevaluation. Biophys. J. 67: 2367-2375.
25. Marin, E. P., A. G. Krishna, T. A. Zvyaga, J. Isele, F. Siebert, and T. P. Sakmar. 2000. The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J. Biol. Chem. 275:1930-1936.
26. Mitchell, D. C., and B. J. Litman. 1999. Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation. Biochemistry. 38:7617-7623.
27. Mitchell, D. C., M. Straume, and B. J. Litman. 1992. Role of sn-1-saturated, sn-2-polyunsaturated phospholipids in control of membrane receptor conformational equilibrium: effects of cholesterol and acyl chain unsaturation on the metarhodopsin I ↔ metarhodopsin II equilibrium. Biochemistry. 31:662-670.
28. Moench, S. J., J. Moreland, D. H. Stewart, and T. G. Dewey. 1994. Fluoresecence studies of the location and membrane accessibility of the palmitoylation sites of rhodopsin. Biochemistry. 33:5791-5796.
29. Motoyama, H., T. Hamanaka, N. Kawase, F. Boucher, and Y. Kito. 1985. Effect of phospholipids and detergents on transitions and equilibrium between the bleaching intermediates of rhodopsin. Can. J. Biochem. Cell. Biol. 63:1152-1159.
30. Nollert, P., H. Kiefer, and F. Jähnig. 1995. Lipid vesicle adsorption versus formation of planar bilayers on solid surfaces. Biophys. J. 69: 1447-1455.
31. O'Brien, D. F., L. F. Costa, and R. A. Ott. 1977. Photochemical functionality of rhodopsin-phospholipid recombinant membranes. Biochemistry. 1295-1303.
32. Ovchinnikov, Y. A., N. G. Abdulaev, and A. S. Bogachuk. 1988. Two adjacent cysteine residues in the C-terminal cytoplasmic fragment of bovine rhodopsin are palmitylated. FEBS Lett. 230:1-5.
33. Papac, D. I., K. R. Thornburg, E. E. Büllesbach, R. K. Crouch, and D. R. Knapp. 1992. Palmitylation of a G-protein coupled receptor. J. Biol. Chem. 267:16889-16894.
34. Pates, R. D., A. Watts, R. Uhl, and D. Marsh. 1985. Lipid-protein interactions in frog rod outer segment disc membranes: characterization by spin labels. Biochim. Biophys. Acta. 814:389-397.
35. Pepperberg, D. R., D. F. Morrison, and P. J. O'Brien. 1995. Depalmitoylation of rhodopsin with hydroxylamine. Methods Enzymol. 250: 348-361.
36. Pohle, W., C. Selle, H. Fritzsche, and H. Binder. 1998. Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. I. Methodology and general phenomena. Biospectroscopy. 4:267-280.
37. Rath, P., L. L. J. DeCaluwé, P. H. M. Bovee-Geurts, W. J. DeGrip, and K. J. Rothschild. 1993. Fourier transform infrared difference spectroscopy of rhodopsin mutants: light activation of rhodopsin causes hydrogen-bonding change in residue aspartic acid-83 during meta II formation. Biochemistry. 32:10277-10282.
38. Ryba, N. J. P., L. I. Horvath, A. Watts, and D. Marsh. 1987. Molecular exchange at the lipid-rhodopsin interface: spin-label electron spin resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. Biochemistry. 26:3234-3240.
39. Sakmar, T. P. 1998. Rhodopsin: a prototypical G protein-coupled receptor. Prog. Nucleic Acid Res. 59:1-33.
40. Schleicher, A., R. Franke, K. P. Hofmann, H. Finkelmann, and W. Welte. 1987. Deoxylysolecithin and a new biphenyl detergent as solubilizing agents for bovine rhodopsin: functional test by formation of metarhodopsin II and binding of G-protein. Biochemistry. 26:5908-5916.
41. Selle, C., and W. Pohle. 1998. Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. II. Water binding versus phase transition. Biospectroscopy. 44:281-294.
42. Sheikh, S. P., T. A. Zvyaga, O. Lichtarge, T. P. Sakmar, and H. R. Bourne. 1996. Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F. Nature. 383:347-350.
43. Zumbulyadis, N., and D. F. O'Brien. 1979. Proton and carbon-13 nuclear magnetic resonance studies of rhodopsin-phospholipid interactions. Biochemistry. 18:5427-5432.