Home LiteratureArticle Details
PMID: 11106612 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

Biophysical journal ·Vol. 79 ·No. 6 ·2000-12-00 ·Pages 3063-71

Isele J, Sakmar TP, Siebert F

Abstract

Rhodopsin is a member of a superfamily of G-protein-coupled receptors that transduce signals across membranes. We used Fourier-transform infrared (FTIR) difference spectroscopy to study the interaction between rhodopsin and lipid bilayer upon receptor activation. A difference band at 1744 cm(-1) (+)/1727 cm(-1) (-) was identified in the FTIR-difference spectrum of rhodopsin mutant D83N/E122Q in which spectral difference bands arising from the carbonyl stretching frequencies of protonated carboxylic acid groups were removed by mutation. As the band was abolished by detergent delipidation, we suggested that it arose from carbonyl groups of phospholipid fatty acid esters. Rhodopsin and the D83N/E122Q mutant were reconstituted into various (13)C-labeled 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine vesicles and probed. The 1744-cm(-1) (+)/1727 cm(-1) (-) band could be unequivocally assigned to a change in the lipid ester carbonyl stretch upon receptor activation, with roughly equal contribution from both lipid esters. The band intensity scaled with the amount of rhodopsin but not with the amount of lipid, excluding the possibility that it was due to the bulk lipid phase. We also excluded the possibility that the lipid band represents a change in the number of boundary lipids or a general alteration in the boundary lipid environment upon formation of metarhodopsin II. Instead, the data suggest that the lipid band represents the change of a specific lipid-receptor interaction that is coupled to protein conformational changes.

MeSH Terms
Amino Acid Substitution Animals Cattle Lipid Bilayers/chemistry,metabolism Phosphatidylcholines Phospholipids/chemistry,metabolism Protein Conformation Recombinant Proteins/chemistry,metabolism Rhodopsin/chemistry,metabolism Rod Cell Outer Segment/physiology Spectroscopy, Fourier Transform Infrared/methods Structure-Activity Relationship
Chemicals
Lipid Bilayers Phosphatidylcholines Phospholipids Recombinant Proteins Rhodopsin 1-palmitoyl-2-oleoylphosphatidylcholine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Isele J
Sektion Biophysik, Institut für Molekulare Medizin und Zellforschung, Albert-Ludwigs-Universität, D-79104 Freiburg, Germany.
Sakmar T P
Siebert F
References (43)
43 references, click to expand
  1. Interactions of the beta-ionone ring with the protein in the visual pigment rhodopsin control the activation mechanism. An FTIR and fluorescence study on artificial vertebrate rhodopsins.
    Biochemistry. 1994 Jun 14;33(23):7389-97 PMID: 8003504
  2. Stochastic simulation of activation in the G-protein cascade of phototransduction.
    Biophys J. 1994 Oct;67(4):1439-54 PMID: 7819482
  3. Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers: a reevaluation.
    Biophys J. 1994 Dec;67(6):2367-75 PMID: 7696476
  4. Depalmitoylation of rhodopsin with hydroxylamine.
    Methods Enzymol. 1995;250:348-61 PMID: 7651164
  5. Lipid vesicle adsorption versus formation of planar bilayers on solid surfaces.
    Biophys J. 1995 Oct;69(4):1447-55 PMID: 8534815
  6. Rhodopsin. Purification and recombination with phospholipids assayed by the metarhodopsin I leads to metarhodopsin II transition.
    Biochemistry. 1974 Aug 13;13(17):3448-58 PMID: 4846291
  7. Photochemical functionality of rhodopsin-phospholipid recombinant membranes.
    Biochemistry. 1977 Apr 5;16(7):1295-303 PMID: 557336
  8. Proton and carbon-13 nuclear magnetic resonance studies of rhodopsin-phospholipid interactions.
    Biochemistry. 1979 Nov 27;18(24):5427-32 PMID: 518847
  9. Boundary lipids and protein mobility in rhodopsin-phosphatidylcholine vesicles. Effect of lipid phase transitions.
    Biochim Biophys Acta. 1980 Feb 15;596(1):28-42 PMID: 6243483
  10. The application of pressure relaxation to the study of the equilibrium between metarhodopsin I and II from bovine retinas.
    FEBS Lett. 1980 Oct 6;119(2):323-6 PMID: 7428948
  11. Use of a density modification technique for isolation of the plasma membrane of rod outer segments.
    Biochim Biophys Acta. 1982 May 7;687(2):296-302 PMID: 7093260
  12. Collisions between nitrogen-14 and nitrogen-15 spin-labels. 2. Investigations on the specificity of the lipid environment of rhodopsin.
    Biochemistry. 1983 Jun 21;22(13):3146-51 PMID: 6882742
  13. Lipid-protein interactions in frog rod outer segment disc membranes. Characterization by spin labels.
    Biochim Biophys Acta. 1985 Apr 11;814(2):389-97 PMID: 2983767
  14. Effects of lipid environment on the light-induced conformational changes of rhodopsin. 1. Absence of metarhodopsin II production in dimyristoylphosphatidylcholine recombinant membranes.
    Biochemistry. 1985 May 21;24(11):2624-32 PMID: 4027217
  15. Effect of phospholipids and detergents on transitions and equilibrium between the bleaching intermediates of rhodopsin.
    Can J Biochem Cell Biol. 1985 Nov;63(11):1152-9 PMID: 4084854
  16. Molecular exchange at the lipid-rhodopsin interface: spin-label electron spin resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants.
    Biochemistry. 1987 Jun 2;26(11):3234-40 PMID: 3038180
  17. 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. 1987 Sep 8;26(18):5908-16 PMID: 3118952
  18. Two adjacent cysteine residues in the C-terminal cytoplasmic fragment of bovine rhodopsin are palmitylated.
    FEBS Lett. 1988 Mar 28;230(1-2):1-5 PMID: 3350146
  19. Fourier transform infrared spectroscopy of 13C = O-labeled phospholipids hydrogen bonding to carbonyl groups.
    Biochemistry. 1988 Oct 18;27(21):8239-49 PMID: 3233207
  20. Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier transform infrared and biochemical investigation.
    Biochemistry. 1989 Jul 11;28(14):5954-62 PMID: 2505843
  21. 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 in equilibrium with metarhodopsin II equilibrium.
    Biochemistry. 1992 Jan 28;31(3):662-70 PMID: 1731921
  22. The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction.
    J Biol Chem. 2000 Jan 21;275(3):1930-6 PMID: 10636894
  23. Mutation of the fourth cytoplasmic loop of rhodopsin affects binding of transducin and peptides derived from the carboxyl-terminal sequences of transducin alpha and gamma subunits.
    J Biol Chem. 2000 Jan 21;275(3):1937-43 PMID: 10636895
  24. Transducin-dependent protonation of glutamic acid 134 in rhodopsin.
    Biochemistry. 2000 Aug 29;39(34):10607-12 PMID: 10956053
  25. Effects of detergents and high pressures upon the metarhodopsin I--metarhodopsin II equilibrium.
    Biochemistry. 1974 Feb 12;13(4):738-45 PMID: 4855767
  26. Palmitylation of a G-protein coupled receptor. Direct analysis by tandem mass spectrometry.
    J Biol Chem. 1992 Aug 25;267(24):16889-94 PMID: 1512231
  27. Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes.
    Biochemistry. 1993 Mar 9;32(9):2438-54 PMID: 8443184
  28. 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. 1993 Oct 5;32(39):10277-82 PMID: 8399169
  29. 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. 1993 Nov 1;90(21):10206-10 PMID: 7901852
  30. Photoactivated conformational changes in rhodopsin: a time-resolved spin label study.
    Science. 1993 Nov 26;262(5138):1416-9 PMID: 8248781
  31. Fluorescence studies of the location and membrane accessibility of the palmitoylation sites of rhodopsin.
    Biochemistry. 1994 May 17;33(19):5791-6 PMID: 8180207
  32. Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F.
    Nature. 1996 Sep 26;383(6598):347-50 PMID: 8848049
  33. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin.
    Science. 1996 Nov 1;274(5288):768-70 PMID: 8864113
  34. Stochastic simulation of the transducin GTPase cycle.
    Biophys J. 1996 Dec;71(6):3051-63 PMID: 8968576
  35. Structure and function of proteins in G-protein-coupled signal transfer.
    Biochim Biophys Acta. 1996 Oct 29;1286(3):285-322 PMID: 8982287
  36. Modulation of the metarhodopsin I/metarhodopsin II equilibrium of bovine rhodopsin by ionic strength--evidence for a surface-charge effect.
    Eur J Biochem. 1997 Jan 15;243(1-2):174-80 PMID: 9030737
  37. Role of the C9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal.
    Biochemistry. 1998 Jan 13;37(2):538-45 PMID: 9425074
  38. Rhodopsin: a prototypical G protein-coupled receptor.
    Prog Nucleic Acid Res Mol Biol. 1998;59:1-34 PMID: 9427838
  39. Spectroscopic evidence for interaction between transmembrane helices 3 and 5 in rhodopsin.
    Biochemistry. 1998 May 19;37(20):7630-9 PMID: 9585578
  40. Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. I. Methodology and general phenomena.
    Biospectroscopy. 1998;4(4):267-80 PMID: 9706385
  41. Fourier transform infrared spectroscopy as a probe for the study of the hydration of lipid self-assemblies. II. Water binding versus phase transitions.
    Biospectroscopy. 1998;4(4):281-94 PMID: 9706386
  42. 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. 1998 Oct 9;436(3):304-8 PMID: 9801137
  43. Effect of protein hydration on receptor conformation: decreased levels of bound water promote metarhodopsin II formation.
    Biochemistry. 1999 Jun 15;38(24):7617-23 PMID: 10387000
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2000-12-00
Pages
3063-71
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1301183
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]