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PMID: 15980173 Published · ppublish English Journal Article

Effect of packing density on rhodopsin stability and function in polyunsaturated membranes.

Biophysical journal ·Vol. 89 ·No. 3 ·2005-09-00 ·Pages 1833-40

Niu SL, Mitchell DC

Abstract

Rod outer segment disk membranes are densely packed with rhodopsin. The recent notion of raft or microdomain structures in disk membranes suggests that the local density of rhodopsin in disk membranes could be much higher than the average density corresponding to the lipid/protein ratio. Little is known about the effect of high packing density of rhodopsin on the structure and function of rhodopsin and lipid membranes. Here we examined the role of rhodopsin packing density on membrane dynamic properties, membrane acyl chain packing, and the structural stability and function of rhodopsin using a combination of biophysical and biochemical techniques. We reconstituted rhodopsin into large unilamellar vesicles consisting of polyunsaturated 18:0,22:6n3PC, which approximates the polyunsaturated nature of phospholipids in disk membranes, with rhodopsin/lipid ratios ranging from 1:422 to 1:40. Our results showed that increased rhodopsin packing density led to reduced membrane dynamics revealed by the fluorescent probe 1,6-diphenyl-1,3,5-hexatriene, increased phospholipid acyl chain packing, and reduced rhodopsin activation, yet it had minimal impact on the structural stability of rhodopsin. These observations imply that densely packed rhodopsin may impede the diffusion and conformational changes of rhodopsin, which could reduce the speed of visual transduction.

MeSH Terms
Animals Anisotropy Biochemistry/methods Biophysics/methods Calorimetry, Differential Scanning Cattle Cell Membrane/metabolism Kinetics Lipid Bilayers/chemistry Lipids/chemistry Membrane Lipids/chemistry Membranes/chemistry,metabolism Phospholipids/chemistry Retina/metabolism Rhodopsin/chemistry Rod Cell Outer Segment Spectrometry, Fluorescence Temperature Time Factors Vision, Ocular
Chemicals
Lipid Bilayers Lipids Membrane Lipids Phospholipids Rhodopsin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Niu Shui-Lin
Section of Fluorescence Studies, Laboratory of Membrane Biochemistry and Biophysics, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, Maryland 20892, USA. sniu@niaaa.nih.gov
Mitchell Drake C
References (55)
55 references, click to expand
  1. G-protein-coupled receptors at a glance.
    J Cell Sci. 2003 Dec 15;116(Pt 24):4867-9 PMID: 14625380
  2. Atomic-force microscopy: Rhodopsin dimers in native disc membranes.
    Nature. 2003 Jan 9;421(6919):127-8 PMID: 12520290
  3. The G protein-coupled receptor rhodopsin in the native membrane.
    FEBS Lett. 2004 Apr 30;564(3):281-8 PMID: 15111110
  4. Desensitization of G protein-coupled receptors and neuronal functions.
    Annu Rev Neurosci. 2004;27:107-44 PMID: 15217328
  5. Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n-3 fatty acid deficiency.
    J Biol Chem. 2004 Jul 23;279(30):31098-104 PMID: 15145938
  6. Effects of detergents and high pressures upon the metarhodopsin I--metarhodopsin II equilibrium.
    Biochemistry. 1974 Feb 12;13(4):738-45 PMID: 4855767
  7. Photochemical functionality of rhodopsin-phospholipid recombinant membranes.
    Biochemistry. 1977 Apr 5;16(7):1295-303 PMID: 557336
  8. Light-induced phosphorylation of rhodopsin in cattle photoreceptor membranes: substrate activation and inactivation.
    Biochemistry. 1977 Sep 6;16(18):4054-60 PMID: 911754
  9. Lipid--protein interactions in bacteriorhodopsin--dimyristoylphosphatidylcholine vesicles.
    Biochemistry. 1981 Feb 17;20(4):840-9 PMID: 7213618
  10. Distinct states of lipid mobility in bovine rod outer segment membranes. Resolution of spin label results.
    Biochim Biophys Acta. 1981 May 20;643(3):673-6 PMID: 6264958
  11. Purification of rhodopsin by concanavalin A affinity chromatography.
    Methods Enzymol. 1982;81:150-3 PMID: 7098858
  12. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman-Delbrück equations.
    Proc Natl Acad Sci U S A. 1982 Jul;79(14):4317-21 PMID: 6956861
  13. Fluorescence energy transfer from diphenylhexatriene to bacteriorhodopsin in lipid vesicles.
    Biophys J. 1983 Jul;43(1):39-45 PMID: 6882861
  14. Phospholipid domains in bovine retinal rod outer segment disk membranes.
    Proc Natl Acad Sci U S A. 1983 Dec;80(23):7188-91 PMID: 6580636
  15. Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys.
    J Clin Invest. 1984 Jan;73(1):272-6 PMID: 6317716
  16. Rhodopsin-egg phosphatidylcholine reconstitution by an octyl glucoside dilution procedure.
    Biochim Biophys Acta. 1985 Jan 25;812(2):369-76 PMID: 3881128
  17. Thermotropic behavior of retinal rod membranes and dispersions of extracted phospholipids.
    J Membr Biol. 1985;85(1):79-86 PMID: 4020856
  18. Effects of lipid environment on the light-induced conformational changes of rhodopsin. 2. Roles of lipid chain length, unsaturation, and phase state.
    Biochemistry. 1985 May 21;24(11):2633-9 PMID: 4027218
  19. Two-dimensional crystallization of bovine rhodopsin.
    Biochim Biophys Acta. 1985 Dec 20;832(3):337-42 PMID: 4074754
  20. Lipid mobility and order in bovine rod outer segment disk membranes. A spin-label study of lipid-protein interactions.
    Biochemistry. 1987 Jan 13;26(1):29-39 PMID: 3030400
  21. Lateral diffusion of proteins in membranes.
    Annu Rev Physiol. 1987;49:163-75 PMID: 3551795
  22. 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
  23. Equilibrium and dynamic structure of large, unilamellar, unsaturated acyl chain phosphatidylcholine vesicles. Higher order analysis of 1,6-diphenyl-1,3,5-hexatriene and 1-[4-(trimethylammonio)phenyl]- 6-phenyl-1,3,5-hexatriene anisotropy decay.
    Biochemistry. 1987 Aug 11;26(16):5113-20 PMID: 3663647
  24. Equilibrium and dynamic bilayer structural properties of unsaturated acyl chain phosphatidylcholine-cholesterol-rhodopsin recombinant vesicles and rod outer segment disk membranes as determined from higher order analysis of fluorescence anisotropy decay.
    Biochemistry. 1988 Oct 4;27(20):7723-33 PMID: 3207703
  25. Lipid-protein interactions mediate the photochemical function of rhodopsin.
    Biochemistry. 1988 Aug 23;27(17):6469-74 PMID: 3219348
  26. Effect of proteins on fluorophore lifetime heterogeneity in lipid bilayers.
    Biochemistry. 1990 Apr 3;29(13):3248-55 PMID: 1692237
  27. Interconversion of metarhodopsins I and II: a branched photointermediate decay model.
    Biochemistry. 1990 Oct 2;29(39):9135-42 PMID: 2271583
  28. Reaction rate and collisional efficiency of the rhodopsin-transducin system in intact retinal rods.
    Biophys J. 1991 Feb;59(2):375-86 PMID: 1901231
  29. A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants.
    Dev Med Child Neurol. 2000 Mar;42(3):174-81 PMID: 10755457
  30. Crystal structure of rhodopsin: A G protein-coupled receptor.
    Science. 2000 Aug 4;289(5480):739-45 PMID: 10926528
  31. Cholesterol dependent recruitment of di22:6-PC by a G protein-coupled receptor into lateral domains.
    Biophys J. 2000 Nov;79(5):2632-43 PMID: 11053136
  32. Membrane protein diffusion sets the speed of rod phototransduction.
    Nature. 2001 May 3;411(6833):90-4 PMID: 11333983
  33. Light- and guanosine 5'-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments.
    J Biol Chem. 2001 Jun 15;276(24):20813-6 PMID: 11319214
  34. Thermal destabilization of rhodopsin and opsin by proteolytic cleavage in bovine rod outer segment disk membranes.
    Biochemistry. 2001 Sep 18;40(37):11176-83 PMID: 11551216
  35. G protein-coupled receptor rhodopsin: a prospectus.
    Annu Rev Physiol. 2003;65:851-79 PMID: 12471166
  36. Biophysics: is rhodopsin dimeric in native retinal rods?
    Nature. 2003 Nov 6;426(6962):30-1; discussion 31 PMID: 14603306
  37. Fatty acid and molecular species compositions of phospholipids and diacylglycerols from rat retinal membranes.
    Exp Eye Res. 1991 Feb;52(2):213-8 PMID: 2013303
  38. Differential scanning calorimetry of bovine rhodopsin in rod-outer-segment disk membranes.
    Eur J Biochem. 1991 Aug 15;200(1):53-9 PMID: 1831759
  39. 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
  40. Signal flow in visual transduction.
    Neuron. 1992 Jun;8(6):995-1002 PMID: 1377000
  41. Kinetic analysis of the activation of transducin by photoexcited rhodopsin. Influence of the lateral diffusion of transducin and competition of guanosine diphosphate and guanosine triphosphate for the nucleotide site.
    Biophys J. 1992 Sep;63(3):616-29 PMID: 1420903
  42. 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
  43. Amplification and kinetics of the activation steps in phototransduction.
    Biochim Biophys Acta. 1993 Mar 1;1141(2-3):111-49 PMID: 8382952
  44. Modulation of rhodopsin function by properties of the membrane bilayer.
    Chem Phys Lipids. 1994 Sep 6;73(1-2):159-80 PMID: 8001180
  45. A role for phospholipid polyunsaturation in modulating membrane protein function.
    Lipids. 1996 Mar;31 Suppl:S193-7 PMID: 8729118
  46. Primary alcohols modulate the activation of the G protein-coupled receptor rhodopsin by a lipid-mediated mechanism.
    J Biol Chem. 1996 Aug 9;271(32):19033-6 PMID: 8702573
  47. Molecular order and dynamics in bilayers consisting of highly polyunsaturated phospholipids.
    Biophys J. 1998 Feb;74(2 Pt 1):879-91 PMID: 9533699
  48. Phosphorus assay in column chromatography.
    J Biol Chem. 1959 Mar;234(3):466-8 PMID: 13641241
  49. Trans fatty acid derived phospholipids show increased membrane cholesterol and reduced receptor activation as compared to their cis analogs.
    Biochemistry. 2005 Mar 22;44(11):4458-65 PMID: 15766276
  50. Optimization of receptor-G protein coupling by bilayer lipid composition I: kinetics of rhodopsin-transducin binding.
    J Biol Chem. 2001 Nov 16;276(46):42801-6 PMID: 11544258
  51. Optimization of receptor-G protein coupling by bilayer lipid composition II: formation of metarhodopsin II-transducin complex.
    J Biol Chem. 2001 Nov 16;276(46):42807-11 PMID: 11544259
  52. Signal-dependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors.
    Curr Biol. 2002 Mar 5;12(5):421-5 PMID: 11882295
  53. Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids.
    Biochemistry. 2002 May 21;41(20):6354-68 PMID: 12009897
  54. Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation.
    J Biol Chem. 2002 Jun 7;277(23):20139-45 PMID: 11889130
  55. Membrane model for the G-protein-coupled receptor rhodopsin: hydrophobic interface and dynamical structure.
    Biophys J. 2004 Apr;86(4):2078-100 PMID: 15041649
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
DOI
10.1529/biophysj.105.061812
Email
sniu@niaaa.nih.gov
Published
2005-09-00
Epub
2005-00-24
Pages
1833-40
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1366686
Subset
IM
Grants
NIAAA NIH HHS · Z01 AA000080-12 · United States
External Links
PubMed source DOI: 10.1529/biophysj.105.061812 PMC Full Text View journal details
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