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. 1980 May;30(2):243–263. doi: 10.1016/S0006-3495(80)85092-2

Light-induced interfacial potentials in photoreceptor membranes.

D S Cafiso, W L Hubbell
PMCID: PMC1328732  PMID: 6266528

Abstract

A rapid change in an interfacial electric potential of isolated bovine rod outer segment disk membranes occurs upon illumination. This potential change, which has been detected by the use of spin-labeled hydrophobic ions, apparently occurs within a low dielectric boundary region of the membrane near the external (cytoplasmic) surface and is positive with respect to the aqueous exterior of the disk. The magnitude of the potential change is pH-and temperature-dependent and appears with a first-order half-time of approximately 7 ms at 21 degrees C. A simple model in which one positive charge per bleached rhodopsin is translocated from the cytoplasmic aqueous space into the membrane low dielectric boundary region readily accounts for all experimental observations. The great similarity of the boundary potential change to the R2 phase of the early receptor potential suggests that the two have the same molecular origin.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersen O. S., Feldberg S., Nakadomari H., Levy S., McLaughlin S. Electrostatic interactions among hydrophobic ions in lipid bilayer membranes. Biophys J. 1978 Jan;21(1):35–70. doi: 10.1016/S0006-3495(78)85507-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andersen O. S., Fuchs M. Potential energy barriers to ion transport within lipid bilayers. Studies with tetraphenylborate. Biophys J. 1975 Aug;15(8):795–830. doi: 10.1016/S0006-3495(75)85856-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Applebury M. L., Zuckerman D. M., Lamola A. A., Jovin T. M. Rhodopsin. Purification and recombination with phospholipids assayed by the metarhodopsin I leads to metarhodopsin II transition. Biochemistry. 1974 Aug 13;13(17):3448–3458. doi: 10.1021/bi00714a005. [DOI] [PubMed] [Google Scholar]
  4. Bennett N. Evidence for differently protonated forms of metarhodopsin II as intermediates in the decay of membrane-bound cattle rhodopsin. Biochem Biophys Res Commun. 1978 Jul 28;83(2):457–465. doi: 10.1016/0006-291x(78)91012-4. [DOI] [PubMed] [Google Scholar]
  5. Cafiso D. S., Hubbell W. L. Estimation of transmembrane pH gradients from phase equilibria of spin-labeled amines. Biochemistry. 1978 Sep 5;17(18):3871–3877. doi: 10.1021/bi00611a030. [DOI] [PubMed] [Google Scholar]
  6. Cafiso D. S., Hubbell W. L. Estimation of transmembrane potentials from phase equilibria of hydrophobic paramagnetic ions. Biochemistry. 1978 Jan 10;17(1):187–195. doi: 10.1021/bi00594a028. [DOI] [PubMed] [Google Scholar]
  7. Castle J. D., Hubbell W. L. Estimation of membrane surface potential and charge density from the phase equilibrium of a paramagnetic amphiphile. Biochemistry. 1976 Nov 2;15(22):4818–4831. doi: 10.1021/bi00667a011. [DOI] [PubMed] [Google Scholar]
  8. Chen Y. S., Hubbell W. L. Temperature- and light-dependent structural changes in rhodopsin-lipid membranes. Exp Eye Res. 1973 Dec 24;17(6):517–532. doi: 10.1016/0014-4835(73)90082-1. [DOI] [PubMed] [Google Scholar]
  9. Cone R. A., Cobbs W. H., 3rd Rhodopsin cycle in the living eye of the rat. Nature. 1969 Mar 1;221(5183):820–822. doi: 10.1038/221820a0. [DOI] [PubMed] [Google Scholar]
  10. Cone R. A. Early receptor potential: photoreversible charge displacement in rhodopsin. Science. 1967 Mar 3;155(3766):1128–1131. doi: 10.1126/science.155.3766.1128. [DOI] [PubMed] [Google Scholar]
  11. Cone R. A. The early receptor potential of the vertebrate eye. Cold Spring Harb Symp Quant Biol. 1965;30:483–491. doi: 10.1101/sqb.1965.030.01.046. [DOI] [PubMed] [Google Scholar]
  12. Emrich H. M., Reich R. The effect of Ca2+ on the metarhodopsin I-II transition. I. Experiments. Pflugers Arch. 1976 Jun 29;364(1):17–21. doi: 10.1007/BF01062906. [DOI] [PubMed] [Google Scholar]
  13. Gaffney B. J., Mich R. J. Letter: A new measurement of surface charge in model and biological lipid membranes. J Am Chem Soc. 1976 May 12;98(10):3044–3045. doi: 10.1021/ja00426a076. [DOI] [PubMed] [Google Scholar]
  14. Hoffmann W., Siebert F., Hofmann K. P., Kreutz W. Two distinct rhodopsin molecules within the disc membrane of vertebrate rod outer segments. Biochim Biophys Acta. 1978 Sep 7;503(3):450–461. doi: 10.1016/0005-2728(78)90144-5. [DOI] [PubMed] [Google Scholar]
  15. Kühn H. Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry. 1978 Oct 17;17(21):4389–4395. doi: 10.1021/bi00614a006. [DOI] [PubMed] [Google Scholar]
  16. Levine B. A., Sackett J., Williams R. J. The binding of organic ions to phospholipid bilayers. Biochim Biophys Acta. 1979 Jan 19;550(2):201–211. doi: 10.1016/0005-2736(79)90207-4. [DOI] [PubMed] [Google Scholar]
  17. Lundström I. Influence of adsorbed charges and dipoles on the gating charges in excitable membranes. FEBS Lett. 1977 Nov 1;83(1):7–10. doi: 10.1016/0014-5793(77)80629-7. [DOI] [PubMed] [Google Scholar]
  18. MATTHEWS R. G., HUBBARD R., BROWN P. K., WALD G. TAUTOMERIC FORMS OF METARHODOPSIN. J Gen Physiol. 1963 Nov;47:215–240. doi: 10.1085/jgp.47.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McConnell D. G., Rafferty C. N., Dilley R. A. The light-induced proton uptake in bovine retinal outer segment fragments. J Biol Chem. 1968 Nov 25;243(22):5820–5826. [PubMed] [Google Scholar]
  20. Norisuye T., Hoffman W. F., Yu H. Intact photoreceptor membrane from bovine rod outer segment: size and shape in bleached state. Biochemistry. 1976 Dec 14;15(25):5678–5682. doi: 10.1021/bi00670a038. [DOI] [PubMed] [Google Scholar]
  21. Pontus M., Delmelle M. Fluid lipid fraction in rod outer segment membrane. Biochim Biophys Acta. 1975 Aug 20;401(2):221–230. doi: 10.1016/0005-2736(75)90306-5. [DOI] [PubMed] [Google Scholar]
  22. Rapp J. The kinetics of intermediate processes in the photolysis of bovine rhodopsin--II. The intermediate decay sequence from lumirhodopsin497 to metarhodopsin380 II. Vision Res. 1979;19(2):137–141. doi: 10.1016/0042-6989(79)90043-9. [DOI] [PubMed] [Google Scholar]
  23. Sale G. J., Towner P., Akhtar M. Functional rhodopsin complex consisting of three noncovalently linked fragments. Biochemistry. 1977 Dec 13;16(25):5641–5649. doi: 10.1021/bi00644a040. [DOI] [PubMed] [Google Scholar]
  24. Stewart J. G., Baker B. N., Williams T. P. Evidence for conformeric states of rhodopsin. Biophys Struct Mech. 1977 Apr 21;3(1):19–29. doi: 10.1007/BF00536450. [DOI] [PubMed] [Google Scholar]
  25. Trissl H. W., Darszon A., Montal M. Rhodopsin in model membranes: charge displacements in interfacial layers. Proc Natl Acad Sci U S A. 1977 Jan;74(1):207–210. doi: 10.1073/pnas.74.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Trissl H. W. Light-induced conformational changes in cattle rhodopsin as probed by measurements of the interface potential. Photochem Photobiol. 1979 Mar;29(3):579–588. doi: 10.1111/j.1751-1097.1979.tb07093.x. [DOI] [PubMed] [Google Scholar]
  27. Tsien R. Y. A virial expansion for discrete charges buried in a membrane. Biophys J. 1978 Nov;24(2):561–567. doi: 10.1016/S0006-3495(78)85402-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Verma S. P., Berliner L. J., Smith I. C. Cation-dependent light-induced structural changes in visual receptor membranes. Biochem Biophys Res Commun. 1973 Dec 10;55(3):704–709. doi: 10.1016/0006-291x(73)91201-1. [DOI] [PubMed] [Google Scholar]
  29. Waggoner A. S., Griffith O. H., Christensen C. R. Magnetic resonance of nitroxide probes in micelle-containing solutions. Proc Natl Acad Sci U S A. 1967 May;57(5):1198–1205. doi: 10.1073/pnas.57.5.1198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. von Sengbusch G., Stieve H. Flash photolysis of rhodopsin. I. Measurements on bovine rod outer segments. Z Naturforsch B. 1971 May;26(5):488–489. [PubMed] [Google Scholar]

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