Abstract
Over a decade and a half ago, when the first visible membrane suspension circular dichroic (CD) spectrum of the purple membrane (PM) was presented, two mechanisms were proposed to account for the observed biphasic shaped CD band: (a) excitonic interactions among the retinals of the sole protein bacteriorhodopsin (bR) in the crystalline structure of the PM, and (b) combination of CD bands with opposite rotational strengths due to a retinal-apoprotein heterogeneity of the bR molecules or due to two possible close-lying long-wavelength transitions of the retinal of the bR with opposite rotational strengths. Since that time, an impressive body of experimental and theoretical evidence has been accumulated, mostly consistent with an exciton model but many at serious odds with any heterogeneity or multiple transition model. Recently, a number of articles have appeared reporting analyses of new experimental observations which are proposed to cast serious doubts on the viability of the exciton model, and therefore, may revive the heterogeneity or multiple transition model as an explanation for the unique shape of the CD band of the PM. The intent of this article is to demonstrate that if all observations found in literature baring on this question are considered in toto and in a consistent manner, they can be interpreted without exception by excitons, and furthermore, that there is no plausible evidence available to warrant the revival of the heterogeneity or multiple transition model as an explanation for the unique shape of the biphasic CD band of the PM.
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Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ahl P. L., Cone R. A. Light activates rotations of bacteriorhodopsin in the purple membrane. Biophys J. 1984 Jun;45(6):1039–1049. doi: 10.1016/S0006-3495(84)84251-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bauer P. J., Dencher N. A., Heyn M. P. Evidence for chromophore-chromophore interactions in the purple membrane from reconstitution experiments of the chromophore-free membrane. Biophys Struct Mech. 1976 Apr 15;2(1):79–92. doi: 10.1007/BF00535654. [DOI] [PubMed] [Google Scholar]
- Bazzi M. D., Woody R. W. Oriented secondary structure in integral membrane proteins. I. Circular dichroism and infrared spectroscopy of cytochrome oxidase in multilamellar films. Biophys J. 1985 Dec;48(6):957–966. doi: 10.1016/S0006-3495(85)83859-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Becher B., Cassim J. Y. Effects of light adaptation on the purple membrane structure of Halobacterium halobium. Biophys J. 1976 Oct;16(10):1183–1200. doi: 10.1016/S0006-3495(76)85767-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Becher B., Ebrey T. G. Evidence for chromophore-chromophore (exciton) interaction in the purple membrane of Halobacterium halobium. Biochem Biophys Res Commun. 1976 Mar 8;69(1):1–6. doi: 10.1016/s0006-291x(76)80263-x. [DOI] [PubMed] [Google Scholar]
- Braiman M. S., Ahl P. L., Rothschild K. J. Millisecond Fourier-transform infrared difference spectra of bacteriorhodopsin's M412 photoproduct. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5221–5225. doi: 10.1073/pnas.84.15.5221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cherry R. J., Heyn M. P., Oesterhelt D. Rotational diffusion and exciton coupling of bacteriorhodopsin in the cell membrane of Halobacterium halobium. FEBS Lett. 1977;78(1):25–30. doi: 10.1016/0014-5793(77)80265-2. [DOI] [PubMed] [Google Scholar]
- Cherry R. J., Müller U. Temperature-dependent aggregation of bacteriorhodopsin in dipalmitoyl- and dimyristoylphosphatidylcholine vesicles. J Mol Biol. 1978 May 15;121(2):283–298. doi: 10.1016/s0022-2836(78)80010-2. [DOI] [PubMed] [Google Scholar]
- Dencher N. A., Dresselhaus D., Zaccai G., Büldt G. Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7876–7879. doi: 10.1073/pnas.86.20.7876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dencher N. A., Heyn M. P. Formation and properties of bacteriorhodopsin monomers in the non-ionic detergents octyl-beta-D-glucoside and Triton X-100. FEBS Lett. 1978 Dec 15;96(2):322–326. doi: 10.1016/0014-5793(78)80427-x. [DOI] [PubMed] [Google Scholar]
- Derguini F., Bigge C. F., Croteau A. A., Balogh-Nair V., Nakanishi K. Visual pigments and bacteriorhodopsins formed from aromatic retinal analogs. Photochem Photobiol. 1984 May;39(5):661–665. doi: 10.1111/j.1751-1097.1984.tb03906.x. [DOI] [PubMed] [Google Scholar]
- Draheim J. E., Cassim J. Y. Large Scale Global Structural Changes of the Purple Membrane during the Photocycle. Biophys J. 1985 Apr;47(4):497–507. doi: 10.1016/S0006-3495(85)83943-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Draheim J. E., Gibson N. J., Cassim J. Y. Dehydration-induced molecular structural changes of purple membrane of halobacterium halobium. Biophys J. 1988 Nov;54(5):931–944. doi: 10.1016/S0006-3495(88)83029-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Du J. J., el-Sayed M. A., Stern L. J., Mogi T., Khorana H. G. Sensitivity of the retinal circular dichroism of bacteriorhodopsin to the mutagenetic single substitution of amino acids: tyrosine. FEBS Lett. 1990 Mar 26;262(2):155–158. doi: 10.1016/0014-5793(90)80178-l. [DOI] [PubMed] [Google Scholar]
- Dér A., Száraz S., Czégé J. Orientation of the chromophore plane in purple membrane. Biophys J. 1988 Dec;54(6):1175–1178. doi: 10.1016/S0006-3495(88)83053-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ebrey T. G., Becher B., Mao B., Kilbride P., Honig B. Exciton interactions and chromophore orientation in the purple membrane. J Mol Biol. 1977 May 25;112(3):377–397. doi: 10.1016/s0022-2836(77)80188-5. [DOI] [PubMed] [Google Scholar]
- El-Sayed M. A., Karvaly B., Fukumoto J. M. Primary step in the bacteriorhodopsin photocycle: photochemistry or excitation transfer? Proc Natl Acad Sci U S A. 1981 Dec;78(12):7512–7516. doi: 10.1073/pnas.78.12.7512. [DOI] [PMC free article] [PubMed] [Google Scholar]
- El-Sayed M. A., Lin C. T., Mason W. R. Is there an excitonic interaction or antenna system in bacteriorhodopsin? Proc Natl Acad Sci U S A. 1989 Jul;86(14):5376–5379. doi: 10.1073/pnas.86.14.5376. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frankel R. D., Forsyth J. M. Time-resolved x-ray diffraction study of photostimulated purple membrane. Biophys J. 1985 Mar;47(3):387–393. doi: 10.1016/S0006-3495(85)83930-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glaeser R. M., Baldwin J., Ceska T. A., Henderson R. Electron diffraction analysis of the M412 intermediate of bacteriorhodopsin. Biophys J. 1986 Nov;50(5):913–920. doi: 10.1016/S0006-3495(86)83532-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glaeser R. M., Jubb J. S., Henderson R. Structural comparison of native and deoxycholate-treated purple membrane. Biophys J. 1985 Nov;48(5):775–780. doi: 10.1016/S0006-3495(85)83835-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godfrey R. E. Photoselection and circular dichroism in the purple membrane. Biophys J. 1982 Apr;38(1):1–6. doi: 10.1016/S0006-3495(82)84523-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grzesiek S., Dencher N. A. Monomeric and aggregated bacteriorhodopsin: Single-turnover proton transport stoichiometry and photochemistry. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9509–9513. doi: 10.1073/pnas.85.24.9509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hauss T., Grzesiek S., Otto H., Westerhausen J., Heyn M. P. Transmembrane location of retinal in bacteriorhodopsin by neutron diffraction. Biochemistry. 1990 May 22;29(20):4904–4913. doi: 10.1021/bi00472a022. [DOI] [PubMed] [Google Scholar]
- Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990 Jun 20;213(4):899–929. doi: 10.1016/S0022-2836(05)80271-2. [DOI] [PubMed] [Google Scholar]
- Henderson R. The purple membrane from Halobacterium halobium. Annu Rev Biophys Bioeng. 1977;6:87–109. doi: 10.1146/annurev.bb.06.060177.000511. [DOI] [PubMed] [Google Scholar]
- Henderson R., Unwin P. N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 1975 Sep 4;257(5521):28–32. doi: 10.1038/257028a0. [DOI] [PubMed] [Google Scholar]
- Heyn M. P., Bauer P. J., Dencher N. A. A natural CD label to probe the structure of the purple membrane from Halobacterium halobium by means of exciton coupling effects. Biochem Biophys Res Commun. 1975 Dec 1;67(3):897–903. doi: 10.1016/0006-291x(75)90761-5. [DOI] [PubMed] [Google Scholar]
- Heyn M. P., Cherry R. J., Müller U. Transient and linear dichroism studies on bacteriorhodopsin: determination of the orientation of the 568 nm all-trans retinal chromophore. J Mol Biol. 1977 Dec 15;117(3):607–620. doi: 10.1016/0022-2836(77)90060-2. [DOI] [PubMed] [Google Scholar]
- Heyn M. P., Westerhausen J., Wallat I., Seiff F. High-sensitivity neutron diffraction of membranes: Location of the Schiff base end of the chromophore of bacteriorhodopsin. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2146–2150. doi: 10.1073/pnas.85.7.2146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffmann W., Restall C. J., Hyla R., Chapman D. Protein rotation and chromophore orientation in reconstituted bacteriorhodopsin vesicles. Biochim Biophys Acta. 1980 Nov 18;602(3):531–538. doi: 10.1016/0005-2736(80)90332-6. [DOI] [PubMed] [Google Scholar]
- Honig B., Ebrey T. G. The structure and spectra of the chromophore of the visual pigments. Annu Rev Biophys Bioeng. 1974;3(0):151–177. doi: 10.1146/annurev.bb.03.060174.001055. [DOI] [PubMed] [Google Scholar]
- Jubb J. S., Worcester D. L., Crespi H. L., Zaccaï G. Retinal location in purple membrane of Halobacterium halobium: a neutron diffraction study of membranes labelled in vivo with deuterated retinal. EMBO J. 1984 Jul;3(7):1455–1461. doi: 10.1002/j.1460-2075.1984.tb01996.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- King G. I., Mowery P. C., Stoeckenius W., Crespi H. L., Schoenborn B. P. Location of the chromophore in bacteriorhodopsin. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4726–4730. doi: 10.1073/pnas.77.8.4726. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klausner R. D., Berman M., Blumenthal R., Weinstein J. N., Caplan S. R. Compartmental analysis of light-induced proton movement in reconstituted bacteriorhodopsin vesicles. Biochemistry. 1982 Jul 20;21(15):3643–3650. doi: 10.1021/bi00258a018. [DOI] [PubMed] [Google Scholar]
- Muccio D. D., Cassim J. Y. Interpretation of the absorption and circular dichroic spectra of oriented purple membrane films. Biophys J. 1979 Jun;26(3):427–440. doi: 10.1016/S0006-3495(79)85263-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muccio D. D., Cassim J. Y. Interpretations of the effects of pH on the spectra of purple membrane. J Mol Biol. 1979 Dec 15;135(3):595–609. doi: 10.1016/0022-2836(79)90166-9. [DOI] [PubMed] [Google Scholar]
- Pande C., Callender R., Henderson R., Pande A. Purple membrane: color, crystallinity, and the effect of dimethyl sulfoxide. Biochemistry. 1989 Jul 11;28(14):5971–5978. doi: 10.1021/bi00440a038. [DOI] [PubMed] [Google Scholar]
- Papadopoulos G. K., Muccio D. D., Hsiao T. L., Cassim J. Y. Comparative studies on the fine structure of purple membrane from Halobacterium Cutirubrum and Halobacterium Halobium. J Membr Biol. 1978 Oct 19;43(2-3):277–294. doi: 10.1007/BF01933483. [DOI] [PubMed] [Google Scholar]
- Popot J. L., Trewhella J., Engelman D. M. Reformation of crystalline purple membrane from purified bacteriorhodopsin fragments. EMBO J. 1986 Nov;5(11):3039–3044. doi: 10.1002/j.1460-2075.1986.tb04603.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rafferty C. N., Cassim J. Y., McConnell D. G. Circular dichroism, optical rotatory dispersion, and absorption studies on the conformation of bovine rhodopsin iw situ and solubilized with detergent. Biophys Struct Mech. 1977 Mar 2;2(4):227–320. [PubMed] [Google Scholar]
- Razi Naqvi K., Gonzalez-Rodriguez J., Cherry R. J., Chapman D. Spectroscopic technique for studying protein rotation in membranes. Nat New Biol. 1973 Oct 24;245(147):249–251. doi: 10.1038/newbio245249a0. [DOI] [PubMed] [Google Scholar]
- Reyenolds J. A., Stoeckenius W. Molecular weight of bacteriorhodopsin solubilized in Triton X-100. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2803–2804. doi: 10.1073/pnas.74.7.2803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schreckenbach T., Walckhoff B., Oesterhelt D. Specificity of the retinal binding site of bacteriorhodopsin: chemical and stereochemical requirements for the binding of retinol and retinal. Biochemistry. 1978 Dec 12;17(25):5353–5359. doi: 10.1021/bi00618a005. [DOI] [PubMed] [Google Scholar]
- Seiff F., Wallat I., Ermann P., Heyn M. P. A neutron diffraction study on the location of the polyene chain of retinal in bacteriorhodopsin. Proc Natl Acad Sci U S A. 1985 May;82(10):3227–3231. doi: 10.1073/pnas.82.10.3227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seiff F., Westerhausen J., Wallat I., Heyn M. P. Location of the cyclohexene ring of the chromophore of bacteriorhodopsin by neutron diffraction with selectively deuterated retinal. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7746–7750. doi: 10.1073/pnas.83.20.7746. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sherman W. V., Caplan S. R. Chromophore mobility in bacteriorhodopsin. Nature. 1977 Jan 20;265(5591):273–274. doi: 10.1038/265273a0. [DOI] [PubMed] [Google Scholar]
- Stoeckenius W., Bogomolni R. A. Bacteriorhodopsin and related pigments of halobacteria. Annu Rev Biochem. 1982;51:587–616. doi: 10.1146/annurev.bi.51.070182.003103. [DOI] [PubMed] [Google Scholar]
- Stoeckenius W., Lozier R. H., Bogomolni R. A. Bacteriorhodopsin and the purple membrane of halobacteria. Biochim Biophys Acta. 1979 Mar 14;505(3-4):215–278. doi: 10.1016/0304-4173(79)90006-5. [DOI] [PubMed] [Google Scholar]
- Tokunaga F., Ebrey T. The blue membrane: the 3-dehydroretinal-based artificial pigment of the purple membrane. Biochemistry. 1978 May 16;17(10):1915–1922. doi: 10.1021/bi00603a018. [DOI] [PubMed] [Google Scholar]
- Woody R. W. Improved calculation of the n-pi rotational strength in polypeptides. J Chem Phys. 1968 Dec 1;49(11):4797–4806. doi: 10.1063/1.1669962. [DOI] [PubMed] [Google Scholar]
- Wu S., El-Sayed M. A. CD spectrum of bacteriorhodopsin: Best evidence against exciton model. Biophys J. 1991 Jul;60(1):190–197. doi: 10.1016/S0006-3495(91)82042-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zimányi L., Tokaji Z., Dollinger G. Circular dichroic spectrum of the L form and the blue light product of the m form of purple membrane. Biophys J. 1987 Jan;51(1):145–148. doi: 10.1016/S0006-3495(87)83319-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van den Berg R., Du-Jeon-Jang, Bitting H. C., El-Sayed M. A. Subpicosecond resonance Raman spectra of the early intermediates in the photocycle of bacteriorhodopsin. Biophys J. 1990 Jul;58(1):135–141. doi: 10.1016/S0006-3495(90)82359-6. [DOI] [PMC free article] [PubMed] [Google Scholar]