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. 1996 May;70(5):2385–2395. doi: 10.1016/S0006-3495(96)79806-5

Correlation between surfactant/micelle structure and the stability of bacteriorhodopsin in solution.

E H Tan 1, R R Birge 1
PMCID: PMC1225215  PMID: 9172764

Abstract

The rate of solubilization and isothermal bleaching of bacteriorhodopsin (bR) in a series of nine alkylammonium surfactants is studied by using time-resolved optical spectroscopy. The surfactant series RN(+)R'(3) covers a range in tail length (R = C(12)H(25), C(14)H(29), or C(16)H(33)) and headgroup size and hydrophobicity (R' = CH(3); C(2)H(5), or C(3)H(7)). The rate of bleaching increases initially with increasing surfactant concentration but decreases at higher concentrations. Possible explanations for this behavior are discussed. The kinetic data are consistent with the penetration of the surfactant into the protein interior. Interaction of the surfactants with the protein is a complicated, multistep process, and the rate curves are a function of at least four variables: 1) the micellar environment, 2) the length of the surfactant tail, 3) the size of the headgroup, and 4) the hydrophobicity of the headgroup. Our data provide new insights into the molecular characteristics that help define the performance of surfactants in the solubilization and denaturation of membrane-bound proteins.

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Selected References

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

  1. Bunton C. A., Wolfe B. The problem of pH in micellar catalyzed reactions. J Am Chem Soc. 1973 May 30;95(11):3742–3749. doi: 10.1021/ja00792a045. [DOI] [PubMed] [Google Scholar]
  2. Carmeli C., Quintanilha A. T., Packer L. Surface charge changes in purple membranes and the photoreaction cycle of bacteriorhodopsin. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4707–4711. doi: 10.1073/pnas.77.8.4707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chang C. H., Chen J. G., Govindjee R., Ebrey T. Cation binding by bacteriorhodopsin. Proc Natl Acad Sci U S A. 1985 Jan;82(2):396–400. doi: 10.1073/pnas.82.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen M., Grätzel M., Thomas J. K. Kinetic studies in bile acid micelles. J Am Chem Soc. 1975 Apr 16;97(8):2052–2057. doi: 10.1021/ja00841a010. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Endo T., Oya M. Conformational changes of a mitochondrial precursor protein on binding to phospholipid vesicles and SDS micelles. A circular dichroism and fluorescence spectroscopy study. FEBS Lett. 1989 Jun 5;249(2):173–177. doi: 10.1016/0014-5793(89)80618-0. [DOI] [PubMed] [Google Scholar]
  7. Engelman D. M., Zaccai G. Bacteriorhodopsin is an inside-out protein. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5894–5898. doi: 10.1073/pnas.77.10.5894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Happe M., Overath P. Bacteriorhodopsin depleted of purple membrane lipids. Biochem Biophys Res Commun. 1976 Oct 18;72(4):1504–1511. doi: 10.1016/s0006-291x(76)80184-2. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Hjelmeland L. M. Solubilization of native membrane proteins. Methods Enzymol. 1990;182:253–264. doi: 10.1016/0076-6879(90)82021-s. [DOI] [PubMed] [Google Scholar]
  14. Jonas R., Koutalos Y., Ebrey T. G. Purple membrane: surface charge density and the multiple effect of pH and cations. Photochem Photobiol. 1990 Dec;52(6):1163–1177. doi: 10.1111/j.1751-1097.1990.tb08455.x. [DOI] [PubMed] [Google Scholar]
  15. Kijima Y., Takagi T., Shigekawa M., Tada M. Protein-protein interaction of detergent-solubilized Ca2(+)-ATPase during ATP hydrolysis analyzed by low-angle laser light scattering photometry coupled with high-performance gel chromatography. Biochim Biophys Acta. 1990 Oct 18;1041(1):1–8. doi: 10.1016/0167-4838(90)90114-u. [DOI] [PubMed] [Google Scholar]
  16. Kushwaha S. C., Kates M., Stoeckenius W. Comparison of purple membrane from Halobacterium cutirubrum and Halobacterium halabium. Biochim Biophys Acta. 1976 Apr 5;426(4):703–710. doi: 10.1016/0005-2736(76)90135-8. [DOI] [PubMed] [Google Scholar]
  17. London E., Khorana H. G. Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures. J Biol Chem. 1982 Jun 25;257(12):7003–7011. [PubMed] [Google Scholar]
  18. Marston F. A., Hartley D. L. Solubilization of protein aggregates. Methods Enzymol. 1990;182:264–276. doi: 10.1016/0076-6879(90)82022-t. [DOI] [PubMed] [Google Scholar]
  19. Massotte D., Aghion J. Bacteriorhodopsin "detergent-monomers," blue shift and velocity of light-dark adaptation. Biochem Biophys Res Commun. 1991 Dec 31;181(3):1301–1305. doi: 10.1016/0006-291x(91)92080-4. [DOI] [PubMed] [Google Scholar]
  20. Miercke L. J., Ross P. E., Stroud R. M., Dratz E. A. Purification of bacteriorhodopsin and characterization of mature and partially processed forms. J Biol Chem. 1989 May 5;264(13):7531–7535. [PubMed] [Google Scholar]
  21. Milder S. J., Thorgeirsson T. E., Miercke L. J., Stroud R. M., Kliger D. S. Effects of detergent environments on the photocycle of purified monomeric bacteriorhodopsin. Biochemistry. 1991 Feb 19;30(7):1751–1761. doi: 10.1021/bi00221a004. [DOI] [PubMed] [Google Scholar]
  22. Neugebauer J. M. Detergents: an overview. Methods Enzymol. 1990;182:239–253. doi: 10.1016/0076-6879(90)82020-3. [DOI] [PubMed] [Google Scholar]
  23. Oesterhelt D., Stoeckenius W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat New Biol. 1971 Sep 29;233(39):149–152. doi: 10.1038/newbio233149a0. [DOI] [PubMed] [Google Scholar]
  24. Packer L., Arrio B., Johannin G., Volfin P. Surface charge of purple membranes measured by laser Doppler velocimetry. Biochem Biophys Res Commun. 1984 Jul 18;122(1):252–258. doi: 10.1016/0006-291x(84)90467-4. [DOI] [PubMed] [Google Scholar]
  25. Padrós E., Duñach M., Sabés M. Induction of the blue form of bacteriorhodopsin by low concentrations of sodium dodecyl sulfate. Biochim Biophys Acta. 1984 Jan 11;769(1):1–7. doi: 10.1016/0005-2736(84)90002-6. [DOI] [PubMed] [Google Scholar]
  26. Renthal R., Hannapel C., Nguyen A. S., Haas P. Regeneration of bacteriorhodopsin in mixed micelles. Biochim Biophys Acta. 1990 Nov 30;1030(1):176–181. doi: 10.1016/0005-2736(90)90254-l. [DOI] [PubMed] [Google Scholar]
  27. Renthal R., Shuler K., Regalado R. Control of bacteriorhodopsin color by chloride at low pH. Significance for the proton pump mechanism. Biochim Biophys Acta. 1990 Apr 26;1016(3):378–384. doi: 10.1016/0005-2728(90)90172-z. [DOI] [PubMed] [Google Scholar]
  28. Seigneuret M., Neumann J. M., Rigaud J. L. Detergent delipidation and solubilization strategies for high-resolution NMR of the membrane protein bacteriorhodopsin. J Biol Chem. 1991 Jun 5;266(16):10066–10069. [PubMed] [Google Scholar]
  29. Shinitzky M., Dianoux A. C., Gitler C., Weber G. Microviscosity and order in the hydrocarbon region of micelles and membranes determined with fluorescent probes. I. Synthetic micelles. Biochemistry. 1971 May 25;10(11):2106–2113. doi: 10.1021/bi00787a023. [DOI] [PubMed] [Google Scholar]
  30. Spudich J. L., McCain D. A., Nakanishi K., Okabe M., Shimizu N., Rodman H., Honig B., Bogomolni R. A. Chromophore/protein interaction in bacterial sensory rhodopsin and bacteriorhodopsin. Biophys J. 1986 Feb;49(2):479–483. doi: 10.1016/S0006-3495(86)83657-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]

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