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Photo-induced proton gradients and ATP biosynthesis produced by vesicles encapsulated in a silica matrix

Nature Materials volume 4, pages 220–224 (2005)Cite this article

Abstract

Sol–gel immobilization of soluble proteins has proven to be a viable method for stabilizing a wide variety of proteins in transparent inorganic matrices1,2,3. The encapsulation of membrane-bound proteins has received much less attention, although work in this area suggests potential opportunities in microarray technology and high-throughput drug screening4,5. The present paper describes a liposome/sol–gel architecture in which the liposome provides membrane structure and protein orientation to two transmembrane proteins, bacteriorhodopsin (bR) and F0F1-ATP synthase; the sol–gel encapsulation converts the liposomal solution into a robust material without compromising the intrinsic activity of the incorporated proteins. Here we report on two different proteoliposome-doped gels (proteogels) whose properties are determined by the transmembrane proteins. Proteogels containing bR proteoliposomes exhibit a stable proton gradient when irradiated with visible light, whereas proteogels containing proteoliposomes with both bR and F0F1-ATP synthase couple the photo-induced proton gradient to the production of ATP. These results demonstrate that materials based on the liposome/sol–gel architecture are able to harness the properties of transmembrane proteins and enable a variety of applications, from power generation and energy storage to the powering of molecular motors, and represent a new technology for performing complex chemical synthesis in a solid-state matrix.

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Figure 1: Encapsulation of proteoliposomes in sol–gel matrices.
Figure 2: Charge and discharge behaviours of a 150-μm proteogel film.
Figure 3: Characterization of a proteogel film.
Figure 4: HPLC chromatograms of fluids extracted from ATP-synthase-doped proteogel.

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References

  1. Avnir, D., Braun, S., Lev, O. & Ottolenghi, M. Enzymes and other proteins entrapped in sol–gel materials. Chem. Mater. 6, 1605–1614 (1994).

    Article  CAS  Google Scholar 

  2. Zink, J. I., Valentine, J. S. & Dunn, B. Biomolecular materials based on sol–gel encapsulated proteins. New J. Chem. 18, 1109–1115 (1994).

    CAS  Google Scholar 

  3. Livage, J., Coradin, T. & Roux, C. Encapsulation of biomolecules in silica gels. J. Phys. Condens. Matter. 13, 673–691 (2001).

    Article  Google Scholar 

  4. Besanger, T. R. & Brennan, J. D. Ion sensing and inhibition studies using the transmembrane ion channel peptide gramicidin a entrapped in sol–gel-derived silica. Anal. Chem. 75, 1094–1101 (2003).

    Article  CAS  Google Scholar 

  5. Besanger, T. R., Easwaramoorthy, B. & Brennan, J. D. Entrapment of highly active membrane-bound receptors in macroporous sol–gel derived silica. Anal. Chem. 76, 6470–6475 (2004).

    Article  CAS  Google Scholar 

  6. Yamanaka, S. A., Charych, D. H., Loy, D. A. & Sasaki, D. Y. Solid phase immobilization of optically responsive liposomes in sol–gel materials for chemical and biological sensing. Langmuir 13, 5049–5053 (1997).

    Article  CAS  Google Scholar 

  7. Nassif, N. et al. Living bacteria in silica gels. Nature Mater. 1, 42–44 (2002).

    Article  CAS  Google Scholar 

  8. Carturan, G., Dal Toso, R., Boninsegna, S. & Dal Monte, R. Encapsulation of functional cells by sol–gel silica: actual progress and perspectives for cell therapy. J. Mater. Chem. 14, 2087–2098 (2004).

    Article  CAS  Google Scholar 

  9. Wu, S. et al. Bacteriorhodopsin encapsulated in transparent sol–gel glass: A new biomaterial. Chem. Mater. 5, 115–120 (1993).

    Article  CAS  Google Scholar 

  10. Oesterhelt, D. & Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature New Biol. 233, 149–152 (1971).

    Article  CAS  Google Scholar 

  11. Oesterhelt, D. & Stoeckenius, W. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31, 667–678 (1974).

    Article  CAS  Google Scholar 

  12. Oesterhelt, D. & Schuhmann, L. Reconsitituion of bacteriorhodopsin. FEBS Lett. 44, 262–265 (1974).

    Article  CAS  Google Scholar 

  13. Birge, R. R. Photophysics and molecular electronic application of the rhodopsins. Annu. Rev. Phys. Chem. 41, 683–733 (1990).

    Article  CAS  Google Scholar 

  14. Birge, R. R. Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin. Biochim. Biophys. Acta. 1016, 293–327 (1990).

    Article  CAS  Google Scholar 

  15. Rigaud, J. L., Bluzat, A. & Buschlen, S. Incorporation of bacteriorhodopsin into large unilamellar liposomes by reverse phase evaporation. Biochem. Biophys. Res. Com. 111, 373–382 (1983).

    Article  CAS  Google Scholar 

  16. Seigneuret, M. & Rigaud, J. L. Use of fluorescent pH probe pyranine to detect heterogeneous directions of proton movement in bacteriorhodopsin reconsituted large liposomes. FEBS Lett. 188, 101–106 (1985).

    Article  CAS  Google Scholar 

  17. Szoka, F. & Papahadjopoulos, D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc. Natl Acad. Sci. USA 75, 4194–4198 (1978).

    Article  CAS  Google Scholar 

  18. Straubinger, R. M., Papahadjopoulos, D. & Hong, K. Endocytosis and intracellular fate of liposomes using pyranine as probe. Biochemistry 29, 4929–4939 (1990).

    Article  CAS  Google Scholar 

  19. Seigneuret, M. & Rigaud, J. L. Analysis of passive and light-driven ion movements in large bacteriorhodopsin liposomes reconstituted by reverse-phase evaporation. 1. Factors governing the passive proton permeability of the membrane. Biochem. 25, 6716–6722 (1986).

    Article  CAS  Google Scholar 

  20. Ferrer, M. L., Monte, F. D. & Levy, D. A novel and simple alcohol-free sol–gel route for encapsulation of labile proteins. Chem. Mater. 14, 3619–3621 (2002).

    Article  CAS  Google Scholar 

  21. Dunn, B. & Zink, J. I. Probes of pore environment and molecule-matrix interfactions in sol–gel materials. Chem. Mater. 9, 2280–2291 (1997).

    Article  CAS  Google Scholar 

  22. Matsuda, A. et al. in Sol–gel Optics (eds Mackenzie, J. D. & Ulrich, D. R.) 62–70 (SPIE, Bellingham, 1990).

    Book  Google Scholar 

  23. Chen, Q., Kenausis, G. L. & Heller, A. Stability of oxidases immobilized in silica gel. J. Am. Chem. Soc. 120, 4582–4585 (1998).

    Article  CAS  Google Scholar 

  24. Nguyen, D. T., Smit, M., Dunn, B. & Zink, J. I. Stabilization of creatine kinase encapsulated in silicate sol–gel materials and unusual temperature effects on its activity. Chem. Mater. 14, 4300–4306 (2002).

    Article  CAS  Google Scholar 

  25. Liu, H. Q. et al. Control of a biomolecular motor-powered nanodevice with an engineered chemical switch. Nature Mater. 1, 173–177 (2002).

    Article  CAS  Google Scholar 

  26. Clemmens, J. et al. Motor-protein “roundabouts”: Microtubules moving on kinesin-coated tracks through engineered networks. Lab on a Chip 4, 83–86 (2004).

    Article  CAS  Google Scholar 

  27. Dencher, N. A. & Heyn, M. P. Bacteriorhodopsin monomers pump protons. FEBS Lett. 108, 307–10 (1979).

    Article  CAS  Google Scholar 

  28. Hazard, A. & Montemagno, C. Improved purification for thermophilic F1F0 ATP synthase using n-dodecyl beta-D-maltoside. Arch. Biochem. Biophys. 407, 117–124 (2002).

    Article  CAS  Google Scholar 

  29. Ozogul, F., Taylor, K. D. A., Quantick, P. C. & Ozogul, Y. A rapid HPLC-determination of ATP-related compounds and its application to herring stored under modified atmosphere. Int. J. Food Sci. Technol. 35, 549–554 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was also partially supported by Center for Cell Mimetic Space Exploration (CMISE), a NASA University Research, Engineering and Technology Institute (URETI), under award number NCC 2-1364. Additional funding was obtained from the National Science Foundation (DMR 0103952 and DMR 0099862).

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Authors and Affiliations

  1. Department of Materials Science and Engineering, University of California, Los Angeles, 90095, California, USA

    Tzy-Jiun M. Luo, Esther Lan & Bruce Dunn

  2. Department of Bioengineering, University of California, Los Angeles, 90095, California, USA

    Ricky Soong & Carlo Montemagno

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Correspondence to Bruce Dunn or Carlo Montemagno.

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Luo, TJ., Soong, R., Lan, E. et al. Photo-induced proton gradients and ATP biosynthesis produced by vesicles encapsulated in a silica matrix. Nature Mater 4, 220–224 (2005). https://doi.org/10.1038/nmat1322

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