Skip to main content

Journal for Biophysical Chemistry

Biosensors based on release of compounds upon disruption of lipid bilayers supported on porous microspheres

Abstract

The authors describe a biosensing concept based on the release of compounds, which are encapsulated within lipid-coated porous silica microspheres, by detergents and toxins that disrupt supported lipid bilayers SLBs on the microspheres. Suspension and microfluidic based methods have been developed to monitor the release of the encapsulated compounds in response to membrane disruption. The authors established that the SLBs on porous microspheres can endure experimental conditions necessary for their incorporation into packed microchannels while maintaining the bilayer integrity and functionality. Model compounds including a nonionic detergent Triton X-100, a membrane active protein (α-hemolysin, and a membrane lytic antimicrobial peptide melittin were successfully utilized to interact with different formulations of SLBs on porous silica microspheres. The results demonstrate the stability of the SLBs on the microspheres for several weeks, and the feasibility of using this system to detect the release of fluorescent dyes as well as other molecular reporters. The latter were detected by their involvement in subsequent biospecific interactions that were detected by fluorescence. This study exemplifies proof of concept for developing new chemical and biochemical sensors and drug delivery systems based on the disruption of lipid membranes coating porous silica microspheres that encapsulate dyes or bioactive compounds.

References

  1. I. V. L. Eschwege, F. Toti, J.-L. Pasquali, and J.-M. Freyssinet, Clin. Exp. Immunol. 103, 171 (1996).

    Article  CAS  Google Scholar 

  2. G. E. Gilbert, D. Drinkwater, S. Barter, and S. B. Clouse, J. Biol. Chem. 267, 15861 (1992).

    CAS  Google Scholar 

  3. A. R. Obringer, N. S. Rote, and A. Walter, J. Immunol. Methods 185, 81 (1995).

    Article  CAS  Google Scholar 

  4. A. Loidl-Stahlhofen, J. Schmitt, J. Nöller, T. Hartmann, H. Brodowsky, J. Schmitt, and J. Keldenich, Adv. Mater. (Weinheim, Ger.) 13, 1829 (2001).

    Article  CAS  Google Scholar 

  5. W. T. Al-Jamal and K. Kostarelos, Nanomedicine 2, 85 (2007).

    Article  CAS  Google Scholar 

  6. M. M. Baksh, M. Jaros, and J. T. Groves, Nature (London) 427, 139 (2004).

    Article  CAS  Google Scholar 

  7. T. Buranda, J. Huang, G. V. Ramarao, L. K. Ista, R. S. Larson, T. L. Ward, L. A. Sklar, and G. P. Lopez, Langmuir 19, 1654 (2003).

    Article  CAS  Google Scholar 

  8. R. W. Davis, A. Flores, T. A. Barrick, J. M. Cox, S. M. Brozik, G. P. Lopez, and J. A. Brozik, Langmuir 23, 3864 (2007).

    Article  CAS  Google Scholar 

  9. R. Galneder, V. Kahl, A. Arbuzova, M. Rebecchi, J. O. Radler, and S. McLaughlin, Biophys. J. 80, 2298 (2001).

    Article  CAS  Google Scholar 

  10. S. P. Moura and A. M. Carmona-Ribeiro, Cell Biochem. Biophys. 44, 446 (2006).

    Article  CAS  Google Scholar 

  11. M. E. Piyasena, T. Buranda, Y. Wu, J. Huang, L. A. Sklar, and G. P. Lopez, Anal. Chem. 76, 6266 (2004).

    Article  CAS  Google Scholar 

  12. A.-L. Troutier and C. Ladavière, Adv. Colloid Interface Sci. 133, 1 (2007).

    Article  CAS  Google Scholar 

  13. E. M. Winter and J. T. Groves, Anal. Chem. 78, 174 (2006).

    Article  CAS  Google Scholar 

  14. R. Zeineldin, M. E. Piyasena, T. S. Bergstedt, L. A. Sklar, D. Whitten, and G. P. Lopez, Cytometry Part A 69, 335 (2006).

    Article  Google Scholar 

  15. T. M. Bayerl and M. Bloom, Biophys. J. 58, 357 (1990).

    Article  CAS  Google Scholar 

  16. A. L. Troutier, T. Delair, C. Pichot, and C. Ladaviere, Langmuir 21,13055 (2005).

    Article  CAS  Google Scholar 

  17. J. Schmitt, B. Danner, and T. M. Bayerl, Langmuir 17, 244 (2001).

    Article  CAS  Google Scholar 

  18. C. P. Yu, A. N. Parikh, and J. T. Groves, Adv. Mater. Weinheim, Ger. 17, 1477 (2005).

    Article  CAS  Google Scholar 

  19. A. Schmitt, J. Nöller, and J. Schmitt, Biochim. Biophys. Acta 1768, 1389 (2007).

    Article  CAS  Google Scholar 

  20. F. M. Goni, M. A. Urbaneja, J. L. R. Arrondo, A. Alonso, A. A. Durrani, and D. Chapman, Eur. J. Biochem. 160, 659 (1986).

    Article  CAS  Google Scholar 

  21. J. Lasch Biochim. Biophys. Acta 1241, 269 (1995).

    Google Scholar 

  22. R. Fussle, S. Bhakdi, A. Sziegoleit, J. Tranumjensen, T. Kranz, and H. J. Wellensiek, J. Cell Biol. 91, 83 (1981).

    Article  CAS  Google Scholar 

  23. F. Gambale and M. Montal, Biophys. J. 53, 771 (1988).

    Article  CAS  Google Scholar 

  24. S. A. Glazier, D. J. Vanderah, A. L. Plant, H. Bayley, G. Valincius, and J. J. Kasianowicz, Langmuir 16, 10428 (2000).

    Article  CAS  Google Scholar 

  25. D. H. Hoch, M. Romeromira, B. E. Ehrlich, A. Finkelstein, B. R. Dasgupta, and L. L. Simpson, Proc. Natl. Acad. Sci. U.S.A. 82, 1692 (1985).

    Article  CAS  Google Scholar 

  26. H. Ostolaza, B. Bartolome, I. O. Dezarate, F. Delacruz, and F. M. Goni, Biochim. Biophys. Acta 1147, 81 (1993).

    Article  CAS  Google Scholar 

  27. M. Palmer, I. Vulicevic, P. Saweljew, A. Valeva, M. Kehoe, and S. Bhakdi, Biochemistry 37, 2378 (1998).

    Article  CAS  Google Scholar 

  28. J. A. Killian, Biochim. Biophys. Acta 1113, 391 (1992).

    CAS  Google Scholar 

  29. S. J. Ludtke, K. He, W. T. Heller, T. A. Harroun, L. Yang, and H. W. Huang, Biochemistry 35, 13723 (1996).

    Article  CAS  Google Scholar 

  30. G. Schwarz, R. T. Zong, and T. Popescu, Biochim. Biophys. Acta 1110, 97 (1992).

    Article  CAS  Google Scholar 

  31. H. Zhao, J.-P. Mattila, J. M. Holopainen, and P. K. J. Kinnunen, Biophys. J. 81, 2979 (2001).

    Article  CAS  Google Scholar 

  32. F. Picard, M. J. Paquet, E. J. Dufourc, and M. Auger, Biophys. J. 74, 857 (1998).

    Article  CAS  Google Scholar 

  33. A. Rohou, J. Nield, and Y. A. Ushkaryov, Toxicon 49, 531 (2007).

    Article  CAS  Google Scholar 

  34. P. F. Kiser, G. Wilson, and D. Needham, Nature (London) 394, 459 (1998).

    Article  CAS  Google Scholar 

  35. T. Buranda, J. Huang, V. H. Perez-Luna, B. Schreyer, L. A. Sklar, and G. P. Lopez, Anal. Chem. 74, 1149 (2002).

    Article  CAS  Google Scholar 

  36. Y. Wu, P. C. Simons, G. P. Lopez, L. A. Sklar, and T. Buranda, Anal. Biochem. 342, 221 (2005).

    Article  CAS  Google Scholar 

  37. R. Sjöback, J. Nygren, and M. Kubista, Spectrochim. Acta, Part A 51, L7 (1995).

    Article  Google Scholar 

  38. D. C. Duffy, J. C. McDonald, O. J. A. Schueller, and G. M. Whitesides, Anal. Chem. 70, 4974 (1998).

    Article  CAS  Google Scholar 

  39. T. Buranda, G. M. Jones, J. P. Nolan, J. Keij, G. P. Lopez, and L. A. Sklar, J. Phys. Chem. B 103, 3399 (1999).

    Article  CAS  Google Scholar 

  40. G. A. Parks, Chem. Rev. Washington, D.C. 65, 177 (1965).

    CAS  Google Scholar 

  41. J. R. Lakowicz, Principles of Fluorescence Spectroscopy, 2nd ed. Plenum, New York, (1999).

    Google Scholar 

  42. See www.avantilipids.com for technical information.

  43. M. Anderson and A. Omri, Adv. Drug Delivery Rev. 11, 33 (2004).

    CAS  Google Scholar 

  44. S. Bhakdi, J. Tranumjensen, and A. Sziegoleit, Infect. Immun. 47, 52 (1985).

    CAS  Google Scholar 

  45. S. J. Moench, J. Moreland, D. H. Stewart, and T. G. Dewey, Biochemistry 33, 5791 (1994).

    Article  CAS  Google Scholar 

  46. S. Rex, J. Bian, J. R. Silvius, and M. Lafleur Biochim. Biophys. Acta 1558, 211 (2002).

    Article  CAS  Google Scholar 

  47. See http://www.ncbi.nlm.nih.gov for -hemolysin Accession No. AAA26598 and alpha-toxin Accession No. P09616.

  48. L. Song, M. R. Hobaugh, C. Shustak, S. Cheley, H. Bayley, and J. E. Gouaux, Science 274, 1859 (1996).

    Article  CAS  Google Scholar 

  49. J. P. Arbuthnott, J. H. Freer, and A. W. Bernheimer, J. Bacteriol. 94, 1170 (1967).

    CAS  Google Scholar 

  50. M. Moayeri and R. A. Welch, Infect. Immun. 62, 4124 (1994).

    CAS  Google Scholar 

  51. V. Noireaux and A. Libchaber, Proc. Natl. Acad. Sci. U.S.A. 101, 17669 (2004).

    Article  CAS  Google Scholar 

  52. B. S. Edwards, T. Oprea, E. R. Prossnitz, and L. A. Sklar, Curr. Opin. Chem. Biol. 8, 392 (2004).

    Article  CAS  Google Scholar 

  53. J. P. Nolan and L. A. Sklar, Trends Biotechnol. 20, 9 (2002).

    Article  CAS  Google Scholar 

  54. L. A. Sklar, B. S. Edwards, S. W. Graves, J. P. Nolan, and E. R. Prossnitz, Annu. Rev. Biophys. Biomol. Struct. 31, 97 (2002).

    Article  CAS  Google Scholar 

  55. A. S. Ladokhin, M. E. Selsted, and S. H. White, Biophys. J. 72, 1762 (1997).

    Article  CAS  Google Scholar 

  56. N. Papo and Y. Shai, Biochemistry 42, 458 (2003).

    Article  CAS  Google Scholar 

  57. A. S. Ladokhin and S. H. White Biochim. Biophys. Acta 1514, 253 (2001).

    Article  CAS  Google Scholar 

  58. T. Benachir and M. Lafleur Biochim. Biophys. Acta 1235, 452 (1995).

    Article  Google Scholar 

  59. D. K. Hincha and J. H. Crowe Biochim. Biophys. Acta 1284, 162 (1996).

    Article  Google Scholar 

  60. R. P. Richter and A. R. Brisson, Biophys. J. 88, 3422 (2005).

    Article  CAS  Google Scholar 

  61. R. P. Richter, N. Maury, and A. R. Brisson, Langmuir 21, 299 (2005).

    Article  CAS  Google Scholar 

  62. D. C. Lee, B. J. Chang, L. P. Yu, S. L. Frey, K. Y. C. Lee, S. Patchipulusu, and C. Hall, Langmuir 20, 11297 (2004).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piyasena, M.E., Zeineldin, R., Fenton, K. et al. Biosensors based on release of compounds upon disruption of lipid bilayers supported on porous microspheres. Biointerphases 3, 38–49 (2008). https://doi.org/10.1116/1.2918743

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1116/1.2918743