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Beyond Saffman-Delbruck approximation: A new regime for 2D diffusion of α-hemolysin complexes in supported lipid bilayer

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Abstract

Cell mechanisms are actively modulated by membrane dynamics. We studied the dynamics of a first-stage biomimetic system by Fluorescence Recovery After Patterned Photobleaching. Using this simple biomimetic system, constituted by \(\alpha\) -hemolysin from Staphylococcus aureus inserted as single heptameric pore or complexes of pores in a glass-supported DMPC bilayer, we observed true diffusion behavior, with no immobile fraction. We find two situations: i) when incubation is shorter than 15 hours, the protein inserts as a heptameric pore and diffuses roughly three times more slowly than its host lipid bilayer; ii) incubation longer than 15 hours leads to the formation of larger complexes which diffuse more slowly. Our results indicate that, while the Saffman-Delbruck model adequately describes the diffusion coefficient D for small radii, D of the objects decreases as 1/R 2 for the size range explored in this study. Additionally, in the presence of inserted proteins, the gel-to-fluid transition of the supported bilayer as well as a temperature shift in the gel-to-fluid transition are observed.

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References

  1. S.J. Singer, G.L. Nicolson, Science 175, 720 (1972)

    Article  ADS  Google Scholar 

  2. T. Heimburg, in Planar Lipid Bilayers (BLMs) and their Applications edited by H.T. Tien, A.L. Ottova (Elsevier, Amsterdam, 2003) p. 269

  3. A.D. Dupuy, D.M. Engelman, Proc. Natl. Acad. Sci. U.S.A. 105, 2848 (2008)

    Article  ADS  Google Scholar 

  4. A.E. Sowers, C.R. Hackenbrock, Biochim. Biophys. Acta. 821, 85 (1985)

    Article  Google Scholar 

  5. M. Frick, K. Schmidt, B.J. Nichols, Curr. Biol. 17, 462 (2007)

    Article  Google Scholar 

  6. M.B. Forstnerb, C.K. Yee, A.N. Parikh, J.T. Groves, J. Am. Chem. Soc. 128, 15221 (2006)

    Article  Google Scholar 

  7. Y. Gambin, R. Lopez-Esparza, M. Reffay, E. Sierecki, N.S. Gov, M. Genest, R.S. Hodges, W. Urbach, Proc. Natl. Acad. Sci. U.S.A. 103, 2098 (2006)

    Article  ADS  Google Scholar 

  8. L.M. Smith, J.L. Rubenstein, J.W. Parce, H.M. McConnell, Biochemistry 19, 5907 (1980)

    Article  Google Scholar 

  9. J. Knol, L. Veenhoff, W.J. Liang, P.J. Henderson, G. Leblanc, B. Poolman, J. Biol. Chem. 271, 15358 (1996)

    Article  Google Scholar 

  10. S. Ramadurai, A. Holt, V. Krasnikov, G. van den Bogaart, J.A. Killian, B. Poolman, J. Am. Chem. Soc. 131, 12650 (2009)

    Article  Google Scholar 

  11. J.R. Thompson, A.J. Heron, Y. Santoso, M.I. Wallace, Nano Lett. 7, 3875 (2007)

    Article  ADS  Google Scholar 

  12. M.T. Paternostre, M. Roux, J.L. Rigaud, Biochemistry 27, 2668 (1988)

    Article  Google Scholar 

  13. P. Girard, J. Pecreaux, G. Lenoir, P. Falson, J.L. Rigaud, P. Bassereau, Biophys. J. 87, 419 (2004)

    Article  ADS  Google Scholar 

  14. N. Kahya, E.I. Pecheur, W.P. de Boeij, D.A. Wiersma, D. Hoekstra, Biophys. J. 81, 1464 (2001)

    Article  Google Scholar 

  15. M.L. Wagner, L.K. Tamm, Biophys. J. 79, 1400 (2000)

    Article  ADS  Google Scholar 

  16. E.A. Smith, J.W. Coym, S.M. Cowell, T. Tokimoto, V.J. Hruby, H.I. Yamamura, M.J. Wirth, Langmuir 21, 9644 (2005)

    Article  Google Scholar 

  17. M. Merzlyakov, E. Li, K. Hristova, Langmuir 22, 1247 (2006)

    Article  Google Scholar 

  18. M. Merzlyakov, E. Li, I. Gitsov, K. Hristova, Langmuir 22, 10145 (2006)

    Article  Google Scholar 

  19. P.G. Saffman, M. Delbruck, Proc. Natl. Acad. Sci. U.S.A. 72, 3111 (1975)

    Article  ADS  Google Scholar 

  20. G. Guigas, M. Weiss, Biophys. J. 95, L25 (2008)

    Article  Google Scholar 

  21. J.R. Abney, B.A. Scalettar, J.C. Owicki, Biophys. J. 55, 817 (1989)

    Article  Google Scholar 

  22. R. Peters, R.J. Cherry, Proc. Natl. Acad. Sci. U.S.A. 79, 4317 (1982)

    Article  ADS  Google Scholar 

  23. W.L. Vaz, M. Criado, V.M. Madeira, G. Schoellmann, T.M. Jovin, Biochemistry 21, 5608 (1982)

    Article  Google Scholar 

  24. T. Hughes, B. Strongin, F.P. Gao, V. Vijayvergiya, D.D. Busath, R.C. Davis, Biophys. J. 87, 311 (2004)

    Article  ADS  Google Scholar 

  25. J. Davoust, P.F. Devaux, L. Leger, EMBO J. 1, 1233 (1982)

    Google Scholar 

  26. L. Szyk, P. Schwinte, J.C. Voegel, P. Schaaf, B. Tinland, J. Phys. Chem. B 106, 6049 (2002)

    Article  Google Scholar 

  27. A.E. Nkodo, B. Tinland, Electrophoresis 23, 2755 (2002)

    Article  Google Scholar 

  28. C. Scomparin, S. Lecuyer, M. Ferreira, T. Charitat, B. Tinland, Eur. Phys. J. E Soft Matter 28, 211 (2009)

    Article  Google Scholar 

  29. T. Charitat, E. Bellet-Amalric, G. Fragneto, F. Garner, Eur. Phys. J. B 8, 583 (1999)

    Article  ADS  Google Scholar 

  30. Alexa Fluor 488 Protein Labeling Kit (A10235), Molecular Probes

  31. L. Jayasinghe, G. Miles, H. Bayley, J. Biol. Chem. 281, 2195 (2006)

    Article  Google Scholar 

  32. D.M. Czajkowsky, S.T. Sheng, Z.F. Shao, J. Mol. Biol. 276, 325 (1998)

    Article  Google Scholar 

  33. A. Aksimentiev, K. Schulten, Biophys. J. 88, 3745 (2005)

    Article  Google Scholar 

  34. M. Montoya, E. Gouaux, Biochim. Biophys. Acta. 1609, 19 (2003)

    Article  Google Scholar 

  35. S. Bhakdi, R. Fussle, J. Tranum-Jensen, Proc. Natl. Acad. Sci. U.S.A. 78, 5475 (1981)

    Article  ADS  Google Scholar 

  36. H. Ikigai, T. Nakae, Biochem. Biophys. Res. Commun. 130, 175 (1985)

    Article  Google Scholar 

  37. N. Tobkes, B.A. Wallace, H. Bayley, Biochemistry 24, 1915 (1985)

    Article  Google Scholar 

  38. R.J. Ward, K. Leonards, J. Struct. Biol. 109, 129 (1982)

    Article  Google Scholar 

  39. J.E. Gouaux, O. Braha, M.R. Hobaugh, L. Song, S. Cheley, C. Shustak, H. Bayley, Proc. Natl. Acad. Sci. U.S.A. 91, 12828 (1994)

    Article  ADS  Google Scholar 

  40. B. Walker, O. Braha, S. Cheley, H. Bayley, Chem. Biol. 2, 99 (1995)

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  42. Y. Fang, S. Cheley, H. Bayley, J. Yang, Biochemistry 36, 9518 (1997)

    Article  Google Scholar 

  43. B. Schuster, D. Pum, O. Braha, H. Bayley, U.B. Sleytr, Biochim. Biophys. Acta. 1370, 280 (1998)

    Article  Google Scholar 

  44. M.S. Malghani, Y. Fang, S. Cheley, H. Bayley, J. Yang, Microsc. Res. Tech. 44, 353 (1999)

    Article  Google Scholar 

  45. O.V. Krasilnikov, P.G. Merzlyak, L.N. Yuldasheva, C.G. Rodrigues, S. Bhakdi, A. Valeva, Mol. Microbiol. 37, 1372 (2000)

    Article  Google Scholar 

  46. G. Menestrina, M. Dalla Serra, M. Comai, M. Coraiola, G. Viero, S. Werner, D.A. Colin, H. Monteil, G. Prevost, Febs Lett. 552, 54 (2003)

    Article  Google Scholar 

  47. J.J. Kasianowicz, E. Brandin, D. Branton, D.W. Deamer, Proc. Natl. Acad. Sci. U.S.A. 93, 13770 (1996)

    Article  ADS  Google Scholar 

  48. L.Q. Gu, O. Braha, S. Conlan, S. Cheley, H. Bayley, Nature 398, 686 (1999)

    Article  ADS  Google Scholar 

  49. M. Akeson, D. Branton, J.J. Kasianowicz, E. Brandin, D.W. Deamer, Biophys. J. 77, 3227 (1999)

    Article  Google Scholar 

  50. J.H. Werner, H. Cai, J.H. Jett, L. Reha-Krantz, R.A. Keller, P.M. Goodwin, J. Biotechnol. 102, 1 (2003)

    Article  Google Scholar 

  51. P.E. Milhiet, F. Gubellini, A. Berquand, P. Dosset, J.L. Rigaud, C. Le Grimellec, D. Levy, Biophys. J. 91, 3268 (2006)

    Article  ADS  Google Scholar 

  52. L.K. Tamm, Biochemistry 27, 1450 (1988)

    Article  Google Scholar 

  53. M.R. Alecio, D.E. Golan, W.R. Veatch, R.R. Rando, Proc. Natl. Acad. Sci. U.S.A. 79, 5171 (1982)

    Article  ADS  Google Scholar 

  54. B.A. Smith, H.M. McConnell, Proc. Natl. Acad. Sci. U.S.A. 75, 2759 (1978)

    Article  ADS  Google Scholar 

  55. E.S. Wu, K. Jacobson, D. Papahadjopoulos, Biochemistry 16, 3936 (1977)

    Article  Google Scholar 

  56. S. Ladha, A.R. Mackie, L.J. Harvey, D.C. Clark, E.J.A. Lea, M. Brullemans, H. Duclohier, Biophys. J. 71, 1364 (1996)

    Article  ADS  Google Scholar 

  57. L. Bakas, H. Ostolaza, W.L. Vaz, F.M. Goni, Biophys. J 71, 1869 (1996)

    Article  Google Scholar 

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

    Article  Google Scholar 

  59. A. Charrier, F. Thibaudau, Biophys. J. 89, 1094 (2005)

    Article  Google Scholar 

  60. D. Keller, N.B. Larsen, I.M. Moller, O.G. Mouritsen, Phys. Rev. Lett. 94, 025701 (2005)

    Article  ADS  Google Scholar 

  61. Z.V. Feng, T.A. Spurlin, A.A. Gewirth, Biophys. J. 88, 2154 (2005)

    Article  Google Scholar 

  62. S. Garcia-Manyes, G. Oncins, F. Sanz, Biophys. J. 89, 4261 (2005)

    Article  Google Scholar 

  63. J. Reid, H. Fung, K. Gehring, P.E. Klebba, H. Nikaido, J. Biol. Chem. 263, 7753 (1988)

    Google Scholar 

  64. E. Yoshihara, H. Yoneyama, T. Nakae, J. Biol. Chem. 266, 952 (1991)

    Google Scholar 

  65. J. Chalmeau, N. Monina, J. Shin, C. Vieu, V. Noireaux, Biochim. Biophys. Acta. 1808, 271 (2011)

    Article  Google Scholar 

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Authors and Affiliations

  1. CNRS, UMR7325, 13288, Aix-Marseille Université, CINaM, 13288, Marseille, France

    Frédéric Harb, Joe Sarkis, Natalie Ferte & Bernard Tinland

  2. Institut de Chimie et Biochimie Moléculaires et Supramoléculaires, UMR 5246 CNRS-INSA, Lyon-Université Lyon 1 - CPE Lyon, Equipe GEMBAS, Villeurbanne, France

    Joe Sarkis

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  1. Frédéric Harb
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Harb, F., Sarkis, J., Ferte, N. et al. Beyond Saffman-Delbruck approximation: A new regime for 2D diffusion of α-hemolysin complexes in supported lipid bilayer. Eur. Phys. J. E 35, 118 (2012). https://doi.org/10.1140/epje/i2012-12118-6

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