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Bending stiffness of biological membranes: What can be measured by neutron spin echo?

  • Michael Mell
  • Lara H. Moleiro
  • Yvonne Hertle
  • Peter Fouquet
  • Ralf Schweins
  • Iván López-Montero
  • Thomas HellwegEmail author
  • Francisco Monroy
Regular Article
Part of the following topical collections:
  1. Neutron Biological Physics

Abstract

Large vesicles obtained by the extrusion method represent adequate membrane models to probe membrane dynamics with neutron radiation. Particularly, the shape fluctuations around the spherical average topology can be recorded by neutron spin echo (NSE). In this paper we report on the applicable theories describing the scattering contributions from bending-dominated shape fluctuations in diluted vesicle dispersions, with a focus on the relative relevance of the master translational mode with respect to the internal fluctuations. Different vesicle systems, including bilayer and non-bilayer membranes, have been scrutinized. We describe the practical ranges where the exact theory of bending fluctuations is applicable to obtain the values of the bending modulus from experiments, and we discuss about the possible internal modes that could be alternatively contributing to shape fluctuations.

Graphical abstract

Keywords

Topical issue: Neutron Biological Physics 

References

  1. 1.
    W. Helfrich, Z. Naturforsch. c 28, 693 (1973).Google Scholar
  2. 2.
    J.F. Nagle, S. Tristram-Nagle, Biochim. Biophys. Acta 1469, 159 (2000).CrossRefGoogle Scholar
  3. 3.
    J. Lyatskaya, Y. Liu, S. Tristram-Nagle, J. Katsaras, J.F. Nagle, Phys. Rev. E 63, 011907 (2000).ADSCrossRefGoogle Scholar
  4. 4.
    G. Brotons, L. Belloni, Th. Zemb, T. Salditt, Europhys. Lett. 75, 992 (2006).ADSCrossRefGoogle Scholar
  5. 5.
    M.M. Blum, M. Mustyakimov, H. Rüterjans, K. Kehe, B.P. Schoenborn, P. Langan, J.C. Chen, Proc. Natl. Acad. Sci. U.S.A. 106, 713 (2009).ADSCrossRefGoogle Scholar
  6. 6.
    E. Schneck, B. Demé, C. Gege, M. Tanaka, Biophys. J. 100, 2151 (2011).ADSCrossRefGoogle Scholar
  7. 7.
    V.I. Gordeliy, M.A. Kiselev, Biophys. J. 69, 1424 (1995).ADSCrossRefGoogle Scholar
  8. 8.
    J. Pencer, F.R. Hallett, Phys. Rev. E 61, 3003 (2000).ADSCrossRefGoogle Scholar
  9. 9.
    P.C. Mason, B.D. Gaulin, R.M. Epand, G.D. Wignall, J.S. Lin, Phys. Rev. E 59, 3361 (1999).ADSCrossRefGoogle Scholar
  10. 10.
    N. Kucerka, J.F. Nagle, S.E. Feller, P. Balgavý, Phys. Rev. E 69, 051903 (2004).ADSCrossRefGoogle Scholar
  11. 11.
    L.R. Arriaga, I. López-Montero, F. Monroy, G. Orts-Gil, B. Farago, T. Hellweg, Biophys. J. 96, 3629 (2009).ADSCrossRefGoogle Scholar
  12. 12.
    L.R. Arriaga, I. López-Montero, G. Orts-Gil, B. Farago, T. Hellweg, F. Monroy, Phys. Rev. E 80, 031908 (2009).ADSCrossRefGoogle Scholar
  13. 13.
    E. Evans, A. Yeung, Chem. Phys. Lipids 73, 39 (1994).CrossRefGoogle Scholar
  14. 14.
    J.T. Jenkins, J. Math. Biol 4, 149 (1977).CrossRefzbMATHGoogle Scholar
  15. 15.
    M.B. Schneider, J.T. Jenkins, W.W. Webb, J. Phys. (Paris) 45, 1457 (1984).CrossRefGoogle Scholar
  16. 16.
    D.A. Boal, Mechanics of the Cell, 2nd edition (Cambridge University Press, Cambridge, 2012).Google Scholar
  17. 17.
    W. Helfrich, R.-M. Servuss, Nuovo Cimento D 3, 137 (1984).ADSCrossRefGoogle Scholar
  18. 18.
    B.J. Berne, R. Pecora, Dynamic Light Scattering (Wiley, New York, 1976).Google Scholar
  19. 19.
    S.W. Lovesey, P. Schofield, J. Phys. C: Solid State Phys. 9, 2843 (1976).ADSCrossRefGoogle Scholar
  20. 20.
    S.T. Milner, S.A. Safran, Phys. Rev. A 36, 4371 (1987).ADSCrossRefGoogle Scholar
  21. 21.
    T. Hellweg, D. Langevin, Phys. Rev. E 57, 6825 (1998).ADSCrossRefGoogle Scholar
  22. 22.
    R. Messager, P. Bassereau, G. Porte, J. Phys. (Paris) 51, 1329 (1990).CrossRefGoogle Scholar
  23. 23.
    A.G. Zilman, R. Granek, Chem. Phys. 284, 195 (2002).ADSCrossRefGoogle Scholar
  24. 24.
    J.S. Huang, S.T. Milner, B. Farago, D. Richter, Phys. Rev. Lett. 59, 2600 (1987).ADSCrossRefGoogle Scholar
  25. 25.
    B. Farago, M. Monkenbusch, K.D. Goecking, D. Richter, J.S. Huang, Physica B 213-214, 712 (1995).Google Scholar
  26. 26.
    T. Hellweg, A. Brulet, T. Sottmann, Phys. Chem. Chem. Phys. 2, 5168 (2000).CrossRefGoogle Scholar
  27. 27.
    S. Komura, T. Takeda, Y. Kawabata, S.K. Ghosh, H. Seto, M. Nagao, Phys. Rev. E 63, 041402 (2001).ADSCrossRefGoogle Scholar
  28. 28.
    B. Farago, M. Gradzielski, J. Chem. Phys. 114, 10105 (2001).ADSCrossRefGoogle Scholar
  29. 29.
    M. Mihailescu, M. Monkenbusch, J. Allgaier, H. Frielinghaus, D. Richter, B. Jakobs, T. Sottmann, Phys. Rev. E 66, 041504 (2002).ADSCrossRefGoogle Scholar
  30. 30.
    A.C. Woodka, P.D. Butler, L. Porcar, B. Farago, M. Nagao, Phys. Rev. Lett. 109, 058102 (2012).ADSCrossRefGoogle Scholar
  31. 31.
    E. Freyssingeas, D. Roux, F. Nallet, J. Phys.: Condens. Matter 8, 2801 (1996).ADSCrossRefGoogle Scholar
  32. 32.
    E. Freyssingeas, F. Nallet, D. Roux, Langmuir 12, 6028 (1996).CrossRefGoogle Scholar
  33. 33.
    J.F. Faucon, M.D. Mitov, P. Méléard, I. Bivas, P. Bothorel, J. Phys. (Paris) 50, 2389 (1989).CrossRefGoogle Scholar
  34. 34.
    J. Pécréaux, H.G. Döbereiner, J. Prost, J.-F. Joanny, P. Bassereau, Eur. Phys. J. E 13, 277 (2004).CrossRefGoogle Scholar
  35. 35.
    A.G. Zilman, R. Granek, Phys. Rev. Lett. 77, 4788 (1996).ADSCrossRefGoogle Scholar
  36. 36.
    R. Granek, Soft Matter 7, 5281 (2011).ADSCrossRefGoogle Scholar
  37. 37.
    R. Granek, J. Phys. II 7, 1761 (1997).CrossRefGoogle Scholar
  38. 38.
    N.G. van Kampen, Stochastic Process in Physics and Chemistry (North-Holland, Amsterdam, 1992).Google Scholar
  39. 39.
    R. Iñiguez-Palomares, H. Acuña-Campa, A. Maldonado, Phys. Rev. E 84, 011604 (2011).ADSCrossRefGoogle Scholar
  40. 40.
    M.H. Nagao, H. Seto, Y. Kawabata, T. Takeda, J. Appl. Crystallogr. 33, 653 (2000).CrossRefGoogle Scholar
  41. 41.
    M. Mihailescu, M. Monkenbusch, H. Endo, J. Allgaier, G. Gompper, J. Stellbrink, D. Richter, B. Jakobs, T. Sottmann, B. Farago, J. Chem. Phys. 115, 9563 (2001).ADSCrossRefGoogle Scholar
  42. 42.
    Z. Yi, M. Nagao, D. Bossev, J. Phys.: Condens. Matter 21, 155104 (2009).ADSCrossRefGoogle Scholar
  43. 43.
    M. Imai, R. Mawatari, K. Nakaya, S. Komura, Eur. Phys. J. E 13, 391 (2004).CrossRefGoogle Scholar
  44. 44.
    M.C. Watson, F.L.H. Brown, Biophys. J. 98, L9 (2010).CrossRefGoogle Scholar
  45. 45.
    M.C. Watson, Y. Peng, Y. Zheng, F.L.H. Brown, J. Chem. Phys. 135, 194701 (2011).ADSCrossRefGoogle Scholar
  46. 46.
    L.R. Arriaga, R. Rodríguez-García, I. López-Montero, B. Farago, T. Hellweg, F. Monroy, Eur. Phys. J. E 31, 105 (2010).CrossRefGoogle Scholar
  47. 47.
    U. Seifert, S.A. Langer, Europhys. Lett. 23, 71 (1993).ADSCrossRefGoogle Scholar
  48. 48.
    M. Kraus, U. Seifert, J. Phys. II 4, 1117 (1994).CrossRefGoogle Scholar
  49. 49.
    T. Pott, P. Méléard, Europhys. Lett. 59, 87 (2002).ADSCrossRefGoogle Scholar
  50. 50.
    R. Rodríguez-García, L.R. Arriaga, M. Mell, L.H. Moleiro, I. López-Montero, F. Monroy, Phys. Rev. Lett. 102, 128201 (2009).CrossRefGoogle Scholar
  51. 51.
    M. Nagao, Phys. Rev. E 80, 031606 (2009).ADSCrossRefGoogle Scholar
  52. 52.
    B.J. Frisken, C. Asman, P.J. Patty, Langmuir 16, 928 (2000).CrossRefGoogle Scholar
  53. 53.
    Z. Li, E. Kesselman, Y. Talmon, M.A. Hillmyer, T.P. Lodge, Science 306, 98 (2004).ADSCrossRefGoogle Scholar
  54. 54.
    A. Wittemann, M. Drechsler, Y. Talmon, M. Ballauff, J. Am. Chem. Soc. 127, 9688 (2005).CrossRefGoogle Scholar
  55. 55.
    S.W. Provencher, Comput. Phys. Commun. 27, 213 (1982).ADSCrossRefGoogle Scholar
  56. 56.
    S.W. Provencher, Comput. Phys. Commun. 27, 229 (1982).ADSCrossRefGoogle Scholar
  57. 57.
    A. Jakes, Collect. Czech. Chem. Commun. 60, 1781 (1995).CrossRefGoogle Scholar
  58. 58.
    P. Brocca, L. Cantù, M. Corti, E.D. Favero, Prog. Colloid Polym. Sci. 115, 181 (2000).CrossRefGoogle Scholar
  59. 59.
    P. Brocca, L. Cantù, M. Corti, E.D. Favero, S. Motta, Langmuir 20, 2141 (2004).CrossRefGoogle Scholar
  60. 60.
    P. Schleger et al., Physica B 266, 49 (1999).ADSCrossRefGoogle Scholar
  61. 61.
    B. Farago, D. Richter, J.S. Huang, S.A. Safran, S.T. Milner, Phys. Rev. Lett. 65, 3348 (1990).ADSCrossRefGoogle Scholar
  62. 62.
    D. Chapman, Q. Rev. Biophys. 8, 185 (1975).CrossRefGoogle Scholar
  63. 63.
    I. López-Montero, L.R. Arriaga, G. Rivas, M. Vélez, F. Monroy, Chem. Phys. Lipids 163, 56 (2010).CrossRefGoogle Scholar
  64. 64.
    W. Rawicz, K.C. Olbrich, T. McInstosh, D. Needham, E. Evans, Biophys. J. 79, 328 (2000).CrossRefGoogle Scholar
  65. 65.
    N. Kucerka, S. Tristram-Nagle, J.F. Nagle, J. Memb. Biol. 208, 193 (2005).CrossRefGoogle Scholar
  66. 66.
    A.C. Woodka, P.D. Butler, L. Porcar, B. Farago, M. Nagao, Phys. Rev. E 80, 031606 (2009).CrossRefGoogle Scholar
  67. 67.
    H. Seto, N.L. Yamada, M. Nagao, M. Hishida, T. Takeda, Eur. Phys. J. E 26, 217 (2008).CrossRefGoogle Scholar
  68. 68.
    R. Rodríguez-García, M. Mell, I. López-Montero, J. Netzel, T. Hellweg, F. Monroy, Soft Matter 7, 1532 (2011).ADSCrossRefGoogle Scholar
  69. 69.
    R. Rodríguez-García, M. Mell, I. López-Montero, F. Monroy, Europhys. Lett. 94, 28009 (2011).ADSCrossRefGoogle Scholar
  70. 70.
    H. Bermúdez et al., Macromolecules 35, 8203 (2002).ADSCrossRefGoogle Scholar
  71. 71.
    M. Nagao, S. Chawang, T. Hawa, Soft Matter 7, 6598 (2011).ADSCrossRefGoogle Scholar
  72. 72.
    M. Nagao, J. Chem. Phys. 135, 074704 (2011).CrossRefGoogle Scholar

Copyright information

© EDP Sciences, SIF, Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michael Mell
    • 1
  • Lara H. Moleiro
    • 1
    • 2
  • Yvonne Hertle
    • 3
  • Peter Fouquet
    • 4
  • Ralf Schweins
    • 5
  • Iván López-Montero
    • 1
  • Thomas Hellweg
    • 3
    Email author
  • Francisco Monroy
    • 1
  1. 1.Departamento de Química Física IUniversidad Complutense de MadridMadridSpain
  2. 2.Physikalische Chemie IUniveristät BayreuthBayreuthGermany
  3. 3.Physikalische und Biophysikalische Chemie IUniversität BielefeldBielefeldGermany
  4. 4.TOF/HR GroupInstitut Laue LangevinGrenoble Cedex 9France
  5. 5.DS/LSS - ILL Soft Matter Partnership LabInstitut Laue LangevinGrenoble Cedex 9France

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