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Fluctuations in Active Membranes

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Book cover Physics of Biological Membranes

Abstract

Active contributions to fluctuations are a direct consequence of metabolic energy consumption in living cells. Such metabolic processes continuously create active forces, which deform the membrane to control motility, proliferation as well as homeostasis. Membrane fluctuations contain therefore valuable information on the nature of active forces, but classical analysis of membrane fluctuations has been primarily centered on purely thermal driving. This chapter provides an overview of relevant experimental and theoretical approaches to measure, analyze, and model active membrane fluctuations. In the focus of the discussion remains the intrinsic problem that the sole fluctuation analysis may not be sufficient to separate active from thermal contributions, since the presence of activity may modify membrane mechanical properties themselves. By combining independent measurements of spontaneous fluctuations and mechanical response, it is possible to directly quantify time and energy-scales of the active contributions, allowing for a refinement of current theoretical descriptions of active membranes.

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Notes

  1. 1.

    Note that ion channels do not require metabolic energy consumption by definition and are hence generally considered as passive. However, when a non-zero (electro)chemical potential difference is maintained across the membrane (generally through the action of ion pumps), their gating activity is expected to be of non-equilibrium character [52].

References

  1. Campelo F, Arnarez C, Marrink SJ, Kozlov MM (2014) Helfrich model of membrane bending: from Gibbs theory of liquid interfaces to membranes as thick anisotropic elastic layers. Adv Colloid Interface Sci 208:25–33

    Article  CAS  PubMed  Google Scholar 

  2. Hochmuth RM, Evans CA, Wiles HC, McCown JT (1983) Mechanical measurement of red cell membrane thickness. Science 220:101–102

    Article  CAS  PubMed  Google Scholar 

  3. Browicz T (1890) Further observation of motion phenomena on red blood cells in pathological states. Zbl med Wissen 28:625–627

    Google Scholar 

  4. Tuvia S, Almagor A, Bitler A, Levin S, Korenstein R, Yedgar S (1997) Cell membrane fluctuations are regulated by medium macroviscosity: evidence for a metabolic driving force. Proc Natl Acad Sci U S A 94:5045–5049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Park Y et al (2010) Metabolic remodeling of the human red blood cell membrane. Proc Natl Acad Sci U S A 107:1289–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Betz T, Lenz M, Joanny JF, Sykes C (2009) ATP-dependent mechanics of red blood cells. Proc Natl Acad Sci U S A 106:15320–15325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Turlier H et al (2016) Equilibrium physics breakdown reveals the active nature of red blood cell flickering. Nat Phys 12:513–519

    Article  CAS  Google Scholar 

  8. Cabot RC (1901) A guide to the clinical examination of the blood, 4th edn. Longmans, Green & Co., London, p 52

    Google Scholar 

  9. Pulvertaft RJV (1949) Vibratory movement in the cytoplasm of erythrocytes. J Clin Path 2:281–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Blowers R, Clarkson EM, Maizels M (1951) Flicker phenomenon in human erythrocytes. J Physiol 113:228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Parpart AK, Hoffman JH (1956) Flicker in erythrocytes. “vibratory movements in the cytoplasm”?. J Cell Comp Physiol 47:295–303

    Article  CAS  PubMed  Google Scholar 

  12. Brochard F, Lennon JF (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys (Paris) 36:1035–1047

    Article  Google Scholar 

  13. Evans J, Gratzer W, Mohandas N, Parker K, Sleep J (2008) Fluctuations of the red blood cell membrane: relation to mechanical properties and lack of ATP dependence. Biophys J 94: 4134–4144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Rodríguez-García R, López-Montero I, Mell M, Egea G, Gov NS, Monroy F (2015) Direct cytoskeleton forces cause membrane softening in red blood cells. Biophys J 108:2794–2806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Prost J, Bruinsma R (1996) Shape fluctuations of active membranes. Europhys Lett 33:321–326

    Article  CAS  Google Scholar 

  16. Ramaswamy S, Toner J, Prost J (2000) Nonequilibrium fluctuations, traveling waves, and instabilities in active membranes. Phys Rev Lett 84:3494–3497

    Article  CAS  PubMed  Google Scholar 

  17. Lin LCL, Gov N, Brown FL (2006) Nonequilibrium membrane fluctuations driven by active proteins. J Chem Phys 124:074903

    Article  CAS  Google Scholar 

  18. Manneville JB, Bassereau P, Lévy D, Prost J (1999) Activity of transmembrane proteins induces magnification of shape fluctuations of lipid membranes. Phys Rev Lett 82:4356–4359

    Article  CAS  Google Scholar 

  19. Manneville JB, Bassereau P, Ramaswamy S, Prost J (2001) Active membrane fluctuations studied by micropipette aspiration. Phys Rev E 64:021908

    Article  CAS  Google Scholar 

  20. Faris MEA, Lacoste D, Pécréaux J, Joanny JF, Prost J, Bassereau P (2009) Membrane tension lowering induced by protein activity. Phys Rev Lett 102:038102

    Article  CAS  Google Scholar 

  21. Girard P, Prost J, Bassereau P (2005) Passive or active fluctuations in membranes containing proteins. Phys Rev Lett 94:088102

    Article  CAS  PubMed  Google Scholar 

  22. Hankins HM, Baldridge RD, Xu P, Graham TR (2015) Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution. Traffic 16:35–47

    Article  CAS  PubMed  Google Scholar 

  23. Rao M, Sarasij RC (2001) Active fusion and fission processes on a fluid membrane. Phys Rev Lett 87:128101

    Article  CAS  PubMed  Google Scholar 

  24. Humphrey D, Duggan C, Saha D, Smith D, Käs J (2002) Active fluidization of polymer networks through molecular motors. Nature 416(6879):413–416

    Article  CAS  PubMed  Google Scholar 

  25. Koenderink GH, Dogic Z, Nakamura F, Bendix PM, MacKintosh FC, Hartwig JH, Stossel TP, Weitz DA (2009) An active biopolymer network controlled by molecular motors. Proc Natl Acad Sci USA 106:15192–15197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wickstrand C, Dods R, Royant A, Neutze R (2015) Bacteriorhodopsin: would the real structural intermediates please stand up?. Biochim Biophys Acta Gen Subj 1850:536–553

    Article  CAS  Google Scholar 

  27. Park Y et al (2006) Diffraction phase and fluorescence microscopy. Opt Express 14:8263–8268

    Article  PubMed  Google Scholar 

  28. Monzel C et al (2015) Measuring fast stochastic displacements of bio-membranes with dynamic optical displacement spectroscopy. Nat Commun 6:8162

    Article  CAS  PubMed  Google Scholar 

  29. Zilker A, Ziegler M, Sackmann E (1992) Spectral analysis of erythrocyte flickering in the 0.3–4μm −1 regime by microinterferometry combined with fast image processing. Phys Rev A 46:7998

    Article  CAS  Google Scholar 

  30. Strey H, Peterson M, Sackmann E (1995) Measurement of erythrocyte membrane elasticity by flicker eigenmode decomposition. Biophys J 69:478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pécréaux J, Döbereiner HG, Prost J, Joanny JF, Bassereau P (2004) Refined contour analysis of giant unilamellar vesicles. Eur Phys J E 13:277–290

    Article  PubMed  CAS  Google Scholar 

  32. Brown AT, Kotar J, Cicuta P (2011) Active rheology of phospholipid vesicles. Phys Rev E 84:021930

    Article  CAS  Google Scholar 

  33. Rädler J, Sackmann E (1993) Imaging optical thicknesses and separation distances of phospholipid vesicles at solid surfaces. J Phys II 3:727–748

    Google Scholar 

  34. Monzel C, Sengupta K (2016) Measuring shape fluctuations in biological membranes. J Phys D Appl Phys 49:24

    Article  CAS  Google Scholar 

  35. Schmidt D, Monzel C, Bihr T, Merkel R, Seifert U, Sengupta K, Smith AS (2014) Signature of a nonharmonic potential as revealed from a consistent shape and fluctuation analysis of an adherent membrane. Phys Rev X 4:021023

    Google Scholar 

  36. Betz T, Sykes C (2012) Time resolved membrane fluctuation spectroscopy. Soft Matter 8: 5317–5326

    Article  CAS  Google Scholar 

  37. Peukes J, Betz T (2014) Direct measurement of the cortical tension during the growth of membrane blebs. Biophys J 107:1810–1820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Henon S, Lenormand G, Richert A, Gallet F (1999) A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J 76:1145–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mills JP, Qie L, Dao M, Lim CT, Suresh S (2004) Nonlinear elastic and viscoelastic deformation of the human red blood cell with optical tweezers. Mol Cell Biomech Tech Science Press 1:169–180

    CAS  Google Scholar 

  40. Yoon YZ, Kotar J, Brown AT, Cicuta P (2011) Red blood cell dynamics: from spontaneous fluctuations to non-linear response. Soft Matter 7:2042–2051

    Article  CAS  Google Scholar 

  41. Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28:693–703

    Article  CAS  PubMed  Google Scholar 

  42. Helfrich WS, Servuss RM (1984) Undulations, steric interaction and cohesion of fluid membranes. Il Nuovo Cimento D 3:137–151

    Article  Google Scholar 

  43. Fournier JB, Ajdari A, Peliti L (2001) Effective-area elasticity and tension of micromanipulated membranes. Phys Rev Lett 86:4970

    Article  CAS  PubMed  Google Scholar 

  44. Doi M, Edwards SF (1988) The theory of polymer dynamics. Oxford Science Publications, New York, pp 88–89

    Google Scholar 

  45. Schlosser F, Rehfeldt F, Schmidt C-F (2015) Force fluctuations in three-dimensional suspended fibroblasts. Philos Trans R Soc B 370:20140028

    Article  CAS  Google Scholar 

  46. Almonacid M et al (2015) Active diffusion positions the nucleus in mouse oocytes. Nat Cell Biol 17:470–479

    Article  CAS  PubMed  Google Scholar 

  47. Mizuno D, Tardin C, Schmidt CF, MacKintosh FC (2007) Nonequilibrium mechanics of active cytoskeletal networks. Science 315:370–373

    Article  CAS  PubMed  Google Scholar 

  48. Lacoste D, Bassereau P (2014) An update on active membranes. In: Liposomes, lipid bilayers and model membranes. CRC Press, Boca Raton, pp 1–18

    Google Scholar 

  49. Milner ST, Safran SA (1987) Dynamical fluctuations of droplet microemulsions and vesicles. Phys Rev A 36:4371

    Article  CAS  Google Scholar 

  50. Lomholt MA (2006) Fluctuation spectrum of quasispherical membranes with force-dipole activity. Phys Rev E 73:061914

    Article  CAS  Google Scholar 

  51. Loubet B, Seifert U, Lomholt MA (2012) Effective tension and fluctuations in active membranes. Phys Rev E 85:031913

    Article  CAS  Google Scholar 

  52. Gadsby DC (2009) Ion channels versus ion pumps: the principal difference, in principle. Nat Rev Mol Cell Biol 10:344–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chen HY (2004) Internal states of active inclusions and the dynamics of an active membrane. Phys Rev Lett 92:168101

    Article  PubMed  CAS  Google Scholar 

  54. Chen H-Y, Mikhailov AS (2010) Dynamics of biomembranes with active multiple-state inclusions. Phys Rev E 81:031901–031911

    Article  CAS  Google Scholar 

  55. Gov NS (2004) Membrane undulations driven by force fluctuations of active proteins. Phys Rev Lett 93:268104–268104

    Article  CAS  PubMed  Google Scholar 

  56. Gov NS, Safran SA (2005) Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J 88:1859–1874

    Article  CAS  PubMed  Google Scholar 

  57. Gov NS, Gopinathan A (2006) Dynamics of membranes driven by actin polymerization. Biophys J 90:454–469

    Article  CAS  PubMed  Google Scholar 

  58. Gov NS (2007) Active elastic network: cytoskeleton of the red blood cell. Phys Rev E 75:011921

    Article  CAS  Google Scholar 

  59. Lacoste D, Lau AWC (2005) Dynamics of active membranes with internal noise. Europhys Lett 70:418–424

    Article  CAS  Google Scholar 

  60. Sankararaman S, Menon GI, Sunil Kumar PB (2002) Two-component fluid membranes near repulsive walls: linearized hydrodynamics of equilibrium and nonequilibrium states. Phys Rev E 66:031914–031916

    Article  CAS  Google Scholar 

  61. Gardiner CW (1985) Handbook of stochastic methods for physics, chemistry and the natural sciences. Springer, Berlin, p 77

    Book  Google Scholar 

  62. Seifert U (1995) The concept of effective tension for fluctuating vesicles. Z Phys B 97:299–309

    Article  CAS  Google Scholar 

  63. Gov N, Zilman A, Safran S (2003) Cytoskeleton confinement and tension of red blood cell membranes. Phys Rev Lett 90:228101

    Article  CAS  PubMed  Google Scholar 

  64. Zilker A, Engelhardt H, Sackmann E (1987) Dynamic reflection interference contrast (RIC) microscopy: a new method to study surface excitations of cells and to measure membrane bending elastic moduli. J Phys (Paris) 48:2139–2151

    Article  Google Scholar 

  65. Rädler JO, Feder TJ, Strey HH, Sackmann E (1995) Fluctuation analysis of tension-controlled undulation forces between giant vesicles and solid substrates. Phys Rev E 51:4526

    Article  Google Scholar 

  66. Sackmann E, Smith AS (2014) Physics of cell adhesion: some lessons from cell-mimetic systems. Soft Matter 10:1644–1659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Fournier J-B, Lacoste D, Raphaël E (2004) Fluctuation spectrum of fluid membranes coupled to an elastic meshwork: jump of the effective surface tension at the mesh size. Phys Rev Lett 92:018102–018104

    Article  PubMed  CAS  Google Scholar 

  68. Dubus C, Fournier JB (2007) A Gaussian model for the membrane of red blood cells with cytoskeletal defects. Europhys Lett 75:181–187

    Article  CAS  Google Scholar 

  69. Auth T, Safran SA, Gov NS (2007) Filament networks attached to membranes: cytoskeletal pressure and local bilayer deformation. New J Phys 9:430–430

    Article  CAS  Google Scholar 

  70. Auth T, Safran SA, Gov NS (2007) Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E 76:051910–051918

    Article  CAS  Google Scholar 

  71. Lin L, Brown F (2004) Dynamics of pinned membranes with application to protein diffusion on the surface of red blood cells. Biophys J 86:764–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Evans EA, Parsegian VA (1986) Thermal-mechanical fluctuations enhance repulsion between bimolecular layers. Proc Natl Acad Sci U S A 83:7132–7136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Prost J, Manneville JB, Bruinsma R (1998) Fluctuation-magnification of non-equilibrium membranes near a wall. Eur Phys J B 1:465–480

    Article  CAS  Google Scholar 

  74. Bell GI (1988) Physical basis of cell-cell adhesion. CRC Press, Boca Raton, p 227

    Google Scholar 

  75. Evans E (1985) Detailed mechanics of membrane-membrane adhesion and separation. I. Continuum of molecular cross-bridges. Biophys J 48:175–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bihr T, Seifert U, Smith AS (2012) Nucleation of ligand-receptor domains in membrane adhesion. Phys Rev Lett 109:258101

    Article  PubMed  CAS  Google Scholar 

  77. Bruinsma R, Behrisch A, Sackmann E (2000) Adhesive switching of membranes: experiment and theory. Phys Rev E 61:4253–4267

    Article  CAS  Google Scholar 

  78. Weikl TR, Asfaw M, Krobath H, Rózycki B, Lipowsky R (2009) Adhesion of membranes via receptor–ligand complexes: domain formation, binding cooperativity, and active processes. Soft Matter 5:3213–3224

    Article  CAS  Google Scholar 

  79. Fehon RG, McClatchey AI, Bretscher A (2010) Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11:276–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Charras GT (2008) A short history of blebbing. J Microsc 231:466–478

    Article  CAS  PubMed  Google Scholar 

  81. Alert R, Casademunt J (2016) Bleb nucleation through membrane peeling. Phys Rev Lett 116:068101

    Article  PubMed  CAS  Google Scholar 

  82. Fedosov DA, Caswell B, Karniadakis GE (2010) A multiscale red blood cell model with accurate mechanics, rheology, and dynamics. Biophys J 98:2215–2225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

H. Turlier acknowledges support from the CNRS/Inserm program ATIP-Avenir, from the Bettencourt-Schueller Foundation, and from the Collège de France. T. Betz is supported by the Deutsche Forschungsgemeinschaft (DFG), Cells-in-Motion Cluster of Excellence (EXC 1003-CiM), University of Münster, Germany.

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Authors and Affiliations

  1. Center for Interdisciplinary Research in Biology, Collège de France, PSL Research University, CNRS UMR7241, Inserm U1050, Paris, France

    Hervé Turlier

  2. Institute of Cell Biology, Center for Molecular Biology of Inflammation, Muenster, Germany

    Timo Betz

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  1. Hervé Turlier
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  2. Timo Betz
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Correspondence to Hervé Turlier .

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Editors and Affiliations

  1. PhysicoChimie Curie (UMR CNRS 168), Institut Curie, Paris, France

    Patricia Bassereau

  2. PhysicoChimie Curie (UMR CNRS 168), Institut Curie, Paris, France

    Pierre Sens

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Turlier, H., Betz, T. (2018). Fluctuations in Active Membranes. In: Bassereau, P., Sens, P. (eds) Physics of Biological Membranes. Springer, Cham. https://doi.org/10.1007/978-3-030-00630-3_21

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