Abstract
Physical and biophysical mechanisms of mechano-sensitivity of cell membranes are reviewed. The possible roles of the lipid matrix and of the cytoskeleton in membrane mechanoreception are discussed. Techniques for generation of static strains and dynamic curvatures of membrane patches are considered. A unified model for stress-activated and stress-inactivated ion channels under static strains is described. A review of work on stress-sensitive pores in lipid-peptide model membranes is presented. The possible role of flexoelectricity in mechano-electric transduction, e.g. in auditory receptors is discussed. Studies of flexoelectricity in model lipid membranes, lipid-peptide membranes and natural membranes containing ion channels are reviewed. Finally, possible applications in molecular electronics of mechanosensors employing some of the recognized principles of mechano-electric transduction in natural membranes are discussed.
Similar content being viewed by others
Abbreviations
- BLM:
-
Layer lipid membrane
- SAC:
-
stress-activated channel
- SIC:
-
stress-inactivated channel
- MCYST:
-
microcystin-LR
- DPhL:
-
diphytanoyl lecithin
- CME:
-
condenser microphone effect
References
Beresnev LA, Blinov LM, Kovshev EI (1982) On the possibility of ferroelectricity in biomembranes. DAN SSSR 265:210–213
Blumenfeld LA (1974) Problemi biologicheskoj fiziki. Nauka, Moscow
Bograchova TJ, Passechnik VI, Sokolov VS (1974) The influence of periodical stretch on the conductivity of modified bilayer lipid membranes. Study Biophys 42:75–76
Brasseur R (1991) Differentiation of lipid-associating helices by use of three-dimensional molecular hydrophobicity potential calculations. J Biol Chem 266:16120–16127
Brehm P, Kullberg R, Moody-Corbett F (1984) Properties of nonjunctional acetylcholine receptor channel on innervated muscle of Xenopus laevis. J Physiol 350:631–648
Brochard F, Lennon JF (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys 36:1035–1047
Clausen C, Fernandez JM (1981) A low cost method for rapid transfer function measurement with direct application to biological impedance analysis. Pfluegers Arch Eur J Physiol 390:290–294
Coronado R, Latorre R (1983) Phospholipid bilayers made from monolayers on patch-clamp pipettes. Biophys J 43:231–236
Delcour AH, Martinac B, Adler J, Kung C (1989) Modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels. Biophys J 56:631–636
Derzhanski A, Petrov AG (1982) Multipole model of the molecular asymmetry in thermotropic and lyotropic liquid crystals. Mol Cryst Liq Cryst 89:339–360
Derzhanski A, Petrov AG, Pavloff YV (1981) Curvature-induced conductive and displacement currents through lipid bilayers. J Phys Lett (Paris) 42: L119-L122
Derzhanski A, Petrov AG, Todorov A (1989) Flexoelectricity of layered and columnar lyotropic phases. Bulg J Phys (Sofia) 16:268–280
Derzhanski A, Petrov AG, Todorov A, Hristova K (1990) Flexoelectricity of lipid bilayers. Liq Cryst 7:439–449
Duwe H-P 1989 Korrelationsanalyse thermischer Formfluktuationen von Vesikeln mittels schneller, digitaler Bildverarbeitung. Dissertation, TU Munich
Duwe H-P, Engelhardt H, Zilker A, Sackmann E (1987) Curvature elasticity of smectic A lipid bilayers and cell plasma membranes. Mol Cryst Liq Cryst 152:1–7
Duwe H-P, Eggl P, Sackmann E (1989) The cell plasma membrane as composite system of two-dimensional liquid crystal and macromolecular network and how to mimick its physical properties. Angew Makromol Chem 166/167:1–19
Evans EA, Hochmuth RM (1978) Mechanochemical properties of membranes. In: Kleinzeller A, Bronner F (eds) Current topics in membranes and transport, vol 10. Academic Press, New York, pp 1–62
Evans EA, Needham D (1986) Giant vesicle bilayers composed of mixtures of lipids, cholesterol and polypeptides. Faraday Discuss Chem Soc 81:267–280
Evans EA, Rawicz W (1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett 64:2094–2097
Fidler N, Fernandez JM (1989) Phase tracking: an improved phase detection technique for cell membrane capacitance measurements. Biophys J 56:1153–1162
Flerov MN (1981) Mechanosensitivity and current-voltage characteristics of ion channels in bilayer lipid membranes. PhD Thesis, Moscow State University
Gruen DWR, Wolfe J (1982) Lateral tensions and pressures in membranes and lipid monolayers. Biochim Biophys Acta 688:572–580
Guharay F, Sachs F (1984) Stretch-activated single ion channel currents in tissue-cultured embrionic chick skeletal muscle. J Physiol 352:685–701
Gustin MC, Zhou X-L, Martinac B, Kung C (1988) A mechanosensitive ion channel in the yeast plasma membrane. Science 242:762–765
Hamill OP, Lane JW McBride Jr DW (1992) Amiloride: a molecular probe for mechanosensitive channels. TiPS 13:373–376
Harbich W Helfrich W (1979) Alignment and opening of giant lecithin vesicles by electric fields. Z Naturforsch 34a:1063–1065
Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch 28c:693–703
Hladky SB, Hayden DA (1984) Ion movements in gramicidin channels. In: Brenner F (ed) Current topics in membranes and transport, vol 21. Academic Press, New York, pp 327–372
Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17:99–124
Huang HW (1986) Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime. Biophys J 50:1061–1070
Hudspeth AJ (1982) Extracellular current flow and the site of transduction by vertebrate hair cells. J Neurosci 2:1–10
Hudspeth AJ (1983) Mechanoelectrical transduction by hair cells in the acousticolateralis sensory system. Ann Rev Neurosci 6:187–215
Joshi C, Fernandez JM (1988) Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis. Biophys J 53:885–892
Katchalski A, Curran PF (1965) Nonequilibrium thermodynamics in biophysics, Chapter 10. Harvard University Press, Cambrige Mass
Kwok R, Evans E (1981) Thermoelasticity of large lecithin bilayer vesicles. Biophys J 35:637–652
Lecar H, Morris CE (1993) Biophysics of mechanotransduction. In: Rubanyi GM (ed) Mechanoreception by the vascular wall. Futura Publ Co, Inc, Mount Kisco, NY, pp 1–11
Lennon JF (1977) Le scintillement de l'erythrocyte. Doctoral thesis, University Paris-Sud, Orsay
Litster JD (1975) Stability of lipid bilayers and red blood cell membranes. Phys Lett 53A:193–194
Loizjanskii LG (1987) Fluid and gas mechanics (in Russian). Moscow, Nauka
Markin VS, Martinac B (1991) Mechanosensitive ion channels as reporters of bilayer expansion. Biophys J 60:1120–1127
Matrinac B, Adler J, Kung C (1990) Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348:261–263
Meyer RB (1969) Piezoelectric effects in liquid crystals. Phys Rev Lett 22:918–922
Mitov MD, Faucon JF, Meleard P, Bothorel P (1992) Thermal fluctuations of membranes. Adv Supramol Chem 2:93–139
Morris CE (1990) Mechanosensitive ion channels. J Membr Biol 113:93–107
Morris CE, Horn R (1991) Failure to elicit neuronal macroscopic mechanosensitive currents anticipated by single-channel studies. Science 251:1246–1249
Morris CE, Sigurdson WJ (1989) Stretch-inactivated ion channels coexist with stretch-activated ion channels. Science 243:807–809
Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci, USA 79:6712–6716
Neumann E, Sowers AE, Jordan CA (eds) (1989) Electroporation and electrofusion in cell biology. Plenum Press, New York London
Ochs AL, Burton RM (1974) Electrical response to vibration of a lipid bilayer membrane. Biophys J 37:667–672
Olesen S-P, Clapham D, Davies PF (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331:168–170
Parisi M, Rivas E (1971) Transient conductance changes induced by pressure in artificial lipidic membranes. Biochim Biophys Acta 233:469–473
Passechnik VI (1972) Modelling of mechanoreception with the help of modified bimolecular membranes. 4th Internat Biophys Congress, Moscow 1972. Abstracts vol 4, E XVIa 5/9, pp 44–45
Passechnik VI (1974) Possible mechanism of functioning of the elementary mechanosensitive center. Biofizika (Moscow) 19:1020–1924
Passechnik VI (1977) The problem of energy transformation in mechanoreceptors. Biofizika (Moscow) 22:1024–1029
Passechnik VI (1983) Viscoelastic properties of biomembrane models and mechanoreception processes. DSc Thesis, Moscow State University
Passechnik VI (1988) Mechanisms of the hearing organ (in Russian). Ace Sci Techn VINITI. Human and Animal Physiol Ser 39:6121
Passechnik VI, Bichkova EJ (1978) Piezoeffect, background conductivity and filtration coefficient of bilayer lipid membranes. Biofizika (Moscow) 23:551–552
Passechnik VI, Flerov MN (1983) Influence of the mechanical deformation of membrane on the parameters of the ion channel formed by gramicidin A. In: Bilayer lipid membranes. Far East Sci Center Acad Sci USSR, Vladivostok, pp 90–110
Passechnik VI, Sokolov VS (1973) Permeability change of modified bimolecular phospholipid membranes accompanying periodical expansion. Biofizika (Moscow) 18:655–660
Passechnik VI, Vitvizki VM (1975) Mechanosensitivity of the membranes modified with the pore-forming substances. Biofizika (Moscow) 20:332–333
Pastushenko VF, Petrov AG (1984) Electromechanical mechanism of pore formation in bilayer lipid membranes. Seventh School Biophys Membrane Transport, Poland, School Proc vol 2:69–91
Petrov AG (1975) Flexoelectric model for active transport. In: Physical and chemical bases of biological information transfer. Plenum Press, New York London, pp 111–125
Petrov AG (1978) Mechanisms of curvature-induced membrane polarization and their influence on some membrane properties. Studia biophysica 74:51–52; Microfiche 4:14–25
Petrov AG (1981) The problem of self-assembly of lipids and proteins into liquid crystalline membrane structures. Sixth School Biophys Membrane Transport, Poland. School Proc Wroclaw 1:116–145
Petrov AG (1984) Flexoelectricity of lyotropics and biomembranes. Nuovo Cimento 3D:174–192
Petrov AG (1986) Molecular physics and biophysical aspects of lyotropic liquid crystalline state of matter. DSc Thesis, Bulgarian Academy of Sciences, Sofia
Petrov AG (1988) Generalized lipid asymmetry and instability phenomena in membranes. Ninth School Biophys Membrane Transport, Poland, School Proc Wroclaw 2:67–86
Petrov AG (1992) Flexoelectricity of membranes and electric double layers. In: Jennings BR, Stoylov SP (eds) Colloid and molecular electrooptics. Inst Physics Publ. Bristol Philadelphia, pp 171–176
Petrov AG, Bivas I (1984) Elastic and flexoelectric aspects of out-ofplane fluctuations in biological and model membranes. Prog Surface Sci 16:386–512
Petrov AG, Derzhanski A (1976) On some problems in the theory of elastic and flexoelectric effects in bilayer lipid membranes and biomembranes. J Phys Suppl 37:C3–155-C3–160
Petrov AG, Derzhanski A (1987) Generalized asymmetry of thermotropic and lyotropic mesogens. Mol Cryst Liq Cryst 151:303–333
Petrov AG, Sokolov VS (1986) Curvature-electric effect in black lipid membranes. Dynamic characteristics. Eur Biophys J 13:139–155
Petrov AG, Seleznev SA, Derzhanski A (1979) Principles and methods of liquid crystal physics applied to the structure and functions of biological membranes. Acta Phys Pol A55:385–405
Petrov AG, Mitov MD, Derzhanski A (1980) Edge energy and pore stability in bilayer lipid membranes. In: Bata L (ed) Adv liquid crystal res appls. Pergamon Press, Oxford, pp 695–737
Petrov AG, Ramsey RL, Usherwood PNR (1989) Curvature-electric effects in artificial and natural membranes studied using patchclamp techniques. Eur Biophys J 17:13–17
Petrov AG, Ramsey RL, Codd GA, Usherwood PNR (1991a) Modelling mechanosensitivity in membranes: Effects of lateral tension on ionic pores in a microcystin-toxin containing membrane. Eur Biophys J 20:17–29
Petrov AG, Todorov AT, Bonev B, Blinov LM, Subachyus DB, Tsvetkova N (1991b) Manifestation of ferroelectricity in lyotropics with chiral additives: Biomembranes' analogs. Ferroelectrics 114:415–427
Petrov AG, Usherwood PNR, Miller BA (1992) Mechano-electricity of guest-host membrane systems: lipid bilayers containing ion channels. Mol Cryst Liq Cryst 215:109–119
Petrov AG, Miller BA, Hrtistova K, Usherwood PNR (1993) Flexoelectric effects in model and native membranes containing ion channels. Eur Biophys J 22:283–300
Sachs F (1986) Biophysics of mechanoreception. Membr Biochem 6:173–195
Sachs F (1987) Baroreceptor mechanisms at the cellular level. Fed Proc 46:12–16
Sachs F (1988) Mechanical transduction in biological systems. CRC Crit Rev Biomed Eng 16:141–169
Sachs F (1989) In: Stein WD, Bronner F (eds) Cell shape: Determinants, regulation and regulatory role. Academic Press, New York, pp 63–92
Sachs F, Lecar H (1991) Stochastic models for mechanical transduction. Biophys J 59:1143–1145
Sackmann E (1978) Dynamic molecular organization in vesicles and membranes. Ber Bunsenges Phys Chem 82:891–909
Sackmann E (1983) Physical foundations of the molecular organization and dynamics of membranes. In: Hoppe W Lohmann W, Markl H, Ziegler H (eds) Biophysics. Springer, Berlin Heidelberg, pp 425–457
Sackmann E (1984) Physical basis of trigger processes and membrane structure. In: Chapman D (ed) Biological membranes. Vol 5. Academic Press, London, pp 105–143
Sackmann E, Duwe H-P, Pfeiffer W (1989) On the biomembranes as composite lamellae of smectic A liquid crystal and macro molecular network: elastic properties, local and collective dynamics. Phys Scr T25:107–113
Sakmann B, Neher E (eds) (1983) Single-channel recordings. Plenum Press, New York
Sansom MSP (1991) The biophysics of peptide models of ion channels. Prog Biophys Mol Biol 55:139–235
Schmidt CF, Baermann M, Isenberg G, Sackmann E (1989) Chain dynamics, mesh size, and diffusive transport in networks of polymerized actin. A quasielastic light scattering and microfluorescence study. Macromolecules 22:3638–3649
Sokabe M, Sachs F, Jing Z (1991) Quantitative videomicroscopy of patch clamped membranes stress, strain, capacitance, and stretch channel activation. Biophys J 59:722–728
Szekely JG, Morash BD (1980) The effect of temperature on capacitance changes in an oscillating model membrane. Biochim Biophys Acta 559:73–80
Todorov AT, Petrov AG, Brandt MO, Fendler JH (1991) Electrical and real-time stroboscopic interferometric measurements of bilayer lipid membrane flexoelectricity. Langmuir 7:3127–3137
Waugh R, Evans E (1979) Thermoelasticity of red blood cell membrane. Biophys J 26:115–132
Zhou X-L, Kung C (1992) A mechanosensitive ion channel in Schizosaccharomices pombe. The EMBO J 11:2869–2875
Zeman K, Engelhard H, Sackmann E (1990) Bending undulations and elasticity of erythrocyte membrane: effects of cell shape and membrane organization. Eur Biophys J 18:203–209
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 48:2139–2151
Author information
Authors and Affiliations
Additional information
Dedicated to Professor Alexander Derzhanski on the occasion of his 60th birthday
Correspondence to: A. G. Petrov
Rights and permissions
About this article
Cite this article
Petrov, A.G., Usherwood, P.N.R. Mechanosensitivity of cell membranes. Eur Biophys J 23, 1–19 (1994). https://doi.org/10.1007/BF00192201
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00192201