Mechanosensitivity of cell membrane may govern creep-strain recovery, osmotic expansion and lysis

• Autorzy: Pawlowski P. H.
• Języki publikacji: EN

Abstrakty

EN

 A simple theoretical model considering cell membrane mechanosensitivity can accurately describe published experimental data on membrane area creeping and recovery, and on osmotic expansion and rupture. The model to data fit reveals real values of membrane tension and elasticity modulus, and the parameters describing membrane organization and kinetics of mechanosensitive membrane traffic, including small solute transport, water permeability, endocytosis, exocytosis, and caveolae formation. This estimation allows for separation and quantitative analysis of the participation of different processes constituting the response of plasmalemma to short time-scale membrane load. The predicted properties of the model were verified for membrane stretching at different osmotic pressures. Finally, a simple hypothesis concerning stressed cell membrane breakdown is postulated.

Słowa kluczowe

PL

cell membrane; surface tension; mechanosensitivity; endocytosis; exocytosis; lysis; osmotic expansion; caveola

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2009
• Tom: 56
• Numer: 3
• Opis fizyczny: p.471-480,fig.,ref.

Twórcy

autor

Pawlowski P. H.

• Institute of Biochemistry and Biophysics, Polish Academy of Sciences, A.Pawinskiego 5a, 02-106 Warsaw, Poland

Bibliografia

• Amin MS, Park YK, Ramachandra NL, Dasari R, Badizadegan K, Feld MS, Popescu G (2007) Microrheology of red blood cell membranes using dynamic scattering microscopy. Opt Express 15: 17001-17009. 
• Ananthakrishnan R, Guck J, Käs J (2006) Cell mechanics: recent advances with a theoretical perspective. Recent Res Devel Biophys 5: 39-69.
• Apodaca G (2002) Modulation of membrane traffic by mechanical stimuli. Am J Physiol Renal Physiol 282: F179-F190.  
• Bausch AR, Ziemann F, Boulbitch AA, Jacobson K, Sackmann E (1998) Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophys J 75: 2038-2049. 
• Boal D (2002) Mechanics of the Cell. University Press, Cambridge.
• Chien S, Sung KLP, Skalak R, Usami S (1978) Theoretical and experimental studies on viscoelastic properties of erythrocyte membrane. Biophys J 24: 463-478. 
• Daily B, Elson EL, Zahalak GI (1984) Cell poking. Determination of the elastic area compressibility modulus of the erythrocyte membrane. Biophys J 45: 671-682. 
• Dao M, Lim CT, Suresha S (2003) Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solids 51: 2259-2280.
• Desprat N, Richert A, Simeon J, Asnacios A (2005) Creep function of a single living cell. Biophys J 88: 2224-2233.  
• Dowgert MF, Wolfe J, Steponkus PL (1987) The mechanics of injury to isolated protoplasts following osmotic contraction and expansion. Plant Physiol 83: 1001-1007. 
• Duszyk M, Schwab B, Zahalak GI, Qian H, Elson EL (1989) Cell poking: quantitative analysis of indentation of thick viscoelastic layers. Biophys J 55: 683-690. 
• Ehrenstein D, Iwasa KH (1996) Viscoelastic relaxation in the membrane of the auditory outer hair cell. Biophys J 71: 1087-1094. 
• Engelhardt H, Sackmann E (1988) On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. Biophys J 54: 495-508. 
• Engström KG, Meiselman HJ (1998) Effects of pressure on red blood cell geometry during micropipette aspiration. Cytometry 23: 22-27. 
• Evans EA, Waugh R, Melnik L (1976) Elastic area compressibility modulus of red cell membrane. Biophys J 16: 585-595 
• Evans EA, Skalak R (1980) Mechanics and Thermodynamics of Biomembranes. CRC Press, Boca Raton, FL.
• Evans EA (1983) Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys J 43: 27-30.  
• Evans E, Heinrich V, Ludwig F, Rawicz W (2003) Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85: 2342-2350. 
• Farago O, Pincus P (2004) Statistical mechanics of bilayer membrane with a fixed projected area. J Chem Phys 120: 2934-2950. 
• Farinas J, Verkman AS (1996) Cell volume and plasma membrane osmotic water permeability in epithelial cell layers measured by interferometry. Biophys J 71: 3511-3522. 
• Firsov NN, Priezzhev AV, Klimova NV, Tyurina AY (2006) Fundamental laws of the deformational behavior of erythrocytes in shear flow. J Eng Phys Thermophys 79: 118-124.
• Fournier JB, Lacoste D, Raphael 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: 018102.1-018102.4. 
• Goldmann WH (2000) Mechanical manipulation of animal cells: cell indentation. Biotechnol Lett 22: 431-435.
• Gov NS, Safran SA (2005) Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J 88: 1859-1874. 
• Guck J, Ananthakrishnan R, Moon TJ, Cunningham CC, Kas J (2000) Optical deformability of soft biological dielectrics. Phys Rev Lett 84: 5451-5454. 
• Guck J, Ananthakrishnan R, Mahmood H, Moon TJ, Cunningham CC, Kas J (2001) The optical stretcher: a novel laser tool to micromanipulate cells. Biophys J 81: 767-784. 
• Hénon 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. 
• Hochmuth RM, Mohandas N, Blackshear PL Jr (1973) Measurement of the elastic modulus for red cell membrane using a fluid mechanical technique. Biophys J 13: 747-762. 
• Hochmuth R (2000) Micropipette aspiration of living cells. J Biomech 33: 15-22. 
• Kon K, Maeda N, Shiga T (1987) Erythrocyte deformation in shear flow: influences of internal viscosity, membrane stiffness, and hematocrit. Blood 69: 727-734. 
• Le Sang Quan KH, Levenson J, Pino MD, Simon A, Devynck MA (1993) In vivo shear flow and erythrocyte membrane fluidity in hypertensive patients. Br J Clin Pharmacol 36: 437-443.  
• Lian GH, Xiang LC, Fa DJ, Qiang JY, Hai HX, Lin LZ, Ying CB, Zhong ZD (2004) Mechanical properties of breast cancer cell membrane studied with optical tweezers. Chinese Phys Let 21: 2543-2546.
• Lim GHW, Wortis M, Mukhopadhyay R (2002) Stomatocyte-discocyte-echinocyte sequence of the human red blood cell: Evidence for the bilayer-couple hypothesis from membrane mechanics. Proc Natl Acad Sci USA 99: 16766-16769 
• Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179: 79-102. 
• Nishi D, Arai T, Inoue K, Takubo T (2005) Measurement of the mechanical properties of living cell using micro hand and developed AFM system. In: Proceedings of IEEE/RSJ International Conference on Intelligent Robots and Systems, 2-6 Aug. 2005, pp. 990-995.
• Noguchi H, Gompper G (2006) Meshless membrane model based on the moving least-squares method. Phys Rev E Stat Nonlin Soft Matter Phys 73: 021903.1-021903.12. 
• Pawlowski PH (2007) Mechanokinetic model of cell membrane; theoretical analysis of plasmalemma homeostasis, growth and division. J Theor Biol 249: 67-76. 
• Pawlowski P, Szutowicz I, Marszalek P, Fikus M (1993) Bioelectrorheological model of the cell. 5. Electrodestruction of cellular membrane in alternating electric field. Biophys J 65: 541-549. 
• Petrov AG, Usherwood PNR (1994) Mechanosensitivity of cell membranes. Eur Biophys J 23: 1-19. 
• Pfafferott C, Nash GB, Meiselman HJ (1985) Red blood cell deformation in shear flow. Effects of internal and external phase viscosity and of in vivo aging. Biophys J 47: 695-704. 
• Poznanski J, Pawlowski P, Fikus M (1992) Bioelectrorheological model of the cell. 3. Viscoelastic shear deformation of the membrane. Biophys J 61: 612-620. 
• Rand RP (1964) Mechanical properties of the red cell membrane. II. Viscoelastic breakdown of the membrane. Biophys J 4: 303-316. 
• Raucher D, Sheetz MP (1999) Characteristics of a membrane reservoir buffering membrane tension. Biophys J 77: 1992-2002. 
• Ruef P, Pöschl JMB, Linderkamp O (2004) Formation and relaxation of erythrocyte membrane tethers in micropipettes. Clin Hemorheol Microcirc 30: 39-46. 
• Sens P, Turner MS (2006) Budded membrane microdomains as tension regulators. Phys Rev E Stat Nonlin Soft Matter Phys 73: 031918. 
• Shao JY, Xu J (2002) A modified micropipette aspiration technique and its application to tether formation from human neutrophils. J Biomech Eng 124: 388-397. 
• Sikorski AF, Hanus-Lorenz B, Jezierski A, Dlużewski AR (2000) Interaction of membrane skeletal proteins with membrane lipid domain. Acta Biochim Polon 47: 565-578. 
• Thoumine O, Ott A, Cardoso O, Meister JJ (1999) Microplates: a new tool for manipulation and mechanical perturbation of individual cells. J Biochem Biophys Methods 39: 47-62. 
• Tu ZC (2006) Elastic theory of membranes. AAPPS Bull 16: 30-33.
• Ursell T, Phillips R, Kondev J, Reeves D, Wiggins PA (2008) The role of lipid bilayer mechanics in mechanosensation. In: Mechanosensitive Ion Channels, pp 37-70 Springer, Netherlands.
• Wang N, Naruse K, Stamenović D, Fredberg JJ, Mijailovich SM, Tolić-Nørrelykke IM, Polte T, Mannix R, Ingber DE (2001) Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci USA 98: 7765-7770.  
• Wang CC, Jian HJ, Wu CW, Lee CH (2008) Cell membrane deformations under magnetic force modulation characterized by optical tracking and non-interferometric widefield profilometry. Microsc Res Tech 71: 594-598. 
• Wanichapichart P, Maswiwat K, Kanchanapoom K (2002) Elastic constant of Dendrobium protoplasts in AC electric fields. Membr Sci Tech 24: 799-806. 
• Wolfe J, Steponkus PL (1983) Mechanical properties of the plasma membrane of isolated plant protoplasts. Mechanism of hyperosmotic and extracellular freezing injury. Plant Physiol 71: 276-285. 
• Wolfe J, Dowgert MF, Steponkus PL (1986) Mechanical study of the deformation and rupture of the plasma membranes of protoplasts during osmotic expansions. J Membr Biol 93: 63-74.
• Yamashina S, Katsumata O (2000) Structural analysis of red blood cell membrane with an atomic force microscope. J Electron Microsc 49: 445-451