Elasticity of the red cell membrane and its relation to hemolytic disorders: An optical tweezers study

Biophysical Journal

Volumn 77, Issue 6, 1999, Pages 3085-3095

  Sleep, John ^a   Wilson, David ^a   Simmons, Robert ^a   Gratzer, Walter ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ERYTHROCYTE MEMBRANE; HEMOLYTIC ANEMIA; MEASUREMENT; MECHANICAL STRESS; PROTEIN PHOSPHORYLATION; STRUCTURE ANALYSIS; VISCOELASTICITY; YOUNG MODULUS;

EID: 0032796312     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(99)77139-0     Document Type: Article

References (55)

1. Berk, D. A., R. M. Hochmuth, and R. E. Waugh. 1989. Viscoelastic properties and rheology. In Red Blood Cell Membranes. P. Agre and J. C. Parker, editors. Marcel Dekker Inc, New York and Basel, pp. 423-454.
2. Boal, D. 1994. Computer simulation of a model network for the erythrocyte cytoskeleton. Biophys. J. 67:521-529.
3. Bronkhorst, P. J. H., G. J. Streeker, J. Grimbergen, E. J. Nijhof, J. J. Sixma, and G. J. Brakenhoff. 1995. A new method to study shape recovery of red blood cells using multiple optical trapping. Biophys. J. 69: 1666-1673.
4. Chabanel, A., M. Flamm, K. L. P. Sung, M. M. Lee, D. Schachter, and S. Chien. 1983. Influence of cholesterol content on red cell membrane viscoelasticity and fluidity. Biophys. J. 44:171-176.
5. Chabanel, A., K. L. P. Sung, J. Rapiejko, J. T. Prchal, S.-C. Liu, and S. Chien. 1989. Viscoelastic properties of red cell membrane in hereditary elliptocytosis. Blood. 73:592-595.
6. Chasis, J. A., and N. Mohandas. 1986. Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein associations. J. Cell Biol. 103: 343-350.
7. Discher, D. E., and N. Mohandas, 1996. Kinematics in red-cell aspiration by fluorescence imaged microdeformation. Biophys. J. 71:1680-1694.
8. Elias, P. M., J. Goerke, and D. S. Friend. 1978. Freeze-fracture identification of sterol-digitonin complexes in cell and liposome membranes. J. Cell Biol. 78:577-593.
9. Evans, E. A. 1973. A new membrane concept applied to the analysis of fluid shear- and micropipette-deformed red blood cells. Biophys. J. 13:941-954.
10. Evans, E. A. 1983. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys. J. 43:27-30.
11. Evans, E. A., and R. M. Hochmuth. 1978. Mechano-chemical properties of membrane. Curr. Top. Membr. Transp. 10:1-64.
12. Evans, E. A., and W. Ravicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64: 2094-2097.
13. Fairbanks G, T. L. Steck, and D. F. H. Wallach. 1971. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 10:2606-2617.
14. Faucon, J. F., M. D. Mitov, P. Meleard, I. Rivas, and P. Bothorel. 1989. Bending elasticity and thermal fluctuations of lipid membranes. Theoretical and experimental requirements. J. Physiol. (Paris). 50: 2389-2392.
15. Fischer, T. M., C. W. M. Haest, M. Stohs, D. Kamp, and B. Deuticke. 1978. Selective alteration of erythrocyte deformability by SH-reagents. Evidence for involvement of spectrin in membrane shear elasticity. Biochim. Biophys. Acta. 510:270-282.
16. Gordon, S., and G. B. Ralston. 1990. Solubilization and denaturation of monomeric actin from erythrocyte membranes by p-chloromercuribenzenesulfonate. Biochim. Biophys. Acta. 1025:43-48.
17. Hall, T. G., and V. Bennett. 1987. Regulatory domains of erythrocyte ankyrin. J. Biol. Chem. 262:10537-10545.
18. Hansen, J. C., R. Skalak, S. Chien, and A. Hoger. 1996. An elastic network model based on the structure of the red blood cell membrane skeleton. Biophys. J. 70:146-166.
19. Hansen, J. C., R. Skalak, S. Chien, and A. Hoger. 1997a. Spectrin properties and the elasticity of the red blood cell membrane skeleton. Biorheology. 34:327-348.
20. Hansen, J. C., R. Skalak, S. Chien, and A. Hoger. 1997b. Influence of network topology on the elasticity of the red blood cell membrane skeleton. Biophys. J. 72:2369-2381.
21. Hemming, N. J., D. J. Anstee, M. A. Staricoff, M. J. A. Tanner, and N. Mohandas. 1995. Identification of the membrane attachment sites for protein 4.1 in the human erythrocyte. J. Biol. Chem. 270:5360-5366.
22. Hénon, S., G. Lenormand, A. Richert, and F. Gallet. 1999. A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys. J. 76:1145-1151.
23. Hochmuth, R. M., and W. L. Hampel. 1979. Surface elasticity and viscosity of red cell membrane. J. Rheology 23:669-680.
24. Jay, A. W. L. 1975. Geometry of the human erythrocyte. I. Effect of albumin on cell geometry. Biophys. J. 15:205-222.
25. Jinbu, Y., S. Sato, T. Nakao, M. Nakao, S. Tsukita, and S. Tsukita. 1984. The role of ankyrin in shape and deformability change of human erythrocyte ghosts. Biochim. Biophys. Acta. 773:237-245.
26. Kadie;s, J., and E. Sackmann, E. 1991. Shape transitions and shape stability of giant phospholipid vesicles in pure water induced by area-to-volume changes. Biophys. J. 60:825-844.
27. Kates, M. 1972. Techniques in Lipidology. North-Holland/American Elsevier, Amsterdam, London, New York. 352-365.
28. Kozlov, M. M., and V. S. Markin. 1987. Model of red blood cell membrane skeleton: electrical and mechanical properties. J. Theor. Biol. 129: 439-452.
29. Kuypers, F. A., R. A. Lewis, M. Hua, M. A. Schott, D. Discher, J. D. Ernst, and B. H. Lubin. 1996. Detection of altered membrane phospholipid asymmetry in subpopulations of human red blood cells using fluorescently labeled annexin V. Blood. 7:1179-1187.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of bacteriophage T4. Nature. 227:680-685.
31. Liu, S.-C., L. H. Derick. P. Agre, and J. Palek. 1990. Alterations of the erythrocyte membrane skeletal infrastructure in hereditary spherocytosis, hereditary elliptocytosis, and pyropoikilocytosis. Blood. 76: 198-206.
32. Liu, S.-C., and J. Palek. 1980. Spectrin tetramer-dimer equilibrium and the stability of erythrocyte membrane skeletons. Nature. 285:586-588.
33. Lux, S. E., and J. Palek. 1995. Disorders of the red cell membrane. In Blood: Principles and Practice of Hematology. R. I. Handin, S. E. Lux, and T. P. Stossel, editors. J. B. Lippincott Co., Philadelphia. 1701-1818.
34. McGough, A. M., and R. Josephs. 1990. On the structure of erythrocyte spectrin in partially expanded membrane skeletons. Proc. Natl. Acad. Sci. USA. 87:5208-5212.
35. Maksymiw, R., S. Sui, H. Gaub, and E. Sackmann. 1987. Electrostatic coupling of spectrin dimers to phosphatidylserine containing lipid lamellae. Biochemistry. 26:2983-2990.
36. Meiselman, H. J., E. A. Evans, and R. M. Hochmuth. 1978. Membrane mechanical properties of ATP-depleted human erythrocytes. Blood. 52: 499-504.
37. Mohandas, N., and E. Evans. 1994. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Ann. Rev. Biophys. Biomol. Struct. 23:787-818.
38. Needham, D., and R. S. Nunn. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesyterol. Biophys. J. 58: 997-1009.
39. Parker, K. H., and C. P. Winlove. 1999. Deformation of spherical vesicles with permeable, constant-area membranes: application to red cells. Biophys. J. 77:3096-3107.
40. Peters, L. L., R. A. Shivadasani, S.-C. Liu, M. Hanspal, K. M. John, J. M. Gonzalez, C. Brugnara, B. Gwynn, N. Mohandas, S. L. Alper, S. H. Orkin, and S. E. Lux. 1996. Anion exchanger 1 (band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell. 86:917-927.
41. Pinder, J. C., A. Pekrun, A. M. Maggs, A. P. R. Brain, and W. B. Gratzer. 1995. Association state of human red blood cell band 3 and its interaction with ankyrin. Blood. 85:2951-2961.
42. Pinder, J. C., A. G. Weeds, and W. B. Gratzer. 1986. Study of actin filament ends in the human red cell membrane. J. Mol. Biol. 191: 461-468.
43. Rangachari, K., G. H. Beaven, G. B. Nash, B. Clough, A. R. Dluzewski, Myint-Oo, R. J. M. Wilson, and W. B. Gratzer. 1989. A study of red cell membrane properties in relation to malarial invasion. Mol. Biochem. Parasitol. 34:63-74.
44. Schneider, M. D., J. T. Jenkins, and W. W. Webb. 1984. Thermal fluctuations of large quasi-spherical bimolecular phospholipid vesicles. J. Physiol. (Paris). 45:1457-1462.
45. Seeman, P. 1967. Transient holes in the erythrocyte membrane during hypotonic hemolysis and stable holes in the membrane after lysis by saponin and lysolecithin. J. Cell Biol. 32:55-70.
46. Seeman, P., D. Cheng, and G. H. Iles. 1973. Structure of membrane holes in osmotic and saponin hemolysis. J. Cell Biol. 56:519-527.
47. Stokke, B. T., A. Mikkelsen, and A. Elgsaeter. 1986a. The human erythrocyte membrane skeleton may be an ionic gel. I. Membrane mechano-chemical properties. Eur. Biophys. J. 13:203-218.
48. Stokke, B. T., A. Mikkelsen, and A. Elgsaeter. 1986b. The human erythrocyte membrane skeleton may be an ionic gel. III. Micropipette aspiration of unswollen erythrocytes. J. Theor. Biol. 123:205-211.
49. Strey, H., M. Peterson, and E. Sackmann. 1995. Measurement of erythrocyte membrane elasticity by flicker eigenmode decomposition. Biophys. J. 69:478-488.
50. Svoboda, K., C. F. Schmidt, D. Branton, and S. M. Block. 1992. Conformation and elasticity of the isolated red blood cell membrane skeleton. Biophys. J. 63:784-793.
51. Treloar, L. R. G. 1975. The Physics of Rubber Elasticity. Clarendon Press, Oxford, U.K. 74-79
52. Tyler, J. M., B. N. Reinhardt, and D. Branton. 1980. Association of erythrocyte membrane proteins. Binding of purified bands 2.1 and 4.1 to spectrin. J. Biol Chem. 255:7034-7049.
53. Vertessy, B. G., and T. L. Steck. 1989. Elasticity of the human red cell membrane skeleton. Effects of temperature and denaturants. Biophys. J. 55:255-262.
54. Waugh, R. E., and P. Agre. 1988. Reduction of erythrocyte membrane viscoelastic coefficients reflect spectrin deficiencies in hereditary spherocytosis. J. Clin. Invest. 81:133-141.
55. Yi, S. J., S.-C. Liu, L. H. Derick, J. Murray, J. E. Barker, M. R. Cho, J. Palek, and D. E. Golan. 1997. Red cell membranes of ankyrin-deficient mice lack band 3 tetramers but contain normal skeletons. Biochemistry. 36:9596-9604.