Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton

Journal of Cell Biology

Volumn 142, Issue 4, 1998, Pages 989-1000

  Tomishige, Michio ^a,b   Sako, Yasushi ^a,c   Kusumi, Akihiro ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Erythrocyte membrane; Lateral diffusion; Membrane skeleton; Optical tweezers; Single particle tracking

Indexed keywords

ERYTHROCYTE BAND 3 PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; SPECTRIN; TRYPSIN;

ARTICLE; CONFORMATIONAL TRANSITION; DIFFUSION; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; HUMAN TISSUE; MEMBRANE BINDING; MEMBRANE STRUCTURE; OSCILLATION; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; CELL MEMBRANE; CYTOSKELETON; DIFFUSION; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; GOLD COLLOID; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, VIDEO; SPECTRIN; TRYPSIN;

EID: 0032563615     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.4.989     Document Type: Article

References (68)

1. Bennett, V. 1985. The membrane skeleton of human erythrocytes and its implications for more complex cells. Annu. Rev. Biochem. 54:273-304.
2. Bennett, V. 1990. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol. Rev. 70:1029-1065.
3. Bennett, V., and P.J. Stenbuck. 1979. The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature. 280:468-473.
4. Bennett, V., and D.M. Gilligan. 1993. The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu. Rev. Cell Biol. 9:27-66.
5. Berk, D.A., and R.M. Hochmuth. 1992. Lateral mobility of integral proteins in red blood cell tethers. Biophys. J. 61:9-18.
6. Blackman. S.M., C.E. Cobb, A.H. Beth, and D.W. Piston. 1996. The orientation of eosin-5-maleimide on human erythrocyte band 3 measured by fluorescence polarization microscopy. Biophys. J. 71:194-208.
7. Bretscher, A. 1991. Microfilament structure and function in the cortical cytoskeleton. Annu. Rev. Cell Biol. 7:337-374.
8. Bussell, S.J., D.L. Koch, and D.A. Hammer. 1995. Effect of hydrodynamic interactions on the diffusion of integral membrane proteins: diffusion in plasma membranes. Biophys. J. 68:1836-1849.
9. Carraway, K.L., and C.A.C. Carraway. 1989. Membrane-cytoskeleton interactions in animal cells. Biochim. Biophys. Acta. 988:147-171.
10. 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.
11. Che, A., I.E. Morrison, R. Pan, and R.J. Cherry. 1997. Restriction by ankyrin of band 3 rotational mobility in human erythrocyte membranes and reconstituted lipid vesicles. Biochemistry. 36:9588-9595.
12. Choquet, D., D.P. Felsenfeld, and M.P. Sheetz. 1997. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell. 10:39-48.
13. Clague, M.J., J.P. Harrison, and R.J. Cherry. 1989. Cytoskeletal restraints of band 3 rotational mobility in human erythrocyte membranes. Biochim. Biophys. Acta. 981:43-50.
14. Cole, N.B., C.L. Smith, N. Sciaky, M, Terasaki, M. Edidin, and J. Lippincott-Schwartz. 1996. Diffusional mobility of Golgi proteins in membranes of living cells. Science. 274:797-801.
15. Corbett, J.D., P. Agre, J. Palek, and D.E. Golan. 1994. Differential control of band 3 lateral and rotational mobility in intact red cells. J. Clin. Invest. 94: 683-688.
16. De Mey, J. 1983. Colloidal gold probes in immunocytochemistry. In Immunocytochemistry. Practical Applications in Patholgy and Biology. J.M. Polak and S. van Noorden, editors. Wright PSG, Bristol, UK. 82-111
17. Edidin, M., S.C. Kuo, and M.P. Sheetz. 1991. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 254:1379-1382.
18. Edidin, M., M.C. Zúñiga, and M.P. Sheetz. 1994. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc. Natl. Acad. Sci. USA. 91:3378-3382.
19. 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.
20. Golan, D.E., and W. Veatch. 1980. Lateral mobility of band 3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: evidence for control by cytoskeletal interactions. Proc. Natl. Acad. Sci. USA. 77:2537-2541.
21. Golan, D.E., M.R. Alecio, W.R. Veatch, and R.R. Rando. 1984. Lateral mobility of phospholipid and cholesterol in the human erythrocyte membrane: effects of protein-lipid interactions. Biochemistry. 23:332-339.
22. Golan, D.E. 1989. Red blood cell membrane protein and lipid diffusion. In Red Blood Cell Membranes. P. Agre and J.C. Parker, editors. Marcel Dekker, New York. 367-400.
23. Golan, D.E., J.D. Corbett, C. Korsgren, H.S. Thatte, S. Hayette, Y. Yawata, and C.M. Cohen. 1996. Control of band 3 lateral and rotational mobility by band 4.2 in intact erythrocytes: release of band 3 oligomers from low-affinity binding sites. Biophys. J. 70:1534-1542.
24. Hargreaves, W.R., K.N. Giedd, A. Verkleij, and D. Branton. 1980. Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles. J. Biol. Chem. 255:11965-11972.
25. Jinbu, Y., S. Sato, T. Nakao, M. Nakao, Sa. Tsukita, Sh. Tsukita, and H. Ishikawa. 1984. The role of ankyrin in shape and deformability change of human erythrocyte ghosts. Biochim. Biophys. Acta. 773:237-245.
26. Joshi, R., and V. Bennett, 1990. Mapping the domain structure of human erythrocyte adducin. J. Biol. Chem. 265:13130-13136.
27. Kusumi, A., Y. Sako, and M. Yamamoto. 1993. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy): effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65:2021-2040.
28. Kusumi. A., and Y. Sako. 1996. Cell surface organization by the membrane skeleton. Curr. Opin. Cell Biol. 8:566-574.
29. Kusumi, A., Y. Sako, T. Fujiwara, and M. Tomishige. 1998. Application of laser tweezers to studies of the fences and tethers of the membrane skeleton that regulate the movements of plasma membrane proteins. Methods Cell Biol. 55:173-194.
30. Lee, G.M., A. Ishihara, and K.A. Jacobson. 1991. Direct observation of Brownian motion of lipids in a membrane. Proc. Natl. Acad. Sci. USA. 88:6274-6278.
31. Leunissen, J.L.M., and J.R. De Mey, 1989. Preparation of gold probes. In Immuno-Gold Labeling in Cell Biology. A.J. Verkleij and J.L. M. Leunissen, editors. CRC Press. Boca Raton, FL. 3-16.
32. Luna, E.J., and A.L. Hitt. 1992. Cytoskeleton-plasma membrane interactions. Science. 258:955-964.
33. Manno, S., Y. Takakuwa, K. Nagao, and N. Mohandas. 1995. Modulation of erythrocyte membrane mechanical function by β-spectrin phosphorylation and dephosphorylation. J. Biol. Chem. 270:5659-5665.
34. Matayoshi, E.D., and T.M. Jovin. 1991. Rotational diffusion of band 3 in erythrocyte membranes. 1. Comparison of ghosts and intact cells. Biochemistry. 30:3527-3538.
35. Michaely, P., and V. Bennett. 1995. The ANK repeats of ervthrocyte ankyrin form two distinct but cooperative binding sites for the erythrocyte anion exchanger. J. Biol. Chem. 270:22050-22057.
36. Nigg, E.A., and R.J. Cherry. 1980. Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface: protein rotational diffusion measurements. Proc. Natl. Acad. Sci. USA. 77:4702-4706.
37. Poo, M., and R.A. Cone. 1974. Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature. 247:438-441.
38. Porter, R.R. 1959. The hydrolysis of rabbit γ-globulin and antibodies with crystalline papain. Biochem. J. 73:119-126.
39. Pumplin, D.W., and R.J. Bloch. 1993. The membrane skeleton. Trends Cell Biol. 3:113-117.
40. Qian, H., M.P. Shectz, and E.L. Elson. 1991. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60:910-921.
41. Saffman, P.G., and M. Delbrück. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
42. Sako, Y., and A. Kusumi. 1994. Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis. J. Cell Biol. 125:1251-1264.
43. Sako, Y., and A. Kusumi. 1995. Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J. Cell Biol. 129:1559-1574.
44. Sako, Y., A. Nagafuchi, S. Tsukita, M. Takeichi, and A. Kusumi. 1998. Cytoplasmic regulation of the movement of E-cadherin on the free cell surface as studied by optical tweezers and single particle tracking: corralling and tethering by the membrane skeleton. J. Cell Biol. 140:1227-1240.
45. Saxton, M.J. 1982. Lateral diffusion in an archipelago (effects of impermeable patches on diffusion in a cell membrane). Biophys. J. 39:165-173.
46. Saxton, M.J. 1987. Lateral diffusion in an archipelago (the effect of mobile obstacles). Biophys. J. 52:989-997.
47. Saxton, M.J. 1989. The spectrin network as a barrier to lateral diffusion in erythrocytes: a percolation analysis. Biophys. J. 55:21-28.
48. Saxton, M.J. 1990. The membrane skeleton of erythrocytes: models of its effect on lateral diffusion. Int. J. Biochem. 22:801-809.
49. Saxton, M.J. 1995. Single-particle tracking: effects of corrals. Biophys. J. 69: 389-398.
50. Saxton, M.J., and K. Jacobson. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
51. Scaramuzzino, D. A., and J.S. Morrow. 1993. Calmodulin-binding domain of recombinant erythrocyte β-adducin. Proc. Natl. Acad. Sci. USA. 90:3398-3402.
52. Schofield, A.E., M.J.A. Tanner, J.C. Pinder, B. Clough, P.M. Bayley, G.B. Nash, A.R. Dluzewski, D.M. Reardon, T.M. Cox, R.J.M. Wilson, and W.B. Gratzer. 1992. Basis of unique red cell membrane properties in hereditary ovalocytosis. J. Mol. Biol. 223:949-958.
53. Schindler, M., D.E. Koppel, and M.P. Sheetz, 1980. Modulation of membrane protein lateral mobility by polyphosphates and polyamines. Proc. Natl. Acad. Sci. USA. 77:1457-1461.
54. Schütz, G.J., H. Schindler, and Th. Schmidt. 1997, Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys. J. 73:1073-1080.
55. Sheets, E.D., G.M. Lee, R. Simson, and K. Jacobson. 1997. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry. 36:12449-12458.
56. Sheetz, M.P., M. Schindler, and D.E. Koppel. 1980. Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes. Nature. 285: 510-512.
57. Sheetz, M.P. 1993. Glycoprotein motility and dynamic domains in fluid plasma membranes. Annu. Rev. Biophys. Biomol. Struct. 22:417-431.
58. Sheetz, M.P. 1998. Laser Tweezers in Cell Biology. Methods in Cell Biology. Vol. 55. Academic Press, San Diego, CA. 228 pp.
59. Simson, R., B. Yang, S.E. Moore, P. Doherty, F.S. Walsh, and K.A. Jacobson. 1998. Structural mosaicism on the submicron scale in the plasma membrane. Biophys. J. 74:297-308.
60. Smith, D.K., and J. Palek. 1982. Modulation of lateral mobility of band 3 in the red cell membrane by oxidative cross-linking of spectrin. Nature. 297:424-425.
61. Steck, T.L., B. Ramos, and E. Strapazen. 1976. Proteolytic dissection of band 3, the predominant transmembrane polypeptide of the human erythrocyte membrane. Biochemistry. 15:1154-1161.
62. Steck, T.L. 1989. Red Cell Shape. In Cell Shape: Determinants, Regulation and Regulatory Role. W.D. Stein and F. Bronner, editors. Academic Press, San Diego, CA. 205-246.
63. Takeuchi, M., H. Miyamoto, Y. Sako, H. Komizu, and A. Kusumi. 1998. Structure of the erythrocyte membrane skeleton as observed by atomic force microscopy. Biophys. J. 74:2171-2183.
64. Tilley, L., G.B. Nash, G.L. Jones, and W.H. Sawyer. 1991. Decreased rotational diffusion of band 3 in Melanesian ovalocytes from Papua, New Guinea. J. Membr. Biol. 121:59-66.
65. Tsuji, A., and S. Ohnishi. 1986. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state. Biochemistry. 25:6133-6139.
66. Tsuji, A., K. Kawasaki, S. Ohnishi, H. Merkle, and A. Kusumi. 1988. Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork. Biochemistry. 27:7447-7452.
67. Wilson, K.M., I.E.G. Morrison, P.R. Smith, N. Fernandez, and R.J. Cherry. 1996. Single particle tracking of cell-surface HLA-DR molecules using R-phycoerythrin labeled monoclonal antibodies and fluorescence digital imaging. J. Cell Sci. 109:2101-2109.
68. 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 nb/nb mice lack band 3 tetramers but contain normal membrane skeleton. Biochemistry. 36: 9596-9604.