The orientation of eosin-5-maleimide on human erythrocyte band 3 measured by fluorescence polarization microscopy

Biophysical Journal

Volumn 71, Issue 1, 1996, Pages 194-208

  Blackman, Scott M ^a   Cobb, Charles E ^a   Beth, Albert H ^a   Piston, David W ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EOSIN; ERYTHROCYTE BAND 3 PROTEIN; MALEIMIDE DERIVATIVE; MEMBRANE PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ERYTHROCYTE GHOST; ERYTHROCYTE MEMBRANE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

MUS;

EID: 0029885486     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79216-0     Document Type: Article

References (76)

1. Axelrod, D. 1979. Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization. Biophys. J. 26: 557-573.
2. Badley, R. A., W. G. Martin, and H. Schneider. 1973. Dynamic behavior of fluorescent probes in lipid bilayer model membranes. Biochemistry, 12:268-275.
3. Beechem, J. M. 1992. Global analysis of biochemical and biophysical data. Methods Enzymol, 210:37-54.
4. Beechem, J. M., E. Gratton, M. Ameloot, J. R. Knutson, and L. Brand. 1991. The global analysis of fluorescence intensity and anisotropy decay data: second generation theory and programs. In Topics in Fluorescence Spectroscopy, Vol. 2: Principles, J. R. Lakowicz, editor. Plenum Press, New York. 241-305.
5. 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.
6. Benz, R., M. T. Tosteson, and D. Schubert. 1984. Formation and properties of tetramers of band 3 protein from human erythrocyte membranes in planar lipid bilayers. Biochim. Biophys. Acta. 775:347-55.
7. Beth, A. H., T. E. Conturo, S. D. Venkataramu, and J. V. Staros. 1986. Dynamics and interactions of the anion channel in intact human erythrocytes: an electron paramagnetic resonance spectroscopic study employing a new membrane-impermeant bifunctional spin-label. Biochemistry. 25:3824-3832.
8. Bevington, P. R. 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York.
9. Bicknese, S., M. Rossi, B. Thevenin, S. B. Shohet, and A. S. Verkman. 1995. Anisotropy decay measurement of segmental dynamics of the anion binding domain in erythrocyte band 3. Biochemistry. 34: 10645-10651.
10. Blackman, S. M., E. J. Hustedt, A. H. Beth, and D. W. Piston. 1995. Orientation studies of the optical probe eosin-5-maleimide covalently bound to erythrocyte band 3 by confocal polarization microscopy. Biophys. J. 68:A291.
11. Blackman, S. M., E. J. Hustedt, C. E. Cobb, D. W. Piston, and A. H. Beth. 1996. Analysis of rotational diffusion measurements of eosin-5-maleimide-labeled band 3 in terms of the uniaxial rotational diffusion model. Biophys. J. 70:A331.
12. Burghardt, T. P., and K. Ajtai. 1994. Following the trajectory of the principal hydrodynamic frame of a protein using multiple probes. Biochemistry. 33:5376-5381.
13. Casey, J. R., and R. A. F. Reithmeier. 1991. Analysis of the oligomeric state of band 3, the anion transport protein of the human erythrocyte membrane, by size exclusion high performance liquid chromatography. Oligomeric stability and origin of heterogeneity. J. Biol. Chem. 266: 15726-15737.
14. Che, A., and R. J. Cherry. 1995. Loss of rotational mobility of band 3 proteins in human erythrocyte membranes induced by antibodies to glycophorin A. Biophys. J. 68:1881-1887.
15. Cherry, R. J., A. Burkli, M. Busslinger, G. Schneider, and G. R. Parish. 1976. Rotational diffusion of band 3 proteins in the human erythrocyte membrane. Nature. 263:389-393.
16. Cherry, R. J., and R. E. Godfrey. 1981. Anisotropic rotation of bacteriorhodopsin in lipid membranes. Biophys. J. 36:257-276.
17. Cobb, C. E., and A. H. Beth. 1990. Identification of the eosinyl-5-maleimide reaction site on the human erythrocyte anion-exchange protein: overlap with the reaction sites of other chemical probes. Biochemistry. 29:8283-8290.
18. Cobb, C. E., E. J. Hustedt, J. M. Beechem, and A. H. Beth. 1993. Protein rotational dynamics investigated with a dual EPR/optical molecular probe: spin-labeled eosin. Biophys. J. 64:605-613.
19. Corbett, J. D., and D. E. Golan. 1993. Band 3 and glycophorin are progressively aggregated in density-fractionated sickle and normal red blood cells. J. Clin. Invest. 91:208-217.
20. Dix, J. A., and A. S. Verkman. 1990. Mapping of fluorescence anisotropy in living cells by ratio imaging. Application to cytoplasmic viscosity. Biophys. J. 57:231-240.
21. Edmonds, A. R. 1960. Angular Momentum in Quantum Mechanics. Princeton University Press, Princeton, NJ.
22. 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.
23. Florine-Casteel, K. 1990. Phospholipid order in gel- and fluid-phase cell-size liposomes measured by digitized video fluorescence polarization microscopy. Biophys. J. 57:1199-1215.
24. Hellen, E. H., and T. P. Burghardt. 1994. Saturation effects in polarized fluorescence photobleaching recovery and steady state fluorescence polarization. Biophys. J. 66:891-897.
25. Heyn, M. P., R. J. Cherry, and U. Müller. 1977. Transient and linear dichroism studies on bacteriorhodopsin: determination of the orientation of the 568 nm all-trans retinal chromophore. J. Mol. Biol. 117:607-620.
26. Hustedt, E. J., and A. H. Beth. 1995. Analysis of saturation-transfer electron paramagnetic resonance spectra of a spin-labeled integral membrane protein, band 3, in terms of the uniaxial rotational diffusion model. Biophys. J. 69:1409-1423.
27. Hustedt, E. J., and A. H. Beth. 1996. The determination of the orientation of a band 3 affinity spin-label relative to the membrane normal axis of the human erythrocyte. Biochemistry. In press.
28. Jähnig, F. 1986. The shape of a membrane protein derived from rotational diffusion. Eur. Biophys. J. 14:63-64.
29. Jennings, M. L. 1984. Oligomeric structure and the anion transport function of human erythrocyte band 3 protein. Mol. Membr. Biol. 80: 105-117.
30. Johnson, P., and P. B. Garland. 1981. Depolarization of fluorescence depletion: a microscopic method for measuring rotational diffusion of membrane proteins on the surface of a single cell. FEBS Lett. 132: 252-256.
31. Jovin, T. M., and W. L. C. Vaz. 1989. Rotational and translational diffusion in membranes measured by fluorescence and phosphorescence methods. Methods Enzymol. 172:471-513.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
33. 2DIDS on labelled band 3, the erythrocyte anion exchange protein. Mol. Membr. Biol. 12:173-182.
34. Lepke, S., and H. Passow. 1976. Effects of incorporated trypsin on anion exchange and membrane proteins in human red blood cell ghosts. Biochim. Biophys. Acta. 455:353-370.
35. Lieberman, D. M., and R. A. F. Reithmeier. 1988. Localization of the carboxyl terminus of band 3 to the cytoplasmic side of the erythrocyte membrane using antibodies against a synthetic peptide. J. Biol. Chem. 263:10022-10028.
36. Lin, S. W., and R. A. Mathies. 1989. Orientation of the protonated retinal Schiff base group in bacteriorhodopsin from absorption linear dichroism. Biophys. J. 56:653-660.
37. Low, P. S. 1986. Structure and function of the cytoplasmic domain of band 3: center of erythrocyte membrane-peripheral protein interactions. Biochim. Biophys. Acta. 864:145-167.
38. Lux, S. E., K. M. John, R. R. Kopito, H. F. Lodish. 1989. Cloning and characterization of band 3, the human erythrocyte anion-exchange protein (AE1). Proc. Natl Acad. Sci. USA. 86:9089-9093.
39. Macara, I. G., S. Kuo, and L. C. Cantley. 1983. Evidence that inhibitors of anion exchange induce a transmembrane conformational change in band 3. J. Biol. Chem. 258:1785-1792.
40. 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.
41. Matayoshi, E. D., W. H. Sawyer, and T. M. Jovin. 1991. Rotational diffusion of hand 3 in erythrocyte membranes. 2. Binding of cytoplasmic enzymes. Biochemistry. 30:3538-3543.
42. McPherson, R. A., W. H. Sawyer, and L. Tilley. 1992. Rotational diffusion of the erythrocyte integral membrane protein band 3: effect of hemichrome binding. Biochemistry. 31:512-518.
43. McPherson, R. A., W. H. Sawyer, and L. Tilley. 1993. Band 3 mobility in camelid elliptocytes: implications for erythrocyte shape. Biochemistry. 32:6696-6702.
44. Morrison, I. E. G., T. J. Mühlebach, and R. J. Cherry. 1986. Rotational diffusion of band 3 reconstituted into lipid vesicles: an application of global analysis. Biochem. Soc. Trans. 14:885-886.
45. Mühlebach, T. J. 1984. Investigation of the rotational diffusion and self-association of band 3 in the erythrocyte membrane and in reconstituted vesicles. Ph.D. thesis. Eidgenössiche Technische Hochschule, Zurich, Switzerland.
46. 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.
47. Palek, J., and S. Lambert. 1990. Genetics of the red cell membrane skeleton. Semin. Hematol. 27:290-332.
48. Pan, R. J., and R. J. Cherry. 1995. Evidence that eosin-5-maleimide binds close to the anion transport site of human erythrocyte band 3: a fluorescence quenching study. Biochemistry. 34:4880-4888.
49. Pimplikar, S. W., and R. A. F. Reithmeier. 1986. Affinity chromatography of band 3, the anion transport protein of erythrocyte membranes. J. Biol. Chem. 261:9770-9778.
50. Press, W. H., S. A. Teukolsky, W. T. Vetterling, and B. P. Flannery. 1992. Numerical Recipes in Fortran: The Art of Scientific Computing, 2nd Ed. Cambridge University Press, New York.
51. Rao, A., P. Martin, R. A. F. Reithmeier, and L. C. Cantley. 1979. Location of the stilbenedisulfonate binding site of the human erythrocyte anion-exchange system by resonance energy transfer. Biochemistry. 18: 4505-4516.
52. Rigler, R., and M. Ehrenberg. 1973. Molecular interactions and structure as analysed by fluorescence relaxation spectroscopy. Q. Rev. Biophys. 6:139-199.
53. Rodgers, W., and M. Glaser. 1993. Distributions of proteins and lipids in the erythrocyte membrane. Biochemistry. 32:12591-12598.
54. Saffman, P. G., and M. Delbrück. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
55. Salhany, J. M. 1990. Erythrocyte Band 3 Protein. CRC Press, Boca Raton, FL.
56. Sandison, D. R., D. W. Piston, R. M. Williams, and W. W. Webb. 1995. Quantitative comparison of background rejection, signal-to-noise ratio, and resolution in confocal and full-field laser scanning microscopes. Appl. Optics. 34:3576-3588.
57. Sandison, D. R., and W. W. Webb. 1994, Background rejection and signal-to-noise optimization in confocal and alternative fluorescence microscopes. Appl. Optics. 33:603-615.
58. Scothorn, D. S., W. E. Wojcicki, E. J. Hustedt, A. H. Beth, and C. E. Cobb. 1996. Synthesis and characterization of a novel spin-labeled affinity probe of human erythrocyte band 3: characteristics of the stilbenedisulfonate binding site. Biochemistry. In press.
59. Staros, J. V., and B. P. Kakkad. 1983. Cross-linking and chymotryptic digestion of the extracytoplasmic domain of the anion exchange channel in intact human erythrocytes. J. Membr. Biol. 74:247-254.
60. Steck, T. L. 1974. The organisation of proteins in the human red blood cell membrane. A review. J. Cell Biol. 62:1-19.
61. Szabo, A. 1984. Theory of fluorescence depolarization in macromolecules and membranes. J. Chem. Phys. 81:150-167.
62. Tanner, M. J., P. G. Martin, and S. High. 1988. The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. Biochem. J. 256:703-712.
63. Thomas, D. D. 1985. Saturation transfer EPR studies of microsecond rotational motions in biological membranes. In The Enzymes of Biological Membranes, Vol. 2, 2nd Ed. A. N. Martonosi, editor. Plenum Press, New York. 287-312.
64. Thomas, D. D. 1986. Rotational diffusion of membrane proteins. In Techniques for the Analysis of Membrane Proteins. C. I. Ragan and R. J. Cherry, editors. Chapman and Hall, London. 377-431.
65. Timbs, M. M., and N. L. Thompson. 1990. Slow rotational mobilities of antibodies and lipids associated with substrate-supported phospholipid monolayers as measured by polarized fluorescence photobleaching recovery. Biophys. J. 58:413-428.
66. Timbs, M. M., and N. L. Thompson. 1993. Measurement of restricted rotational diffusion of fluorescent lipids in supported planar phospholipid monolayers using angle-dependent polarized fluorescence photobleaching recovery. Biopolymers. 33:45-57.
67. 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.
68. Van der Heide, U. A., B. Orbons, H. C. Gerritsen, and Y. K. Levine. 1992. The orientation of transition moments of dye molecules used in fluorescence studies of muscle systems. Eur. Biophys. J. 21:263-272.
69. Van der Heide, U. A., O. E. Rem, H. C. Gerritsen, E. L. de Beer, P. Schiereck, I. P. Trayer, and Y. K. Levine. 1994. A fluorescence depolarization study of the orientational distribution of cross-bridges in muscle fibres. Eur. Biophys. J. 23:369-378.
70. Van der Meer, W., R. H. P. Kooyman, and Y. K. Levine. 1982. A theory of fluorescence depolarization in macroscopically ordered membrane systems. Chem. Phys. 66:39-50.
71. Wang, D. N. 1994. Band 3 protein: structure, flexibility and function. FEBS Lett. 346:26-31.
72. Wang, D. N., W. Kühlbrandt, V. E. Sarabia, and R. A. F. Reithmeier. 1993. Two-dimensional structure of the membrane domain of human band 3, the anion transport protein of the erythrocyte membrane, EMBO J. 12:2233-2239.
73. Wang, D. N., V. E. Sarabia, R. A. F. Reithmeier, and W. Kühlbrandt. 1994. Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, band 3. EMBO J. 13:3230-3235.
74. Wegener, W. A. 1984. Fluorescence recovery spectroscopy as a probe of slow rotational motions. Biophys. J. 46:795-803.
75. Weinstein, R. S., J. K. Khodadad, and T. L. Steck. 1980. The band 3 protein intramembrane particle of the human red blood cell. In Membrane Transport in Erythrocytes. U. V. Llassen, H. H. Ussing, and J. O. Wieth, editors. Munksgaard, Copenhagen. 35-50.
76. Zannoni, C., A. Arcioni, and P. Cavatorta. 1983. Fluorescence depolarization in liquid crystals and membrane bilayers. Chem. Phys. Lipids. 32:179-250.