Relocation of the disulfonic stilbene sites of AE1 (band 3) on the basis of fluorescence energy transfer measurements

Biochemistry

Volumn 43, Issue 38, 2004, Pages 11917-11931

  Knauf, Philip A ^a   Law, Foon Yee ^a   Leung, Tze Wah Vivian ^a   Atherton, Stephen J ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVITY RESONATORS; CYTOLOGY; ENERGY TRANSFER; FLUORESCENCE; MEMBRANES; PH EFFECTS; PHOTONS;

DISULFONIC STILBENE; FLUORESCENCE RESONANCE ENERGY TRANSFER (FRET); INNER MEMBRANES;

LIPIDS;

4 BENZAMIDO 4' ISOTHIOCYANOSTILBENE 2,2' DISULFONATE; 5 MALEIMIDOFLUORESCEIN; ERYTHROCYTE BAND 3 PROTEIN; GLUTAMIC ACID; MALEIMIDE DERIVATIVE; STILBENE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; LIPID BILAYER; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; STEADY STATE;

4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; 4-ACETAMIDO-4'-ISOTHIOCYANATOSTILBENE-2,2'-DISULFONIC ACID; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; CELL MEMBRANE; CHLORIDES; DIMERIZATION; ERYTHROCYTES; FLUORESCEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 4644352935     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048622a     Document Type: Article

References (75)

1. Lux, S. E., John, K. M., Kopito, R. R., and Lodish, H. F. (1989) Cloning and characterization of band 3, the human erythrocyte anion-exchange protein (AE1), Proc. Natl. Acad. Sci. U.S.A. 86, 9089-9093.
2. Jennings, M. L. (1992) Cellular anion transport, in The Kidney: Physiology and Pathophysiology (Seldin, D. W., and Giebisch, G., Eds.) pp 113-145, Raven Press, New York.
3. Knauf, P. A. (1989) Kinetics of anion transport, in The Red Cell Membrane (Raess, B. U., and Tunnicliff, G., Eds.) pp 171-200, Humana Press, Clifton, NJ.
4. Knauf, P. A., and Pal, P. (2003) Band 3 mediated transport, in Red Cell Membrane Transport in Health and Disease (Bernhardt, I., and Ellory, J. C., Eds.) pp 253-301, Springer, Berlin.
5. Passow, H. (1986) Molecular aspects of band 3 protein-mediated anion transport across the red blood cell membrane, Rev. Physiol. Biochem. Pharmacol. 103, 61-223.
6. Alper, S. L. (1991) The band 3-related anion exchanger (AE) gene family, Annu. Rev. Physiol. 53, 549-564.
7. Jennings, M. L. (1992) Anion transport proteins, in The Kidney: Physiology and Pathophysiology (Seldin, D. W., and Giebisch, G., Eds.) pp 503-535, Raven Press, New York.
8. Simon, J. S., Deshmukh, G., Couch, F. J., Merajver, S. D., Weber, B. L., Van Vooren, P., Tissil, F., Szpirer, J., Szpirer, C., Alper, S. L., Jacob, H. J., and Brosius, F. C., III (1996) Chromosomal mapping of the rat Slc4a family of anion exchanger genes, Ae1, Ae2, and Ae3, Mamm. Genome 7, 380-382.
9. Wang, D. N., Sarabia, V. E., Reithmeier, R. A. F., and Kuhlbrandt, W. (1994) Three-dimensional map of the dimeric membrane domain of the human erythrocyte anion exchanger, band 3, EMBO J. 13, 3230-3235.
10. 2DIDS), J. Membr. Biol. 70, 199-216.
11. Rakitzis, E. T., Gilligan, P. J., and Hoffman, J. F. (1978) Kinetic analysis of the inhibtion of sulfate transport in human red blood cells by isothiocyanates, J. Membr. Biol. 41, 101-115.
12. - transport site of human red blood cells by a kinetic analysis of the inhibitory effects of a chemical probe, Biochim. Biophys. Acta 508, 357-363.
13. Wood, P. G., Müller, H., Sovak, M., and Passow, H. (1992) Role of Lys 558 and Lys 869 in substrate and inhibitor binding to the murine band 3 protein: a study of the effects of site-directed mutagenesis of the band 3 protein expressed in the oocytes of Xenopus laevis, J. Membr. Biol. 127, 139-148.
14. Aranibar, N., Ostermeier, C., Legrum, B., Rüterjans, H., and Passow, H. (1994) Influence of stilbene disulfonates on the accessibility of the substrate-binding site for anions in the band 3 protein (AEB1), Renal Physiol. Biochem. 17, 187-189.
15. Salhany, J. M., Sloan, R. L., Cordes, K. A., and Schopfer, L. M. (1994) Kinetic evidence for ternary complex formation and allosteric interactions in chloride and stilbenedisulfonate binding to band 3, Biochemistry 33, 11909-11916.
16. Knauf, P. A., Ries, E. A., Romanow, L. A., Bahar, S., and Szekeres, E. S. (1993) DNDS (4,4′-dinitrostilbene-2,2′-disulfonate) does not act as a purely competitive inhibitor of red blood cell band 3-mediated anion exchange, Biophys. J. 64, A307.
17. Falke, J. J., and Chan, S. I. (1986) Molecular mechanisms of band 3 inhibitors. 1. Transport site inhibitors, Biochemistry 25, 7888-7894.
18. Kaplan, J. H., Scorah, K., Fasold, H., and Passow, H. (1976) Sidedness of the inhibitory action of disulfonic acids on chloride equilibrium exchange and net transport across the human erythrocyte membrane, FEBS Lett. 62, 182-185.
19. Fröhlich, O. (1982) The external anion binding site of the human erythrocyte anion transporter: DNDS binding and competition with chloride, J. Membr. Biol. 65, 111-123.
20. 2DIDS. Evidence for two conformations of the transport site of the human erythrocyte anion exchange protein, J. Gen. Physiol. 83, 657-681.
21. Rao, A., Martin, P., Reithmeier, R. A. F., and Cantley, L. C. (1979) Location of the stilbene disulfonate binding site of the human erythrocyte an ion-exchange system by resonance energy transfer, Biochemistry 18, 4505-4516.
22. Thevenin, B. J., Bicknese, S. E., Verkman, A. S., and Shohet, S. B. (1996) Distance between Cys-201 in erythrocyte band 3 and the bilayer measured by single-photon radioluminescence, Biophys. J. 71, 2645-2655.
23. 2DIDS (4,4′-diisothiocyanodihydrostilbene-2,2′-disulfonic acid) molecule, J. Biol. Chem. 269, 1918-1926.
24. Zhu, Q., Lee, D. W., and Casey, J. R. (2003) Novel topology in C-terminal region of the human plasma membrane anion exchanger, AE1, J. Biol. Chem. 278, 3112-3120.
25. Zhu, Q., and Casey, J. R. (2004) The substrate anion selectivity filter in the human erythrocyte Cl-/HCO3 exchange protein, AE1, J. Biol. Chem. 279, 23565-23573.
26. Jarolim, P., Murray, J. L., Rubin, H. L., Smart, E., and Moulds, J. M. (1997) Blood group antigens Rb(a), Tr(a), and Wd(a) are located in the third ectoplasmic loop of erythroid band 3, Transfusion 37, 607-615.
27. Jarolim, P., Murray, J. L., Rubin, H. L., Coghlan, G., and Zelinski, T. (1997) A Thr552 → Ile substitution in erythroid band 3 gives rise to the Warrior blood group antigen, Transfusion 37, 398-405.
28. Fujinaga, J., Tang, X.-B., and Casey, J. R. (1999) Topology of the membrane domain of human erythrocyte anion exchange protein, AE1, J. Biol. Chem. 274, 6626-6633.
29. Popov, M., Li, J., and Reithmeier, R. A. F. (1999) Transmembrane folding of the human erythrocyte anion exchanger (AE1, band 3) determined by scanning and insertional N-glycosylation mutagenesis, Biochem. J. 339, 269-279.
30. Macara, I. G., and Cantley, L. C. (1981) Interactions between transport inhibitors at the anion binding sites of the band 3 dimer, Biochemistry 20, 5095-5105.
31. Huang, Y., Lemieux, M. J., Song, J., Auer, M., and Wang, D. N. (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli, Science 301, 616-620.
32. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trezeguet, V., Lauquin, G. J., and Brandolin, G. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside, Nature 426, 39-44.
33. Knauf, P. A., Law, F.-Y., and Atherton, S. J. (1999) Relocation of the disulfonic stilbene (DS) sites of band 3 (AE1) on the basis of fluorescence lifetime measurements, Biophys. J. 76, A233.
34. Steck, T. L., and Kant, J. A. (1974) Preparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes, Methods Enzymol. 31, 172-180.
35. Bennett, V. (1983) Proteins involved in membrane-cytoskeleton association in human erythrocytes: spectrin, ankyrin, and band 3, Methods Enzymol. 96, 313-324.
36. Jennings, M. L., and Nicknish, J. S. (1984) Erythrocyte band 3 protein: evidence for multiple membrane-crossing segments in the 17 000-dalton chymotryptic fragment, Biochemistry 23, 6432-6436.
37. Kotaki, A., Naoi, M., and Yagi, K. (1971) A diaminostilbene dye as a hydrophobic probe for proteins, Biochim. Biophys. Acta 229, 547-556.
38. Maddy, A. H. (1964) A fluorescent label for the outer components of the plamsa membrane, Biochim. Biophys. Acta 880, 390-399.
39. Knauf, P. A., and Brahm, J. (1989) Functional asymmetry of the anion exchange protein, capnophorin: effects on substrate and inhibitor binding, Methods Enzymol. 173, 432-453.
40. Knauf, P. A., Raha, N. M., and Spinelli, L. J. (2000) The noncompetitive inhibitor WW781 senses changes in erythrocyte anion exchanger (AE1) transport site conformation and substrate binding, J. Gen. Physiol. 115, 159-173.
41. Bicknese, S., Rossi, M., Thevenin, B. J., Shohet, S. B., and Verkman, A. S. (1995) Anisotropy decay measurement of segmental dynamics of the anion binding domain in erythrocyte band 3, Biochemistry 34, 10645-10651.
42. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
43. Lieberman, D. M., and Reithmeier, R. A. F. (1983) Characterization of the stilbenedisulfonate binding site of the band 3 polypeptide of human erythrocyte membrane, Biochemistry 22, 4028-4032.
44. Knauf, P. A., Law, F.-Y., and Hahn, K. (1995) An oxonol dye is the most potent known inhibitor of band 3-mediated anion exchange, Am. J. Physiol. (Cell Physiol.) 269, C1073-C1077.
45. Dale, R. E., Eisinger, J., and Blumberg, W. E. (1979) The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer, Biophys. J. 26, 161-194.
46. Förster, T. (1959) Transfer mechanisms of electronic excitation, Discuss. Faraday Soc. 27, 7-17.
47. Arnold, B. R., Atherton, S. J., Fand, S., Goodman, J. L., and Could, I. R. (1997) Combined application of picosecond transient absorption and emission measurements in studies of radical-ion pair dynamics, Photochem. Photobiol. 65, 15-22.
48. Birch, D. J. S., and Imhof, R. E. (1991) Time-domain fluorescence spectroscopy using time-correlated single-photon counting, in Topics in Fluorescence Spectroscopy (Lakowicz, J. R., Ed.) pp 1-95, Plenum Press, New York.
49. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, Kluwer Academic/Plenum Publishers, New York.
50. Lakowicz, J. R. (1983) Principles of Fluorescence Spectroscopy, Plenum Press, New York.
51. Hillel, Z., and Wu, C.-W. (1976) Statistical interpretation of fluorescence energy transfer measurements in macromolecular systems, Biochemistry 15, 2105-2113.
52. Casey, J. R., and Reithmeier, R. A. F. (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 hetrogeneity, J. Biol. Chem. 266, 15726-15737.
53. Salhany, J. M., Cordes, K. A., and Sloan, R. L. (2000) Mechanism of band 3 dimer dissociation during incubation of erythrocyte membranes at 37 °C, Biochem. J. 345, 33-41.
54. Blackman S. M., Piston, D. W., and Beth, A. H. (1998) Oligomeric state of human erythrocyte band 3 measured by fluorescence resonance energy homotransfer, Biophys. J. 75, 1117-1130.
55. Janas, T., Bjerrum, P. J., Brahm, J., and Wieth, J. O. (1989) Kinetics of reversible DIDS inhibition of chloride self-exchange in human erythrocytes. Am. J. Physiol. (Cell Physiol.) 257, C601-C606.
56. Thevenin, B. J., Periasamy, N., Shohet, S. B., and Verkman, A. S. (1994) Segmental dynamics of the cytoplasmic domain of erythrocyte band 3 determined by time-resolved fluorescence anisotropy: sensitivity to pH and ligand binding, Proc. Natl. Acad. Sci. U.S.A. 91, 1741-1745.
57. Thevenin, B. J., Willardson, B. M., and Low, P. S. (1989) The redox state of cysteines 201 and 317 of the erythrocyte anion exchanger is critical for ankyrin binding, J. Biol. Chem. 264, 15886-15892.
58. Leenders, R., Roslund, J., and Visser, J. W. G. (1995) Time-resolved tryptophan fluorescence in flavodoxins, J. Fluoresc. 5, 349-353.
59. Jia, Y., Sytnik, A., Li, L., Vladimirov, S., Cooperman, B. S., and Hochstrasser, R. M. (1997) Nonexponential kinetics of a single tRNAPhe molecule under physiological conditions, Proc. Natl. Acad. Sci. U.S.A. 94, 7932-7936.
60. Cobb, C. E., and Beth, A. H. (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.
61. Thevenin, B. J., Bicknese, S. E., Verkman, A. S., and Shohet, S. B. (1996) Distance between Cys-201 in erythrocyte band 3 and the bilayer measured by single-photon radioluminescence, Biophys. J. 71, 2645-2655.
62. Zhang, D., Kiyatkin, A., Bolin, J. T., and Low, P. S. (2000) Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3, Blood 96, 2925-2933.
63. Zhou, J., and Low, P. S. (2001) Characterization of the reversible conformational equilibrium in the cytoplasmic domain of human erythrocyte membrane band 3, J. Biol. Chem. 276, 38147-38151.
64. Bahar, S., Gunter, C. T., Wu, C., Kennedy, S. D., and Knauf, P. A. (1999) Persistence of external chloride and DIDS binding after chemical modification of Glu-681 in human band 3, Am. J. Physiol. (Cell Physiol.) 277, C791-C799.
65. 681 of human AE1 protein, the erythrocyte anion exchanger, J. Biol. Chem. 273, 22545-22553.
66. Jennings, M. L., and Anderson, M. P. (1987) Chemical modification and labeling of glutamate residues at the stilbenedisulfonate site of human red blood cell band 3 protein, J. Biol. Chem. 262, 1691-1697.
67. Jennings, M. L., and Al-Rhaiyel, S. (1988) Modification of a carboxyl group that appears to cross the permeability barrier in the red blood cell anion transporter, J. Gen. Physiol. 92, 161-178.
68. Jennings, M. L., and Smith, J. S. (1992) Anion-proton cotransport through the human red blood cell band 3 protein: role of glutamate 681, J. Biol. Chem. 267, 13964-13971.
69. Jennings, M. L. (1995) Rapid electrogenic sulfate-chloride exchange mediated by chemically modified band 3 in human erythrocytes, J. Gen. Physiol. 105, 21-47.
70. Sekler, L, Lo, R. S., and Kopito, R. R. (1995) A conserved glutamate is responsible for ion selectivity and pH dependence of the mammalian anion exchangers AE1 and AE2, J. Biol. Chem. 270, 28751-28758.
71. Tang, X.-B., and Casey, J. R. (1999) Trapping of inhibitor-induced conformational changes in the erythrocyte membrane anion exchanger AE1, Biochemistry 38, 14565-14572.
72. Canfield, V. A., and Macey, R. I. (1984) Anion exchange in human erythrocytes has a large activation volume, Biochim. Biophys. Acta 778, 379-384.
73. Cha, A., Snyder, G. E., Selvin, P. R., and Bezanilla, F. (1999) Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy, Nature 402, 809-813.
74. Glauner, K. S., Mannuzzu, L. M., Gandhi, C. S., and Isacoff, E. Y. (1999) Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel, Nature 402, 813-817.
75. Jennings, M. L., and Passow, H. (1979) Anion transport across the erythrocyte membrane, in situ proteolysis of band 3 protein, and cross-linking of proteolytic fragments by 4,4′-diisothiocyano-dihydrostilbene-2, 2′-disulfonate, Biochim. Biophys. Acta 554, 498-519.