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Se-mediated domain-domain communication in Band 3 of human erythrocytes

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Abstract

Na2SeO3 could affect the anion flux of Band 3 of inside-out erythrocyte membrane vesicles (IOVs). Such effect was believed to be based on the interaction of SH groups of Band 3 with Na2SeO3. This effect could be eliminated when the cytoplasmic domain of Band 3 was proteolytically removed by trypsin. This suggested that SH groups in the cytoplasmic domain were involved in such interaction. Measurement of the pH dependence of intrinsic fluorescence intensity provided evidence that conformational changes of Band 3 occurred as a consequence of interaction with selenite. KI quenching of intrinsic fluorescence of Band 3 could also show that there was a conformational change in the cytoplasmic domain of Band 3 after reaction with Na2SeO3. Such conformational change in turn could be transmitted to the membrane domain of Band 3 monitored by quenching of intrinsic fluorescence of Band 3 using hypocrellin B (HB) (a photosensitive pigment obtained from a parasitic fungus growing in Yunnan, China).

It is suggested that the cytoplasmic domain of Band 3 is not necessary for its anion flux, but is essential for the regulation (e.g., by Se) of its active site located at the membrane domain, and hence, it may provide evidence of communication between the cytoplasmic domain and the membrane domain of Band 3.

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Abbreviations

DPA:

dipicolinic acid

IOVs:

inside-out vesicles

NPM:

N-(l-pyrenyl) maleimide

NEM:

N-ethylmaleimide

PCMB:

p-chloromercuribenzoic acid

HB:

hypocrellin B

TES:

N-Tris-(hydroxymethyl)-methyl-2-aminoethane sulfonic acid

Trp:

tryptophan

Cys:

cysteine

SDS:

sodium dodecyl sulfate

DMSO:

dimethysulfoxide

References

  1. G. Fairbanks, T. L. Steck, and D. F. H. Wallach. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane,Biochemistry 10, 2606–2617 (1971).

    Article  PubMed  CAS  Google Scholar 

  2. P. S. Low. Structure and function of the cytoplasmic domain of Band 3: center of erythrocyte membrane-peripheral protein interactions,Biochim. Biophys. Acta 864, 145–167 (1986).

    PubMed  CAS  Google Scholar 

  3. V. Bennett and P. J. Stenbuck. Association between ankyrin and the cytoplasmic domain of Band 3 from the human erythrocyte membrane,J. Biol. Chem. 255, 6424–6432 (1980).

    PubMed  CAS  Google Scholar 

  4. J. M. Salhany, K. A. Cordes, and E. D. Gaines. Light-scattering measurement of hemoglobin binding to the erythrocyte membrane,Biochemistry 19, 1447–1454 (1980).

    Article  PubMed  CAS  Google Scholar 

  5. P. S. Low, P. Rathinavelu, and M. L. Harrison. Regulation of glycolysis via reversible enzyme binding to the membrane protein, Band 3,J. Biol. Chem. 268, 14,627–14,631 (1993).

    CAS  Google Scholar 

  6. S. Grinstein, S. Ship, and A. Rothstein. Anion transport in relation to proteolytic dissection of Band 3 protein,Biochim. Biophys. Acta 507, 294–304 (1978).

    Article  PubMed  CAS  Google Scholar 

  7. A. E. Lindsey, K. Schneider, D. M. Simmons, R. Baron, B. S. Lee, and R. R. Kopito. Functional expression and subcellular location of an anion exchanger cloned from choriodplexus,Proc. Natl. Acad. Sci. USA 87, 5278–5282 (1990).

    Article  PubMed  CAS  Google Scholar 

  8. J. M. Salhany.Erythrocyte Band 3 Protein, CRC, Boca Raton, FL (1990).

    Google Scholar 

  9. M. Sami, S. Malik, and A. Watts. Structural stability of the erythrocyte anion transport, band 3, in native membrane and in detergent micelles,Biochim. Biophys. Acta 1105, 148–154 (1992).

    Article  PubMed  CAS  Google Scholar 

  10. H. Ideguchi, K. Okubo, A. Ishikawa, Y. Futata, and N. Hamasaki. Band 3-memphis is associated with a lower transport rate of phosphoenolpyruvate,Br. J. Haematol. 82, 122–125 (1992).

    PubMed  CAS  Google Scholar 

  11. L. M. Schopfer and J. M. Salhany. Factors determining the conformation and quaternary structure of isolated human erythrocyte Band 3 in detergent solution,Biochemistry 31, 12,610–12,617 (1992).

    Article  CAS  Google Scholar 

  12. D. N. Wang. Band 3 protein: structure, flexibility and function,FEBS Lett. 346, 26–314 (1994).

    Article  PubMed  CAS  Google Scholar 

  13. F. Y. Yang and W. H. Wo. Role of Se in stabilization of human erythrocyte membrane skeleton,Biochem. Int. 15, 475–482 (1989).

    Google Scholar 

  14. J. Yang and F. Y. Yang. Se induces conformation change of spectrin from human erythrocyte membrane,Acta Biophys. Sinica 4, 372–378 (1988).

    Google Scholar 

  15. F. Y. Yang, J. Yang, and Z. M. Liu. The role of Se in the interconversion of polymeric states of spectrin from human erythrocyte,BioFactors 3, 49–52 (1991).

    PubMed  CAS  Google Scholar 

  16. J. Yang and F. Y. Yang. The effect of selenium on the function of anion transporter (Band 3) of erythrocyte membrane,BioFactors 4, 29–32 (1992).

    PubMed  CAS  Google Scholar 

  17. M. Ramjeesingh, A. Gaarn, and A. Rothstein. The location of the three cysteine residues in the primary structure of the intrinsic segments of Band 3 protein, and applications concerning the arrangement of Band 3 protein in the bilayer,Biochim. Biophys. Acta,729, 150–160 (1983).

    Article  PubMed  CAS  Google Scholar 

  18. A. Rao. Disposition of Band 3 polypeptide in the human erythrocyte membrane,J. Biol. Chem. 254, 3503–3511 (1979).

    PubMed  CAS  Google Scholar 

  19. M. Ramjeesingh, S. Grinstein, and A. Rothstein. A Intrinsic segments of Band 3 that are associated with anion transport across red blood cell membranes,J. Membr. Biol. 57, 95–102 (1980).

    Article  PubMed  CAS  Google Scholar 

  20. J. T. Dodge, C. Mitchell, and D. J. Hanahan. The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes,Arch Biochem. Biophys.,100, 119–130 (1963).

    Article  PubMed  CAS  Google Scholar 

  21. T. L. Steck and J. A. Kant. Preparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes,Methods Enzymol. 31, 172–180 (1974).

    Article  PubMed  CAS  Google Scholar 

  22. W. W. Bender, H. Garan, and H. C. Berg. Proteins of the human erythrocyte membrane as modified by pronase,J. Mol. Biol. 58, 783–797 (1971).

    Article  PubMed  CAS  Google Scholar 

  23. A. C. Newton and W. H. Huestis. Efflux of dipicolinic acid from human erythrocytes, sealed membrane fragments, and Band 3-liposome complexes: A fluorescence probe for the erythrocyte anion transporter,Anal. Biochem. 156, (1986).

  24. C. Feng, Z. Y. Guan, and Y. P. Tu. A new method for the measuring the anion transfer across the membranes of red cell inside-out vesicles.Prog. Biochem. Biophys. 22, 154–158 (1995).

    CAS  Google Scholar 

  25. S. Lindenthal and D. Schubert. Monomeric erythrocyte band 3 protein transports anions,Proc. Natl Acad. Sci. USA 88, 6540–6544 (1991).

    Article  PubMed  CAS  Google Scholar 

  26. K. C. Appell and P. S. Low. Evaluation of structural interdependence of membrane-spanning and cytoplasmic domains of Band 3,Biochemistry 21, 2151–2157 (1982).

    Article  PubMed  CAS  Google Scholar 

  27. J. M. Tyler, W. R. Hargreaves, and D. Branton. Purification of two spectrin-binding proteins: Biochemical and electron microscopic evidence for site-specific reassociation between spectrin and Bands 2.1 and 4.1,Proc. Natl. Acad. Sci. USA 76, 5192–5196 (1979).

    Article  PubMed  CAS  Google Scholar 

  28. S. Grinstein, S. Ship, and A. Rothstein. Anion transport in relation to proteolytic dissection of Band 3 protein,Biochim. Biophys. Acta 507, 294–304 (1978).

    Article  PubMed  CAS  Google Scholar 

  29. S. Lepke and H. Passow. Effect of incorporated trypsin on anion exchange and membrane proteins in human red blood cell ghosts,Biochim. Biophys. Acta 455, 353–370 (1976).

    Article  PubMed  CAS  Google Scholar 

  30. T. L. Steck, B. Ramos, and E. Strapazon. Proteolytic dissection of Band 3, the predominant transmembrane polypeptide of the human erythrocyte membrane,Biochemistry 15, 1154–1161 (1976).

    Article  CAS  Google Scholar 

  31. V. G. Bieri and D. F. H. Wallach. Variations of lipid-protein interactions in erythrocyte ghosts as a function of temperature and pH in physiological and non-physiological ranges,Biochim. Biophys. Acta,406, 415–423 (1975).

    Article  PubMed  CAS  Google Scholar 

  32. T. J. Mueller and M. Morrison. The transmembrane proteins in the plasma membrane of normal human erythrocytes,J. Biol. Chem. 249, 7568–7573 (1974).

    PubMed  CAS  Google Scholar 

  33. D. Jay and L. Cantley. Structural aspects of the red cell anion exchange protein,Annu. Rev. Biochem,55, 511–538 (1986).

    Article  PubMed  CAS  Google Scholar 

  34. Z. Y. Zhang, N. H. Wang, Q. Wan, and M. F. Li. ESR studies of singlet oxygen and free radicals generated during photosensitization of Hypocrellion B,Free Radical Biol. Med. 14, 1–9 (1993).

    Article  CAS  Google Scholar 

  35. J. Du and L. S. Cheng. The effect of Hypocrellin B on the lipid bilayer of erythrocyte membrane.Acta Biologiae Experimentalis Sinica 24, 153–160 (1991).

    PubMed  CAS  Google Scholar 

  36. J. C. Yue, J. F. Qing, S. Sun, and S. Z. Pan. Hypocrellin B induce intrinsic fluorescence quenching of erythrocyte membrane proteins,Photographic Sci. Photochem. 11, 228–235 (1993).

    CAS  Google Scholar 

  37. Y. P. Tu and F. Y. Yang. Fluorescence study of transmembrane Ca2+ gradientmediated conformational changes of sarcoplasmic reticulum Ca2+-ATPase,Biosci. Rep. 14, 309–317 (1994).

    Article  PubMed  CAS  Google Scholar 

  38. J. C. Yue and Y. P. Tu. Fluorescence quenching study of sarcoplasmic reticulum Ca2+-ATPase using hypocrellin B,Chin. Sci. Bull. 40, 76–79 (1995).

    Google Scholar 

  39. T. Yamaguchi and E. Kimoto. Inhibition of phosphate transport across the human erythrocyte membrane by chemical modification of sulfhydryl groups,Biochemistry 31, 1968–1973 (1992).

    Article  PubMed  CAS  Google Scholar 

  40. Y. P. Tu and F. Y. Yang. Zn2+-mediated domain-domain communication in human erythrocyte Band 3,J. Biochem. (Tokyo) 118, 161–167 (1995).

    CAS  Google Scholar 

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Yang, F.Y., Fen, C. & Tu, Y.P. Se-mediated domain-domain communication in Band 3 of human erythrocytes. Biol Trace Elem Res 55, 279–295 (1996). https://doi.org/10.1007/BF02785286

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  • DOI: https://doi.org/10.1007/BF02785286

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