Structural studies on the effects of the deletion in the red cell anion exchanger (band 3, AE1) associated with South East Asian ovalocytosis

Journal of Molecular Biology

Volumn 285, Issue 3, 1999, Pages 1289-1307

  Chambers, Eric J ^a   Bloomberg, Graham B ^a   Ring, Susan M ^a   Tanner, Michael J A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Cell free translation; Human erythrocyte anion transporter; NMR; South East Asian ovalocytosis; Synthetic peptide

Indexed keywords

CHLOROFORM; ERYTHROCYTE BAND 3 PROTEIN; METHANOL; PROTON; SYNTHETIC PEPTIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANION EXCHANGE; ARTICLE; ASIA; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ELLIPTOCYTOSIS; HUMAN; HUMAN CELL; HYDROPHOBICITY; MICROSOME MEMBRANE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALIA;

EID: 0033593271     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2392     Document Type: Article

References (75)

1. Aggeli A., Bannister M. L., Bell M., Boden N., Findlay J. B. C., Hunter M., Knowles P. F., Yang J. Conformation and ion-channeling activity of a 27-residue peptide modeled on the single-transmembrane segment of the IsK (minK) protein. Biochemistry. 37:1998;8121-8131.
2. Aurora R., Rose G. D. Helix capping. Protein Sci. 7:1998;21-38.
3. Bax A., Davies D. G. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65:1985;335-360.
4. Bax A., Ikara M., Kay L. E., Torchia D. A., Tschuclin R. Comparison of different modes of two-dimensional reverse-correlation NMR for the study of proteins. J. Magn. Reson. 86:1990;304-318.
5. Blundell T., Barlow D., Borkakoti N., Thornton J. Solvent-induced distortions and the curvature of α-helices. Nature. 306:1983;281-283.
6. Booth P. B., Serjeantson S., Woodfield D. G., Amato D. Selective depression of blood group antigens associated with hereditary ovalocytosis among Melanesians. Vox Sang. 32:1977;99-110.
7. Braer A., Lie-Injo L. E., Welch Q. B., Lewis A. N. Genetic factors and Malaria in the Temuan. Am. J. Hum. Genet. 28:1976;179-188.
8. Brock C. J., Tanner M. J. A. The human erythrocyte anion transport protein. Further amino acid sequence from the integral membrane domain homologous with the murine protein. Biochem. J. 235:1986;899-901.
9. Brunger A. T. X-PLOR (version 3.1) Manual of a System for Crystallography and NMR. 1992;Yale University, New Haven.
10. Chapman R. E., Munro S. The functioning of the yeast golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway. EMBO J. 13:1994;4896-4907.
11. Che A., Cherry R. J., Bannister L. H., Dluzewski A. R. Aggregration of band 3 in hereditary ovalocytic red blood cell membranes. J. Cell Sci. 105:1993;655-660.
12. Chernova M. N., Jarolim P., Palek J., Alper S. L. Overexpression of AE1 Prague, but not of AE1 SAO, inhibits wild-type AE1 trafficking in Xenopus oocytes. J. Mem. Biol. 148:1995;203-210.
13. Cobb C. E., Beth A. H. 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. 29:1990;8283-8290.
14. 1H magnetization transfer. J. Magn. Reson. 84:1989;417-424.
15. Dluzewski A. R., Nash G. B., Wilson R. J. M., Rearden D. M., Gratzer W. B. Invasion of hereditary ovalocytes by Plasmodium falciparum in vitro and its relationship to intracellular ATP concentration. Mol. Biochem. Parasitol. 55:1992;1-8.
16. Doak D. G., Mulvey D., Kawaguchi K., Villalain J., Campbell I. D. Structural studies of synthetic peptides dissected from the voltage-gated sodium channel. J. Mol. Biol. 258:1996;672-687.
17. Gargaro A. R., Bloomberg G. B., Dempsey C. E., Murray M., Tanner M. J. A. The solution structures of the first and second transmembrane- spanning segments of band 3. Eur. J. Biochem. 221:1994;445-454.
18. Genton B., Al-Yaman F., Mgone C. S., Alexander N., Paniu M. M., Alpers M. P., Mokela D. Ovalocytosis and cerebral malaria. Nature. 378:1995;564-565.
19. Gray T. M., Matthews B. W. Intrahelical hydrogen bonding of serine, threonine and cysteine residues within α-helices and its relevance to membrane-bound proteins. J. Mol. Biol. 175:1984;75-81.
20. 1H multiple quantum coherence spectroscopy. FEBS Letters. 243:1989;93-98.
21. Groves J. D., Tanner M. J. A. Glycophorin A facilitates the expression of human band 3-mediated anion transport in Xenopus oocytes. J. Biol. Chem. 267:1992;22163-22170.
22. Groves J. D., Tanner M. J. A. Role of N-glycosylation in the expression of human band 3-mediated anion transport. Mol. Mem. Biol. 11:1994;31-38.
23. Groves J. D., Tanner M. J. A. Co-expressed complementary fragments of the human red cell anion exchanger (band3 AE1) generate stilbene disulfonate-sensitive anion sport. J. Biol. Chem. 270:1995;9097-9105.
24. Groves J. D., Ring S. M., Schofield A. E., Tanner M. J. A. The expression of the abnormal human red cell anion transporter from South-East Asian ovalocytes (band3 SAO) inXenopus oocytes. FEBS Letters. 330:1993;180-190.
25. Hamasaki N., Okubo, Kuma H., Kang D., Yae Y. Proteolytic cleavage sites of band 3 protein in alkali-treated membranes: fidelity of hydropathy prediction for band 3 protein. J. Biochem. (Tokyo). 122:1997;577-585.
26. Hyberts S. G., Goldberg M. S., Havel T. F., Wagner G. The solution structure of eglin c based on measurements of many NOEs and coupling constants and its comparison with X-ray structures. Protein Sci. 1:1992;736-751.
27. Jarolim R., Palek J., Amato D., Hassan K., Sapak R., Nurse G. T., Rubin H. L., Zhai S., Sahr K. E., Liu S.-C. Deletion in erythrocyte band 3 gene in malaria-resistant Southeast Asian ovalocytosis. Proc. Natl Acad. Sci. USA. 88:1991;11022-11026.
28. Jennings M. L., Nicknish J. S. Erythrocyte band 3 protein: evidence for multiple membrane-crossing segments in the 17000-Dalton chymotryptic fragment. Biochemistry. 23:1984;6432-6436.
29. Jones G. L., Edmundsen H. M., Wesche D., Al E. Human erythrocyte band 3 has an altered N-terminus in malaria-resistant Melanesian ovalocytes. Biochim. Biophys. Acta. 1096:1991;33-40.
30. Karplus M. Contact electron-spin coupling of nuclear magnetic moments. J. Chem. Phys. 30:1959;11-15.
31. Kopito R. R., Lodish H. F. Primary structure and transmembrane orientation of the murine anion exchange protein. Nature. 316:1985;234-238.
32. Kumar A., Ernst R. R., Wuthrich K. A two-dimensional nuclear overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95:1980;1-6.
33. Kuma H., Inoue K., Fu G., Ando S., Lee S., Sugihara G., Hamasaki N. Secondary structures of synthetic peptides corresponding to the first membrane-contact portion of normal band 3 and its deletion mutant (Southeast Asian ovalocytosis). J. Biochem. (Tokyo). 124:1998;509-518.
34. Laemmli U. K. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
35. Liu S.-C., Zhai S., Palek J., Golan D. E., Amato D., Hassan K., Nurse G. T., Babona D., Coetzer T., Jarolim P., Zaik M., Borwein S. Molecular defects of the band 3 protein in Southeast Asian ovalocytosis. New Eng. J. Med. 323:1990;1530-1538.
36. Liu S.-C., Jarolim P., Rubin H. L., Palek J. The homozygous state for the band 3 protein mutation in Southeast Asian ovalocytosis may be lethal. Blood. 88:1994;3590-3591.
37. Liu S.-C., Palek J., Yi S. J., Nichols P. E., Derick L. H., Chiou S.-S., Amato D., Corbett J. D., Cho M. R., Goran D. E. Molecular basis of altered red blood cell membrane properties in Southeast Asian ovalocytosis: role of the mutant band 3 protein in band 3 oligomerization and retention by the membrane skeleton. Blood. 86:1995;349-358.
38. MacKenzie K. R., Prestegard J. H., Engelmann D. M. A transmembrane helix dimer: structure and implications. Science. 276:1997;131-133.
39. Mawby W. J., Findlay J. B. C. Characterisation and partial sequence of di-iodosulphophenyl isothiocyanate-binding peptide from human erythrocyte anion transport protein. Biochem. J. 205:1982;465-475.
40. Mohandas N., Lie-Injo L. E., Friedman M., Mak J. W. Rigid membranes of malayan ovalocytes: a likely genetic barrier against malaria. Blood. 63:1984;1385-1392.
41. Mohandas N., Winardi R., Knowles D., Leung A., Parra M., George E., Conboy J., Chasis J. Molecular basis for membrane rigidity of hereditary ovalocytosis. A novel mechanism involving the cytoplasmic domain of band 3. J. Clin. Invest. 89:1992;686-692.
42. Moriyama R., Ideguchi H., Lombardo C. R., Dort H. M. V., Low P. S. Structural and functional characterization of band 3 from Southeast Asian ovalocytosis. J. Biol. Chem. 267:1992;25792-25797.
43. Morris A. L., MacArthur M. W., Hutchinson E. G., Thornton J. Stereochemical quality of protein structure coordinates. Proteins: Struct. Funct. Genet. 12:1992;345-364.
44. Morris G. A., Freeman R. Selective excitation in Fourier transform nuclear magnetic resonance. J. Magn. Reson. 29:1978;433-462.
45. Munro S. A comparison of the transmembrane domains of Golgi and plasma membrane proteins. Biochem. Soc. Trans. 23:1995;527-530.
46. Oikawa K., Lieberman D. M., Reithmeier R. A. F. Conformation and stability of the anion transport protein of human erythrocyte membranes. Biochemistry. 24:1985;2843-2848.
47. 2DIDS (4,4′-diisothiocyanodihydrostilbene-2,2′-disulfonic acid) molecule. J. Biol. Chem. 269:1994;1918-1926.
48. Otting G., Wuthrich K. Efficient purging scheme for proton-detected heteronuclear two-dimensional nmr. J. Magn. Reson. 76:1988;569-574.
49. Piantini U., Sorensen 0. W., Ernst R. R. Multiple quantum filters for elucidating nmr coupling networks. J. Am. Chem. Soc. 104:1982;6800-6801.
50. Popov M., Tam L. Y., Li J., Reithmeier R. A. F. Mapping the ends of transmembrane segments in a polytopic membrane protein. J. Biol. Chem. 272:1997;18325-18332.
51. Primrose W. U. Sample preparation. Roberts G. C. K. NMR of Macromolecules. A Practical Approach. 1993;7-34 IRL Press, Oxford.
52. Quanta. Polygen Corporation. 1996.
53. Rance M. Improved techniques for homonuclear rotating-frame and isotropic mixing experiments. J. Magn. Reson. 74:1987;557-564.
54. Rayner J. C., Pelham H. R. B. Transmembrane domam-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J. 16:1997;1832-1841.
55. Reithmeier R. A. F. The erythrocyte anion transporter (band 3). Curr. Opin. Struct. Biol. 3:1993;515-523.
56. Sarabia V. E., Casey J. R., Reithmeier R. A. F. Molecular characterization of the band 3 protein from Southeast Asian ovalocytosis. J. Biol. Chem. 268:1993;10676-10680.
57. Saul A., Lamont G., Sawyer W. H., Kidson C. Decreased membrane deformability in Melanesian ovalocytes from Papua New Guinea. J. Cell Biol. 98:1984;1348-1354.
58. Schofield A. E., Reardon D. M., Tanner M. J. A. Defective anion transport activity of the abnormal band 3 in hereditary ovalocytic red blood cells. Nature. 355:1992a;836-838.
59. Schofield A. E., Tanner M. J. A., Pinder J. C., Clough B., Bayley P. M., Nash G. B., Dluzewski A. R., Reardon D. M., Cox T. M., Wilson R. J. M., Gratzer W. B. Basis of unique red cell membrane properties in hereditary ovalocytosis. J. Mol. Biol. 223:1992b;949-958.
60. Serjeantson S., Bryson K., Amoto D., Babona D. Malaria and hereditary ovalocytosis. Human Genet. 37:1977;161-168.
61. Shaka A. J., Freeman R. Simplification of nmr spectra by filtration through multiple quantum coherence. J. Magn. Reson. 51:1983;169-173.
62. Smythe J. S., Spring F. A., Gardner B., Parsons S. F., Judson P. A., Anstee D. J. Monoclonal antibodies recognizing epitopes on the extracellular face and intracellular N-terminus of the human erythrocyte anion transporter (band 3) and their application to the analysis of Southeast Asian ovalocytes. Blood. 85:1995;2929-2936.
63. States D. J., Haberkorn R. A., Ruben D. J. A two-dimensional nuclear overhauser experiment with pure absorption in four quadrants. J. Magn. Reson. 48:1982;286-292.
64. Tam L. Y., Loo T. W., Clarke D. M., Reithmeier R. A. F. Identification of an internal topogenic signal sequence in human band 3, the erythrocyte anion exchanger. J. Biol. Chem. 269:1994;32542-32550.
65. Tanner M. J. A. Molecular and cellular biology of the erythrocyte anion exchanger. Semin. Hematol. 30:1993;34-57.
66. Tanner M. J. A., Martin P. G., High S. The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. Biochem. J. 256:1988;703-712.
67. Tilley L., Nash G. B., Jones G. L., Sawyer W. H. Decreased rotational diffusion of band 3 in melanesian ovalocytes from Papua New Guinea. J. Mem. Biol. 121:1991;59-66.
68. von Heijne G. Proline kinks in transmembrane α-helices. J. Mol. Biol. 218:1991;499-503.
69. von Heijne G., Manoil C. Membrane proteins: from sequence to structure. Protein Eng. 4:1990;109-112.
70. Wang D. N. Band 3 protein: structure, flexibility and function. FEBS Letters. 346:1994;26-31.
71. Wang L., Groves J. D., Mawby W. J., Tanner M. J. A. Complementation studies with co-expressed fragments of the human red cell anion transporter (band 3; AE1): the role of some exofacial loops in anion transport. J. Biol. Chem. 272:1997;10631-10638.
72. Webb R. J., Malcolm East J., Sharma R. P., Lee A. G. Hydrophobic mismatch and the incorporation of peptides into lipid bilayers: a possible mechanism for retention in the golgi. Biochemistry. 37:1998;673-679.
73. Wishart D. S., Sykes B. D., Richards F. M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry. 31:1992;1647-1651.
74. Woolfson D. N., Mortishire-Smith R. J., Williams D. H. Conserved positioning of proline residues in membrane-spanning helices of ion-channel proteins. Biochem. Biophys. Res. Commun. 175:1991;733-737.
75. Wuthrich K. NMR of Proteins and Nucleic Acids. 1986;John Wiley & Sons, New York.