Trafficking defects of the Southeast Asian ovalocytosis deletion mutant of anion exchanger 1 membrane proteins

Biochemical Journal

Volumn 392, Issue 3, 2005, Pages 425-434

  Cheung, Joanne C ^a   Cordat, Emmanuelle ^a   Reithmeier, Reinhart A F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anion exchanger 1 (AE1); Distal renal tubular acidosis (dRTA); Kidney; Membrane protein; Southeast Asian ovalocytosis (SAO)

Indexed keywords

ABSORPTION; BIOLOGICAL MEMBRANES; BODY FLUIDS; CELL CULTURE; DIMERS; GENETIC ENGINEERING; ION EXCHANGE; PROTONS;

ANION EXCHANGER 1 (AE1); DISTAL RENAL TUBULAR ACIDOSIS (DRTA); KIDNEY; MEMBRANE PROTEIN; SOUTHEAST ASIAN OVALOCYTOSIS (SAO);

PROTEINS;

BICARBONATE; MEMBRANE PROTEIN; PROTON;

ABSORPTION; ANION EXCHANGE; ARTICLE; BASOLATERAL MEMBRANE; CELL SURFACE; ELLIPTOCYTOSIS; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; ERYTHROCYTE; GENE DELETION; HUMAN; HUMAN CELL; KIDNEY; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION;

ANIMALS; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; ASIA, SOUTHEASTERN; CELL LINE; DIMERIZATION; DOGS; ELLIPTOCYTOSIS, HEREDITARY; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TRANSPORT;

EID: 29644446870     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051076     Document Type: Article

References (46)

1. Reithmeier, R. A. F. (2001) A membrane metabolon linking carbonic anhydrase with chloride/bicarbonate anion exchangers. Blood Cells Mol. Dis. 27, 85-89
2. Sterling, D., Reithmeier, R. A. F. and Casey, J. R. (2001) A transport metabolon: functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. J. Biol. Chem. 276, 47886-47894
3. Reithmeier, R. A. F., Chan, S. L. and Popov, M. (1996) Structure of the erythrocyte band 3 anion exchanger. In Transport Processes in Eukaryotic and Prokaryotic Organisms, vol. 2 (Konings, W. N., Kaback, H. R. and Lolkema, J. S., eds.), pp. 281-309, Elsevier Science, Amsterdam
4. Grinstein, S., Ship, S. and Rothstein, A. (1978) Anion transport in relation to proteolytic dissection of band 3 protein. Biochim. Biophys. Acta 507, 294-304
5. Iolascon, A., Miraglia del Giudice, E., Perrotta, S., Alloisio, N., Morle, L. and Delaunay, J. (1998) Hereditary spherocytosis: from clinical to molecular defects. Haematologica 83, 240-257
6. Tanner, M. J. A. (2002) Band 3 anion exchanger and its involvement in erythrocyte and kidney disorders. Curr. Opin. Hematol. 9, 133-139
7. Jarolim, P., Palek, J., Amato, D., Hassan, K., Sapak, P., Nurse, G. T., Rubin, H. L., Zhai, S., Sahr, K. E. and Liu, S. C. (1991) Deletion in erythrocyte band 3 gene in malaria-resistant Southeast Asian ovalocytosis. Proc. Natl. Acad. Sci. U.S.A. 88, 11022-11026
8. 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. et al. (1992) Basis of unique red cell membrane properties in hereditary ovalocytosis. J. Mol. Biol. 223, 949-958
9. Lie-Injo, L. E. (1965) Hereditary ovalocytosis and haemoglobin E-ovalocytosis in Malayan aborigines. Nature (London) 208, 1329
10. Genton, B., al-Yaman, F., Mgone, C. S., Alexander, N., Paniu, M. M., Alpers, M. P. and Mokela, D. (1995) Ovalocytosis and cerebral malaria. Nature (London) 378, 564-565
11. Mohandas, N., Lie-Injo, L. E., Friedman, M. and Mak, J. W. (1984) Rigid membranes of Malayan ovalocytes: a likely genetic barrier against malaria. Blood 63, 1385-1392
12. Vasuvattakul, S., Yenchitsomanus, P. T., Vachuanichsanong, P., Thuwajit, P., Kaitwatcharachai, C., Laosombat, V., Malasit, P., Wilairat, P. and Nimmannit, S. (1999) Autosomal recessive distal renal tubular acidosis associated with Southeast Asian ovalocytosis. Kidney Int. 56, 1674-1682
13. Liu, S. C., Jarolim, P., Rubin, H. L., Palek, J., Amato, D., Hassan, K., Zaik, M. and Sapak, P. (1994) The homozygous state for the band 3 protein mutation in Southeast Asian ovalocytosis may be lethal. Blood 84, 3590-3591
14. Sarabia, V. E., Casey, J. R. and Reithmeier, R. A. F. (1993) Molecular characterization of the band 3 protein from Southeast Asian ovalocytes. J. Biol. Chem. 268, 10676-10680
15. Moriyama, R., Ideguchi, H., Lombardo, C. R., Van Dort, H. M. and Low, P. S. (1992) Structural and functional characterization of band 3 from Southeast Asian ovalocytes. J. Biol. Chem. 267, 25792-25797
16. Schofield, A. E., Reardon, D. M. and Tanner, M. J. A. (1992) Defective anion transport activity of the abnormal band 3 in hereditary ovalocytic red blood cells. Nature (London) 355, 836-868
17. Cheung, J. C. and Reithmeier, R. A. F. (2005) Membrane integration and topology of the first transmembrane segment in normal and Southeast Asian ovalocytosis human erythrocyte anion exchanger 1. Mol. Membr. Biol. 22, 203-214
18. Jennings, M. L. and Gosselink, P. G. (1995) Anion exchange protein in Southeast Asian ovalocytes: heterodimer formation between normal and variant subunits. Biochemistry 34, 3588-3595
19. Salhany, J. M. and Schopfer, L. M. (1996) Interactions between mutant and wild-type band 3 subunits in hereditary Southeast Asian ovalocytic red blood cell membranes. Biochemistry 35, 251-257
20. Kuma, H., Abe, Y., Askin, D., Bruce, L. J., Hamasaki, T., Tanner, M. J. A. and Hamasaki, N. (2002) Molecular basis and functional consequences of the dominant effects of the mutant band 3 on the structure of normal band 3 in Southeast Asian ovalocytosis. Biochemistry 41, 3311-3320
21. Groves, J. D., Ring, S. M., Schofield, A. E. and Tanner, M. J. A. (1993) The expression of the abnormal human red cell anion transporter from South-East Asian ovalocytes (band 3 SAO) in Xenopus oocytes. FEBS Lett. 330, 186-190
22. Chernova, M. N., Jarolim, P., Palek, J. and Alper, S. L. (1995) Overexpression of AE1 Prague, but not of AE1 SAO, inhibits wild-type AE1 trafficking in Xenopus oocytes. J. Membr. Biol. 148, 203-210
23. Groves, J. D. and Tanner, M. J. A. (1992) Glycophorin A facilitates the expression of human band 3-mediated anion transport in Xenopus oocytes. J. Biol. Chem. 267, 22163-22170
24. Beckmann, R., Smythe, J. S., Anstee, D. J. and Tanner, M. J. A. (2001) Coexpression of band 3 mutants and Rh polypeptides: differential effects of band 3 on the expression of the Rh complex containing D polypeptide and the Rh complex containing CcEe polypeptide. Blood 97, 2496-2505
25. Lozzio, C. B. and Lozzio, B. B. (1975) Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45, 321-334
26. 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
27. Tam, L. Y., Landolt-Marticorena, C. and Reithmeier, R. A. F. (1996) Glycosylation of multiple extracytosolic loops in Band 3, a model polytopic membrane protein. Biochem. J. 318, 645-648
28. Li, J., Quilty, J., Popov, M. and Reithmeier, R. A. F. (2000) Processing of N-linked oligosaccharide depends on its location in the anion exchanger, AE1, membrane glycoprotein. Biochem. J. 349, 51-57
29. Quilty, J. A., Li, J. and Reithmeier, R. A. F. (2002) Impaired trafficking of distal renal tubular acidosis mutants of the human kidney anion exchanger kAE1. Am. J. Physiol. Renal Physiol. 282, F810-F820
30. Cordat, E., Li, J. and Reithmeier, R. A. F. (2003) Carboxyl-terminal truncations of human anion exchanger impair its trafficking to the plasma membrane. Traffic 4, 642-651
31. Graham, F. L. and van der Eb, A. J. (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467
32. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
33. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76, 4350-4354
34. Cheung, J. C. and Reithmeier, R. A. F. (2004) Palmitoylation is not required for trafficking of human anion exchanger 1 to the cell surface. Biochem. J. 378, 1015-1021
35. Quilty, J. A. and Reithmeier, R. A. F. (2000) Trafficking and folding defects in hereditary spherocytosis mutants of the human red cell anion exchanger. Traffic 1, 987-998
36. Quilty, J. A., Cordat, E. and Reithmeier, R. A. F. (2002) Impaired trafficking of human kidney anion exchanger (kAE1) caused by hetero-oligomer formation with a truncated mutant associated with distal renal tubular acidosis. Biochem. J. 368, 895-903
37. Kittanakom, S., Cordat, E., Akkarapatumwong, V., Yenchitsomanus, P. T. and Reithmeier, R. A. F. (2004) Trafficking defects of a novel autosomal recessive distal renal tubular acidosis mutant (S773P) of the human kidney anion exchanger (kAE1). J. Biol. Chem. 279, 40960-40971
38. Cordat, E., Kittanakom, S., Yenchitsomanus, P., Li, J., Du, K., Lukacs, G. L. and Reithmeier, R. A. F. (2005) Dominant and recessive distal renal acidosis mutations of the human kidney anion exchanger 1 induce distinct trafficking defects in epithelial cells. Traffic, in the press
39. Toye, A. M., Banting, G. and Tanner, M. J. A. (2004) Regions of human kidney anion exchanger 1 (kAE1) required for basolateral targeting of kAE1 in polarised kidney cells: mis-targeting explains dominant renal tubular acidosis (dRTA). J. Cell Sci. 117, 1399-1410
40. Devonald, M. A., Smith, A. N., Poon, J. P., Ihrke, G. and Karet, F. E. (2003) Non-polarized targeting of AE1 causes autosomal dominant distal renal tubular acidosis. Nat. Genet. 33, 125-127
41. Denning, G. M., Anderson, M. P., Amara, J. F., Marshall, J., Smith, A. E. and Welsh, M. J. (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature (London) 358, 761-764
42. Nigg, E. A., Bron, C., Girardet, M. and Cherry, R. J. (1980) Band 3-glycophorin A association in erythrocyte membrane demonstrated by combining protein diffusion measurements with antibody-induced cross-linking. Biochemistry 19, 1887-1893
43. Bruce, L. J., Ring, S. M., Anstee, D. J., Reid, M. E., Wilkinson, S. and Tanner, M. J. A. (1995) Charges in the blood group Wright antigens are associated with a mutation at amino acid 658 in human erythrocyte band 3: a site of interaction between band 3 and glycophorin A under certain conditions. Blood 85, 541-547
44. Bruce, L. J., Groves, J. D., Okubo, Y., Thilaganathan, B. and Tanner, M. J. A. (1994) Altered band 3 structure and function in glycophorin A- and B-deficient (MkMk) red blood cells. Blood 84, 916-922
45. Young, M. T., Beckmann, R., Toye, A. M. and Tanner, M. J. A. (2000) Red-cell glycophorin A-band 3 interactions associated with the movement of band 3 to the cell surface. Biochem. J. 350, 53-60
46. Tanphaichitr, V. S., Sumboonnanonda, A., Ideguchi, H., Shayakul, C., Brugnara, C., Takao, M., Veerakul, G. and Alper, S. L. (1998) Novel AE1 mutations in recessive distal renal tubular acidosis. Loss-of-function is rescued by glycophorin A. J. Clin. Invest. 102, 2173-2179