A substrate access tunnel in the cytosolic domain is not an essential feature of the solute carrier 4 (SLC4) family of bicarbonate transporters

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 33848-33860

  Shnitsar, Volodymyr ^a   Li, Jing ^a   Li, Xuyao ^a   Calmettes, Charles ^a   Basu, Arghya ^b   Casey, Joseph R ^b   Moraes, Trevor F ^a   Reithmeier, Reinhart A F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE EXPRESSION; CONFORMATIONAL CHANGE; DISORDERED REGIONS; ESSENTIAL FEATURES; FUNCTIONAL EXPRESSION; HYDROGEN BONDED NETWORK; PROTEIN INTERACTION; STRUCTURAL ALTERATIONS;

ARGININE; CELL MEMBRANES; CHLORINE COMPOUNDS; PH;

ION EXCHANGE;

BICARBONATE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MEMBRANE PROTEIN; SOLUTE CARRIER 4 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANION EXCHANGE; ARTICLE; BIOTINYLATION; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; HYDROGEN BOND; IMMUNOLOCALIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

ANION EXCHANGER 1 (AE1); ANION TRANSPORT; BAND 3; MEMBRANE PROTEINS; PROTEIN FOLDING; SITE-DIRECTED MUTAGENESIS; SLC4; TRAFFICKING; TRANSPORTERS; X-RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; SODIUM-BICARBONATE SYMPORTERS;

EID: 84888390929     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.511865     Document Type: Article

References (70)

1. 3-exchangers. J. Nephrol. 15, S41-53
2. Romero, M. F. (2005) Molecular pathophysiology of SLC4 bicarbonate transporters. Curr. Opin. Nephrol. Hypertens. 14, 495-501
3. Alper, S. L. (2006) Molecular physiology of SLC4 anion exchangers. Exp. Physiol. 91, 153-161
4. Cordat, E., and Casey, J. R. (2009) Bicarbonate transport in cell physiology and disease. Biochem. J. 417, 423-439
5. Tanner, M. J. (2002) Band 3 anion exchanger and its involvement in erythrocyte and kidney disorders. Curr. Opin. Hematol. 9, 133-139
6. Bruce, L. J., and Tanner, M. J. (1999) Erythroid band 3 variants and disease. Baillieres Best Pract. Res. Clin. Haematol. 12, 637-654
7. Brosius, F. C, 3rd, Alper, S. L., Garcia, A. M., and Lodish, H. F. (1989) The major kidney band 3 gene transcript predicts an amino-terminal truncated band 3 polypeptide. J. Biol. Chem. 264, 7784-7787
8. Alper, S. L., Kopito, R. R., Libresco, S. M., and Lodish, H. F. (1988) Cloning and characterization of a murine band 3-related cDNA from kidney and from a lymphoid cell line. J. Biol. Chem. 263, 17092-17099
9. Yenchitsomanus, P. T., Kittanakom, S., Rungroj, N, Cordat, E., and Reithmeier, R. A. (2005) Molecular mechanisms of autosomal dominant and recessive distal renal tubular acidosis caused by SLC4A1 (AE1) mutations. J. Mol. Genet. Med. 1, 49-62
10. Cordat, E. (2006) Unraveling trafficking of the kidney anion exchanger 1 in polarized MDCK epithelial cells. Biochem. Cell Biol. 84, 949-959
11. Quilty, J. A., and Reithmeier, R. A. (2000) Trafficking and folding defects in hereditary spherocytosis mutants of the human red cell anion exchanger. Traffic 1, 987-998
12. Bruce, L. J., Wrong, O., Toye, A. M., Young, M. T., Ogle, G., Ismail, Z., Sinha, A. K., McMaster, P., Hwaihwanje, I., Nash, G. B., Hart, S., Lavu, E., Palmer, R., Othman, A., Unwin, R. J., and Tanner, M. J. (2000) Band 3 mutations, renal tubular acidosis and South-East Asian ovalocytosis in Malaysia and Papua New Guinea: loss of up to 95% band 3 transport in red cells. Biochem. J. 350, 41-51
13. Toye, A. M., Bruce, L. J., Unwin, R. J., Wrong, O., and Tanner, M. J. (2002) Band 3 Walton, a C-terminal deletion associated with distal renal tubular acidosis, is expressed in the red cell membrane but retained internally in kidney cells. Blood 99, 342-347
14. Quilty, J. A., Li, J., and Reithmeier, R. A. (2002) Impaired trafficking of distal renal tubular acidosis mutants of the human kidney anion exchanger kAE1. Am. J. Physiol. Renal Physiol. 282, F810-F820
15. Patterson, S. T., and Reithmeier, R. A. (2010) Cell surface rescue of kidney anion exchanger 1 mutants by disruption of chaperone interactions. J. Biol. Chem. 285, 33423-33434
16. Popov, M., and Reithmeier, R. A. (1999) Calnexin interaction with N-glycosylation mutants of a polytopic membrane glycoprotein, the human erythrocyte anion exchanger 1 (band 3). J. Biol. Chem. 274, 17635-17642
17. Bustos, S. P., and Reithmeier, R. A. (2011) Protein 4.2 interaction with hereditary spherocytosis mutants of the cytoplasmic domain of human anion exchanger 1. Biochem. J. 433, 313-322
18. Bustos, S. P., and Reithmeier, R. A. (2006) Structure and stability of hereditary spherocytosis mutants of the cytosolic domain of the erythrocyte anion exchanger 1 protein. Biochemistry 45, 1026-1034
19. Toye, A. M., Parker, M. D., Daly, CM., Lu, J., Virkki, L. V., Pelletier, M. F., and Boron, W. F. (2006) The human NBCe1-A mutant R881C, associated with proximal renal tubular acidosis, retains function but is mistargeted in polarized renal epithelia. Am. J. Physiol. Cell Physiol. 291, C788-C801
20. Igarashi, T., Inatomi, J., Sekine, T., Cha, S. H., Kanai, Y., Kunimi, M., Tsukamoto, K., Satoh, H., Shimadzu, M., Tozawa, F., Mori, T., Shiobara, M., Seki, G., and Endou, H. (1999) Mutations in SLC4A4 cause permanent isolated proximal renal tubular acidosis with ocular abnormalities. Nat. Genet. 23, 264-266
21. Dinour, D., Chang, M. H., Satoh, J., Smith, B. L., Angle, N., Knecht, A., Serban, I., Holtzman, E. J., and Romero, M. F. (2004) A novel missense mutation in the sodium bicarbonate cotransporter (NBCe1/SLC4A4) causes proximal tubular acidosis and glaucoma through ion transport defects. J. Biol. Chem. 279, 52238-52246
22. Horita, S., Yamada, H., Inatomi, J., Moriyama, N., Sekine, T., Igarashi, T., Endo, Y., Dasouki, M., Ekim, M., Al-Gazali, L., Shimadzu, M., Seki, G., and Fujita, T. (2005) Functional analysis of NBC1 mutants associated with proximal renal tubular acidosis and ocular abnormalities. J. Am. Soc. Nephrol. 16, 2270-2278
23. Chang, M. H., Di Piero, J., Sönnichsen, F. D., and Romero, M. F. (2008) Entry to "HCO3T tunnel" revealed by SLC4A4 human mutation and structural model. J. Biol. Chem. 283, 18402-18410
24. 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
25. 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
26. Low, P. S., Westfall, M. A., Allen, D. P., and Appell, K. C (1984) Characterization of the reversible conformational equilibrium of the cytoplasmic domain of erythrocyte membrane band 3. J. Biol. Chem. 259, 13070-13076
27. 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
28. Casey, J. R., Grinstein, S., and Orlowski, J. (2010) Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11, 50-61
29. Cordat, E., Li, J., and Reithmeier, R. A. (2003) Carboxyl-terminal truncations of human anion exchanger impair its trafficking to the plasma membrane. Traffic 4, 642-651
30. Cordat, E., Kittanakom, S., Yenchitsomanus, P. T., Li, J., Du, K., Lukacs, G. L., and Reithmeier, R. A. (2006) Dominant and recessive distal renal tubular acidosis mutations of kidney anion exchanger 1 induce distinct trafficking defects in MDCK cells. Traffic 7, 117-128
31. Sterling, D., Reithmeier, R. A., and Casey, J. R. (2001) A transport metabolon. Functional interaction of carbonic anhydrase II and chloride/bicarbonate exchangers. J. Biol. Chem. 276, 47886-47894
32. Loiselle, F. B., and Casey, J. R. (2003) Measurement of intracellular pH. Methods Mol. Biol. 227, 259-280
33. Thomas, J. A., Buchsbaum, R. N., Zimniak, A., and Racker, E. (1979) Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18, 2210-2218
34. Jennings, M. L., Anderson, M. P., and Monaghan, R. (1986) Monoclonal antibodies against human erythrocyte band 3 protein. Localization of proteolytic cleavage sites and stilbene disulfonate-binding lysine residues. J. Biol. Chem. 261, 9002-9010
35. Pang, A. J., Bustos, S. P., and Reithmeier, R. A. (2008) Structural characterization of the cytosolic domain of kidney chloride/bicarbonate anion exchanger 1 (kAE1). Biochemistry 47, 4510-4517
36. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C, and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
37. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41
38. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
39. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C, Richardson, J. S., Terwilliger, T. C, and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
40. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450
41. Li, J., Quilty, J., Popov, M., and Reithmeier, R. A. (2000) Processing of N-linked oligosaccharide depends on its location in the anion exchanger, AE1, membrane glycoprotein. Biochem. J. 349, 51-57
42. 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
43. Chernova, M. N., Stewart, A. K., Barry, P. N., Jennings, M. L., and Alper, S. L. (2008) Mouse Ae1 E699Q mediates SO/anion exchange with [SO]-dependent reversal of wild-type pHo sensitivity. Am. J. Physiol. Cell Physiol. 295, C302-C312
44. Kay, M. M., Bosman, G. J., and Lawrence, C. (1988) Functional topography of band 3: specific structural alteration linked to functional aberrations in human erythrocytes. Proc. Natl. Acad. Sci. U. S. A. 85, 492-496
45. Bruce, L. J., Kay, M. M., Lawrence, C, and Tanner, M. J. (1993) Band 3 HT, a human red-cell variant associated with acanthocytosis and increased anion transport, carries the mutation Pro-868→Leu in the membrane domain of band 3. Biochem. J. 293, 317-320
46. Cheung, J. C, Cordat, E., and Reithmeier, R. A. (2005) Trafficking defects of the Southeast Asian ovalocytosis deletion mutant of anion exchanger 1 membrane proteins. Biochem. J. 392, 425-434
47. Casey, J. R., Ding, Y., and Kopito, R. R. (1995) The role of cysteine residues in the erythrocyte plasma membrane anion exchange protein, AE1. J. Biol. Chem. 270, 8521-8527
48. Jennings, M. L., and Anderson, M. P. (1987) Chemical modification and labeling of glutamate residues at the stilbene disulfonate site of human red blood cell band 3 protein. J. Biol. Chem. 262, 1691-1697
49. Chernova, M. N., Jiang, L., Crest, M., Hand, M., Vandorpe, D. H, Strange, K., and Alper, S. L. (1997) Electrogenic sulfate/chloride exchange in Xenopus oocytes mediated by murine AE1 E699Q. J. Gen. Physiol. 109, 345-360
50. Groves, J. D., and Tanner, M. J. (1992) Glycophorin A facilitates the expression of human band 3-mediated anion transport in Xenopus oocytes. J. Biol. Chem. 267, 22163-22170
51. Bruce, L. J., Groves, J. D., Okubo, Y., Thilaganathan, B., and Tanner, M. J. (1994) Altered band 3 structure and function in glycophorin A- and B-deficient (MkMk) red blood cells. Blood 84, 916-922
52. Groves, J. D., and Tanner, M. J. (1994) The effects of glycophorin A on the expression of the human red cell anion transporter (band 3) in Xenopus oocytes. J. Membr. Biol. 140, 81-88
53. Wang, C C, Badylak, J. A., Lux, S. E., Moriyama, R., Dixon, J. E., and Low, P. S. (1992) Expression, purification, and characterization of the functional dimeric cytoplasmic domain of human erythrocyte band 3 in Escherichia coli. Protein Sci. 1, 1206-1214
54. Kiyatkin, A. B., Natarajan, P., Munshi, S., Minor, W., Johnson, J. E., and Low, P. S. (1995) Crystallization and preliminary x-ray analysis of the cytoplasmic domain of human erythrocyte band 3. Proteins 22, 293-297
55. Appell, K. C, and Low, P. S. (1981) Partial structural characterization of the cytoplasmic domain of the erythrocyte membrane protein, band 3. J. Biol. Chem. 256, 11104-11111
56. Walder, J. A., Chatterjee, R., Steck, T. L., Low, P. S., Musso, G. F., Kaiser, E. T., Rogers, P. H., and Arnone, A. (1984) The interaction of hemoglobin with the cytoplasmic domain of band 3 of the human erythrocyte membrane. J. Biol. Chem. 259, 10238-10246
57. Chang, S. H., and Low, P. S. (2003) Identification of a critical ankyrinbinding loop on the cytoplasmic domain of erythrocyte membrane band 3 by crystal structure analysis and site-directed mutagenesis. J. Biol. Chem. 278, 6879-6884
58. 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
59. Johnson, D. E., and Casey, J. R. (2011) Cytosolic H+ microdomain developed around AE1 during AE1-mediated Cl"/HCO3" exchange. J. Physiol. 589, 1551-1569
60. Wang, C. C, Moriyama, R., Lombardo, C R., and Low, P. S. (1995) Partial characterization of the cytoplasmic domain of human kidney band 3. J. Biol. Chem. 270, 17892-17897
61. 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
62. 2+-o-phenanthroline cross-linking. J. Biol. Chem. 254, 6151-6155
63. Rao, A., and Reithmeier, R. A. (1979) Reactive sulfhydryl groups of the band 3 polypeptide from human erythrocyte membranes. Location in the primary structure. J. Biol. Chem. 254, 6144-6150
64. Steck, T. L. (1972) Cross-linking the major proteins of the isolated erythrocyte membrane. J. Mol. Biol. 66, 295-305
65. Humphreys, B. D., Jiang, L., Chernova, M. N., and Alper, S. L. (1994) Functional characterization and regulation by pH of murine AE2 anion exchanger expressed in Xenopus oocytes. Am. J. Physiol. Cell Physiol. 267, C1295-C1307
66. Stewart, A. K., Chernova, M. N., Kunes, Y. Z., and Alper, S. L. (2001) Regulation of AE2 anion exchanger by intracellular pH: critical regions of the NH2-terminal cytoplasmic domain. Am. J. Physiol. Cell Physiol. 281, C1344-C1354
67. Alper, S. L., Chernova, M. N., and Stewart, A. K. (2002) How pH regulates a pH regulator: a regulatory hot spot in the N-terminal cytoplasmic domain of the AE2 anion exchanger. Cell Biochem. Biophys. 36, 123-136
68. Alper, S. L., Chernova, M. N., and Stewart, A. K. (2001) Regulation of Na+-independent Cr/HCO exchangers by pH. JOP2, 171-175
69. Stewart, A. K., Kerr, N., Chernova, M. N., Alper, S. L., and Vaughan-Jones, R. D. (2004) Acute pH-dependent regulation of AE2-mediated anion exchange involves discrete local surfaces of the NH2-terminal cytoplasmic domain. J. Biol. Chem. 279, 52664-52676
70. Kurschat, C. E., Shmukler, B. E., Jiang, L., Wilhelm, S., Kim, E. H., Chernova, M. N., Kinne, R. K., Stewart, A. K., and Alper, S. L. (2006) Alkalineshifted pHo sensitivity of AE2c1-mediated anion exchange reveals novel regulatory determinants in the AE2 N-terminal cytoplasmic domain. J. Biol. Chem. 281, 1885-1896