A biochemical framework for SLC4A11, the plasma membrane protein defective in corneal dystrophies

Biochemistry

Volumn 50, Issue 12, 2011, Pages 2157-2169

  Vilas, Gonzalo L ^a   Morgan, Patricio E ^b   Loganathan, Sampath K ^a   Quon, Anita ^a   Casey, Joseph R ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC DOMAINS; CYTOSOLIC; EFFECTIVE CONCENTRATION; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMAN PLASMAS; HYDROPATHY ANALYSIS; MISFOLDED PROTEINS; PLASMA MEMBRANE PROTEIN; POINT MUTATIONS; PRE-INCUBATION; PROTEIN BINDING; TOPOLOGY MODEL;

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; CELL MEMBRANES; RESINS; SODIUM; TOPOLOGY;

PROTEINS;

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; BICARBONATE; MEMBRANE PROTEIN; RESIN; SLC4A11 PROTEIN; STILBENEDISULFONIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CONTROLLED STUDY; CORNEA DYSTROPHY; CYTOPLASM; CYTOSOLIC FRACTION; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEFECT; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

4-ACETAMIDO-4'-ISOTHIOCYANATOSTILBENE-2,2'-DISULFONIC ACID; ALLELES; AMINO ACID SEQUENCE; ANION TRANSPORT PROTEINS; ANTIPORTERS; CELL EXTRACTS; CELL MEMBRANE; CORNEAL DYSTROPHIES, HEREDITARY; ENDOPLASMIC RETICULUM; EPITOPES; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; TEMPERATURE; TRYPSIN;

EID: 79952928648     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101887z     Document Type: Article

References (56)

1. Parker, M. D., Ourmozdi, E. P., and Tanner, M. J. (2001) Human BTR1, a new bicarbonate transporter superfamily member and human AE4 from kidney Biochem. Biophys. Res. Commun. 282, 1103-1109 (Pubitemid 32912838)
2. Lopez, I. A., Rosenblatt, M. I., Kim, C., Galbraith, G. C., Jones, S. M., Kao, L., Newman, D., Liu, W., Yeh, S., Pushkin, A., Abuladze, N., and Kurtz, I. (2009) Slc4a11 gene disruption in mice: cellular targets of sensorineuronal abnormalities J. Biol. Chem. 284, 26882-26896
3. - transporters Pfluegers Arch. 447, 496-509
4. Desir, J., Moya, G., Reish, O., Van Regemorter, N., Deconinck, H., David, K. L., Meire, F. M., and Abramowicz, M. J. (2007) Borate transporter SLC4A11 mutations cause both Harboyan syndrome and non-syndromic corneal endothelial dystrophy J. Med. Genet. 44, 322-326 (Pubitemid 46732626)
5. Vithana, E. N., Morgan, P., Sundaresan, P., Ebenezer, N. D., Tan, D. T., Mohamed, M. D., Anand, S., Khine, K. O., Venkataraman, D., Yong, V. H., Salto-Tellez, M., Venkatraman, A., Guo, K., Hemadevi, B., Srinivasan, M., Prajna, V., Khine, M., Casey, J. R., Inglehearn, C. F., and Aung, T. (2006) Mutations in sodium-borate cotransporter SLC4A11 cause recessive congenital hereditary endothelial dystrophy (CHED2) Nat. Genet. 38, 755-757 (Pubitemid 43980595)
6. Vithana, E. N., Morgan, P. E., Ramprasad, V., Tan, D. T., Yong, V. H., Venkataraman, D., Venkatraman, A., Yam, G. H., Nagasamy, S., Law, R. W., Rajagopal, R., Pang, C. P., Kumaramanickevel, G., Casey, J. R., and Aung, T. (2008) SLC4A11 mutations in Fuchs endothelial corneal dystrophy Hum. Mol. Genet. 17, 656-666 (Pubitemid 351292255)
7. Klintworth, G. K. (2009) Corneal dystrophies Orphanet. J. Rare Dis. 4, 7
8. Cordat, E. and Casey, J. R. (2009) Bicarbonate transport in cell physiology and disease Biochem. J. 417, 423-439
9. +-independent SLC4 anion exchangers J. Exp. Biol. 212, 1672-1683
10. +-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation Mol. Cell 16, 331-341 (Pubitemid 39504788)
11. Jiao, X., Sultana, A., Garg, P., Ramamurthy, B., Vemuganti, G. K., Gangopadhyay, N., Hejtmancik, J. F., and Kannabiran, C. (2007) Autosomal recessive corneal endothelial dystrophy (CHED2) is associated with mutations in SLC4A11 J. Med. Genet. 44, 64-68 (Pubitemid 46142841)
12. Desir, J. and Abramowicz, M. (2008) Congenital hereditary endothelial dystrophy with progressive sensorineural deafness (Harboyan syndrome) Orphanet. J. Rare Dis. 3, 28
13. Groeger, N., Froehlich, H., Maier, H., Olbrich, A., Kostin, S., Braun, T., and Boettger, T. (2010) Slc4a11 prevents osmotic imbalance leading to corneal endothelial dystrophy, deafness, and polyuria J. Biol. Chem. 285, 14467-14474
14. Hemadevi, B., Veitia, R. A., Srinivasan, M., Arunkumar, J., Prajna, N. V., Lesaffre, C., and Sundaresan, P. (2008) Identification of mutations in the SLC4A11 gene in patients with recessive congenital hereditary endothelial dystrophy Arch. Ophthalmol. 126, 700-708 (Pubitemid 351679567)
15. Pimplikar, S. W. and Reithmeier, R. A. F. (1986) Affinity chromatography of band 3, the anion transport protein of erythrocyte membranes J. Biol. Chem. 261, 9770-9778 (Pubitemid 17214106)
16. Pimplikar, S. W. and Reithmeier, R. A. F. (1988) Studies on the interaction of matrix-bound inhibitor with band 3, the anion transport protein of erythrocyte membranes Biochim. Biophys. Acta 942, 253-261
17. 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
18. 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 (Pubitemid 37062687)
19. Ruetz, S., Lindsey, A. E., and Kopito, R. R. (1993) Function and biosynthesis of erythroid and nonerythroid anion exchangers Soc. Gen. Physiol. Ser. 48, 193-200 (Pubitemid 23137977)
20. Laemmli, U. K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4 Nature 227, 680-685
21. - exchanger, AE1 Biochemistry 49, 9226-9240
22. Takida, S. and Wedegaertner, P. B. (2003) Heterotrimer formation, together with isoprenylation, is required for plasma membrane targeting of Gbetagamma J. Biol. Chem. 278, 17284-17290 (Pubitemid 36799611)
23. Jennings, M. L., Anderson, M. P., and Monaghan, R. (1986) Monoclonal antibodies against human erythrocyte band 3 protein: localization of proteolytic cleavage sites and stilbenedisulfonate-binding lysine residues J. Biol. Chem. 261, 9002-9010 (Pubitemid 17205106)
24. 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 (Pubitemid 8267428)
25. Zhao, R. and Reithmeier, R. A. (2001) Expression and characterization of the anion transporter homologue YNL275w in Saccharomyces cerevisiae Am. J. Physiol. Cell. Physiol. 281, C33-C45
26. Zhu, Q., Lee, D. W. K., 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 (Pubitemid 36801221)
27. Lieberman, D. M. and Reithmeier, R. A. F. (1988) Localization of the carboxyl terminus of band 3 to the cytoplasmic side of the erythrocyte membrane using antibodies raised against a synthetic peptide J. Biol. Chem. 263, 10022-10028
28. Helbig, A. O., Heck, A. J., and Slijper, M. (2010) Exploring the membrane proteome-challenges and analytical strategies J. Proteomics 73, 868-878
29. Dorwart, M. R., Shcheynikov, N., Baker, J. M., Forman-Kay, J. D., Muallem, S., and Thomas, P. J. (2008) Congenital chloride-losing diarrhea causing mutations in the stas domain result in misfolding and mistrafficking of SLC26A3 J. Biol. Chem. 283, 8711-8722
30. Cui, L., Aleksandrov, L., Chang, X. B., Hou, Y. X., He, L., Hegedus, T., Gentzsch, M., Aleksandrov, A., Balch, W. E., and Riordan, J. R. (2007) Domain interdependence in the biosynthetic assembly of CFTR J. Mol. Biol. 365, 981-994 (Pubitemid 46014191)
31. Cabantchik, Z. I. and Greger, R. (1992) Chemical probes for anion transporters of mammalian membranes Am. J. Physiol. 262, C803-C827
32. Kittanakom, S., Cordat, E., Akkarapatumwong, V., Yenchitsomanus, P. T., and Reithmeier, R. A. (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 (Pubitemid 39287696)
33. Quilty, J. A., Cordat, E., and Reithmeier, R. A. (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. 13, 895-903 (Pubitemid 36042692)
34. Riazuddin, S. A., Vithana, E. N., Seet, L. F., Liu, Y., Al-Saif, A., Koh, L. W., Heng, Y. M., Aung, T., Meadows, D. N., Eghrari, A. O., Gottsch, J. D., and Katsanis, N. (2010) Missense mutations in the sodium borate co-transporter SLC4A11 cause late onset Fuchs corneal dystrophy Hum. Mutat. 31, 1261-1268
35. Wang, Y., Bartlett, M. C., Loo, T. W., and Clarke, D. M. (2006) Specific rescue of cystic fibrosis transmembrane conductance regulator processing mutants using pharmacological chaperones Mol. Pharmacol. 70, 297-302
36. Robert, R., Carlile, G. W., Liao, J., Balghi, H., Lesimple, P., Liu, N., Kus, B., Rotin, D., Wilke, M., de Jonge, H. R., Scholte, B. J., Thomas, D. Y., and Hanrahan, J. W. (2010) Correction of the delta phe508 cystic fibrosis transmembrane conductance regulator trafficking defect by the bioavailable compound glafenine Mol. Pharmacol. 77, 922-930
37. Aldave, A. J., Yellore, V. S., Bourla, N., Momi, R. S., Khan, M. A., Salem, A. K., Rayner, S. A., Glasgow, B. J., and Kurtz, I. (2007) Autosomal recessive CHED associated with novel compound heterozygous mutations in SLC4A11 Cornea 26, 896-900 (Pubitemid 47220572)
38. Desir, J., Moya, G., Reish, O., Van Regemorter, N., Deconinck, H., David, K. L., Meire, F. M., and Abramowicz, M. (2007) Borate transporter SLC4A11 mutations cause both Harboyan syndrome and non-syndromic corneal endothelial dystrophy J. Med. Genet. 44, 322-326 (Pubitemid 46732626)
39. Kumar, A., Bhattacharjee, S., Prakash, D. R., and Sadanand, C. S. (2007) Genetic analysis of two Indian families affected with congenital hereditary endothelial dystrophy: two novel mutations in SLC4A11 Mol. Vision 13, 39-46 (Pubitemid 46111845)
40. Ramprasad, V. L., Ebenezer, N. D., Aung, T., Rajagopal, R., Yong, V. H., Tuft, S. J., Viswanathan, D., El-Ashry, M. F., Liskova, P., Tan, D. T., Bhattacharya, S. S., Kumaramanickavel, G., and Vithana, E. N. (2007) Novel SLC4A11 mutations in patients with recessive congenital hereditary endothelial dystrophy (CHED2) Hum. Mutat. 28, 522-523
41. Sultana, A., Garg, P., Ramamurthy, B., Vemuganti, G. K., and Kannabiran, C. (2007) Mutational spectrum of the SLC4A11 gene in autosomal recessive congenital hereditary endothelial dystrophy Mol. Vision 13, 1327-1332 (Pubitemid 47163215)
42. Aldahmesh, M., Khan, A., Meyer, B., and Alkuraya, F. (2009) Mutational spectrum of SLC4A11 in autosomal recessive CHED in Saudi Arabia Invest. Ophthalmol. Visual Sci. 50, 4142-4145
43. 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 (Konings, W. N., Kaback, H. R., and Lolkema, J. S., Eds.) pp 281 - 309, Elsevier Science, Amsterdam, The Netherlands.
44. Tang, X. B., Fujinaga, J., Kopito, R., and Casey, J. R. (1998) Topology of the region surrounding Glu681 of human AE1 protein, the erythrocyte anion exchanger J. Biol. Chem. 273, 22545-22553 (Pubitemid 28399822)
45. Tang, X.-B., Kovacs, M., Sterling, D., and Casey, J. R. (1999) Identification of residues lining the translocation pore of human AE1, plasma membrane anion exchange protein J. Biol. Chem. 274, 3557-3564 (Pubitemid 29077197)
46. - exchange protein, AE1 J. Biol. Chem. 279, 23565-23573 (Pubitemid 38685670)
47. Cordat, E. and Casey, J. R. (2009) Bicarbonate transport in cell physiology and disease Biochem. J. 417, 423-439
48. Jennings, M. L. and Passow, H. (1979) Anion transport across the erythrocyte membrane in situ proteoysis of band 3 protein, and cross-linking of proteolytic fragments by 4,4′-diisothiocyanodihydrostilbene-2,2′- disulfonate Biochim. Biophys. Acta 554, 498-519 (Pubitemid 9234264)
49. 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 (Pubitemid 27193553)
50. - tunnel" revealed by SLC4A4 human mutation and structural model J. Biol. Chem. 283, 18402-18410
51. Wang, D. N. (1994) Band 3 protein: structure, flexibility and function FEBS Lett. 346, 26-31 (Pubitemid 24183822)
52. Chen, L. M., Liu, Y., and Boron, W. F. (2011) Role of an extracellular loop in determining the stoichiometry of Na/HCO3 cotransporters. J. Physiol., published online before print January 4, 2011, doi: 10.1113/jphysiol.2010.19873.
53. 2-) transporters: classification, function, structure, genetic diseases, and knockout models Am. J. Physiol. Renal Physiol. 290, F580-F599
54. 2DIDS (4,4′-diisothiocyanodihydrostilbene-2,2′-disulfonic acid) molecule J. Biol. Chem. 269, 1918-1926
55. Cormet-Boyaka, E., Jablonsky, M., Naren, A. P., Jackson, P. L., Muccio, D. D., and Kirk, K. L. (2004) Rescuing cystic fibrosis transmembrane conductance regulator (CFTR)-processing mutants by transcomplementation Proc. Natl. Acad. Sci. U.S.A. 101, 8221-8226 (Pubitemid 38698081)
56. Tan, L., Cai, Z. Q., and Lai, N. S. (2009) Accuracy and sensitivity of the dynamic ocular thermography and inter-subjects ocular surface temperature (OST) in Chinese young adults Contact Lens Anterior Eye 32, 78-83