Cystinuria-specific rBAT(R365W) mutation reveals two translocation pathways in the amino acid transporter rBAT-b0,+AT

Biochemical Journal

Volumn 377, Issue 3, 2004, Pages 665-674

  Pineda, Marta ^a   Wagner, Carsten A ^b   Bröer, Angelika ^c   Stehberger, Paul A ^d   Kaltenbach, Simone ^d   Gelpí, Josep Ll ^a   Martín Del Río, Rafael ^e   Zorzano, Antonio ^a   Palacín, Manuel ^a   Lang, Florian ^d   Bröer, Stefan ^c,d  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

Antiporter; Cystinuria; Epithelial transport; Heteromeric amino acid transporter; Membrane transport; Structure function relationship

Indexed keywords

AMINO ACIDS; CATALYSIS; CELL MEMBRANES; DISSOCIATION; MUTAGENS;

PLASMA MEMBRANE;

BIOCHEMISTRY;

AMINO ACID; AMINO ACID TRANSPORTER; ANTIPORTER; ARGININE; LEUCINE; LYSINE; MUTANT PROTEIN; PROTEIN RBAT; PROTEIN SUBUNIT; TRYPSIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CYSTINURIA; DISSOCIATION; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FUNCTION; TEMPERATURE DEPENDENCE;

ANIMALIA;

EID: 10744224231     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/bj20030956     Document Type: Article

References (40)

1. Wagner, C. A., Lang, F. and Broer, S. (2001) Function and structure of heterodimeric amino acid transporters. Am. J. Physiol. Cell Physiol. 281, C1077-C1093
2. Chillaron, J., Roca, R., Valencia, A., Zorzano, A. and Palacin, M. (2001) Heteromeric amino acid transporters: biochemistry, genetics, and physiology. Am. J. Physiol. Renal Physiol. 281, F995-F1018
3. Verrey, F., Jack, D. L., Paulsen, I. T., Saier, Jr, M. H. and Pfeiffer, R. (1999) New glycoprotein-associated amino acid transporters. J. Membr. Biol. 172, 181-192
4. Deves, R. and Boyd, C. A. (2000) Surface antigen CD98(4R2): not a single membrane protein, but a family of proteins with multiple functions. J. Membr. Biol. 173, 165-177
5. Broer, S. and Wagner, C. A. (2002) Structure-function relationships of heterodimeric amino acid transporters. Cell Biochem. Biophys. 36, 155-168
6. Verrey, F., Meier, C., Rossier, G. and Kuhn, L. C. (2000) Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflugers Arch. 440, 503-512
7. Reig, N., Chillaron, J., Bartoccioni, P., Fernandez, E., Bendahan, A., Zorzano, A., Kanner, B., Palacin, M. and Bertran, J. (2002) The light subunit of system b(0,+) is fully functional in the absence of the heavy subunit. EMBO J. 21, 4906-4914
8. Peter, G. J., Panova, T. B., Christie, G. R. and Taylor, P. M. (2000) Cysteine residues in the C-terminus of the neutral-and basic-amino-acid transporter heavy-chain subunit contribute to functional properties of the system b0,+-type amino acid transporter. Biochem. J. 351, 677-682
9. Rajan, D. P., Huang, W., Kekuda, R., George, R. L., Wang, J., Conway, S. J., Devoe, L. D., Leibach, F. H., Prasad, P. D. and Ganapathy, V. (2000) Differential influence of the 4F2 heavy chain and the protein related to b(0,+) amino acid transport on substrate affinity of the heteromeric b(0,+) amino acid transporter. J. Biol. Chem. 275, 14331-14335
10. Feliubadalo, L., Font, M., Purroy, J., Rousaud, F., Estivill, X., Nunes, V., Golomb, E., Centola, M., Aksentijevich, I., Kreiss, Y. et al. (1999) Non-type I cystinuria caused by mutations in SLC7A9, encoding a subunit (b0,+AT) of rBAT. International Cystinuria Consortium. Nat. Genet. 23, 52-57
11. Pfeiffer, R., Loffing, J., Rossier, G., Bauch, C., Meier, C., Eggermann, T., Loffing-Cueni, D., Kuhn, L. C. and Verrey, F. (1999) Luminal heterodimeric amino acid transporter defective in cystinuria. Mol. Biol. Cell 10, 4135-4147
12. Bauch, C. and Verrey, F. (2002) Apical heterodimeric cystine and cationic amino acid transporter expressed in MDCK cells. Am. J. Physiol. Renal Physiol. 283, F181-F189
13. Fernandez, E., Carrascal, M., Rousaud, F., Abian, J., Zorzano, A., Palacin, M. and Chillaron, J. (2002) rBAT-b(0,+)AT heterodimer is the main apical reabsorption system for cystine in the kidney. Am. J. Physiol. Renal Physiol. 283, F540-F548
14. Font, M. A., Feliubadalo, L., Estivill, X., Nunes, V., Golomb, E., Kreiss, Y., Pras, E., Bisceglia, L., d'Adamo, A. P., Zelante, L. et al. (2001) Functional analysis of mutations in SLC7A9, and genotype-phenotype correlation in non-Type I cystinuria. Hum. Mol. Genet. 10, 305-316
15. Calonge, M. J., Gasparini, P., Chillaron, J., Chillon, M., Gallucci, M., Rousaud, F., Zelante, L., Testar, X., Dallapiccola, B., Di Silverio, F. et al. (1994) Cystinuria caused by mutations in rBAT, a gene involved in the transport of cystine. Nat. Genet. 6, 420-425
16. Dello Strologo, L., Pras, E., Pontesilli, C., Beccia, E., Ricci-Barbini, V., de Sanctis, L., Ponzone, A., Gallucci, M., Bisceglia, L., Zelante, L. et al. (2002) Comparison between SLC3A1 and SLC7A9 cystinuria patients and carriers: a need for a new classification. J. Am. Soc. Nephrol. 13, 2547-2553
17. Chillaron, J., Estevez, R., Samarzija, I., Waldegger, S., Testar, X., Lang, F., Zorzano, A., Busch, A. and Palacin, M. (1997) An intracellular trafficking defect in type I cystinuria rBAT mutants M467T and M467K. J. Biol. Chem. 272, 9543-9549
18. Palacin, M., Borsani, G. and Sebastio, G. (2001) The molecular bases of cystinuria and lysinuric protein intolerance. Curr. Opin. Genet. Dev. 11, 328-335
19. Bertran, J., Werner, A., Moore, M. L., Stange, G., Markovich, D., Biber, J., Testar, X., Zorzano, A., Palacin, M. and Murer, H. (1992) Expression cloning of a cDNA from rabbit kidney cortex that induces a single transport system for cystine and dibasic and neutral amino acids. Proc. Natl. Acad. Sci. U.S.A. 89, 5601-5605
20. Wells, R. G. and Hediger, M. A. (1992) Cloning of a rat kidney cDNA that stimulates dibasic and neutral amino acid transport and has sequence similarity to glucosidases. Proc. Natl. Acad. Sci. U.S.A. 89, 5596-5600
21. Busch, A. E., Herzer, T., Waldegger, S., Schmidt, F., Palacin, M., Biber, J., Markovich, D., Murer, H. and Lang, F. (1994) Opposite directed currents induced by the transport of dibasic and neutral amino acids in Xenopus oocytes expressing the protein rBAT. J. Biol. Chem. 269, 25581-25586
22. Chillaron, J., Estevez, R., Mora, C., Wagner, C. A., Suessbrich, H., Lang, F., Gelpi, J. L., Testar, X., Busch, A. E., Zorzano, A. et al. (1996) Obligatory amino acid exchange via systems b0,+-like and y+L-like. A tertiary active transport mechanism for renal reabsorption of cystine and dibasic amino acids. J. Biol. Chem. 271, 17761-17770
23. Coady, M. J., Jalal, F., Chen, X., Lemay, G., Berteloot, A. and Lapointe, J. Y. (1994) Electrogenic amino acid exchange via the rBAT transporter. FEBS Lett. 356, 174-178
24. Wagner, C. A., Friedrich, B., Setiawan, I., Lang, F. and Broer, S. (2000) The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell. Physiol. Biochem. 10, 1-12
25. Bertran, J., Werner, A., Chillaron, J., Nunes, V., Biber, J., Testar, X., Zorzano, A., Estivill, X., Murer, H. and Palacin, M. (1993) Expression cloning of a human renal cDNA that induces high affinity transport of L-cystine shared with dibasic amino acids in Xenopus oocytes. J. Biol. Chem. 268, 14842-14849
26. +-independent isoleucine transport activity from rat brain in Xenopus laevis oocytes. Biochim. Biophys. Acta 1192, 95-100
27. Mosckovitz, R., Udenfriend, S., Felix, A., Heimer, E. and Tate, S. S. (1994) Membrane topology of the rat kidney neutral and basic amino acid transporter. FASEB J. 8, 1069-1074
28. Wang, Y. and Tate, S. S. (1995) Oligomeric structure of a renal cystine transporter: implications in cystinuria. FEBS Lett. 368, 389-392
29. Gasparini, P. Calonge, M. J., Bisceglia, L., Purroy, J., Dianzani, I., Notarangelo, A., Rousaud, F., Gallucci, M., Testar, X., Ponzone, A. et al. (1995) Molecular genetics of cystinuria: identification of four new mutations and seven polymorphisms, and evidence for genetic heterogeneity. Am. J. Hum. Genet. 57, 781-788
30. Meier, C., Ristic, Z., Klauser, S. and Verrey, F. (2002) Activation of system L heterodimeric amino acid exchangers by intracellular substrates. Embo J. 21, 580-589
31. Stegen, C., Matskevich, I., Wagner, C. A., Paulmichl, M., Lang, F. and Broer, S. (2000) Swelling-induced taurine release without chloride channel activity in Xenopus laevis oocytes expressing anion channels and transporters. Biochim. Biophys. Acta 1467, 91-100
32. Torras-Llort, M., Torrents, D., Soriano-Garcia, J. F., Gelpi, J. L., Estevez, R., Ferrer, R., Palacin, M. and Moreto, M. (2001) Sequential amino acid exchange across b(0,+)-like system in chicken brush border jejunum. J. Membr. Biol. 180, 213-220
33. Palacin, M., Goodyer, P., Nunes, V. and Gasparini, P. (2001) Cystinuria. In Metabolic and Molecular Basis of Inherited Diseases (Scriver, C. R., Beaudet, A. L., Sly, S. W. and Valle, D., eds.), pp. 4909-4932, McGraw-Hill, New York
34. Albers, A., Lahme, S., Wagner, C., Kaiser, P., Zerres, K., Capasso, G., Pica, A., Palacin, M., Lang, F., Bichler, K. H. et al. (1999) Mutations in the SLC3A1 gene in cystinuric patients: frequencies and identification of a novel mutation. Genet. Test. 3, 227-231
35. Ward, C. L. and Kopito, R. R. (1994) Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J. Biol. Chem. 269, 25710-25718
36. 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
37. Saadi, I., Chen, X. Z., Hediger, M., Ong, P., Pereira, P., Goodyer, P. and Rozen, R. (1998) Molecular genetics of cystinuria: mutation analysis of SLC3A1 and evidence for another gene in type I (silent) phenotype. Kidney Int. 54, 48-55
38. Coady, M. J., Chen, X. Z. and Lapointe, J. Y. (1996) rBAT is an amino acid exchanger with variable stoichiometry. J. Membr. Biol. 149, 1-8
39. Palmieri, F., Indiveri, C., Bisaccia, F. and Kramer, R. (1993) Functional properties of purified and reconstituted mitochondrial metabolite carriers. J. Bioenerg. Biomembr. 25, 525-535
40. Restrepo, D., Cronise, B. L., Snyder, R. B. and Knauf, P. A. (1992) A novel method to differentiate between ping-pong and simultaneous exchange kinetics and its application to the anion exchanger of the HL60 cell. J. Gen. Physiol. 100, 825-846