Cloning and functional expression of the first eukaryotic Na +-tryptophan symporter, AgNAT6

Journal of Experimental Biology

Volumn 212, Issue 10, 2009, Pages 1559-1567

  Meleshkevitch, Ella A ^a   Robinson, Marvin ^b   Popova, Lyudmila B ^b,c   Miller, Melissa M ^b   Harvey, William R ^b   Boudko, Dmitri Y ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

AgNAT8; NAT; Synergy.

Indexed keywords

COTRANSPORTER; SODIUM; TRYPTOPHAN;

AMINO ACID SEQUENCE; ANIMAL; ANOPHELES GAMBIAE; ARTICLE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; LARVA; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; LARVA; MOLECULAR SEQUENCE DATA; PHYLOGENY; SODIUM; SYMPORTERS; TRYPTOPHAN;

ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS); EUKARYOTA; HEXAPODA; XENOPUS LAEVIS;

EID: 66149135239     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.027383     Document Type: Article

References (41)

1. Androutsellis-Theotokis, A., Goldberg, N. R., Ueda, K., Beppu, T., Beckman, M. L., Das, S., Javitch, J. A. and Rudnick, G. (2003). Characterization of a functional bacterial homologue of sodium-dependent neurotransmitter transporters. J. Biol. Chem. 278, 12703-12709.
2. Boudko, D. Y., Kohn, A. B., Meleshkevitch, E. A., Dasher, M. K., Seron, T. J., Stevens, B. R. and Harvey, W. R. (2005a). Ancestry and progeny of nutrient amino acid transporters. Proc. Natl. Acad. Sci. USA 102, 1360-1365.
3. Boudko, D. Y., Stevens, B. R., Donly, B. C. and Harvey, W. R. (2005b). Nutrient amino acid and neurotransmitter transporters. In Comprehensive Molecular Insect Science, vol. 4 (ed. K. Iatrou, S. S. Gill and L. I. Gilbert), pp. 255-309. Amsterdam: Elsevier.
4. Broer, A., Wagner, C. A., Lang, F. and Broer, S. (2000). The heterodimeric amino acid transporter 4F2hc/y(+)LAT2 mediates arginine efflux in exchange with glutamine. Biochem. J. 349, 787-795.
5. Broer, A., Klingel, K., Kowalczuk, S., Rasko, J. E. J., Cavanaugh, J. and Broer, S. (2004). Molecular cloning of mouse amino acid transport system B-0, a neutral amino acid transporter related to Hartnup disorder. J. Biol. Chem. 279, 24467-24476.
6. Broer, A., Tietze, N., Kowalczuk, S., Chubb, S., Munzinger, M., Bak, L. K. and Broer, S. (2006). The orphan transporter v7-3 (slc6a15) is a Na+-dependent neutral amino acid transporter (B0AT2). Biochem. J. 393, 421-430.
7. Broer, S. (2008). Amino acid transport across mammalian intestinal and renal epithelia. Physiol. Rev. 88, 249-286.
8. Brooks, D. J., Fresco, J. R., Lesk, A. M. and Singh, M. (2002). Evolution of amino acid frequencies in proteins over deep time: inferred order of introduction of amino acids into the genetic code. Mol. Biol. Evol. 19, 1645-1655.
9. Castagna, M., Shayakul, C., Trotti, D., Sacchi, V. F., Harvey, W. R. and Hediger, M. A. (1998). Cloning and characterization of a potassium-coupled amino acid transporter. Proc. Natl. Acad. Sci. USA 95, 5395-5400.
10. Chakrabarti, A. C. (1994). Permeability of membranes to amino acids and modified amino acids: mechanisms involved in translocation. Amino Acids 6, 213-229.
11. Chakrabarti, A. C. and Deamer, D. W. (1994). Permeation of membranes by the neutral form of amino acids and peptides: relevance to the origin of peptide translocation. J. Mol. Evol. 39, 1-5.
12. Chen, N. H., Reith, M. E. and Quick, M. W. (2004). Synaptic uptake and beyond: the sodium- and chloride-dependent neurotransmitter transporter family SLC6. Pflugers Arch. 447, 519-531.
13. Clements, A. N. (1992). The Biology of Mosquitoes. London: Chapman & Hall.
14. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
15. Fernandez, E., Torrents, D., Zorzano, A., Palacin, M. and Chillaron, J. (2005). Identification and functional characterization of a novel low affinity aromaticpreferring amino acid transporter (arpAT). One of the few proteins silenced during primate evolution. J. Biol. Chem. 280, 19364-19372.
16. Forrest, L. R., Tavoulari, S., Zhang, Y. W., Rudnick, G. and Honig, B. (2007). Identification of a chloride ion binding site in Na+/Cl-dependent transporters. Proc. Natl. Acad. Sci. USA 104, 12761-12766.
17. Harvey, W. R., Boudko, D. Y., Rheault, M. R. and Okech, B. A. (2009). NHEVNAT: an H+ V-ATPase electrically coupled to a Na+:nutrient amino acid transporter (NAT) forms an Na+/H+ exchanger (NHE). J. Exp. Biol. 212, 347-357.
18. Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R. et al. (2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129-149.
19. Jespersen, T., Grunnet, M., Angelo, K., Klaerke, D. A. and Olesen, S. P. (2002). Dual-function vector for protein expression in both mammalian cells and Xenopus laevis oocytes. Biotechniques 32, 536-538.
20. Kanai, Y. and Hediger, M. A. (2004). The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch. 447, 469-479.
21. Kim, D. K., Kanai, Y., Chairoungdua, A., Matsuo, H., Cha, S. H. and Endou, H. (2001). Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. J. Biol. Chem 276, 17221-17228.
22. Marti-Renom, M. A., Stuart, A. C., Fiser, A., Sanchez, R., Melo, F. and Sali, A. (2000). Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29, 291-325.
23. Mastroberardino, L., Spindler, B., Pfeiffer, R., Skelly, P. J., Loffing, J., Shoemaker, C. B. and Verrey, F. (1998). Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature 395, 288-291.
24. Meleshkevitch, E. A., Assis-Nascimento, P., Popova, L. B., Miller, M. M., Kohn, A. B., Phung, E. N., Mandal, A., Harvey, W. R. and Boudko, D. Y. (2006). Molecular characterization of the first aromatic nutrient transporter from the sodium neurotransmitter symporter family. J. Exp. Biol. 209, 3183-3198.
25. Miller, M. M., Popova, L. B., Meleshkevitch, E. A., Tran, P. V. and Boudko, D. Y. (2008). The invertebrate B(0) system transporter, D. melanogaster NAT1, has unique d-amino acid affinity and mediates gut and brain functions. Insect Biochem. Mol. Biol. 38, 923-931.
26. Nicholas, K. B., Nicholas, H. B., Jr and Deerfield, D. W., II (1997). GeneDoc: analysis and visualization of genetic variation. EMBNET News 4, 14.
27. Okech, B. A., Boudko, D. Y., Linser, P. J. and Harvey, W. R. (2008a). Cationic pathway of pH regulation in larvae of Anopheles gambiae. J. Exp. Biol. 211, 957-968.
28. Okech, B. A., Meleshkevitch, E. A., Miller, M. M., Popova, L. B., Harvey, W. R. and Boudko, D. Y. (2008b). Synergy and specificity of two Na+-aromatic amino acid symporters in the model alimentary canal of mosquito larvae. J. Exp. Biol. 211, 1594-1602.
29. Quick, M. and Stevens, B. R. (2001). Amino acid transporter CAATCH1 is also an amino acid-gated cation channel. J. Biol. Chem. 276, 33413-33418.
30. Rajan, D. P., Kekuda, R., Huang, W., Wang, H., Devoe, L. D., Leibach, F. H., Prasad, P. D. and Ganapathy, V. (1999). Cloning and expression of a b(0,+)-like amino acid transporter functioning as a heterodimer with 4F2hc instead of rBAT. A new candidate gene for cystinuria. J. Biol. Chem. 274, 29005-29010.
31. Ramsay, J. A. (1950). Osmotic regulation in mosquito larvae. J. Exp. Biol. 27, 145-157.
32. Roux, M. J. and Supplisson, S. (2000). Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383.
33. Sali, A. and Blundell, T. L. (1993). Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.
34. Sloan, J. L. and Mager, S. (1999). Cloning and functional expression of a human Na+ and Cl-dependent neutral and cationic amino acid transporter B0+. J. Biol. Chem. 274, 23740-23745.
35. Sneath, P. H. A. and Sokal, R. R. (1973). Numerical Taxonomy: The Principles and Practice of Numerical Classification. San Francisco, CA: W. H. Freeman.
36. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
37. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
38. Ueda, K., Yamashita, A., Ishikawa, J., Shimada, M., Watsuji, T. O., Morimura, K., Ikeda, H., Hattori, M. and Beppu, T. (2004). Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res. 32, 4937-4944.
39. Yamashita, A., Singh, S. K., Kawate, T., Jin, Y. and Gouaux, E. (2005). Crystal structure of a bacterial homologue of Na+/Cl-dependent neurotransmitter transporters. Nature 437, 215-223.
40. Zomot, E., Bendahan, A., Quick, M., Zhao, Y., Javitch, J. A. and Kanner, B. I. (2007). Mechanism of chloride interaction with neurotransmitter:sodium symporters. Nature 449, 726-730.
41. Zuckerkandl, E. and Pauling, L. (1965). Evolutionary Divergence and Convergence in Proteins. New York: Academic Press.