SLC17: A functionally diverse family of organic anion transporters

Molecular Aspects of Medicine

Volumn 34, Issue 2-3, 2013, Pages 350-359

  Reimer, Richard J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Neurotransmitter transporter; Organic anion transport; Sialin; SLC17; Type I phosphate transporter; Vesicular glutamate transporter; Vesicular nucleotide transporter

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ACETYLSALICYLIC ACID; BUMETANIDE; DICARBOXYLIC ACID DERIVATIVE; FUROSEMIDE; GLUTAMIC ACID DERIVATIVE; GLYCOPROTEIN; NEUROTRANSMITTER; ORGANIC ANION TRANSPORTER; PENICILLIN DERIVATIVE; PENICILLIN G; PHOSPHATE; PROBENECID; PROTEIN INHIBITOR; PROTEIN SLC17; PROTEIN SLC17A3; PROTEIN SLC17A4; SIALIN PROTEIN; SODIUM PHOSPHATE COTRANSPORTER 1; SODIUM PHOSPHATE COTRANSPORTER 2; UNCLASSIFIED DRUG; URATE; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3; VESICULAR NUCLEOTIDE TRANSPORTER PROTEIN;

ANION TRANSPORT; BINDING AFFINITY; DNA POLYMORPHISM; DRUG PROTEIN BINDING; EXPERIMENTAL MODEL; GENE; GENETIC ASSOCIATION; HUMAN; MOLECULAR CLONING; MOLECULAR GENETICS; MOLECULAR MECHANICS; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHATE TRANSPORT; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SCHIZOPHRENIA; SCL17A1 GENE; SCL17A2 GENE; SCL17A3 GENE; SCL17A4 GENE; SCL17A5 GENE; SCL17A6 GENE; SCL17A7 GENE; SCL17A8 GENE; SCL17A9 GENE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HUMANS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; N-ACETYLNEURAMINIC ACID; NEUROTRANSMITTER AGENTS; ORGANIC ANION TRANSPORTERS; PHYLOGENY; PROTEIN CONFORMATION; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE I; SYMPORTERS; TRANSPORT VESICLES; URIC ACID;

EID: 84875157300     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2012.05.004     Document Type: Review

References (46)

1. S.K. Ahmed, J.L. Etoga, S.A. Patel, R.J. Bridges, and C.M. Thompson Use of the hydantoin isostere to produce inhibitors showing selectivity toward the vesicular glutamate transporter versus the obligate exchange transporter system x(c)(-) Bioorg. Med. Chem. Lett. 21 2011 4358 4362
2. Y. Aihara, H. Mashima, H. Onda, S. Hisano, H. Kasuya, T. Hori, S. Yamada, H. Tomura, Y. Yamada, I. Inoue, I. Kojima, and J. Takeda Molecular cloning of a novel brain-type Na(+)-dependent inorganic phosphate cotransporter J. Neurochem. 74 2000 2622 2625
3. B. Alberts, J. Wilson, and T. Hunt Molecular Biology of the Cell fifth ed. 2008 Garland Science New York
4. J. Almqvist, Y. Huang, A. Laaksonen, D.N. Wang, and S. Hovmoller Docking and homology modeling explain inhibition of the human vesicular glutamate transporters Protein Sci. 16 2007 1819 1829
5. P. Aula, and W.A. Gahl C. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, The Metabolic and Molecular Bases of Inherited Disease 2001 McGraw-Hill New York 5109 5120
6. J. Biber, M. Custer, A. Werner, B. Kaissling, and H. Murer Localization of NaPi-1, a Na/Pi cotransporter, in rabbit kidney proximal tubules. II. Localization by immunohistochemistry Pflugers Arch. 424 1993 210 215
7. C. Cheret, A. Doyen, M. Yaniv, and M. Pontoglio Hepatocyte nuclear factor 1 alpha controls renal expression of the Npt1-Npt4 anionic transporter locus J. Mol. Biol. 322 2002 929 941
8. P. Courville, M. Quick, and R.J. Reimer Structure-function studies of the SLC17 transporter sialin identify crucial residues and substrate-induced conformational changes J. Biol. Chem. 285 2010 19316 19323
9. A. Dehghan, A. Kottgen, Q. Yang, S.J. Hwang, W.L. Kao, F. Rivadeneira, E. Boerwinkle, D. Levy, A. Hofman, B.C. Astor, E.J. Benjamin, C.M. van Duijn, J.C. Witteman, J. Coresh, and C.S. Fox Association of three genetic loci with uric acid concentration and risk of gout: a genome-wide association study Lancet 372 2008 1953 1961
10. S. El Mestikawy, A. Wallen-Mackenzie, G.M. Fortin, L. Descarries, and L.E. Trudeau From glutamate co-release to vesicular synergy: vesicular glutamate transporters Nat. Rev. Neurosci. 12 2011 204 216
11. R.T. Fremeau Jr.; K. Kam, T. Qureshi, J. Johnson, D.R. Copenhagen, J. Storm-Mathisen, F.A. Chaudhry, R.A. Nicoll, and R.H. Edwards Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites Science 304 2004 1815 1819
12. J. Gualix, J. Pintor, and M.T. Miras-Portugal Characterization of nucleotide transport into rat brain synaptic vesicles J. Neurochem. 73 1999 1098 1104
13. T.S. Hnasko, N. Chuhma, H. Zhang, G.Y. Goh, D. Sulzer, R.D. Palmiter, S. Rayport, and R.H. Edwards Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo Neuron 65 2010 643 656
14. M. Iharada, T. Miyaji, T. Fujimoto, M. Hiasa, N. Anzai, H. Omote, and Y. Moriyama Type 1 sodium-dependent phosphate transporter (SLC17A1 Protein) is a Cl(-)-dependent urate exporter J. Biol. Chem. 285 2010 26107 26113
15. N. Juge, Y. Yoshida, S. Yatsushiro, H. Omote, and Y. Moriyama Vesicular glutamate transporter contains two independent transport machineries J. Biol. Chem. 281 2006 39499 39506
16. N. Juge, J.A. Gray, H. Omote, T. Miyaji, T. Inoue, C. Hara, H. Uneyama, R.H. Edwards, R.A. Nicoll, and Y. Moriyama Metabolic control of vesicular glutamate transport and release Neuron 68 2010 99 112
17. P. Jutabha Human sodium phosphate transporter 4 (hNPT4/SLC17A3) as a common renal secretory pathway for drugs and urate J. Biol. Chem. 285 2010 35123 35132
18. M. Kolz Meta-analysis of 28,141 individuals identifies common variants within five new loci that influence uric acid concentrations PLoS Genet. 5 2009 e1000504
19. Larsson, M.; Sawada, K.; Morland, C.; Hiasa, M.; Ormel, L.; Moriyama, Y.; Gundersen, V.; 2012. Functional and anatomical identification of a vesicular transporter mediating neuronal ATP release. Cereb. Cortex.
20. Y.A. Luqmani Nucleotide uptake by isolated cholinergic synaptic vesicles: evidence for a carrier of adenosine 5′-triphosphate Neuroscience 6 1981 1011 1021
21. T. Miyaji, N. Echigo, M. Hiasa, S. Senoh, H. Omote, and Y. Moriyama Identification of a vesicular aspartate transporter Proc. Natl. Acad. Sci. USA 105 2008 11720 11724
22. K. Miyamoto, S. Haito-Sugino, S. Kuwahara, A. Ohi, K. Nomura, M. Ito, M. Kuwahata, S. Kido, S. Tatsumi, I. Kaneko, and H. Segawa Sodium-dependent phosphate cotransporters: lessons from gene knockout and mutation studies J. Pharm. Sci. 100 2011 3719 3730
23. P. Morin, C. Sagne, and B. Gasnier Functional characterization of wild-type and mutant human sialin Embo J. 23 2004 4560 4570
24. H. Murer, N. Hernando, I. Forster, and J. Biber Proximal tubular phosphate reabsorption: molecular mechanisms Physiol. Rev. 80 2000 1373 1409
25. B. Ni, P.R. Rosteck Jr.; N.S. Nadi, and S.M. Paul Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter Proc. Natl. Acad. Sci. USA 91 1994 5607 5611
26. E.D. Ozkan, F.S. Lee, and T. Ueda A protein factor that inhibits ATP-dependent glutamate and gamma-aminobutyric acid accumulation into synaptic vesicles: purification and initial characterization Proc. Natl. Acad. Sci. USA 94 1997 4137 4142
27. N. Pietrancosta, A. Kessler, F.C. Favre-Besse, N. Triballeau, T. Quentin, B. Giros, S. El Mestikawy, and F.C. Acher Rose Bengal analogs and vesicular glutamate transporters (VGLUTs) Bioorg. Med. Chem. 18 2010 6922 6933
28. L.M. Prolo, H. Vogel, and R.J. Reimer The lysosomal sialic acid transporter sialin is required for normal CNS myelination J. Neurosci. 29 2009 15355 15365
29. R.J. Reimer, and R.H. Edwards Organic anion transport is the primary function of the SLC17/type I phosphate transporter family Pflugers Arch. 447 2004 629 635
30. J. Ruel, S. Emery, R. Nouvian, T. Bersot, B. Amilhon, J.M. Van Rybroek, G. Rebillard, M. Lenoir, M. Eybalin, B. Delprat, T.A. Sivakumaran, B. Giros, S. El Mestikawy, T. Moser, R.J. Smith, M.M. Lesperance, and J.L. Puel Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice Am. J. Hum. Genet. 83 2008 278 292
31. M. Sardiello, M. Palmieri, A. di Ronza, D.L. Medina, M. Valenza, V.A. Gennarino, C. Di Malta, F. Donaudy, V. Embrione, R.S. Polishchuk, S. Banfi, G. Parenti, E. Cattaneo, and A. Ballabio A gene network regulating lysosomal biogenesis and function Science 325 2009 473 477
32. M.N. Sathe, K. Woo, C. Kresge, A. Bugde, K. Luby-Phelps, M.A. Lewis, and A.P. Feranchak Regulation of purinergic signaling in biliary epithelial cells by exocytosis of SLC17A9-dependent ATP-enriched vesicles J. Biol. Chem. 286 2011 25363 25376
33. K. Sawada, N. Echigo, N. Juge, T. Miyaji, M. Otsuka, H. Omote, A. Yamamoto, and Y. Moriyama Identification of a vesicular nucleotide transporter Proc. Natl. Acad. Sci. USA 105 2008 5683 5686
34. S. Schenck, S.M. Wojcik, N. Brose, and S. Takamori A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles Nat. Neurosci. 12 2009 156 162
35. R.P. Seal, X. Wang, Y. Guan, S.N. Raja, C.J. Woodbury, A.I. Basbaum, and R.H. Edwards Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors Nature 462 2009 651 655
36. R.P. Seal, O. Akil, E. Yi, C.M. Weber, L. Grant, J. Yoo, A. Clause, K. Kandler, J.L. Noebels, E. Glowatzki, L.R. Lustig, and R.H. Edwards Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3 Neuron 57 2008 263 275
37. J. Shi Common variants on chromosome 6p22.1 are associated with schizophrenia Nature 460 2009 753 757
38. Y. Shigeri, R.P. Seal, and K. Shimamoto Molecular pharmacology of glutamate transporters, EAATs and VGLUTs Brain Res. Brain Res. Rev. 45 2004 250 265
39. S. Sreedharan, J.H. Shaik, P.K. Olszewski, A.S. Levine, H.B. Schioth, and R. Fredriksson Glutamate, aspartate and nucleotide transporters in the SLC17 family form four main phylogenetic clusters: evolution and tissue expression BMC Genomics 11 2010 17
40. C.M. Thompson, E. Davis, C.N. Carrigan, H.D. Cox, R.J. Bridges, and J.M. Gerdes Inhibitor of the glutamate vesicular transporter (VGLUT) Curr. Med. Chem. 12 2005 2041 2056
41. A. Tokunaga, M. Tsukimoto, H. Harada, Y. Moriyama, and S. Kojima Involvement of SLC17A9-dependent vesicular exocytosis in the mechanism of ATP release during T cell activation J. Biol. Chem. 285 2010 17406 17416
42. S.M. Voglmaier, and R.H. Edwards Do different endocytic pathways make different synaptic vesicles? Curr. Opin. Neurobiol. 17 2007 374 380
43. A. Wallen-Mackenzie, H. Wootz, and H. Englund Genetic inactivation of the vesicular glutamate transporter 2 (VGLUT2) in the mouse: what have we learnt about functional glutamatergic neurotransmission? Ups. J. Med. Sci. 115 2010 11 20
44. C.C. Wreden, M. Wlizla, and R.J. Reimer Varied mechanisms underlie the free sialic acid storage disorders J. Biol. Chem. 280 2005 1408 1416
45. H. Yabuuchi, I. Tamai, K. Morita, T. Kouda, K. Miyamoto, E. Takeda, and A. Tsuji Hepatic sinusoidal membrane transport of anionic drugs mediated by anion transporter Npt1 J. Pharmacol. Exp. Ther. 286 1998 1391 1396
46. J. Yin, A. Hashimoto, M. Izawa, K. Miyazaki, G.Y. Chen, H. Takematsu, Y. Kozutsumi, A. Suzuki, K. Furuhata, F.L. Cheng, C.H. Lin, C. Sato, K. Kitajima, and R. Kannagi Hypoxic culture induces expression of sialin, a sialic acid transporter, and cancer-associated gangliosides containing non-human sialic acid on human cancer cells Cancer Res. 66 2006 2937 2945