1932

Abstract

Vesicular neurotransmitter transporters are responsible for the accumulation of neurotransmitters in secretory vesicles and play essential roles in chemical transmission. The SLC17 family contributes to sequestration of anionic neurotransmitters such as glutamate, aspartate, and nucleotides. Identification and subsequent cellular and molecular biological studies of SLC17 transporters unveiled the principles underlying the actions of these transporters. Recent progress in reconstitution methods in combination with postgenomic approaches has advanced studies on neurotransmitter transporters. This review summarizes the molecular properties of SLC17-type transporters and recent findings regarding the novel SLC18 transporter.

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2016-01-06
2024-04-20
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Literature Cited

  1. Chaudhry FA, Boulland JL, Jenstad M, Bredahl MK, Edwards RH. 1.  2008. Pharmacology of neurotransmitter transport into secretory vesicles. Handb. Exp. Pharmacol. 184:77–106 [Google Scholar]
  2. Omote H, Miyaji T, Juge N, Moriyama Y. 2.  2011. Vesicular neurotransmitter transporter: bioenergetics and regulation of glutamate transport. Biochemistry 50:255558–65 [Google Scholar]
  3. Omote H, Moriyama Y. 3.  2013. Vesicular neurotransmitter transporters: an approach for studying transporters with purified proteins. Physiology 28:139–50 [Google Scholar]
  4. Reimer RJ. 4.  2013. SLC17: a functionally diverse family of organic anion transporters. Mol. Asp. Med. 34:2–3350–59 [Google Scholar]
  5. Eiden LE, Schäfer MKH, Weihe E, Schütz B. 5.  2004. The vesicular amine transporter family (SLC18): amine/proton antiporters required for vesicular accumulation and regulated exocytotic secretion of monoamines and acetylcholine. Pflüg. Arch. 447:5636–40 [Google Scholar]
  6. Hiasa M, Miyaji T, Haruna Y, Takeuchi T, Harada Y. 6.  et al. 2014. Identification of a mammalian vesicular polyamine transporter. Sci. Rep. 4:6836 [Google Scholar]
  7. Gasnier B. 7.  2003. The SLC32 transporter, a key protein for the synaptic release of inhibitory amino acids. Pflüg. Arch. 447:5756–59 [Google Scholar]
  8. Juge N, Omote H, Moriyama Y. 8.  2013. Vesicular GABA transporter (VGAT) transports β-alanine. J. Neurochem. 127:4482–86 [Google Scholar]
  9. El Mestikawy S, Wallén-Mackenzie A, Fortin GM, Descarries L, Trudeau LE. 9.  2011. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci. 12:4204–16 [Google Scholar]
  10. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P. 10.  et al. 2004. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:4983–1002 [Google Scholar]
  11. Miyazaki T, Fukaya M, Shimizu H, Watanabe M. 11.  2003. Subtype switching of vesicular glutamate transporters at parallel fibre–Purkinje cell synapses in developing mouse cerebellum. Eur. J. Neurosci. 17:122563–72 [Google Scholar]
  12. Hayashi M, Yamada H, Uehara S, Morimoto R, Muroyama A. 12.  et al. 2003. Secretory granule-mediated co-secretion of l-glutamate and glucagon triggers glutamatergic signal transmission in islet of Langerhans. J. Biol. Chem. 278:31966–74 [Google Scholar]
  13. Moriyama Y, Yamamoto A. 13.  2004. Glutamatergic chemical transmission: Look! Here, there, and anywhere. J. Biochem. 135:2155–63 [Google Scholar]
  14. Morimoto R, Uehara S, Yatsushiro S, Juge N, Hua Z. 14.  et al. 2006. Secretion of l-glutamate from osteoclasts through transcytosis. EMBO J. 25:184175–86 [Google Scholar]
  15. Fremeau RT, Kam K, Qureshi T, Johnson J, Copenhagen DR. 15.  et al. 2004. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:56781815–19 [Google Scholar]
  16. Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I. 16.  et al. 2006. Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J. Neurosci. 26:4612055–66 [Google Scholar]
  17. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R. 17.  et al. 2004. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. PNAS 101:187158–63 [Google Scholar]
  18. Naito S, Ueda T. 18.  1985. Characterization of glutamate uptake into synaptic vesicles. J. Neurochem. 44:199–109 [Google Scholar]
  19. Tabb JS, Kish PE, Van Dyke R, Ueda T. 19.  1992. Glutamate transport into synaptic vesicles: roles of membrane potential, pH gradient, and intravesicular pH. J. Biol. Chem. 267:2215412–18 [Google Scholar]
  20. Moriyama Y, Yamamoto A. 20.  1995. Vesicular l-glutamate transporter in microvesicles from bovine pineal glands. J. Biol. Chem. 270:3822314–20 [Google Scholar]
  21. Takamori S, Rhee JS, Rosenmund C, Jahn R. 21.  2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:6801189–94 [Google Scholar]
  22. Bellocchio EE, Reimer RJ, Fremeau RT Jr., Edwards RH. 22.  2000. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:5481957–60 [Google Scholar]
  23. El Mestikawy S, Wallén-Mackenzie A, Fortin GM, Descarries L, Trudeau LE. 23.  2011. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci. 12:4204–16 [Google Scholar]
  24. Juge N, Yoshida Y, Yatsushiro S, Omote H, Moriyama Y. 24.  2006. Vesicular glutamate transporter contains two independent transport machineries. J. Biol. Chem. 281:5139499–506 [Google Scholar]
  25. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D. 25.  et al. 2010. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:5643–56 [Google Scholar]
  26. Hnasko TS, Edwards RH. 26.  2012. Neurotransmitter corelease: mechanism and physiological role. Annu. Rev. Physiol. 74:225–43 [Google Scholar]
  27. Juge N, Gray JA, Omote H, Miyaji T, Inoue T. 27.  et al. 2010. Metabolic control of vesicular glutamate transport and release. Neuron 68:199–112 [Google Scholar]
  28. Burger PM, Mehl E, Cameron PL, Maycox PR, Baumert M. 28.  et al. 1989. Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate. Neuron 3:6715–20 [Google Scholar]
  29. Johnson RG, Scarpa A. 29.  1979. Protonmotive force and catecholamine transport in isolated chromaffin granules. J. Biol. Chem. 254:103750–60 [Google Scholar]
  30. Russell JT. 30.  1984. ΔpH, H+ diffusion potentials, and Mg2+ ATPase in neurosecretory vesicles isolated from bovine neurohypophyses. J. Biol. Chem. 259:159496–507 [Google Scholar]
  31. Werner A, Moore ML, Mantei N, Biber J, Semenza G, Murer H. 31.  1991. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex. PNAS 88:219608–12 [Google Scholar]
  32. Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK. 32.  2008. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177:4889–98 [Google Scholar]
  33. Pavón LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C. 33.  2008. Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J. Biol. Chem 283:2013520–27 [Google Scholar]
  34. Pavón LR, Karlsson PM, Carlsson J, Samyn D, Persson B. 34.  et al. 2010. Functionally important amino acids in the Arabidopsis thylakoid phosphate transporter: homology modeling and site-directed mutagenesis. Biochemistry 49:306430–39 [Google Scholar]
  35. Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K. 35.  et al. 2015. AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat. Commun. 6:5925 [Google Scholar]
  36. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S. 36.  2003. Structure and mechanism of the lactose permease of Escherichia coli. Science 301:5633610–15 [Google Scholar]
  37. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN. 37.  2003. Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:5633616–20 [Google Scholar]
  38. Miyaji T, Echigo N, Hiasa M, Senoh S, Omote H, Moriyama Y. 38.  2008. Identification of a vesicular aspartate transporter. PNAS 105:3311720–24 [Google Scholar]
  39. Almqvist J, Huang Y, Laaksonen A, Wang DN, Hovmöller S. 39.  2007. Docking and homology modeling explain inhibition of the human vesicular glutamate transporters. Protein Sci. 16:91819–29 [Google Scholar]
  40. Hartinger J, Jahn R. 40.  1993. An anion binding site that regulates the glutamate transporter of synaptic vesicles. J. Biol. Chem. 268:3123122–27 [Google Scholar]
  41. Wolosker H, de Souza DO, de Meis L. 41.  1996. Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J. Biol. Chem. 271:2011726–31 [Google Scholar]
  42. Schenck S, Wojcik SM, Brose N, Takamori S. 42.  2009. A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles. Nat. Neurosci. 12:2156–62 [Google Scholar]
  43. Busch AE, Schuster A, Waldegger S, Wagner CA, Zempel G. 43.  et al. 1996. Expression of a renal type I sodium/phosphate transporter (NaPi-1) induces a conductance in Xenopus oocytes permeable for organic and inorganic anions. PNAS 93:115347–51 [Google Scholar]
  44. Bröer S, Schuster A, Wagner CA, Bröer A, Forster I. 44.  et al. 1998. Chloride conductance and Pi transport are separate functions induced by the expression of NaPi-1 in Xenopus oocytes. J. Membr. Biol. 164:171–77 [Google Scholar]
  45. Preobraschenski J, Zander JF, Suzuki T, Ahnert-Hilger G, Jahn R. 45.  2014. Vesicular glutamate transporters use flexible anion and cation binding sites for efficient accumulation of neurotransmitter. Neuron 84:61287–301 [Google Scholar]
  46. Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J. 46.  et al. 2007. Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J. Neurosci. 27:328616–27 [Google Scholar]
  47. Vining EP. 47.  1999. Clinical efficacy of the ketogenic diet. Epilepsy Res. 37:3181–90 [Google Scholar]
  48. Tavares RG, Santos CE, Tasca CI, Wajner M, Souza DO. 48.  et al. 2000. Inhibition of glutamate uptake into synaptic vesicles of rat brain by the metabolites accumulating in maple syrup urine disease. J. Neurol. Sci. 181:1–244–49 [Google Scholar]
  49. Thompson CM, Davis E, Carrigan CN, Cox HD, Bridges RJ. 49.  et al. 2005. Inhibitor of the glutamate vesicular transporter (VGLUT). Curr. Med. Chem. 12:182041–56 [Google Scholar]
  50. Roseth S, Fykse EM, Fonnum F. 50.  1998. Uptake of l-glutamate into synaptic vesicles: competitive inhibition by dyes with biphenyl and amino- and sulphonic acid-substituted naphthyl groups. Biochem. Pharmacol. 56:91243–49 [Google Scholar]
  51. Tamura Y, Ogita K, Ueda T. 51.  2014. A new VGLUT-specific potent inhibitor: pharmacophore of Brilliant Yellow. Neurochem. Res. 39:1117–28 [Google Scholar]
  52. Ogita K, Hirata K, Bole DG, Yoshida S, Tamura Y. 52.  et al. 2001. Inhibition of vesicular glutamate storage and exocytotic release by Rose Bengal. J. Neurochem. 77:134–42 [Google Scholar]
  53. Bartlett RD, Esslinger CS, Thompson CM, Bridges RJ. 53.  1998. Substituted quinolines as inhibitors of l-glutamate transport into synaptic vesicles. Neuropharmacology 37:7839–46 [Google Scholar]
  54. Ganong AH, Lanthorn TH, Cotman CW. 54.  1983. Kynurenic acid inhibits synaptic and acidic amino acid–induced responses in the rat hippocampus and spinal cord. Brain Res. 273:1170–74 [Google Scholar]
  55. Verheijen FW, Verbeek E, Aula N, Beerens CE, Havelaar AC. 55.  et al. 1999. A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat. Genet. 23:4462–65 [Google Scholar]
  56. Morin P, Sagne C, Gasnier B. 56.  2004. Functional characterization of wild-type and mutant human sialin. EMBO J. 23:234560–70 [Google Scholar]
  57. Wreden CC, Wlizla M, Reimer RJ. 57.  2005. Varied mechanisms underlie the free sialic acid storage disorders. J. Biol. Chem. 280:21408–16 [Google Scholar]
  58. Haataja L, Parkkola R, Sonninen P, Vanhanen SL, Schleutker J. 58.  et al. 1994. Phenotypic variation and magnetic resonance imaging (MRI) in Salla disease, a free sialic acid storage disorder. Neuropediatrics 25:5238–44 [Google Scholar]
  59. Alajoki L, Varho T, Posti K, Aula P, Korhonen T. 59.  2004. Neurocognitive profiles in Salla disease. Dev. Med. Child. Neurol. 46:12832–37 [Google Scholar]
  60. Aula P, Gahl WA. 60.  2001. Disorders of free sialic acid storage. The Metabolic and Molecular Bases of Inherited Disease CR Scriver, AL Beaudet, WS Sly, D Valle 5109–20 New York: McGraw-Hill [Google Scholar]
  61. Nadler JV, Vaca KW, White WF, Lynch GS, Cotman CW. 61.  1976. Aspartate and glutamate as possible transmitters of excitatory hippocampal afferents. Nature 260:5551538–40 [Google Scholar]
  62. Yatsushiro S, Yamada H, Kozaki S, Kumon H, Michibata H. 62.  et al. 1997. l-aspartate but not the d form is secreted through microvesicle-mediated exocytosis and is sequestered through Na+-dependent transporter in rat pinealocytes. J. Neurochem. 69:1340–47 [Google Scholar]
  63. Gundersen V, Chaudhry FA, Bjaalie JG, Fonnum F, Ottersen OP, Storm-Mathisen J. 63.  1998. Synaptic vesicular localization and exocytosis of l-aspartate in excitatory nerve terminals. J. Neurosci. 18:166059–70 [Google Scholar]
  64. Dingledine R, Borges K, Bowie D, Traynelis SF. 64.  1999. The glutamate receptor ion channels. Pharmacol. Rev. 51:17–61 [Google Scholar]
  65. Bliss TVP, Collingridge GL. 65.  1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:640731–39 [Google Scholar]
  66. Aula N, Kopra O, Jalanko A, Peltonen L. 66.  2004. Sialin expression in the CNS implicates extralysosomal function in neurons. Neurobiol. Dis. 15:2251–61 [Google Scholar]
  67. Miyaji T, Omote H, Moriyama Y. 67.  2011. Functional characterization of vesicular excitatory amino acid transport by human sialin. J. Neurochem. 119:11–5 [Google Scholar]
  68. Lodder-Gadaczek J, Gieselmann V, Eckhardt M. 68.  2013. Vesicular uptake of N-acetylaspartylglutamate is catalysed by sialin (SLC17A5). Biochem. J. 454:131–38 [Google Scholar]
  69. Prolo LM, Vogel H, Reimer RJ. 69.  2009. The lysosomal sialic acid transporter sialin is required for normal CNS myelination. J. Neurosci. 29:4915355–65 [Google Scholar]
  70. Morland C, Nordengen K, Larsson M, Prolo LM, Farzampour Z. 70.  et al. 2013. Vesicular uptake and exocytosis of l-aspartate is independent of sialin. FASEB J 27:31264–74 [Google Scholar]
  71. Burnstock G. 71.  2007. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 87:2659–797 [Google Scholar]
  72. Winkler H, Carmichael SW. 72.  1982. The chromaffin granule. The Secretory Granule AM Poisner, JM Trifaró 3–79 Amsterdam: Elsevier Biomedical [Google Scholar]
  73. Johnson RG. 73.  1988. Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol. Rev. 68:1232–307 [Google Scholar]
  74. Hutton JC, Penn EJ, Peshavaria M. 74.  1983. Low-molecular-weight constituents of isolated insulin-secretory granules: bivalent cations, adenine nucleotides and inorganic phosphate. Biochem. J. 210:2297–305 [Google Scholar]
  75. Kostron H, Winkler H, Peer LJ, König P. 75.  1977. Uptake of adenosine triphosphate by isolated adrenal chromaffin granules: a carrier-mediated transport. Neuroscience 2:1159–66 [Google Scholar]
  76. Weber A, Winkler H. 76.  1981. Specificity and mechanism of nucleotide uptake by adrenal chromaffin granules. Neuroscience 6:112269–76 [Google Scholar]
  77. Weber A, Westhead EW, Winkler H. 77.  1983. Specificity and properties of the nucleotide carrier in chromaffin granules from bovine adrenal medulla. Biochem. J. 210:3789–94 [Google Scholar]
  78. Rudnick G. 78.  2008. Vesicular ATP transport is a hard (V)NUT to crack. PNAS 105:165949–50 [Google Scholar]
  79. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M. 79.  et al. 2008. Identification of a vesicular nucleotide transporter. PNAS 105:155683–86 [Google Scholar]
  80. Miyaji T, Sawada K, Omote H, Moriyama Y. 80.  2011. Divalent cation transport by vesicular nucleotide transporter. J. Biol. Chem. 286:5042881–87 [Google Scholar]
  81. Hiasa M, Togawa N, Miyaji T, Omote H, Yamamoto A, Moriyama Y. 81.  2014. Essential role of vesicular nucleotide transporter in vesicular storage and release of nucleotides in platelets. Physiol. Rep. 2:6e12034 [Google Scholar]
  82. Kato Y, Omote H, Miyaji T. 82.  2013. Inhibitors of ATP release inhibit vesicular nucleotide transporter. Biol. Pharm. Bull. 36:111688–91 [Google Scholar]
  83. Larsson M, Sawada K, Morland C, Hiasa M, Ormel L. 83.  et al. 2012. Functional and anatomical identification of a vesicular transporter mediating neuronal ATP release. Cereb. Cortex 22:51203–14 [Google Scholar]
  84. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E. 84.  et al. 2003. Storage and release of ATP from astrocytes in culture. J. Biol. Chem. 278:21354–62 [Google Scholar]
  85. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E. 85.  et al. 2007. Exocytotic release of ATP from cultured astrocytes. J. Biol. Chem. 282:3928749–58 [Google Scholar]
  86. Zhang Z, Chen G, Zhou W, Song A, Xu T. 86.  et al. 2007. Regulated ATP release from astrocytes through lysosome exocytosis. Nat. Cell Biol. 9:8945–53 [Google Scholar]
  87. Iwatsuki K, Ichikawa R, Hiasa M, Moriyama Y, Torii K. 87.  et al. 2009. Identification of the vesicular nucleotide transporter (VNUT) in taste cells. Biochem. Biophys. Res. Commun. 388:11–5 [Google Scholar]
  88. Mihara H, Boudaka A, Sugiyama T, Moriyama Y, Tominaga M. 88.  2011. Transient receptor potential vanilloid 4 (TRPV4)-dependent calcium influx and ATP release in mouse oesophageal keratinocytes. J. Physiol. 589:3471–82 [Google Scholar]
  89. Wolf-Johnston AS, Hanna-Mitchell AT, Buffington CA, Shinde S, Roppolo JR. 89.  et al. 2012. Alterations in the non-neuronal acetylcholine synthesis and release machinery in esophageal epithelium. Life Sci. 91:21–221065–69 [Google Scholar]
  90. Vessey KA, Fletcher EL. 90.  2012. Rod and cone pathway signalling is altered in the P2X7 receptor knock out mouse. PLOS ONE 7:e29990 [Google Scholar]
  91. Haanes KA, Novak I. 91.  2010. ATP storage and uptake by isolated pancreatic zymogen granules. Biochem. J. 429:2303–11 [Google Scholar]
  92. Geisler JC, Corbin KL, Li Q, Feranchak AP, Nunemaker CS, Li C. 92.  2013. Vesicular nucleotide transporter-mediated ATP release regulates insulin secretion. Endocrinology 154:2675–84 [Google Scholar]
  93. Tokunaga A, Tsukimoto M, Harada H, Moriyama Y, Kojima S. 93.  2010. Involvement of SLC17A9-dependent vesicular exocytosis in the mechanism of ATP release during T cell activation. J. Biol. Chem. 285:2317406–16 [Google Scholar]
  94. Sakaki H, Tsukimoto M, Harada H, Moriyama Y, Kojima S. 94.  2013. Autocrine regulation of macrophage activation via exocytosis of ATP and activation of P2Y11 receptor. PLOS ONE 8:e59778 [Google Scholar]
  95. Sesma JI, Kreda SM, Okada SF, van Heusden C, Moussa L. 95.  et al. 2013. Vesicular nucleotide transporter regulates the nucleotide content in airway epithelial mucin granules. Am. J. Physiol. Cell Physiol. 304:10C976–84 [Google Scholar]
  96. Sathe MN, Woo K, Kresge C, Bugde A, Luby-Phelps K. 96.  et al. 2011. Regulation of purinergic signaling in biliary epithelial cells by exocytosis of SLC17A9-dependent ATP-enriched vesicles. J. Biol. Chem. 286:2825363–76 [Google Scholar]
  97. Shinozaki Y, Nomura M, Iwatsuki K, Moriyama Y, Gachet C, Koizumi S. 97.  2014. Microglia trigger astrocyte-mediated neuroprotection via purinergic gliotransmission. Sci. Rep. 4:4329 [Google Scholar]
  98. Sakamoto S, Miyaji T, Hiasa M, Ichikawa R, Uematsu A. 98.  et al. 2014. Impairment of vesicular ATP release affects glucose metabolism and increases insulin sensitivity. Sci. Rep. 4:6689 [Google Scholar]
  99. Uchino H, Tamai I, Yamashita K, Minemoto Y, Sai Y. 99.  et al. 2000. p-Aminohippuric acid transport at renal apical membrane mediated by human inorganic phosphate transporter NPT1. Biochem. Biophys. Res. Commun. 270:1254–59 [Google Scholar]
  100. Iharada M, Miyaji T, Fujimoto T, Hiasa M, Anzai N. 100.  et al. 2010. Type 1 sodium-dependent phosphate transporter (SLC17A1 protein) is a Cl-dependent urate exporter. J. Biol. Chem. 285:3426107–13 [Google Scholar]
  101. Stark K, Reinhard W, Grassl M, Erdmann J, Schunkert H. 101.  et al. 2009. Common polymorphisms influencing serum uric acid levels contribute to susceptibility to gout, but not to coronary artery disease. PLOS ONE 4:11e7729 [Google Scholar]
  102. Togawa N, Miyaji T, Izawa S, Omote H, Moriyama Y. 102.  2012. Na+/phosphate co-transporter homologue (SLC17A4 protein) is an intestinal organic anion exporter. Am. J. Physiol. Cell Physiol. 302:11C1652–60 [Google Scholar]
  103. Ogden KK, Traynelis SF. 103.  2011. New advances in NMDA receptor pharmacology. Trends Pharmacol. Sci. 32:726–33 [Google Scholar]
  104. Jacobsson JA, Stephansson O, Fredriksson R. 104.  2010. C6ORF192 forms a unique evolutionary branch among solute carriers (SLC16, SLC17, and SLC18) and is abundantly expressed in several brain regions. J. Mol. Neurosci. 41:2230–42 [Google Scholar]
  105. Juge N, Moriyama S, Miyaji T, Kawakami M, Iwai H. 105.  et al. 2015. Plasmodium falciparum chloroquine resistance transporter is a H+-coupled polyspecific nutrient and drug exporter. PNAS 112:113356–61 [Google Scholar]
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