The sodium-dependent ascorbic acid transporter family SLC23

Molecular Aspects of Medicine

Volumn 34, Issue 2-3, 2013, Pages 436-454

  Bürzle, Marc ^a   Suzuki, Yoshiro ^a   Ackermann, Daniel ^a,b   Miyazaki, Hiroki ^a   Maeda, Nobuyo ^c   Clémençon, Benjamin ^a   Burrier, Robert ^a,d   Hediger, Matthias A ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d Stemina Biomarker Discovery   (United States)

Author keywords

Ascorbic acid; Nucleobase; Oxidative stress; SLC23; SVCT1; SVCT2; SVCT3; Transporter

Indexed keywords

ASCORBIC ACID; CYCLIC AMP DEPENDENT PROTEIN KINASE; DICLOFENAC; HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; NUCLEOBASE TRANSPORTER; PROTEIN KINASE C; PROTEIN SLC23; PROTEIN SVCT1; PROTEIN SVCT2; PROTEIN SVCT3; PROTEIN UAPA; PROTEIN URAA; SAQUINAVIR; SNBT1 PROTEIN; SODIUM ASCORBIC ACID COTRANSPORTER; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ASCORBIC ACID BLOOD LEVEL; ASCORBIC ACID DEFICIENCY; ATHEROSCLEROSIS; BLOOD BRAIN BARRIER; CANCER PREVENTION; CANCER RISK; CARDIOVASCULAR DISEASE; CELL SURFACE; DRUG DELIVERY SYSTEM; DRUG PROTEIN BINDING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIABILITY; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; KNOCKOUT MOUSE; LYMPHOMA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREMATURE LABOR; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SODIUM TRANSPORT; STOMACH CANCER; STRUCTURE ACTIVITY RELATION; TISSUE DISTRIBUTION; VITAMIN BLOOD LEVEL; VITAMIN C TRANSPORT; VITAMIN METABOLISM;

AMINO ACID SEQUENCE; ANIMALS; ASCORBIC ACID; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIGENE FAMILY; PHYLOGENY; PROTEIN CONFORMATION; RATS; SEQUENCE ALIGNMENT; SODIUM-COUPLED VITAMIN C TRANSPORTERS; SPECIES SPECIFICITY;

EID: 84875167844     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2012.12.002     Document Type: Review

References (119)

1. N. Ahmed, M. Kansara, and M.V. Berridge Acute regulation of glucose transport in a monocyte-macrophage cell line: GLUT-3 affinity for glucose is enhanced during the respiratory burst Biochem. J. 327 2 1997 369 375
2. A. Amano, T. Aigaki, N. Maruyama, and A. Ishigami Ascorbic acid depletion enhances expression of the sodium-dependent vitamin C transporters, SVCT1 and SVCT2, and uptake of ascorbic acid in livers of SMP30/GNL knockout mice Arch. Biochem. Biophys. 496 1 2010 38 44
3. C. Angulo, M.A. Castro, C.I. Rivas, D. Segretain, R. Maldonado, A.J. Yañez, J.C. Slebe, J.C. Vera, and I.I. Concha Molecular identification and functional characterization of the vitamin C transporters expressed by Sertoli cells J. Cell. Physiol. 217 3 2008 708 716
4. A. Astuya, T. Caprile, M. Castro, K. Salazar, M.d.l.A. García, K. Reinicke, F. Rodríguez, J.C. Vera, C. Millán, V. Ulloa, M. Low, F. Martínez, and F. Nualart Vitamin C uptake and recycling among normal and tumor cells from the central nervous system J. Neurosci. Res. 79 1-2 2005 146 156
5. V.R. Babaev, L. Li, S. Shah, S. Fazio, M.F. Linton, and J.M. May Combined vitamin C and vitamin E deficiency worsens early atherosclerosis in apolipoprotein E-deficient mice Arterioscler. Thromb. Vasc. Biol. 30 9 2010 1751 1757
6. V.R. Babaev, R.R. Whitesell, L. Li, M.F. Linton, S. Fazio, and J.M. May Selective macrophage ascorbate deficiency suppresses early atherosclerosis Free Radic. Biol. Med. 50 1 2011 27 36
7. U.V. Berger, and M.A. Hediger The vitamin C transporter SVCT2 is expressed by astrocytes in culture but not in situ Neuroreport 11 7 2000 1395 1399
8. U.V. Berger, X.-C.M. Lu, W. Liu, Z. Tang, B.S. Slusher, and M.A. Hediger Effect of middle cerebral artery occlusion on mRNA expression for the sodium-coupled vitamin C transporter SVCT2 in rat brain J. Neurochem. 86 4 2003 896 906
9. C. Biondi, B. Pavan, A. Dalpiaz, S. Medici, L. Lunghi, and F. Vesce Expression and characterization of vitamin C transporter in the human trophoblast cell line HTR-8/SVneo: effect of steroids, flavonoids and NSAIDs Mol. Hum. Reprod. 13 1 2007 77 83
10. G. Bjelakovic, D. Nikolova, R.G. Simonetti, and C. Gluud Antioxidant supplements for prevention of gastrointestinal cancers: a systematic review and meta-analysis Lancet 364 9441 2004 1219 1228
11. G. Block Vitamin C and cancer prevention: the epidemiologic evidence Am. J. Clin. Nutr. 53 1 1991 270S 282S
12. M. Castro, T. Caprile, A. Astuya, C. Millán, K. Reinicke, J.C. Vera, O. Vásquez, L.G. Aguayo, and F. Nualart High-affinity sodium-vitamin C co-transporters (SVCT) expression in embryonic mouse neurons J. Neurochem. 78 4 2001 815 823
13. M. Chatterjee, R. Saluja, V. Kumar, A. Jyoti, G. Kumar Jain, M. Kumar Barthwal, and M. Dikshit Ascorbate sustains neutrophil NOS expression, catalysis, and oxidative burst Free Radic. Biol. Med. 45 8 2008 1084 1093
14. A.A. Chen, C.J. Marsit, B.C. Christensen, E.A. Houseman, M.D. McClean, J.F. Smith, J.T. Bryan, M.R. Posner, H.H. Nelson, and K.T. Kelsey Genetic variation in the vitamin C transporter, SLC23A2, modifies the risk of HPV16-associated head and neck cancer Carcinogenesis 30 6 2009 977 981
15. J.P. Christiane Brahimi-Horn The role of the hypoxia-inducible factor in tumor metabolism growth and invasion Bull. Cancer 93 8 2006 E73 80
16. A.G. Clark, A.L. Rohrbaugh, I. Otterness, and V.B. Kraus The effects of ascorbic acid on cartilage metabolism in guinea pig articular cartilage explants Matrix Biol. 21 2 2002 175 184
17. C.P. Corpe, J.-H. Lee, O. Kwon, P. Eck, J. Narayanan, K.L. Kirk, and M. Levine 6-Bromo-6-deoxy-l-ascorbic acid J. Biol. Chem. 280 7 2005 5211 5220
18. C.P. Corpe, H. Tu, P. Eck, J. Wang, R. Faulhaber-Walter, J. Schnermann, S. Margolis, S. Padayatty, H. Sun, Y. Wang, R.L. Nussbaum, M.G. Espey, and M. Levine Vitamin C transporter Slc23a1 links renal reabsorption, vitamin C tissue accumulation, and perinatal survival in mice J. Clin. Invest. 120 4 2010 1069 1083
19. A. Dalpiaz, B. Pavan, M. Scaglianti, F. Vitali, F. Bortolotti, C. Biondi, A. Scatturin, S. Tanganelli, L. Ferraro, P. Prasad, and S. Manfredini Transporter-mediated effects of diclofenamic acid and its ascorbyl pro-drug in the in vivo neurotropic activity of ascorbyl nipecotic acid conjugate J. Pharm. Sci. 93 1 2004 78 85
20. A. Dalpiaz, B. Pavan, S. Vertuani, F. Vitali, M. Scaglianti, F. Bortolotti, C. Biondi, A. Scatturin, S. Tanganelli, L. Ferraro, G. Marzola, P. Prasad, and S. Manfredini Ascorbic and 6-Br-ascorbic acid conjugates as a tool to increase the therapeutic effects of potentially central active drugs Eur. J. Pharm. Sci. 24 4 2005 259 269
21. R. Daruwala, J. Song, W.S. Koh, S.C. Rumsey, and M. Levine Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2 FEBS Lett. 460 3 1999 480 484
22. H. de Koning, and G. Diallinas Nucleobase transporters (Review) Mol. Membr. Biol. 17 2 2000 75 94
23. K. Dhariwal, W. Hartzell, and M. Levine Ascorbic acid and dehydroascorbic acid measurements in human plasma and serum Am. J. Clin. Nutr. 54 4 1991 712 716
24. G. Diallinas, and C. Scazzocchio A gene coding for the uric acid-xanthine permease of Aspergillus nidulans: inactivational cloning, characterization, and sequence of a cis-acting mutation Genetics 122 2 1989 341 350
25. G. Diallinas, J. Valdez, V. Sophianopoulou, A. Rosa, and C. Scazzocchio Chimeric purine transporters of Aspergillus nidulans define a domain critical for function and specificity conserved in bacterial, plant and metazoan homologues EMBO J. 17 14 1998 3827 3837
26. S. Englard, and S. Seifter The biochemical functions of ascorbic acid Annu. Rev. Nutr. 6 1 1986 365 406
27. H.C. Erichsen, S.A.M. Engel, P.K. Eck, R. Welch, M. Yeager, M. Levine, A.M. Siega-Riz, A.F. Olshan, and S.J. Chanock Genetic variation in the sodium-dependent vitamin C transporters, SLC23A1, and SLC23A2 and risk for preterm delivery Am. J. Epidemiol. 163 3 2006 245 254
28. C.A. Faaland, J.E. Race, G. Ricken, F.J. Warner, W.J. Williams, and E.J. Holtzman Molecular characterization of two novel transporters from human and mouse kidney and from LLC-PK1 cells reveals a novel conserved family that is homologous to bacterial and Aspergillus nucleobase transporters Biochim. Biophys. Acta Gene Struct. Expr. 1442 2-3 1998 353 360
29. P.A. Friedman, and M.L. Zeidel Victory at C Nat. Med. 5 6 1999 620 621
30. P. Gao, H. Zhang, R. Dinavahi, F. Li, Y. Xiang, V. Raman, Z.M. Bhujwalla, D.W. Felsher, L. Cheng, J. Pevsner, L.A. Lee, G.L. Semenza, and C.V. Dang HIF-dependent antitumorigenic effect of antioxidants in vivo Cancer Cell 12 3 2007 230 238
31. J.M. Gaziano, R.J. Glynn, and W.G. Christen Vitamins E and C in the prevention of prostate and total cancer in men: the physicians' health study ii randomized controlled trial JAMA 301 1 2009 52 62
32. B. Gess, C. Lohmann, H. Halfter, and P. Young Sodium-dependent vitamin C transporter 2 (SVCT2) is necessary for the uptake of l-ascorbic acid into Schwann cells Glia 58 3 2010 287 299
33. B. Gess, D. Röhr, R. Fledrich, M.W. Sereda, I. Kleffner, A. Humberg, J. Nowitzki, J.-K. Strecker, H. Halfter, and P. Young Sodium-dependent vitamin C transporter 2 deficiency causes hypomyelination and extracellular matrix defects in the peripheral nervous system J. Neurosci. 31 47 2011 17180 17192
34. B. Gess, S. Sevimli, J.-K. Strecker, P. Young, and W.-R. Schäbitz Sodium-dependent vitamin C transporter 2 (SVCT2) expression and activity in brain capillary endothelial cells after transient ischemia in mice PLoS ONE 6 2 2011 e17139
35. A. Godoy, V. Ormazabal, G. Moraga-Cid, F.A. Zúñiga, P. Sotomayor, V. Barra, O. Vasquez, V. Montecinos, L. Mardones, C. Guzmán, M. Villagrán, L.G. Aguayo, S.A. Oñate, A.M. Reyes, J.G. Cárcamo, C.I. Rivas, and J.C. Vera Mechanistic insights and functional determinants of the transport cycle of the ascorbic acid transporter SVCT2 J. Biol. Chem. 282 1 2007 615 624
36. C.A. Gonzalez, and E. Riboli Diet and cancer prevention: contributions from the European prospective investigation into cancer and nutrition (EPIC) study Eur. J. Cancer 46 14 2010 2555 2562
37. L. Gorfinkiel, G. Diallinas, and C. Scazzocchio Sequence and regulation of the UapA gene encoding a uric acid-xanthine permease in the fungus Aspergillus nidulans J. Biol. Chem. 268 31 1993 23376 23381
38. S. Goudela, P. Karatza, M. Koukaki, S. Frillingos, and G. Diallinas Comparative substrate recognition by bacterial and fungal purine transporters of the NAT/NCS2 family Mol. Membr. Biol. 22 3 2005 263 275
39. C. Gournas, I. Papageorgiou, and G. Diallinas The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role Mol. BioSyst. 4 5 2008 404 416
40. D.A. Griffith, and S.M. Jarvis High affinity sodium-dependent nucleobase transport in cultured renal epithelial cells (LLC-PK1) J. Biol. Chem. 268 27 1993 20085 20090
41. D.A. Griffith, and S.M. Jarvis Characterization of a sodium-dependent concentrative nucleobase-transport system in guinea-pig kidney cortex brush-border membrane vesicles Biochem. J. 303 Pt 3 1994 901 905
42. M.J. Guimaraes, J.F. Bazan, A. Zlotnik, M.V. Wiles, J.C. Grimaldi, F. Lee, and T. McClanahan A new approach to the study of haematopoietic development in the yolk sac and embryoid bodies Development 121 10 1995 3335 3346
43. F.E. Harrison, S.M. Dawes, M.E. Meredith, V.R. Babaev, L. Li, and J.M. May Low vitamin C and increased oxidative stress and cell death in mice that lack the sodium-dependent vitamin C transporter SVCT2 Free Radical Biol. Med. 49 5 2010 821 829
44. K. Kaneko, S. Fujimori, H. Itoh, Y. Nakayama, H. Oyama, T. Kanbayashi, H. Miyashita, and I. Akaoka Renal handling of hypoxanthine and xanthine in normal subjects and in four cases of idiopathic renal hypouricemia J. Rheumatol. 1988 325 330
45. J.S. Kang, H.N. Kim, D.J. Jung, J.E. Kim, G.H. Mun, Y.S. Kim, D. Cho, D.H. Shin, Y.-I. Hwang, and W.J. Lee Regulation of UVB-induced IL-8 and MCP-1 production in skin keratinocytes by increasing vitamin C uptake via the redistribution of SVCT-1 from the cytosol to the membrane J. Invest. Dermatol. 127 3 2006 698 706
46. R. Kannan, A. Stolz, Q. Ji, P.D. Prasad, and V. Ganapathy Vitamin C transport in human lens epithelial cells: evidence for the presence of SVCT2 Exp. Eye Res. 73 2 2001 159 165
47. H.J. Knowles, R.R. Raval, A.L. Harris, and P.J. Ratcliffe Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells Cancer Res. 63 8 2003 1764 1768
48. J. Korcok, S.J. Dixon, T.C.Y. Lo, and J.X. Wilson Differential effects of glucose on dehydroascorbic acid transport and intracellular ascorbate accumulation in astrocytes and skeletal myocytes Brain Res. 993 1-2 2003 201 207
49. V. Kosti, G. Lambrinidis, V. Myrianthopoulos, G. Diallinas, and E. Mikros Identification of the substrate recognition and transport pathway in a eukaryotic member of the nucleobase-ascorbate transporter (NAT) family PLoS ONE 7 7 2012 e41939
50. M. Koukaki, A. Vlanti, S. Goudela, A. Pantazopoulou, H. Gioule, S. Tournaviti, and G. Diallinas The nucleobase-ascorbate transporter (NAT) signature motif in UapA defines the function of the purine translocation pathway J. Mol. Biol. 350 3 2005 499 513
51. M. Kraupp, and R. Marz Membrane transport of nucleobases: interaction with inhibitors Gen. Pharmacol. Vasc. Syst. 26 6 1995 1185 1190
52. S.-M. Kuo, M.E. MacLean, K. McCormick, and J.X. Wilson Gender and sodium-ascorbate transporter isoforms determine ascorbate concentrations in mice J. Nutr. 134 9 2004 2216 2221
53. J. Lee, C. Oh, G. Mun, J. Kim, Y. Chung, Y. Hwang, D. Shin, and W. Lee Immunohistochemical localization of sodium-dependent l-ascorbic acid transporter 1 protein in rat kidney Histochem. Cell Biol. 126 4 2006 491 494
54. W.J. Liang, D. Johnson, and S.M. Jarvis Vitamin C transport systems of mammalian cells Mol. Membr. Biol. 18 1 2001 87 95
55. W.-J. Liang, D. Johnson, L.-S. Ma, and S.M. Jarvis Regulation of the human vitamin C transporters expressed in COS-1 cells by protein kinase C Am. J. Physiol. Cell Physiol. 283 6 2002 C1696 C1704
56. J. Lin, N.R. Cook, C. Albert, E. Zaharris, J.M. Gaziano, M. Van Denburgh, J.E. Buring, and J.E. Manson Vitamins C and E and beta carotene supplementation and cancer risk: a randomized controlled trial J. Natl. Cancer Inst. 101 1 2009 14 23
57. M. Low, D. Sandoval, E. Avilés, F. Pérez, F. Nualart, and J. Henríquez The ascorbic acid transporter SVCT2 is expressed in slow-twitch skeletal muscle fibres Histochem. Cell Biol. 131 5 2009 565 574
58. M. Low, D. Sandoval, B. Morales, F. Nualart, and J.P. Henríquez Up-regulation of the vitamin C transporter SVCT2 upon differentiation and depolarization of myotubes FEBS Lett. 585 2 2011 390 396
59. F. Lu, S. Li, Y. Jiang, J. Jiang, H. Fan, G. Lu, D. Deng, S. Dang, X. Zhang, J. Wang, and N. Yan Structure and mechanism of the uracil transporter UraA Nature 472 7342 2011 243 246
60. S. Luo, Z. Wang, V. Kansara, D. Pal, and A.K. Mitra Activity of a sodium-dependent vitamin C transporter (SVCT) in MDCK-MDR1 cells and mechanism of ascorbate uptake Int. J. Pharm. 358 1-2 2008 168 176
61. S. Luo, Z. Wang, M. Patel, V. Khurana, X. Zhu, D. Pal, and A.K. Mitra Targeting SVCT for enhanced drug absorption: Synthesis and in vitro evaluation of a novel vitamin C conjugated prodrug of saquinavir Int. J. Pharm. 414 1-2 2011 77 85
62. E.A. Lutsenko, J.M. Carcamo, and D.W. Golde A human sodium-dependent vitamin C transporter 2 isoform acts as a dominant-negative inhibitor of ascorbic acid transport Mol. Cell. Biol. 24 8 2004 3150 3156
63. B. Mackenzie, A.C. Illing, and M.A. Hediger Transport model of the human Na+-coupled l-ascorbic acid (vitamin C) transporter SVCT1 Am. J. Physiol. Cell Physiol. 294 2 2008 C451 C459
64. E.R. Margaret Ascorbate regulation and its neuroprotective role in the brain Trends Neurosci. 23 5 2000 209 216
65. J.M. May, J. Huang, and Z.-c. Qu Macrophage uptake and recycling of ascorbic acid: response to activation by lipopolysaccharide Free Radic. Biol. Med. 39 11 2005 1449 1459
66. J.M. May, L. Li, Z.-c. Qu, and J. Huang Ascorbate uptake and antioxidant function in peritoneal macrophages Arch. Biochem. Biophys. 440 2 2005 165 172
67. J.M. May, L. Li, and Z.-c. Qu Oxidized LDL up-regulates the ascorbic acid transporter SVCT2 in endothelial cells Mol. Cell. Biochem. 343 1 2010 217 222
68. C. Meintanis, A.D. Karagouni, and G. Diallinas Amino acid residues N450 and Q449 are critical for the uptake capacity and specificity of UapA, a prototype of a nucleobase-ascorbate transporter family Mol. Membr. Biol. 17 1 2000 47 57
69. M.E. Meredith, F.E. Harrison, and J.M. May Differential regulation of the ascorbic acid transporter SVCT2 during development and in response to ascorbic acid depletion Biochem. Biophys. Res. Commun. 414 4 2011 737 742
70. A. Montel-Hagen, S. Kinet, N. Manel, C. Mongellaz, R. Prohaska, J.L. Battini, J. Delaunay, M. Sitbon, and N. Taylor Erythrocyte GLUT1 triggers dehydroascorbic acid uptake in mammals unable to synthesize vitamin C Cell 132 6 2008 1039 1048
71. T. Nagase, N. Seki, K. Ishikawa, M. Ohira, Y. Kawarabayasi, O. Ohara, A. Tanaka, H. Kotani, N. Miyajima, and N. Nomura Prediction of the coding sequences of unidentified human genes. VI. The coding sequences of 80 new genes (KIAA0201-KIAA0280) deduced by analysis of cDNA clones from cell line KG-1 and brain DNA Res. 3 5 1996 321 329
72. H. Nakayama, S. Akiyama, M. Inagaki, Y. Gotoh, and K. Oguchi Dehydroascorbic acid and oxidative stress in haemodialysis patients Nephrol. Dial. Transplant. 16 3 2001 574 579
73. M. Nishikimi, R. Fukuyama, S. Minoshima, N. Shimizu, and K. Yagi Cloning and chromosomal mapping of the human nonfunctional gene for l-gulono-gamma- lactone oxidase, the enzyme for l-ascorbic acid biosynthesis missing in man J. Biol. Chem. 269 18 1994 13685 13688
74. + cooperativity, conformational stability, and subcellular localization J. Biol. Chem. 285 47 2010 36471 36485
75. A. Pantazopoulou, and G. Diallinas The first transmembrane segment (TMS1) of UapA contains determinants necessary for expression in the plasma membrane and purine transport Mol. Membr. Biol. 23 4 2006 337 348
76. P. Patak, H.S. Willenberg, and S.R. Bornstein Vitamin C is an important cofactor for both adrenal cortex and adrenal medulla Endocr. Res. 30 4 2004 871 875
77. R.E. Patterson, E. White, A.R. Kristal, M.L. Neuhouser, and J.D. Potter Vitamin supplements and cancer risk: the epidemiologic evidence Cancer Causes Control 8 5 1997 786 802
78. J.M. Peake Vitamin C: effects of exercise and requirements with training Int. J. Sport. Nutr. Exerc. Metab. 13 2 2003 125 151
79. G. Powis, and L. Kirkpatrick Hypoxia inducible factor-1{alpha} as a cancer drug target Mol Cancer Ther. 3 5 2004 647 654
80. H. Qiao, and J.M. May Macrophage differentiation increases expression of the ascorbate transporter (SVCT2) Free Radic. Biol. Med. 46 8 2009 1221 1232
81. H. Qiao, J. Bell, S. Juliao, L. Li, and J.M. May Ascorbic acid uptake and regulation of type I collagen synthesis in cultured vascular smooth muscle cells J. Vasc. Res. 46 1 2009 15 24
82. D.P. Rajan, W. Huang, B. Dutta, L.D. Devoe, F.H. Leibach, V. Ganapathy, and P.D. Prasad Human placental sodium-dependent vitamin C transporter (SVCT2): molecular cloning and transport function Biochem. Biophys. Res. Commun. 262 3 1999 762 768
83. J.C. Reidling, V.S. Subramanian, T. Dahhan, M. Sadat, and H.M. Said Mechanisms and regulation of vitamin C uptake: studies of the hSVCT systems in human liver epithelial cells Am. J. Physiol. Gastrointest. Liver Physiol. 295 6 2008 G1217 G1227
84. R.C. Rose, and A.M. Bode Ocular ascorbate transport and metabolism Comp. Biochem. Physiol. A: Comp. Physiol. 100 2 1991 273 285
85. S.A. Rubin, S. Dey, and J.C. Reidling Functional analysis of two regulatory regions of the human Na+-dependent vitamin C transporter 2, SLC23A2, in human vascular smooth muscle cells Biochim. Biophys. Acta Gene Struct. Expr. 1732 1-3 2005 76 81
86. S.C. Rumsey, O. Kwon, G.W. Xu, C.F. Burant, I. Simpson, and M. Levine Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid J. Biol. Chem. 272 30 1997 18982 18989
87. S.C. Rumsey, R. Daruwala, H. Al-Hasani, M.J. Zarnowski, I.A. Simpson, and M. Levine Dehydroascorbic acid transport by GLUT4 in Xenopus oocytes and isolated rat adipocytes J. Biol. Chem. 275 36 2000 28246 28253
88. S. Salmaso, J.S. Pappalardo, R.R. Sawant, T. Musacchio, K. Rockwell, P. Caliceti, and V.P. Torchilin Targeting glioma cells in vitro with ascorbate-conjugated pharmaceutical nanocarriers Bioconjug. Chem. 20 12 2009 2348 2355
89. I. Savini, M. Valeria Catani, G. Duranti, R. Ceci, S. Sabatini, and L. Avigliano Vitamin C homeostasis in skeletal muscle cells Free Radic. Biol. Med. 38 7 2005 898 907
90. I. Savini, M.V. Catani, R. Arnone, A. Rossi, G. Frega, D. Del Principe, and L. Avigliano Translational control of the ascorbic acid transporter SVCT2 in human platelets Free Radic. Biol. Med. 42 5 2007 608 616
91. I. Savini, A. Rossi, M.V. Catani, R. Ceci, and L. Avigliano Redox regulation of vitamin C transporter SVCT2 in C2C12 myotubes Biochem. Biophys. Res. Commun. 361 2 2007 385 390
92. A. Schmitt, R. Salvayre, J. Delchambre, and A. Nègre-Salvayre Prevention by alpha-tocopherol and rutin of glutathione and ATP depletion induced by oxidized LDL in cultured endothelial cells Br. J. Pharmacol. 116 3 1995 1985 1990
93. G.L. Semenza Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1 Annu Rev Cell Dev Biol. 15 1 1999 551 578
94. C.K. Sen Antioxidants in exercise nutrition Sports Med. 31 13 2001 891 908
95. T. Seno, N. Inoue, K. Matsui, J. Ejiri, K. Hirata, S. Kawashima, and M. Yokoyama Functional expression of sodium-dependent vitamin C transporter 2 in human endothelial cells J. Vasc. Res. 41 4 2004 345 351
96. C.F. Skibola, P.M. Bracci, E. Halperin, A. Nieters, A. Hubbard, R.A. Paynter, D.R. Skibola, L. Agana, N. Becker, P. Tressler, M.S. Forrest, S. Sankararaman, L. Conde, E.A. Holly, and M.T. Smith Polymorphisms in the estrogen receptor 1 and vitamin C and matrix metalloproteinase gene families are associated with susceptibility to lymphoma PLoS ONE 3 7 2008 e2816
97. S. Sotiriou, S. Gispert, J. Cheng, Y. Wang, A. Chen, S. Hoogstraten-Miller, G.F. Miller, O. Kwon, M. Levine, S.H. Guttentag, and R.L. Nussbaum Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival Nat. Med. 8 5 2002 514 517
98. H. Steiling, K. Longet, A. Moodycliffe, R. Mansourian, E. Bertschy, H. Smola, C. Mauch, and G. Williamson Sodium-dependent vitamin C transporter isoforms in skin: distribution, kinetics, and effect of UVB-induced oxidative stress Free Radic. Biol. Med. 43 5 2007 752 762
99. U.P. Steinbrecher Role of superoxide in endothelial-cell modification of low-density lipoproteins Biochim. Biophys. Acta Lipids Lipid Metab. 959 1 1988 20 30
100. U.P. Steinbrecher, S. Parthasarathy, D.S. Leake, J.L. Witztum, and D. Steinberg Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids Proc. Natl. Acad. Sci. U.S.A. 81 12 1984 3883 3887
101. V.S. Subramanian, J.S. Marchant, M.J. Boulware, and H.M. Said A C-terminal region dictates the apical plasma membrane targeting of the human sodium-dependent vitamin C transporter-1 in polarized epithelia J. Biol. Chem. 279 26 2004 27719 27728
102. +-dependent vitamin C transporter functionality Biochem. Biophys. Res. Commun. 374 1 2008 123 127
103. V.S. Subramanian, J.S. Marchant, and H.M. Said Molecular determinants dictating cell surface expression of the human sodium-dependent vitamin C transporter-2 in human liver cells Am. J. Physiol. Gastrointest. Liver Physiol. 298 2 2010 G267 G274
104. N.J. Timpson, N.G. Forouhi, M.-J. Brion, R.M. Harbord, D.G. Cook, P. Johnson, A. McConnachie, R.W. Morris, S. Rodriguez, J.a. Luan, S. Ebrahim, S. Padmanabhan, G. Watt, K.R. Bruckdorfer, N.J. Wareham, P.H. Whincup, S. Chanock, N. Sattar, D.A. Lawlor, and G. Davey Smith Genetic variation at the SLC23A1 locus is associated with circulating concentrations of l-ascorbic acid (vitamin C): evidence from 5 independent studies with >15,000 participants Am. J. Clin. Nutr. 92 2 2010 375 382
105. H. Tsukaguchi, T. Tokui, B. Mackenzie, U.V. Berger, X.-Z. Chen, Y. Wang, R.F. Brubaker, and M.A. Hediger A family of mammalian Na+-dependent l-ascorbic acid transporters Nature 399 6731 1999 70 75
106. S. Varma, C.E. Campbell, and S.-M. Kuo Functional role of conserved transmembrane segment 1 residues in human sodium-dependent vitamin C transporters† Biochemistry 47 9 2008 2952 2960
107. S. Varma, K. Sobey, C.E. Campbell, and S.-M. Kuo Hierarchal contribution of N- and C-terminal sequences to the differential localization of homologous sodium-dependent vitamin C transporters, SVCT1 and SVCT2, in epithelial cells† Biochemistry 48 13 2009 2969 2980
108. A.M. Velho, and S.M. Jarvis Topological studies of hSVCT1, the human sodium-dependent vitamin C transporter and the influence of N-glycosylation on its intracellular targeting Exp. Cell Res. 315 13 2009 2312 2321
109. M.C.M. Vissers, and R.P. Wilkie Ascorbate deficiency results in impaired neutrophil apoptosis and clearance and is associated with up-regulation of hypoxia-inducible factor 1α J. Leukoc. Biol. 81 5 2007 1236 1244
110. H. Wang, B. Dutta, W. Huang, L.D. Devoe, F.H. Leibach, V. Ganapathy, and P.D. Prasad Human Na+-dependent vitamin C transporter 1 (hSVCT1): primary structure, functional characteristics and evidence for a non-functional splice variant Biochim. Biophys. Acta Biomembr. 1461 1 1999 1 9
111. Y. Wang, B. Mackenzie, H. Tsukaguchi, S. Weremowicz, C.C. Morton, and M.A. Hediger Human vitamin C (l-ascorbic acid) transporter SVCT1 Biochem. Biophys. Res. Commun. 267 2 2000 488 494
112. W.W. Wells, and D.P. Xu Dehydroascorbate reduction J. Bioenerg. Biomembr. 26 4 1994 369 377
113. J.X. Wilson Regulation of vitamin C transport Annu. Rev. Nutr. 25 1 2005 105 125
114. M.E. Wright, G. Andreotti, J. Lissowska, M. Yeager, W. Zatonski, S.J. Chanock, W.-H. Chow, and L. Hou Genetic variation in sodium-dependent ascorbic acid transporters and risk of gastric cancer in Poland Eur. J. Cancer 45 10 2009 1824 1830
115. X. Wu, N. Itoh, T. Taniguchi, J. Hirano, T. Nakanishi, and K. Tanaka Stimulation of differentiation in sodium-dependent vitamin C transporter 2 overexpressing MC3T3-E1 osteoblasts Biochem. Biophys. Res. Commun. 317 4 2004 1159 1164
116. X. Wu, L.H. Zeng, T. Taniguchi, and Q.M. Xie Activation of PKA and phosphorylation of sodium-dependent vitamin C transporter 2 by prostaglandin E2 promote osteoblast-like differentiation in MC3T3-E1 cells Cell Death Differ. 14 10 2007 1792 1801
117. X. Wu, T. Iguchi, N. Itoh, K. Okamoto, T. Takagi, K. Tanaka, and T. Nakanishi Ascorbic acid transported by sodium-dependent vitamin C transporter 2 stimulates steroidogenesis in human choriocarcinoma cells Endocrinology 149 1 2008 73 83
118. T. Yamamoto, Y. Moriwaki, S. Takahashi, T. Hada, and K. Higashino Renal excretion of purine bases. Effects of probenecid, benzbromarone and pyrazinamide Nephron 48 2 1988 116 120
119. S. Yamamoto, K. Inoue, T. Murata, S. Kamigaso, T. Yasujima, J. Maeda, Y. Yoshida, K. Ohta, and H. Yuasa Identification and functional characterization of the first nucleobase transporter in mammals J. Biol. Chem. 285 9 2010 6522 6531