Low vitamin C and increased oxidative stress and cell death in mice that lack the sodium-dependent vitamin C transporter SVCT2

Free Radical Biology and Medicine

Volumn 49, Issue 5, 2010, Pages 821-829

  Harrison, F E ^a   Dawes, S M ^b   Meredith, M E ^b   Babaev, V R ^a   Li, L ^b   May, J M ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ascorbic acid; Brain; Development; Free radicals; Oxidative stress; SVCT2

Indexed keywords

ACETAL; ASCORBIC ACID; BIOLOGICAL MARKER; CARRIER PROTEIN; CARRIER PROTEIN SVCT2; F 4 ISOPROSTANE DERIVATIVE; ISOKETAL; ISOPROSTANE DERIVATIVE; MALONALDEHYDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BRAIN CORTEX; BRAIN HEMORRHAGE; BRAIN STEM; CELL DEATH; CELL LOSS; CONTROLLED STUDY; FEMALE; FETUS; GENOTYPE; HISTOPATHOLOGY; LIVER; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PLACENTA; PRIORITY JOURNAL; PROGENY; TISSUE LEVEL;

MUS;

EID: 77955092602     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.06.008     Document Type: Article

References (42)

1. Lind J. A Treatise on the Scurvy in Three Parts: Containing an inquiry into the nature, causes, and cures of that disease: Together with a critical and chronological view of what has been published on the subject 1980, Classics of Medicine Library, Birmingham, AL.
2. Hughes R.E., Hurley R.J., Jones P.R. The retention of ascorbic acid by guinea-pig tissues. Br. J. Nutr. 1971, 26:433-438.
3. Harrison F.E., May J.M. Vitamin C function in the brain: Vital role of the ascorbate transporter SVCT2. Free Radic. Biol. Med. 2009, 46:719-730.
4. +-dependent L-ascorbic acid transporters. Nature 1999, 399:70-75.
5. Savini I., Rossi A., Pierro C., Avigliano L., Catani M.V. SVCT1 and SVCT2: Key proteins for vitamin C uptake. Amino Acids 2007, 34:347-355.
6. Sotiriou S., Gispert S., Cheng J., Wang Y., Chen A., Hoogstraten-Miller S., Miller G.F., Kwon O., Levine M., Guttentag S.H., Nussbaum R.L. Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat. Med. 2002, 8:514-517.
7. Bornstein S.R., Yoshida-Hiroi M., Sotiriou S., Levine M., Hartwig H.G., Nussbaum R.L., Eisenhofer G. Impaired adrenal catecholamine system function in mice with deficiency of the ascorbic acid transporter (SVCT2). FASEB J. 2003, 17:1928-1930.
8. Eldridge C.F., Bunge M.B., Bunge R.P., Wood P.M. Differentiation of axon-related Schwann cells in vitro. I. Ascorbic acid regulates basal lamina assembly and myelin formation. J. Cell Biol. 1987, 105:1023-1034.
9. Cammack J., Ghasemzadeh B., Adams R.N. The pharmacological profile of glutamate-evoked ascorbic acid efflux measured by in vivo electrochemistry. Brain Res. 1991, 565:17-22.
10. Miele M., Boutelle M.G., Fillenz M. The physiologically induced release of ascorbate in rat brain is dependent on impulse traffic, calcium influx and glutamate uptake. Neuroscience 1994, 62:87-91.
11. Grunewald R.A. Ascorbic acid in the brain. Brain Res. Brain Res. Rev. 1993, 18:123-133.
12. Rebec G.V., Pierce R.C. A vitamin as neuromodulator: Ascorbate release into the extracellular fluid of the brain regulates dopaminergic and glutamatergic transmission. Prog. Neurobiol. 1994, 43:537-565.
13. Harrison F.E., Yu S.S., Van Den Bossche K.L., Li L., May J.M., McDonald M.P. Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J. Neurochem. 2008, 106:1198-1208.
14. Maeda N., Hagihara H., Nakata Y., Hiller S., Wilder J., Reddick R. Aortic wall damage in mice unable to synthesize ascorbic acid. Proc. Natl Acad. Sci. USA 2000, 97:841-846.
15. Pachla L.A., Kissinger P.T. Analysis of ascorbic acid by liquid chromatography with amperometric detection. Methods Enzymol. 1979, 62:15-24.
16. May J.M., Qu Z.C., Mendiratta S. Protection and recycling of α-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch. Biochem. Biophys. 1998, 349:281-289.
17. Harrison F.E., May J.M., McDonald M.P. Vitamin C deficiency increases basal exploratory activity but decreases scopolamine-induced activity in APP/PSEN1 transgenic mice. Pharmacol. Biochem. Behav. 2010, 94:543-552.
18. Roberts L.J., Montine T.J., Markesbery W.R., Tapper A.R., Hardy P., Chemtob S., Dettbarn W.D., Morrow J.D. Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J. Biol. Chem. 1998, 273:13605-13612.
19. Davies S.S., Amarnath V., Roberts L.J. Isoketals: Highly reactive gamma-ketoaldehydes formed from the H2-isoprostane pathway. Chem. Phys. Lipids 2004, 128:85-99.
20. Rajan D.P., Huang W., Dutta B., Devoe L.D., Leibach F.H., Ganapathy V., Prasad P.D. Human placental sodium-dependent vitamin C transporter (SVCT2): Molecular cloning and transport function. Biochem. Biophys. Res. Commun. 1999, 262:762-768.
21. Biondi C., Pavan B., Dalpiaz A., Medici S., Lunghi L., Vesce F. 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. 2007, 13:77-83.
22. Corpe C.P., Tu H., Eck P., Wang J., Faulhaber-Walter R., Schnermann J., Margolis S., Padayatty S., Sun H., Wang Y., Nussbaum R.L., Espey M.G., Levine M. Vitamin C transporter Slc23a1 links renal reabsorption, vitamin C tissue accumulation, and perinatal survival in mice. J. Clin. Invest. 2010, 120:1069-1083.
23. Klesges L.M., Murray D.M., Brown J.E., Cliver S.P., Goldenberg R.L. Relations of cigarette smoking and dietary antioxidants with placental calcification. Am. J. Epidemiol. 1998, 147:127-135.
24. Choi J.L., Rose R.C. Transport and metabolism of ascorbic acid in human placenta. Am. J. Physiol. 1989, 257:C110-113.
25. Rybakowski C., Mohar B., Wohlers S., Leichtweiss H.P., Schroder H. The transport of vitamin C in the isolated human near-term placenta. Eur. J. Obstet. Gynecol. Reprod. Biol. 1995, 62:107-114.
26. Fischer H., Schwarzer C., Illek B. Vitamin C controls the cystic fibrosis transmembrane conductance regulator chloride channel. Proc. Natl Acad. Sci. USA 2004, 101:3691-3696.
27. Kratzing C.C., Kelly J.D. Ascorbic acid synthesis by the mammalian fetus. Int. J. Vitam. Nutr. Res. 1986, 56:101-103.
28. Kuo S.M., MacLean M.E., McCormick K., Wilson J.X. Gender and sodium-ascorbate transporter isoforms determine ascorbate concentrations in mice. J. Nutr. 2004, 134:2216-2221.
29. Kratzing C.C., Kelly J.D., Kratzing J.E. Ascorbic acid in fetal rat brain. J. Neurochem. 1985, 44:1623-1624.
30. 1H MRS. Magn. Reson. Med. 2006, 55:979-983.
31. Roberts L.J., Fessel J.P. The biochemistry of the isoprostane, neuroprostane, and isofuran pathways of lipid peroxidation. Chem. Phys. Lipids 2004, 128:173-186.
32. Harrison F.E., Hosseini A.H., Dawes S.M., Weaver S., May J.M. Ascorbic acid attenuates scopolamine-induced spatial learning deficits in the water maze. Behav. Brain Res. 2009, 205:550-558.
33. Gould D.B., Phalan F.C., Breedveld G.J., van Mil S.E., Smith R.S., Schimenti J.C., Aguglia U., van der Knaap M.S., Heutink P., John S.W. Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science 2005, 308:1167-1171.
34. Garcia Mde L., Salazar K., Millan C., Rodriguez F., Montecinos H., Caprile T., Silva C., Cortes C., Reinicke K., Vera J.C., Aguayo L.G., Olate J., Molina B., Nualart F. Sodium vitamin C cotransporter SVCT2 is expressed in hypothalamic glial cells. Glia 2005, 50:32-47.
35. Qiao H., May J.M. Development of ascorbate transporters in brain cortical capillary endothelial cells in culture. Brain Res. 2008, 1208:79-86.
36. Qiao H., Li L., Qu Z.C., May J.M. Cobalt-induced oxidant stress in cultured endothelial cells: Prevention by ascorbate in relation to HIF-1alpha. Biofactors 2009, 35:306-313.
37. Steiling H., Longet K., Moodycliffe A., Mansourian R., Bertschy E., Smola H., Mauch C., Williamson G. Sodium-dependent vitamin C transporter isoforms in skin: Distribution, kinetics, and effect of UVB-induced oxidative stress. Free Radic. Biol. Med. 2007, 43:752-762.
38. Hill K.E., Montine T.J., Motley A.K., Li X., May J.M., Burk R.F. Combined deficiency of vitamins E and C causes paralysis and death in guinea pigs. Am. J. Clin. Nutr. 2003, 77:1484-1488.
39. Burk R.F., Christensen J.M., Maguire M.J., Austin L.M., Whetsell W.O., May J.M., Hill K.E., Ebner F.F. A combined deficiency of vitamins E and C causes severe central nervous system damage in guinea pigs. J. Nutr. 2006, 136:1576-1581.
40. Johnston C.S., Thompson L.L. Vitamin C status of an outpatient population. J. Am. Coll. Nutr. 1998, 17:366-370.
41. Levine M., Wang Y., Padayatty S.J., Morrow J. A new recommended dietary allowance of vitamin C for healthy young women. Proc. Natl Acad. Sci. USA 2001, 98:9842-9846.
42. Salmenpera L. Vitamin C nutrition during prolonged lactation: Optimal in infants while marginal in some mothers. Am. J. Clin. Nutr. 1984, 40:1050-1056.