Chronic vitamin C deficiency promotes redox imbalance in the brain but does not alter sodium-dependent vitamin C transporter 2 expression

Nutrients

Volumn 6, Issue 5, 2014, Pages 1809-1822

  Paidi, Maya D ^a   Schjoldager, Janne G ^a   Lykkesfeldt, Jens ^a   Tveden Nyborg, Pernille ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Oxidative stress; Redox imbalance; SVCT2; Vitamin C deficiency

Indexed keywords

DEHYDROASCORBIC ACID; GLUTATHIONE; MALONALDEHYDE; SODIUM ASCORBIC ACID COTRANSPORTER; ASCORBIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASCORBIC ACID DEFICIENCY; CHEMICAL ANALYSIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GUINEA PIG; LIPID OXIDATION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BLOOD; BRAIN; CHRONIC DISEASE; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY;

ANIMALS; ASCORBIC ACID; ASCORBIC ACID DEFICIENCY; BRAIN; CHRONIC DISEASE; FEMALE; GENE EXPRESSION REGULATION; GUINEA PIGS; LIPID METABOLISM; MALONDIALDEHYDE; OXIDATION-REDUCTION; OXIDATIVE STRESS; SODIUM-COUPLED VITAMIN C TRANSPORTERS;

EID: 84899715211     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6051809     Document Type: Article

References (50)

1. Bayir, H.; Kagan, V. E.; Tyurina, Y. Y.; Tyurin, V.; Ruppel, R. A.; Adelson, P. D.; Graham, S. H.; Janesko, K.; Clark, R. S. B.; Kochanek, P. M. Assessment of antioxidant reserves and oxidative stress in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatr. Res. 2002, 51, 571-578.
2. Miura, S.; Ishida-Nakajima, W.; Ishida, A.; Kawamura, M.; Ohmura, A.; Oguma, R.; Sato, Y.; Takahashi, T. Ascorbic acid protects the newborn rat brain from hypoxic-ischemia. Brain Dev. 2009, 31, 307-317.
3. Rice, M. E. Ascorbate regulation and its neuroprotective role in the brain. Trends Neurosci. 2000, 23, 209-216.
4. Rebec, G. V.; Pierce, R. A vitamin as neuromodulator: Ascorbate release into the extracellular fluid of the brain regulates dopaminergic and glutamatergic transmission. Prog. Neurobiol. 1994, 43, 537-565.
5. Hughes, R.; Hurley, R.; Jones, P. The retention of ascorbic acid by guinea-pig tissues. Br. J. Nutr. 1971, 26, 433-438.
6. Rice, M.; Russo-Menna, I. Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neuroscience 1997, 82, 1213-1223.
7. Hilscherova, K.; Blankenship, A.; Nie, M.; Coady, K.; Upham, B.; Trosko, J.; Giesy, J. Oxidative stress in liver and brain of the hatchling chicken (Gallus domesticus) following in ovo injection with TCDD. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 2003, 136, 29-45.
8. Rice, M.; Forman, R.; Chen, B.; Avshalumov, M.; Cragg, S.; Drew, K. Brain antioxidant regulation in mammals and anoxia-tolerant reptiles: Balanced for neuroprotection and neuromodulation. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 2002, 133, 515-525.
9. Sánchez-Moreno, C.; Paniagua, M.; Madrid, A.; Martín, A. Protective effect of vitamin C against the ethanol mediated toxic effects on human brain glial cells. J. Nutr. Biochem. 2003, 14, 606-613.
10. Hart, J.-M.; Chang, B.-J.; Li, T.-Z.; Choe, N.-H.; Quan, F.-S.; Jang, B.-J.; Cho, I.-H.; Hong, H.-N.; Lee, J.-H. Protective effects of ascorbic acid against lead-induced apoptotic neurodegeneration in the developing rat hippocampus in vivo. Brain Res. 2007, 1185, 68-74.
11. Markesbery, W.; Lovell, M. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 1998, 19, 33-36.
12. Butterfield, D. A.; Reed, T.; Perluigi, M.; de Marco, C.; Coccia, R.; Cini, C.; Sultana, R. Elevated protein-bound levels of the lipid peroxidation product, 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci. Lett. 2006, 397, 170-173.
13. Dhariwal, K.; Hartzell, W.; Levine, M. Ascorbic acid and dehydroascorbic acid measurements in human plasma and serum. Am. J. Clin. Nutr. 1991, 54, 712-716.
14. Lindblad, M.; Tveden-Nyborg, P.; Lykkesfeldt, J. Regulation of Vitamin C Homeostasis during Deficiency. Nutrients 2013, 5, 2860-2879.
15. Harrison, F.; May, J. Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic. Biol. Med. 2009, 46, 719-730.
16. Tsukaguchi, H.; Tokui, T.; Mackenzie, B.; Berger, U. V.; Chen, X. Z.; Wang, Y.; Brubaker, R. F.; Hediger, M. A. A family of mammalian Na-dependent L-ascorbic acid transporters. Nature 1999, 399, 70-75.
17. Sotiriou, S.; Gispert, S.; Cheng, J.; Wang, Y.; Chen, A.; Hoogstraten-Miller, S.; Miller, G.; Kwon, O.; Levine, M.; Guttentag, S. Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat. Med. 2002, 8, 514-517.
18. Harrison, F.; Dawes, S.; Meredith, M.; Babaev, V.; Li, L.; May, J. Low vitamin C increased oxidative stress cell death in mice that lack the sodium-dependent vitamin C transporter SVCT2. Free Radic. Biol. Med. 2010, 49, 821-829.
19. Tveden-Nyborg, P.; Hasselholt, S.; Miyashita, N.; Moos, T.; Poulsen, H. E.; Lykkesfeldt, J. Chronic Vitamin C Deficiency does not Accelerate Oxidative Stress in Ageing Brains of Guinea Pigs. Basic Clin. Pharmacol. Toxicol. 2012, 110, 524-529.
20. Harrison, F.; Green, R.; Dawes, S.; May, J. Vitamin C distribution and retention in the mouse brain. Brain Res. 2010, 1348, 181-186.
21. Mardones, L.; Zúñiga, F. A.; Villagrán, M.; Sotomayor, K.; Mendoza, P.; Escobar, D.; González, M.; Ormazabal, V.; Maldonado, M.; Oñate, G. Essential role of intracellular glutathione in controlling ascorbic acid transporter expression and function in rat hepatocytes and hepatoma cells. Free Radic. Biol. Med. 2012, 52, 1874-1887.
22. Meredith, M. E.; Harrison, F.; May, J. Differential regulation of the ascorbic acid transporter SVCT2 during development and in response to ascorbic acid depletion. Biochem. Biophys. Res. Commun. 2011, 414, 737-742.
23. Amano, A.; Aigaki, T.; Maruyama, N.; Ishigami, A. 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. 2010, 496, 38-44.
24. Nishikimi, M.; Kawai, T.; Yagi, K. Guinea pigs possess a highly mutated gene for L-gulono-gamma-lactone oxidase, the key enzyme for L-ascorbic acid biosynthesis missing in this species. J. Biol. Chem. 1992, 267, 21967-21972.
25. Lykkesfeldt, J.; Perez Trueba, G.; Poulsen, H.; Christen, S. Vitamin C deficiency in weanling guinea pigs: Differential expression of oxidative stress and DNA repair in liver and brain. Br. J. Nutr. 2007, 98, 1116-1119.
26. Tveden-Nyborg, P.; Johansen, L. K.; Raida, Z.; Villumsen, C. K.; Larsen, J. O.; Lykkesfeldt, J. Vitamin C deficiency in early postnatal life impairs spatial memory and reduces the number of hippocampal neurons in guinea pigs. Am. J. Clin. Nutr. 2009, 90, 540-546.
27. Tveden-Nyborg, P.; Vogt, L.; Schjoldager, J. G.; Jeannet, N.; Hasselholt, S.; Paidi, M. D.; Christen, S.; Lykkesfeldt, J. Maternal Vitamin C Deficiency during Pregnancy Persistently Impairs Hippocampal Neurogenesis in Offspring of Guinea Pigs. PLoS One 2012, 7, e48488.
28. Lykkesfeldt, J. Determination of Ascorbic Acid and Dehydroascorbic Acid in Biological Samples by High-Performance Liquid Chromatography Using Subtraction Methods: Reliable Reduction with Tris[2-carboxyethyl] phosphine Hydrochloride. Anals Biochem. 2000, 282, 89-93.
29. Lykkesfeldt, J. Determination of malondialdehyde as dithiobarbituric acid adduct in biological samples by HPLC with fluorescence detection: Comparison with ultraviolet-visible spectrophotometry. Clin. Chem. 2001, 47, 1725-1727.
30. Hissin, P. J.; Hilf, R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. An. Biochem. 1976, 74, 214-226.
31. Clark, A. G.; Rohrbaugh, A. L.; Otterness, I.; Kraus, V. B. The effects of ascorbic acid on cartilage metabolism in guinea pig articular cartilage explants. Matrix Biol. 2002, 21, 175-184.
32. May, J. M.; Qu, Z.; Qiao, H.; Koury, M. J. Maturational loss of the vitamin C transporter in erythrocytes. Biochem. Biophys. Res. Commun. 2007, 360, 295-298.
33. Savini, I.; Rossi, A.; Catani, M. V.; Ceci, R.; Avigliano, L. Redox regulation of vitamin C transporter SVCT2 in C2C12 myotubes. Biochem. Biophys. Res. Commun. 2007, 361, 385-390.
34. Schjoldager, J. G.; Tveden-Nyborg, P.; Lykkesfeldt, J. Prolonged maternal vitamin C deficiency overrides preferential fetal ascorbate transport but does not influence perinatal survival in guinea pigs. Br. J. Nutr. 2013, 110, 1573-1579.
35. -/- mice during development. Brain Res. 2010, 1349, 143-152.
36. Johnston, C. S.; Meyer, C.; Srilakshmi, J. Vitamin C elevates red blood cell glutathione in healthy adults. Am. J. Clin. Nutr. 1993, 58, 103-105.
37. Lykkesfeldt, J. Increased oxidative damage in vitamin C deficiency is accompanied by induction of ascorbic acid recycling capacity in young but not mature guinea pigs. Free Radic. Res. 2002, 36, 567-574.
38. Castro, M.; Caprile, T.; Astuya, A.; Millán, C.; Reinicke, K.; Vera, J. C.; Vásquez, O.; Aguayo, L. G.; Nualart, F. High-affinity sodium-vitamin C co-transporters (SVCT) expression in embryonic mouse neurons. J. Neurochem. 2001, 78, 815-823.
39. García, M. D. L. A.; Salazar, K.; Millán, C.; Rodríguez, F.; Montecinos, H.; Caprile, T.; Silva, C.; Cortes, C.; Reinicke, K.; Vera, J. C. Sodium vitamin C cotransporter SVCT2 is expressed in hypothalamic glial cells. Glia 2005, 50, 32-47.
40. Mun, G.; Kim, M.; Lee, J.; Kim, H.; Chung, Y.; Chung, Y.; Kang, J.; Hwang, Y.; Oh, S.; Kim, J. Immunohistochemical study of the distribution of sodium-dependent vitamin C transporters in adult rat brain. J. Neurosci. Res. 2006, 83, 919-928.
41. May, J. M. Vitamin C Transport and Its Role in the Central Nervous System. In Water Soluble Vitamins; Olaf, S., Ed.; Springer: Dordrech, The Netherlands, 2012, 56, pp. 85-103.
42. Savini, I.; Catani, M. V.; Arnone, R.; Rossi, A.; Frega, G.; Del Principe, D.; Avigliano, L. Translational control of the ascorbic acid transporter SVCT2 in human platelets. Free Radic. Biol. Med. 2007, 42, 608-616.
43. +-dependent L-ascorbic acid transporter SVCT2 expressed in brainstem cells, neurons, and neuroblastoma cells is inhibited by flavonoids. J. Neurochem. 2009, 108, 563-577.
44. Nualart, F.; Castro, T.; Low, M.; Henríquez, J. P.; Oyarce, K.; Cisternas, P.; García, A.; Yáñez, A. J.; Bertinat, R.; Montecinos, V. P. Dynamic expression of the sodium-vitamin C co-transporters, SVCT1 and SVCT2, during perinatal kidney development. Histochem. Cell Biol. 2013, 139, 233-247.
45. Harrison, F.; Yu, S.; van den Bossche, K.; Li, L.; May, J.; McDonald, M. Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J. Neurochem. 2008, 106, 1198-1208.
46. Paidi, M. D.; Schjoldager, J. G.; Lykkesfeldt, J.; Tveden-Nyborg, P. Prenatal vitamin C deficiency results in differential levels of oxidative stress during late gestation in foetal guinea pig brains. Redox Biol. 2014, 2, 361-367.
47. Berger, U. V.; Lu, X. C. M.; Liu, W.; Tang, Z.; Slusher, B. S.; Hediger, M. A. Effect of middle cerebral artery occlusion on mRNA expression for the sodium-coupled vitamin C transporter SVCT2 in rat brain. J. Neurochem. 2003, 86, 896-906.
48. Gess, B.; Sevimli, S.; Strecker, J. K.; Young, P.; Schäbitz, W. R. Sodium-dependent vitamin C transporter 2 (SVCT2) expression and activity in brain capillary endothelial cells after transient ischemia in mice. PLoS One 2011, 6, e17139.
49. +-dependent vitamin C transporter functionality. Biochem. Biophys. Res. Commun. 2008, 374, 123-127.
50. Chi, X.; May, J. M. Oxidized lipoprotein induces the macrophage ascorbate transporter (SVCT2): Protection by intracellular ascorbate against oxidant stress and apoptosis. Arch. Biochem. Biophys. 2009, 485, 174-182.