Liver metabolic/oxidative stress induces hepatic and extrahepatic changes in the expression of the vitamin C transporters SVCT1 and SVCT2

European Journal of Nutrition

Volumn 53, Issue 2, 2014, Pages 401-412

  Hierro, Carlos ^a   Monte, Maria J ^a,b   Lozano, Elisa ^a   Gonzalez Sanchez, Ester ^a   Marin, Jose J G ^a,b   Macias, Rocio I R ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Ascorbic acid; Cholestasis; Diabetes; Obesity

Indexed keywords

3 [2 [2 CHLORO 4 [3 (2,6 DICHLOROPHENYL) 5 ISOPROPYL 4 ISOXAZOLYLMETHOXY]PHENYL]VINYL]BENZOIC ACID; ASCORBIC ACID; BILE ACID; FARNESOID X RECEPTOR; MESSENGER RNA; RETINOID X RECEPTOR ALPHA; SODIUM ASCORBIC ACID COTRANSPORTER; SODIUM ASCORBIC ACID COTRANSPORTER 1; SODIUM ASCORBIC ACID COTRANSPORTER 2; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B1; TAUROCHENODEOXYCHOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CHOLESTASIS; CONTROLLED STUDY; DOWN REGULATION; FATTY LIVER; GENE EXPRESSION; GENETIC TRANSFECTION; HEPATOMA CELL; HISTOPATHOLOGY; HUMAN; ILEUM; KIDNEY; LIVER; LIVER METABOLISM; LUNG PARENCHYMA; MALE; METABOLIC STRESS; NONHUMAN; OBESITY; OXIDATIVE STRESS; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; VITAMIN METABOLISM;

ANIMALIA; RATTUS;

ANIMALS; ASCORBIC ACID; BILE ACIDS AND SALTS; BIOLOGICAL AVAILABILITY; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHOLESTASIS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FATTY LIVER; GENE EXPRESSION; HUMANS; KIDNEY; LIVER; LIVER NEOPLASMS; MALE; OBESITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, ZUCKER; RNA, MESSENGER; SODIUM-COUPLED VITAMIN C TRANSPORTERS; STRESS, PHYSIOLOGICAL;

EID: 84896698043     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-013-0536-4     Document Type: Article

References (46)

1. Wilson JX (2005) Regulation of vitamin C transport. Ann Rev Nutr 25:105-125. doi: 10.1146/annurev.nutr.25.050304.092647
2. Dhariwal KR, Hartzell WO, Levine M (1991) Ascorbic acid and dehydroascorbic acid measurements in human plasma and serum. Am J Clin Nutr 54:712-716
3. Tsukaguchi H, Tokui T, Mackenzie B, Berger UV, Chen XZ, Wang Y, Brubaker RF, Hediger MA (1999) A family of mammalian Na + -dependent L-ascorbic acid transporters. Nature 399:70-75. doi: 10.1038/19986
4. Marin JJ, Serrano MA, Perez MJ, Macias RI (2009) Molecular bases of the cellular handling of vitaqmin C. Transport and metabolism in health and disease. In: Columbus F (ed) Vitamin C: Daily Requirements. Dietary sources and adverse effects Nova Science Publishers, Hauppauge
5. Brubacher D, Moser U, Jordan P (2000) Vitamin C concentrations in plasma as a function of intake: a meta-analysis. Int J Vitam Nutr Res 70:226-237
6. Macias RI, Hierro C, de Juan SC, Jimenez F, Gonzalez-San Martin F, Marin JJ (2011) Hepatic expression of sodium-dependent vitamin C transporters: ontogeny, subtissular distribution and effect of chronic liver diseases. Br J Nutr 106:1814-1825. doi: 10.1017/S0007114511002273
7. Michels AJ, Joisher N, Hagen TM (2003) Age-related decline of sodium-dependent ascorbic acid transport in isolated rat hepatocytes. Arch Biochem Biophys 410:112-120
8. Kuo SM, MacLean ME, McCormick K, Wilson JX (2004) Gender and sodium-ascorbate transporter isoforms determine ascorbate concentrations in mice. J Nutr 134:2216-2221
9. Leevy CM, Thompson A, Baker H (1970) Vitamins and liver injury. Am J Clin Nutr 23:493-499
10. Perez MJ, Castano B, Jimenez S, Serrano MA, Gonzalez-Buitrago JM, Marin JJ (2008) Role of vitamin C transporters and biliverdin reductase in the dual pro-oxidant and anti-oxidant effect of biliary compounds on the placental-fetal unit in cholestasis during pregnancy. Toxicol Appl Pharmacol 232:327-336. doi: 10.1016/j.taap.2008.07.013
11. Perez MJ, Castano B, Gonzalez-Buitrago JM, Marin JJ (2007) Multiple protective effects of melatonin against maternal cholestasis-induced oxidative stress and apoptosis in the rat fetal liver-placenta-maternal liver trio. J Pineal Res 43:130-139. doi: 10.1111/j.1600-079X.2007.00453.x
12. Mardones L, Zuniga FA, Villagran M, Sotomayor K, Mendoza P, Escobar D, Gonzalez M, Ormazabal V, Maldonado M, Onate G, Angulo C, Concha, II, Reyes AM, Carcamo JG, Barra V, Vera JC, Rivas CI (2012) Essential role of intracellular glutathione in controlling ascorbic acid transporter expression and function in rat hepatocytes and hepatoma cells. Free Radic Biol Med. doi: 10.1016/j.freeradbiomed.2012.02.017
13. Ohta Y, Kongo M, Sasaki E, Ishiguro I, Harada N (2000) Protective effect of melatonin against alpha-naphthylisothiocyanate-induced liver injury in rats. J Pineal Res 29:15-23
14. Kashiba M, Oka J, Ichikawa R, Kasahara E, Inayama T, Kageyama A, Kageyama H, Osaka T, Umegaki K, Matsumoto A, Ishikawa T, Nishikimi M, Inoue M, Inoue S (2002) Impaired ascorbic acid metabolism in streptozotocin-induced diabetic rats. Free Radic Biol Med 33:1221-1230
15. Monte MJ, Morales AI, Arevalo M, Alvaro I, Macias RI, Marin JJ (1996) Reversible impairment of neonatal hepatobiliary function by maternal cholestasis. Hepatology 23:1208-1217. doi: 10.1002/hep.510230540
16. Rakieten N, Rakieten ML, Nadkarni MR (1963) Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep 29:91-98
17. Pizarro M, Balasubramaniyan N, Solis N, Solar A, Duarte I, Miquel JF, Suchy FJ, Trauner M, Accatino L, Ananthanarayanan M, Arrese M (2004) Bile secretory function in the obese Zucker rat: evidence of cholestasis and altered canalicular transport function. Gut 53:1837-1843. doi: 10.1136/gut.2003.037689
18. Corpe CP, Burant CF (1996) Hexose transporter expression in rat small intestine: effect of diet on diurnal variations. Am J Physiol 271:G211-G216
19. Monte MJ, Dominguez S, Palomero MF, Macias RI, Marin JJ (1999) Further evidence of the usefulness of bile acids as molecules for shuttling cytostatic drugs toward liver tumors. J Hepatol 31:521-528
20. Berry MN, Friend DS (1969) High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J Cell Biol 43:506-520
21. Cassio D, Macias RI, Grosse B, Marin JJ, Monte MJ (2007) Expression, localization, and inducibility by bile acids of hepatobiliary transporters in the new polarized rat hepatic cell lines, Can 3-1 and Can 10. Cell Tissue Res 330:447-460. doi: 10.1007/s00441-007-0494-3
22. Mashige F, Imai K, Osuga T (1976) A simple and sensitive assay of total serum bile acids. Clin Chim Acta 70:79-86
23. Marin JJG, Villanueva GR, Esteller A (1988) Diabetes-induced cholestasis in the rat: possible role of hyperglycemia and hypoinsulinemia. Hepatology 8:332-340
24. Maulen NP, Henriquez EA, Kempe S, Carcamo JG, Schmid-Kotsas A, Bachem M, Grunert A, Bustamante ME, Nualart F, Vera JC (2003) Up-regulation and polarized expression of the sodium-ascorbic acid transporter SVCT1 in post-confluent differentiated CaCo-2 cells. J Biol Chem 278:9035-9041. doi: 10.1074/jbc.M205119200
25. Boyer JC, Campbell CE, Sigurdson WJ, Kuo SM (2005) Polarized localization of vitamin C transporters, SVCT1 and SVCT2, in epithelial cells. Biochem Biophys Res Commun 334:150-156. doi: 10.1016/j.bbrc.2005.06.069
26. Amano A, Aigaki T, Maruyama N, Ishigami A (2010) 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 496:38-44. doi: 10.1016/j.abb.2010.01.012
27. MacDonald L, Thumser AE, Sharp P (2002) Decreased expression of the vitamin C transporter SVCT1 by ascorbic acid in a human intestinal epithelial cell line. Br J Nutr 87:97-100. doi: 10.1079/BJN2001492
28. Adeghate E (2004) Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol Cell Biochem 261:187-191
29. Russell JW, Berent-Spillson A, Vincent AM, Freimann CL, Sullivan KA, Feldman EL (2008) Oxidative injury and neuropathy in diabetes and impaired glucose tolerance. Neurobiol Dis 30:420-429. doi: 10.1016/j.nbd.2008.02.013
30. Koneru B, Reddy MC, dela Torre AN, Patel D, Ippolito T, Ferrante RJ (1995) Studies of hepatic warm ischemia in the obese Zucker rat. Transplantation 59:942-946
31. Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM (1997) Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci USA 94:2557-2562
32. Jain SK, Croad JL, Velusamy T, Rains JL, Bull R (2010) Chromium dinicocysteinate supplementation can lower blood glucose, CRP, MCP-1, ICAM-1, creatinine, apparently mediated by elevated blood vitamin C and adiponectin and inhibition of NFkappaB, Akt, and Glut-2 in livers of zucker diabetic fatty rats. Mol Nutr Food Res 54:1371-1380. doi: 10.1002/mnfr.200900177
33. Foster DJ, Ravikumar P, Bellotto DJ, Unger RH, Hsia CC (2010) Fatty diabetic lung: altered alveolar structure and surfactant protein expression. Am J Physiol Lung Cell Mol Physiol 298:L392-L403. doi: 10.1152/ajplung.00041.2009
34. Wu X, Iguchi T, Hirano J, Fujita I, Ueda H, Itoh N, Tanaka K, Nakanishi T (2007) Upregulation of sodium-dependent vitamin C transporter 2 expression in adrenals increases norepinephrine production and aggravates hyperlipidemia in mice with streptozotocin-induced diabetes. Biochem Pharmacol 74:1020-1028. doi: 10.1016/j.bcp.2007.05.024
35. Yue DK, McLennan S, Fisher E, Heffernan S, Capogreco C, Ross GR, Turtle JR (1989) Ascorbic acid metabolism and polyol pathway in diabetes. Diabetes 38:257-261
36. Seghieri G, Martinoli L, Miceli M, Ciuti M, D'Alessandri G, Gironi A, Palmieri L, Anichini R, Bartolomei G, Franconi F (1994) Renal excretion of ascorbic acid in insulin dependent diabetes mellitus. Int J Vitam Nutr Res 64:119-124
37. Perez MJ, Macias RI, Duran C, Monte MJ, Gonzalez-Buitrago JM, Marin JJ (2005) Oxidative stress and apoptosis in fetal rat liver induced by maternal cholestasis. Protective effect of ursodeoxycholic acid. J Hepatol 43:324-332. doi: 10.1016/j.jhep.2005.02.028
38. Wang P, Gong G, Wei Z, Li Y (2010) Ethyl pyruvate prevents intestinal inflammatory response and oxidative stress in a rat model of extrahepatic cholestasis. J Surg Res 160:228-235. doi: 10.1016/j.jss.2009.03.027
39. Aguirre R, May JM (2008) Inflammation in the vascular bed: importance of vitamin C. Pharmacol Ther 119:96-103. doi: 10.1016/j.pharmthera.2008.05.002
40. Perez MJ, Briz O (2009) Bile-acid-induced cell injury and protection. World J Gastroenterol 15:1677-1689
41. Allen K, Jaeschke H, Copple BL (2011) Bile acids induce inflammatory genes in hepatocytes: a novel mechanism of inflammation during obstructive cholestasis. Am J Pathol 178:175-186. doi: 10.1016/j.ajpath.2010.11.026
42. Zhang Y, Hong JY, Rockwell CE, Copple BL, Jaeschke H, Klaassen CD (2012) Effect of bile duct ligation on bile acid composition in mouse serum and liver. Liver Int 32:58-69. doi: 10.1111/j.1478-3231.2011.02662.x
43. Donner MG, Schumacher S, Warskulat U, Heinemann J, Haussinger D (2007) Obstructive cholestasis induces TNF-alpha- and IL-1 -mediated periportal downregulation of Bsep and zonal regulation of Ntcp, Oatp1a4, and Oatp1b2. Am J Physiol Gastrointest Liver Physiol 293:G1134-G1146. doi: 10.1152/ajpgi.00079. 2007
44. Kullak-Ublick GA, Stieger B, Meier PJ (2004) Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 126:322-342
45. Zhang J, Luo B, Tang L, Wang Y, Stockard CR, Kadish I, Van Groen T, Grizzle WE, Ponnazhagan S, Fallon MB (2009) Pulmonary angiogenesis in a rat model of hepatopulmonary syndrome. Gastroenterology 136:1070-1080. doi: 10.1053/j.gastro.2008.12.001
46. Monasterolo L, Peiretti A, Elias MM (1993) Rat renal functions during the first days post-bile duct ligation. Ren Fail 15:461-467