Cited by 139Vitamin C and Antioxidants ResearchNutrition, Genetics, and DiseaseGenetic Associations and Epidemiology

Human Genetic Variation Influences Vitamin C Homeostasis by Altering Vitamin C Transport and Antioxidant Enzyme Function

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Michels, Alexander J., Hagen, Tory M., Frei, Balz·2013·Annual Review of Nutrition

Abstract

New evidence for the regulation of vitamin C homeostasis has emerged from several studies of human genetic variation. Polymorphisms in the genes encoding sodium-dependent vitamin C transport proteins are strongly associated with plasma ascorbate levels and likely impact tissue cellular vitamin C status. Furthermore, genetic variants of proteins that suppress oxidative stress or detoxify oxidatively damaged biomolecules, i.e., haptoglobin, glutathione-S-transferases, and possibly manganese superoxide dismutase, affect ascorbate levels in the human body. There also is limited evidence for a role of glucose transport proteins. In this review, we examine the extent of the variation in these genes, their impact on vitamin C status, and their potential role in altering chronic disease risk. We conclude that future epidemiological studies should take into account genetic variation in order to successfully determine the role of vitamin C nutriture or supplementation in human vitamin C status and chronic disease risk.

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  • SNPs of SLC23A1 were characterized as both synonymous and non-synonymous, with the greatest diversity found in the African population, producing proteins of lower functionality.

    “SNPs of SLC23A1 were characterized as both synonymous and non-synonymous SNPs (with the greatest diversity found in the African population) producing proteins of lower functionality.”

    From Vitamin C-Sources, Physiological Role, Kinetics, Deficiency, Use, Toxicity, and Determination (2021) · cites this paper as [83]

    The SLC23A1 Genomic Characterization section identifies one synonymous and three nonsynonymous coding SNPs and reports reduced ascorbate transport for proteins produced by the nonsynonymous variants. It says African American populations show the greatest observed SNP diversity, not African populations generally. The claim also overextends the reduced-function finding to synonymous SNPs. (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • In the case of SNPs of SLC23A2, all studied polymorphisms were synonymous.

    “In the case of SNPs of SLC23A2, all studied polymorphisms were synonymous [80,83].”

    From Vitamin C-Sources, Physiological Role, Kinetics, Deficiency, Use, Toxicity, and Determination (2021) · cites this paper as [83]

    The “Genomic Characterization of SLC23A2” section says that all analyzed SNPs within the protein-coding region were synonymous. It also says most analyzed SNPs were in intronic or untranslated regions, so the claim overextends “synonymous” to all studied polymorphisms. (LLM, conf=0.90)

    Experimental — accuracy not yet measured
  • The strongest evidence to decrease circulating vitamin C levels was found for several common SNPs of SLC23A1 due to reduced renal reabsorption.

    “The strongest evidence to decrease circulating vitamin C levels was found for several common SNPs of SLC23A1 due to reduced renal reabsorption.”

    From Vitamin C-Sources, Physiological Role, Kinetics, Deficiency, Use, Toxicity, and Determination (2021) · cites this paper as [83]

    The Summary reports a significant decline in circulating vitamin C for one SLC23A1 SNP (rs33972313), while two others showed nonsignificant reductions. The “Genetic Variation in SLC23A1 and Vitamin C Status” section proposes reduced renal reabsorption as a mechanism, drawing on knockout-mouse findings, but does not establish it as the cause of the observed human SNP associations. Thus, the claim overstates both the evidence for several SNPs and the certainty of the mechanism. (LLM, conf=0.87)

    Experimental — accuracy not yet measured
  • The effect of individual SNPs on the vitamin C system level has an additive character, depending on genotype and allele dosage.

    “An effect of individual SNPs on the vitamin C system level has an additive character, which depends on genotype and an allele dosage (additive) effect that was also described.”

    From Vitamin C-Sources, Physiological Role, Kinetics, Deficiency, Use, Toxicity, and Determination (2021) · cites this paper as [83]

    The section “Genetic Variation in SLC23A1 and Vitamin C Status” (page unavailable) reports approximately 6 μM lower circulating ascorbate per rs33972313 allele, supporting an additive effect for that SNP. It does not establish an additive effect for individual SNPs generally; it notes that a per-allele effect for rs10063949 was not observed in another cohort. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • An elevation of vitamin C levels was also seldomly described.

    “However, an elevation of vitamin C levels was also seldomly described [80,82,83].”

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Research works printed but not linked: 89

  1. [1]Ambrosone CB Freudenheim JL Thompson PA Bowman E Vena JE 1999 Manganese superoxide dismutase (MnSOD) genetic polymorphisms, dietary antioxidants, and risk of breast cancer Cancer Res 59 602 6 9973207
  2. [2]Andrew AS Gui J Sanderson AC Mason RA Morlock EV 2009 Bladder cancer SNP panel predicts susceptibility and survival Hum Genet 125 527 39 19252927 PMC2763504
  3. [3]Asleh R Levy AP 2010 Divergent effects of alpha-tocopherol and vitamin C on the generation of dysfunctional HDL associated with diabetes and the Hp 2-2 genotype Antioxid Redox Signal 12 209 17 19769483 PMC2821143
  4. [4]Birlouez-Aragon I Saavedra G Tessier FJ Galinier A Ait-Ameur L 2010 A diet based on high-heat-treated foods promotes risk factors for diabetes mellitus and cardiovascular diseases Am J Clin Nutr 91 1220 26 20335546
  5. [5]Block G Jensen CD Dalvi TB Norkus EP Hudes M 2009 Vitamin C treatment reduces elevated C-reactive protein Free Radic Biol Med 46 70 77 18952164 PMC2631578
  6. [6]Block G Shaikh N Jensen CD Volberg V Holland N 2011 Serum vitamin C and other biomarkers differ by genotype of phase 2 enzyme genes GSTM1 and GSTT1 Am J Clin Nutr 94 929 37 21813807 PMC3155929
  7. [7]Boekholdt SM Meuwese MC Day NE Luben R Welch A 2006 Plasma concentrations of ascorbic acid and C-reactive protein, and risk of future coronary artery disease, in apparently healthy men and women: the EPIC-Norfolk prospective population study Br J Nutr 96 516 22 16925857
  8. [8]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 56 15993839
  9. [9]Cahill LE El-Sohemy A 2009 Vitamin C transporter gene polymorphisms, dietary vitamin C and serum ascorbic acid J Nutrigenet Nutrigenomics 2 292 301 20588054
  10. [10]Cahill LE El-Sohemy A 2010 Haptoglobin genotype modifies the association between dietary vitamin C and serum ascorbic acid deficiency Am J Clin Nutr 92 1494 500 20926521
  11. [11]Cahill LE Fontaine-Bisson B El-Sohemy A 2009 Functional genetic variants of glutathione S-transferase protect against serum ascorbic acid deficiency Am J Clin Nutr 90 1411 17 19710200
  12. [12]Canova C Dunster C Kelly FJ Minelli C Shah PL 2012 PM10-induced hospital admissions for asthma and chronic obstructive pulmonary disease: the modifying effect of individual characteristics Epidemiology 23 607 15 22531667
  13. [13]Carr AC Frei B 1999 Toward a new recommended dietary allowance for vitamin C based on antioxidant and health effects in humans Am J Clin Nutr 69 1086 107 10357726
  14. [14]Chavez J Chung WG Miranda CL Singhal M Stevens JF Maier CS 2010 Site-specific protein adducts of 4-hydroxy-2(E)-nonenal in human THP-1 monocytic cells: Protein carbonylation is diminished by ascorbic acid Chem Res Toxicol 23 37 47 20043646 PMC2825578
  15. [16]Church SL Grant JW Meese EU Trent JM 1992 Sublocalization of the gene encoding manganese superoxide dismutase (MnSOD/SOD2) to 6q25 by fluorescence in situ hybridization and somatic cell hybrid mapping Genomics 14 823 25 1427917
  16. [18]Cox SE Doherty C Atkinson SH Nweneka CV Fulford AJ 2007 Haplotype association between haptoglobin (Hp2) and Hp promoter SNP (A-61C) may explain previous controversy of haptoglobin and malaria protection PLoS ONE 2 e362 Creation of the SLC23A1 knockout mouse, linking renal reabsorption to SVCT1 function 17426810 PMC1838521
  17. [19]Dehghan M Akhtar-Danesh N McMillan CR Thabane L 2007 Is plasma vitamin C an appropriate biomarker of vitamin C intake? A systematic review and meta-analysis Nutr J 6 41 17997863 PMC2200644
  18. [20]Delanghe J Langlois M Duprez D De Buyzere M Clement D 1999 Haptoglobin polymorphism and peripheral arterial occlusive disease Atherosclerosis 145 287 92 10488955
  19. [21]Delanghe JR Langlois MR Boelaert JR Van Acker J Van Wanzeele F 1998 Haptoglobin polymorphism, iron metabolism and mortality in HIV infection AIDS 12 1027 32 9662199
  20. [22]Dherani M Murthy GV Gupta SK Young IS Maraini G 2008 Blood levels of vitamin C, carotenoids and retinol are inversely associated with cataract in a North Indian population Invest Ophthalmol Vis Sci 49 3328 35 18421094
  21. [23]Duarte MM Moresco RN Duarte T Santi A Bagatini MD 2010 Oxidative stress in hypercholesterolemia and its association with Ala16Val superoxide dismutase gene polymorphism Clin Biochem 43 1118 23 20627099
  22. [24]Duarte-Salles T Mendez MA Morales E Bustamante M Rodriguez-Vicente A 2012 Dietary benzo(a)pyrene and fetal growth: effect modification by vitamin C intake and glutathione S-transferase P1 polymorphism Environ Int 45 1 8 22565211 PMC3855239
  23. [25]Dusinska M Ficek A Horska A Raslova K Petrovska H 2001 Glutathione S-transferase polymorphisms influence the level of oxidative DNA damage and antioxidant protection in humans Mutat Res 482 47 55 11535248
  24. [26]Eck P Erichsen HC Taylor JG Yeager M Hughes AL 2004 Comparison of the genomic structure and variation in the two human sodium-dependent vitamin C transporters, SLC23A1 and SLC23A2 Hum Genet 115 285 94 First association of GST polymorphisms with ascorbic acid levels in humans 15316768
  25. [28]Erichsen HC Peters U Eck P Welch R Schoen RE 2008 Genetic variation in sodium-dependent vitamin C transporters SLC23A1 and SLC23A2 and risk of advanced colorectal adenoma Nutr Cancer 60 652 59 18791929 PMC3490215
  26. [29]Fischer H Schwarzer C Illek B 2004 Vitamin C controls the cystic fibrosis transmembrane conductance regulator chloride channel Proc Natl Acad Sci USA 101 3691 96 14993613 PMC373524
  27. [30]Frei B Birlouez-Aragon I Lykkesfeldt J 2012 Authors’ perspective: What is the optimum intake of vitamin C in humans? Crit Rev Food Sci Nutr 52 815 29 22698272
  28. [31]Frikke-Schmidt H Lykkesfeldt J 2009 Role of marginal vitamin C deficiency in atherogenesis: in vivo models and clinical studies Basic Clin Pharmacol Toxicol 104 419 33 Extensive review of the factors involved in vitamin C research in humans, including evaluation of current RDAs 19489786
  29. [32]Gale CR Martyn CN Winter PD Cooper C 1995 Vitamin C and risk of death from stroke and coronary heart disease in cohort of elderly people BMJ 310 1563 66 7787644 PMC2549941
  30. [33]Gamazon ER Ziliak D Im HK LaCroix B Park DS 2012 Genetic architecture of microRNA expression: implications for the transcriptome and complex traits Am J Hum Genet 90 1046 63 22658545 PMC3370272
  31. [35]Goldenberg H Schweinzer E 1994 Transport of vitamin C in animal and human cells J Bioenerg Biomembr 26 359 67 7844110
  32. [36]Goldenstein H Levy NS Levy AP 2012 Haptoglobin genotype and its role in determining heme-iron mediated vascular disease Pharmacol Res 66 1 6 22465143 PMC3345090
  33. [37]Han J Colditz GA Hunter DJ 2007 Manganese superoxide dismutase polymorphism and risk of skin cancer (United States) Cancer Causes Control 18 79 89 17186424
  34. [38]Haque R Chun E Howell JC Sengupta T Chen D Kim H 2012 MicroRNA-30b-mediated regulation of catalase expression in human ARPE-19 cells PLoS ONE 7 e42542 22880027 PMC3412823
  35. [39]Hayes JD Flanagan JU Jowsey IR 2005 Glutathione transferases Annu Rev Pharmacol Toxicol 45 51 88 15822171
  36. [40]Henriquez-Sanchez P Sanchez-Villegas A Doreste-Alonso J Ortiz-Andrellucchi A Pfrimer K Serra-Majem L 2009 Dietary assessment methods for micronutrient intake: a systematic review on vitamins Br J Nutr 102 Suppl 1 S10 37 20100364
  37. [41]Higasa S Tsujimura M Hiraoka M Nakayama K Yanagisawa Y 2007 Polymorphism of glutathione S-transferase P1 gene affects human vitamin C metabolism Biochem Biophys Res Commun 364 708 13 17964545
  38. [42]Horska A Mislanova C Bonassi S Ceppi M Volkovova K Dusinska M 2011 Vitamin C levels in blood are influenced by polymorphisms in glutathione S-transferases Eur J Nutr 50 437 46 21152927
  39. [43]Jenab M Riboli E Ferrari P Sabate J Slimani N 2006 Plasma and dietary vitamin C levels and risk of gastric cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) Carcinogenesis 27 2250 57 16774936
  40. [44]Juraschek SP Guallar E Appel LJ Miller ER 3rd 2012 Effects of vitamin C supplementation on blood pressure: a meta-analysis of randomized controlled trials Am J Clin Nutr 95 1079 88 22492364 PMC3325833
  41. [46]Kasvosve I Delanghe JR Gomo ZA Gangaidzo IT Khumalo H 2002 Effect of transferrin polymorphism on the metabolism of vitamin C in Zimbabwean adults Am J Clin Nutr 75 321 25 11815325
  42. [47]Khaw KT Bingham S Welch A Luben R Wareham N 2001 Relation between plasma ascorbic acid and mortality in men and women in EPIC-Norfolk prospective study: a prospective population study. European Prospective Investigation into Cancer and Nutrition Lancet 357 657 63 11247548
  43. [48]Klepper J Vera JC De Vivo DC 1998 Deficient transport of dehydroascorbic acid in the glucose transporter protein syndrome Ann Neurol 44 286 87 9708557
  44. [49]Klepper J Wang D Fischbarg J Vera JC Jarjour IT 1999 Defective glucose transport across brain tissue barriers: a newly recognized neurological syndrome Neurochem Res 24 587 94 10227690
  45. [50]Kumar M Lu Z Takwi AA Chen W Callander NS 2011 Negative regulation of the tumor suppressor p53 gene by microRNAs Oncogene 30 843 53 20935678 PMC3021102
  46. [51]Langlois MR Delanghe JR De Buyzere ML Bernard DR Ouyang J 1997 Effect of haptoglobin on the metabolism of vitamin C Am J Clin Nutr 66 606 10 9280180
  47. [52]Lee YC Huang HY Chang CJ Cheng CH Chen YT 2010 Mitochondrial GLUT10 facilitates dehydroascorbic acid import and protects cells against oxidative stress: mechanistic insight into arterial tortuosity syndrome Hum Mol Genet 19 3721 33 20639396
  48. [53]Levine M Conry-Cantilena C Wang Y Welch RW Washko PW 1996 Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance Proc Natl Acad Sci USA 93 3704 9 8623000 PMC39676
  49. [55]Levy AP Asleh R Blum S Levy NS Miller-Lotan R 2010 Haptoglobin: basic and clinical aspects Antioxid Redox Signal 12 293 304 19659435
  50. [56]Lykkesfeldt J Poulsen HE 2010 Is vitamin C supplementation beneficial? Lessons learned from randomised controlled trials Br J Nutr 103 1251 59 20003627
  51. [57]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 25 21733302
  52. [58]Maulen NP Henriquez EA Kempe S Carcamo JG Schmid-Kotsas A 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 41 12381735
  53. [59]May JM Qu ZC Qiao H Koury MJ 2007 Maturational loss of the vitamin C transporter in erythrocytes Biochem Biophys Res Commun 360 295 98 17586466 PMC1964531
  54. [60]McIlwain CC Townsend DM Tew KD 2006 Glutathione S-transferase polymorphisms: cancer incidence and therapy Oncogene 25 1639 48 16550164 PMC6361140
  55. [61]Meredith ME Harrison FE May JM 2011 Differential regulation of the ascorbic acid transporter SVCT2 during development and in response to ascorbic acid depletion Biochem Biophys Res Commun 414 737 42 22001929 PMC3210393
  56. [62]Michels AJ Frei BB Stipanuk MH Caudill MA 2012 Vitamin C Biochemical, Physiological, and Molecular Aspects of Human Nutrition 626 54 St. Louis, Mo Elsevier/Saunders
  57. [63]Michels AJ Hagen TM 2009 Hepatocyte nuclear factor 1 is essential for transcription of sodium-dependent vitamin C transporter protein 1 Am J Physiol Cell Physiol 297 C1220 27 19741195 PMC2826896
  58. [64]Miranda CL Reed RL Kuiper HC Alber S Stevens JF 2009 Ascorbic acid promotes detoxification and elimination of 4-hydroxy-2(E)-nonenal in human monocytic THP-1 cells Chem Res Toxicol 22 863 74 19326901 PMC2730585
  59. [65]Myint PK Luben RN Welch AA Bingham SA Wareham NJ Khaw KT 2008 Plasma vitamin C concentrations predict risk of incident stroke over 10 y in 20 649 participants of the European Prospective Investigation into Cancer Norfolk prospective population study Am J Clin Nutr 87 64 69 18175738
  60. [66]Na N Delanghe JR Taes YE Torck M Baeyens WR Ouyang J 2006 Serum vitamin C concentration is influenced by haptoglobin polymorphism and iron status in Chinese Clin Chim Acta 365 319 24 16256097
  61. [67]Park KU Song J Kim JQ 2004 Haptoglobin genotypic distribution (including Hp0 allele) and associated serum haptoglobin concentrations in Koreans J Clin Pathol 57 1094 95 A broad overview of vitamin C, with a review of ascorbate chemistry, biology, nutrition, and health effects of supplementation 15452167 PMC1770454
  62. [68]Pfister R Sharp SJ Luben R Wareham NJ Khaw KT 2011 Plasma vitamin C predicts incident heart failure in men and women in European Prospective Investigation into Cancer and Nutrition—Norfolk prospective study Am Heart J 162 246 53 21835284
  63. [69]Portugal CC da Encarnacao TG Socodato R Moreira SR Brudzewsky D 2012 Nitric oxide modulates sodium vitamin C transporter 2 (SVCT-2) protein expression via protein kinase G (PKG) and nuclear factor-κB (NF-κB) J Biol Chem 287 3860 72 22041898 PMC3281729
  64. [70]Qiao H May JM 2009 Macrophage differentiation increases expression of the ascorbate transporter (SVCT2) Free Radic Biol Med 46 1221 32 19232538 PMC3732409
  65. [71]Qiao H May JM 2011 CpG methylation at the USF-binding site mediates cell-specific transcription of human ascorbate transporter SVCT2 exon 1a Biochem J 440 73 84 21770893 PMC3709574
  66. [72]Qiao H May JM 2011 Regulation of the human ascorbate transporter SVCT2 exon 1b gene by zinc-finger transcription factors Free Radic Biol Med 50 1196 209 21335086 PMC3070803
  67. [74]Ravindran RD Vashist P Gupta SK Young IS Maraini G 2011 Inverse association of vitamin C with cataract in older people in India Ophthalmology 118 1958 65 e2 21705085 PMC3185206
  68. [75]Reidling JC Rubin SA 2011 Promoter analysis of the human ascorbic acid transporters SVCT1 and 2: mechanisms of adaptive regulation in liver epithelial cells J Nutr Biochem 22 344 50 20471816 PMC2923671
  69. [76]Rubin SA Dey S Reidling JC 2005 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 1732 76 81 16380174
  70. [77]Rumsey SC Daruwala R Al-Hasani H Zarnowski MJ Simpson IA Levine M 2000 Dehydroascorbic acid transport by GLUT4 in Xenopus oocytes and isolated rat adipocytes J Biol Chem 275 28246 53 10862609
  71. [78]Rumsey SC Kwon O Xu GW Burant CF Simpson I Levine M 1997 Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid J Biol Chem 272 18982 89 9228080
  72. [79]Savini I Catani MV Arnone R Rossi A Frega G 2007 Translational control of the ascorbic acid transporter SVCT2 in human platelets Free Radic Biol Med 42 608 16 17291984
  73. [80]Savini I Rossi A Catani MV Ceci R Avigliano L 2007 Redox regulation of vitamin C transporter SVCT2 in C2C12 myotubes Biochem Biophys Res Commun 361 385 90 17643393
  74. [81]Siedlinski M Postma DS van Diemen CC Blokstra A Smit HA Boezen HM 2008 Lung function loss, smoking, vitamin C intake, and polymorphisms of the glutamate-cysteine ligase genes Am J Respir Crit Care Med 178 13 19 18420959
  75. [83]Sotiriou S Gispert S Cheng J Wang Y Chen A 2002 Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival Nat Med 8 514 17 11984597
  76. [84]Sutton A Imbert A Igoudjil A Descatoire V Cazanave S 2005 The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability Pharmacogenet Genomics 15 311 19 15864132
  77. [85]Timpson NJ Forouhi NG Brion MJ Harbord RM Cook DG 2010 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 92 375 82 20519558 PMC3605792
  78. [86]Tsukaguchi H Tokui T Mackenzie B Berger UV Chen XZ 1999 A family of mammalian Na+-dependent L-ascorbic acid transporters Nature 399 70 75 10331392
  79. [87]Valero MP Fletcher AE De Stavola BL Vioque J Alepuz VC 2002 Vitamin C is associated with reduced risk of cataract in a Mediterranean population J Nutr 132 1299 306 12042450
  80. [88]Vardi M Levy AP 2012 Is it time to screen for the haptoglobin genotype to assess the cardiovascular risk profile and vitamin E therapy responsiveness in patients with diabetes? Curr Diab Rep 12 274 79 22427005 PMC3590812
  81. [89]Vera JC Rivas CI Fischbarg J Golde DW 1993 Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid Nature 364 79 82 8316303
  82. [90]Voko Z Hollander M Hofman A Koudstaal PJ Breteler MM 2003 Dietary antioxidants and the risk of ischemic stroke: the Rotterdam Study Neurology 61 1273 75 14610137
  83. [91]Wang H Dutta B Huang W Devoe LD Leibach FH 1999 Human Na(+)-dependent vitamin C transporter 1 (hSVCT1): primary structure, functional characteristics and evidence for a non-functional splice variant Biochim Biophys Acta 1461 1 9 Development of the SVCT2 knockout mouse, originally named SLC23A1, linking perinatal survival with ascorbate levels 10556483
  84. [92]Wilms LC Claughton TA de Kok TM Kleinjans JC 2007 GSTM1 and GSTT1 polymorphism influences protection against induced oxidative DNA damage by quercetin and ascorbic acid in human lymphocytes in vitro Food Chem Toxicol 45 2592 96 17706336
  85. [93]Wilson JX 2005 Regulation of vitamin C transport Annu Rev Nutr 25 105 25 First association of SLC23A1 polymorphisms with plasma or serum ascorbate levels in human volunteers 16011461
  86. [95]Ye Z Song H 2008 Antioxidant vitamins intake and the risk of coronary heart disease: meta-analysis of cohort studies Eur J Cardiovasc Prev Rehabil 15 26 34 18277182
  87. [96]Yuan LH Meng LP Ma WW Li S Feng JF 2012 The role of glutathione S-transferase M1 and T1 gene polymorphisms and fruit and vegetable consumption in antioxidant parameters in healthy subjects Br J Nutr 107 928 33 21896242
  88. [97]Zanon-Moreno V Ciancotti-Olivares L Asencio J Sanz P Ortega-Azorin C 2011 Association between a SLC23A2 gene variation, plasma vitamin C levels, and risk of glaucoma in a Mediterranean population Mol Vis 17 2997 3004 22171153 PMC3236071
  89. [98]Zhou H Brock J Liu D Board PG Oakley AJ 2012 Structural insights into the dehydroascorbate reductase activity of human omega-class glutathione transferases J Mol Biol 420 190 203 22522127

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Authors
Michels, A. J., Hagen, T. M., & Frei, B.
Affiliations
Oregon State University (US)
Venue
Annual Review of Nutrition
Published
2013-07-17
Volume
33
Issue
1
Pages
45-70
ISSN
  • 0199-9885 (ISSN-L)
  • 1545-4312
OpenAlex
W2138137527
Cited by
139
References
9
Citations by year
2026: 5 · 2025: 12 · 2024: 12 · 2023: 9 · 2022: 15 · 2021: 17 · 2020: 10 · 2019: 12 · 2018: 11 · 2017: 5 · 2016: 9 · 2015: 5 · 2014: 12 · 2013: 5
FWCI
1.17
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Nutrition (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Environmental Health Sciences (T32ES007060)
Topics
  • Health Sciences › Nursing › Nutrition and Dietetics › Vitamin C and Antioxidants Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Nutrition, Genetics, and Disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Keywords
genetic polymorphism, sodium-dependent vitamin C transporters, vitamin C, haptoglobin, glutathione S-transferase, manganese superoxide dismutase, oxidative stress, antioxidant enzymes, chronic disease risk, vitamin C supplementation
MeSH terms
Animals, Ascorbic Acid, Biological Transport, Homeostasis, Humans, Oxidoreductases, Genetic Variation, Sodium-Coupled Vitamin C Transporters

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