Maternal Vitamin C Deficiency during Pregnancy Persistently Impairs Hippocampal Neurogenesis in Offspring of Guinea Pigs

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Tveden Nyborg, Pernille ^a   Vogt, Lucile ^b   Schjoldager, Janne G ^a   Jeannet, Natalie ^b   Hasselholt, Stine ^a   Paidi, Maya D ^a   Christen, Stephan ^b,c   Lykkesfeldt, Jens ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCORBIC ACID DEFICIENCY; BODY WEIGHT; BRAIN DEVELOPMENT; BRAIN SIZE; BRAIN WEIGHT; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DEVELOPMENTAL DISORDER; DRUG MEGADOSE; FEMALE; GUINEA PIG; HIPPOCAMPUS; IN VIVO STUDY; LOW DRUG DOSE; MALE; MATERNAL DISEASE; MAZE TEST; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DISORDER; STEREOLOGY; VITAMIN BLOOD LEVEL; VITAMIN SUPPLEMENTATION;

ANIMALS; ANIMALS, NEWBORN; ASCORBIC ACID DEFICIENCY; BODY WEIGHT; BRAIN; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; DENTATE GYRUS; FEMALE; GUINEA PIGS; HIPPOCAMPUS; MATERNAL EXPOSURE; MAZE LEARNING; NEUROGENESIS; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

ANIMALIA; CAVIA;

EID: 84868333197     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048488     Document Type: Article

References (52)

1. Tveden-Nyborg P, Johansen LK, Raida Z, Villumsen CK, Larsen JO, et al. (2009) Vitamin C deficiency in early postnatal life impairs spatial memory and reduces the number of hippocampal neurons in guinea pigs. Am J Clin Nutr 90: 540-6.
2. Lykkesfeldt J, Trueba GP, Poulsen HE, Christen S, (2007) Vitamin C deficiency in weanling guinea pigs: differential expression of oxidative stress and DNA repair in liver and brain. Br J Nutr 98: 1116-9.
3. Kratzing CC, Kelly JD, Kratzing JE, (1985) Ascorbic acid in fetal rat brain. J Neurochem 44: 1623-4.
4. Harrison FE, Meredith ME, Dawes SM, Saskowski JL, May JM, (2010) Low ascorbic acid and increased oxidative stress in gulo(-/-) mice during development. Brain Res 1349: 143-52.
5. Haramoto M, Tatemoto H, Muto N, (2008) Essential role of ascorbic acid in neural differentiation and development: High levels of ascorbic acid 2-glucoside effectively enhance nerve growth factor-induced neurite formation and elongation in PC12 cells. Journal of Health Science 54: 43-9.
6. Lee JY, Chang MY, Park CH, Kim HY, Kim JH, et al. (2003) Ascorbate-induced differentiation of embryonic cortical precursors into neurons and astrocytes. J Neurosci Res 73: 156-65.
7. Qiu S, Li L, Weeber EJ, May JM, (2007) Ascorbate transport by primary cultured neurons and its role in neuronal function and protection against excitotoxicity. J Neurosci Res 85: 1046-56.
8. Harrison FE, Dawes SM, Meredith ME, Babaev VR, Li L, et al. (2010) Low vitamin C and increased oxidative stress and cell death in mice that lack the sodium-dependent vitamin C transporter SVCT2. Free Radic Biol Med 49: 821-9.
9. Sotiriou S, Gispert S, Cheng J, Wang YH, Chen A, et al. (2002) Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nature Medicine 8: 514-7.
10. Milby K, Oke A, Adams RN, (1982) Detailed mapping of ascorbate distribution in rat brain. Neurosci Lett 28: 169-74.
11. Mefford IN, Oke AF, Adams RN, (1981) Regional distribution of ascorbate in human brain. Brain Res 212: 223-6.
12. Harrison FE, Green RJ, Dawes SM, May JM, (2010) Vitamin C distribution and retention in the mouse brain. Brain Res 1348: 181-6.
13. Mun GH, Kim MJ, Lee JH, Kim HJ, Chung YH, et al. (2006) Immunohistochemical study of the distribution of sodium-dependent vitamin C transporters in adult rat brain. J Neurosci Res 83: 919-28.
14. Tsukaguchi H, Tokui T, Mackenzie B, Berger UV, Chen XZ, et al. (1999) A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 399: 70-5.
15. Dobbing J, Sands J, (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3: 79-83.
16. Dobbing J, Sands J (1970) Growth and Development of Brain and Spinal Cord of Guinea Pig. Brain Research 17: 115-&.
17. Blandau RJ, Young WC, (1939) The effects of delayed fertilization on the development of the guinea pig ovum. American Journal of Anatomy 64: 303-29.
18. Lykkesfeldt J, Moos T, (2005) Age-dependent change in Vitamin C status: a phenomenon of maturation rather than of ageing. Mech Ageing Dev 126: 892-8.
19. Tveden-Nyborg P, Hasselholt S, Miyashita N, Moos T, Poulsen HE, et al. (2011) Chronic Vitamin C Deficiency does not Accelerate Oxidative Stress in Ageing Brains of Guinea Pigs. Basic Clin Pharmacol Toxicol 110: 524-9.
20. Guidi S, Ciani E, Severi S, Contestabile A, Bartesaghi R, (2005) Postnatal neurogenesis in the dentate gyrus of the guinea pig. Hippocampus 15: 285-301.
21. Lykkesfeldt J, (2012) Ascorbate and dehydroascorbic acid as biomarkers of oxidative stress: validity of clinical data depends on vacutainer system used. Nutr Res 32: 66-9.
22. Dalm S, Grootendorst J, de Kloet ER, Oitzl MS, (2000) Quantification of swim patterns in the Morris water maze. Behav Res Methods Instrum Comput 32: 134-9.
23. Dringenberg HC, Richardson DP, Brien JF, Reynolds JN, (2001) Spatial learning in the guinea pig: cued versus non-cued learning, sex differences, and comparison with rats. Behavioural Brain Research 124: 97-101.
24. Vorhees CV, Williams MT, (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1: 848-58.
25. Morris RGM, (1981) Spatial Localization Does Not Require the Presence of Local Cues. Learning and Motivation 12: 239-60.
26. Schenk F, Morris RGM, (1985) Dissociation Between Components of Spatial Memory in Rats After Recovery from the Effects of Retrohippocampal Lesions. Experimental Brain Research 58: 11-28.
27. Morris R, (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11: 47-60.
28. Lykkesfeldt J, (2000) 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. Anal Biochem 282: 89-93.
29. Lykkesfeldt J, (2007) Ascorbate and dehydroascorbic acid as reliable biomarkers of oxidative stress: analytical reproducibility and long-term stability of plasma samples subjected to acidic deproteinization. Cancer Epidemiol Biomarkers Prev 16: 2513-6.
30. Rapisarda C, Bacchelli B, (1977) The brain of the guinea pig in stereotaxic coordinates. Arch Sci Biol (Bologna) 61: 1-37.
31. Sury MD, Agarinis C, Widmer HR, Leib SL, Christen S, (2008) JNK is activated but does not mediate hippocampal neuronal apoptosis in experimental neonatal pneumococcal meningitis. Neurobiol Dis 32: 142-50.
32. Tang X, Falls DL, Li X, Lane T, Luskin MB, (2007) Antigen-retrieval procedure for bromodeoxyuridine immunolabeling with concurrent labeling of nuclear DNA and antigens damaged by HCl pretreatment. J Neurosci 27: 5837-44.
33. Lykkesfeldt J, (2002) 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 36: 567-74.
34. Frikke-Schmidt H, Tveden-Nyborg P, Birck MM, Lykkesfeldt J, (2011) High dietary fat and cholesterol exacerbates chronic vitamin C deficiency in guinea pigs. Br J Nutr 105: 54-61.
35. Rakipovski G, Raun K, Lykkesfeldt J, (2011) Fluctuating hyperglycaemia increases oxidative stress response in lean rats compared to sustained hyperglycaemia despite lower glycaemic exposure. Diab Vasc Dis Res 8: 295-8.
36. Norkus EP, Bassi J, Rosso P, (1979) Maternal-fetal transfer of ascorbic acid in the guinea pig. J Nutr 109: 2205-12.
37. Rajan DP, Huang W, Dutta B, Devoe LD, Leibach FH, et al. (1999) Human placental sodium-dependent vitamin C transporter (SVCT2): molecular cloning and transport function. Biochem Biophys Res Commun 262: 762-8.
38. Prasad PD, Huang W, Wang H, Leibach FH, Ganapathy V, (1998) Transport mechanisms for vitamin C in the JAR human placental choriocarcinoma cell line. Biochim Biophys Acta 1369: 141-51.
39. Wolf H, Grunwald M, Kruggel F, Riedel-Heller SG, Angerhofer S, et al. (2001) Hippocampal volume discriminates between normal cognition; questionable and mild dementia in the elderly. Neurobiol Aging 22: 177-86.
40. Yucel M, Solowij N, Respondek C, Whittle S, Fornito A, et al. (2008) Regional brain abnormalities associated with long-term heavy cannabis use. Arch Gen Psychiatry 65: 694-701.
41. Hollander dB, Schouw M, Groot P, Huisman H, Caan M, et al. (2012) Preliminary evidence of hippocampal damage in chronic users of ecstasy. J Neurol Neurosurg Psychiatry 83: 83-5.
42. Smith AD, Refsum H, (2009) Vitamin B-12 and cognition in the elderly. Am J Clin Nutr 89: 707S-11S.
43. Harrison FE, May JM, (2009) Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic Biol Med 46: 719-30.
44. 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.
45. 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.
46. Norkus EP, Rosso P, (1981) Effects of maternal intake of ascorbic acid on the postnatal metabolism of this vitamin in the guinea pig. J Nutr 111: 624-30.
47. Norkus EP, Rosso P, (1975) Changes in ascorbic acid metabolism of the offspring following high maternal intake of this vitamin in the pregnant guinea pig. Ann N Y Acad Sci 258: 401-9.
48. Isaacs EB, Lucas A, Chong WK, Wood SJ, Johnson CL, et al. (2000) Hippocampal volume and everyday memory in children of very low birth weight. Pediatr Res 47: 713-20.
49. Thompson DK, Wood SJ, Doyle LW, Warfield SK, Lodygensky GA, et al. (2008) Neonate hippocampal volumes: prematurity, perinatal predictors, and 2-year outcome. Ann Neurol 63: 642-51.
50. Mallard EC, Rehn A, Rees S, Tolcos M, Copolov D, (1999) Ventriculomegaly and reduced hippocampal volume following intrauterine growth-restriction: implications for the aetiology of schizophrenia. Schizophr Res 40: 11-21.
51. Sapolsky RM, (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57: 925-35.
52. Tveden-Nyborg P, Lykkesfeldt J, (2009) Does vitamin C deficiency result in impaired brain development in infants? Redox Rep 14: 2-6.