Effect of vitamin C deficiency during postnatal development on adult behavior: Functional phenotype of Gulo(-/-) knockout mice

Genes, Brain and Behavior

Volumn 11, Issue 3, 2012, Pages 269-277

  Chen, Y ^a,b   Curran, C P ^a,c   Nebert, D W ^a   Patel, K V ^a   Williams, M T ^a   Vorhees, C V ^a,c  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c NORTHERN KENTUCKY UNIVERSITY   (United States)

Author keywords

Acoustic startle response; Ascorbic acid; Elevated zero maze; L gulono lactone oxidase; Locomotor activity; Methamphetamine challenge; Morris water maze; Novel object recognition; Oxidative stress in brain; Vitamin C

Indexed keywords

ASCORBIC ACID; DRINKING WATER; METHAMPHETAMINE;

ABNORMAL BEHAVIOR; ADULT BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; ASCORBIC ACID DEFICIENCY; BEHAVIOR; BRAIN DYSFUNCTION; BRAIN LEVEL; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE SEVERITY; FEMALE; HYPERACTIVITY; KNOCKOUT MOUSE; MOTOR DYSFUNCTION; MOUSE; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SENSORIMOTOR NEUROPATHY; SENSORY GATING; VITAMIN SUPPLEMENTATION;

ANIMALS; ANIMALS, NEWBORN; ASCORBIC ACID; ASCORBIC ACID DEFICIENCY; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FEMALE; L-GULONOLACTONE OXIDASE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; PREGNANCY;

ANIMALIA; GULO; MUS; PRIMATES;

EID: 84862789281     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2011.00762.x     Document Type: Article

References (51)

1. Amaro, S., Planas, A.M. & Chamorro, A. (2008) Uric acid administration in patients with acute stroke: a novel approach to neuroprotection. Expert Rev Neurother 8, 259-270.
2. Bailey, K.R., Rustay, N.R. & Crawley, J.N. (2006) Behavioral phenotyping of transgenic and knockout mice: practical concerns and potential pitfalls. ILAR J 47, 124-131.
3. Branchi, I., Bichler, Z., Berger-Sweeney, J. & Ricceri, L. (2003) Animal models of mental retardation: from gene to cognitive function. Neurosci Biobehav Rev 27, 141-153.
4. Clark, R.E., Zola, S.M. & Squire, L.R. (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20, 8853-8860.
5. Clarke, M.W., Burnett, J.R. & Croft, K.D. (2008) Vitamin E in human health and disease. Crit Rev Clin Lab Sci 45, 417-450.
6. Crawley, J.N. (1999) Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res 835, 18-26.
7. Crawley, J.N. (2000) What's wrong with my mouse? Behavioral phenotyping of transgenic and knockout mice. Wiley-Liss, New York.
8. Crawley, J.N. (2007) What's wrong with my mouse? Behavioral phenotyping of transgenic and knockout mice. John Wiley & Sons, Hoboken, NJ.
9. Curran, C.P., Nebert, D.W., Genter, M.B., Patel, K.V., Schaefer, T.L., Skelton, M.R., Williams, M.T. & Vorhees, C.V. (2011) In utero and lactational exposure to PCBs in mice: adult offspring show altered learning and memory depending on Cyp1a2 and Ahr genotypes. Environ Health Perspect 119, 1286-1293.
10. Dalton, T.P., Chen, Y., Schneider, S.N., Nebert, D.W. & Shertzer, H.G. (2004) Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic Biol Med 37, 1511-1526.
11. De Araujo, D.P., Lobato, R.F., Cavalcanti, J.R., Sampaio, L.R., Araujo, P.V., Silva, M.C., Neves, K.R., Fonteles, M.M., Sousa, F.C. & Vasconcelos, S.M. (2011) Contributions of antioxidant activity of lipoic acid in reducing neurogenerative progression of Parkinson's disease: a review. Int J Neurosci 121, 51-57.
12. Dhanasekaran, M. & Ren, J. (2005) The emerging role of coenzyme Q-10 in aging, neurodegeneration, cardiovascular disease, cancer and diabetes mellitus. Curr Neurovasc Res 2, 447-459.
13. Diliberto, E.J. Jr & Allen, P.L. (1981) Mechanism of dopamine β-hydroxylation: semidehydroascorbate as the enzyme oxidation product of ascorbate. J Biol Chem 256, 3385-3393.
14. Englard, S. & Seifter, S. (1986) The biochemical functions of ascorbic acid. Annu Rev Nutr 6, 365-406.
15. Harrison, F.E. & May, J.M. (2009) Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic Biol Med 46, 719-730.
16. Harrison, F.E., Yu, S.S., Van Den Bossche, K.L., Li, L., May, J.M. & McDonald, M.P. (2008) Elevated oxidative stress and sensorimotor deficits but normal cognition in mice that cannot synthesize ascorbic acid. J Neurochem 106, 1198-1208.
17. Harrison, F.E., Meredith, M.E., Dawes, S.M., Saskowski, J.L. & May, J.M. (2010) Low ascorbic acid and increased oxidative stress in Gulo(-/-) mice during development. Brain Res 1349, 143-152.
18. Hornig, D. (1975) Distribution of ascorbic acid, metabolites and analogues in man and animals. Ann NY Acad Sci 258, 103-118.
19. Hultqvist, M., Olsson, L.M., Gelderman, K.A. & Holmdahl, R. (2009) The protective role of ROS in autoimmune disease. Trends Immunol 30, 201-208.
20. Hur, W. & Gray, N.S. (2011) Small-molecule modulators of antioxidant response pathway. Curr Opin Chem Biol 15, 162-173.
21. Jones, D.P. (2006) Redefining oxidative stress. Antioxid Redox Signal 8, 1865-1879.
22. Kiyatkin, E.A. & Rebec, G.V. (1998) Ascorbate modulates glutamate-induced excitations of striatal neurons. Brain Res 812, 14-22.
23. Luthra, P.M., Barodia, S.K. & Raghubir, R. (2009) Antagonism of haloperidol-induced swim impairment in L-DOPA and caffeine treated mice: a pre-clinical model to study Parkinson's disease. J Neurosci Methods 178, 284-290.
24. MacQueen, G.M., Ramakrishnan, K., Croll, S.D., Siuciak, J.A., Yu, G., Young, L.T. & Fahnestock, M. (2001) Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression. Behav Neurosci 115, 1145-1153.
25. Maeda, N., Hagihara, H., Nakata, Y., Hiller, S., Wilder, J. & Reddick, R. (2000) Aortic wall damage in mice unable to synthesize ascorbic acid. Proc Natl Acad Sci USA 97, 841-846.
26. Mark, K.A., Soghomonian, J.J. & Yamamoto, B.K. (2004) High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J Neurosci 24, 11449-11456.
27. Mark, K.A., Quinton, M.S., Russek, S.J. & Yamamoto, B.K. (2007) Dynamic changes in vesicular glutamate transporter-1 function and expression related to methamphetamine-induced glutamate release. J Neurosci 27, 6823-6831.
28. Meister, A. (1994) Glutathione, ascorbate, and cellular protection. Cancer Res 54, 1969s-1975s.
29. Meredith, M.E., Harrison, F.E. & May, J.M. (2011) Differential regulation of the ascorbic acid transporter SVCT2 during development and in response to ascorbic acid depletion. Biochem Biophys Res Commun 414, 737-742.
30. Nishikimi, M., Fukuyama, R., Minoshima, S., Shimizu, N. & Yagi, K. (1994) Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-γ-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J Biol Chem 269, 13685-13688.
31. Obulesu M., Dowlathabad M.R. & Bramhachari P.V. 2011 Carotenoids and Alzheimer disease: an insight into therapeutic role of retinoids in animal models. Neurochem Int 59, 535-541.
32. Oria, R.B., Costa, C.M., Santos, T.J. & Vieira, C.M. (2003) Pharmacological, morphological, and behavioral analysis of motor impairment in experimentally vitamin C-deficient guinea pigs. Arq Neuropsiquiatr 61, 25-33.
33. Packer, L. & Cadenas, E. (2011) Lipoic acid: energy metabolism and redox regulation of transcription and cell signaling. J Clin Biochem Nutr 48, 26-32.
34. Paylor, R., Spencer, C.M., Yuva-Paylor, L.A. & Pieke-Dahl, S. (2006) The use of behavioral test batteries, II: effect of test interval. Physiol Behav 87, 95-102.
35. Rebec, G.V., Witowski, S.R., Sandstrom, M.I., Rostand, R.D. & Kennedy, R.T. (2005) Extracellular ascorbate modulates cortically-evoked glutamate dynamics in rat striatum. Neurosci Lett 378, 166-170.
36. Reiter, R.J., Manchester, L.C. & Tan, D.X. (2010) Neurotoxicants: free-radical mechanisms and melatonin protection. Curr Neuropharmacol 8, 194-210.
37. 2, a necessary evil for cell signaling. Science 312, 1882-1883.
38. Runchel, C., Matsuzawa, A. & Ichijo, H. (2011) Mitogen-activated protein kinases in mammalian oxidative stress responses. Antioxid Redox Signal 15, 205-218.
39. Senft, A.P., Dalton, T.P. & Shertzer, H.G. (2000) Determining glutathione and glutathione disulfide using the fluorescence probe o-phthalaldehyde. Anal Biochem 280, 80-86.
40. Shepherd, J.K., Grewal, S.S., Fletcher, A., Bill, D.J., & Dourish, C.T. (1994) Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology 116, 56-64.
41. Stephans, S.E. & Yamamoto, B.K. (1994) Methamphetamine-induced neurotoxicity: roles for glutamate and dopamine efflux. Synapse 17, 203-209.
42. Stuchlik, A., Rehakova, L., Telensky, P. & Vales, K. (2007) Morris water maze learning in Long-Evans rats is differentially affected by blockade of D1-like and D2-like dopamine receptors. Neurosci Lett 422, 169-174.
43. Tamasy, V., Koranyi, L. & Phelps, C.P. (1981) The role of dopaminergic and serotonergic mechanisms in the development of swimming ability of young rats. Dev Neurosci 4, 389-400.
44. 1H NMR spectroscopy. NMR Biomed 23, 1038-1043.
45. +-dependent L-ascorbic acid transporters. Nature 399, 70-75.
46. Tveden-Nyborg, P., Johansen, L.K., Raida, Z., Villumsen, C.K., Larsen, J.O. & Lykkesfeldt, J. (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, 540-546.
47. van den Bos, R. & Cools, A.R. (2003) Switching to cue-directed behavior: specific for ventral striatal dopamine but not ventral pallidum/substantia innominata GABA as revealed by a swimming-test procedure in rats. Neuroscience 118, 1141-1149.
48. Vorhees, C.V. (1996) Design considerations in the use of behavioral test batteries for the detection of CNS dysfunction in laboratory animals. Ment Retard Dev Dis Res Rev 2, 227-233.
49. Vorhees, C.V. (1997) Methods for detecting long-term CNS dysfunction after prenatal exposure to neurotoxicants. Drug Chem Toxicol 20, 387-399.
50. Vorhees, C.V. & Williams, M.T. (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1, 848-858.
51. Zannoni, V., Lynch, M., Goldstein, S. & Sato, P. (1974) A rapid micromethod for the determination of ascorbic acid in plasma and tissues. Biochem Med 11, 41-48.