High-dose of vitamin C supplementation reduces amyloid plaque burden and ameliorates pathological changes in the brain of 5XFAD mice

Cell Death and Disease

Volumn 5, Issue 2, 2014, Pages

  Kook, S Y ^a   Lee, K M ^a   Kim, Y ^a   Cha, M Y ^a   Kang, S ^a   Baik, S H ^a   Lee, H ^a   Park, R ^a   Mook Jung, I ^a  

^a Seoul National University College of Medicine   (South Korea)

Author keywords

apoptosis; Bak; H1.2 CTD; linker histone; PKC

Indexed keywords

ASCORBIC ACID; GULONOLACTONE OXIDASE;

5XFAD MOUSE; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN MITOCHONDRION; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG DOSE COMPARISON; DRUG MEGADOSE; FEMALE; GLIOSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MORPHOLOGY; MOUSE; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; VITAMIN BLOOD LEVEL;

ALZHEIMER DISEASE; ANIMALS; ASCORBIC ACID; BLOOD-BRAIN BARRIER; CAPILLARIES; CEREBRAL CORTEX; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FEMALE; GLIOSIS; HIPPOCAMPUS; L-GULONOLACTONE OXIDASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MITOCHONDRIA; PLAQUE, AMYLOID; TIGHT JUNCTIONS;

EID: 84896778095     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.26     Document Type: Article

References (57)

1. Ellis RJ, Olichney JM, Thal LJ, Mirra SS, Morris JC, Beekly D et al. Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: The CERAD experience, Part XV. Neurology 1996; 46: 1592-1596.
2. Baloyannis SJ. Mitochondrial alterations in Alzheimer's disease. J Alzheimer's Dis 2006; 9 126.
3. Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr 2000; 71: 621S-629S.
4. Perry G, Nunomura A, Hirai K, Takeda A, Aliev G, Smith MA. Oxidative damage in Alzheimer's disease: The metabolic dimension. Int J Dev Neurosci 2000; 18: 417-421.
5. Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K et al. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc Natl Acad Sci USA 2004; 101: 2070-2075.
6. Andersen JK. Oxidative stress in neurodegeneration: Cause or consequence? Nat Med 2004; 10(Suppl)): S18-S25.
7. Harrison FE, Hosseini AH, McDonald MP, May JM. Vitamin C reduces spatial learning deficits in middle-Aged and very old APP/PSEN1 transgenic and wild-Type mice. Pharmacol Biochem Behav 2009; 93: 443-450.
8. Murakami K, Murata N, Ozawa Y, Kinoshita N, Irie K, Shirasawa T et al. Vitamin C restores behavioral deficits and amyloid-beta oligomerization without affecting plaque formation in a mouse model of Alzheimer's disease. J Alzheimer's Dis 2011; 26: 7-18.
9. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J et al. Intraneuronal beta-Amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: Potential factors in amyloid plaque formation. J Neurosci 2006; 26: 10129-10140.
10. Sotiriou S, Gispert S, Cheng J, Wang Y, Chen A, Hoogstraten-Miller S et al. Ascorbic-Acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat Med 2002; 8: 514-517.
11. Charlton KE, Rabinowitz TL, Geffen LN, Dhansay MA. Lowered plasma vitamin C, but not vitamin E, concentrations in dementia patients. J Nutr Health Aging 2004; 8: 99-107.
12. Lin JL, Huang YH, Shen YC, Huang HC, Liu PH. Ascorbic acid prevents blood-brain barrier disruption and sensory deficit caused by sustained compression of primary somatosensory cortex. J Cereb Blood Flow Metab 2010; 30: 1121-1136.
13. Feuring M, Schultz A, Long-Term Hersemeyer K. High intake of vitamin C decreases size and increases quantity of liver mitochondria in Guinea-pigs. J Int Med Res 2011; 39 2334.
14. Claudio L. Ultrastructural features of the blood-brain barrier in biopsy tissue from Alzheimer's disease patients. Acta Neuropathol 1996; 91: 6-14.
15. Heyman A, Fillenbaum GG, Welsh-Bohmer KA, Gearing M, Mirra SS, Mohs RC et al. Cerebral infarcts in patients with autopsy-proven Alzheimer's disease: CERAD, part XVIII. Consortium to Establish a Registry for Alzheimer's Disease. Neurology 1998; 51: 159-162.
16. Carr AC, Frei B. Toward a new recommended dietary allowance for vitamin C based on antioxidant and health effects in humans. Am J Clin Nutr 1999; 69: 1086-1107.
17. Nandi A, Mukhopadhyay CK, Ghosh MK, Chattopadhyay DJ, Chatterjee IB. Evolutionary significance of vitamin C biosynthesis in terrestrial vertebrates. Free Radic Biol Med 1997 1047-1054.
18. Moon M, Hong HS, Nam DW, Baik SH, Song H, Kook SY et al. Intracellular amyloid-beta accumulation in calcium-binding protein-deficient neurons leads to amyloid-beta plaque formation in animal model of Alzheimer's disease. J Alzheimers Dis 2012; 29: 615-628.
19. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica 1991; 82: 239-259.
20. Kook SY, Hong HS, Moon M, Ha CM, Chang S, Mook-Jung I. Abeta(1)(-)(4)(2)-RAGE interaction disrupts tight junctions of the blood-brain barrier via Ca(2)(+)-calcineurin signaling. J Neurosci 2012; 32: 8845-8854.
21. Kalaria RN. The blood-brain barrier and cerebrovascular pathology in Alzheimer's disease. Ann N Y Acad Sci 1999; 893: 113-125.
22. Schreibelt G, Kooij G, Reijerkerk A, van Doorn R, Gringhuis SI, van der Pol S et al. Reactive oxygen species alter brain endothelial tight junction dynamics via RhoA, PI3 kinase, and PKB signaling. FASEB J 2007; 21: 3666-3676.
23. Abbott NJ. Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 2002; 200: 629-638.
24. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.
25. Goodenough DA, Revel JP. A fine structural analysis of intercellular junctions in the mouse liver. J Cell Biol 1970; 45: 272-290.
26. Hong HS, Hwang JY, Son SM, Kim YH, Moon M, Inhee MJ. FK506 reduces amyloid plaque burden and induces MMP-9 in AbetaPP/PS1 double transgenic mice. J Alzheimers Dis 2010; 22: 97-105.
27. Manczak M, Mao P, Calkins MJ, Cornea A, Reddy AP, Murphy MP et al. Mitochondriatargeted antioxidants protect against amyloid-beta toxicity in Alzheimer's disease neurons. J Alzheimers Dis 2010; 20(Suppl 2)): S609-S631.
28. Eckert A, Hauptmann S, Scherping I, Rhein V, Muller-Spahn F, Gotz J et al. Soluble betaamyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice. Neurodegener Dis 2008; 5: 157-159.
29. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 2006; 26: 9057-9068.
30. Cha MY, Han SH, Son SM, Hong HS, Choi YJ, Byun J et al. Mitochondria-specific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death. PLoS One 2012; 7: E34929.
31. Medina S, Martinez M, Hernanz A. Antioxidants inhibit the human cortical neuron apoptosis induced by hydrogen peroxide, tumor necrosis factor alpha, dopamine and beta-Amyloid peptide 1-42. Free Rad Res 2002; 36: 1179-1184.
32. Rosales-Corral S, Tan DX, Reiter RJ, Valdivia-Velazquez M, Martinez-Barboza G, Acosta-Martinez JP et al. Orally administered melatonin reduces oxidative stress and proinflammatory cytokines induced by amyloid-beta peptide in rat brain: A comparative, in vivo study versus vitamin C and E. J Pineal Res 2003; 35: 80-84.
33. Wagner GC, Carelli RM, Jarvis MF. Ascorbic acid reduces the dopamine depletion induced by methamphetamine and the 1-methyl-4-phenyl pyridinium ion. Neuropharmacology 1986; 25: 559-561.
34. Rebec GV, Barton SJ, Marseilles AM, Collins K. Ascorbate treatment attenuates the Huntington behavioral phenotype in mice. Neuroreport 2003; 14: 1263-1265.
35. Heo JH, Hyon L, Lee KM. The possible role of antioxidant vitamin C in Alzheimer's disease treatment and prevention. Am J Alzheimer's Dis Other Demen 2013; 28: 120-125.
36. Harrison FE, Allard J, Bixler R, Usoh C, Li L, May JM et al. Antioxidants and cognitive training interact to affect oxidative stress and memory in APP/PSEN1 mice. Nutr Neurosci 2009; 12: 203-218.
37. Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci 2005; 25: 3032-3040.
38. Harrison FE, May JM. Vitamin C function in the brain: Vital role of the ascorbate transporter SVCT2. Free Rad Biol Med 2009; 46: 719-730.
39. Carrano A, Hoozemans JJ, van der Vies SM, Rozemuller AJ, van Horssen J, de Vries HE. Amyloid Beta induces oxidative stress-mediated blood-brain barrier changes in capillary amyloid angiopathy. Antioxid Redox Signal 2011; 15: 1167-1178.
40. Enciu AM, Gherghiceanu M, Popescu BO. Triggers and effectors of oxidative stress at blood-brain barrier level: Relevance for brain ageing and neurodegeneration. Oxid Med Cell Longev 2013; 2013: 297512.
41. Pratico D. Alzheimer's disease and oxygen radicals: New insights. Biochem Pharmacol 2002; 63: 563-567.
42. Montine TJ, Neely MD, Quinn JF, Beal MF, Markesbery WR, Roberts LJ et al. Lipid peroxidation in aging brain and Alzheimer's disease. Free Rad Biol Med 2002; 33 626.
43. Riviere S, Birlouez-Aragon I, Nourhashemi F, Vellas B. Low plasma vitamin C in Alzheimer patients despite an adequate diet. Int J Geriatr Psychiatry 1998; 13: 749-754.
44. Schippling S, Kontush A, Arlt S, Buhmann C, Sturenburg HJ, Mann U et al. Increased lipoprotein oxidation in Alzheimer's disease. Free Rad Biol Med 2000; 28: 351-360.
45. Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, Giliberto L et al. Oxidative stress activates a positive feedback between the gamma-And beta-secretase cleavages of the beta-Amyloid precursor protein. J Neurochem 2008; 104: 683-695.
46. Strazielle N, Ghersi-Egea JF, Ghiso J, Dehouck MP, Frangione B, Patlak C et al. In vitro evidence that beta-Amyloid peptide 1-40 diffuses across the blood-brain barrier and affects its permeability. J Neuropathol Exp Neurol 2000; 59: 29-38.
47. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA. Involvement of oxidative stress in Alzheimer disease. J Neuropathol Exp Neurol 2006; 65: 631-641.
48. Bogdanovic N, Zilmer M, Zilmer K, Rehema A, Karelson E. The Swedish APP670/671 Alzheimer's disease mutation: The first evidence for strikingly increased oxidative injury in the temporal inferior cortex. Dement Geriatr Cogn Disord 2001; 12: 364-370.
49. Zhu X, Smith MA, Perry G, Aliev G. Mitochondrial failures in Alzheimer's disease. Am J Alzheimers Dis Other Demen 2004; 19: 345-352.
50. Kc S, Carcamo JM, Golde DW. Vitamin C enters mitochondria via facilitative glucose transporter 1 (Glut1) and confers mitochondrial protection against oxidative injury. FASEB J 2005; 19: 1657-1667.
51. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: Machineries and mechanisms. Cell 2009; 138: 628-644.
52. Seelert H, Dani DN, Dante S, Hauss T, Krause F, Schafer E et al. From protons to OXPHOS supercomplexes and Alzheimer's disease: Structure-dynamics- function relationships of energy-Transducing membranes. Biochimica et Biophysica Acta 2009 657-671.
53. Chan DC. Mitochondria: Dynamic organelles in disease, aging, and development. Cell 2006; 125: 1241-1252.
54. Li Z, Okamoto K, Hayashi Y, Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004; 119: 873-887.
55. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005; 47: 365-378.
56. Kim H, Bae S, Yu Y, Kim Y, Kim HR, Hwang YI et al. The analysis of vitamin C concentration in organs of gulo(-/-) mice upon vitamin C withdrawal. Immune Netw 2012; 12: 18-26.
57. Franklin KB, Paxions G. The Mouse Brain in Stereotaxic Coordinates. Academic Press: San Diego, CA, USA, 1997.