Vitamin E: Curse or benefit in Alzheimer’s disease? A systematic investigation of the impact of α-, γ- and δ-tocopherol on Aβ generation and degradation in neuroblastoma cells

Journal of Nutrition, Health and Aging

Volumn 19, Issue 6, 2015, Pages 646-654

  Grimm, Marcus O W ^a,c   Stahlmann, C P ^a   Mett, J ^a   Haupenthal, V J ^a   Zimmer, V C ^a   Lehmann, J ^a   Hundsdorfer B ^a   Endres, K ^b   Grimm, H S ^a   Hartmann, T ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c NONE   (Germany)

Author keywords

Alzheimer s disease; Amyloid ; A degradation; Tocopherol; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; AMYLOID BETA PROTEIN; BETA ACTIN; BETA SECRETASE; DELTA TOCOPHEROL; GAMMA SECRETASE; GAMMA TOCOPHEROL; LACTATE DEHYDROGENASE; NICASTRIN; PRESENILIN 1; PRESENILIN 2; ANTIOXIDANT; DELTA-TOCOPHEROL; INSULINASE; SECRETASE; TOCOPHEROL;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL VIABILITY; ENDOSOME; ENZYME ACTIVITY; HUMAN; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; WESTERN BLOTTING; AMYLOIDOSIS; BIOSYNTHESIS; CHEMICALLY INDUCED; DRUG EFFECTS; LIPID PEROXIDATION; METABOLISM; NEUROBLASTOMA; TUMOR CELL LINE;

ALPHA-TOCOPHEROL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; AMYLOIDOSIS; ANTIOXIDANTS; CELL LINE, TUMOR; GAMMA-TOCOPHEROL; HUMANS; INSULYSIN; LIPID PEROXIDATION; NEUROBLASTOMA; PROTEOLYSIS; TOCOPHEROLS;

EID: 84938344172     PISSN: 12797707     EISSN: 17604788     Source Type: Journal    
DOI: 10.1007/s12603-015-0506-z     Document Type: Article

References (70)

1. Tabet N, Birks J, and Grimley Evans J. Vitamin E for Alzheimer’s disease. Cochrane Database Syst Rev 2000, CD002854.
2. Netscher T. Synthesis of vitamin E. Vitam Horm 2007;76, 155–202.
3. Rigotti A. Absorption, transport, and tissue delivery of vitamin E. Mol Aspects Med 2007;28, 423–36.
4. Banks R, Speakman JR, and Selman C. Vitamin E supplementation and mammalian lifespan. Mol Nutr Food Res 54, 719–25.
5. Wagner KH, Kamal-Eldin A, and Elmadfa I. Gamma-tocopherol—an underestimated vitamin? Ann Nutr Metab 2004;48, 169–88.
6. Vatassery GT, Bauer T, and Dysken M. High doses of vitamin E in the treatment of disorders of the central nervous system in the aged. Am J Clin Nutr 1999;70, 793–801.
7. Pitchumoni SS and Doraiswamy PM. Current status of antioxidant therapy for Alzheimer’s Disease. J Am Geriatr Soc 1998;46, 1566–72.
8. Meydani M. Vitamin E. Lancet 1995;345, 170–5.
9. Grundman M. Vitamin E and Alzheimer disease: the basis for additional clinical trials. Am J Clin Nutr 2000;71, 630S-6S.
10. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, and Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci U S A 1985;82, 4245–9.
11. Haass C. Take five—BACE and the gamma-secretase quartet conduct Alzheimer’s amyloid beta-peptide generation. EMBO J 2004;23, 483–8.
12. Zinser EG, Hartmann T, and Grimm MO. Amyloid beta-protein and lipid metabolism. Biochim Biophys Acta 2007;1768, 1991–2001.
13. Grimm MO, Grimm HS, Tomic I, Beyreuther K, Hartmann T, and Bergmann C. Independent inhibition of Alzheimer disease beta- and gamma-secretase cleavage by lowered cholesterol levels. J Biol Chem 2008;283, 11302–11.
14. Grimm MO, Grosgen S, Riemenschneider M, Tanila H, Grimm HS, and Hartmann T. From brain to food: analysis of phosphatidylcholins, lyso-phosphatidylcholins and phosphatidylcholin-plasmalogens derivates in Alzheimer’s disease human post mortem brains and mice model via mass spectrometry. J Chromatogr A 2011;1218, 7713–22.
15. Grimm MO, Kuchenbecker J, Grosgen S, Burg VK, Hundsdorfer B, Rothhaar TL et al. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J Biol Chem 2011;286, 14028–39.
16. Grimm MO, Rothhaar TL, Grosgen S, Burg VK, Hundsdorfer B, Haupenthal VJ et al. Trans fatty acids enhance amyloidogenic processing of the Alzheimer amyloid precursor protein (APP). J Nutr Biochem 2012;23, 1214–23.
17. Burg VK, Grimm HS, Rothhaar TL, Grosgen S, Hundsdorfer B, Haupenthal VJ et al. Plant sterols the better cholesterol in Alzheimer’s disease? A mechanistical study. J Neurosci 2013;33, 16072–87.
18. Grimm MO, Haupenthal VJ, Rothhaar TL, Zimmer VC, Grosgen S, Hundsdorfer B et al. Effect of Different Phospholipids on alpha-Secretase Activity in the Non-Amyloidogenic Pathway of Alzheimer’s Disease. Int J Mol Sci 2013;14, 5879–98.
19. Rothhaar TL, Grosgen S, Haupenthal VJ, Burg VK, Hundsdorfer B, Mett J et al. Plasmalogens inhibit APP processing by directly affecting gamma-secretase activity in Alzheimer’s disease. Scientific World Journal 2012, 141240.
20. Butterfield DA, Hensley K, Harris M, Mattson M, and Carney J. beta-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer’s disease. Biochem Biophys Res Commun 1994;200, 710–5.
21. Meda L, Cassatella MA, Szendrei GI, Otvos L, Jr., Baron P, Villalba M et al. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 1995;374, 647–50.
22. Zoeller RA, Morand OH, and Raetz CR. A possible role for plasmalogens in protecting animal cells against photosensitized killing. J Biol Chem 1988;263, 11590–6.
23. Kamal-Eldin A and Appelqvist LA. The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 1996;31, 671–701.
24. Kontush K and Schekatolina S. Vitamin E in neurodegenerative disorders: Alzheimer’s disease. Ann N Y Acad Sci 2004;1031, 249–62.
25. Roy S, Lado BH, Khanna S, and Sen CK. Vitamin E sensitive genes in the developing rat fetal brain: a high-density oligonucleotide microarray analysis. FEBS Lett 2002;530, 17–23.
26. Rota C, Rimbach G, Minihane AM, Stoecklin E, and Barella L. Dietary vitamin E modulates differential gene expression in the rat hippocampus: potential implications for its neuroprotective properties. Nutr Neurosci 2005;8, 21–9.
27. Grimm HS, Beher D, Lichtenthaler SF, Shearman MS, Beyreuther K, and Hartmann T. gamma-Secretase cleavage site specificity differs for intracellular and secretory amyloid beta. J Biol Chem 2003;278, 13077–85.
28. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985;150, 76–85.
29. Ida N, Hartmann T, Pantel J, Schroder J, Zerfass R, Forstl H et al. Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J Biol Chem 1996;271, 22908–14.
30. Livak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25, 402–8.
31. Rohan de Silva HA, Jen A, Wickenden C, Jen LS, Wilkinson SL, and Patel AJ. Cell-specific expression of beta-amyloid precursor protein isoform mRNAs and proteins in neurons and astrocytes. Brain Res Mol Brain Res 1997;47, 147–56.
32. Burton GW and Traber MG. Vitamin E: antioxidant activity, biokinetics, and bioavailability. Annu Rev Nutr 1990;10, 357–82.
33. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, and Selkoe DJ. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 1999;398, 513–7.
34. De Strooper B. Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 2003;38, 9–12.
35. Ahn K, Shelton CC, Tian Y, Zhang X, Gilchrist ML, Sisodia SS et al. Activation and intrinsic gamma-secretase activity of presenilin 1. Proc Natl Acad Sci U S A 2010;107, 21435–40.
36. Herreman A, Serneels L, Annaert W, Collen D, Schoonjans L, and De Strooper B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat Cell Biol 2000;2, 461–2.
37. Shirotani K, Edbauer D, Prokop S, Haass C, and Steiner H. Identification of distinct gamma-secretase complexes with different APH-1 variants. J Biol Chem 2004;279, 41340–5.
38. Meckler X and Checler F. Visualization of Specific gamma-Secretase Complexes using Bimolecular Fluorescence Complementation. J Alzheimers Dis 2014;40, 161–76.
39. Sinha S and Lieberburg I. Cellular mechanisms of beta-amyloid production and secretion. Proc Natl Acad Sci U S A 1999;96, 11049–53.
40. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P et al. Beta-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999;286, 735–41.
41. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL et al. BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat Neurosci 2001;4, 233–4.
42. Huse JT, Liu K, Pijak DS, Carlin D, Lee VM, and Doms RW. Beta-secretase processing in the trans-Golgi network preferentially generates truncated amyloid species that accumulate in Alzheimer’s disease brain. J Biol Chem 2002;277, 16278–84.
43. Vassar R, Kovacs DM, Yan R, and Wong PC. The beta-secretase enzyme BACE in health and Alzheimer’s disease: regulation, cell biology, function, and therapeutic potential. J Neurosci 2009;29, 12787–94.
44. Eckman EA and Eckman CB. Abeta-degrading enzymes: modulators of Alzheimer’s disease pathogenesis and targets for therapeutic intervention. Biochem Soc Trans 2005;33, 1101–5.
45. Kurochkin IV and Goto S. Alzheimer’s beta-amyloid peptide specifically interacts with and is degraded by insulin degrading enzyme. FEBS Lett 1994;345, 33–7.
46. Qiu WQ, Walsh DM, Ye Z, Vekrellis K, Zhang J, Podlisny MB et al. Insulin-degrading enzyme regulates extracellular levels of amyloid beta-protein by degradation. J Biol Chem 1998;273, 32730–8.
47. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP et al. Metabolic regulation of brain Abeta by neprilysin. Science 2001;292, 1550–2.
48. Hersh LB and Rodgers DW. Neprilysin and amyloid beta peptide degradation. Curr Alzheimer Res 2008;5, 225–31.
49. Grimm MO, Mett J, Stahlmann CP, Haupenthal VJ, Zimmer VC, and Hartmann T. Neprilysin and Abeta Clearance: Impact of the APP Intracellular Domain in NEP Regulation and Implications in Alzheimer’s Disease. Front Aging Neurosci 2013;5, 98.
50. Azzi A, Gysin R, Kempna P, Munteanu A, Negis Y, Villacorta L et al. Vitamin E mediates cell signaling and regulation of gene expression. Ann N Y Acad Sci 2004;1031, 86–95.
51. Campbell SE, Stone WL, Whaley SG, Qui M, and Krishnan K. Gamma (gamma) tocopherol upregulates peroxisome proliferator activated receptor (PPAR) gamma (gamma) expression in SW 480 human colon cancer cell lines. BMC Cancer 2003;3, 25.
52. Li-Weber M, Weigand MA, Giaisi M, Suss D, Treiber MK, Baumann S et al. Vitamin E inhibits CD95 ligand expression and protects T cells from activation-induced cell death. J Clin Invest 2002;110, 681–90.
53. Glauert HP. Vitamin E and NF-kappaB activation: a review. Vitam Horm 2007;76, 135–53.
54. Yevenes LF, Klein A, Castro JF, Marin T, Leal N, Leighton F et al. Lysosomal vitamin E accumulation in Niemann-Pick type C disease. Biochim Biophys Acta 2012;1822, 150–60.
55. Kryscio RJ, Abner EL, Schmitt FA, Goodman PJ, Mendiondo M, Caban-Holt A et al. A randomized controlled Alzheimer’s disease prevention trial’s evolution into an exposure trial: the PREADViSE Trial. J Nutr Health Aging 2013;17, 72–5.
56. Sutachan JJ, Casas Z, Albarracin SL, Stab BR, 2nd, Samudio I, Gonzalez J et al. Cellular and molecular mechanisms of antioxidants in Parkinson’s disease. Nutr Neurosci 2012;15, 120–6.
57. Yang CS, Lu G, Ju J, and Li GX. Inhibition of inflammation and carcinogenesis in the lung and colon by tocopherols. Ann N Y Acad Sci 2010;1203, 29–34.
58. Vance TM, Su J, Fontham ET, Koo SI, and Chun OK. Dietary antioxidants and prostate cancer: a review. Nutr Cancer 2013;65, 793–801.
59. Stone WL, Krishnan K, Campbell SE, and Palau VE. The role of antioxidants and pro-oxidants in colon cancer. World J Gastrointest Oncol 2014;6, 55–66.
60. Ozkanlar S and Akcay F. Antioxidant vitamins in atherosclerosis—animal experiments and clinical studies. Adv Clin Exp Med 2012;21, 115–23.
61. Riccioni G, D’Orazio N, Salvatore C, Franceschelli S, Pesce M, and Speranza L. Carotenoids and vitamins C and E in the prevention of cardiovascular disease. Int J Vitam Nutr Res 2012;82, 15–26.
62. Ohshima Y, Mizuno T, Yamada K, Matsumoto S, Nagakane Y, Kondo M et al. Low vitamin and carotenoid levels are related to cerebral white matter lesions. J Nutr Health Aging 2013;17, 456–60.
63. Goldenstein H, Levy NS, Lipener YT, and Levy AP. Patient selection and vitamin E treatment in diabetes mellitus. Expert Rev Cardiovasc Ther 2013;11, 319–26.
64. Lopes da Silva S, Vellas B, Elemans S, Luchsinger J, Kamphuis P, Yaffe K et al. Plasma nutrient status of patients with Alzheimer’s disease: Systematic review and meta-analysis. Alzheimers Dement, 2014;10, 485–502
65. Mangialasche F, Solomon A, Kareholt I, Hooshmand B, Cecchetti R, Fratiglioni L et al. Serum levels of vitamin E forms and risk of cognitive impairment in a Finnish cohort of older adults. Exp Gerontol 2013;48, 1428–35.
66. Arlt S, Muller-Thomsen T, Beisiegel U, and Kontush A. Effect of one-year vitamin C- and E-supplementation on cerebrospinal fluid oxidation parameters and clinical course in Alzheimer’s disease. Neurochem Res 2012;37, 2706–14.
67. Sung S, Yao Y, Uryu K, Yang H, Lee VM, Trojanowski JQ et al. Early vitamin E supplementation in young but not aged mice reduces Abeta levels and amyloid deposition in a transgenic model of Alzheimer’s disease. FASEB J 2004;18, 323–5.
68. Crichton GE, Bryan J, and Murphy KJ. Dietary antioxidants, cognitive function and dementia—a systematic review. Plant Foods Hum Nutr 2013;68, 279–92.
69. Li FJ, Shen L, and Ji HF. Dietary intakes of vitamin E, vitamin C, and beta-carotene and risk of Alzheimer’s disease: a meta-analysis. J Alzheimers Dis 2012;31, 253–8.
70. Galasko DR, Peskind E, Clark CM, Quinn JF, Ringman JM, Jicha GA et al. Antioxidants for Alzheimer disease: a randomized clinical trial with cerebrospinal fluid biomarker measures. Arch Neurol 2012;69, 836–41.