Home LiteratureArticle Details
PMID: 12077180 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A novel function of monomeric amyloid beta-protein serving as an antioxidant molecule against metal-induced oxidative damage.

Zou K, Gong JS, Yanagisawa K, Michikawa M

Abstract

Aggregated and oligomeric amyloid beta-protein (Abeta) is known to exhibit neurotoxicity. However, the action of Abeta monomers on neurons is not fully understood. We have studied aggregation state-dependent actions of Abeta and found an oligomer-specific effect of Abeta on lipid metabolism in neurons (Michikawa et al., 2001). Here, we show a novel function of monomeric Abeta1-40, which is the major species found in physiological fluid, as a natural antioxidant molecule that prevents neuronal death caused by transition metal-induced oxidative damage. Monomeric Abeta1-40, which is demonstrated by SDS-PAGE after treatment with glutaraldehyde, protects neurons cultured in a medium containing 1.5 microm Fe(II) without antioxidant molecules. Metal ion chelators such as EDTA, CDTA (trans-1,2-diaminocyclohexane-N,N,N',N'-tetraacetic acid), and DTPA (diethylenetriamine-N,N,N',N",N"-penta-acetic acid, an iron-binding protein, transferrin, and antioxidant scavengers such as catalase, glutathione, and vitamin E also inhibit neuronal death under the same conditions. Monomeric Abeta1-40 inhibits neuronal death caused by Cu(II), Fe(II), and Fe(III) but does not protect neurons against H2O2-induced damage. Monomeric Abeta1-40 inhibits the reduction of Fe(III) induced by vitamin C and the generation of superoxides and prevents lipid peroxidation induced by Fe(II). Abeta1-42 remaining as a monomer also exhibits antioxidant and neuroprotective effects. In contrast, oligomeric and aggregated Abeta1-40 and Abeta1-42 lose their neuroprotective activity. These results indicate that monomeric Abeta protects neurons by quenching metal-inducible oxygen radical generation and thereby inhibiting neurotoxicity. Because aggregated Abeta is known to be an oxygen radical generator, our results provide a novel concept that the aggregation-dependent biological effects of Abeta are dualistic, being either an oxygen radical generator or its inhibitor.

MeSH Terms
Amyloid beta-Peptides/pharmacology Animals Antioxidants/pharmacology Ascorbic Acid/antagonists & inhibitors Cell Death/drug effects Cells, Cultured Chelating Agents/pharmacology Copper/antagonists & inhibitors Culture Media Ferric Compounds/metabolism Iron/antagonists & inhibitors Lipid Peroxidation/drug effects Metals/antagonists & inhibitors Neurons/cytology,drug effects Neuroprotective Agents/pharmacology Oxidative Stress/drug effects Peptide Fragments/pharmacology Rats Rats, Sprague-Dawley Superoxides/metabolism Tachykinins/pharmacology
Chemicals
Amyloid beta-Peptides Antioxidants Chelating Agents Culture Media Ferric Compounds Metals Neuroprotective Agents Peptide Fragments Tachykinins amyloid beta-protein (1-40) Superoxides Copper Iron Ascorbic Acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Zou Kun
Department of Dementia Research, National Institute for Longevity Sciences, Obu, Aichi 474-8522, Japan.
Gong Jian-Sheng
Yanagisawa Katsuhiko
Michikawa Makoto
References (54)
54 references, click to expand
  1. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides.
    Science. 1990 Oct 12;250(4978):279-82 PMID: 2218531
  2. Mechanochemical mechanism for peptidyl free radical generation by amyloid fibrils.
    FEBS Lett. 1997 Feb 24;403(3):230-5 PMID: 9091307
  3. The relationship between the aggregational state of the amyloid-beta peptides and free radical generation by the peptides.
    J Neurochem. 2001 Jun;77(6):1425-32 PMID: 11413227
  4. Amyloid beta-protein affects cholesterol metabolism in cultured neurons: implications for pivotal role of cholesterol in the amyloid cascade.
    J Neurosci Res. 2002 Nov 1;70(3):438-46 PMID: 12391604
  5. Alzheimer's disease: a central role for amyloid.
    J Neuropathol Exp Neurol. 1994 Sep;53(5):438-47 PMID: 8083687
  6. Amyloid-beta is an antioxidant for lipoproteins in cerebrospinal fluid and plasma.
    Free Radic Biol Med. 2001 Jan 1;30(1):119-28 PMID: 11134902
  7. Quantitation of amyloid beta-protein (A beta) in the cortex during aging and in Alzheimer's disease.
    Am J Pathol. 1998 Jun;152(6):1633-40 PMID: 9626067
  8. Apolipoprotein E4 induces neuronal cell death under conditions of suppressed de novo cholesterol synthesis.
    J Neurosci Res. 1998 Oct 1;54(1):58-67 PMID: 9778150
  9. Cu(II) potentiation of alzheimer abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction.
    J Biol Chem. 1999 Dec 24;274(52):37111-6 PMID: 10601271
  10. The relationship between Abeta-associated free radical generation and Abeta fibril formation revealed by negative stain electron microscopy and thioflavine-T fluorometric assay.
    Neurosci Lett. 2001 May 18;304(1-2):65-8 PMID: 11335056
  11. The role of iron in beta amyloid toxicity.
    Biochem Biophys Res Commun. 1995 Nov 13;216(2):702-7 PMID: 7488167
  12. Dramatic aggregation of Alzheimer abeta by Cu(II) is induced by conditions representing physiological acidosis.
    J Biol Chem. 1998 May 22;273(21):12817-26 PMID: 9582309
  13. Characterization of copper interactions with alzheimer amyloid beta peptides: identification of an attomolar-affinity copper binding site on amyloid beta1-42.
    J Neurochem. 2000 Sep;75(3):1219-33 PMID: 10936205
  14. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice.
    Neuron. 2001 Jun;30(3):665-76 PMID: 11430801
  15. Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state.
    J Neurosci. 1993 Apr;13(4):1676-87 PMID: 8463843
  16. Copper, iron and zinc in Alzheimer's disease senile plaques.
    J Neurol Sci. 1998 Jun 11;158(1):47-52 PMID: 9667777
  17. Amyloid plaque core protein in Alzheimer disease and Down syndrome.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4245-9 PMID: 3159021
  18. The Alzheimer's disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures.
    J Neurosci. 1999 Nov 1;19(21):9170-9 PMID: 10531420
  19. Apolipoprotein E and antioxidants have different mechanisms of inhibiting Alzheimer's beta-amyloid fibril formation in vitro.
    Biochemistry. 1998 Dec 22;37(51):17882-9 PMID: 9922155
  20. In situ oxidative catalysis by neurofibrillary tangles and senile plaques in Alzheimer's disease: a central role for bound transition metals.
    J Neurochem. 2000 Jan;74(1):270-9 PMID: 10617129
  21. Rapid induction of Alzheimer A beta amyloid formation by zinc.
    Science. 1994 Sep 2;265(5177):1464-7 PMID: 8073293
  22. Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12243-7 PMID: 7991613
  23. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine.
    J Neurosci. 1996 Feb 15;16(4):1324-36 PMID: 8778284
  24. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein.
    Biochem Biophys Res Commun. 1984 May 16;120(3):885-90 PMID: 6375662
  25. A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3270-4 PMID: 8159737
  26. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons.
    J Neurosci. 1999 Oct 15;19(20):8876-84 PMID: 10516307
  27. Oxygen toxicity, oxygen radicals, transition metals and disease.
    Biochem J. 1984 Apr 1;219(1):1-14 PMID: 6326753
  28. Evidence that the beta-amyloid plaques of Alzheimer's disease represent the redox-silencing and entombment of abeta by zinc.
    J Biol Chem. 2000 Jun 30;275(26):19439-42 PMID: 10801774
  29. The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction.
    Biochemistry. 1999 Jun 15;38(24):7609-16 PMID: 10386999
  30. Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture.
    J Biol Chem. 1995 Apr 21;270(16):9564-70 PMID: 7721886
  31. Hydrogen peroxide mediates amyloid beta protein toxicity.
    Cell. 1994 Jun 17;77(6):817-27 PMID: 8004671
  32. Quantification of beta-sheet amyloid fibril structures with thioflavin T.
    Methods Enzymol. 1999;309:274-84 PMID: 10507030
  33. New insights on how metals disrupt amyloid beta-aggregation and their effects on amyloid-beta cytotoxicity.
    J Biol Chem. 2001 Aug 24;276(34):32293-9 PMID: 11423547
  34. Growth of a rat neuroblastoma cell line in serum-free supplemented medium.
    Proc Natl Acad Sci U S A. 1979 Jan;76(1):514-7 PMID: 284369
  35. Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay.
    J Biol Chem. 1996 Sep 13;271(37):22908-14 PMID: 8798471
  36. Zinc-induced Alzheimer's Abeta1-40 aggregation is mediated by conformational factors.
    J Biol Chem. 1997 Oct 17;272(42):26464-70 PMID: 9334223
  37. Calcium-destabilizing and neurodegenerative effects of aggregated beta-amyloid peptide are attenuated by basic FGF.
    Brain Res. 1993 Sep 3;621(1):35-49 PMID: 8221072
  38. A novel action of alzheimer's amyloid beta-protein (Abeta): oligomeric Abeta promotes lipid release.
    J Neurosci. 2001 Sep 15;21(18):7226-35 PMID: 11549733
  39. Iron accumulation in Alzheimer disease is a source of redox-generated free radicals.
    Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9866-8 PMID: 9275217
  40. beta-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10836-40 PMID: 8248178
  41. Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer's disease.
    Neurology. 1998 Dec;51(6):1562-6 PMID: 9855502
  42. Soluble multimeric Alzheimer beta(1-40) pre-amyloid complexes in dilute solution.
    Neurobiol Aging. 1995 Sep-Oct;16(5):755-64 PMID: 8532108
  43. Oligomerization of endogenous and synthetic amyloid beta-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red.
    Biochemistry. 1998 Mar 17;37(11):3602-11 PMID: 9521679
  44. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease.
    Neurobiol Aging. 1998 Jan-Feb;19(1):33-6 PMID: 9562500
  45. Characterization of beta-amyloid peptide from human cerebrospinal fluid.
    J Neurochem. 1993 Nov;61(5):1965-8 PMID: 8229004
  46. Metal chelation as a potential therapy for Alzheimer's disease.
    Ann N Y Acad Sci. 2000;920:292-304 PMID: 11193167
  47. Morphology and toxicity of Abeta-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease.
    J Biol Chem. 1996 Aug 23;271(34):20631-5 PMID: 8702810
  48. Oxidative stress induces intracellular accumulation of amyloid beta-protein (Abeta) in human neuroblastoma cells.
    Biochemistry. 2000 Jun 13;39(23):6951-9 PMID: 10841777
  49. Modulation of A beta adhesiveness and secretase site cleavage by zinc.
    J Biol Chem. 1994 Apr 22;269(16):12152-8 PMID: 8163520
  50. Oxidative damage is the earliest event in Alzheimer disease.
    J Neuropathol Exp Neurol. 2001 Aug;60(8):759-67 PMID: 11487050
  51. Pyruvate released by astrocytes protects neurons from copper-catalyzed cysteine neurotoxicity.
    J Neurosci. 2001 May 15;21(10):3322-31 PMID: 11331361
  52. Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43).
    Neuron. 1994 Jul;13(1):45-53 PMID: 8043280
  53. Neuronal oxidative stress precedes amyloid-beta deposition in Down syndrome.
    J Neuropathol Exp Neurol. 2000 Nov;59(11):1011-7 PMID: 11089579
  54. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis.
    J Neurosci. 2001 Jun 15;21(12):4183-7 PMID: 11404403
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-06-15
Pages
4833-41
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6757724
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com