Home LiteratureArticle Details
PMID: 8892349 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

In vivo and in vitro evidence supporting a role for the inflammatory cytokine interleukin-1 as a driving force in Alzheimer pathogenesis.

Neurobiology of aging ·Vol. 17 ·No. 5 ·1996-00-00 ·Pages 761-6

Sheng JG, Ito K, Skinner RD, Mrak RE, Rovnaghi CR, Van Eldik LJ, Griffin WS

Abstract

Interleukin-1 (IL-1), an inflammatory cytokine overexpressed in the neuritic plaques of Alzheimer's disease, activates astrocytes and enhances production and processing of beta-amyloid precursor protein (beta-APP). Activated astrocytes, overexpressing S100 beta, are a prominent feature of these neuritic plaques, and the neurite growth-promoting properties of S100 beta have been implicated in the formation of dystrophic neurites overexpressing beta-APP in neuritic plaques. These facts collectively suggest that elevated levels of the inflammatory cytokine IL-1 drive S100 beta and beta-APP overexpression and dystrophic neurite formation in Alzheimer's disease. To more directly assess this driver potential for IL-1, we analyzed IL-1 induction of S100 beta expression in vivo and in vitro, and of beta-APP expression in vivo. Synthetic IL-1 beta was injected into the right cerebral hemispheres of 13 rats. Nine additional rats were injected with phosphate-buffered saline, and seven rats served as uninjected controls. The number of astrocytes expressing detectable levels of S100 beta in tissue sections from IL-1-injected brains was 1.5 fold that of either control group (p < 0.01), while tissue S100 beta levels were approximately threefold that of controls (p < 0.05). The tissue levels of two beta-APP isoforms (approximately 130 and 135 kDa) were also significantly elevated in IL-1-injected brains (p < 0.05). C6 glioma cells, treated in vitro for 24 h with either IL-1 beta or IL-1 alpha, showed significant increases in both S100 beta and S100 beta mRNA levels. These results provide evidence that IL-1 upregulates both S100 beta and beta-APP expression, in vivo and vitro, and support the idea that overexpression of IL-1 in Alzheimer's disease drives astrocytic overexpression of S100 beta, favoring the growth of dystrophic neurites necessary for evolution of diffuse amyloid deposits into neuritic beta-amyloid plaques.

MeSH Terms
Alzheimer Disease/pathology Amyloid beta-Protein Precursor/biosynthesis Animals Astrocytes/metabolism Blotting, Northern Blotting, Western Brain Chemistry/drug effects,physiology Brain Neoplasms/metabolism Glioma/metabolism Humans Immunohistochemistry In Situ Hybridization Interleukin-1/physiology Rats Rats, Sprague-Dawley S100 Proteins/biosynthesis Tumor Cells, Cultured Up-Regulation/physiology
Chemicals
Amyloid beta-Protein Precursor Interleukin-1 S100 Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Sheng J G
Arkansas Children's Hospital Research Center, Department of Veterans' Affairs Medical Center, Little Rock, AR, USA.
Ito K
Skinner R D
Mrak R E
Rovnaghi C R
Van Eldik L J
Griffin W S
References (30)
30 references, click to expand
  1. Increased S100 beta neurotrophic activity in Alzheimer's disease temporal lobe.
    Neurobiol Aging. 1992 Jan-Feb;13(1):1-7 PMID: 1371849
  2. Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer beta/A4 amyloid protein precursor.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10075-8 PMID: 1359534
  3. Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus.
    Science. 1987 Feb 20;235(4791):880-4 PMID: 2949367
  4. Brain interleukin-1 beta in Alzheimer's disease and vascular dementia.
    Methods Find Exp Clin Pharmacol. 1994 Mar;16(2):141-51 PMID: 8007743
  5. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7611-5 PMID: 2529544
  6. Reduction in S100 protein beta subunit mRNA in C6 rat glioma cells following treatment with anti-microtubular drugs.
    J Biol Chem. 1987 Mar 15;262(8):3562-6 PMID: 3818655
  7. The regulation of amyloid beta protein precursor secretion and its modulatory role in cell adhesion.
    Neuron. 1989 Dec;3(6):689-94 PMID: 2518372
  8. Glial cytokines in Alzheimer's disease: review and pathogenic implications.
    Hum Pathol. 1995 Aug;26(8):816-23 PMID: 7635444
  9. Functions and mechanisms of interleukin 1 in the brain.
    Trends Pharmacol Sci. 1991 Nov;12(11):430-6 PMID: 1796497
  10. Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1 alpha immunoreactivity.
    J Neurochem. 1994 Nov;63(5):1872-9 PMID: 7931344
  11. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution.
    J Neuropathol Exp Neurol. 1995 Mar;54(2):276-81 PMID: 7876895
  12. Interleukin-1 binding sites on astrocytes.
    Neuroscience. 1993 Feb;52(3):725-33 PMID: 8450969
  13. Interleukin 1 regulates synthesis of amyloid beta-protein precursor mRNA in human endothelial cells.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7606-10 PMID: 2508093
  14. Trophic effect of beta-amyloid precursor protein on cerebral cortical neurons in culture.
    Biochem Biophys Res Commun. 1991 Nov 27;181(1):265-71 PMID: 1958195
  15. The amyloid protein precursor of Alzheimer's disease is a mediator of the effects of nerve growth factor on neurite outgrowth.
    Neuron. 1992 Jul;9(1):129-37 PMID: 1632967
  16. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization.
    J Neurosci. 1988 Jul;8(7):2485-90 PMID: 2470873
  17. Expression of amyloid precursor protein mRNAs in endothelial, neuronal and glial cells: modulation by interleukin-1.
    Brain Res Mol Brain Res. 1992 Nov;16(1-2):128-34 PMID: 1334190
  18. Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome.
    Ann Neurol. 1985 Mar;17(3):278-82 PMID: 3158266
  19. S100 is present in developing chicken neurons and Schwann cells and promotes motor neuron survival in vivo.
    J Neurobiol. 1992 Jun;23(4):451-66 PMID: 1634890
  20. Chromosomal localization of murine interleukin-1 alpha and beta genes.
    Genomics. 1989 Oct;5(3):481-5 PMID: 2613234
  21. Microglial interleukin-1 alpha expression in brain regions in Alzheimer's disease: correlation with neuritic plaque distribution.
    Neuropathol Appl Neurobiol. 1995 Aug;21(4):290-301 PMID: 7494597
  22. Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease.
    Science. 1987 Feb 20;235(4791):877-80 PMID: 3810169
  23. Gene encoding the beta subunit of S100 protein is on chromosome 21: implications for Down syndrome.
    Science. 1988 Mar 11;239(4845):1311-3 PMID: 2964086
  24. Alzheimer's disease: pathology to potential treatments?
    Trends Pharmacol Sci. 1992 Apr;13(4):131-3 PMID: 1589905
  25. Is amyloidogenesis during Alzheimer's disease due to an IL-1-/IL-6-mediated 'acute phase response' in the brain?
    Immunol Today. 1991 Jul;12(7):217-9 PMID: 1909530
  26. S100 beta protein expression in Alzheimer disease: potential role in the pathogenesis of neuritic plaques.
    J Neurosci Res. 1994 Nov 1;39(4):398-404 PMID: 7884819
  27. S100 beta as a neurotrophic factor.
    Prog Brain Res. 1990;86:169-81 PMID: 2087556
  28. S100 beta expression in Alzheimer's disease: relation to neuropathology in brain regions.
    Biochim Biophys Acta. 1994 Sep 29;1223(3):398-403 PMID: 7918676
  29. A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid deposition.
    J Neuropathol Exp Neurol. 1989 Nov;48(6):674-91 PMID: 2677252
  30. Gliosis in human brain: relationship to size but not other properties of astrocytes.
    Brain Res. 1993 Jan 8;600(1):161-5 PMID: 8422583
Article Info
Journal
Neurobiology of aging
Abbr.
Neurobiol Aging
ISSN
0197-4580
Published
1996-00-00
Pages
761-6
Language
English
Region
United States
NLM ID
8100437
PMCID
PMC3886636
Subset
IM
Grants
NIA NIH HHS · P01 AG012411 · United States
NIA NIH HHS · AG10208 · United States
NIA NIH HHS · AG12411 · United States
NINDS NIH HHS · NS27414 · United States
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