Home LiteratureArticle Details
PMID: 19710322 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice.

Yan P, Bero AW, Cirrito JR, Xiao Q, Hu X, Wang Y, Gonzales E, Holtzman DM, Lee JM

Abstract

Amyloid plaques are primarily composed of extracellular aggregates of amyloid-beta (Abeta) peptide and are a pathological signature of Alzheimer's disease. However, the factors that influence the dynamics of amyloid plaque formation and growth in vivo are largely unknown. Using serial intravital multiphoton microscopy through a thinned-skull cranial window in APP/PS1 transgenic mice, we found that amyloid plaques appear and grow over a period of weeks before reaching a mature size. Growth was more prominent early after initial plaque formation: plaques grew faster in 6-month-old compared with 10-month-old mice. Plaque growth rate was also size-related, as smaller plaques exhibited more rapid growth relative to larger plaques. Alterations in interstitial Abeta concentrations were associated with changes in plaque growth. Parallel studies using multiphoton microscopy and in vivo microdialysis revealed that pharmacological reduction of soluble extracellular Abeta by as little as 20-25% was associated with a dramatic decrease in plaque formation and growth. Furthermore, this small reduction in Abeta synthesis was sufficient to reduce amyloid plaque load in 6-month-old but not 10-month-old mice, suggesting that treatment early in disease pathogenesis may be more effective than later treatment. In contrast to thinned-skull windows, no significant plaque growth was observed under open-skull windows, which demonstrated extensive microglial and astrocytic activation. Together, these findings indicate that individual amyloid plaque growth in vivo occurs over a period of weeks and may be influenced by interstitial Abeta concentration as well as reactive gliosis.

MeSH Terms
Age Factors Alzheimer Disease/complications,genetics,metabolism,pathology Amyloid Precursor Protein Secretases/pharmacology Amyloid beta-Peptides/metabolism Amyloid beta-Protein Precursor/genetics Analysis of Variance Animals Brain/metabolism,pathology Diagnostic Imaging/methods Disease Models, Animal Enzyme-Linked Immunosorbent Assay/methods Female Gliosis/metabolism,pathology Male Mice Mice, Transgenic Microdialysis/methods Photons Plaque, Amyloid/drug effects,pathology Presenilin-1/genetics Time Factors
Chemicals
Amyloid beta-Peptides Amyloid beta-Protein Precursor Presenilin-1 Amyloid Precursor Protein Secretases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Yan Ping
Department of Neurology and the Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Bero Adam W
Cirrito John R
Xiao Qingli
Hu Xiaoyan
Wang Yan
Gonzales Ernesto
Holtzman David M
Lee Jin-Moo
References (48)
48 references, click to expand
  1. Longitudinal assessment of Alzheimer's beta-amyloid plaque development in transgenic mice monitored by in vivo magnetic resonance microimaging.
    J Magn Reson Imaging. 2006 Sep;24(3):530-6 PMID: 16892201
  2. Chronic treatment with the gamma-secretase inhibitor LY-411,575 inhibits beta-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation.
    J Biol Chem. 2004 Mar 26;279(13):12876-82 PMID: 14709552
  3. X-34, a fluorescent derivative of Congo red: a novel histochemical stain for Alzheimer's disease pathology.
    J Histochem Cytochem. 2000 Sep;48(9):1223-32 PMID: 10950879
  4. In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer's transgenic mice.
    J Neurosci. 2005 Oct 26;25(43):10041-8 PMID: 16251453
  5. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics.
    Science. 2002 Jul 19;297(5580):353-6 PMID: 12130773
  6. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain.
    Nature. 1999 Apr 8;398(6727):518-22 PMID: 10206645
  7. Amyloid-beta antibody treatment leads to rapid normalization of plaque-induced neuritic alterations.
    J Neurosci. 2003 Nov 26;23(34):10879-83 PMID: 14645482
  8. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches.
    Nat Neurosci. 2004 Nov;7(11):1181-3 PMID: 15475950
  9. Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex.
    Nat Neurosci. 2007 May;10(5):549-51 PMID: 17417634
  10. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13287-92 PMID: 9371838
  11. gamma -Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase.
    Science. 2001 Dec 7;294(5549):2179-81 PMID: 11679632
  12. Extracellular amyloid formation and associated pathology in neural grafts.
    Nat Neurosci. 2003 Apr;6(4):370-7 PMID: 12598899
  13. In vivo multiphoton imaging of a transgenic mouse model of Alzheimer disease reveals marked thioflavine-S-associated alterations in neurite trajectories.
    J Neuropathol Exp Neurol. 2003 Feb;62(2):137-45 PMID: 12578223
  14. Growth arrest of individual senile plaques in a model of Alzheimer's disease observed by in vivo multiphoton microscopy.
    J Neurosci. 2001 Feb 1;21(3):858-64 PMID: 11157072
  15. Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs.
    J Biol Chem. 1992 Jan 5;267(1):546-54 PMID: 1730616
  16. Existing plaques and neuritic abnormalities in APP:PS1 mice are not affected by administration of the gamma-secretase inhibitor LY-411575.
    Mol Neurodegener. 2009 May 06;4:19 PMID: 19419556
  17. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease.
    Nature. 2008 Feb 7;451(7179):720-4 PMID: 18256671
  18. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease.
    Science. 2008 Sep 19;321(5896):1686-9 PMID: 18802001
  19. Plaque-derived oxidative stress mediates distorted neurite trajectories in the Alzheimer mouse model.
    J Neuropathol Exp Neurol. 2006 Nov;65(11):1082-9 PMID: 17086105
  20. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance.
    J Neurosci. 2008 Apr 16;28(16):4283-92 PMID: 18417708
  21. Acute stress increases interstitial fluid amyloid-beta via corticotropin-releasing factor and neuronal activity.
    Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10673-8 PMID: 17551018
  22. Cortical synaptic integration in vivo is disrupted by amyloid-beta plaques.
    J Neurosci. 2004 May 12;24(19):4535-40 PMID: 15140924
  23. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host.
    Science. 2006 Sep 22;313(5794):1781-4 PMID: 16990547
  24. Plaque-induced neurite abnormalities: implications for disruption of neural networks in Alzheimer's disease.
    Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5274-9 PMID: 10220456
  25. Type-specific evolution of amyloid plaque and angiopathy in APPsw mice.
    Neurosci Lett. 2006 Feb 27;395(1):37-41 PMID: 16298484
  26. Imaging Abeta plaques in living transgenic mice with multiphoton microscopy and methoxy-X04, a systemically administered Congo red derivative.
    J Neuropathol Exp Neurol. 2002 Sep;61(9):797-805 PMID: 12230326
  27. Moderate reduction of gamma-secretase attenuates amyloid burden and limits mechanism-based liabilities.
    J Neurosci. 2007 Oct 3;27(40):10849-59 PMID: 17913918
  28. Alzheimer's disease: genes, proteins, and therapy.
    Physiol Rev. 2001 Apr;81(2):741-66 PMID: 11274343
  29. The lack of accumulation of senile plaques or amyloid burden in Alzheimer's disease suggests a dynamic balance between amyloid deposition and resolution.
    J Neuropathol Exp Neurol. 1993 Nov;52(6):594-600 PMID: 8229078
  30. Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice.
    Science. 2009 Feb 27;323(5918):1211-5 PMID: 19251629
  31. [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease.
    Neurology. 2006 Aug 8;67(3):446-52 PMID: 16894106
  32. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ.
    Nat Med. 2003 Apr;9(4):453-7 PMID: 12612547
  33. Time course of the development of Alzheimer-like pathology in the doubly transgenic PS1+APP mouse.
    Exp Neurol. 2002 Feb;173(2):183-95 PMID: 11822882
  34. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life.
    J Neurosci. 2003 Oct 1;23(26):8844-53 PMID: 14523085
  35. Microglial transplantation increases amyloid-beta clearance in Alzheimer model rats.
    FEBS Lett. 2007 Feb 6;581(3):475-8 PMID: 17240371
  36. Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide.
    J Biol Chem. 2002 Nov 22;277(47):44754-9 PMID: 12223485
  37. Quantitative histological analysis of amyloid deposition in Alzheimer's double transgenic mouse brain.
    Neuroscience. 2000;101(4):939-44 PMID: 11113343
  38. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo.
    Neuron. 2008 Apr 10;58(1):42-51 PMID: 18400162
  39. Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities.
    Neurobiol Dis. 2005 Apr;18(3):602-17 PMID: 15755686
  40. Simplified quantification of Pittsburgh Compound B amyloid imaging PET studies: a comparative analysis.
    J Nucl Med. 2005 Dec;46(12):1959-72 PMID: 16330558
  41. Persistent amyloidosis following suppression of Abeta production in a transgenic model of Alzheimer disease.
    PLoS Med. 2005 Dec;2(12):e355 PMID: 16279840
  42. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease.
    Nat Med. 2007 Apr;13(4):432-8 PMID: 17351623
  43. Kinetic modeling of amyloid binding in humans using PET imaging and Pittsburgh Compound-B.
    J Cereb Blood Flow Metab. 2005 Nov;25(11):1528-47 PMID: 15944649
  44. Anti-Abeta antibody treatment promotes the rapid recovery of amyloid-associated neuritic dystrophy in PDAPP transgenic mice.
    J Clin Invest. 2005 Feb;115(2):428-33 PMID: 15668737
  45. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks.
    Neuron. 2008 Jul 31;59(2):214-25 PMID: 18667150
  46. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo.
    Neuron. 2005 Dec 22;48(6):913-22 PMID: 16364896
  47. Determination of guinea-pig cortical gamma-secretase activity ex vivo following the systemic administration of a gamma-secretase inhibitor.
    Neuropharmacology. 2005 Jun;48(7):1002-11 PMID: 15857627
  48. Two-year follow-up of amyloid deposition in patients with Alzheimer's disease.
    Brain. 2006 Nov;129(Pt 11):2856-66 PMID: 16854944
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2009-08-26
Pages
10706-14
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC2756291
Subset
IM
Grants
NINDS NIH HHS · P30 NS057105 · United States
NINDS NIH HHS · R01 NS048283 · United States
NINDS NIH HHS · R01 NS048283-05 · United States
NINDS NIH HHS · P01 NS032636 · United States
NIA NIH HHS · R37 AG013956 · United States
NINDS NIH HHS · R01 NS067905-01A2 · United States
NINDS NIH HHS · P01 NS032636-149001 · United States
NIA NIH HHS · R37 AG13956 · United States
NINDS NIH HHS · P01 NS032636-139001 · United States
NINDS NIH HHS · R01 NS048283-04 · United States
NINDS NIH HHS · R01 NS067905 · 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