Abstract
Senile plaques accumulate over the course of decades in the brains of patients with Alzheimer's disease. A fundamental tenet of the amyloid hypothesis of Alzheimer's disease is that the deposition of amyloid-beta precedes and induces the neuronal abnormalities that underlie dementia. This idea has been challenged, however, by the suggestion that alterations in axonal trafficking and morphological abnormalities precede and lead to senile plaques. The role of microglia in accelerating or retarding these processes has been uncertain. To investigate the temporal relation between plaque formation and the changes in local neuritic architecture, we used longitudinal in vivo multiphoton microscopy to sequentially image young APPswe/PS1d9xYFP (B6C3-YFP) transgenic mice. Here we show that plaques form extraordinarily quickly, over 24 h. Within 1-2 days of a new plaque's appearance, microglia are activated and recruited to the site. Progressive neuritic changes ensue, leading to increasingly dysmorphic neurites over the next days to weeks. These data establish plaques as a critical mediator of neuritic pathology.
MeSH Terms
Alzheimer Disease/genetics,metabolism,pathology
Amyloid beta-Peptides/genetics,metabolism,toxicity
Animals
Axons/metabolism
Disease Models, Animal
Disease Progression
Mice
Mice, Transgenic
Microglia/metabolism
Neurites/metabolism,pathology
Plaque, Amyloid/genetics,metabolism,pathology
Time Factors
Chemicals
Amyloid beta-Peptides
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Meyer-Luehmann Melanie
Alzheimer's Disease Research Laboratory, Department of Neurology, MassGeneral Institute for Neurodegenerative Disease, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, USA.
Spires-Jones Tara L
Prada Claudia
Garcia-Alloza Monica
de Calignon Alix
Rozkalne Anete
Koenigsknecht-Talboo Jessica
Holtzman David M
Bacskai Brian J
Hyman Bradley T
References (27)
27 references, click to expand
-
Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse.
Nature. 1999 Jul 8;400(6740):173-7
PMID: 10408445
-
Microglial response to amyloid plaques in APPsw transgenic mice.
Am J Pathol. 1998 Jan;152(1):307-17
PMID: 9422548
-
beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis.
J Neurosci. 2001 Feb 15;21(4):1179-88
PMID: 11160388
-
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
-
The relationship of amyloid plaques to cerebral capillaries in Alzheimer's disease.
Am J Pathol. 1990 Dec;137(6):1435-46
PMID: 2260630
-
Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo.
Nature. 2002 Apr 4;416(6880):535-9
PMID: 11932745
-
A specific amyloid-beta protein assembly in the brain impairs memory.
Nature. 2006 Mar 16;440(7082):352-7
PMID: 16541076
-
Co-expression of multiple transgenes in mouse CNS: a comparison of strategies.
Biomol Eng. 2001 Jun;17(6):157-65
PMID: 11337275
-
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
-
Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice.
Science. 1996 Oct 4;274(5284):99-102
PMID: 8810256
-
Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls.
Am J Pathol. 2005 Aug;167(2):527-43
PMID: 16049337
-
Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion.
Mol Cell Biol. 2000 Jun;20(11):4106-14
PMID: 10805752
-
Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease.
Neurobiol Aging. 2004 May-Jun;25(5):663-74
PMID: 15172746
-
Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease.
Science. 2005 Feb 25;307(5713):1282-8
PMID: 15731448
-
Imaging of amyloid-beta deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy.
Nat Med. 2001 Mar;7(3):369-72
PMID: 11231639
-
Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy.
J Neurosci. 2005 Aug 3;25(31):7278-87
PMID: 16079410
-
Quantitative analysis of senile plaques in Alzheimer disease: observation of log-normal size distribution and molecular epidemiology of differences associated with apolipoprotein E genotype and trisomy 21 (Down syndrome).
Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3586-90
PMID: 7724603
-
Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host.
Science. 2006 Sep 22;313(5794):1781-4
PMID: 16990547
-
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
-
Plaque-induced abnormalities in neurite geometry in transgenic models of Alzheimer disease: implications for neural system disruption.
J Neuropathol Exp Neurol. 2001 Aug;60(8):753-8
PMID: 11487049
-
Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease.
Neuron. 2006 Feb 16;49(4):489-502
PMID: 16476660
-
Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease.
J Neuroimmunol. 1989 Oct;24(3):173-82
PMID: 2808689
-
System Xc- and apolipoprotein E expressed by microglia have opposite effects on the neurotoxicity of amyloid-beta peptide 1-40.
J Neurosci. 2006 Mar 22;26(12):3345-56
PMID: 16554485
-
Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie?
Cell. 1993 Jun 18;73(6):1055-8
PMID: 8513491
-
Aging renders the brain vulnerable to amyloid beta-protein neurotoxicity.
Nat Med. 1998 Jul;4(7):827-31
PMID: 9662375
-
Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein.
Nature. 1995 Feb 9;373(6514):523-7
PMID: 7845465
-
Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase.
Hum Mol Genet. 2004 Jan 15;13(2):159-70
PMID: 14645205