Imaging of cerebrovascular pathology in animal models of Alzheimer's disease

Klohs, Jan; Rudin, Markus; Shimshek, Derya R.; Beckmann, Nicolau

doi:10.3389/fnagi.2014.00032

Cited by 82Alzheimer's disease research and treatmentsBarrier Structure and Function StudiesNeurological Disease Mechanisms and Treatments

Imaging of cerebrovascular pathology in animal models of Alzheimer's disease

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Klohs, Jan, Rudin, Markus, Shimshek, Derya R., Beckmann, Nicolau·2014·Frontiers in Aging Neuroscience

DOI 10.3389/fnagi.2014.00032PMC PMC3952109

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Abstract

In Alzheimer's disease (AD), vascular pathology may interact with neurodegeneration and thus aggravate cognitive decline. As the relationship between these two processes is poorly understood, research has been increasingly focused on understanding the link between cerebrovascular alterations and AD. This has at last been spurred by the engineering of transgenic animals, which display pathological features of AD and develop cerebral amyloid angiopathy to various degrees. Transgenic models are versatile for investigating the role of amyloid deposition and vascular dysfunction, and for evaluating novel therapeutic concepts. In addition, research has benefited from the development of novel imaging techniques, which are capable of characterizing vascular pathology in vivo. They provide vascular structural read-outs and have the ability to assess the functional consequences of vascular dysfunction as well as to visualize and monitor the molecular processes underlying these pathological alterations. This article focusses on recent in vivo small animal imaging studies addressing vascular aspects related to AD. With the technical advances of imaging modalities such as magnetic resonance, nuclear and microscopic imaging, molecular, functional and structural information related to vascular pathology can now be visualized in vivo in small rodents. Imaging vascular and parenchymal amyloid-β (Aβ) deposition as well as Aβ transport pathways have been shown to be useful to characterize their dynamics and to elucidate their role in the development of cerebral amyloid angiopathy and AD. Structural and functional imaging read-outs have been employed to describe the deleterious affects of Aβ on vessel morphology, hemodynamics and vascular integrity. More recent imaging studies have also addressed how inflammatory processes partake in the pathogenesis of the disease. Moreover, imaging can be pivotal in the search for novel therapies targeting the vasculature.

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Fixation alters the magnitude of water diffusion in tissue, but measures of the directionality of diffusion are less affected.
“Fixation does alter the magnitude of water diffusion in the tissue, but measures of the directionality of diffusion are less affected [44][45][46].”
From Diffusion tensor imaging reveals whole-brain microstructural changes in the P301L mouse model of tauopathy. (2020) · cites this paper as [46]
The section on chronic cerebral hypoperfusion describes arterial water as a diffusible tracer, and the imaging-techniques table mentions diffusion tensor imaging, but neither addresses tissue fixation. Searches for fixation, diffusivity, and anisotropy found no passage comparing fixation’s effects on diffusion magnitude and directionality. (LLM, conf=0.72)
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Aβ is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis
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Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage.
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Binding of the Positron Emission Tomography Tracer Pittsburgh Compound-B Reflects the Amount of Amyloid-β in Alzheimer's Disease Brain But Not in Transgenic Mouse Brain
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Early-onset and Robust Cerebral Microvascular Accumulation of Amyloid β-Protein in Transgenic Mice Expressing Low Levels of a Vasculotropic Dutch/Iowa Mutant Form of Amyloid β-Protein Precursor
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Cerebral amyloid angiopathy and its relationship to Alzheimer’s disease
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Cyclohexanehexol inhibitors of Aβ aggregation prevent and reverse Alzheimer phenotype in a mouse model
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Age-associated reductions in cerebral blood flow are independent from regional atrophy
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Aβ40 Inhibits Amyloid DepositionIn Vivo
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“Other reports suggested that Aβ40 can inhibit fibril formation and even inhibit amyloid deposition (Jarrett et al., 1993; Kim et al., 2007).”
Background
In vivo detection of amyloid-β deposits by near-infrared imaging using an oxazine-derivative probe
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Fibrinogen and β-Amyloid Association Alters Thrombosis and Fibrinolysis: A Possible Contributing Factor to Alzheimer's Disease
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Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein
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Pathological alterations of the cerebral microvasculature in Alzheimer's disease and related dementing disorders
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Valsartan lowers brain β-amyloid protein levels and improves spatial learning in a mouse model of Alzheimer disease
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Novel Therapeutic Approach for the Treatment of Alzheimer's Disease by Peripheral Administration of Agents with an Affinity to β-Amyloid
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Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease
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Blood–brain barrier P-glycoprotein function in Alzheimer's disease
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Consequence of Aβ immunization on the vasculature of human Alzheimer's disease brain
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Characterization of Pathology in Transgenic Mice Over-Expressing Human Genomic and cDNA Tau Transgenes
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Neuroinflammation and Neuronal Loss Precede Aβ Plaque Deposition in the hAPP-J20 Mouse Model of Alzheimer’s Disease
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Brain microbleeds and Alzheimer’s disease: innocent observation or key player?
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Longitudinal, Quantitative Assessment of Amyloid, Neuroinflammation, and Anti-Amyloid Treatment in a Living Mouse Model of Alzheimer's Disease Enabled by Positron Emission Tomography
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Passive Amyloid Immunotherapy Clears Amyloid and Transiently Activates Microglia in a Transgenic Mouse Model of Amyloid Deposition
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Microvasculature changes and cerebral amyloid angiopathy in Alzheimer’s disease and their potential impact on therapy
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Novel 18F-Labeled Arylquinoline Derivatives for Noninvasive Imaging of Tau Pathology in Alzheimer Disease
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Spontaneous Hemorrhagic Stroke in a Mouse Model of Cerebral Amyloid Angiopathy
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Cerebrovascular autoregulation is profoundly impaired in mice overexpressing amyloid precursor protein
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Time sequence of maturation of dystrophic neurites associated with Aβ deposits in APP/PS1 transgenic mice
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Hippocampal Neuron Loss Exceeds Amyloid Plaque Load in a Transgenic Mouse Model of Alzheimer's Disease
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Circle of Willis Atherosclerosis Is a Risk Factor for Sporadic Alzheimer’s Disease
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Anesthesia and the Quantitative Evaluation of Neurovascular Coupling
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Cerebrovascular atherosclerosis correlates with Alzheimer pathology in neurodegenerative dementias
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Microbleed Topography, Leukoaraiosis, and Cognition in Probable Alzheimer Disease From the Sunnybrook Dementia Study
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Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer's disease
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The Arctic Alzheimer mutation facilitates early intraneuronal Aβ aggregation and senile plaque formation in transgenic mice
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ASL Perfusion MRI Predicts Cognitive Decline and Conversion From MCI to Dementia
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Voxel-level comparison of arterial spin-labeled perfusion MRI and FDG-PET in Alzheimer disease
Chen, Y., Wolk, D. A., Reddin, J. S., Korczykowski, M., Martínez‐Sánchez, P., Musiek, E. S., Newberg, A. B., Julin, P., Arnold, S. E., Greenberg, J. H., et al. (2011) · Neurology · doi:10.1212/wnl.0b013e31823a0ef7 · Cited by 259 · see citing works
Intracellular Aβ and cognitive deficits precede β-amyloid deposition in transgenic arcAβ mice
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Interstitial fluid drainage is impaired in ischemic stroke and Alzheimer’s disease mouse models
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Cerebral hypoperfusion accelerates cerebral amyloid angiopathy and promotes cortical microinfarcts
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Florbetapir PET analysis of amyloid-β deposition in the presenilin 1 E280A autosomal dominant Alzheimer's disease kindred: a cross-sectional study
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Does vascular pathology contribute to Alzheimer changes?
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Persistent Amyloidosis following Suppression of Aβ Production in a Transgenic Model of Alzheimer Disease
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Simultaneous BOLD fMRI and fiber-optic calcium recording in rat neocortex
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Circle of Willis atherosclerosis: association with Alzheimer’s disease, neuritic plaques and neurofibrillary tangles
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MDR1‐P‐Glycoprotein (ABCB1) Mediates Transport of Alzheimer’s Amyloid‐β Peptides—Implications for the Mechanisms of Aβ Clearance at the Blood–Brain Barrier
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Vascular β-amyloid and early astrocyte alterations impair cerebrovascular function and cerebral metabolism in transgenic arcAβ mice
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Early formation of mature amyloid‐β protein deposits in a mutant APP transgenic model depends on levels of Aβ1–42
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Prominent Cerebral Amyloid Angiopathy in Transgenic Mice Overexpressing the London Mutant of Human APP in Neurons
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Functional Connectivity fMRI of the Rodent Brain: Comparison of Functional Connectivity Networks in Rat and Mouse
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Arterial Spin Labeling Blood Flow MRI: Its Role in the Early Characterization of Alzheimer's Disease
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Behavioral disturbances in transgenic mice overexpressing the V717F Β-amyloid precursor protein.
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Expression and functional characterization of ABCG2 in brain endothelial cells and vessels
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Aβ-peptides enhance vasoconstriction in cerebral circulation
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ABCG2 Is Upregulated in Alzheimer's Brain with Cerebral Amyloid Angiopathy and May Act as a Gatekeeper at the Blood–Brain Barrier for Aβ 1–40 Peptides
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Dentate gyrus volume is reduced before onset of plaque formation in PDAPP mice: A magnetic resonance microscopy and stereologic analysis
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Cerebral Microvascular Amyloid β Protein Deposition Induces Vascular Degeneration and Neuroinflammation in Transgenic Mice Expressing Human Vasculotropic Mutant Amyloid β Precursor Protein
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PS2APP Transgenic Mice, Coexpressing hPS2mut and hAPPswe, Show Age-Related Cognitive Deficits Associated with Discrete Brain Amyloid Deposition and Inflammation
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Demonstration of poly-N-acetyl lactosamine residues in ameboid and ramified microglial cells in rat brain by tomato lectin binding.
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Blood–brain barrier permeability in Alzheimer's disease: a case–control MRI study
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The Role of the Cell Surface LRP and Soluble LRP in Blood-Brain Barrier Aβ Clearance in Alzheimers Disease
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Cognitive Deficits and Delayed Neuronal Loss in a Mouse Model of Multiple Microinfarcts
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Astrocyte-mediated control of cerebral microcirculation
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Dense-Core Plaques in Tg2576 and PSAPP Mouse Models of Alzheimer's Disease Are Centered on Vessel Walls
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Reduced Spine Density in Specific Regions of CA1 Pyramidal Neurons in Two Transgenic Mouse Models of Alzheimer's Disease
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Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition
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Behavioral disturbances in transgenic mice overexpressing the V717F Β-amyloid precursor protein.
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Two‐Photon Imaging of Astrocytic Ca2+ Signaling and the Microvasculature in Experimental Mice Models of Alzheimer's Disease
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Mechanism of Cerebral β-Amyloid Angiopathy: Murine and Cellular Models
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Electrophysiological properties of microglial cells in normal and pathologic rat brain slices
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Angiotensin Receptor Blocker Prevented β-Amyloid-Induced Cognitive Impairment Associated With Recovery of Neurovascular Coupling
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Scavenger receptor class B type I (SR-BI) regulates perivascular macrophages and modifies amyloid pathology in an Alzheimer mouse model
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Age-dependent rescue by simvastatin of Alzheimer’s disease cerebrovascular and memory deficits
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Apolipoprotein E Markedly Facilitates Age-Dependent Cerebral Amyloid Angiopathy and Spontaneous Hemorrhage in Amyloid Precursor Protein Transgenic Mice
Fryer, J. D., Taylor, J. W., DeMattos, R. B., Bales, K. R., Paul, S. M., Parsadanian, M., & Holtzman, D. M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07889.2003 · Cited by 160 · see citing works
Deglycosylated Anti-Amyloid-β Antibodies Eliminate Cognitive Deficits and Reduce Parenchymal Amyloid with Minimal Vascular Consequences in Aged Amyloid Precursor Protein Transgenic Mice
Wilcock, D. M., Alamed, J., Gottschall, P. E., Grimm, J., Rosenthal, A., Pons, J., Ronan, V., Symmonds, K., Gordon, M. N., & Morgan, D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0695-06.2006 · Cited by 154 · see citing works
Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched Typical Western Diet (TWD)
Hooijmans, C. R., Rutters, F., Dederen, P. J. W. C., Gambarota, G., Veltien, A. A., Groen, T. V., Broersen, L. M., Lütjohann, D., Heerschap, A., Tanila, H., et al. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.06.007 · Cited by 154 · see citing works
Imaging of Atherosclerosis
Owen, D. R., Lindsay, A. C., Choudhury, R. P., & Fayad, Z. A. (2010) · Annual Review of Medicine · doi:10.1146/annurev-med-041709-133809 · Cited by 154 · see citing works
Amyloid-β-dependent compromise of microvascular structure and function in a model of Alzheimer’s disease
Dorr, A. E., Sahota, B., Chinta, L. V., Brown, M. E., Lai, A. Y., Ma, K., Hawkes, C. A., McLaurin, J., & Stefanovic, B. (2012) · Brain · doi:10.1093/brain/aws243 · Cited by 153 · see citing works
Vascular Remodeling versus Amyloid β-Induced Oxidative Stress in the Cerebrovascular Dysfunctions Associated with Alzheimer's Disease
Tong, X., Nicolakakis, N., Kocharyan, A., & Hamel, É. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4031-05.2005 · Cited by 153 · see citing works
Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease
Lau, J. C., Lerch, J. P., Sled, J. G., Henkelman, R. M., Evans, A. C., & Bedell, B. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.252 · Cited by 151 · see citing works
In vivo axonal transport rates decrease in a mouse model of Alzheimer's disease
Smith, K. D. B., Kallhoff, V., Zheng, H., & Pautler, R. G. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.01.046 · Cited by 150 · see citing works
Rapid Microglial Response Around Amyloid Pathology after Systemic Anti-Aβ Antibody Administration in PDAPP Mice
Koenigsknecht-Talboo, J., Meyer-Luehmann, M., Parsadanian, M., Garcia-Alloza, M., Finn, M. B., Hyman, B. T., Bacskai, B. J., & Holtzman, D. M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4147-08.2008 · Cited by 149 · see citing works
Multiple events lead to dendritic spine loss in triple transgenic Alzheimer’s disease mice
Bittner, T., Fuhrmann, M., Burgold, S., Ochs, S. M., Hoffmann, N., Mitteregger, G., Kretzschmar, H., LaFerla, F. M., & Herms, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015477 · Cited by 149 · see citing works
Micro MRI of the mouse brain using a novel 400 MHz cryogenic quadrature RF probe
Baltes, C., Radzwill, N., Bosshard, S., Marek, D., & Rudin, M. (2009) · NMR in Biomedicine · doi:10.1002/nbm.1396 · Cited by 149 · see citing works
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Imaging cerebral microbleeds using susceptibility weighted imaging: One step toward detecting vascular dementia
Ayaz, M., Boikov, A. S., Haacke, E. M., Kido, D. K., & Kirsch, W. M. (2009) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22001 · Cited by 148 · see citing works
Age-Dependent Cerebrovascular Abnormalities and Blood Flow Disturbances in APP23 Mice Modeling Alzheimer's Disease
Beckmann, N., Schuler, A., Mueggler, T., Meyer, E. P., Wiederhold, K., Staufenbiel, M., & Krucker, T. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-24-08453.2003 · Cited by 148 · see citing works
Self-citation
Treatment with an Amyloid-β Antibody Ameliorates Plaque Load, Learning Deficits, and Hippocampal Long-Term Potentiation in a Mouse Model of Alzheimer's Disease
Hartman, R. E., Izumi, Y., Bales, K. R., Paul, S. M., Wozniak, D. F., & Holtzman, D. M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0664-05.2005 · Cited by 147 · see citing works
Measuring blood volume and vascular transfer constant from dynamic, T‐weighted contrast‐enhanced MRI
Johnson, G., Wetzel, S. G., Cha, S., Babb, J. S., & Tofts, P. S. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20049 · Cited by 145 · see citing works
PK11195 labels activated microglia in Alzheimer's disease and in vivo in a mouse model using PET
Venneti, S., Lopresti, B. J., Wang, G., Hamilton, R. L., Mathis, C. A., Klunk, W. E., Apte, U. M., & Wiley, C. A. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.11.005 · Cited by 138 · see citing works
Staged decline of neuronal function in vivo in an animal model of Alzheimer's disease
Grienberger, C., Rochefort, N. L., Adelsberger, H., Henning, H. A., Hill, D. N., Reichwald, J., Staufenbiel, M., & Konnerth, A. (2012) · Nature Communications · doi:10.1038/ncomms1783 · Cited by 138 · see citing works
Capillary cerebral amyloid angiopathy is associated with vessel occlusion and cerebral blood flow disturbances
Thal, D. R., Capetillo-Zarate, E., Larionov, S., Staufenbiel, M., Zurbruegg, S., & Beckmann, N. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.01.017 · Cited by 138 · see citing works
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Cerebrovascular Dysfunction in Amyloid Precursor Protein Transgenic Mice: Contribution of Soluble and Insoluble Amyloid-β Peptide, Partial Restoration via γ-Secretase Inhibition
Han, B. H., Zhou, M.-L., Abousaleh, F., Brendza, R. P., Dietrich, H. H., Koenigsknecht-Talboo, J., Cirrito, J. R., Milner, E., Holtzman, D. M., & Zipfel, G. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4686-08.2008 · Cited by 138 · see citing works
Noninvasive in vivo MRI detection of neuritic plaques associated with iron in APP[V717I] transgenic mice, a model for Alzheimer's disease
Vanhoutte, G., Dewachter, I., Borghgraef, P., Leuven, F. V., & der Linden, A. V. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20385 · Cited by 137 · see citing works
In VivoPositron Emission Tomographic Imaging of Glial Responses to Amyloid-β and Tau Pathologies in Mouse Models of Alzheimer's Disease and Related Disorders
Maeda, J., Zhang, M.-R., Okauchi, T., Ji, B., Ono, M., Hattori, S., Kumata, K., Iwata, N., Saido, T. C., Trojanowski, J. Q., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3076-10.2011 · Cited by 136 · see citing works
Long-TermIn VivoImaging of β-Amyloid Plaque Appearance and Growth in a Mouse Model of Cerebral β-Amyloidosis
Hefendehl, J. K., Wegenast‐Braun, B. M., Liebig, C., Eicke, D., Milford, D., Calhoun, M. E., Kohsaka, S., Eichner, M., & Jucker, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5147-10.2011 · Cited by 136 · see citing works
Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease
O’Leary, T. P., & Brown, R. E. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.01.039 · Cited by 134 · see citing works
Parenchymal and vascular Aβ‐deposition and its effects on the degeneration of neurons and cognition in Alzheimer's disease
Thal, D. R., Griffin, W. S. T., & Braak, H. (2008) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00411.x · Cited by 134 · see citing works
Immunotherapy Reduces Vascular Amyloid- in PDAPP Mice
Schroeter, S., Khan, K., Barbour, R., Doan, M., Chen, M., Guido, T., Gill, D., Basi, G., Schenk, D., Seubert, P., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2377-07.2008 · Cited by 133 · cited 1× · see citing works
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Background
Impact of Angiotensin Receptor Blockers on Alzheimer Disease Neuropathology in a Large Brain Autopsy Series
Hajjar, I. M., Brown, L. L., Mack, W. J., & Chui, H. (2012) · Archives of Neurology · doi:10.1001/archneurol.2012.1010 · Cited by 131 · see citing works
Nonhypotensive Dose of Telmisartan Attenuates Cognitive Impairment Partially Due to Peroxisome Proliferator-Activated Receptor-γ Activation in Mice With Chronic Cerebral Hypoperfusion
Washida, K., Ihara, M., Nishio, K., Fujita, Y., Maki, T., Yamada, M., Takahashi, J., Wu, X., Kihara, T., Ito, H., et al. (2010) · Stroke · doi:10.1161/strokeaha.110.583948 · Cited by 131 · see citing works
Vasoactive effects of Aβin isolated human cerebrovessels and in a transgenic mouse model of Alzheimer's disease: Role of inflammation
Paris, D., Humphrey, J., Quadros, A., Patel, N., Crescentini, R., Crawford, F., & Mullan, M. (2003) · Neurological Research · doi:10.1179/016164103101201940 · Cited by 127 · see citing works
Siglec-9 is a novel leukocyte ligand for vascular adhesion protein-1 and can be used in PET imaging of inflammation and cancer
Aalto, K., Autio, A. K., Kiss, E. A., Elima, K., Nymalm, Y., Veres, T. Z., Marttila‐Ichihara, F., Elovaara, H., Saanijoki, T., Crocker, P. R., et al. (2011) · Blood · doi:10.1182/blood-2010-09-311076 · Cited by 127 · see citing works
Intracerebroventricular amyloid-β antibodies reduce cerebral amyloid angiopathy and associated micro-hemorrhages in aged Tg2576 mice
Thakker, D. R., Weatherspoon, M. R., Harrison, J., Keene, T. E., Lane, D. S., Kaemmerer, W. F., Stewart, G. R., & Shafer, L. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813404106 · Cited by 124 · see citing works
Hybrid FMT–CT imaging of amyloid-β plaques in a murine Alzheimer's disease model
Hyde, D. E., DEKLEINE, R., MacLaurin, S. A., Miller, E. L., BROOKS, D., Krucker, T., & Ntziachristos, V. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.038 · Cited by 123 · see citing works
Amyloid beta deposition is related to decreased glucose transporter-1 levels and hippocampal atrophy in brains of aged APP/PS1 mice
Hooijmans, C. R., Graven, C., Dederen, P. J. W. C., Tanila, H., van Groen, T., & Kiliaan, A. J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.08.063 · Cited by 121 · see citing works
Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging
Sun, S.-W., Song, S.-K., Harms, M. P., Lin, S.-J., Holtzman, D. M., Merchant, K. M., & Kotyk, J. J. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2004.09.006 · Cited by 121 · see citing works
Expression of intercellular adhesion molecule 1 (ICAM-1) in Alzheimer’s disease
Frohman, E. M., Frohman, T. C., Gupta, S., de Fougerolles, A., & van den Noort, S. (1991) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(91)90202-i · Cited by 120 · see citing works
Increased regional cerebral glucose uptake in an APP/PS1 model of Alzheimer's disease
Poisnel, G., Hérard, A., Tayara, N. E. T. E., Bourrin, E., Volk, A., Kober, F., Delatour, B., Delzescaux, T., Debeir, T., Rooney, T., et al. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.09.026 · Cited by 120 · see citing works
Impaired neurogenesis, neuronal loss, and brain functional deficits in the APPxPS1-Ki mouse model of Alzheimer's disease
Faure, A., Verret, L., Bozon, B., El Tannir El Tayara, N., Ly, M., Kober, F., Dhenain, M., Rampon, C., & Delatour, B. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.03.009 · Cited by 112 · see citing works
Multi-component apparent diffusion coefficients in human brain: Relationship to spin-lattice relaxation
Mulkern, R. V., Zengingönül, H. P., Robertson, R. L., Bogner, P., Zou, K. H., Guðbjartsson, H., Guttmann, C. R. G., Holtzman, D. H., Kyriakos, W. E., Jolesz, F. A., et al. (2000) · Magnetic Resonance in Medicine · doi:10.1002/1522-2594(200008)44:2 · Cited by 109 · see citing works
Bioluminescence imaging of Aβ deposition in bigenic mouse models of Alzheimer's disease
Watts, J. C., Giles, K., Grillo, S. K., Lemus, A., DeArmond, S. J., & Prusiner, S. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019034108 · Cited by 109 · see citing works
Amyloid-β Deposition Is Associated with Decreased Hippocampal Glucose Metabolism and Spatial Memory Impairment in APP/PS1 Mice
Sadowski, M., Pankiewicz, J. E., Scholtzova, H., Ji, Y., Quartermain, D., Jensen, C. H., Duff, K., Nixon, R. A., Gruen, R. J., & Wısnıewskı, T. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.5.418 · Cited by 108 · see citing works
Aging Increased Amyloid Peptide and Caused Amyloid Plaques in Brain of Old APP/V717I Transgenic Mice by a Different Mechanism than Mutant Presenilin1
Dewachter, I., Dorpe, J. V., Smeijers, L., Gilis, M., Kuipéri, C., Laenen, I., Caluwaerts, N., Moechars, D., Checler, F., Vanderstichele, H., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06452.2000 · Cited by 104 · see citing works
Statin therapy in Alzheimer's disease
Sparks, D. L., Sabbagh, M., Connor, D. J., Soares, H. D., Lopez, J., Stankovic, G. R., Johnson‐Traver, S., Ziolkowski, C. H. J., & Browne, P. J. (2006) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2006.00689.x · Cited by 104 · see citing works
Age related changes in brain metabolites observed by 1H MRS in APP/PS1 mice
Öberg, J., Spenger, C., Wang, F., Andersson, A. D. R., Westman, E., Skoglund, P., Sunnemark, D., Norinder, U., Klason, T., Wahlund, L., et al. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.03.002 · Cited by 103 · see citing works
Compromised Hemodynamic Response in Amyloid Precursor Protein Transgenic Mice
Mueggler, T., Sturchler, C., Kindler, D., Rausch, M., Staufenbiel, M., & Rudin, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07218.2002 · Cited by 103 · see citing works
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Prediction of hemorrhage in acute ischemic stroke using permeability MR imaging.
Kassner, A., Roberts, T. P. L., Taylor, K. S., Silver, F. L., & Mikulis, D. J. (2005) · PubMed Central · Cited by 102 · see citing works
Intravital imaging of amyloid plaques in a transgenic mouse model using optical-resolution photoacoustic microscopy
Hu, S., Yan, P., Maslov, K., Lee, J., & Wang, L. V. (2009) · Optics Letters · doi:10.1364/ol.34.003899 · Cited by 100 · see citing works
In vivo multiphoton imaging reveals gradual growth of newborn amyloid plaques over weeks
Burgold, S., Bittner, T., Dorostkar, M. M., Kieser, D., Fuhrmann, M., Mitteregger, G., Kretzschmar, H. A., Schmidt, B., & Herms, J. W. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0787-6 · Cited by 98 · see citing works
Early-onset subicular microvascular amyloid and neuroinflammation correlate with behavioral deficits in vasculotropic mutant amyloid β-protein precursor transgenic mice
Xu, F., Grande, A., Robinson, J. K., Previti, M. L., Vasek, M. J., Davis, J., & Nostrand, W. E. V. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.01.043 · Cited by 95 · see citing works
Analysis of input functions from different arterial branches with gamma variate functions and cluster analysis for quantitative blood volume measurements
Rausch, M., Scheffler, K., Rudin, M., & Radue, E. W. (2000) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(00)00219-8 · Cited by 95 · see citing works
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MR properties of rat sciatic nerve following trauma
Stanisz, G. J., Midha, R., Munro, C. A., & Henkelman, R. M. (2001) · Magnetic Resonance in Medicine · doi:10.1002/1522-2594(200103)45:3 · Cited by 95 · see citing works
Secondary microvascular degeneration in amyloid angiopathy of patients with hereditary cerebral hemorrhage with amyloidosis, Dutch type (HCHWA-D)
Vinters, H. V., Natté, R., Maat–Schieman, M. L. C., van Duinen, S. G., Hegeman-Kleinn, I. M., Welling‐Graafland, C., Haan, J., & Roos, R. A. C. (1998) · Acta Neuropathologica · doi:10.1007/s004010050793 · Cited by 92 · see citing works
Characterization of 7- and 19-month-old Tg2576 mice using multimodal in vivo imaging: limitations as a translatable model of Alzheimer's disease
Luo, F. R., Rustay, N. R., Ebert, U., Hradil, V. P., Cole, T. B., Llano, D. A., Mudd, S. R., Zhang, Y., Fox, G. B., & Day, M. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.08.005 · Cited by 88 · see citing works
Cognitive impairment in PDAPP mice depends on ApoE and ACT-catalyzed amyloid formation
Nilsson, L. N. G., Arendash, G. W., Leighty, R. E., Costa, D. A., Low, M. A., Garcia, M. F., Cracciolo, J. R., Rojiani, A. M., Wu, X., Bales, K. R., et al. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.12.011 · Cited by 87 · see citing works
In vivo evaluation of amyloid deposition and brain glucose metabolism of 5XFAD mice using positron emission tomography
Rojas, S., Herance, J. R., Gispert, J. D., Abad, S., Llongarriu, È. T., Jiménez, X., Pareto, D., Perpiñá, U., Sarroca, S., Rodrı́guez, E., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.12.027 · Cited by 87 · see citing works
Detection of Cerebral Microbleeds with Quantitative Susceptibility Mapping in the Arcabeta Mouse Model of Cerebral Amyloidosis
Klohs, J., Deistung, A., Schweser, F., Grandjean, J., Dominietto, M., Waschkies, C., Nitsch, R. M., Knuesel, I., Reichenbach, J. R., & Rudin, M. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2011.118 · Cited by 83 · see citing works
Self-citation
Longitudinal Amyloid Imaging in Mouse Brain with 11C-PIB: Comparison of APP23, Tg2576, and APPswe-PS1dE9 Mouse Models of Alzheimer Disease
Snellman, A., Lopez‐Picon, F. R., Rokka, J., Salmona, M., Forloni, G., Scheinin, M., Solin, O. H., Rinne, J. O., & Haaparanta‐Solin, M. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.110163 · Cited by 82 · see citing works
Age-Dependent Impairment of Somatosensory Response in the Amyloid Precursor Protein 23 Transgenic Mouse Model of Alzheimer's Disease
Mueggler, T., Kindler, D., Rausch, M., Staufenbiel, M., & Rudin, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08231.2003 · Cited by 81 · see citing works
Self-citation
Kinetics of Cerebral Amyloid Angiopathy Progression in a Transgenic Mouse Model of Alzheimer Disease
Robbins, E. M., Betensky, R. A., Domnitz, S. B., Purcell, S. M., Garcı́a-Alloza, M., Greenberg, C., Rebeck, G. W., Hyman, B. T., Greenberg, S. M., Frosch, M. P., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3854-05.2006 · Cited by 78 · see citing works
Early onset amyloid lesions lead to severe neuritic abnormalities and local, but not global neuron loss in APPPS1 transgenic mice
Rupp, N. J., Wegenast‐Braun, B. M., Radde, R., Calhoun, M. E., & Jucker, M. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.08.014 · Cited by 77 · see citing works
Can PET Data Differentiate Alzheimer's Disease from Vascular Dementia?
Nagata, K., MARUYA, H., Yuya, H., Terashi, H., Mito, Y., Kato, H., Sato, M., Satoh, Y., Watahiki, Y., Hirata, Y., et al. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06375.x · Cited by 77 · see citing works

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Jensen J. H. Chandra R. (2000). MR imaging of microvasculature. Magn. Reson. Med. 44, 224– 230 10.1002/1522-2594(200008)44:2<224::AID-MRM9>3.0.CO;2-M 10918321 · DOI

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Cerebrovascular Smooth Muscle Cells as the Drivers of Intramural Periarterial Drainage of the Brain
Aldea, R., Weller, R. O., Wilcock, D. M., Carare, R. O., & Richardson, G. W. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00001 · Cited by 335 · see citing works
Cerebrovascular pathology during the progression of experimental Alzheimer's disease
Giannoni, P., Arango-Lievano, M., das Neves, I., Rousset, M.-C., Baranger, K., Rivera, S., Jeanneteau, F. D., Claeysen, S., & Marchi, N. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.01.001 · Cited by 146 · see citing works
Causes and consequences of baseline cerebral blood flow reductions in Alzheimer’s disease
Bracko, O., Hernández, J. C. C., Park, L., Nishimura, N., & Schaffer, C. B. (2021) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x20982383 · Cited by 122 · see citing works
Where are we? The anatomy of the murine cortical meninges revisited for intravital imaging, immunology, and clearance of waste from the brain
Coles, J. A., Myburgh, E., Brewer, J. M., & McMenamin, P. G. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.002 · Cited by 123 · see citing works
A Review and Hypothesized Model of the Mechanisms That Underpin the Relationship Between Inflammation and Cognition in the Elderly
Fard, M. T., & Stough, C. K. K. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00056 · Cited by 121 · see citing works
An Integrated View on Vascular Dysfunction in Alzheimer’s Disease
Klohs, J. (2019) · Neurodegenerative Diseases · doi:10.1159/000505625 · Cited by 111 · see citing works
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Ultra High-Resolution In vivo Computed Tomography Imaging of Mouse Cerebrovasculature Using a Long Circulating Blood Pool Contrast Agent
Starosolski, Z. A., Villamizar, C., Rendon, D. A., Paldino, M. J., Milewicz, D. M., Ghaghada, K. B., & Annapragada, A. (2015) · Scientific Reports · doi:10.1038/srep10178 · Cited by 100 · see citing works
Cerebral small vessel disease and Alzheimer’s disease
Cai, Z., Wang, C., He, W., Tu, H., Tang, Z., Xiao, M., & Yan, L. (2015) · Clinical Interventions in Aging · doi:10.2147/cia.s90871 · Cited by 98 · see citing works
Ultrasound with microbubbles improves memory, ameliorates pathology and modulates hippocampal proteomic changes in a triple transgenic mouse model of Alzheimer's disease
Shen, Y., Hua, L., Yeh, C., Shen, L., Ying, M., Zhang, Z., Liu, G., Li, S., Chen, S., Chen, X., et al. (2020) · Theranostics · doi:10.7150/thno.44152 · Cited by 95 · see citing works
High fat diet worsens Alzheimer’s disease-related behavioral abnormalities and neuropathology in APP/PS1 mice, but not by synergistically decreasing cerebral blood flow.
Bracko, O., Vinarcsik, L. K., Cruz Hernández, J. C., Ruiz-Uribe, N. E., Haft-Javaherian, M., Falkenhain, K., Ramanauskaite, E. M., Ali, M., Mohapatra, A., Swallow, M. A., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-65908-y · Cited by 85 · see citing works
Neurovascular uncoupling in the triple transgenic model of Alzheimer's disease: Impaired cerebral blood flow response to neuronal-derived nitric oxide signaling
Lourenço, C. F., Ledo, A., Barbosa, R. M., & Laranjinha, J. A. N. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.01.013 · Cited by 84 · see citing works
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Additional file 4 of Cerebral amyloid angiopathy aggravates perivascular clearance impairment in an Alzheimer’s disease mouse model
Kim, S. H., Ahn, J. H., Yang, H., Lee, P., Koh, G. Y., & Jeong, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13199131
Additional file 3 of Cerebral amyloid angiopathy aggravates perivascular clearance impairment in an Alzheimer’s disease mouse model
Kim, S. H., Ahn, J. H., Yang, H., Lee, P., Koh, G. Y., & Jeong, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13199128
Additional file 2 of Cerebral amyloid angiopathy aggravates perivascular clearance impairment in an Alzheimer’s disease mouse model
Kim, S. H., Ahn, J. H., Yang, H., Lee, P., Koh, G. Y., & Jeong, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13199125
Additional file 1 of Cerebral amyloid angiopathy aggravates perivascular clearance impairment in an Alzheimer’s disease mouse model
Kim, S. H., Ahn, J. H., Yang, H., Lee, P., Koh, G. Y., & Jeong, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13199122
Additional file 5 of Cerebral amyloid angiopathy aggravates perivascular clearance impairment in an Alzheimer’s disease mouse model
Kim, S. H., Ahn, J. H., Yang, H., Lee, P., Koh, G. Y., & Jeong, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13199134

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Authors: Klohs, J., Rudin, M., Shimshek, D. R., & Beckmann, N.
Affiliations: University of Zurich (CH)
Novartis (Switzerland) (CH)
Corresponding author: Beckmann, Nicolau
ORCID: Klohs, Jan
Rudin, Markus
Shimshek, Derya R.
Beckmann, Nicolau
Venue: Frontiers in Aging Neuroscience
Publisher: Frontiers Media SA
Published: 2014-03-13
Volume: 6
Pages: 32-32
ISSN: 1663-4365 (ISSN-L)
DOI: 10.3389/fnagi.2014.00032
PMC: PMC3952109
OpenAlex: W2150972825
Cited by: 82
References: 281
Citations by year: 2026: 1 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 10 · 2020: 16 · 2019: 10 · 2018: 6 · 2017: 8 · 2016: 7 · 2015: 7 · 2014: 1
FWCI: 0.90
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Aging Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
ETH Zürich Research Collection (cc-by)
Zurich Open Repository and Archive (University of Zurich)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: Alzheimer's disease, cerebrovascular pathology, cerebral amyloid angiopathy, amyloid-beta deposition, amyloid-beta transport, vascular dysfunction, transgenic animal models, in vivo imaging, small animal imaging, hemodynamics, vascular inflammation, vascular integrity, neurovascular unit

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Imaging of cerebrovascular pathology in animal models of Alzheimer's disease

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