Neuroimaging of mouse models of Alzheimer’s disease

Jullienne, Amandine; Trinh, Michelle V.; Obenaus, Andre

doi:10.3390/biomedicines10020305

Cited by 33Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Neuroimaging of mouse models of Alzheimer’s disease

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Jullienne, Amandine, Trinh, Michelle V., Obenaus, Andre·2022·Biomedicines

DOI 10.3390/biomedicines10020305PMC PMC8869427

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Abstract

Magnetic resonance imaging (MRI) and positron emission tomography (PET) have made great strides in the diagnosis and our understanding of Alzheimer’s Disease (AD). Despite the knowledge gained from human studies, mouse models have and continue to play an important role in deciphering the cellular and molecular evolution of AD. MRI and PET are now being increasingly used to investigate neuroimaging features in mouse models and provide the basis for rapid translation to the clinical setting. Here, we provide an overview of the human MRI and PET imaging landscape as a prelude to an in-depth review of preclinical imaging in mice. A broad range of mouse models recapitulate certain aspects of the human AD, but no single model simulates the human disease spectrum. We focused on the two of the most popular mouse models, the 3xTg-AD and the 5xFAD models, and we summarized all known published MRI and PET imaging data, including contrasting findings. The goal of this review is to provide the reader with broad framework to guide future studies in existing and future mouse models of AD. We also highlight aspects of MRI and PET imaging that could be improved to increase rigor and reproducibility in future imaging studies.

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Age-related brain atrophy and myelin loss are observed on advanced high-field MRI in the 3×Tg-AD model.
“Alongside the progression of AD pathology, age-related brain atrophy and myelin loss are observed on advanced high-field MRI (Ni, 2021; Jullienne et al., 2022; Bergamino et al., 2023).”
From Multimodal MRI combined with RNA sequencing reveals pathological signatures in the 9-month-old 3×Tg-AD mouse brain (2026) · cites this paper as Jullienne et al., 2022
Section 4.2.1 reports MRI-observed cortical atrophy in 18-month-old 3xTg-AD mice, and the Summary describes volumetric declines with increasing age. But section 4.2.4 reports no changes in myelin staining in mice aged 11–17 months; it does not support the claimed myelin loss. The supplied passages do not establish that these findings were observed specifically on high-field MRI (page numbers unavailable). (LLM, conf=0.87)
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Evaluation of the neuroprotective effect of taurine in Alzheimer’s disease using functional molecular imaging
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Early pathologic amyloid induces hypersynchrony of BOLD resting‐state networks in transgenic mice and provides an early therapeutic window before amyloid plaque deposition
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White matter alterations in early‐stage Alzheimer's disease: A tract‐specific study
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“…[121], Qin et al., 2013 [182], Shu et al., 2013 [183] MRI–multishell dMRI Increased ODI Decreased NDI Increased intracellular volume fraction (ICVF) Wen et al., 2019 [47], Fu et al., 2020 [48] Colgan et al., 2016 [189], Colon-Perez et al., 2019 [191] The reader should note that there exist…”
Background
Age-Dependent Modulation of Synaptic Plasticity and Insulin Mimetic Effect of Lipoic Acid on a Mouse Model of Alzheimer’s Disease
Sancheti, H., Akopian, G. K., Yin, F., Brinton, R. D., Walsh, J. P., & Cadenas, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069830 · Cited by 95 · see citing works
Microstructural White Matter Alterations in Mild Cognitive Impairment and Alzheimer’s Disease
Fu, X., Shrestha, S., Sun, M., Wu, Q., Luo, Y., Zhang, X., Yin, J., & Ni, H. (2019) · Clinical Neuroradiology · doi:10.1007/s00062-019-00805-0 · Cited by 95 · see citing works
Longitudinal neuroimaging biomarkers differ across Alzheimer’s disease phenotypes
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In vivo imaging of tau pathology using multi-parametric quantitative MRI
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Neuroprotective effects of bee venom phospholipase A2 in the 3xTg AD mouse model of Alzheimer’s disease
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Diffusion Magnetic Resonance Imaging-Based Biomarkers for Neurodegenerative Diseases
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Subtle behavioral changes and increased prefrontal-hippocampal network synchronicity in APPNL−G−F mice before prominent plaque deposition
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Does Microglial Activation Influence Hippocampal Volume and Neuronal Function in Alzheimer’s Disease and Parkinson’s Disease Dementia?
Femminella, G. D., Ninan, S., Atkinson, R., Fan, Z., Brooks, D. J., & Edison, P. (2016) · Journal of Alzheimer’s Disease · doi:10.3233/jad-150827 · Cited by 88 · 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
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Three-dimensional analysis of synaptic organization in the hippocampal CA1 field in Alzheimer’s disease
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In vivo evaluation of amyloid deposition and brain glucose metabolism of 5XFAD mice using positron emission tomography
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In vivo Imaging of Glial Activation in Alzheimer's Disease
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<i>In vivo</i> imaging of microglial activation by positron emission tomography with <scp>[<sup>11</sup>C]PBR28</scp> in the <scp>5XFAD</scp> model of <scp>A</scp>lzheimer's disease
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Age-Dependent Impairment of Somatosensory Response in the Amyloid Precursor Protein 23 Transgenic Mouse Model of Alzheimer's Disease
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Fluorodeoxyglucose-Positron Emission Tomography in the differential diagnosis of early-onset dementia: a prospective, community-based study
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Early Detection of Cerebral Glucose Uptake Changes in the 5XFAD Mouse
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Contributions of a high-fat diet to Alzheimer’s disease-related decline: A longitudinal behavioural and structural neuroimaging study in mouse models
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The Validity and Reliability of 6 Sets of Clinical Criteria to Classify Alzheimer’s Disease and Vascular Dementia in Cases Confirmed Post-Mortem: Added Value of a Decision Tree Approach
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Longitudinal assessment of Alzheimer's β‐amyloid plaque development in transgenic mice monitored by in vivo magnetic resonance microimaging
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Role of Myo-Inositol by Magnetic Resonance Spectroscopy in Early Diagnosis of Alzheimer’s Disease in APP/PS1 Transgenic Mice
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MICEST: A potential tool for non-invasive detection of molecular changes in Alzheimer's disease
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A multicenter 1 H-MRS study of the medial temporal lobe in AD and MCI
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Gray and white matter degeneration revealed by diffusion in an Alzheimer mouse model
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Impaired Eyeblink Conditioning and Decreased Hippocampal Volume in PDAPP V717F Mice
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Early Alterations in Functional Connectivity and White Matter Structure in a Transgenic Mouse Model of Cerebral Amyloidosis
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In vivo PET imaging of neuroinflammation in Alzheimer’s disease
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Age-related decline in white matter integrity in a mouse model of tauopathy: an in vivo diffusion tensor magnetic resonance imaging study
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Ensemble Classification of Alzheimer's Disease and Mild Cognitive Impairment Based on Complex Graph Measures from Diffusion Tensor Images
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Significance of Blood and Cerebrospinal Fluid Biomarkers for Alzheimer’s Disease: Sensitivity, Specificity and Potential for Clinical Use
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Noninvasive Magnetic Resonance Imaging Detection of Cerebral Amyloid Angiopathy-Related Microvascular Alterations Using Superparamagnetic Iron Oxide Particles in APP Transgenic Mouse Models of Alzheimer's Disease: Application to Passive Aβ Immunotherapy
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Resting-state abnormalities in amnestic mild cognitive impairment: a meta-analysis
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Volumetric MRI and MRS provide sensitive measures of Alzheimer's disease neuropathology in inducible Tau transgenic mice (rTg4510)
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Imaging the microvessel caliber and density: Principles and applications of microvascular MRI
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A longitudinal multimodal in vivo molecular imaging study of the 3xTg-AD mouse model shows progressive early hippocampal and taurine loss
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Cortical atrophy and hypoperfusion in a transgenic mouse model of Alzheimer's disease
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Long-term RF exposure on behavior and cerebral glucose metabolism in 5xFAD mice
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Regional hypometabolism in the 3xTg mouse model of Alzheimer's disease
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Intraneuronal amyloid β and reduced brain volume in a novel APP T714I mouse model for Alzheimer's disease
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Restricted diffusion in the brain of transgenic mice with cerebral amyloidosis
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1H NMR Metabolomic Signatures in Five Brain Regions of the AβPPswe Tg2576 Mouse Model of Alzheimer's Disease at Four Ages
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Genetics of Alzheimer’s Disease: the Importance of Polygenic and Epistatic Components
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Quantitative MRI reveals aging‐associated T2 changes in mouse models of Alzheimer's disease
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Proton and Phosphorus Magnetic Resonance Spectroscopy of a Mouse Model of Alzheimer's Disease
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Inhibition of Colony-Stimulating Factor 1 Receptor by PLX3397 Prevents Amyloid Beta Pathology and Rescues Dopaminergic Signaling in Aging 5xFAD Mice
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Hypermetabolic State in the 7-Month-Old Triple Transgenic Mouse Model of Alzheimer'S Disease and the Effect of Lipoic Acid: A 13C-NMR Study
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Diffusion kurtosis imaging to detect amyloidosis in an APP/PS1 mouse model for Alzheimer's disease
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Genetic quality assurance and genetic monitoring of laboratory mice and rats: FELASA Working Group Report
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Characterization and preclinical evaluation of the cGMP grade DNA based vaccine, AV-1959D to enter the first-in-human clinical trials
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Self-citation
Remote sites of structural atrophy predict later amyloid formation in a mouse model of Alzheimer's disease
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The human hippocampus and its subfield volumes across age, sex and APOE e4 status
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Long-term Dantrolene Treatment Reduced Intraneuronal Amyloid in Aged Alzheimer Triple Transgenic Mice
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Spatial learning and memory impairments are associated with increased neuronal activity in 5XFAD mouse as measured by manganese-enhanced magnetic resonance imaging
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Design of a multivalent bifunctional chelator for diagnostic 64 Cu PET imaging in Alzheimer’s disease
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Deficits in axonal transport in hippocampal-based circuitry and the visual pathway in APP knock-out animals witnessed by manganese enhanced MRI
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Small-Animal PET Imaging of Tau Pathology with 18F-THK5117 in 2 Transgenic Mouse Models
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Monitoring blood flow alterations in the Tg2576 mouse model of Alzheimer's disease by in vivo magnetic resonance angiography at 17.6T
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Regional metabolic alteration of Alzheimer's disease in mouse brain expressing mutant human APP-PS1 by 1H HR-MAS☆
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Sex- and age-specific modulation of brain GABA levels in a mouse model of Alzheimer's disease
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Voxel-based diffusion tensor imaging of an APP/PS1 mouse model of Alzheimer’s disease.
Shu, X., Qin, Y.-Y., Zhang, S., Jiang, J.-J., Zhang, Y., Zhao, L.-Y., Shan, D., & Zhu, W.-Z. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8418-6 · Cited by 41 · see citing works
Neurite orientation dispersion and density imaging reveals white matter and hippocampal microstructure changes produced by Interleukin-6 in the TgCRND8 mouse model of amyloidosis
Colon-Perez, L. M., Ibanez, K. R., Suarez, M., Torroella, K., Acuna, K., Ofori, E., Levites, Y., Vaillancourt, D. E., Golde, T. E., Chakrabarty, P., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116138 · Cited by 41 · see citing works
The fornix provides multiple biomarkers to characterize circuit disruption in a mouse model of Alzheimer’s disease.
Badea, A., Kane, L., Anderson, R. J., Qi, Y., Foster, M., Cofer, G. P., Medvitz, N., Buckley, A. F., Badea, A. K., Wetsel, W. C., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.08.014 · Cited by 39 · see citing works
Uses of Human MR and PET Imaging in Research of Neurodegenerative Brain Diseases
Schwarz, C. G. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01030-9 · Cited by 39 · see citing works
A stereotaxic MRI template set of mouse brain with fine sub-anatomical delineations: Application to MEMRI studies of 5XFAD mice
Nie, B., Wu, D., Liang, S., Liu, H., Sun, X., Li, P., Huang, Q., Zhang, T., Feng, T., Ye, S., et al. (2018) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2018.10.014 · Cited by 39 · see citing works
Evaluation of white matter integrity in ex vivo brains of amyloid plaque-bearing APPsw transgenic mice using magnetic resonance diffusion tensor imaging
Harms, M. P., Kotyk, J. J., & Merchant, K. M. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.01.002 · Cited by 38 · see citing works
Autoregulation of Cerebral Blood Flow to Changes in Arterial Pressure in Mild Alzheimer's Disease
Zazulia, A. R., Videen, T. O., Morris, J. C., & Powers, W. J. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.135 · Cited by 38 · see citing works
Early cortical thickness changes predict β-amyloid deposition in a mouse model of Alzheimer's disease
Grand’Maison, M., Zehntner, S. P., Ho, M., Hébert, F., Wood, A., Carbonell, F., Zijdenbos, A. P., Hamel, É., & Bedell, B. J. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.02.005 · Cited by 38 · see citing works
Vascular pathology of 20-month-old hypercholesterolemia mice in comparison to triple-transgenic and APPSwDI Alzheimer's disease mouse models
Hohsfield, L. A., Daschil, N., Orädd, G., Strömberg, I., & Humpel, C. (2014) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2014.10.006 · Cited by 37 · see citing works
Longitudinal evaluation of a novel BChE PET tracer as an early in vivo biomarker in the brain of a mouse model for Alzheimer disease
Rejc, L., Gómez‐Vallejo, V., Joya, A., Moreno, Ó., Egimendia, A., Castellnou, P., Ríos, X., Cossío, U., Baz, Z., Passannante, R., et al. (2021) · Theranostics · doi:10.7150/thno.54589 · Cited by 37 · see citing works
Detection of vascular alterations by in vivo magnetic resonance angiography and histology in APP/PS1 mouse model of Alzheimer’s disease
Tayara, N. E. T. E., Delatour, B., Volk, A., & Dhénain, M. (2010) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-009-0194-y · Cited by 36 · see citing works
Combination therapy in a transgenic model of Alzheimer's disease
Aytan, N., Choi, J., Carreras, I., Kowall, N. W., Jenkins, B. G., & Dedeoglu, A. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.10.001 · Cited by 36 · see citing works
Evidence in support of chromosomal sex influencing plasma based metabolome vs APOE genotype influencing brain metabolome profile in humanized APOE male and female mice
Shang, Y., Mishra, A., Wang, T., Wang, Y., Desai, M. K., Chen, S., Mao, Z., Do, L., Bernstein, A. S., Trouard, T. P., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0225392 · Cited by 36 · see citing works
In vivo Imaging With 18F-FDG- and 18F-Florbetaben-PET/MRI Detects Pathological Changes in the Brain of the Commonly Used 5XFAD Mouse Model of Alzheimer's Disease
Franke, T. N., Irwin, C., Bayer, T. A., Brenner, W., Beindorff, N., Bouter, C., & Bouter, Y. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00529 · Cited by 36 · see citing works
Brain metabolism in tau and amyloid mouse models of Alzheimer's disease: An MRI study
Wei, Z., Xu, J., Chen, L., Hirschler, L., Barbier, E., Li, T., Wong, P. C., & Lu, H. (2021) · NMR in Biomedicine · doi:10.1002/nbm.4568 · Cited by 36 · see citing works
PET imaging of reactive astrocytes in neurological disorders
Liu, Y., Jiang, H., Qin, X., Tian, M., & Zhang, H. (2021) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-021-05640-5 · Cited by 35 · see citing works
Functional and structural connectome properties in the 5XFAD transgenic mouse model of Alzheimer’s disease
Kesler, S. R., Acton, P., Rao, V., & Ray, W. J. (2018) · Network Neuroscience · doi:10.1162/netn_a_00048 · Cited by 34 · cited 3× · see citing works
“In male 5xFAD mice, the authors showed that structural networks exhibited higher path lengths and a lower small-worldness in 6-month-old 5xFAD mice compared to controls [75].”
BackgroundMethodInfluential
Contrast-enhanced MR microscopy of amyloid plaques in five mouse models of amyloidosis and in human Alzheimer’s disease brains.
Dudeffant, C., Vandesquille, M., Herbert, K., Garin, C. M., Alves, S., Blanchard, V., Comoy, E. E., Petit, F., & Dhenain, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-05285-1 · Cited by 34 · see citing works
Butyrylcholinesterase-knockout reduces fibrillar β-amyloid and conserves 18FDG retention in 5XFAD mouse model of Alzheimer’s disease
DeBay, D. R., Reid, G. A., Macdonald, I. R., Mawko, G., Burrell, S., Martin, E. V., Bowen, C. V., & Darvesh, S. (2017) · Brain Research · doi:10.1016/j.brainres.2017.07.009 · Cited by 33 · see citing works
Hybrid PET/MRI enables high-spatial resolution, quantitative imaging of amyloid plaques in an Alzheimer’s disease mouse model
Frost, G. R., Longo, V. A., Li, T., Jonas, L. A., Judenhofer, M. S., Cherry, S. R., Koutcher, J. A., Lekaye, C., ZANZONICO, P. B., & Li, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-67284-z · Cited by 33 · see citing works
Increased Cerebral Vascular Reactivity in the Tau Expressing rTg4510 Mouse: Evidence against the Role of Tau Pathology to Impair Vascular Health in Alzheimer's Disease
Wells, J. A., Holmes, H. E., O’Callaghan, J. M., Colgan, N. C., Ismail, O., Fisher, E., Siow, B. M., Murray, T. K., Schwarz, A. J., O’Neill, M. J., et al. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.224 · Cited by 32 · see citing works
R-flurbiprofen improves tau, but not Aß pathology in a triple transgenic model of Alzheimer's disease
Carreras, I., McKee, A. C., Choi, J., Aytan, N., Kowall, N. W., Jenkins, B. G., & Dedeoglu, A. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.025 · Cited by 32 · see citing works
Evaluation of Class IIa Histone Deacetylases Expression and In Vivo Epigenetic Imaging in a Transgenic Mouse Model of Alzheimer’s Disease
Chen, Y., Lu, C.-H., Ke, C., Chiu, S.-J., Chang, C., Yang, B., Gelovani, J. G., & Liu, R.-S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168633 · Cited by 32 · see citing works
Early-in-life neuroanatomical and behavioural trajectories in a triple transgenic model of Alzheimer’s disease
Kong, V., Devenyi, G. A., Gallino, D., Ayranci, G., Germann, J., Rollins, C., & Chakravarty, M. M. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1691-4 · Cited by 32 · see citing works
Head-to-head comparison of 11C-PiB and 18F-FC119S for Aβ imaging in healthy subjects, mild cognitive impairment patients, and Alzheimer's disease patients
Byun, B. H., Kim, B. I., Park, S. Y., Ko, I. O., Lee, K. C., Kim, K. M., Kim, Y. K., Lee, J., Bu, S. H., Kim, J. H., et al. (2017) · Medicine · doi:10.1097/md.0000000000006441 · Cited by 31 · see citing works
Partial Inhibition of Mitochondrial Complex I Reduces Tau Pathology and Improves Energy Homeostasis and Synaptic Function in 3xTg-AD Mice
Stojakovic, A., Chang, S.-Y., Nesbitt, J. J., Pichurin, N. P., Ostroot, M., Aikawa, T., Kanekiyo, T., & Trushina, E. V. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-201015 · Cited by 31 · see citing works
Microvascular cerebral blood volume changes in aging APPswe/PS1dE9 AD mouse model: a voxel-wise approach
Zerbi, V., Jansen, D., Dederen, P. J. W. C., Veltien, A. A., Hamans, B. C., Liu, Y., Heerschap, A., & Kiliaan, A. J. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0448-8 · Cited by 31 · see citing works
Quantitative evaluation of MRI and histological characteristics of the 5xFAD Alzheimer mouse brain
Spencer, N. G., Bridges, L., Elderfield, K., Amir, K., Austen, B., & Howe, F. A. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.071 · Cited by 30 · see citing works
Aβ pathology downregulates brain mGluR5 density in a mouse model of Alzheimer
Lee, M., Lee, H., Park, I. S., Park, J. A., Kwon, Y., Ryu, Y. H., Kim, C. H., Kang, J. H., Hyun, I. Y., Lee, K. C., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.02.003 · Cited by 30 · see citing works
Association of Memory Impairment With Concomitant Tau Pathology in Patients With Cerebral Amyloid Angiopathy
Schoemaker, D., Charidimou, A., Zotin, M. C. Z., Raposo, N., Johnson, K. A., Sanchez, J. S., Greenberg, S. M., & Viswanathan, A. (2021) · Neurology · doi:10.1212/wnl.0000000000011745 · Cited by 30 · see citing works
Alzheimer’s disease: a tale of two diseases?
Nardini, E., Hogan, R., Flamier, A., & Bernier, G. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.308070 · Cited by 30 · see citing works
N-acetylaspartate, choline, myoinositol, glutamine and glutamate (glx) concentration changes in proton MR spectroscopy (1H MRS) in patients with mild cognitive impairment (MCI)
Walecki, J. M., Barcikowska, M., Ćwikła, J. B., & Gabryelewicz, T. (2011) · Medical Science Monitor · doi:10.12659/msm.882112 · Cited by 29 · see citing works
In vivo detection of gray matter neuropathology in the 3xTg mouse model of alzheimer’s disease with diffusion tensor imaging.
Snow, W. M., Dale, R., O’Brien-Moran, Z., Buist, R., Peirson, D., Martin, M., & Albensi, B. C. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170136 · Cited by 29 · see citing works
Striatum and entorhinal cortex atrophy in AD mouse models: MRI comprehensive analysis
Micotti, E., Paladini, A., Balducci, C., Tolomeo, D., Frasca, A., Marizzoni, M., Filibian, M., Caroli, A., Valbusa, G., Dix, S. L., et al. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.10.027 · Cited by 28 · see citing works
Cerebrospinal Fluid Amyloid Beta, Tau Levels, Apolipoprotein, and 1H-MRS Brain Metabolites in Alzheimer's Disease: A Systematic Review
Piersson, A. D., Mohamad, M., Rajab, F., & Suppiah, S. (2020) · Academic Radiology · doi:10.1016/j.acra.2020.06.006 · Cited by 28 · see citing works
Automated Detection of Amyloid-β-Related Cortical and Subcortical Signal Changes in a Transgenic Model of Alzheimer's Disease using High-Field MRI
Teipel, S. J., Kaza, E., Hadlich, S., Bauer, A. J., Brüning, T., Plath, A.-S., Krohn, M., Scheffler, K., Walker, L. C., Lotze, M., et al. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101035 · Cited by 28 · see citing works
Specific white matter tracts and diffusion properties predict conversion from mild cognitive impairment to Alzheimer’s disease.
Stone, D. B., Ryman, S. G., Hartman, A. P., Wertz, C. J., Vakhtin, A. A., & Initiative, A. D. N. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.711579 · Cited by 28 · see citing works
Parkin prevents cortical atrophy and Aβ-induced alterations of brain metabolism: 13C NMR and magnetic resonance imaging studies in AD models
Algarzae, N. K., Hebron, M. L., Miessau, M., & Moussa, C. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.057 · Cited by 27 · see citing works
Association of Amyloid Burden, Brain Atrophy and Memory Deficits in Aged Apolipoprotein ε4 Mice
Yin, J., Turner, G. H., Coons, S. W., Maalouf, M., Reiman, E. M., & Shi, J. (2014) · Current Alzheimer Research · doi:10.2174/156720501103140329220007 · Cited by 27 · see citing works
Longitudinal Magnetic Resonance Spectroscopy as Marker of Cognitive Deterioration in Mild Cognitive Impairment
Modrego, P., & Fayed, N. (2011) · American Journal of Alzheimers Disease & Other Dementias · doi:10.1177/1533317511433809 · Cited by 26 · see citing works
Magnetic resonance spectroscopy analysis of neurochemical changes in the atrophic hippocampus of APP/PS1 transgenic mice
Liang, S., Huang, J., Liu, W., Jin, H., Li, L., Zhang, X., Nie, B., Lin, R., Tao, J., Zhao, S., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.08.005 · Cited by 26 · see citing works
Imaging Transcriptomics in Neurodegenerative Diseases
Mroczek, M., Desouky, A., & Sirry, W. (2020) · Journal of Neuroimaging · doi:10.1111/jon.12827 · Cited by 26 · see citing works
Gray matter changes related to microglial activation in Alzheimer's disease
Nicastro, N., Malpetti, M., Mak, E., Williams, G. B., Bevan-Jones, W. R., Carter, S. F., Passamonti, L., Fryer, T., Hong, Y. T., Aigbirhio, F., et al. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.06.010 · Cited by 25 · see citing works
Diffusion MRI detects basal forebrain cholinergic abnormalities in the 3xTg‐AD mouse model of Alzheimer's disease
Falangola, M. F., Nie, X., Ward, R., Dhiman, S., Voltin, J., Nietert, P. J., & Jensen, J. H. (2021) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2021.06.022 · Cited by 25 · see citing works
Effects of glucose, insulin, and insulin resistance on cerebral 18F-FDG distribution in cognitively normal older subjects
Ishibashi, K., Onishi, A., Fujiwara, Y., Ishiwata, K., & Ishii, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181400 · Cited by 24 · see citing works
Systematic Evaluation of Magnetic Resonance Imaging and Spectroscopy Techniques for Imaging a Transgenic Model of Alzheimer's Disease (AβPP/PS1)
Esteras, N., Alquézar, C., Bartolomé, F. B., Antequera, D., Barrios, L., Carro, E., Cerdán, S., & Martín‐Requero, Á. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-111967 · Cited by 23 · see citing works
Magnetic resonance spectroscopy in vivo of neurochemicals in a transgenic model of Alzheimer's disease: A longitudinal study of metabolites, relaxation time, and behavioral analysis in TASTPM and wild‐type mice
Forster, D. M., Davies, K. E., & Williams, S. R. (2012) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24349 · Cited by 23 · see citing works
APPswe/PS1dE9 mice with cortical amyloid pathology show a reduced NAA/Cr ratio without apparent brain atrophy: A MRS and MRI study
Kuhla, A., Rühlmann, C., Lindner, T., Polei, S., Hadlich, S., Krause, B. J., Vollmar, B., & Teipel, S. J. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.06.009 · Cited by 23 · see citing works
Early Detection of Aβ Deposition in the 5xFAD Mouse by Amyloid PET
Oh, S. J., Lee, H., Kang, K. J., Han, S. J., Lee, Y. J., Lee, K. C., Lim, S. M., Yoon, D., Kim, K. M., Park, J. A., et al. (2018) · Contrast Media & Molecular Imaging · doi:10.1155/2018/5272014 · Cited by 23 · see citing works
Neurofibrillary tangles and plaques are not accompanied by white matter pathology in aged triple transgenic-Alzheimer disease mice
Kastyak-Ibrahim, M. Z., Di Curzio, D. L., Buist, R., Herrera, S. L., Albensi, B. C., Del Bigio, M. R., & Martin, M. (2013) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2013.06.013 · Cited by 23 · see citing works
Age‑ and brain region‑associated alterations of cerebral blood flow in early Alzheimer's disease assessed in AβPPSWE/PS1ΔE9 transgenic mice using arterial spin labeling
Guo, Y., Li, X., Zhang, M., Chen, N., Wu, S., Lei, J., Wang, Z., Wang, R., Wang, J., & Liu, H. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.9950 · Cited by 23 · see citing works
Standardized Herbal Formula PM012 Decreases Cognitive Impairment and Promotes Neurogenesis in the 3xTg AD Mouse Model of Alzheimer’s Disease
Ye, M., Chung, H., An, Y. H., Lim, S.-J., Choi, W., Yu, A., Kim, J. S., Kang, M., Cho, S., Shim, I., et al. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9458-x · Cited by 22 · see citing works
PET Imaging in Huntington’s Disease
Roussakis, A., & Piccini, P. P. (2015) · Journal of Huntington s Disease · doi:10.3233/jhd-150171 · Cited by 22 · see citing works
Alterations of functional circuitry in aging brain and the impact of mutated APP expression
Bearer, E. L., Manifold-Wheeler, B. C., Medina, C. S., Gonzales, A., Chaves, F. L., & Jacobs, R. E. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.06.018 · Cited by 22 · see citing works
Multifaceted assessment of the APP/PS1 mouse model for Alzheimer’s disease: Applying MRS, DTI, and ASL
Shen, Z., Lei, J., Li, X., Wang, Z., Bao, X., & Wang, R. (2018) · Brain Research · doi:10.1016/j.brainres.2018.08.001 · Cited by 22 · see citing works
Diffusion MRI detects longitudinal white matter changes in the 3xTg-AD mouse model of Alzheimer's disease
Nie, X., Falangola, M. F., Ward, R., McKinnon, E. T., Helpern, J. A., Nietert, P. J., & Jensen, J. H. (2019) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2018.12.003 · Cited by 22 · see citing works
Reduction of hippocampal N‐acetyl aspartate level in aged APPSwe/PS1dE9 transgenic mice is associated with degeneration of CA3 pyramidal neurons
Xu, W., Zhan, Y., Huang, W., Wang, X., Zhang, S., & Lei, H. C. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22479 · Cited by 21 · see citing works
Differential effects of apoE and apoJ mimetic peptides on the action of an anti-Aβ scFv in 3xTg-AD mice
Montoliu‐Gaya, L., Güell‐Bosch, J., Esquerda-Canals, G., Roda, A. R., Serra-Mir, G., Lope‐Piedrafita, S., Sánchez‐Quesada, J. L., & Villegas, S. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.07.012 · Cited by 21 · see citing works

Flagged first, then by citations

3 of the 232 references couldn’t be matched to a known paper.

Sorted by citations

Alcohol Use Disorder and Dementia: A Review
Zahr, N. M. (2024) · Alcohol research · doi:10.35946/arcr.v44.1.03 · Cited by 38 · see citing works
Cortical cerebrovascular and metabolic perturbations in the 5xFAD mouse model of Alzheimer’s disease
Jullienne, A., Szu, J. I., Quan, R., Trinh, M. V., Norouzi, T., Noarbe, B. P., Bedwell, A. A., Eldridge, K., Persohn, S. A., Territo, P. R., et al. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1220036 · Cited by 30 · see citing works
Self-citation
Astrocyte-specific knockout of YKL-40/Chi3l1 reduces Aβ burden and restores memory functions in 5xFAD mice
Zeng, X., Cheung, S. K. K., Shi, M., Or, P. M. Y., Li, Z., Liu, J. Y. H., Ho, W. L.-H., Liu, T., Lu, K., Rudd, J. A., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02970-z · Cited by 27 · see citing works
Advancing Alzheimer’s Therapeutics: Exploring the Impact of Physical Exercise in Animal Models and Patients
Andrade-Guerrero, J., Rodríguez-Arellano, P., Barron-Leon, N., Orta‐Salazar, E., Ledesma-Alonso, C., Díaz-Cintra, S. Y., & Soto-Rojas, L. O. (2023) · Cells · doi:10.3390/cells12212531 · Cited by 27 · see citing works
Progressive Vascular Abnormalities in the Aging 3xTg-AD Mouse Model of Alzheimer’s Disease
Jullienne, A., Quan, R., Szu, J. I., Trinh, M. V., Behringer, E. J., & Obenaus, A. (2022) · Biomedicines · doi:10.3390/biomedicines10081967 · Cited by 19 · see citing works
Self-citation
Neurodegenerative changes in the brains of the 5xFAD Alzheimer's disease model mice investigated by high‐field and high‐resolution magnetic resonance imaging and multi‐nuclei magnetic resonance spectroscopy
Yoo, C.-H., Kim, J., Baek, H.-M., Chang, K.-A., & Choe, B.-Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065073 · Cited by 13 · see citing works
Age-dependent microstructure alterations in 5xFAD mice by high-resolution diffusion tensor imaging
Maharjan, S., Tsai, A. P., Lin, P. B., Ingraham, C., Jewett, M. R., Landreth, G. E., Oblak, A. L., & Wang, N. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.964654 · Cited by 11 · see citing works
“Different MRI techniques have been used to study the brain structure and function of 5xFAD mice (Mlynarik et al., 2012; Igarashi et al., 2020; Jullienne et al., 2022).”
Method
Abnormal [18F]NIFENE binding in transgenic 5xFAD mouse model of Alzheimer's disease: In vivo PET/CT imaging studies of α4β2* nicotinic acetylcholinergic receptors and in vitro correlations with Aβ plaques
Liang, C., Nguyen, G. A. H., Danh, T. B., Sandhu, A. K., Melkonyan, L. L., Syed, A. U., & Mukherjee, J. (2023) · Synapse · doi:10.1002/syn.22265 · Cited by 11 · see citing works
Characterization of cerebrovascular changes in Alzheimer’s disease mice by photoacoustic imaging
Li, X., Zhang, Z., Shi, H., & Zhou, F. (2024) · Journal of Innovative Optical Health Sciences · doi:10.1142/s179354582450007x · Cited by 9 · see citing works
Apolipoprotein-E deficiency leads to brain network alteration characterized by diffusion MRI and graph theory
Stapleton, M. C., Koch, S., Cortes, D. R. E., Wyman, S. K., Schwab, K. E., Mueller, S. G., McKennan, C. G., Boehm‐Sturm, P., & Wu, Y. L. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1183312 · Cited by 6 · see citing works
Astrocytes, via RTP801, contribute to cognitive decline by disrupting GABAergic‐regulated connectivity and driving neuroinflammation in an Alzheimer's disease mouse model
Chicote‐González, A., Solana‐Balaguer, J., Garcia‐Segura, P., Campoy‐Campos, G., Pérez, I. P., Pérez‐Navarro, E., Rodríguez, M. J., Alberch, J., Giralt, A., Sòria, G., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70051 · Cited by 7 · see citing works
Exercise-induced modulation of miRNAs and gut microbiome: a holistic approach to neuroprotection in Alzheimer’s disease
Wang, R., Li, J., Li, X., Guo, Y., Chen, P., & Tian, P. (2025) · Reviews in the Neurosciences · doi:10.1515/revneuro-2025-0013 · Cited by 7 · see citing works
WhatNIs N-ough for MRI-Based Animal Neuroimaging?
Grandjean, J., Lake, E. M. R., Pagani, M., & Mandino, F. (2024) · eNeuro · doi:10.1523/eneuro.0531-23.2024 · Cited by 5 · see citing works
Interferon-induced protein IFIT3 as a molecular nexus of neuroinflammation in Alzheimer’s disease and HIV-associated neurocognitive disorders
Das, R. K., Sahoo, N., Roy, D., Nguyen, L., Rodrigo, H., Duttaroy, A. K., Fields, J. A., & Roy, U. (2026) · Journal of Neuroinflammation · doi:10.1186/s12974-026-03713-6 · Cited by 4 · see citing works
The Alzheimer's disease 5xFAD mouse model is best suited to investigate pretargeted imaging approaches beyond the blood-brain barrier
van den Broek, S. L., Sehlin, D., Andersen, J. V., Aldana, B. I., Beschörner, N., Nedergaard, M., Knudsen, G. M., Syvänen, S., & Herth, M. M. (2022) · Frontiers in Nuclear Medicine · doi:10.3389/fnume.2022.1001722 · Cited by 4 · see citing works
The Granular Retrosplenial Cortex Is Necessary in Male Rats for Object-Location Associative Learning and Memory, But Not Spatial Working Memory or Visual Discrimination and Reversal, in the Touchscreen Operant Chamber
Sheppard, P. A. S., Oomen, C. A., Bussey, T. J., & Saksida, L. M. (2024) · eNeuro · doi:10.1523/eneuro.0120-24.2024 · Cited by 3 · see citing works
Integrative analysis of proteomic and MRI data reveals protein associations with brain imaging features in Alzheimer’s disease
Afxenti, S., Bourdakou, M. M., Loizidou, E. M., Zachariou, M., Lambrianides, A., Pantzaris, M., & Spyrou, G. M. (2025) · Expert Review of Proteomics · doi:10.1080/14789450.2025.2584129 · Cited by 3 · see citing works
Copper Peptides in Regenerative Aesthetic Dermatology
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Authors: Jullienne, A., Trinh, M. V., & Obenaus, A.
Affiliations: University of California, Irvine (US)
Department of Pediatrics, University of California, Irvine, CA 92697, USA
ORCID: Jullienne, Amandine
Obenaus, Andre
Venue: Biomedicines
Publisher: MDPI AG
Published: 2022-01-28
Volume: 10
Issue: 2
Pages: 305
ISSN: 2227-9059 (ISSN-L)
DOI: 10.3390/biomedicines10020305
PMC: PMC8869427
OpenAlex: W4210462365
Cited by: 32
References: 232
Citations by year: 2026: 8 · 2025: 8 · 2024: 6 · 2023: 6 · 2022: 4
FWCI: 0.83
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Biomedicines (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institute on Aging (AG054345-01, AG054349-01)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: Alzheimer's disease, mouse models of Alzheimer's disease, 3xTg-AD mice, 5xFAD mice, magnetic resonance imaging, positron emission tomography, imaging biomarkers

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Neuroimaging of mouse models of Alzheimer’s disease

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