Modeling Alzheimer’s disease with iPSC-derived brain cells

Penney, Jay; Ralvenius, William T.; Tsai, Li-Huei

doi:10.1038/s41380-019-0468-3

Cited by 482Pluripotent Stem Cells ResearchAlzheimer's disease research and treatmentsNeurogenesis and neuroplasticity mechanisms

Modeling Alzheimer’s disease with iPSC-derived brain cells

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Penney, Jay, Ralvenius, William T., Tsai, Li-Huei·2020·Molecular Psychiatry

DOI 10.1038/s41380-019-0468-3PMC PMC6906186

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Abstract

Alzheimer's disease is a devastating neurodegenerative disorder with no cure. Countless promising therapeutics have shown efficacy in rodent Alzheimer's disease models yet failed to benefit human patients. While hope remains that earlier intervention with existing therapeutics will improve outcomes, it is becoming increasingly clear that new approaches to understand and combat the pathophysiology of Alzheimer's disease are needed. Human induced pluripotent stem cell (iPSC) technologies have changed the face of preclinical research and iPSC-derived cell types are being utilized to study an array of human conditions, including neurodegenerative disease. All major brain cell types can now be differentiated from iPSCs, while increasingly complex co-culture systems are being developed to facilitate neuroscience research. Many cellular functions perturbed in Alzheimer's disease can be recapitulated using iPSC-derived cells in vitro, and co-culture platforms are beginning to yield insights into the complex interactions that occur between brain cell types during neurodegeneration. Further, iPSC-based systems and genome editing tools will be critical in understanding the roles of the numerous new genes and mutations found to modify Alzheimer's disease risk in the past decade. While still in their relative infancy, these developing iPSC-based technologies hold considerable promise to push forward efforts to combat Alzheimer's disease and other neurodegenerative disorders.

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A majority of Alzheimer's disease risk genes identified through genome-wide association studies are highly expressed in microglia, suggesting a key role in microglial dysfunction.
“A majority of AD risk genes identified through genome-wide association studies are highly expressed in microglia, the brain’s innate immune cells, suggesting a key role in microglial dysfunction (Kummer et al., 2021; Penney et al., 2020; Teipel et al., 2022).”
From A novel molecular class that recruits HDAC/MECP2 complexes to PU.1 motifs reduces neuroinflammation (2023) · cites this paper as Penney et al., 2020
The Microglia section (page unavailable) says GWAS identified a surprising number of microglial genes as late-onset AD risk factors and links those findings to microglial dysfunction. It does not establish that a majority of GWAS-identified AD risk genes are highly expressed in microglia; the Alzheimer’s disease section instead says many are expressed primarily in non-neuronal brain cells. (LLM, conf=0.86)
Experimental — accuracy not yet measured
AD risk variants are enriched in genes that are highly expressed in microglia.
“Population genetics has revealed that AD risk variants are enriched in genes that are highly expressed in microglia (Penney et al., 2020).”
From A novel molecular class that recruits HDAC/MECP2 complexes to PU.1 motifs reduces neuroinflammation (2023) · cites this paper as Penney et al., 2020
iPS cell systems can model aspects of AD pathology.
“While it is well documented that iPS cell systems can model aspects of AD pathology (Penney et al., 2020; Nelson et al., 2023)”
From APOE3 Christchurch modulates β-catenin/Wnt signaling in iPS cell-derived cerebral organoids from Alzheimer’s cases (2024) · cites this paper as Penney et al., 2020

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Rapid and efficient induction of functional astrocytes from human pluripotent stem cells
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Functionality of Endothelial Cells and Pericytes From Human Pluripotent Stem Cells Demonstrated in Cultured Vascular Plexus and Zebrafish Xenografts
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Molecular Mechanisms of Alzheimer Disease Protection by the A673T Allele of Amyloid Precursor Protein
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The Astrocyte: Powerhouse and Recycling Center
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Functional Studies of Missense TREM2 Mutations in Human Stem Cell-Derived Microglia
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Elevated Coding Mutation Rate During the Reprogramming of Human Somatic Cells into Induced Pluripotent Stem Cells
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Induced pluripotent stem cells: at the heart of cardiovascular precision medicine
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Aberrant iPSC-derived human astrocytes in Alzheimer's disease
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Characterization and Molecular Profiling of PSEN1 Familial Alzheimer's Disease iPSC-Derived Neural Progenitors
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The presenilin-1 ΔE9 mutation results in reduced γ-secretase activity, but not total loss of PS1 function, in isogenic human stem cells
Woodruff, G., Young, J. E., Martinez, F. J., Buen, F., Gore, A., Kinaga, J., Li, Z., Yuan, S. H., Zhang, K., & Goldstein, L. S. B. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.018 · Cited by 177 · see citing works
CRISPR/Cas9-Correctable mutation-related molecular and physiological phenotypes in iPSC-derived Alzheimer’s PSEN2 N141I neurons
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Cerebral organoids model human brain development and microcephaly
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Diffusible, highly bioactive oligomers represent a critical minority of soluble Aβ in Alzheimer’s disease brain
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Reproducibility of Molecular Phenotypes after Long-Term Differentiation to Human iPSC-Derived Neurons: A Multi-Site Omics Study
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Human Induced Pluripotent Stem Cell-Derived Microglia-Like Cells Harboring TREM2 Missense Mutations Show Specific Deficits in Phagocytosis
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Direct reprogramming of human astrocytes into neural stem cells and neurons
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Stem cell derived basal forebrain cholinergic neurons from Alzheimer’s disease patients are more susceptible to cell death
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Acid sphingomyelinase modulates the autophagic process by controlling lysosomal biogenesis in Alzheimer’s disease
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Neuronal apolipoprotein E4 increases cell death and phosphorylated tau release in alzheimer disease
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Drug screening for human genetic diseases using iPSC models
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Alzheimer Presenilin-1 Mutations Dramatically Reduce Trimming of Long Amyloid β-Peptides (Aβ) by γ-Secretase to Increase 42-to-40-Residue Aβ
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Oxidative stress and altered mitochondrial protein expression in the absence of amyloid-β and tau pathology in iPSC-derived neurons from sporadic Alzheimer's disease patients
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Sustained synchronized neuronal network activity in a human astrocyte co-culture system
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Calories or protein? The effect of dietary restriction on lifespan in rodents is explained by calories alone
Speakman, J. R., Mitchell, S. E., & Mazidi, M. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.03.011 · Cited by 131 · see citing works
Efficient Differentiation of Human Embryonic and Induced Pluripotent Stem Cells into Functional Astrocytes
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Mitophagy Failure in Fibroblasts and iPSC-Derived Neurons of Alzheimer’s Disease-Associated Presenilin 1 Mutation
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Prevention of β-amyloid induced toxicity in human iPS cell-derived neurons by inhibition of Cyclin-dependent kinases and associated cell cycle events
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Human Neurospheroid Arrays for In Vitro Studies of Alzheimer’s Disease
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The neuronal endosomal-lysosomal system in Alzheimer's disease
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Direct Induction and Functional Maturation of Forebrain GABAergic Neurons from Human Pluripotent Stem Cells
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Alzheimer's disease-related amyloid-β induces synaptotoxicity in human iPS cell-derived neurons
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Stabilizing the Retromer Complex in a Human Stem Cell Model of Alzheimer’s Disease Reduces TAU Phosphorylation Independently of Amyloid Precursor Protein
Young, J. E., Fong, L. K., Frankowski, H., Petsko, G. A., Small, S. A., & Goldstein, L. S. B. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.01.031 · Cited by 105 · see citing works
Single-Cell Detection of Secreted Aβ and sAPPα from Human IPSC-Derived Neurons and Astrocytes
Liao, M.-C., Muratore, C., Gierahn, T. M., Sullivan, S. E., Srikanth, P., Jager, P. L. D., Love, J. C., & Young‐Pearse, T. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2735-15.2016 · Cited by 96 · see citing works
Efficient derivation of cortical glutamatergic neurons from human pluripotent stem cells: A model system to study neurotoxicity in Alzheimer's disease
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Effect of Potent γ-Secretase Modulator in Human Neurons Derived From Multiple Presenilin 1–Induced Pluripotent Stem Cell Mutant Carriers
Liu, Q., Waltz, S., Woodruff, G., Ouyang, J., Israel, M. A., Herrera, C. M., Sarsoza, F. M., Tanzi, R. E., Koo, E. H., Ringman, J. M., et al. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.2482 · Cited by 89 · see citing works
Cell-type Dependent Alzheimer's Disease Phenotypes: Probing the Biology of Selective Neuronal Vulnerability
Muratore, C., Zhou, C. Q., Liao, M., Fernandez, M. A., Taylor, W. M., Lagomarsino, V. N., Pearse, R. V., Rice, H. C., Negri, J. M., He, A., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.10.015 · Cited by 82 · see citing works
The diverse actions of astrocytes during synaptic development
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N-butylidenephthalide Attenuates Alzheimer's Disease-Like Cytopathy in Down Syndrome Induced Pluripotent Stem Cell-Derived Neurons
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Clonal genetic and hematopoietic heterogeneity among human-induced pluripotent stem cell lines
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Human mitochondrial transcriptional factor A breaks the mitochondria-mediated vicious cycle in Alzheimer’s disease
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Diversity of oligodendrocytes and their progenitors
Dimou, L., & Simons, M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.09.015 · Cited by 77 · see citing works
iPSCs and fibroblast subclones from the same fibroblast population contain comparable levels of sequence variations
Kwon, E. M., Connelly, J. P., Hansen, N. F., Donovan, F. X., Winkler, T., Davis, B. W., Alkadi, H., Chandrasekharappa, S. C., Dunbar, C. E., Mullikin, J. C., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616035114 · Cited by 76 · see citing works
Cardiac differentiation of pluripotent stem cells and implications for modeling the heart in health and disease
Devalla, H. D., & Passier, R. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aah5457 · Cited by 75 · see citing works
Concise Review: Assessing the Genome Integrity of Human Induced Pluripotent Stem Cells: What Quality Control Metrics?
Assou, S., Bouckenheimer, J., & De Vos, J. (2018) · Stem Cells · doi:10.1002/stem.2797 · Cited by 74 · see citing works
The Impact of APP on Alzheimer-like Pathogenesis and Gene Expression in Down Syndrome iPSC-Derived Neurons
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PPARδ activation by bexarotene promotes neuroprotection by restoring bioenergetic and quality control homeostasis
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Induced Pluripotent Stem Cell Generation-Associated Point Mutations Arise during the Initial Stages of the Conversion of These Cells
Sugiura, M., Kasama, Y., Araki, R., Hoki, Y., Sunayama, M., Uda, M., Nakamura, M., Ando, S., & Abe, M. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.11.006 · Cited by 68 · see citing works
Phenotypic Screening Identifies Modulators of Amyloid Precursor Protein Processing in Human Stem Cell Models of Alzheimer’s Disease
Brownjohn, P. W., Smith, J. C., Portelius, E., Serneels, L., Kvartsberg, H., Strooper, B. D., Blennow, K., Zetterberg, H., & Livesey, F. J. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.02.006 · Cited by 67 · see citing works
Association of Rare Coding Mutations With Alzheimer Disease and Other Dementias Among Adults of European Ancestry
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Nobiletin Reduces Intracellular and Extracellular β-Amyloid in iPS Cell-Derived Alzheimer’s Disease Model Neurons
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Early pathogenic event of Alzheimer’s disease documented in iPSCs from patients with PSEN1 mutations
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The landscape of aging
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TLR4 Cross-Talk With NLRP3 Inflammasome and Complement Signaling Pathways in Alzheimer's Disease
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The complexity of Alzheimer’s disease: an evolving puzzle
Ferrari, C., & Sorbi, S. (2021) · Physiological Reviews · doi:10.1152/physrev.00015.2020 · Cited by 324 · see citing works
Lipid accumulation induced by APOE4 impairs microglial surveillance of neuronal-network activity
Victor, M. B., Leary, N., Luna, X., Meharena, H. S., Scannail, A. N., Bozzelli, P. L., Samaan, G., Murdock, M. H., von Maydell, D., Effenberger, A. H., et al. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.07.005 · Cited by 316 · see citing works
Self-citation
Proteomic landscape of Alzheimer’s Disease: novel insights into pathogenesis and biomarker discovery
Bai, B., Vanderwall, D., Li, Y., Wang, X., Poudel, S., Wang, H., Dey, K. K., Chen, P., Yang, K., & Peng, J. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00474-z · Cited by 252 · see citing works
Mechanisms of hyperexcitability in Alzheimer’s disease hiPSC-derived neurons and cerebral organoids vs isogenic controls
Ghatak, S., Dolatabadi, N., Trudler, D., Zhang, X., Wu, Y., Mohata, M., Ambasudhan, R., Talantova, M., & Lipton, S. A. (2019) · eLife · doi:10.7554/elife.50333 · Cited by 227 · see citing works
Mitophagy pathways in health and disease
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Cellular senescence at the crossroads of inflammation and Alzheimer's disease
Guerrero, A., De Strooper, B., & Arancibia-Cárcamo, I. L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.06.007 · Cited by 236 · see citing works
Regenerative Stem Cell Therapy for Neurodegenerative Diseases: An Overview
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Modeling Sporadic Alzheimer's Disease in Human Brain Organoids under Serum Exposure
Chen, X., Sun, G., Tian, E., Zhang, M., Davtyan, H., Beach, T. G., Reiman, E. M., Blurton‐Jones, M., Holtzman, D. M., & Shi, Y. (2021) · Advanced Science · doi:10.1002/advs.202101462 · Cited by 200 · see citing works
Interpretable learning based Dynamic Graph Convolutional Networks for Alzheimer’s Disease analysis
Zhu, Y., Ma, J., Yuan, C., & Zhu, X. (2021) · Information Fusion · doi:10.1016/j.inffus.2021.07.013 · Cited by 178 · see citing works
Integrative metabolomics‐genomics approach reveals key metabolic pathways and regulators of Alzheimer's disease
Horgusluoglu, E., Neff, R., Song, W., Wang, M., Wang, Q., Arnold, M., Krumsiek, J., Galindo‐Prieto, B., Ming, C., Nho, K., et al. (2022) · Alzheimer's & Dementia · doi:10.1002/alz.12468 · Cited by 175 · see citing works
Cellular rejuvenation: molecular mechanisms and potential therapeutic interventions for diseases
Ji, S., Xiong, M., Chen, H., Liu, Y., Zhou, L., Hong, Y., Wang, M., Wang, C., Fu, X., & Sun, X. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01343-5 · Cited by 166 · see citing works
3D Bioprinting Pluripotent Stem Cell Derived Neural Tissues Using a Novel Fibrin Bioink Containing Drug Releasing Microspheres
Sharma, R., Smits, I. P. M., la Vega, L. D., Lee, C., & Willerth, S. M. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00057 · Cited by 146 · see citing works
Single-Cell Transcriptomics of Parkinson’s Disease Human In Vitro Models Reveals Dopamine Neuron-Specific Stress Responses
Fernandes, H. J. R., Patikas, N., Foskolou, S., Field, S. F., Park, J.-E., Byrne, M. L., Bassett, A. R., & Metzakopian, E. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108263 · Cited by 138 · see citing works
Cell of all trades: oligodendrocyte precursor cells in synaptic, vascular, and immune functionPreprint
Akay, L. A., Effenberger, A. H., & Tsai, L. (2021) · Genes & Development · doi:10.1101/gad.344218.120 · Cited by 142 · see citing works
Self-citation
Induced Pluripotent Stem Cell (iPSC)-Based Neurodegenerative Disease Models for Phenotype Recapitulation and Drug Screening
Chang, C.-Y., Ting, H.-C., Liu, C.-A., Su, H., Chiou, T., Lin, S., Harn, H., & Ho, T. (2020) · Molecules · doi:10.3390/molecules25082000 · Cited by 133 · see citing works
Applications of iPSC-derived beta cells from patients with diabetes
Maxwell, K. G., & Millman, J. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100238 · Cited by 118 · see citing works
Detecting the Stages of Alzheimer’s Disease with Pre-trained Deep Learning Architectures
Savaş, S. (2021) · Arabian Journal for Science and Engineering · doi:10.1007/s13369-021-06131-3 · Cited by 133 · see citing works
Recent progress in translational engineered in vitro models of the central nervous system
Nikolakopoulou, P., Rauti, R., Voulgaris, D., Shlomy, I., Maoz, B. M., & Herland, A. (2020) · Brain · doi:10.1093/brain/awaa268 · Cited by 128 · see citing works
Neuropathogenesis-on-chips for neurodegenerative diseases
Amartumur, S., Nguyen, H. M., Huynh, T., Kim, T. S., Woo, R., Oh, E., Kim, K. K., Lee, L. P., & Heo, C. (2024) · Nature Communications · doi:10.1038/s41467-024-46554-8 · Cited by 120 · see citing works
Identification of Therapeutic Targets for Amyotrophic Lateral Sclerosis Using PandaOmics – An AI-Enabled Biological Target Discovery Platform
Pun, F. W., Liu, B. H. M., Long, X., Leung, H. W., Leung, G. H. D., Mewborne, Q. T., Gao, J., Shneyderman, A., Ozerov, I. V., Wang, J., et al. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.914017 · Cited by 115 · see citing works
“A recent study investigating Alzheimer’s progression in the human brain highlighted the importance of integrating human data with data generated using cell lines and animal models, in order to better understand various stages of disease evolution (Penney et al., 2020).”
Background
Genetics, Functions, and Clinical Impact of Presenilin-1 (PSEN1) Gene
Bagaria, J., Bagyinszky, E., & An, S. S. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810970 · Cited by 117 · see citing works
Clinical Trials in Alzheimer’s Disease: A Hurdle in the Path of Remedy
Oxford, A. E., Stewart, E. S., & Rohn, T. T. (2020) · International Journal of Alzheimer s Disease · doi:10.1155/2020/5380346 · Cited by 109 · see citing works
Improved modeling of human AD with an automated culturing platform for iPSC neurons, astrocytes and microglia
Bassil, R., Shields, K., Granger, K., Zein, I., Ng, S., & Chih, B. (2021) · Nature Communications · doi:10.1038/s41467-021-25344-6 · Cited by 106 · see citing works
Alzheimer’s disease beyond amyloid: Can the repetitive failures of amyloid-targeted therapeutics inform future approaches to dementia drug discovery?
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Authors: Penney, J., Ralvenius, W. T., & Tsai, L.-H.
Affiliations: Massachusetts Institute of Technology (US)
Corresponding author: Tsai, Li-Huei
ORCID: Penney, Jay
Ralvenius, William T.
Tsai, Li-Huei
Venue: Molecular Psychiatry
Publisher: Springer Science and Business Media LLC
Published: 2019-08-07
Volume: 25
Issue: 1
Pages: 148-167
ISSN: 1359-4184 (ISSN-L)
1476-5578
DOI: 10.1038/s41380-019-0468-3
PMC: PMC6906186
OpenAlex: W2964627277
Cited by: 471
References: 235
Citations by year: 2026: 54 · 2025: 66 · 2024: 78 · 2023: 84 · 2022: 77 · 2021: 65 · 2020: 41 · 2019: 6
FWCI: 4.18
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Molecular Psychiatry (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
IslandScholar (University of Prince Edward Island) (submittedVersion)
Funders: National Science Foundation
Cure Alzheimer's Fund
Robert A. and Renee E. Belfer Family Foundation
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (177920)
National Institutes of Health (NS051874)
National Institute on Aging (RF1AG054012)
National Institute of Neurological Disorders and Stroke (R37NS051874)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: Alzheimer's disease, induced pluripotent stem cells, neurodegeneration, co-culture model, disease modeling, genome editing, Alzheimer's disease risk genes, preclinical research
MeSH terms: Alzheimer Disease, Brain, Cell Differentiation, Humans, Models, Biological, Neurons, Neurodegenerative Diseases, Induced Pluripotent Stem Cells

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Modeling Alzheimer’s disease with iPSC-derived brain cells

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