Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures

Summary: Advancements in human induced pluripotent stem cell (hiPSC) technology have enabled co-culture models for disease modeling in physiologically relevant systems. However, co-culturing protocols face challenges in usability and consistency. Here, we introduce a robust, reproducible hiPSC-deriv...

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Main Authors: Alexandra M. Lish, Nancy Ashour, Richard V. Pearse, II, Paige C. Galle, Gwendolyn A. Orme, Sarah E. Heuer, Courtney R. Benoit, Kellianne D. Alexander, Elyssa F.L. Grogan, Gizem Terzioglu, Allegra Scarpa, Andrew M. Stern, Nicholas Seyfried, Vilas Menon, Tracy L. Young-Pearse
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725005480
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author Alexandra M. Lish
Nancy Ashour
Richard V. Pearse, II
Paige C. Galle
Gwendolyn A. Orme
Sarah E. Heuer
Courtney R. Benoit
Kellianne D. Alexander
Elyssa F.L. Grogan
Gizem Terzioglu
Allegra Scarpa
Andrew M. Stern
Nicholas Seyfried
Vilas Menon
Tracy L. Young-Pearse
author_facet Alexandra M. Lish
Nancy Ashour
Richard V. Pearse, II
Paige C. Galle
Gwendolyn A. Orme
Sarah E. Heuer
Courtney R. Benoit
Kellianne D. Alexander
Elyssa F.L. Grogan
Gizem Terzioglu
Allegra Scarpa
Andrew M. Stern
Nicholas Seyfried
Vilas Menon
Tracy L. Young-Pearse
author_sort Alexandra M. Lish
collection DOAJ
description Summary: Advancements in human induced pluripotent stem cell (hiPSC) technology have enabled co-culture models for disease modeling in physiologically relevant systems. However, co-culturing protocols face challenges in usability and consistency. Here, we introduce a robust, reproducible hiPSC-derived co-culture system integrating astrocytes, neurons, and microglia. This model leverages cryopreserved cells, enabling co-cultures within 20 days post-thaw. Comparing monocultures and tricultures, we demonstrate how cell-cell interactions shape transcriptional and functional states across all three cell types. Neurons in triculture exhibit increased spine density and activity, while astrocytes and microglia show altered responses to proinflammatory stimulation. Surprisingly, the presence of astrocytes induces upregulation of disease-associated microglia (DAM) genes, including TREM2, SPP1, APOE, and GPNMB in microglia. Additionally, while familial Alzheimer’s disease neurons induce a prototypical inflammatory response in microglia, the DAM signature is significantly dampened. Collectively, this study establishes a versatile human triculture model as a valuable resource for dissecting neuron-glia interactions and their role in neurodegenerative disease.
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spelling doaj-art-19ae6ba0cfd841d892ed78777924df492025-08-20T03:07:50ZengElsevierCell Reports2211-12472025-06-0144611577710.1016/j.celrep.2025.115777Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple culturesAlexandra M. Lish0Nancy Ashour1Richard V. Pearse, II2Paige C. Galle3Gwendolyn A. Orme4Sarah E. Heuer5Courtney R. Benoit6Kellianne D. Alexander7Elyssa F.L. Grogan8Gizem Terzioglu9Allegra Scarpa10Andrew M. Stern11Nicholas Seyfried12Vilas Menon13Tracy L. Young-Pearse14Ann Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USADepartment of Biochemistry, Emory School of Medicine, Atlanta, GA, USACenter for Translational and Computational Neuroimmunology, Department of Neurology and the Taub Institute for the Study of Alzheimer’s Disease and the Aging Brain, Columbia University Irving Medical Center, New York, NY, USAAnn Romney Center for Neurologic Diseases, Department of Neurology, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA; Corresponding authorSummary: Advancements in human induced pluripotent stem cell (hiPSC) technology have enabled co-culture models for disease modeling in physiologically relevant systems. However, co-culturing protocols face challenges in usability and consistency. Here, we introduce a robust, reproducible hiPSC-derived co-culture system integrating astrocytes, neurons, and microglia. This model leverages cryopreserved cells, enabling co-cultures within 20 days post-thaw. Comparing monocultures and tricultures, we demonstrate how cell-cell interactions shape transcriptional and functional states across all three cell types. Neurons in triculture exhibit increased spine density and activity, while astrocytes and microglia show altered responses to proinflammatory stimulation. Surprisingly, the presence of astrocytes induces upregulation of disease-associated microglia (DAM) genes, including TREM2, SPP1, APOE, and GPNMB in microglia. Additionally, while familial Alzheimer’s disease neurons induce a prototypical inflammatory response in microglia, the DAM signature is significantly dampened. Collectively, this study establishes a versatile human triculture model as a valuable resource for dissecting neuron-glia interactions and their role in neurodegenerative disease.http://www.sciencedirect.com/science/article/pii/S2211124725005480CP: NeuroscienceCP: Stem cell research
spellingShingle Alexandra M. Lish
Nancy Ashour
Richard V. Pearse, II
Paige C. Galle
Gwendolyn A. Orme
Sarah E. Heuer
Courtney R. Benoit
Kellianne D. Alexander
Elyssa F.L. Grogan
Gizem Terzioglu
Allegra Scarpa
Andrew M. Stern
Nicholas Seyfried
Vilas Menon
Tracy L. Young-Pearse
Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
Cell Reports
CP: Neuroscience
CP: Stem cell research
title Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
title_full Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
title_fullStr Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
title_full_unstemmed Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
title_short Astrocyte induction of disease-associated microglia is suppressed by acute exposure to fAD neurons in human iPSC triple cultures
title_sort astrocyte induction of disease associated microglia is suppressed by acute exposure to fad neurons in human ipsc triple cultures
topic CP: Neuroscience
CP: Stem cell research
url http://www.sciencedirect.com/science/article/pii/S2211124725005480
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