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Article ; Online: Demystifying Microglia: And Now the Work Begins.

Dorman, Leah C / Molofsky, Anna V

2019 Volume 50, Issue 1, Page(s) 11–13

Abstract: Microglia actively shape the developing brain, but their transcriptional diversity is not well understood. Complementary studies by Hammond et al. (2018) and Li et al. (2019) characterize the microglial transcriptome at single cell resolution, ... ...

Abstract	Microglia actively shape the developing brain, but their transcriptional diversity is not well understood. Complementary studies by Hammond et al. (2018) and Li et al. (2019) characterize the microglial transcriptome at single cell resolution, highlighting their diversity during development, aging, and pathology.
MeSH term(s)	Brain ; Microglia ; Myeloid Cells ; RNA ; Sequence Analysis, RNA
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2019-01-15
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	1217235-2
ISSN	1097-4180 ; 1074-7613
ISSN (online)	1097-4180
ISSN	1074-7613
DOI	10.1016/j.immuni.2018.12.025
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Article ; Online: In situ and transcriptomic identification of microglia in synapse-rich regions of the developing zebrafish brain.

Silva, Nicholas J / Dorman, Leah C / Vainchtein, Ilia D / Horneck, Nadine C / Molofsky, Anna V

Nature communications

2021 Volume 12, Issue 1, Page(s) 5916

Abstract: Microglia are brain resident macrophages that play vital roles in central nervous system (CNS) development, homeostasis, and pathology. Microglia both remodel synapses and engulf apoptotic cell corpses during development, but whether unique molecular ... ...

Abstract	Microglia are brain resident macrophages that play vital roles in central nervous system (CNS) development, homeostasis, and pathology. Microglia both remodel synapses and engulf apoptotic cell corpses during development, but whether unique molecular programs regulate these distinct phagocytic functions is unknown. Here we identify a molecularly distinct microglial subset in the synapse rich regions of the zebrafish (Danio rerio) brain. We found that ramified microglia increased in synaptic regions of the midbrain and hindbrain between 7 and 28 days post fertilization. In contrast, microglia in the optic tectum were ameboid and clustered around neurogenic zones. Using single-cell mRNA sequencing combined with metadata from regional bulk sequencing, we identified synaptic-region associated microglia (SAMs) that were highly enriched in the hindbrain and expressed multiple candidate synapse modulating genes, including genes in the complement pathway. In contrast, neurogenic associated microglia (NAMs) were enriched in the optic tectum, had active cathepsin activity, and preferentially engulfed neuronal corpses. These data reveal that molecularly distinct phagocytic programs mediate synaptic remodeling and cell engulfment, and establish the zebrafish hindbrain as a model for investigating microglial-synapse interactions.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Antigens, Differentiation, B-Lymphocyte/genetics ; Antigens, Differentiation, B-Lymphocyte/immunology ; Cathepsin B/genetics ; Cathepsin B/immunology ; Gene Expression Regulation, Developmental ; Genes, Reporter ; Green Fluorescent Proteins/genetics ; Green Fluorescent Proteins/metabolism ; Histocompatibility Antigens Class II/genetics ; Histocompatibility Antigens Class II/immunology ; Mesencephalon/cytology ; Mesencephalon/growth & development ; Mesencephalon/immunology ; Microglia/cytology ; Microglia/immunology ; Neurogenesis/genetics ; Neurogenesis/immunology ; Neurons/cytology ; Neurons/immunology ; Phagocytosis ; Rhombencephalon/cytology ; Rhombencephalon/growth & development ; Rhombencephalon/immunology ; Single-Cell Analysis ; Superior Colliculi/cytology ; Superior Colliculi/growth & development ; Superior Colliculi/immunology ; Synapses/immunology ; Synapses/metabolism ; Synapses/ultrastructure ; Transcriptome ; Zebrafish ; Zebrafish Proteins/genetics ; Zebrafish Proteins/immunology
Chemical Substances	Antigens, Differentiation, B-Lymphocyte ; Histocompatibility Antigens Class II ; Zebrafish Proteins ; enhanced green fluorescent protein ; invariant chain ; Green Fluorescent Proteins (147336-22-9) ; Cathepsin B (EC 3.4.22.1)
Language	English
Publishing date	2021-10-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-26206-x
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Group 2 innate lymphoid cells promote inhibitory synapse development and social behavior.

Barron, Jerika J / Mroz, Nicholas M / Taloma, Sunrae E / Dahlgren, Madelene W / Ortiz-Carpena, Jorge / Dorman, Leah C / Vainchtein, Ilia D / Escoubas, Caroline C / Molofsky, Ari B / Molofsky, Anna V

bioRxiv : the preprint server for biology

2023

Abstract: The innate immune system plays essential roles in brain synaptic development, and immune dysregulation is implicated in neurodevelopmental diseases. Here we show that a subset of innate lymphocytes (group 2 innate lymphoid cells, ILC2s) is required for ... ...

Abstract	The innate immune system plays essential roles in brain synaptic development, and immune dysregulation is implicated in neurodevelopmental diseases. Here we show that a subset of innate lymphocytes (group 2 innate lymphoid cells, ILC2s) is required for cortical inhibitory synapse maturation and adult social behavior. ILC2s expanded in the developing meninges and produced a surge of their canonical cytokine Interleukin-13 (IL-13) between postnatal days 5-15. Loss of ILC2s decreased cortical inhibitory synapse numbers in the postnatal period where as ILC2 transplant was sufficient to increase inhibitory synapse numbers. Deletion of the IL-4/IL-13 receptor (
Language	English
Publishing date	2023-03-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.16.532850
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Article ; Online: Microglial pattern recognition via IL-33 promotes synaptic refinement in developing corticothalamic circuits in mice.

Han, Rafael T / Vainchtein, Ilia D / Schlachetzki, Johannes C M / Cho, Frances S / Dorman, Leah C / Ahn, Eunji / Kim, Dong Kyu / Barron, Jerika J / Nakao-Inoue, Hiromi / Molofsky, Ari B / Glass, Christopher K / Paz, Jeanne T / Molofsky, Anna V

The Journal of experimental medicine

2022 Volume 220, Issue 2

Abstract: Microglia are critical regulators of brain development that engulf synaptic proteins during postnatal synapse remodeling. However, the mechanisms through which microglia sense the brain environment are not well defined. Here, we characterized the ... ...

Abstract	Microglia are critical regulators of brain development that engulf synaptic proteins during postnatal synapse remodeling. However, the mechanisms through which microglia sense the brain environment are not well defined. Here, we characterized the regulatory program downstream of interleukin-33 (IL-33), a cytokine that promotes microglial synapse remodeling. Exposing the developing brain to a supraphysiological dose of IL-33 altered the microglial enhancer landscape and increased binding of stimulus-dependent transcription factors including AP-1/FOS. This induced a gene expression program enriched for the expression of pattern recognition receptors, including the scavenger receptor MARCO. CNS-specific deletion of IL-33 led to increased excitatory/inhibitory synaptic balance, spontaneous absence-like epileptiform activity in juvenile mice, and increased seizure susceptibility in response to chemoconvulsants. We found that MARCO promoted synapse engulfment, and Marco-deficient animals had excess thalamic excitatory synapses and increased seizure susceptibility. Taken together, these data define coordinated epigenetic and functional changes in microglia and uncover pattern recognition receptors as potential regulators of postnatal synaptic refinement.
MeSH term(s)	Animals ; Mice ; Microglia/metabolism ; Interleukin-33/metabolism ; Synapses/metabolism ; Brain/metabolism ; Seizures/metabolism ; Mice, Inbred C57BL
Chemical Substances	Interleukin-33
Language	English
Publishing date	2022-12-15
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20220605
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Zs.MG 45: Show issues

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Article ; Online: Single-cell and spatial multi-omics highlight effects of anti-integrin therapy across cellular compartments in ulcerative colitis.

Mennillo, Elvira / Kim, Yang Joon / Lee, Gyehyun / Rusu, Iulia / Patel, Ravi K / Dorman, Leah C / Flynn, Emily / Li, Stephanie / Bain, Jared L / Andersen, Christopher / Rao, Arjun / Tamaki, Stanley / Tsui, Jessica / Shen, Alan / Lotstein, Madison L / Rahim, Maha / Naser, Mohammad / Bernard-Vazquez, Faviola / Eckalbar, Walter /

Cho, Soo-Jin / Beck, Kendall / El-Nachef, Najwa / Lewin, Sara / Selvig, Daniel R / Terdiman, Jonathan P / Mahadevan, Uma / Oh, David Y / Fragiadakis, Gabriela K / Pisco, Angela / Combes, Alexis J / Kattah, Michael G

Nature communications

2024 Volume 15, Issue 1, Page(s) 1493

Abstract: Ulcerative colitis (UC) is driven by immune and stromal subsets, culminating in epithelial injury. Vedolizumab (VDZ) is an anti-integrin antibody that is effective for treating UC. VDZ is known to inhibit lymphocyte trafficking to the intestine, but its ... ...

Abstract	Ulcerative colitis (UC) is driven by immune and stromal subsets, culminating in epithelial injury. Vedolizumab (VDZ) is an anti-integrin antibody that is effective for treating UC. VDZ is known to inhibit lymphocyte trafficking to the intestine, but its broader effects on other cell subsets are less defined. To identify the inflammatory cells that contribute to colitis and are affected by VDZ, we perform single-cell transcriptomic and proteomic analyses of peripheral blood and colonic biopsies in healthy controls and patients with UC on VDZ or other therapies. Here we show that VDZ treatment is associated with alterations in circulating and tissue mononuclear phagocyte (MNP) subsets, along with modest shifts in lymphocytes. Spatial multi-omics of formalin-fixed biopsies demonstrates trends towards increased abundance and proximity of MNP and fibroblast subsets in active colitis. Spatial transcriptomics of archived specimens pre-treatment identifies epithelial-, MNP-, and fibroblast-enriched genes related to VDZ responsiveness, highlighting important roles for these subsets in UC.
MeSH term(s)	Humans ; Colitis, Ulcerative/drug therapy ; Colitis, Ulcerative/genetics ; Integrins/genetics ; Multiomics ; Proteomics ; Gastrointestinal Agents/therapeutic use ; Treatment Outcome ; Retrospective Studies
Chemical Substances	Integrins ; Gastrointestinal Agents
Language	English
Publishing date	2024-02-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-45665-6
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Article: Single-cell and spatial multi-omics highlight effects of anti-integrin therapy across cellular compartments in ulcerative colitis.

bioRxiv : the preprint server for biology

2024

Abstract	Ulcerative colitis (UC) is driven by immune and stromal subsets, culminating in epithelial injury. Vedolizumab (VDZ) is an anti-integrin antibody that is effective for treating UC. VDZ is known to inhibit lymphocyte trafficking to the intestine, but its broader effects on other cell subsets are less defined. To identify the inflammatory cells that contribute to colitis and are affected by VDZ, we performed single-cell transcriptomic and proteomic analyses of peripheral blood and colonic biopsies in healthy controls and patients with UC on VDZ or other therapies. Here we show that VDZ treatment is associated with alterations in circulating and tissue mononuclear phagocyte (MNP) subsets, along with modest shifts in lymphocytes. Spatial multi-omics of formalin-fixed biopsies demonstrates trends towards increased abundance and proximity of MNP and fibroblast subsets in active colitis. Spatial transcriptomics of archived specimens pre-treatment identifies epithelial-, MNP-, and fibroblast-enriched genes related to VDZ responsiveness, highlighting important roles for these subsets in UC.
Language	English
Publishing date	2024-01-03
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.21.525036
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Article ; Online: Type-I-interferon-responsive microglia shape cortical development and behavior.

Escoubas, Caroline C / Dorman, Leah C / Nguyen, Phi T / Lagares-Linares, Christian / Nakajo, Haruna / Anderson, Sarah R / Barron, Jerika J / Wade, Sarah D / Cuevas, Beatriz / Vainchtein, Ilia D / Silva, Nicholas J / Guajardo, Ricardo / Xiao, Yinghong / Lidsky, Peter V / Wang, Ellen Y / Rivera, Brianna M / Taloma, Sunrae E / Kim, Dong Kyu / Kaminskaya, Elizaveta /

Nakao-Inoue, Hiromi / Schwer, Bjoern / Arnold, Thomas D / Molofsky, Ari B / Condello, Carlo / Andino, Raul / Nowakowski, Tomasz J / Molofsky, Anna V

Cell

2024 Volume 187, Issue 8, Page(s) 1936–1954.e24

Abstract: Microglia are brain-resident macrophages that shape neural circuit development and are implicated in neurodevelopmental diseases. Multiple microglial transcriptional states have been defined, but their functional significance is unclear. Here, we ... ...

Abstract	Microglia are brain-resident macrophages that shape neural circuit development and are implicated in neurodevelopmental diseases. Multiple microglial transcriptional states have been defined, but their functional significance is unclear. Here, we identify a type I interferon (IFN-I)-responsive microglial state in the developing somatosensory cortex (postnatal day 5) that is actively engulfing whole neurons. This population expands during cortical remodeling induced by partial whisker deprivation. Global or microglial-specific loss of the IFN-I receptor resulted in microglia with phagolysosomal dysfunction and an accumulation of neurons with nuclear DNA damage. IFN-I gain of function increased neuronal engulfment by microglia in both mouse and zebrafish and restricted the accumulation of DNA-damaged neurons. Finally, IFN-I deficiency resulted in excess cortical excitatory neurons and tactile hypersensitivity. These data define a role for neuron-engulfing microglia during a critical window of brain development and reveal homeostatic functions of a canonical antiviral signaling pathway in the brain.
MeSH term(s)	Animals ; Mice ; Interferon Type I/metabolism ; Microglia/metabolism ; Neurons/metabolism ; Zebrafish ; Brain/cytology ; Brain/growth & development
Chemical Substances	Interferon Type I
Language	English
Publishing date	2024-03-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2024.02.020
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Zs.A 1167: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
Zs.MG 58: Show issues

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Article: Type I interferon responsive microglia shape cortical development and behavior.

Escoubas, Caroline C / Dorman, Leah C / Nguyen, Phi T / Lagares-Linares, Christian / Nakajo, Haruna / Anderson, Sarah R / Cuevas, Beatriz / Vainchtein, Ilia D / Silva, Nicholas J / Xiao, Yinghong / Lidsky, Peter V / Wang, Ellen Y / Taloma, Sunrae E / Nakao-Inoue, Hiromi / Schwer, Bjoern / Andino, Raul / Nowakowski, Tomasz J / Molofsky, Anna V

bioRxiv : the preprint server for biology

2023

Abstract: Microglia are brain resident phagocytes that can engulf synaptic components and extracellular matrix as well as whole neurons. However, whether there are unique molecular mechanisms that regulate these distinct phagocytic states is unknown. Here we ... ...

Abstract	Microglia are brain resident phagocytes that can engulf synaptic components and extracellular matrix as well as whole neurons. However, whether there are unique molecular mechanisms that regulate these distinct phagocytic states is unknown. Here we define a molecularly distinct microglial subset whose function is to engulf neurons in the developing brain. We transcriptomically identified a cluster of Type I interferon (IFN-I) responsive microglia that expanded 20-fold in the postnatal day 5 somatosensory cortex after partial whisker deprivation, a stressor that accelerates neural circuit remodeling.
Language	English
Publishing date	2023-03-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.04.29.441889
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Article ; Online: Microglial Remodeling of the Extracellular Matrix Promotes Synapse Plasticity.

Nguyen, Phi T / Dorman, Leah C / Pan, Simon / Vainchtein, Ilia D / Han, Rafael T / Nakao-Inoue, Hiromi / Taloma, Sunrae E / Barron, Jerika J / Molofsky, Ari B / Kheirbek, Mazen A / Molofsky, Anna V

Cell

2020 Volume 182, Issue 2, Page(s) 388–403.e15

Abstract: Synapse remodeling is essential to encode experiences into neuronal circuits. Here, we define a molecular interaction between neurons and microglia that drives experience-dependent synapse remodeling in the hippocampus. We find that the cytokine ... ...

Abstract	Synapse remodeling is essential to encode experiences into neuronal circuits. Here, we define a molecular interaction between neurons and microglia that drives experience-dependent synapse remodeling in the hippocampus. We find that the cytokine interleukin-33 (IL-33) is expressed by adult hippocampal neurons in an experience-dependent manner and defines a neuronal subset primed for synaptic plasticity. Loss of neuronal IL-33 or the microglial IL-33 receptor leads to impaired spine plasticity, reduced newborn neuron integration, and diminished precision of remote fear memories. Memory precision and neuronal IL-33 are decreased in aged mice, and IL-33 gain of function mitigates age-related decreases in spine plasticity. We find that neuronal IL-33 instructs microglial engulfment of the extracellular matrix (ECM) and that its loss leads to impaired ECM engulfment and a concomitant accumulation of ECM proteins in contact with synapses. These data define a cellular mechanism through which microglia regulate experience-dependent synapse remodeling and promote memory consolidation.
MeSH term(s)	Aging ; Animals ; Extracellular Matrix/metabolism ; Fear ; Gene Expression Regulation ; Hippocampus/metabolism ; Interleukin-1 Receptor-Like 1 Protein/genetics ; Interleukin-1 Receptor-Like 1 Protein/metabolism ; Interleukin-33/genetics ; Interleukin-33/metabolism ; Memory ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Microglia/physiology ; Neuronal Plasticity/physiology ; Neurons/metabolism ; Signal Transduction
Chemical Substances	Interleukin-1 Receptor-Like 1 Protein ; Interleukin-33
Language	English
Publishing date	2020-07-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2020.05.050
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Article: Microglial Remodeling of the Extracellular Matrix Promotes Synapse Plasticity

Nguyen, Phi T / Dorman, Leah C / Pan, Simon / Vainchtein, Ilia D / Han, Rafael T / Nakao-Inoue, Hiromi / Taloma, Sunrae E / Barron, Jerika J / Molofsky, Ari B / Kheirbek, Mazen A / Molofsky, Anna V

Cell. 2020 July 23, v. 182, no. 2

2020

Abstract	Synapse remodeling is essential to encode experiences into neuronal circuits. Here, we define a molecular interaction between neurons and microglia that drives experience-dependent synapse remodeling in the hippocampus. We find that the cytokine interleukin-33 (IL-33) is expressed by adult hippocampal neurons in an experience-dependent manner and defines a neuronal subset primed for synaptic plasticity. Loss of neuronal IL-33 or the microglial IL-33 receptor leads to impaired spine plasticity, reduced newborn neuron integration, and diminished precision of remote fear memories. Memory precision and neuronal IL-33 are decreased in aged mice, and IL-33 gain of function mitigates age-related decreases in spine plasticity. We find that neuronal IL-33 instructs microglial engulfment of the extracellular matrix (ECM) and that its loss leads to impaired ECM engulfment and a concomitant accumulation of ECM proteins in contact with synapses. These data define a cellular mechanism through which microglia regulate experience-dependent synapse remodeling and promote memory consolidation.
Keywords	adults ; cytokines ; extracellular matrix ; fearfulness ; gain-of-function mutation ; hippocampus ; memory ; mice ; neonates ; neuroglia ; neurons ; neuroplasticity ; plasticity ; proteins ; synapse
Language	English
Dates of publication	2020-0723
Size	p. 388-403.e15.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2020.05.050
Database	NAL-Catalogue (AGRICOLA)

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