ArticleScience (New York, N.Y.)2021
Barcoded viral tracing of single-cell interactions in central nervous system inflammation.
Open access · greenAbstract read
In one paragraph
Article in Science (New York, N.Y.), 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 177 papers, 1 of them a synthesis that pooled it.
0numbers the graph read from it
0cells of the map it votes in
177citing papers in PubMed, 1 pooled it
19.2field-weighted citation impact, top 1% of its field
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Who cites it
177 citing papers in PubMed, 1 synthesis or guideline pooled it, 270 citations in OpenAlex.
- The impact of physical exercise on neuroinflammation mechanism in Alzheimer's disease.Frontiers in aging neuroscience · 2024Pooled it
- Mapping brain-wide monosynaptic inputs to single neurons with ROInet-seq.Cell reports methods · 2026Article
- Trace-n-Seq combines retrograde fluorescent tracing with sorting and single-cell sequencing of innervating peripheral neurons.Nature protocols · 2026Review
- An applicable and efficient retrograde monosynaptic circuit mapping tool for larval zebrafish.eLife · 2026Article
- Barcoded Rabies In Situ Connectomics for high-throughput reconstruction of neural circuits.Nature communications · 2026Article
- Antigen presentation by CD40Nature · 2026Article
- Activity-dependent protein synthesis in neurons requires microglial-metabolic coupling.Cell metabolism · 2026Article
- SORLA up-regulation suppresses pathological effects in aged tauopathy mouse brain.Science advances · 2026Article
- Forkhead box versus NF-κB hippocampal snRNA-seq profiles distinguish anti-Drebrin- and anti-GAD65-positive encephalitis.Journal of neuroinflammation · 2026Article
- Microglial mitochondria transfer to astrocytes via GPNMB-enriched extracellular vesicles alleviates cognitive deficits in tauopathy mice.Nature neuroscience · 2026Article
- Friend or foe? Glial-vascular interactions in health and neurodegenerative disease.Pharmacological reviews · 2026Review
- A synaptoid connectome differentiates tanycytic subpopulations and underlies neuroglial communication and neuroendocrine regulation.Nature communications · 2026Article
- Protocol to produce and apply barcoded rabies virus for single-neuron input mapping in mice.STAR protocols · 2026Article
- Glial cells in chronic inflammation: diversity, dysfunction and therapeutic targeting.Nature reviews. Immunology · 2026Review
- Glia and semaphorins in neurodegenerative diseases: The frontier for new therapeutics.Neural regeneration research · 2026Article
- A distinct vagus-beta cell neural circuit senses glucose and modulates insulin secretion.Molecular metabolism · 2026Article
- Transsynaptic tracing techniques to interrogate neuronal connectivity of glioblastomas.Nature protocols · 2026Review
- Substance abuse and inflammation: consequences beyond the brain.Trends in immunology · 2026Review
- Satellite microglia-like cells in human dorsal root ganglia and changes with diabetic neuropathy.bioRxiv : the preprint server for biology · 2026Article
- Astrocyte-driven immunosuppression in the brain tumor microenvironment.Nature immunology · 2026Review
117 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
31 authors at 7 institutions in 3 countries.
Iain C Clark *Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0001-9082-0253
Cristina Gutiérrez-Vázquez *Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-3846-4631
Michael A Wheeler *Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-0689-6384
Zhaorong LiAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-5268-6986
Veit RothhammerAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Mathias LinnerbauerAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-5528-5141
Liliana M SanmarcoAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-2075-8826
Lydia GuoAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-6702-1223
Manon BlainNeuroimmunology Unit, Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC H3A 2B4, Canada.
Stephanie E J ZandeeNeuroimmunology Research Laboratory, Centre de Recherche du Centre Hospitalier de l'Université de Montréal (CRCHUM), Montreal, QC H2X 0A9, Canada.ORCID https://orcid.org/0000-0003-0812-676X
Chun-Cheih ChaoAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0003-4108-2658
Katelyn V BattermanDepartment of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA 02118, USA.ORCID https://orcid.org/0000-0001-7912-7028
Marius SchwabenlandInstitute of Neuropathology, University of Freiburg, D-79106 Freiburg, Germany.ORCID https://orcid.org/0000-0003-2205-5427
Peter LotfyAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0003-0809-7073
Amalia Tejeda-VelardeAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-7061-8725
Patrick HewsonAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-5257-882X
Carolina Manganeli PolonioAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0003-0460-0161
Michael W ShultisAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Yasmin SalemAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-7612-024X
Emily C TjonAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.
Pedro H Fonseca-CastroAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-7191-2387
Davis M BoruckiAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0001-8669-6720
Kalil Alves de LimaAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-9149-168X
Agustin PlasenciaAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-7415-0947
Adam R AbateDepartment of Bioengineering and Therapeutic Sciences, University of California, San Francisco, California Institute for Quantitative Biosciences, San Francisco, CA 94158, USA.ORCID https://orcid.org/0000-0001-9614-4831
Douglas L RoseneDepartment of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA 02118, USA.ORCID https://orcid.org/0000-0001-8719-1441
Kevin J HodgettsAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA.ORCID https://orcid.org/0000-0002-4317-3230
Marco PrinzInstitute of Neuropathology, University of Freiburg, D-79106 Freiburg, Germany.ORCID https://orcid.org/0000-0002-0349-1955
Jack P AntelNeuroimmunology Unit, Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC H3A 2B4, Canada.ORCID https://orcid.org/0000-0002-5148-0636
Alexandre PratNeuroimmunology Research Laboratory, Centre de Recherche du Centre Hospitalier de l'Université de Montréal (CRCHUM), Montreal, QC H2X 0A9, Canada.ORCID https://orcid.org/0000-0001-6188-0580
Francisco J QuintanaAnn Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA. fquintana@bwh.harvard.edu.ORCID https://orcid.org/0000-0001-8156-0736
Brigham and Women's Hospital · USBroad Institute · USBoston University · USCentre Hospitalier de l’Université de Montréal · CAMontreal Neurological Institute and Hospital · CAQB3 · USUniversity of Freiburg · DE
Funding
VectorP30CA006516 · NCI · DANA-FARBER CANCER INSTITUTE · PI JENNIFER W MACK · 1985 to 2026
$330.6MTraining in the Molecular Biology of Neurodegeneration and Alzheimer's DiseaseT32AG000222 · NIA · HARVARD UNIVERSITY (MEDICAL SCHOOL) · PI Bruce A YANKNER · 1992 to 2026
$18.5MMulti-omic dissection of the transcriptional, epigenetic, and proteomic signatures of cells infected with latent HIVR01AI149699 · NIAID · BRIGHAM AND WOMEN'S HOSPITAL · PI ABATE, ADAM R., QUINTANA, FRANCISCO J. · 2020 to 2024
$3.8MAHR-mediated immunosuppression in glioblastomaR01ES029136 · NIEHS · BRIGHAM AND WOMEN'S HOSPITAL · PI Francisco J. Quintana, DAVID A REARDON · 2019 to 2026
$3.3MCancer Immunology Training GrantT32CA207021 · NCI · DANA-FARBER CANCER INST · PI WUCHERPFENNIG, KAI W · 2016 to 2020
$2.4MDecoding the language of inflammation between central nervous system resident immune cellsDP2AI154435 · NIAID · UNIVERSITY OF CALIFORNIA BERKELEY · PI Iain Clark · 2021 to 2026
$2.4MRegulation of CNS AutoimmunityR01AI126880 · NIAID · BRIGHAM AND WOMEN'S HOSPITAL · PI QUINTANA, FRANCISCO J. · 2017 to 2021
$2.1MControl of Local CNS InflammationR01NS102807 · NINDS · BRIGHAM AND WOMEN'S HOSPITAL · PI QUINTANA, FRANCISCO J. · 2018 to 2022
$1.8MMolecular Control of Astrocytes in CNS InflammationR00NS114111 · NINDS · BRIGHAM AND WOMEN'S HOSPITAL · PI WHEELER, MICHAEL ALEX · 2023 to 2025
$783kWhite Matter Pathology and Infiltrating T cells in the Brain of Cognitively Impaired Aging Rhesus MonkeysR21AG061678 · NIA · BOSTON UNIVERSITY MEDICAL CAMPUS · PI ROSENE, DOUGLAS L · 2019 to 2020
$454kMyelin-reactivity of a novel population of T cells infiltrating the normal aging monkey brainF30AG063463 · NIA · BOSTON UNIVERSITY MEDICAL CAMPUS · PI TRECARTIN, KATELYN · 2019 to 2022
$203kMolecular Control of Astrocytes in CNS InflammationK99NS114111 · NINDS · BRIGHAM AND WOMEN'S HOSPITAL · PI WHEELER, MICHAEL ALEX · 2020 to 2021
$189kNCI NIH HHS P30 CA006516NCI NIH HHS T32 CA207021NIAID NIH HHS DP2 AI154435NIAID NIH HHS R01 AI126880NIAID NIH HHS R01 AI149699NIA NIH HHS F30 AG063463NIA NIH HHS R21 AG061678NIA NIH HHS T32 AG000222NIEHS NIH HHS R01 ES029136NINDS NIH HHS F32 NS101790NINDS NIH HHS K99 NS114111NINDS NIH HHS R00 NS114111NINDS NIH HHS R01 NS102807
Abstract
Cell-cell interactions control the physiology and pathology of the central nervous system (CNS). To study astrocyte cell interactions in vivo, we developed rabies barcode interaction detection followed by sequencing (RABID-seq), which combines barcoded viral tracing and single-cell RNA sequencing (scRNA-seq). Using RABID-seq, we identified axon guidance molecules as candidate mediators of microglia-astrocyte interactions that promote CNS pathology in experimental autoimmune encephalomyelitis (EAE) and, potentially, multiple sclerosis (MS). In vivo cell-specific genetic perturbation EAE studies, in vitro systems, and the analysis of MS scRNA-seq datasets and CNS tissue established that Sema4D and Ephrin-B3 expressed in microglia control astrocyte responses via PlexinB2 and EphB3, respectively. Furthermore, a CNS-penetrant EphB3 inhibitor suppressed astrocyte and microglia proinflammatory responses and ameliorated EAE. In summary, RABID-seq identified microglia-astrocyte interactions and candidate therapeutic targets.
Indexed as
Cell CommunicationSingle-Cell AnalysisAnimalsAntigens, CDAstrocytesBrainCentral Nervous SystemEncephalomyelitis, Autoimmune, ExperimentalEphrin-B3Herpesvirus 1, SuidHumansMaleMiceMice, Inbred C57BLMicrogliaMitochondriaAntigens, CDCD100 antigenEphrin-B3mTOR protein, mouseNerve Tissue ProteinsNF-kappa BPLXNB1 protein, humanPlxnb1 protein, mousePLXNB2 protein, humanPlxnb2 protein, mouseReactive Oxygen SpeciesReceptor, EphB3Receptors, Cell SurfaceSema4d protein, mouseSemaphorinsTOR Serine-Threonine Kinases
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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.