TREM2 activation on microglia promotes myelin debris clearance and remyelination in a model of multiple sclerosis

Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed...

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Bibliographic Details
Published inActa neuropathologica Vol. 140; no. 4; pp. 513 - 534
Main Authors Cignarella, Francesca, Filipello, Fabia, Bollman, Bryan, Cantoni, Claudia, Locca, Alberto, Mikesell, Robert, Manis, Melissa, Ibrahim, Adiljan, Deng, Li, Benitez, Bruno A., Cruchaga, Carlos, Licastro, Danilo, Mihindukulasuriya, Kathie, Harari, Oscar, Buckland, Michael, Holtzman, David M., Rosenthal, Arnon, Schwabe, Tina, Tassi, Ilaria, Piccio, Laura
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer Berlin Heidelberg 01.10.2020
Springer
Springer Nature B.V
Subjects
Adult
Aged
Analysis
Animals
Antibodies
Central nervous system
Cuprizone
Demyelination
Disease Models, Animal
Ethylenediaminetetraacetic acid
Female
Gene expression
Glial stem cells
Humans
Macrophages
Male
Medicine
Medicine & Public Health
Membrane Glycoproteins - metabolism
Mice
Mice, Inbred C57BL
Mice, Knockout
Microglia
Microglia - metabolism
Middle Aged
Multiple sclerosis
Multiple Sclerosis - metabolism
Multiple Sclerosis - pathology
Myelin
Myelin Sheath - metabolism
Myelin Sheath - pathology
Myelination
Neurodegenerative diseases
Neurosciences
Oligodendrocytes
Original Paper
Pathology
Phagocytes
Phagocytosis - physiology
Receptors, Immunologic - metabolism
Remyelination - physiology
Viral antibodies
Online AccessGet full text

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Abstract Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed by microglia and promotes microglial survival, proliferation, and phagocytic activity. Herein we demonstrate that TREM2 was highly expressed on myelin-laden phagocytes in active demyelinating lesions in the CNS of subjects with MS. In gene expression studies, macrophages from subjects with TREM2 genetic deficiency displayed a defect in phagocytic pathways. Treatment with a new TREM2 agonistic antibody promoted the clearance of myelin debris in the cuprizone model of CNS demyelination. Effects included enhancement of myelin uptake and degradation, resulting in accelerated myelin debris removal by microglia. Most importantly, antibody-dependent TREM2 activation on microglia increased density of oligodendrocyte precursors in areas of demyelination, as well as the formation of mature oligodendrocytes thus enhancing remyelination and axonal integrity. These results are relevant as they propose TREM2 on microglia as a potential new target to promote remyelination.
AbstractList Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed by microglia and promotes microglial survival, proliferation, and phagocytic activity. Herein we demonstrate that TREM2 was highly expressed on myelin-laden phagocytes in active demyelinating lesions in the CNS of subjects with MS. In gene expression studies, macrophages from subjects with TREM2 genetic deficiency displayed a defect in phagocytic pathways. Treatment with a new TREM2 agonistic antibody promoted the clearance of myelin debris in the cuprizone model of CNS demyelination. Effects included enhancement of myelin uptake and degradation, resulting in accelerated myelin debris removal by microglia. Most importantly, antibody-dependent TREM2 activation on microglia increased density of oligodendrocyte precursors in areas of demyelination, as well as the formation of mature oligodendrocytes thus enhancing remyelination and axonal integrity. These results are relevant as they propose TREM2 on microglia as a potential new target to promote remyelination.
Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed by microglia and promotes microglial survival, proliferation, and phagocytic activity. Herein we demonstrate that TREM2 was highly expressed on myelin-laden phagocytes in active demyelinating lesions in the CNS of subjects with MS. In gene expression studies, macrophages from subjects with TREM2 genetic deficiency displayed a defect in phagocytic pathways. Treatment with a new TREM2 agonistic antibody promoted the clearance of myelin debris in the cuprizone model of CNS demyelination. Effects included enhancement of myelin uptake and degradation, resulting in accelerated myelin debris removal by microglia. Most importantly, antibody-dependent TREM2 activation on microglia increased density of oligodendrocyte precursors in areas of demyelination, as well as the formation of mature oligodendrocytes thus enhancing remyelination and axonal integrity. These results are relevant as they propose TREM2 on microglia as a potential new target to promote remyelination.
Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed by microglia and promotes microglial survival, proliferation, and phagocytic activity. Herein we demonstrate that TREM2 was highly expressed on myelin-laden phagocytes in active demyelinating lesions in the CNS of subjects with MS. In gene expression studies, macrophages from subjects with TREM2 genetic deficiency displayed a defect in phagocytic pathways. Treatment with a new TREM2 agonistic antibody promoted the clearance of myelin debris in the cuprizone model of CNS demyelination. Effects included enhancement of myelin uptake and degradation, resulting in accelerated myelin debris removal by microglia. Most importantly, antibody-dependent TREM2 activation on microglia increased density of oligodendrocyte precursors in areas of demyelination, as well as the formation of mature oligodendrocytes thus enhancing remyelination and axonal integrity. These results are relevant as they propose TREM2 on microglia as a potential new target to promote remyelination.Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune mechanisms. Microglia are critical for the clearance of myelin debris in areas of demyelination, a key step to allow remyelination. TREM2 is expressed by microglia and promotes microglial survival, proliferation, and phagocytic activity. Herein we demonstrate that TREM2 was highly expressed on myelin-laden phagocytes in active demyelinating lesions in the CNS of subjects with MS. In gene expression studies, macrophages from subjects with TREM2 genetic deficiency displayed a defect in phagocytic pathways. Treatment with a new TREM2 agonistic antibody promoted the clearance of myelin debris in the cuprizone model of CNS demyelination. Effects included enhancement of myelin uptake and degradation, resulting in accelerated myelin debris removal by microglia. Most importantly, antibody-dependent TREM2 activation on microglia increased density of oligodendrocyte precursors in areas of demyelination, as well as the formation of mature oligodendrocytes thus enhancing remyelination and axonal integrity. These results are relevant as they propose TREM2 on microglia as a potential new target to promote remyelination.
Audience Academic
Author Ibrahim, Adiljan
Filipello, Fabia
Mihindukulasuriya, Kathie
Mikesell, Robert
Buckland, Michael
Cantoni, Claudia
Locca, Alberto
Holtzman, David M.
Bollman, Bryan
Deng, Li
Schwabe, Tina
Manis, Melissa
Benitez, Bruno A.
Cruchaga, Carlos
Rosenthal, Arnon
Cignarella, Francesca
Piccio, Laura
Tassi, Ilaria
Harari, Oscar
Licastro, Danilo
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  givenname: Francesca
  surname: Cignarella
  fullname: Cignarella, Francesca
  organization: Department of Neurology, Washington University School of Medicine, Alector
– sequence: 2
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  surname: Filipello
  fullname: Filipello, Fabia
  organization: Department of Neurology, Washington University School of Medicine, Department of Biomedical Sciences, Humanitas University
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  surname: Bollman
  fullname: Bollman, Bryan
  organization: Department of Neurology, Washington University School of Medicine
– sequence: 4
  givenname: Claudia
  surname: Cantoni
  fullname: Cantoni, Claudia
  organization: Department of Neurology, Washington University School of Medicine
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  surname: Locca
  fullname: Locca, Alberto
  organization: Department of Neurology, Washington University School of Medicine
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  fullname: Mikesell, Robert
  organization: Department of Neurology, Washington University School of Medicine
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  organization: Department of Neurology, Washington University School of Medicine
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  fullname: Ibrahim, Adiljan
  organization: Alector
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  fullname: Deng, Li
  organization: Department of Neurology, Washington University School of Medicine, Department of Anesthesiology, First Affiliated Hospital of Soochow University
– sequence: 10
  givenname: Bruno A.
  surname: Benitez
  fullname: Benitez, Bruno A.
  organization: Department of Psychiatry, Washington University School of Medicine, Hope Center for Neurological Disorders, Washington University School of Medicine, NeuroGenomics and Informatics, Washington University School of Medicine
– sequence: 11
  givenname: Carlos
  surname: Cruchaga
  fullname: Cruchaga, Carlos
  organization: Department of Psychiatry, Washington University School of Medicine, Hope Center for Neurological Disorders, Washington University School of Medicine, NeuroGenomics and Informatics, Washington University School of Medicine
– sequence: 12
  givenname: Danilo
  surname: Licastro
  fullname: Licastro, Danilo
  organization: ARGO Open Lab Platform for Genome sequencing
– sequence: 13
  givenname: Kathie
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  fullname: Mihindukulasuriya, Kathie
  organization: Department of Psychiatry, Washington University School of Medicine, NeuroGenomics and Informatics, Washington University School of Medicine
– sequence: 14
  givenname: Oscar
  surname: Harari
  fullname: Harari, Oscar
  organization: Department of Psychiatry, Washington University School of Medicine, Hope Center for Neurological Disorders, Washington University School of Medicine, NeuroGenomics and Informatics, Washington University School of Medicine
– sequence: 15
  givenname: Michael
  surname: Buckland
  fullname: Buckland, Michael
  organization: Brain and Mind Centre, University of Sydney
– sequence: 16
  givenname: David M.
  surname: Holtzman
  fullname: Holtzman, David M.
  organization: Department of Neurology, Washington University School of Medicine, Hope Center for Neurological Disorders, Washington University School of Medicine
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  givenname: Arnon
  surname: Rosenthal
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  organization: Alector
– sequence: 18
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  fullname: Schwabe, Tina
  organization: Alector
– sequence: 19
  givenname: Ilaria
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  givenname: Laura
  orcidid: 0000-0002-8760-109X
  surname: Piccio
  fullname: Piccio, Laura
  email: picciol@wustl.edu, laura.piccio@sydney.edu.au
  organization: Department of Neurology, Washington University School of Medicine, NeuroGenomics and Informatics, Washington University School of Medicine, Brain and Mind Centre, University of Sydney
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32772264$$D View this record in MEDLINE/PubMed
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Snippet Multiple sclerosis (MS) is an inflammatory, demyelinating, and neurodegenerative disease of the central nervous system (CNS) triggered by autoimmune...
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Index Database
Enrichment Source
Publisher
StartPage 513
SubjectTerms Adult
Aged
Analysis
Animals
Antibodies
Central nervous system
Cuprizone
Demyelination
Disease Models, Animal
Ethylenediaminetetraacetic acid
Female
Gene expression
Glial stem cells
Humans
Macrophages
Male
Medicine
Medicine & Public Health
Membrane Glycoproteins - metabolism
Mice
Mice, Inbred C57BL
Mice, Knockout
Microglia
Microglia - metabolism
Middle Aged
Multiple sclerosis
Multiple Sclerosis - metabolism
Multiple Sclerosis - pathology
Myelin
Myelin Sheath - metabolism
Myelin Sheath - pathology
Myelination
Neurodegenerative diseases
Neurosciences
Oligodendrocytes
Original Paper
Pathology
Phagocytes
Phagocytosis - physiology
Receptors, Immunologic - metabolism
Remyelination - physiology
Viral antibodies
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Title TREM2 activation on microglia promotes myelin debris clearance and remyelination in a model of multiple sclerosis
URI https://link.springer.com/article/10.1007/s00401-020-02193-z
https://www.ncbi.nlm.nih.gov/pubmed/32772264
https://www.proquest.com/docview/2480551257
https://www.proquest.com/docview/2432431986
https://pubmed.ncbi.nlm.nih.gov/PMC7498497
Volume 140
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