Astrocyte-oligodendrocyte interaction regulates central nervous system regeneration.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
08 06 2023
Historique:
received: 18 10 2022
accepted: 18 05 2023
medline: 12 6 2023
pubmed: 9 6 2023
entrez: 8 6 2023
Statut: epublish

Résumé

Failed regeneration of myelin around neuronal axons following central nervous system damage contributes to nerve dysfunction and clinical decline in various neurological conditions, for which there is an unmet therapeutic demand. Here, we show that interaction between glial cells - astrocytes and mature myelin-forming oligodendrocytes - is a determinant of remyelination. Using in vivo/ ex vivo/ in vitro rodent models, unbiased RNA sequencing, functional manipulation, and human brain lesion analyses, we discover that astrocytes support the survival of regenerating oligodendrocytes, via downregulation of the Nrf2 pathway associated with increased astrocytic cholesterol biosynthesis pathway activation. Remyelination fails following sustained astrocytic Nrf2 activation in focally-lesioned male mice yet is restored by either cholesterol biosynthesis/efflux stimulation, or Nrf2 inhibition using the existing therapeutic Luteolin. We identify that astrocyte-oligodendrocyte interaction regulates remyelination, and reveal a drug strategy for central nervous system regeneration centred on targeting this interaction.

Identifiants

pubmed: 37291151
doi: 10.1038/s41467-023-39046-8
pii: 10.1038/s41467-023-39046-8
pmc: PMC10250470
doi:

Substances chimiques

NF-E2-Related Factor 2 0
Cholesterol 97C5T2UQ7J

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3372

Subventions

Organisme : Medical Research Council
ID : MRC/V031260/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N02256/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M020827/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/V031260/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

© 2023. The Author(s).

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Auteurs

Irene Molina-Gonzalez (I)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.
Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK.

Rebecca K Holloway (RK)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.
Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK.

Zoeb Jiwaji (Z)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Owen Dando (O)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Sarah A Kent (SA)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.
Wellcome Trust Translational Neuroscience PhD programme, Edinburgh, UK.

Katie Emelianova (K)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Amy F Lloyd (AF)

Cell Signalling and Immunology, School of Life Sciences, University of Dundee, Dundee, DD1 5EH, UK.

Lindsey H Forbes (LH)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.
Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK.

Ayisha Mahmood (A)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.
Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK.

Thomas Skripuletz (T)

Department of Clinical Neuroimmunology and Neurochemistry, Department of Neurology, Medizinische Hochschule Hannover, Hannover, 30625, Germany.

Viktoria Gudi (V)

Department of Clinical Neuroimmunology and Neurochemistry, Department of Neurology, Medizinische Hochschule Hannover, Hannover, 30625, Germany.

James A Febery (JA)

Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Jeffrey A Johnson (JA)

Division of Pharmaceutical Sciences, University of Wisconsin, Madison, WI, 53705, USA.
Molecular and Environmental Toxicology Centre, University of Wisconsin, Madison, WI, 53706, USA.
Center for Neuroscience, University of Wisconsin, Madison, WI, 53705, USA.
Waisman Centre, University of Wisconsin, Madison, WI, 53705, USA.

Jill H Fowler (JH)

Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Tanja Kuhlmann (T)

Institute of Neuropathology, University Hospital Muenster, Muenster, D-48129, Germany.

Anna Williams (A)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Centre for Regenerative Medicine, Institute for Regeneration and Repair, University of Edinburgh, Edinburgh, EH16 5UU, UK.

Siddharthan Chandran (S)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Martin Stangel (M)

Department of Clinical Neuroimmunology and Neurochemistry, Department of Neurology, Medizinische Hochschule Hannover, Hannover, 30625, Germany.

Andrew J M Howden (AJM)

Cell Signalling and Immunology, School of Life Sciences, University of Dundee, Dundee, DD1 5EH, UK.

Giles E Hardingham (GE)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK.

Veronique E Miron (VE)

United Kingdom Dementia Research Institute at The University of Edinburgh, Edinburgh Medical School, Edinburgh, EH16 4TJ, UK. veronique.miron@unityhealth.to.
United Kingdom Multiple Sclerosis Society Edinburgh Centre for Multiple Sclerosis Research, University of Edinburgh, Edinburgh, EH16 4TJ, UK. veronique.miron@unityhealth.to.
Center for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH16 4SB, UK. veronique.miron@unityhealth.to.
Medical Research Council Centre for Reproductive Health, University of Edinburgh, Edinburgh, EH16 4TJ, UK. veronique.miron@unityhealth.to.
BARLO Multiple Sclerosis Centre, St.Michael's Hospital, Toronto, ON, M5B 1W8, Canada. veronique.miron@unityhealth.to.
Keenan Centre for Biomedical Research at St.Michael's Hospital, Toronto, ON, M5B 1T8, Canada. veronique.miron@unityhealth.to.
Department of Immunology, University of Toronto, Toronto, ON, M5S 1A8, Canada. veronique.miron@unityhealth.to.

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