A retroviral link to vertebrate myelination through retrotransposon-RNA-mediated control of myelin gene expression.

ERV LTR convergent evolution endogenous retrovirus long terminal repeat myelination oligodendrocyte oligodendrocyte progenitor cells retrotransposon transposable element

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
15 Feb 2024
Historique:
received: 12 12 2022
revised: 12 10 2023
accepted: 07 01 2024
medline: 17 2 2024
pubmed: 17 2 2024
entrez: 16 2 2024
Statut: ppublish

Résumé

Myelin, the insulating sheath that surrounds neuronal axons, is produced by oligodendrocytes in the central nervous system (CNS). This evolutionary innovation, which first appears in jawed vertebrates, enabled rapid transmission of nerve impulses, more complex brains, and greater morphological diversity. Here, we report that RNA-level expression of RNLTR12-int, a retrotransposon of retroviral origin, is essential for myelination. We show that RNLTR12-int-encoded RNA binds to the transcription factor SOX10 to regulate transcription of myelin basic protein (Mbp, the major constituent of myelin) in rodents. RNLTR12-int-like sequences (which we name RetroMyelin) are found in all jawed vertebrates, and we further demonstrate their function in regulating myelination in two different vertebrate classes (zebrafish and frogs). Our study therefore suggests that retroviral endogenization played a prominent role in the emergence of vertebrate myelin.

Identifiants

DOI: 10.1016/j.cell.2024.01.011 PMID: 38364788
pubmed: 38364788
pii: S0092-8674(24)00013-8
doi: 10.1016/j.cell.2024.01.011
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

814-830.e23

Informations de copyright

Copyright © 2024 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Tanay Ghosh (T)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK; Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK. Electronic address: writetotanay@gmail.com.

Rafael G Almeida (RG)

Centre for Discovery Brain Sciences, MS society Edinburgh Centre for MS Research, University of Edinburgh, Chancellor's Building, 49 Little France Crescent, Edinburgh EH16 4SB, UK.

Chao Zhao (C)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK; Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK.

Abdelkrim Mannioui (A)

Sorbonne Université, Institut de Biologie Paris-Seine (IBPS), Aquatic Facility, 75005 Paris, France.

Elodie Martin (E)

Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, 75013 Paris, France.

Alex Fleet (A)

Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK.

Civia Z Chen (CZ)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK; Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK.

Peggy Assinck (P)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK; Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK.

Sophie Ellams (S)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK.

Ginez A Gonzalez (GA)

Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK.

Stephen C Graham (SC)

Division of Virology, Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge CB2 1QP, UK.

David H Rowitch (DH)

Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Paediatrics, University of Cambridge, Cambridge, UK.

Katherine Stott (K)

Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, UK.

Ian Adams (I)

MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh EH4 2XU, UK.

Bernard Zalc (B)

Sorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, 75013 Paris, France.

Nick Goldman (N)

European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome, Genome Campus, Hinxton, Cambridge CB10 1SD, UK.

David A Lyons (DA)

Centre for Discovery Brain Sciences, MS society Edinburgh Centre for MS Research, University of Edinburgh, Chancellor's Building, 49 Little France Crescent, Edinburgh EH16 4SB, UK.

Robin J M Franklin (RJM)

Altos Labs-Cambridge Institute of Science, Cambridge CB21 6GP, UK; Wellcome-MRC Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 0AW, UK; Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0AW, UK. Electronic address: rfranklin@altoslabs.com.

Classifications MeSH