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Research Article
Pushing myelination – developmental regulation of myosin expression drives oligodendrocyte morphological differentiation
Helena Sofia Domingues, Mateusz M. Urbanski, Sandra Macedo-Ribeiro, Amr Almaktari, Azka Irfan, Yamely Hernandez, Haibo Wang, João Bettencourt Relvas, Boris Rubinstein, Carmen V. Melendez-Vasquez, Inês Mendes Pinto
Journal of Cell Science 2020 133: jcs232264 doi: 10.1242/jcs.232264 Published 5 August 2020
Helena Sofia Domingues
1International Iberian Nanotechnology Laboratory (INL), 4715-330 Braga, Portugal
2Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, 4200-135 Porto, Portugal
3Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, 4200-135 Porto, Portugal
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Mateusz M. Urbanski
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
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Sandra Macedo-Ribeiro
2Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, 4200-135 Porto, Portugal
3Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, 4200-135 Porto, Portugal
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Amr Almaktari
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
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  • ORCID record for Amr Almaktari
Azka Irfan
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
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  • ORCID record for Azka Irfan
Yamely Hernandez
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
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  • ORCID record for Yamely Hernandez
Haibo Wang
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
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João Bettencourt Relvas
2Instituto de Investigação e Inovação em Saúde (I3S), Universidade do Porto, 4200-135 Porto, Portugal
3Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, 4200-135 Porto, Portugal
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Boris Rubinstein
5Stowers Institute for Medical Research, Kansas City, MO 64110, USA
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Carmen V. Melendez-Vasquez
4Department of Biological Sciences, Hunter College City University of New York, New York, NY 10065, USA
6The Graduate Center, City University of New York (CUNY), New York, NY 10016, USA
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  • For correspondence: melendez@genectr.hunter.cuny.edu ines.m.pinto@inl.int
Inês Mendes Pinto
1International Iberian Nanotechnology Laboratory (INL), 4715-330 Braga, Portugal
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  • ORCID record for Inês Mendes Pinto
  • For correspondence: melendez@genectr.hunter.cuny.edu ines.m.pinto@inl.int

Handling Editor: Giampietro Schiavo

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ABSTRACT

Oligodendrocytes are the central nervous system myelin-forming cells providing axonal electrical insulation and higher-order neuronal circuitry. The mechanical forces driving the differentiation of oligodendrocyte precursor cells into myelinating oligodendrocytes are largely unknown, but likely require the spatiotemporal regulation of the architecture and dynamics of the actin and actomyosin cytoskeletons. In this study, we analyzed the expression pattern of myosin motors during oligodendrocyte development. We report that oligodendrocyte differentiation is regulated by the synchronized expression and non-uniform distribution of several members of the myosin network, particularly non-muscle myosins 2B and 2C, which potentially operate as nanomechanical modulators of cell tension and myelin membrane expansion at different cell stages.

This article has an associated First Person interview with the first author of the paper.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: H.S.D., B.R., C.V.M.-V., I.M.P.; Methodology: H.S.D., C.V.M.-V., I.M.P.; Formal analysis: H.S.D., C.V.M.-V., I.M.P.; Investigation: H.S.D., M.M.U., S.M.-R., A.A., A.I., Y.H., H.W., J.B.R., B.R., C.V.M.-V., I.M.P.; Writing - original draft: H.S.D., I.M.P.; Writing - review & editing: H.S.D., C.V.M.-V., I.M.P.; Supervision: C.V.M.-V., I.M.P.; Funding acquisition: C.V.M.-V., I.M.P.

  • Funding

    H.S.D. received financial support by Fundação para a Ciência e Tecnologia (FCT) through a post-doctoral fellowship with the reference SFRH/BPD/90268/2012. S.M.-R. and J.B.R. were supported by FEDER (Fundo Europeu de Desenvolvimento Regional) funds through Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement in the framework of Project Norte-01-0145-FEDER-000008 (Porto Neurosciences and Neurologic Disease Research Initiative at I3S). C.V.M.-V., M.M.U. and H.W. were supported by the National Institutes of Health (SC1NS000001) and by a Research Centers in Minority Institutions Program grant from the National Center for Research Resources (G12 RR003037). I.M.P. received financial support from the Marie Curie COFUND Programme “NanoTRAINforGrowth”, from the European Union's Seventh Framework Programme for research, technological development and demonstration under grant agreement no 600375. This article is a result of the project Nanotechnology based functional solutions (NORTE-01-0145-FEDER-000019), co-financed by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). Deposited in PMC for release after 12 months.

  • Supplementary information

    Supplementary information available online at https://jcs.biologists.org/lookup/doi/10.1242/jcs.232264.supplemental

  • Received March 22, 2019.
  • Accepted June 24, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Myosinome
  • Oligodendrocyte differentiation
  • Myelination
  • Cell tension
  • Membrane expansion

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Research Article
Pushing myelination – developmental regulation of myosin expression drives oligodendrocyte morphological differentiation
Helena Sofia Domingues, Mateusz M. Urbanski, Sandra Macedo-Ribeiro, Amr Almaktari, Azka Irfan, Yamely Hernandez, Haibo Wang, João Bettencourt Relvas, Boris Rubinstein, Carmen V. Melendez-Vasquez, Inês Mendes Pinto
Journal of Cell Science 2020 133: jcs232264 doi: 10.1242/jcs.232264 Published 5 August 2020
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Research Article
Pushing myelination – developmental regulation of myosin expression drives oligodendrocyte morphological differentiation
Helena Sofia Domingues, Mateusz M. Urbanski, Sandra Macedo-Ribeiro, Amr Almaktari, Azka Irfan, Yamely Hernandez, Haibo Wang, João Bettencourt Relvas, Boris Rubinstein, Carmen V. Melendez-Vasquez, Inês Mendes Pinto
Journal of Cell Science 2020 133: jcs232264 doi: 10.1242/jcs.232264 Published 5 August 2020

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