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Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury

Author

Listed:
  • Elisa M. Floriddia

    (Karolinska Institutet, Biomedicum)

  • Tânia Lourenço

    (Karolinska Institutet, Biomedicum
    Biocant, Technology Transfer Association
    University of Coimbra)

  • Shupei Zhang

    (Karolinska Institutet, Biomedicum)

  • David Bruggen

    (Karolinska Institutet, Biomedicum)

  • Markus M. Hilscher

    (Stockholm University
    Cartana AB)

  • Petra Kukanja

    (Karolinska Institutet, Biomedicum)

  • João P. Gonçalves dos Santos

    (Karolinska Institutet, Biomedicum)

  • Müge Altınkök

    (Karolinska Institutet, Biomedicum)

  • Chika Yokota

    (Stockholm University)

  • Enric Llorens-Bobadilla

    (Karolinska Institutet, Biomedicum)

  • Sara B. Mulinyawe

    (Stanford University School of Medicine)

  • Mário Grãos

    (Biocant, Technology Transfer Association
    University of Coimbra)

  • Lu O. Sun

    (Stanford University School of Medicine
    University of Texas Southwestern Medical Center)

  • Jonas Frisén

    (Karolinska Institutet, Biomedicum)

  • Mats Nilsson

    (Stockholm University)

  • Gonçalo Castelo-Branco

    (Karolinska Institutet, Biomedicum
    Karolinska Institutet)

Abstract

Mature oligodendrocytes (MOLs) show transcriptional heterogeneity, the functional consequences of which are unclear. MOL heterogeneity might correlate with the local environment or their interactions with different neuron types. Here, we show that distinct MOL populations have spatial preference in the mammalian central nervous system (CNS). We found that MOL type 2 (MOL2) is enriched in the spinal cord when compared to the brain, while MOL types 5 and 6 (MOL5/6) increase their contribution to the OL lineage with age in all analyzed regions. MOL2 and MOL5/6 also have distinct spatial preference in the spinal cord regions where motor and sensory tracts run. OL progenitor cells (OPCs) are not specified into distinct MOL populations during development, excluding a major contribution of OPC intrinsic mechanisms determining MOL heterogeneity. In disease, MOL2 and MOL5/6 present different susceptibility during the chronic phase following traumatic spinal cord injury. Our results demonstrate that the distinct MOL populations have different spatial preference and different responses to disease.

Suggested Citation

  • Elisa M. Floriddia & Tânia Lourenço & Shupei Zhang & David Bruggen & Markus M. Hilscher & Petra Kukanja & João P. Gonçalves dos Santos & Müge Altınkök & Chika Yokota & Enric Llorens-Bobadilla & Sara B, 2020. "Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19453-x
    DOI: 10.1038/s41467-020-19453-x
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    Cited by:

    1. Enrica Boda & Martina Lorenzati & Roberta Parolisi & Brian Harding & Gianmarco Pallavicini & Luca Bonfanti & Amanda Moccia & Stephanie Bielas & Ferdinando Di Cunto & Annalisa Buffo, 2022. "Molecular and functional heterogeneity in dorsal and ventral oligodendrocyte progenitor cells of the mouse forebrain in response to DNA damage," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Yongheng Fan & Xianming Wu & Sufang Han & Qi Zhang & Zheng Sun & Bing Chen & Xiaoyu Xue & Haipeng Zhang & Zhenni Chen & Man Yin & Zhifeng Xiao & Yannan Zhao & Jianwu Dai, 2023. "Single-cell analysis reveals region-heterogeneous responses in rhesus monkey spinal cord with complete injury," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Thaddeus J. Kunkel & Alice Townsend & Kyle A. Sullivan & Jean Merlet & Edward H. Schuchman & Daniel A. Jacobson & Andrew P. Lieberman, 2023. "The cholesterol transporter NPC1 is essential for epigenetic regulation and maturation of oligodendrocyte lineage cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Kaya J. E. Matson & Daniel E. Russ & Claudia Kathe & Isabelle Hua & Dragan Maric & Yi Ding & Jonathan Krynitsky & Randall Pursley & Anupama Sathyamurthy & Jordan W. Squair & Boaz P. Levi & Gregoire Co, 2022. "Single cell atlas of spinal cord injury in mice reveals a pro-regenerative signature in spinocerebellar neurons," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Stefano Suzzi & Tommaso Croese & Adi Ravid & Or Gold & Abbe R. Clark & Sedi Medina & Daniel Kitsberg & Miriam Adam & Katherine A. Vernon & Eva Kohnert & Inbar Shapira & Sergey Malitsky & Maxim Itkin &, 2023. "N-acetylneuraminic acid links immune exhaustion and accelerated memory deficit in diet-induced obese Alzheimer’s disease mouse model," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Floriane Bretheau & Adrian Castellanos-Molina & Dominic Bélanger & Maxime Kusik & Benoit Mailhot & Ana Boisvert & Nicolas Vallières & Martine Lessard & Matthias Gunzer & Xiaoyu Liu & Éric Boilard & Ni, 2022. "The alarmin interleukin-1α triggers secondary degeneration through reactive astrocytes and endothelium after spinal cord injury," Nature Communications, Nature, vol. 13(1), pages 1-22, December.

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