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Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes
BACKGROUND: Oligodendrocytes are glial cells that support and insulate axons in the central nervous system through the production of myelin. Oligodendrocytes arise throughout embryonic and early postnatal development from oligodendrocyte precursor cells (OPCs), and recent work demonstrated that they...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9131697/ https://www.ncbi.nlm.nih.gov/pubmed/35610641 http://dx.doi.org/10.1186/s12915-022-01325-z |
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author | Hilscher, Markus M. Langseth, Christoffer Mattsson Kukanja, Petra Yokota, Chika Nilsson, Mats Castelo-Branco, Gonçalo |
author_facet | Hilscher, Markus M. Langseth, Christoffer Mattsson Kukanja, Petra Yokota, Chika Nilsson, Mats Castelo-Branco, Gonçalo |
author_sort | Hilscher, Markus M. |
collection | PubMed |
description | BACKGROUND: Oligodendrocytes are glial cells that support and insulate axons in the central nervous system through the production of myelin. Oligodendrocytes arise throughout embryonic and early postnatal development from oligodendrocyte precursor cells (OPCs), and recent work demonstrated that they are a transcriptional heterogeneous cell population, but the regional and functional implications of this heterogeneity are less clear. Here, we apply in situ sequencing (ISS) to simultaneously probe the expression of 124 marker genes of distinct oligodendrocyte populations, providing comprehensive maps of the corpus callosum, cingulate, motor, and somatosensory cortex in the brain, as well as gray matter (GM) and white matter (WM) regions in the spinal cord, at postnatal (P10), juvenile (P20), and young adult (P60) stages. We systematically compare the abundances of these populations and investigate the neighboring preference of distinct oligodendrocyte populations. RESULTS: We observed that oligodendrocyte lineage progression is more advanced in the juvenile spinal cord compared to the brain, corroborating with previous studies. We found myelination still ongoing in the adult corpus callosum while it was more advanced in the cortex. Interestingly, we also observed a lateral-to-medial gradient of oligodendrocyte lineage progression in the juvenile cortex, which could be linked to arealization, as well as a deep-to-superficial gradient with mature oligodendrocytes preferentially accumulating in the deeper layers of the cortex. The ISS experiments also exposed differences in abundances and population dynamics over time between GM and WM regions in the brain and spinal cord, indicating regional differences within GM and WM, and we found that neighboring preferences of some oligodendroglia populations are altered from the juvenile to the adult CNS. CONCLUSIONS: Overall, our ISS experiments reveal spatial heterogeneity of oligodendrocyte lineage progression in the brain and spinal cord and uncover differences in the timing of oligodendrocyte differentiation and myelination, which could be relevant to further investigate functional heterogeneity of oligodendroglia, especially in the context of injury or disease. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01325-z. |
format | Online Article Text |
id | pubmed-9131697 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91316972022-05-26 Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes Hilscher, Markus M. Langseth, Christoffer Mattsson Kukanja, Petra Yokota, Chika Nilsson, Mats Castelo-Branco, Gonçalo BMC Biol Research Article BACKGROUND: Oligodendrocytes are glial cells that support and insulate axons in the central nervous system through the production of myelin. Oligodendrocytes arise throughout embryonic and early postnatal development from oligodendrocyte precursor cells (OPCs), and recent work demonstrated that they are a transcriptional heterogeneous cell population, but the regional and functional implications of this heterogeneity are less clear. Here, we apply in situ sequencing (ISS) to simultaneously probe the expression of 124 marker genes of distinct oligodendrocyte populations, providing comprehensive maps of the corpus callosum, cingulate, motor, and somatosensory cortex in the brain, as well as gray matter (GM) and white matter (WM) regions in the spinal cord, at postnatal (P10), juvenile (P20), and young adult (P60) stages. We systematically compare the abundances of these populations and investigate the neighboring preference of distinct oligodendrocyte populations. RESULTS: We observed that oligodendrocyte lineage progression is more advanced in the juvenile spinal cord compared to the brain, corroborating with previous studies. We found myelination still ongoing in the adult corpus callosum while it was more advanced in the cortex. Interestingly, we also observed a lateral-to-medial gradient of oligodendrocyte lineage progression in the juvenile cortex, which could be linked to arealization, as well as a deep-to-superficial gradient with mature oligodendrocytes preferentially accumulating in the deeper layers of the cortex. The ISS experiments also exposed differences in abundances and population dynamics over time between GM and WM regions in the brain and spinal cord, indicating regional differences within GM and WM, and we found that neighboring preferences of some oligodendroglia populations are altered from the juvenile to the adult CNS. CONCLUSIONS: Overall, our ISS experiments reveal spatial heterogeneity of oligodendrocyte lineage progression in the brain and spinal cord and uncover differences in the timing of oligodendrocyte differentiation and myelination, which could be relevant to further investigate functional heterogeneity of oligodendroglia, especially in the context of injury or disease. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01325-z. BioMed Central 2022-05-25 /pmc/articles/PMC9131697/ /pubmed/35610641 http://dx.doi.org/10.1186/s12915-022-01325-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Hilscher, Markus M. Langseth, Christoffer Mattsson Kukanja, Petra Yokota, Chika Nilsson, Mats Castelo-Branco, Gonçalo Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title | Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title_full | Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title_fullStr | Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title_full_unstemmed | Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title_short | Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
title_sort | spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9131697/ https://www.ncbi.nlm.nih.gov/pubmed/35610641 http://dx.doi.org/10.1186/s12915-022-01325-z |
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