Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes
Abstract 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 t...
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| Format: | Article |
| Language: | English |
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BMC
2022-05-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01325-z |
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| author | Markus M. Hilscher Christoffer Mattsson Langseth Petra Kukanja Chika Yokota Mats Nilsson Gonçalo Castelo-Branco |
| author_facet | Markus M. Hilscher Christoffer Mattsson Langseth Petra Kukanja Chika Yokota Mats Nilsson Gonçalo Castelo-Branco |
| author_sort | Markus M. Hilscher |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-12T18:18:06Z |
| format | Article |
| id | doaj.art-8ebec61e086345adbd3180bca6c5fb7d |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-12T18:18:06Z |
| publishDate | 2022-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-8ebec61e086345adbd3180bca6c5fb7d2022-12-22T03:21:32ZengBMCBMC Biology1741-70072022-05-0120111810.1186/s12915-022-01325-zSpatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypesMarkus M. Hilscher0Christoffer Mattsson Langseth1Petra Kukanja2Chika Yokota3Mats Nilsson4Gonçalo Castelo-Branco5Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm UniversityScience for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm UniversityLaboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Karolinska Institutet, BiomedicumScience for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm UniversityScience for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm UniversityLaboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Karolinska Institutet, BiomedicumAbstract 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.https://doi.org/10.1186/s12915-022-01325-zOligodendrocytesLineage progressionSpatial transcriptomicsIn situ sequencingCortexCorpus callosum |
| spellingShingle | Markus M. Hilscher Christoffer Mattsson Langseth Petra Kukanja Chika Yokota Mats Nilsson Gonçalo Castelo-Branco Spatial and temporal heterogeneity in the lineage progression of fine oligodendrocyte subtypes BMC Biology Oligodendrocytes Lineage progression Spatial transcriptomics In situ sequencing Cortex Corpus callosum |
| 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 | Oligodendrocytes Lineage progression Spatial transcriptomics In situ sequencing Cortex Corpus callosum |
| url | https://doi.org/10.1186/s12915-022-01325-z |
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