Transcriptional Convergence of Oligodendrocyte Lineage Progenitors during Development

Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-...

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Published inDevelopmental cell Vol. 46; no. 4; pp. 504 - 517.e7
Main Authors Marques, Sueli, van Bruggen, David, Vanichkina, Darya Pavlovna, Floriddia, Elisa Mariagrazia, Munguba, Hermany, Väremo, Leif, Giacomello, Stefania, Falcão, Ana Mendanha, Meijer, Mandy, Björklund, Åsa Kristina, Hjerling-Leffler, Jens, Taft, Ryan James, Castelo-Branco, Gonçalo
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 20.08.2018
Cell Press
Subjects
Animals
Cell Differentiation - physiology
Cell Lineage - physiology
Cell Proliferation - physiology
Cells, Cultured
myelin
neural development
neural progenitors
oligodendrocyte
oligodendrocyte precursor cell
Oligodendroglia - cytology
pericyte
platelet-derived growth factor receptor alpha
Receptor, Platelet-Derived Growth Factor alpha - metabolism
single-cell RNA-seq
Spinal Cord - metabolism
Stem Cells - cytology
transcription factors
transcriptomics
myelin
oligodendrocyte precursor cell
pericyte
transcription factors
platelet-derived growth factor receptor alpha
oligodendrocyte
transcriptomics
neural progenitors
single-cell RNA-seq
neural development
Online AccessGet full text
ISSN1534-5807
1878-1551
1878-1551
DOI10.1016/j.devcel.2018.07.005

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Abstract Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions. [Display omitted] •OPCs arising from different parts of the CNS are highly similar to one another•Pre-OPCs converge into similar transcriptional and electrophysiological OPC states•E13.5 Pdgfra+ cells give rise mainly to OPCs in the post-natal CNS•E13.5 Pdgfra+ cells also give rise to cells of the pericyte lineage Marques, van Bruggen, Vanichkina et al. present a bulk and single-cell transcriptomics resource of mouse forebrain and spinal cord Pdgfra+ cells at embryonic and post-natal stages. Embryonic Pdgfra+ cells produce distinct post-natal cell lineages. Post-natal oligodendrocyte precursor cells arising from different CNS regions are ultimately highly similar.
AbstractList Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions.
Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions. • OPCs arising from different parts of the CNS are highly similar to one another • Pre-OPCs converge into similar transcriptional and electrophysiological OPC states • E13.5 Pdgfra + cells give rise mainly to OPCs in the post-natal CNS • E13.5 Pdgfra + cells also give rise to cells of the pericyte lineage Marques, van Bruggen, Vanichkina et al. present a bulk and single-cell transcriptomics resource of mouse forebrain and spinal cord Pdgfra+ cells at embryonic and post-natal stages. Embryonic Pdgfra+ cells produce distinct post-natal cell lineages. Post-natal oligodendrocyte precursor cells arising from different CNS regions are ultimately highly similar.
Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions. [Display omitted] •OPCs arising from different parts of the CNS are highly similar to one another•Pre-OPCs converge into similar transcriptional and electrophysiological OPC states•E13.5 Pdgfra+ cells give rise mainly to OPCs in the post-natal CNS•E13.5 Pdgfra+ cells also give rise to cells of the pericyte lineage Marques, van Bruggen, Vanichkina et al. present a bulk and single-cell transcriptomics resource of mouse forebrain and spinal cord Pdgfra+ cells at embryonic and post-natal stages. Embryonic Pdgfra+ cells produce distinct post-natal cell lineages. Post-natal oligodendrocyte precursor cells arising from different CNS regions are ultimately highly similar.
Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions.Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear whether there is a correlation between these waves and different oligodendrocyte (OL) states at adult stages. Here, we present bulk and single-cell transcriptomics resources providing insights on how transitions between these states occur. We found that post-natal OPCs from brain and spinal cord present similar transcriptional signatures. Moreover, post-natal OPC progeny of E13.5 Pdgfra+ cells present electrophysiological and transcriptional profiles similar to OPCs derived from subsequent specification waves, indicating that Pdgfra+ pre-OPCs rewire their transcriptional network during development. Single-cell RNA-seq and lineage tracing indicates that a subset of E13.5 Pdgfra+ cells originates cells of the pericyte lineage. Thus, our results indicate that embryonic Pdgfra+ cells in the CNS give rise to distinct post-natal cell lineages, including OPCs with convergent transcriptional profiles in different CNS regions.
Author Björklund, Åsa Kristina
Hjerling-Leffler, Jens
Meijer, Mandy
Floriddia, Elisa Mariagrazia
Falcão, Ana Mendanha
Marques, Sueli
Väremo, Leif
Taft, Ryan James
Vanichkina, Darya Pavlovna
Munguba, Hermany
van Bruggen, David
Giacomello, Stefania
Castelo-Branco, Gonçalo
AuthorAffiliation 5 Science for Life Laboratory, Department of Biology and Biological Engineering, Chalmers University of Technology, Kemivägen 10, Göteborg 412 96, Sweden
6 Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Box 1031, 17121 Solna, Sweden
3 Institute for Molecular Bioscience, University of Queensland, St Lucia, QLD 4067, Australia
2 Gene and Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, NSW 2050, Australia
1 Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
7 Science for Life Laboratory, Department of Cell and Molecular Biology, Uppsala University, Husargatan 3, 75237 Uppsala, Sweden
4 Illumina, Inc., San Diego, CA 92122, USA
AuthorAffiliation_xml – name: 3 Institute for Molecular Bioscience, University of Queensland, St Lucia, QLD 4067, Australia
– name: 4 Illumina, Inc., San Diego, CA 92122, USA
– name: 7 Science for Life Laboratory, Department of Cell and Molecular Biology, Uppsala University, Husargatan 3, 75237 Uppsala, Sweden
– name: 6 Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Box 1031, 17121 Solna, Sweden
– name: 5 Science for Life Laboratory, Department of Biology and Biological Engineering, Chalmers University of Technology, Kemivägen 10, Göteborg 412 96, Sweden
– name: 2 Gene and Stem Cell Therapy Program, Centenary Institute, University of Sydney, Camperdown, NSW 2050, Australia
– name: 1 Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
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  surname: Marques
  fullname: Marques, Sueli
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
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  givenname: David
  surname: van Bruggen
  fullname: van Bruggen, David
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
– sequence: 3
  givenname: Darya Pavlovna
  surname: Vanichkina
  fullname: Vanichkina, Darya Pavlovna
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– sequence: 4
  givenname: Elisa Mariagrazia
  surname: Floriddia
  fullname: Floriddia, Elisa Mariagrazia
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
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  surname: Munguba
  fullname: Munguba, Hermany
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
– sequence: 6
  givenname: Leif
  surname: Väremo
  fullname: Väremo, Leif
  organization: Science for Life Laboratory, Department of Biology and Biological Engineering, Chalmers University of Technology, Kemivägen 10, Göteborg 412 96, Sweden
– sequence: 7
  givenname: Stefania
  surname: Giacomello
  fullname: Giacomello, Stefania
  organization: Science for Life Laboratory, Department of Biochemistry and Biophysics, Stockholm University, Box 1031, 17121 Solna, Sweden
– sequence: 8
  givenname: Ana Mendanha
  surname: Falcão
  fullname: Falcão, Ana Mendanha
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
– sequence: 9
  givenname: Mandy
  surname: Meijer
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  surname: Björklund
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  givenname: Jens
  surname: Hjerling-Leffler
  fullname: Hjerling-Leffler, Jens
  organization: Laboratory of Molecular Neurobiology, Department Medical Biochemistry and Biophysics, Biomedicum, Karolinska Institutet, Stockholm 17177, Sweden
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  givenname: Ryan James
  surname: Taft
  fullname: Taft, Ryan James
  organization: Institute for Molecular Bioscience, University of Queensland, St Lucia, QLD 4067, Australia
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  givenname: Gonçalo
  surname: Castelo-Branco
  fullname: Castelo-Branco, Gonçalo
  email: goncalo.castelo-branco@ki.se
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Issue 4
Keywords myelin
oligodendrocyte precursor cell
pericyte
transcription factors
platelet-derived growth factor receptor alpha
oligodendrocyte
transcriptomics
neural progenitors
single-cell RNA-seq
neural development
Language English
License This is an open access article under the CC BY license.
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Snippet Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear...
Pdgfra+ oligodendrocyte precursor cells (OPCs) arise in distinct specification waves during embryogenesis in the central nervous system (CNS). It is unclear...
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SubjectTerms Animals
Cell Differentiation - physiology
Cell Lineage - physiology
Cell Proliferation - physiology
Cells, Cultured
myelin
neural development
neural progenitors
oligodendrocyte
oligodendrocyte precursor cell
Oligodendroglia - cytology
pericyte
platelet-derived growth factor receptor alpha
Receptor, Platelet-Derived Growth Factor alpha - metabolism
single-cell RNA-seq
Spinal Cord - metabolism
Stem Cells - cytology
transcription factors
transcriptomics
Title Transcriptional Convergence of Oligodendrocyte Lineage Progenitors during Development
URI https://dx.doi.org/10.1016/j.devcel.2018.07.005
https://www.ncbi.nlm.nih.gov/pubmed/30078729
https://www.proquest.com/docview/2084338621
https://pubmed.ncbi.nlm.nih.gov/PMC6104814
https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-160092
https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-363938
https://research.chalmers.se/publication/504781
http://kipublications.ki.se/Default.aspx?queryparsed=id:138953176
Volume 46
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