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Cited by 395Neurogenesis and neuroplasticity mechanismsNeonatal and fetal brain pathologyMultiple Sclerosis Research Studies

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Differentiation and Death of Premyelinating Oligodendrocytes in Developing Rodent Brain

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Trapp, Bruce D., Nishiyama, Akiko, Cheng, David, Macklin, Wendy·1997·The Journal of Cell Biology
DOI 10.1083/jcb.137.2.459PMC PMC2139778
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Abstract

Previous studies have indicated that newly formed oligodendrocytes are dynamic cells whose production, survival, and differentiation depend upon axonal influences. This study has characterized the appearance and fate of newly formed oligodendrocytes in developing rat brain. Oligodendrocytes appear in predictable locations and radially extend DM-20-positive processes that cover 80-microm domains in the cortex and 40-microm domains in the corpus callosum. These premyelinating oligodendrocytes have one of two fates: they myelinate axons or degenerate. Between 7 and 21 d after birth, approximately 20% of premyelinating oligodendrocytes identified in the cerebral cortex were degenerating. Oligodendrocytes that ensheathed axons expressed and selectively targeted proteolipid protein to compact myelin and did not degenerate. These observations support the hypothesis that axonal influences affect oligodendrocyte survival, differentiation, and expression of proteolipid protein gene products.

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Figure 1 Comparison of the distribution of DM-20/PLP immunoreactivity in sections from 11- (A) and 21-d-old (B) rat brain. The increased distribution of immunoreactivity in B reflects the developmental progression of myelination. Premyelinating oligodendrocytes are concentrated at the leading edge of myelinated fibers projecting toward the pial surface (A, arrowheads) and in layer I of the cortex. Premyelinating oligodendrocytes radially extend multiple processes that cover distinct neuropil domains (C, arrowheads). While most premyelinating oligodendrocytes in the cerebral cortex are separated from each other, occasional pairs are detected (C, asterisk). Processes of adjacent cells rarely overlap even when cells appear in pairs. Myelinating oligodendrocytes (C, arrows) send processes to vertically oriented DM-20/PLP–positive myelin internodes. Other regions of DM-20/PLP immunoreactivity is fragmented (D, arrowheads) and covers approximately the same neuropil area as healthy-appearing premyelinating oligodendrocytes (D, arrow). Bars: (A and B) 200 μm; (C and D) 50 μm.
Figure 1 Comparison of the distribution of DM-20/PLP immunoreactivity in sections from 11- (A) and 21-d-old (B) rat brain. The increased distribution of immunoreactivity in B reflects the developmental progression of myelination. Premyelinating oligodendrocytes are concentrated at the leading edge of myelinated fibers projecting toward the pial surface (A, arrowheads) and in layer I of the cortex. Premyelinating oligodendrocytes radially extend multiple processes that cover distinct neuropil domains (C, arrowheads). While most premyelinating oligodendrocytes in the cerebral cortex are separated from each other, occasional pairs are detected (C, asterisk). Processes of adjacent cells rarely overlap even when cells appear in pairs. Myelinating oligodendrocytes (C, arrows) send processes to vertically oriented DM-20/PLP–positive myelin internodes. Other regions of DM-20/PLP immunoreactivity is fragmented (D, arrowheads) and covers approximately the same neuropil area as healthy-appearing premyelinating oligodendrocytes (D, arrow). Bars: (A and B) 200 μm; (C and D) 50 μm.CC BY-NC-SA · PubMed Central
Figure 2 Premyelinating oligodendrocytes in the corpus callosum from 7- (A and B) and 11-d-old (C) rats. DM-20/PLP–positive premyelinating oligodendrocytes occur in clusters (A and B, arrowheads) in the corpus callosum. Clustered perikarya appear before evidence of myelin formation (A) and persist during active myelination (B and C). Bars, 50 μm.
Figure 2 Premyelinating oligodendrocytes in the corpus callosum from 7- (A and B) and 11-d-old (C) rats. DM-20/PLP–positive premyelinating oligodendrocytes occur in clusters (A and B, arrowheads) in the corpus callosum. Clustered perikarya appear before evidence of myelin formation (A) and persist during active myelination (B and C). Bars, 50 μm.CC BY-NC-SA · PubMed Central
Figure 3 Premyelinating oligodendrocytes in cerebral cortex and corpus callosum have different morphologies. Confocal images of single (A and C) and reconstructions of 20 (B and D) 1-μm-thick optical sections of DM-20/PLP–positive premyelinating oligodendrocytes from the cerebral cortex (A and B) and corpus callosum (C and D). Cortical cells (A and B) extend an orderly array of processes that tend to branch in a Y-shaped manner as they terminate. Premyelinating oligodendrocytes in the corpus callosum (C and D) occur in groups and extend processes in a less orderly and overlapping fashion. Bars, 10 μm.
Figure 3 Premyelinating oligodendrocytes in cerebral cortex and corpus callosum have different morphologies. Confocal images of single (A and C) and reconstructions of 20 (B and D) 1-μm-thick optical sections of DM-20/PLP–positive premyelinating oligodendrocytes from the cerebral cortex (A and B) and corpus callosum (C and D). Cortical cells (A and B) extend an orderly array of processes that tend to branch in a Y-shaped manner as they terminate. Premyelinating oligodendrocytes in the corpus callosum (C and D) occur in groups and extend processes in a less orderly and overlapping fashion. Bars, 10 μm.CC BY-NC-SA · PubMed Central
Figure 4 Premyelinating oligodendrocytes differentiate into myelinating oligodendrocytes. DM-20/PLP–positive oligodendrocytes before myelination (A), during early stages of axonal ensheathment (B, arrowheads), and during active myelination (C). Bar, 10 μm.
Figure 4 Premyelinating oligodendrocytes differentiate into myelinating oligodendrocytes. DM-20/PLP–positive oligodendrocytes before myelination (A), during early stages of axonal ensheathment (B, arrowheads), and during active myelination (C). Bar, 10 μm.CC BY-NC-SA · PubMed Central
Figure 5 Comparison of the distribution of DM-20/PLP (red) and PLP (green) in confocal images of oligodendrocytes. Areas of colocalization appear yellow. During early stages of axonal ensheathment, DM-20/PLP immunoreactivity is evenly distributed on oligodendrocyte processes (A, red) and developing myelin internodes (A, red and yellow), while PLP-specific immunoreactivity is restricted to perinuclear cytoplasm and developing myelin internodes (A, yellow). In more mature oligodendrocytes, DM-20/PLP is detected in oligodendrocyte processes and myelin, while PLP is restricted to perinuclear cytoplasm and myelin (B, yellow). Asterisks and arrowheads denote nucleus of cell and myelin internodes. Bars, 10 μm.
Figure 5 Comparison of the distribution of DM-20/PLP (red) and PLP (green) in confocal images of oligodendrocytes. Areas of colocalization appear yellow. During early stages of axonal ensheathment, DM-20/PLP immunoreactivity is evenly distributed on oligodendrocyte processes (A, red) and developing myelin internodes (A, red and yellow), while PLP-specific immunoreactivity is restricted to perinuclear cytoplasm and developing myelin internodes (A, yellow). In more mature oligodendrocytes, DM-20/PLP is detected in oligodendrocyte processes and myelin, while PLP is restricted to perinuclear cytoplasm and myelin (B, yellow). Asterisks and arrowheads denote nucleus of cell and myelin internodes. Bars, 10 μm.CC BY-NC-SA · PubMed Central
Figure 6 Comparison of DM-20/PLP immunoreactivity and nuclear chromatin staining in developing rat brain. Premyelinating oligodendrocytes with DM-20/PLP immunoreactivity evenly distributed on their surface (A) have diffuse nuclear chromatin staining (A, inset). Premyelinating oligodendrocytes with fragmented DM-20/PLP staining (B) and DM-20/PLP–positive necrotic-appearing cells (C) have condensed and fragmented nuclear chromatin (B and C, inset). A, B, and C were photographed with bright field optics; insets were photographed with ultraviolet optics. Bar, 10 μm.
Figure 6 Comparison of DM-20/PLP immunoreactivity and nuclear chromatin staining in developing rat brain. Premyelinating oligodendrocytes with DM-20/PLP immunoreactivity evenly distributed on their surface (A) have diffuse nuclear chromatin staining (A, inset). Premyelinating oligodendrocytes with fragmented DM-20/PLP staining (B) and DM-20/PLP–positive necrotic-appearing cells (C) have condensed and fragmented nuclear chromatin (B and C, inset). A, B, and C were photographed with bright field optics; insets were photographed with ultraviolet optics. Bar, 10 μm.CC BY-NC-SA · PubMed Central
Figure 7 Premyelinating oligodendrocytes are generated from NG2-positive progenitor cells. Confocal images of sections (30-μmthick) from 7-d-old rat cerebral cortices that were immunostained with NG2 (green) and DM-20/PLP (red) antibodies. A network of NG2-positive cells covers the cortical neuropil (A, green). DM-20/PLP–positive premyelinating cells are less abundant (A, red). A small but consistent population of cells are weakly stained by both NG2 and DM-20/PLP antibodies (B and C, arrowheads). NG2 immunoreactivity is punctate on the plasma membrane of these cells, whereas DM-20/PLP appears punctate in perinuclear cytoplasm on proximal cell processes (B and C). Bars, 10 μm.
Figure 7 Premyelinating oligodendrocytes are generated from NG2-positive progenitor cells. Confocal images of sections (30-μmthick) from 7-d-old rat cerebral cortices that were immunostained with NG2 (green) and DM-20/PLP (red) antibodies. A network of NG2-positive cells covers the cortical neuropil (A, green). DM-20/PLP–positive premyelinating cells are less abundant (A, red). A small but consistent population of cells are weakly stained by both NG2 and DM-20/PLP antibodies (B and C, arrowheads). NG2 immunoreactivity is punctate on the plasma membrane of these cells, whereas DM-20/PLP appears punctate in perinuclear cytoplasm on proximal cell processes (B and C). Bars, 10 μm.CC BY-NC-SA · PubMed Central
Figure 8 Schematic summary of oligodendrocyte lineage in vivo. Progenitor cells produce premyelinating oligodendrocytes. Premyelinating oligodendrocytes occupy distinct neuropil domains and depend on axonal signal(s) for survival. Images are two-dimensional reconstructions of confocal images.
Figure 8 Schematic summary of oligodendrocyte lineage in vivo. Progenitor cells produce premyelinating oligodendrocytes. Premyelinating oligodendrocytes occupy distinct neuropil domains and depend on axonal signal(s) for survival. Images are two-dimensional reconstructions of confocal images.CC BY-NC-SA · PubMed Central

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  1. Nishiyama, 1996, Interaction between NG2 proteoglycan and PDGF α receptor on 02A progenitor cells is required for optimal response to PDGF, J Neurosci Res, 43, 315, 10.1002/(SICI)1097-4547(19960201)43:3<315::AID-JNR6>3.0.CO;2-M · DOI

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Metadata

Authors
Trapp, B. D., Nishiyama, A., Cheng, D., & Macklin, W.
Affiliations
Cleveland Clinic (US)
ORCID
Venue
The Journal of Cell Biology
Publisher
Rockefeller University Press
Published
1997-04-21
Volume
137
Issue
2
Pages
459-468
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.137.2.459
PMC
PMC2139778
OpenAlex
W2097849969
Cited by
395
References
41
Citations by year
2026: 7 · 2025: 10 · 2024: 9 · 2023: 16 · 2022: 14 · 2021: 23 · 2020: 26 · 2019: 16 · 2018: 13 · 2017: 15 · 2016: 12 · 2015: 13 · 2014: 13 · 2013: 10 · 2012: 7
FWCI
4.80
Type
journal article
Language
en
Open access
Locations
  • The Journal of Cell Biology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • National Multiple Sclerosis Society
  • Multiple Sclerosis Society
  • National Institutes of Health
  • National Institute of Neurological Disorders and Stroke (NS25304, R01NS029818, R01NS025304, NS 29818)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
  • Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Keywords
oligodendrocyte differentiation, oligodendrocyte death, myelination, proteolipid protein, DM20, oligodendrocyte survival, cerebral cortex, corpus callosum, postnatal brain development
MeSH terms
Animals, Axons, Brain, Cell Differentiation, Cerebral Cortex, Chromatin, Corpus Callosum, Nerve Tissue Proteins, Oligodendroglia, Cell Death, Rats, Sprague-Dawley, Myelin Proteolipid Protein, Rats

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