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Differentiation and death of premyelinating oligodendrocytes in developing rodent brain.

Trapp BD, Nishiyama A, Cheng D, Macklin W - J. Cell Biol. (1997)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurosciences, Research Institute, The Cleveland Clinic Foundation, Ohio 44195, USA.

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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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.
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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.

Mentions: To determine if premyelinating oligodendrocytes could be identified with DM-20/PLP antibodies, sections of developing rat brain were immunostained with a monoclonal antibody directed against the 13 carboxy-terminal amino acids common to both proteins. In the cerebral cortex, myelination occurs in a predictable temporal and spatial sequence during the first three postnatal weeks. Myelination begins rostral to corpus callosum and progresses to the pial surface. Fig. 1 A demonstrates the distribution of DM20/PLP immunoreactivity in 11-d-old rat brain. Vertically oriented DM-20/PLP–positive, myelinated fibers extend from the deep cortical layers toward the pial surface. Patches of DM-20/PLP staining were also present near the leading edge of the myelination front (Fig. 1 A, arrowheads) and in layer I of the cortex. Most brain regions containing patches of DM-20/PLP immunoreactivity at 11 d are myelinated by 21 d (Fig. 1 B). When examined at higher magnification, many of these patches consisted of single cells that symmetrically radiated DM-20/PLP–positive processes (Fig. 1 C, arrowheads). Occasionally, these cells occurred in pairs (Fig. 1 C, asterisk), and processes of these paired cells occupied separate neuropil domains. Other DM-20/PLP–positive cells were connected to developing myelin internodes (Fig 1 C, arrows) and were located in deeper layers of the cortex. Some areas of DM-20/PLP immunoreactivity were fragmented and covered neuropil areas that were similar in size to oligodendrocytes that radially extend multiple processes (Fig. 1 D, arrowheads). These profiles represent dying oligodendrocytes, and they are described in detail below.


Differentiation and death of premyelinating oligodendrocytes in developing rodent brain.

Trapp BD, Nishiyama A, Cheng D, Macklin W - J. Cell Biol. (1997)

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.
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Related In: Results  -  Collection

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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.
Mentions: To determine if premyelinating oligodendrocytes could be identified with DM-20/PLP antibodies, sections of developing rat brain were immunostained with a monoclonal antibody directed against the 13 carboxy-terminal amino acids common to both proteins. In the cerebral cortex, myelination occurs in a predictable temporal and spatial sequence during the first three postnatal weeks. Myelination begins rostral to corpus callosum and progresses to the pial surface. Fig. 1 A demonstrates the distribution of DM20/PLP immunoreactivity in 11-d-old rat brain. Vertically oriented DM-20/PLP–positive, myelinated fibers extend from the deep cortical layers toward the pial surface. Patches of DM-20/PLP staining were also present near the leading edge of the myelination front (Fig. 1 A, arrowheads) and in layer I of the cortex. Most brain regions containing patches of DM-20/PLP immunoreactivity at 11 d are myelinated by 21 d (Fig. 1 B). When examined at higher magnification, many of these patches consisted of single cells that symmetrically radiated DM-20/PLP–positive processes (Fig. 1 C, arrowheads). Occasionally, these cells occurred in pairs (Fig. 1 C, asterisk), and processes of these paired cells occupied separate neuropil domains. Other DM-20/PLP–positive cells were connected to developing myelin internodes (Fig 1 C, arrows) and were located in deeper layers of the cortex. Some areas of DM-20/PLP immunoreactivity were fragmented and covered neuropil areas that were similar in size to oligodendrocytes that radially extend multiple processes (Fig. 1 D, arrowheads). These profiles represent dying oligodendrocytes, and they are described in detail below.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurosciences, Research Institute, The Cleveland Clinic Foundation, Ohio 44195, USA.

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.

Show MeSH
Related in: MedlinePlus