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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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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.
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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.

Mentions: Premyelinating oligodendrocytes detected in the developing corpus callosum were strikingly different from those in the cerebral cortex. DM-20/PLP–positive cell bodies usually occurred in clusters of two to four cells (Fig. 2, A and B, arrowheads) that were oriented parallel to developing axons. These cells extended multiple processes that appeared to overlap extensively. At postnatal day 7, some clusters of DM-20/PLP–positive cells did not include obvious developing myelin internodes (Fig. 2 A; also see Fig. 3, C and D), while others did (Fig. 2 B, arrows). By postnatal day 11, the corpus callosum contained many clusters of DM-20/PLP–positive cells and developing myelin internodes (Fig. 2 C). Since our analysis suggested that premyelinating oligodendrocytes in the cerebral cortex had more orderly arranged processes than those in the corpus callosum, sections stained with DM-20/PLP antibodies were analyzed by confocal microscopy (Fig. 3). Fig. 3 A is a single confocal image (∼1.0-μm-thick) of a premyelinating oligodendrocyte in the developing cerebral cortex. Fig. 3 B is a stack of 20 confocal images (∼20-μm-thick) of the same cell. The relatively symmetrical and nonoverlapping distribution of the DM-20/PLP–positive processes is apparent in both images. When a similar comparison was performed on a cluster of premyelinating oligodendrocytes in the developing corpus callosum (Fig. 3, C and D), their processes arborized and overlapped extensively. Our initial immunocytochemical analysis also suggested that premyelinating oligodendrocytes occupied larger neuropil domains in the cerebral cortex than in the corpus callosum. Therefore, the radius of the area occupied by cell bodies and processes of individual DM-20/PLP–positive premyelinating oligodendrocytes in P7 corpus callosum and cerebral cortex was compared. The radius of premyelinating cells was 78.5 ± 8.2 μm (n = 60) in the cortex and 39.8 ± 9.5 μm (n = 45) in the corpus callosum. Student's t test demonstrated that this difference was statistically significant (P < 0.001).


Differentiation and death of premyelinating oligodendrocytes in developing rodent brain.

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

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.
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Related In: Results  -  Collection

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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.
Mentions: Premyelinating oligodendrocytes detected in the developing corpus callosum were strikingly different from those in the cerebral cortex. DM-20/PLP–positive cell bodies usually occurred in clusters of two to four cells (Fig. 2, A and B, arrowheads) that were oriented parallel to developing axons. These cells extended multiple processes that appeared to overlap extensively. At postnatal day 7, some clusters of DM-20/PLP–positive cells did not include obvious developing myelin internodes (Fig. 2 A; also see Fig. 3, C and D), while others did (Fig. 2 B, arrows). By postnatal day 11, the corpus callosum contained many clusters of DM-20/PLP–positive cells and developing myelin internodes (Fig. 2 C). Since our analysis suggested that premyelinating oligodendrocytes in the cerebral cortex had more orderly arranged processes than those in the corpus callosum, sections stained with DM-20/PLP antibodies were analyzed by confocal microscopy (Fig. 3). Fig. 3 A is a single confocal image (∼1.0-μm-thick) of a premyelinating oligodendrocyte in the developing cerebral cortex. Fig. 3 B is a stack of 20 confocal images (∼20-μm-thick) of the same cell. The relatively symmetrical and nonoverlapping distribution of the DM-20/PLP–positive processes is apparent in both images. When a similar comparison was performed on a cluster of premyelinating oligodendrocytes in the developing corpus callosum (Fig. 3, C and D), their processes arborized and overlapped extensively. Our initial immunocytochemical analysis also suggested that premyelinating oligodendrocytes occupied larger neuropil domains in the cerebral cortex than in the corpus callosum. Therefore, the radius of the area occupied by cell bodies and processes of individual DM-20/PLP–positive premyelinating oligodendrocytes in P7 corpus callosum and cerebral cortex was compared. The radius of premyelinating cells was 78.5 ± 8.2 μm (n = 60) in the cortex and 39.8 ± 9.5 μm (n = 45) in the corpus callosum. Student's t test demonstrated that this difference was statistically significant (P < 0.001).

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