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Functional gap junctions in the schwann cell myelin sheath.

Balice-Gordon RJ, Bone LJ, Scherer SS - J. Cell Biol. (1998)

Bottom Line: Gap junctions are localized to periodic interruptions in the compact myelin called Schmidt-Lanterman incisures and to paranodes; these regions contain at least one gap junction protein, connexin32 (Cx32).The radial diffusion of low molecular weight dyes across the myelin sheath was not interrupted in myelinating Schwann cells from cx32- mice, indicating that other connexins participate in forming gap junctions in these cells.Owing to the unique geometry of myelinating Schwann cells, a gap junction-mediated radial pathway may be essential for rapid diffusion between the adaxonal and perinuclear cytoplasm, since this radial pathway is approximately one million times faster than the circumferential pathway.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, The University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074, USA. rbaliceg@mail.med.upenn.edu

ABSTRACT
The Schwann cell myelin sheath is a multilamellar structure with distinct structural domains in which different proteins are localized. Intracellular dye injection and video microscopy were used to show that functional gap junctions are present within the myelin sheath that allow small molecules to diffuse between the adaxonal and perinuclear Schwann cell cytoplasm. Gap junctions are localized to periodic interruptions in the compact myelin called Schmidt-Lanterman incisures and to paranodes; these regions contain at least one gap junction protein, connexin32 (Cx32). The radial diffusion of low molecular weight dyes across the myelin sheath was not interrupted in myelinating Schwann cells from cx32- mice, indicating that other connexins participate in forming gap junctions in these cells. Owing to the unique geometry of myelinating Schwann cells, a gap junction-mediated radial pathway may be essential for rapid diffusion between the adaxonal and perinuclear cytoplasm, since this radial pathway is approximately one million times faster than the circumferential pathway.

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Evidence for functional gap junctions in the incisures of  cx32- mice. Shown is a portion of a myelinated fiber from the  sciatic nerve of a cx32- mouse after injection of 5,6-carboxyfluorescein; the location of incisures is marked with white arrowheads. The intensity profile is illustrated for this fiber (scale,  0–255 intensity levels) across a line perpendicular to its long axis  at the location indicated by the black arrowhead. As in myelinating Schwann cells from wild-type mice, a train track pattern is apparent on at least one side of the axon. Bar, 10 μm.
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Figure 8: Evidence for functional gap junctions in the incisures of cx32- mice. Shown is a portion of a myelinated fiber from the sciatic nerve of a cx32- mouse after injection of 5,6-carboxyfluorescein; the location of incisures is marked with white arrowheads. The intensity profile is illustrated for this fiber (scale, 0–255 intensity levels) across a line perpendicular to its long axis at the location indicated by the black arrowhead. As in myelinating Schwann cells from wild-type mice, a train track pattern is apparent on at least one side of the axon. Bar, 10 μm.

Mentions: Since Cx32 is the only gap junction protein known to be localized to incisures, we evaluated the possibility that Cx32 is necessary for the diffusion of small molecular mass dyes across the myelin sheath by injecting myelinating Schwann cells from cx32- mice. We teased myelinated fibers from 4-mo-old mice, when few sciatic fibers are demyelinated (Anzini et al., 1997; Nelles et al., 1996; Scherer et al., 1998), avoiding any fibers that appeared abnormal, and injected them with 5,6-carboxyfluorescein by iontophoresis. When viewed with polarized light, myelinated fibers in cx32- mice had incisures, which was confirmed by MAG-immunostaining (Scherer et al., 1998). The mean resting potential (−6 ± 3 mV) in myelinating Schwann cells from cx32- mice was similar to that observed in wild type mice. Double train tracks of fluorescence (Fig. 8, left) and doublets in each peak of the line histogram analysis (Fig. 8, right) were observed in all of the successfully injected fibers (n = six fibers from three mice). Moreover, the mean rate of diffusion was estimated to be 4.09 ± 0.67 μm/s (n = five fibers from three mice; average ± SEM; range 2.02–7.58). This rate is not significantly different from that observed in myelinating Schwann cells from wild type mice (Student's t test). Thus, the absence of Cx32 does not appear to affect the radial pathway of dye diffusion across the myelin sheath, indicating that there are functional gap junctions in the incisures of cx32- mice.


Functional gap junctions in the schwann cell myelin sheath.

Balice-Gordon RJ, Bone LJ, Scherer SS - J. Cell Biol. (1998)

Evidence for functional gap junctions in the incisures of  cx32- mice. Shown is a portion of a myelinated fiber from the  sciatic nerve of a cx32- mouse after injection of 5,6-carboxyfluorescein; the location of incisures is marked with white arrowheads. The intensity profile is illustrated for this fiber (scale,  0–255 intensity levels) across a line perpendicular to its long axis  at the location indicated by the black arrowhead. As in myelinating Schwann cells from wild-type mice, a train track pattern is apparent on at least one side of the axon. Bar, 10 μm.
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Related In: Results  -  Collection

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Figure 8: Evidence for functional gap junctions in the incisures of cx32- mice. Shown is a portion of a myelinated fiber from the sciatic nerve of a cx32- mouse after injection of 5,6-carboxyfluorescein; the location of incisures is marked with white arrowheads. The intensity profile is illustrated for this fiber (scale, 0–255 intensity levels) across a line perpendicular to its long axis at the location indicated by the black arrowhead. As in myelinating Schwann cells from wild-type mice, a train track pattern is apparent on at least one side of the axon. Bar, 10 μm.
Mentions: Since Cx32 is the only gap junction protein known to be localized to incisures, we evaluated the possibility that Cx32 is necessary for the diffusion of small molecular mass dyes across the myelin sheath by injecting myelinating Schwann cells from cx32- mice. We teased myelinated fibers from 4-mo-old mice, when few sciatic fibers are demyelinated (Anzini et al., 1997; Nelles et al., 1996; Scherer et al., 1998), avoiding any fibers that appeared abnormal, and injected them with 5,6-carboxyfluorescein by iontophoresis. When viewed with polarized light, myelinated fibers in cx32- mice had incisures, which was confirmed by MAG-immunostaining (Scherer et al., 1998). The mean resting potential (−6 ± 3 mV) in myelinating Schwann cells from cx32- mice was similar to that observed in wild type mice. Double train tracks of fluorescence (Fig. 8, left) and doublets in each peak of the line histogram analysis (Fig. 8, right) were observed in all of the successfully injected fibers (n = six fibers from three mice). Moreover, the mean rate of diffusion was estimated to be 4.09 ± 0.67 μm/s (n = five fibers from three mice; average ± SEM; range 2.02–7.58). This rate is not significantly different from that observed in myelinating Schwann cells from wild type mice (Student's t test). Thus, the absence of Cx32 does not appear to affect the radial pathway of dye diffusion across the myelin sheath, indicating that there are functional gap junctions in the incisures of cx32- mice.

Bottom Line: Gap junctions are localized to periodic interruptions in the compact myelin called Schmidt-Lanterman incisures and to paranodes; these regions contain at least one gap junction protein, connexin32 (Cx32).The radial diffusion of low molecular weight dyes across the myelin sheath was not interrupted in myelinating Schwann cells from cx32- mice, indicating that other connexins participate in forming gap junctions in these cells.Owing to the unique geometry of myelinating Schwann cells, a gap junction-mediated radial pathway may be essential for rapid diffusion between the adaxonal and perinuclear cytoplasm, since this radial pathway is approximately one million times faster than the circumferential pathway.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, The University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6074, USA. rbaliceg@mail.med.upenn.edu

ABSTRACT
The Schwann cell myelin sheath is a multilamellar structure with distinct structural domains in which different proteins are localized. Intracellular dye injection and video microscopy were used to show that functional gap junctions are present within the myelin sheath that allow small molecules to diffuse between the adaxonal and perinuclear Schwann cell cytoplasm. Gap junctions are localized to periodic interruptions in the compact myelin called Schmidt-Lanterman incisures and to paranodes; these regions contain at least one gap junction protein, connexin32 (Cx32). The radial diffusion of low molecular weight dyes across the myelin sheath was not interrupted in myelinating Schwann cells from cx32- mice, indicating that other connexins participate in forming gap junctions in these cells. Owing to the unique geometry of myelinating Schwann cells, a gap junction-mediated radial pathway may be essential for rapid diffusion between the adaxonal and perinuclear cytoplasm, since this radial pathway is approximately one million times faster than the circumferential pathway.

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