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Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival.

Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, Trapp BD - J. Cell Biol. (1999)

Bottom Line: We demonstrate that L1 is present on axons and Schwann cells of sensory unmyelinated fibers, but only on Schwann cells of sympathetic unmyelinated fibers.In L1-deficient sensory nerves, Schwann cells formed but failed to retain normal axonal ensheathment.In nerve transplant studies, loss of axonal-L1, but not Schwann cell-L1, reproduced the L1-deficient phenotype.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106, USA.

ABSTRACT
This study investigated the function of the adhesion molecule L1 in unmyelinated fibers of the peripheral nervous system (PNS) by analysis of L1- deficient mice. We demonstrate that L1 is present on axons and Schwann cells of sensory unmyelinated fibers, but only on Schwann cells of sympathetic unmyelinated fibers. In L1-deficient sensory nerves, Schwann cells formed but failed to retain normal axonal ensheathment. L1-deficient mice had reduced sensory function and loss of unmyelinated axons, while sympathetic unmyelinated axons appeared normal. In nerve transplant studies, loss of axonal-L1, but not Schwann cell-L1, reproduced the L1-deficient phenotype. These data establish that heterophilic axonal-L1 interactions mediate adhesion between unmyelinated sensory axons and Schwann cells, stabilize the polarization of Schwann cell surface membranes, and mediate a trophic effect that assures axonal survival.

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Unmyelinated fibers in adult L1-deficient sympathetic nerves and P7 L1/MAG-deficient sural nerve appear normal. In the cervical sympathetic trunk (CST), an unmyelinated autonomic nerve, from wild-type (A) and L1-deficient mice (B), axons were normally segregated and surrounded by Schwann cell processes. In electron micrographs of sural nerves from P7 wild-type (C) and L1/MAG-deficient mice (D), Schwann cells surround multiple axons (C and D, arrows). Occasional axons are ensheathed by fragments of basal lamina (C and D, arrowheads) and many axons have segregated into one-to-one relationships with Schwann cells (C and D, asterisks). Sural nerves, sciatic nerves, and dorsal roots from P7 L1-deficient mice displayed none of the unmyelinated fiber phenotypes present in adult L1-deficient nerves. Ax, Axon; My, Myelinated fiber. Bars, 1 μm.
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Figure 3: Unmyelinated fibers in adult L1-deficient sympathetic nerves and P7 L1/MAG-deficient sural nerve appear normal. In the cervical sympathetic trunk (CST), an unmyelinated autonomic nerve, from wild-type (A) and L1-deficient mice (B), axons were normally segregated and surrounded by Schwann cell processes. In electron micrographs of sural nerves from P7 wild-type (C) and L1/MAG-deficient mice (D), Schwann cells surround multiple axons (C and D, arrows). Occasional axons are ensheathed by fragments of basal lamina (C and D, arrowheads) and many axons have segregated into one-to-one relationships with Schwann cells (C and D, asterisks). Sural nerves, sciatic nerves, and dorsal roots from P7 L1-deficient mice displayed none of the unmyelinated fiber phenotypes present in adult L1-deficient nerves. Ax, Axon; My, Myelinated fiber. Bars, 1 μm.

Mentions: Unmyelinated fibers in the cervical sympathetic trunk (CST), a predominantly unmyelinated autonomic nerve were also analyzed. Wild-type nonmyelinating Schwann cells of the CST engulf single axons in cytoplasmic troughs. At P60, the ultrastructure of wild-type (Fig. 3 A) and L1-deficient (Fig. 3 B) CST unmyelinated fibers was similar.


Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival.

Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, Trapp BD - J. Cell Biol. (1999)

Unmyelinated fibers in adult L1-deficient sympathetic nerves and P7 L1/MAG-deficient sural nerve appear normal. In the cervical sympathetic trunk (CST), an unmyelinated autonomic nerve, from wild-type (A) and L1-deficient mice (B), axons were normally segregated and surrounded by Schwann cell processes. In electron micrographs of sural nerves from P7 wild-type (C) and L1/MAG-deficient mice (D), Schwann cells surround multiple axons (C and D, arrows). Occasional axons are ensheathed by fragments of basal lamina (C and D, arrowheads) and many axons have segregated into one-to-one relationships with Schwann cells (C and D, asterisks). Sural nerves, sciatic nerves, and dorsal roots from P7 L1-deficient mice displayed none of the unmyelinated fiber phenotypes present in adult L1-deficient nerves. Ax, Axon; My, Myelinated fiber. Bars, 1 μm.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2169489&req=5

Figure 3: Unmyelinated fibers in adult L1-deficient sympathetic nerves and P7 L1/MAG-deficient sural nerve appear normal. In the cervical sympathetic trunk (CST), an unmyelinated autonomic nerve, from wild-type (A) and L1-deficient mice (B), axons were normally segregated and surrounded by Schwann cell processes. In electron micrographs of sural nerves from P7 wild-type (C) and L1/MAG-deficient mice (D), Schwann cells surround multiple axons (C and D, arrows). Occasional axons are ensheathed by fragments of basal lamina (C and D, arrowheads) and many axons have segregated into one-to-one relationships with Schwann cells (C and D, asterisks). Sural nerves, sciatic nerves, and dorsal roots from P7 L1-deficient mice displayed none of the unmyelinated fiber phenotypes present in adult L1-deficient nerves. Ax, Axon; My, Myelinated fiber. Bars, 1 μm.
Mentions: Unmyelinated fibers in the cervical sympathetic trunk (CST), a predominantly unmyelinated autonomic nerve were also analyzed. Wild-type nonmyelinating Schwann cells of the CST engulf single axons in cytoplasmic troughs. At P60, the ultrastructure of wild-type (Fig. 3 A) and L1-deficient (Fig. 3 B) CST unmyelinated fibers was similar.

Bottom Line: We demonstrate that L1 is present on axons and Schwann cells of sensory unmyelinated fibers, but only on Schwann cells of sympathetic unmyelinated fibers.In L1-deficient sensory nerves, Schwann cells formed but failed to retain normal axonal ensheathment.In nerve transplant studies, loss of axonal-L1, but not Schwann cell-L1, reproduced the L1-deficient phenotype.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, School of Medicine, Case Western Reserve University, Cleveland, Ohio 44106, USA.

ABSTRACT
This study investigated the function of the adhesion molecule L1 in unmyelinated fibers of the peripheral nervous system (PNS) by analysis of L1- deficient mice. We demonstrate that L1 is present on axons and Schwann cells of sensory unmyelinated fibers, but only on Schwann cells of sympathetic unmyelinated fibers. In L1-deficient sensory nerves, Schwann cells formed but failed to retain normal axonal ensheathment. L1-deficient mice had reduced sensory function and loss of unmyelinated axons, while sympathetic unmyelinated axons appeared normal. In nerve transplant studies, loss of axonal-L1, but not Schwann cell-L1, reproduced the L1-deficient phenotype. These data establish that heterophilic axonal-L1 interactions mediate adhesion between unmyelinated sensory axons and Schwann cells, stabilize the polarization of Schwann cell surface membranes, and mediate a trophic effect that assures axonal survival.

Show MeSH
Related in: MedlinePlus