Elsevier

Developmental Biology

Volume 79, Issue 2, October 1980, Pages 334-355
Developmental Biology

Full paper
Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration

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Abstract

The development of the node of Ranvier has been previously described using thin-section electron microscopy. Using freeze-fracture, we have examined the development of glial and axonal membrane specializations before and during myelination. The spinal roots of the newborn rat are composed of bundles of unmyelinated and partially myelinated axons. At this early stage of development, the axons are engulfed by Schwann cells, while certain axons are segregated into a one to one relationship with myelinating cells. Patches of uniformly shaped 150- to 300-Å particles are readily distinguished against a relatively nonparticulate axonal E face. Patches of less uniform particles are found in the axonal P face, however, they are difficult to distinguish from a particulate background. Thin processes are found closely applied to the axonal membrane on the sides of a particle patch. While engulfing the axon with one or two noncompacted windings, the Schwann cell is predominantly restricted to one side of such a particle patch. As the number of windings covering the axon increases, so does the size of the particle patch, until an annulus of particles, similar to that of an adult node, is observed. The paucity of isolated particle patches in axolemma suggests that recognition and segregation of axons by Schwann cells are followed by a rapid initiation of myelination. Throughout the early periods of myelination there is evidence of endocytotic and exocytotic events at the nodal membrane associated with the appearance of 230-Å dimeric particles in the axolemma. Despite the paucity of windings and complete absence of compaction, the fracture faces of the glial and axonal membranes show linear organizations of particles. Scalloped regions in the P face of the nodal axolemma display dimeric-particle rows oriented along the scallop. These rows adopt a more circumferential orientation when the overlying glial process is wound into a paranodal location. While the spacing of dimeric-particle rows is maintained at a constant 360 Å, the number of rows per scallop necessarily decreases with compaction of the paranodal loops until a state similar to that of the adult, in which there are approximately two rows per scallop, is reached. In regions of close apposition between axon and Schwann cell, a linear arrangement of 160- and 75-Å particles in the glial fracture faces occurs prior to the appearance of tight junctions between glial loops and prior to compaction. Though the paranodes on each side of most nodes observed developed symmetrically, some asymmetric half-nodes have been observed.

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    This work was supported by grants: M. H. Ellisman, from the National Institutes of Health (NS 14718) and the Muscular Dystrophy Association of America; Clayton A. Wiley-Livingston was supported by N.I.G.M.S. training grant #PHS G MQ 7198.

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