Distribution of particle aggregates in the internodal axolemma and adaxonal schwann cell membrane of rodent peripheral nerve

doi:10.1016/0022-510X(85)90117-0

Journal of the Neurological Sciences

Volume 67, Issue 2, February 1985, Pages 213-222

https://doi.org/10.1016/0022-510X(85)90117-0 Get rights and content

Abstract

Freeze-fracture studies on myelinated fibres from the internodal regions of rat and mouse sciatic nerve show symmetrical particle aggregates within the adaxonal Schwann cell plasmalemma and particle clusters in the axolemma. These are mainly confined to the vicinity of the internal mesaxon and the Schmidt-Lanterman incisures. The Schwann cell particle aggregates are concentrated as bands over the cytoplasmic pockets of Schmidt-Lanterman incisures and the paramesaxonal pockets. In the axolemma there are linear rows of particle aggregates along the groove related to the inner mesaxon and in bands to either side of it. The morphological features suggest the possibility of metabolic coupling between the axoplasm and the Schwann cell cytoplasm via the periaxonal space.

References (24)

G. Allt et al.
Demyelination — A failure of cell communication
J. Neurol. Sci.
(1982)
D.J. Milek et al.
An immunological characterization of the basic proteins of rodent sciatic nerve myelin
Brain Res.
(1981)
R.G. Miller et al.
Particle rosettes in the periaxonal Schwann cell membrane and particle clusters in the axolemma of the rat sciatic nerve
Brain Res.
(1977)
C. Stolinski et al.
Freeze-fracture replication of mammalian peripheral nerve — A review
J. Neurol. Sci.
(1982)
H. Weinberg et al.
Studies on the control of myelinogenesis, Part 2 (Evidence for neuronal regulation of myelin production)
Brain Res.
(1976)
A. Aguayo et al.
Potential of Schwann cells from unmyelinated nerves to produce myelin — A quantitative ultrastructural and radiographic study
J. Neurocytol.
(1976)
M.J. Cullen et al.
Electron microscopic study of intramembranous changes in protein-extracted peripheral nervous system myelin
Anat. Rec.
(1983)
R.L. Friede et al.
The clefts of Schmidt-Lanterman — A quantitative electron microscopic study of their structure in developing and adult sciatic nerves of the rat
Anat. Rec.
(1969)
R.C. Hughes
Membrane Glycoprotein — A Review of Structure and Function
(1976)
N. Krishnan et al.
Penetration of peroxidase into peripheral nerve fibers
Amer. J. Anat.
(1973)

F.X. Omlin et al.

Immunocytochemical localization of basic protein in major dense line regions of central and peripheral myelin

J. Cell Biol.

(1982)

J. Rosenbluth

Intramembranous particle distribution in nerve fiber membranes

Experientia (Basel)

(1983)

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Molecular disruptions of the panglial syncytium block potassium siphoning and axonal saltatory conduction: pertinence to neuromyelitis optica and other demyelinating diseases of the central nervous system
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Citation Excerpt :
This suggested even then that the axonal rosettes might have an unrecognized role in saltatory conduction, possibly corresponding to voltage-gated K+ channels (Stolinski et al., 1985). Equally important, the same freeze-fracture replicas (Miller and Pinto da Silva, 1977; Stolinski et al., 1981, 1985) revealed that the innermost (adaxonal) layer of Schwann cell myelin membrane overlying the juxtaparanodal axonal plasma membrane also contained distinctive rosettes of P-face (protoplasmic leaflet) particles (Fig. 4B1, B2, arrowheads) of exactly the same spacing as the axonal E-face particle rosettes (Fig. 4B1, arrowheads; B3, large arrow). On rare occasions, the fracture plane stepped from axonal to Schwann cell plasma membranes within an individual rosette (Fig. 4B3, large arrow), revealing that the axonal E-face particles were precisely aligned with the particles in the P-face rosettes in the myelin plasma membrane (Stolinski et al., 1981), demonstrating structural coupling and, therefore, implying functional coupling of the two distinct types of rosette particles.
The panglial syncytium maintains ionic conditions required for normal neuronal electrical activity in the central nervous system (CNS). Vital among these homeostatic functions is “potassium siphoning,” a process originally proposed to explain astrocytic sequestration and long-distance disposal of K⁺ released from unmyelinated axons during each action potential. Fundamentally different, more efficient processes are required in myelinated axons, where axonal K⁺ efflux occurs exclusively beneath and enclosed within the myelin sheath, precluding direct sequestration of K⁺ by nearby astrocytes. Molecular mechanisms for entry of excess K⁺ and obligatorily-associated osmotic water from axons into innermost myelin are not well characterized, whereas at the output end, axonally-derived K⁺ and associated osmotic water are known to be expelled by Kir4.1 and aquaporin-4 channels concentrated in astrocyte endfeet that surround capillaries and that form the glia limitans. Between myelin (input end) and astrocyte endfeet (output end) is a vast network of astrocyte “intermediaries” that are strongly inter-linked, including with myelin, by abundant gap junctions that disperse excess K⁺ and water throughout the panglial syncytium, thereby greatly reducing K⁺-induced osmotic swelling of myelin. Here, I review original reports that established the concept of potassium siphoning in unmyelinated CNS axons, summarize recent revolutions in our understanding of K⁺ efflux during axonal saltatory conduction, then describe additional components required by myelinated axons for a newly-described process of voltage-augmented “dynamic” potassium siphoning. If any of several molecular components of the panglial syncytium are compromised, K⁺ siphoning is blocked, myelin is destroyed, and axonal saltatory conduction ceases. Thus, a common thread linking several CNS demyelinating diseases is the disruption of potassium siphoning/water transport within the panglial syncytium. Continued progress in molecular identification and subcellular mapping of glial ion and water channels will lead to a better understanding of demyelinating diseases of the CNS and to development of improved treatment regimens.
Functional Organization of the Nodes of Ranvier
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This chapter reviews the molecular architecture of the nodes of Ranvier. The recent advances in the molecular anatomy of myelinated axons highlight several functional issues. One of the most surprising is that peripheral nervous system (PNS) myelin sheaths do not mainly act as electrical insulators of axons. The radial pathway for ion diffusion formed by gap junctions is not compatible with this common view and reducing capacitance is the likely role of myelin sheaths. Second, the intricate organization of the nodal, paranodal, juxtaparanodal, and internodal axonal domains relate closely to the organization of the myelin sheath itself. Although the details are still incomplete, the emerging evidence indicates that a molecular dialogue between myelinating glial cells and axons results in the local differentiation of their complementary cellular domains. Finally, the organization of the axonal membrane is disrupted by a number of mutations and disease processes that affect myelin sheaths, with functional consequences that are beginning to make sense.
Altered connexin expression after peripheral nerve injury
1996, Molecular and Cellular Neurosciences
The identification of connexin32 (Cx32) in myelinating Schwann cells and the association of Cx32 mutations with peripheral neuropathies suggest a functional role for gap junction proteins in the nerve. However, after nerve crush injury, Cx32 expression dramatically decreases in Schwann cells in the degenerating region, returning to control levels at newly formed nodes of Ranvier and Schmidt–Lantermann incisures by 30 days. The present study examined increases in expression of other connexins that occur after peripheral nerve injury. A 56/58-kDa connexin46 (Cx46) protein species was detected in adult rat sciatic nerve, along with very low levels of Cx46 mRNA. However, by 3 days after crush injury, coincident with changes in Schwann cell phenotype, Cx46 mRNA rapidly increased in the degenerating regions. Additionally, the 56/58-kDa Cx46 protein species present in adult nerve decreased and a 53-kDa Cx46 species, which was also present in cultured Schwann cells, became apparent. Connexin43 (Cx43) mRNA and protein, which was localized to perineurial cells in adult nerve, dramatically increased in endoneurial fibroblasts in the crush and distal regions by 3 days, coincident with macrophage infiltration. By 12 days after injury, Cx43 decreased and was comparable to normal nerve. These results suggest that enhanced expression of Cx46 and Cx43, by nonneuronal cells, may be important for the injury and regenerative responses of peripheral nerves.
Potassium channel-dependent changes in the volume of developing mouse Schwann cells
1991, Brain Research
Physiological roles of voltage-gated K⁺ channels in developing mouse Schwann cells were investigated using whole-cell variation of the patch-clamp technique. In neonatal myelin-associated Schwann cells, local cytoplasmic swellings were induced when membrane potential (MP) was kept more negative than zero-current potential (membrane hyperpolarization) and they decreased in sizes when MP was kept positive. A lack of changes of cytoplasmic volume Schwann cells of 17- to 18-day-old embryos or in neonatal myelin-associated cells in a solution containing Ba²⁺ suggested that activation of Ba²⁺-sensitive K⁺ channels caused cytoplasmic volume changes. Significant increase in magnitudes of Ba²⁺-sensitive K⁺ currents in neonatal myelin-associated cells after membrane hyperpolarization suggested that these K⁺ channels locate in adaxonal Schwann cell membrane and probably determine the sites of Schmidt-Lanterman incisures.
Macromolecular structure of the Schwann cell membrane. Perinodal microvilli
1987, Journal of the Neurological Sciences
The macromolecular structure of perinodal Schwann cell membrane was examined with freeze-fracture electron microscopy. Perinodal microvillous-like processes of Schwann cells exhibit an asymmetrical partitioning of intramembranous particles (IMPs), with a moderate (∼ 900/μm²) density of particles on P-faces and a lower (∼ 300/μm²) density of IMPs on E-faces. The densities of IMPs observed on the fracture faces of perinodal processes are similar to those within the outer membrane of the Schwann cell proper. On both fracture faces of the perinodal processes and the Schwann cell membrane proper, a high (∼ 45%) percentage of the IMPs displayed a large (⩾ 9.6 nm) diameter. Specialized junctions (i.e., gap junctions, tight junctions) between adjacent perinodal Schwann cell processes or between perinodal processes and nodal axolemmal were not observed.
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^☆: Financial support from the Medical Research Council is gratefully acknowledged (Project Grant G8224298N).

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Distribution of particle aggregates in the internodal axolemma and adaxonal schwann cell membrane of rodent peripheral nerve☆

Abstract

J. Neurol. Sci.

Brain Res.

Brain Res.

J. Neurol. Sci.

Brain Res.

Potential of Schwann cells from unmyelinated nerves to produce myelin — A quantitative ultrastructural and radiographic study

J. Neurocytol.

Electron microscopic study of intramembranous changes in protein-extracted peripheral nervous system myelin

Anat. Rec.

The clefts of Schmidt-Lanterman — A quantitative electron microscopic study of their structure in developing and adult sciatic nerves of the rat

Anat. Rec.

Membrane Glycoprotein — A Review of Structure and Function

Penetration of peroxidase into peripheral nerve fibers

Amer. J. Anat.

Immunocytochemical localization of basic protein in major dense line regions of central and peripheral myelin

J. Cell Biol.

Intramembranous particle distribution in nerve fiber membranes

Experientia (Basel)