Distribution of Schwann cell cytoplasm and plasmalemmal vesicles (caveolae) in peripheral myelin sheaths. An electron microscopic study with thin sections and freeze-fracturing

Enrico Mugnaini, Kirsten K. Osen, Bruce Schnapp, Victor L. Friedrich

Research output: Contribution to journalArticle

73 Citations (Scopus)

Abstract

The mode of distribution of Schwann cell cytoplasm in the various regions of the peripheral myelin sheath is reviewed using freeze-fractured and thin sectioned nerves from bullfrogs, chickens and cats, perfused with an aldehyde mixture or fixed in situ with potassium permanganate. It is shown that the peripheral myelin sheath consists of two domains: one 'semi-compact' at the outer and the inner turns, and one 'compact,' extending from the second to the next-to-last turns. In the semi-compact domain no major dense line is formed, although the cytoplasmic layer may be as thin as 50 Å. As is well known, a major dense line is formed instead in the compact domain. The whole sheath is bordered by a 'marginal cytoplasmic belt.' This communicates with a cytoplasmic reticulum present in the semi-compact domains and with a reticulum (formed by longitudinal and circumferential incisures) in the compact domain. Many cytoplasmic channels in the semi-compact domain end blindly, as do many of the longitudinal and the circumferential incisures. It is speculated that these cytoplasmic networks are in a dynamic state, and that the changes within the semi-compact domain may be faster than those in the compact region. Numerous uncoated vesicles, 600-1100 Å in diameter, open onto the plasmalemma in the perinuclear region, along the outer mesaxon, and in the larger cytoplasmic trabeculae on the outer surface of the sheath. These plasmalemmal vesicles (caveolae) do not occur on the thinner cytoplasmic channels, on the inner surface of the sheath or on the incisures. Horseradish peroxidase studies indicate that the plasmalemmal vesicles become filled with the enzyme but do not migrate into the cytoplasm within a 4 h period. The movement of cytoplasm within the myelin sheath and the significance of the vesicles are discussed. The matter is important, since there are indications from in vitro studies of cultured nervous tissue and of teased fibres, that movements take place in the myelin sheath. These are presumably related to cytoplasmic translocations capable of producing 'outpocketings and invaginations' of the sheath's contour and may also involve the Schmidt-Lanterman incisures (Murray and Hermann, 1965; Singer and Bryant, 1969; Gitlin and Singer, 1974). Although in vivo observation of intact nerves for several hours did not reveal conspicuous movements (Williams and Hall, 1970, 1971), it is an attractive hypothesis that cytoplasmic movements are involved both in the formation and maintenance of the myelin sheath and in pathologic alterations (Robertson, 1958; Webster, 1965, 1971).

Original languageEnglish (US)
Pages (from-to)647-668
Number of pages22
JournalJournal of Neurocytology
Volume6
Issue number6
DOIs
StatePublished - Dec 1977
Externally publishedYes

Fingerprint

Freeze Fracturing
Caveolae
Schwann Cells
Myelin Sheath
Cytoplasm
Electrons
Reticulum
Potassium Permanganate
Rana catesbeiana
Nerve Tissue
Horseradish Peroxidase
Aldehydes
Chickens
Cats
Maintenance
Observation
Enzymes

ASJC Scopus subject areas

  • Neuroscience(all)
  • Histology
  • Anatomy
  • Cell Biology

Cite this

Distribution of Schwann cell cytoplasm and plasmalemmal vesicles (caveolae) in peripheral myelin sheaths. An electron microscopic study with thin sections and freeze-fracturing. / Mugnaini, Enrico; Osen, Kirsten K.; Schnapp, Bruce; Friedrich, Victor L.

In: Journal of Neurocytology, Vol. 6, No. 6, 12.1977, p. 647-668.

Research output: Contribution to journalArticle

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abstract = "The mode of distribution of Schwann cell cytoplasm in the various regions of the peripheral myelin sheath is reviewed using freeze-fractured and thin sectioned nerves from bullfrogs, chickens and cats, perfused with an aldehyde mixture or fixed in situ with potassium permanganate. It is shown that the peripheral myelin sheath consists of two domains: one 'semi-compact' at the outer and the inner turns, and one 'compact,' extending from the second to the next-to-last turns. In the semi-compact domain no major dense line is formed, although the cytoplasmic layer may be as thin as 50 {\AA}. As is well known, a major dense line is formed instead in the compact domain. The whole sheath is bordered by a 'marginal cytoplasmic belt.' This communicates with a cytoplasmic reticulum present in the semi-compact domains and with a reticulum (formed by longitudinal and circumferential incisures) in the compact domain. Many cytoplasmic channels in the semi-compact domain end blindly, as do many of the longitudinal and the circumferential incisures. It is speculated that these cytoplasmic networks are in a dynamic state, and that the changes within the semi-compact domain may be faster than those in the compact region. Numerous uncoated vesicles, 600-1100 {\AA} in diameter, open onto the plasmalemma in the perinuclear region, along the outer mesaxon, and in the larger cytoplasmic trabeculae on the outer surface of the sheath. These plasmalemmal vesicles (caveolae) do not occur on the thinner cytoplasmic channels, on the inner surface of the sheath or on the incisures. Horseradish peroxidase studies indicate that the plasmalemmal vesicles become filled with the enzyme but do not migrate into the cytoplasm within a 4 h period. The movement of cytoplasm within the myelin sheath and the significance of the vesicles are discussed. The matter is important, since there are indications from in vitro studies of cultured nervous tissue and of teased fibres, that movements take place in the myelin sheath. These are presumably related to cytoplasmic translocations capable of producing 'outpocketings and invaginations' of the sheath's contour and may also involve the Schmidt-Lanterman incisures (Murray and Hermann, 1965; Singer and Bryant, 1969; Gitlin and Singer, 1974). Although in vivo observation of intact nerves for several hours did not reveal conspicuous movements (Williams and Hall, 1970, 1971), it is an attractive hypothesis that cytoplasmic movements are involved both in the formation and maintenance of the myelin sheath and in pathologic alterations (Robertson, 1958; Webster, 1965, 1971).",
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