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A submicroscopic vesicular component of Schwann cells and nerve satellite cells
E.rtwrimenftrl
Cell
I
6, 543-545
A SUBMICROSCOPIC
543
(1954)
VESICULAR
CELLS
AND
NERVE
COMPONENT SATELLITE
E. D. P. DE ROBERTIS’ Department
0-f Anatomy,
CELLS1
and H. S. BENNETT of Washington,
Uniwrsity Received
OF SCHWANN
January
Seattle,
Wash.,
U.S.A.
28, 1954
P.uA~J< (3) has recently described a vesicular component in the cndothelial cells of blood capillaries. This component was recognizable in the form of spherical or oval vesicles of globules about 650 p\ in diameter. These vesicles could be seen throughout the cytoplasm of the endothelial cell, but were most abundant in the cytoplasmic region immediately adJacent to the inner and outer capillary cell membranes, where many of them were observed to open into the capillary lumen or into the pericapillary intercellular space. l’alade suggested that these vesicles might bear a relation to capillary permeability. More specifically, he suggested that they might represent a system for transporting fluids across the capillary wall by a process analogous to that of pinocytosis described by Lewis (2). In Lewis’s classical paper and motion picture tlrpicting this process, cells in tissue culture were observed to take in globules of fluid from the surrounding medium, the uptake of fluid being accompanied by vigorous cgtoplasmic motion at the edge of the cell, as if globules were being surrounded and engulfed by clasping folds of cytoplasm. Globules so taken in at the edge of the cell could then be observed by means of the light microscope to be transported as tiny vesicles to other portions of the cell several microns away. Since then pinocytosis has become a familiar phenomenon to observers of a wide variety of living cells in tissue culture or in transparent chambers. l’alade interpreted his electron micrographs as suggesting that a similar process might be occurring in capillary endothclial cells, but involving vesicles of submicroscopic dimensions. The purpose of this note is to confirm Palade’s findings with respect to blood capillaries, to concur in his interpretation, to show that Schwann cells and satellite cells of sympathetic neurones contain a similar vesicular component and to suggest that these cells may likewise transfer materials in an analogous manner. Sympathetic ganglia of the leopard frog (Kann pipiens) and of the bullfrog (Rana caksbiana) and the gracilis muscle of the mouse were fixed in Palade’s (4) buffered ostnic fixative, embedded in methacrylate and sectioned. Thin sections studied in the electron microscope revealed numerous capillaries showing the vesicles described by Palade (3), varying in diameter from X50-650 W (mean of 26 measurements, 520 A). These vesicles can be noted in Fig. 1 (a section from the sympathetic nerve ganglion of Rana pipiens), and in Fig. 4 (from the sympathetic ganglion of Rana catesbiana). 1 This
work
was supported
in part
by grants
the Eli Lilly Company; and the Hiologic&md z Present Montevideo,
address Uruguay.
-~
Department
of Cell
from
the Life
Insurance
Medical
Research
Fund,
Medical Research Fund of the State of Washington: L1ltrastructure,
Instituto
de Ciencias
Experimenlnl
Riol6gicas.
Cell Research
6
544
E. D, P. De Robertis
All figures are electron ganglia of the leopard Key: RUC S
micrographs of buffered osmic fixed sections of portions frog (Figs. 1, 2 and 3) and bullfrog (Figs. 3 and 5).
Cl ~~ capillary lumen; EC - endothelial - red blood cell; SC - satellite cell; sites of stomata or openings of vesicles.
Experimenfrd
and H. S. Bennett
Cell Hesearch
6
of sympathetic
cell; IS ~- intercellular space; N nerve cell body; SchC -- Schwann cell; \’ ~- vesicular component;
Vesicles in Schwann cells
545
The vesicles appear in greatest abundance at the capillary cell surfaces, particularly at the pericapillary surface. Many of the vesicles are oval or elongated, and some can be seen to open through tiny stomata or tubules into the pericapillary space (see X, Figs. 1 and 4). In Fig. 1 the capillary cell just referred to borders on a connective tissue space containing collagen and other connective tissue components. This space is in turn bordered on the left by a satellite cell attendant to a sympathetic ganglion cell, a portion of which occupies the upper left corner of the figure. Vesicles similar to those in the capillary are demonstrated within the cytoplasm of the satellite cell. Vesicles of this nature are likewise to be seen in the portions of satellite cells from the leopard frog shown in Figs. 2 and 3. Here some of the vesicles can be noted piercing the satellite cell wall by small tubules or stamata (at X), and similar vesicles can be seen within the neuronal cytoplasm in Fig. 2. Fig. 5 shows a tangential section through a portion of a Schwann cell from the sympathetic nerve of the bullfrog. A striking array of globules or vesicles is shown, most abundantly at the outer cell surface of the Schwann cell. Measurements of the diameters of 23 vesicles in satellite cells averaged 680 A, and of 30 vesicles in Schwann cells yielded a mean of 510 A. It is possible that these vesicles were encountered in Schwann cells by Hess and Lansing (l), who describe “circles” 300-300 A in diameter in the “neurilemma as it inflects at the node”. They suggest that these “holes” may be “pores or extensions . . . of the neurilcmma or membrane of the cell of Schwann”, and cite indications that such structure may exist elsewhere in the Schwann cells. However, their micrographs as reproduced do not show resolution or contrast sufficient to justify a certain conclusion regarding the identity of these “circles”. We are receptive to Palacle’s suggestion that the capillary vesicles may represent fluid globules in process of transport across the capillary cell, arguing that since uptake and transport by cells of fluid in vesicles of microscopic size is such a familiar and widespread phenomenon, it is altogether reasonable to postulate an ability of cells to move fluid in a similar manner in vacuoles of submicroscopic size. The very close resemblance of the vesicles in the Schwann cells to those in capillaries implies a similar function, and suggests that the Schwann cells and satellite cells may mediate exchange of materials between nerve cell and intercellular space in part by pumping material in tiny vesicles from one surface of the cell to the other, perhaps working the intravesicular contents over in passage, selectively adding to or removing substances along the way. These observations imply that the permeability properties of cellular membranes may be very complex, and are not likely to be described aclccluately by consiclcrations based on assumptions that such membranes function mainly as simple filters characterized by pores of certain sizes, as postulated by l’appcnheimcr (5). REFERENCES 1. 2. 3. 4. 5.
HESS, A., and I.ASSINO, .I. I., dntrt. Itec., 117, 175 (1953). IAmv~s, 11’. I~., Ifull. .Johrw Hopkins Hospital, 49, 17 (1931). I’ALADE, G. I:., J. Sppl. I’hys., 24, 1424 (1953). ~.J. Eq’tl. Med., 95, 28.5 (1052). PAITESHIXMEH, .J. R., HEXKIN, E. II., and UORRERO, L. M., Amer.
J. Physiol.,
Experimentnl
167, 13 (1951).
Cell Research
6
Cell
I
6, 543-545
A SUBMICROSCOPIC
543
(1954)
VESICULAR
CELLS
AND
NERVE
COMPONENT SATELLITE
E. D. P. DE ROBERTIS’ Department
0-f Anatomy,
CELLS1
and H. S. BENNETT of Washington,
Uniwrsity Received
OF SCHWANN
January
Seattle,
Wash.,
U.S.A.
28, 1954
P.uA~J< (3) has recently described a vesicular component in the cndothelial cells of blood capillaries. This component was recognizable in the form of spherical or oval vesicles of globules about 650 p\ in diameter. These vesicles could be seen throughout the cytoplasm of the endothelial cell, but were most abundant in the cytoplasmic region immediately adJacent to the inner and outer capillary cell membranes, where many of them were observed to open into the capillary lumen or into the pericapillary intercellular space. l’alade suggested that these vesicles might bear a relation to capillary permeability. More specifically, he suggested that they might represent a system for transporting fluids across the capillary wall by a process analogous to that of pinocytosis described by Lewis (2). In Lewis’s classical paper and motion picture tlrpicting this process, cells in tissue culture were observed to take in globules of fluid from the surrounding medium, the uptake of fluid being accompanied by vigorous cgtoplasmic motion at the edge of the cell, as if globules were being surrounded and engulfed by clasping folds of cytoplasm. Globules so taken in at the edge of the cell could then be observed by means of the light microscope to be transported as tiny vesicles to other portions of the cell several microns away. Since then pinocytosis has become a familiar phenomenon to observers of a wide variety of living cells in tissue culture or in transparent chambers. l’alade interpreted his electron micrographs as suggesting that a similar process might be occurring in capillary endothclial cells, but involving vesicles of submicroscopic dimensions. The purpose of this note is to confirm Palade’s findings with respect to blood capillaries, to concur in his interpretation, to show that Schwann cells and satellite cells of sympathetic neurones contain a similar vesicular component and to suggest that these cells may likewise transfer materials in an analogous manner. Sympathetic ganglia of the leopard frog (Kann pipiens) and of the bullfrog (Rana caksbiana) and the gracilis muscle of the mouse were fixed in Palade’s (4) buffered ostnic fixative, embedded in methacrylate and sectioned. Thin sections studied in the electron microscope revealed numerous capillaries showing the vesicles described by Palade (3), varying in diameter from X50-650 W (mean of 26 measurements, 520 A). These vesicles can be noted in Fig. 1 (a section from the sympathetic nerve ganglion of Rana pipiens), and in Fig. 4 (from the sympathetic ganglion of Rana catesbiana). 1 This
work
was supported
in part
by grants
the Eli Lilly Company; and the Hiologic&md z Present Montevideo,
address Uruguay.
-~
Department
of Cell
from
the Life
Insurance
Medical
Research
Fund,
Medical Research Fund of the State of Washington: L1ltrastructure,
Instituto
de Ciencias
Experimenlnl
Riol6gicas.
Cell Research
6
544
E. D, P. De Robertis
All figures are electron ganglia of the leopard Key: RUC S
micrographs of buffered osmic fixed sections of portions frog (Figs. 1, 2 and 3) and bullfrog (Figs. 3 and 5).
Cl ~~ capillary lumen; EC - endothelial - red blood cell; SC - satellite cell; sites of stomata or openings of vesicles.
Experimenfrd
and H. S. Bennett
Cell Hesearch
6
of sympathetic
cell; IS ~- intercellular space; N nerve cell body; SchC -- Schwann cell; \’ ~- vesicular component;
Vesicles in Schwann cells
545
The vesicles appear in greatest abundance at the capillary cell surfaces, particularly at the pericapillary surface. Many of the vesicles are oval or elongated, and some can be seen to open through tiny stomata or tubules into the pericapillary space (see X, Figs. 1 and 4). In Fig. 1 the capillary cell just referred to borders on a connective tissue space containing collagen and other connective tissue components. This space is in turn bordered on the left by a satellite cell attendant to a sympathetic ganglion cell, a portion of which occupies the upper left corner of the figure. Vesicles similar to those in the capillary are demonstrated within the cytoplasm of the satellite cell. Vesicles of this nature are likewise to be seen in the portions of satellite cells from the leopard frog shown in Figs. 2 and 3. Here some of the vesicles can be noted piercing the satellite cell wall by small tubules or stamata (at X), and similar vesicles can be seen within the neuronal cytoplasm in Fig. 2. Fig. 5 shows a tangential section through a portion of a Schwann cell from the sympathetic nerve of the bullfrog. A striking array of globules or vesicles is shown, most abundantly at the outer cell surface of the Schwann cell. Measurements of the diameters of 23 vesicles in satellite cells averaged 680 A, and of 30 vesicles in Schwann cells yielded a mean of 510 A. It is possible that these vesicles were encountered in Schwann cells by Hess and Lansing (l), who describe “circles” 300-300 A in diameter in the “neurilemma as it inflects at the node”. They suggest that these “holes” may be “pores or extensions . . . of the neurilcmma or membrane of the cell of Schwann”, and cite indications that such structure may exist elsewhere in the Schwann cells. However, their micrographs as reproduced do not show resolution or contrast sufficient to justify a certain conclusion regarding the identity of these “circles”. We are receptive to Palacle’s suggestion that the capillary vesicles may represent fluid globules in process of transport across the capillary cell, arguing that since uptake and transport by cells of fluid in vesicles of microscopic size is such a familiar and widespread phenomenon, it is altogether reasonable to postulate an ability of cells to move fluid in a similar manner in vacuoles of submicroscopic size. The very close resemblance of the vesicles in the Schwann cells to those in capillaries implies a similar function, and suggests that the Schwann cells and satellite cells may mediate exchange of materials between nerve cell and intercellular space in part by pumping material in tiny vesicles from one surface of the cell to the other, perhaps working the intravesicular contents over in passage, selectively adding to or removing substances along the way. These observations imply that the permeability properties of cellular membranes may be very complex, and are not likely to be described aclccluately by consiclcrations based on assumptions that such membranes function mainly as simple filters characterized by pores of certain sizes, as postulated by l’appcnheimcr (5). REFERENCES 1. 2. 3. 4. 5.
HESS, A., and I.ASSINO, .I. I., dntrt. Itec., 117, 175 (1953). IAmv~s, 11’. I~., Ifull. .Johrw Hopkins Hospital, 49, 17 (1931). I’ALADE, G. I:., J. Sppl. I’hys., 24, 1424 (1953). ~.J. Eq’tl. Med., 95, 28.5 (1052). PAITESHIXMEH, .J. R., HEXKIN, E. II., and UORRERO, L. M., Amer.
J. Physiol.,
Experimentnl
167, 13 (1951).
Cell Research
6