Comprehensive Physiology Wiley Online Library

Ultrastructure of Vascular Smooth Muscle

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Contractile Apparatus
1.1 Filaments
1.2 Dense Bodies and Surface Patches
1.3 Extracellular and Cell‐to‐Cell Connections: Mechanical Coupling
2 Organelles
2.1 Sarcoplasmic Reticulum
2.2 Surface Vesicles
2.3 Golgi Apparatus and Other Intracellular Organelles
3 Cell Junctions: Electrical and Metabolic Coupling
3.1 Structure
3.2 Function
Figure 1. Figure 1.

Transverse (220 nm thick) section of rabbit portal‐anterior mesentric vein. Thick myosin filaments (large arrow) are surrounded by thin actin filaments (double‐headed arrow). Intermediate 10‐nm filaments (small arrows) are associated with dense bodies (DB) or are in bundles (lower left). 200 kV.

From Somlyo et al. 198
Figure 2. Figure 2.

Chicken gizzard myosin molecules.

From Elliott et al. 42
Figure 3. Figure 3.

Stereo pair of electron photomicrographs of 160‐nm thick longitudinal section cut near surface of vascular smooth muscle fiber. When three‐dimensional image is viewed in stereo viewer, a 2.3‐μm long myosin filament (ends marked by arrows) is completely included within the section. Note also, below upper arrow, dense body with associated 10‐nm filaments. Microtubule runs along right side of cell adjacent to surface vesicles. Tannic acid 8% in fixative; lead citrate‐stained section. Tilt ± 10°.

From Ashton, Somlyo, and Somlyo 3
Figure 4. Figure 4.

Stereo pairs of electron photomicrographs of portions of 4 from a series of 8 serial transverse sections 0.47 μm thick from rabbit portal‐anterior mesenteric veins. Thick filaments present in sections 1 labeled A–G. Group of thick filaments, labeled 1–9, starts in sections 2 and 3. Filaments complete in set of 8 sections, ending in sections 6 and 7. Dense body (II) found in sections 1 and 2. Actin filaments seen in subsequent sections in regions continuous with dense body II. Another dense body (III) continuous throughout 8 sections. Note, particularly in section 4, that, due to oblique orientation, the view on right gives appearance of short ribbons. Profile of filament D becomes very small in section 4 and is absent in subsequent section (not shown), showing taper of myosin filaments. Not stained with lead. View on left, tilt + 15°; view on right, tilt + 5°.

From Ashton, Somlyo, and Somlyo 3
Figure 5. Figure 5.

Six consecutive single (not stereo) serial 140‐nm thick transverse sections of vascular smooth muscle demonstrating tapering of ends of myosin filaments. Three filaments (B, C, D) appear in sections 2 and 3, and another, A, ends in section 5. Fifth filament, E, appears in section 5. Whereas shanks appear to be up to 20 nm wide (slightly obliquely running filaments presenting oversize profiles), ends taper down to approximately 12 nm (C and D) or smaller (B in section 2; A in section 5). Surface dense body (DB) is seen at top of each section. Tannic acid in fixative, 2%; sections stained with lead citrate.

From Ashton, Somlyo, and Somlyo 3
Figure 6. Figure 6.

Stereo electron photomicrograph of 100‐nm thick transverse section showing a thick filament surrounded by 12 thin filaments. When viewed in stereo 3 cross‐bridges in region of arrow occur at different levels and run between thick and thin filaments. There is suggestion of other cross‐bridges lying close to thick filament. Tannic acid 2% in glutaraldehyde. Section stained with aqueous uranyl acetate and lead citrate. 0°, −7°. 200 kV.

From Ashton, Somlyo, and Somlyo 3
Figure 7. Figure 7.

Tracing of smooth muscle cell from one transverse 0.47‐μm section from series where thick filaments were followed through 8 consecutive sections. Tracing shows only filaments that begin or end in this section. X, filament first appears; O, filament terminates. Note that filaments tend to appear or terminate in small groups. Shaded areas and dots represent, respectively, dense bodies and 10‐nm filaments.

From Ashton, Somlyo, and Somlyo 3
Figure 8. Figure 8.

gTransverse section of portion of smooth muscle cell from rabbit portal–anterior mesenteric vein. Muscle was fixed in 2% glutaraldehyde for 30 min, frozen in supercooled Freon 22, sectioned at −110°C, picked up from dry knife onto a drop of frozen sucrose solution, allowed to melt, and negatively stained with 3% ammonium molybdate. This technique excludes effects of osmium and dehydration. Rosettes of thick filaments surrounded by thin filaments are present, as well as a few 10‐nm intermediate filaments, large arrows.

A. V. Somlyo and F. T. Ashton, unpublished observations
Figure 9. Figure 9.

Three stereo pairs of electron photomicrographs of transverse sections of dense bodies from vascular smooth muscle cells, demonstrating association of actin with dense bodies. A and B, dense bodies with some substructure and amorphous material surrounded by 10‐nm filaments. When viewed in stereo, profiles approximately size of actin filaments are visible (small arrows). Sections 100 nm thick stained with aqueous uranyl acetate and lead citrate. Tilt ± 4°. C, dense body is shown with latticelike structure whose spacing is similar to that of actin filaments. Actin size profiles are visible (small arrow), as well as 10‐nm filaments (double arrow). Section 100 nm thick stained with lead citrate. Tilt ± 3.5°.

From Ashton, Somlyo, and Somlyo 3
Figure 10. Figure 10.

Photomicrograph of 80‐nm thick longitudinal section of 2 smooth muscle cells showing actin filaments (arrows) passing over surface vesicles and attaching to surface dense body (DB). Section stained with lead citrate.

From Ashton, Somlyo, and Somlyo 3
Figure 11. Figure 11.

Transverse section of part of smooth muscle cell from rabbit main pulmonary artery. Four portions of sarcoplasmic reticulum (SR) approach surface membrane associated with surface vesicles (SV). Dense bodies (DB) alternate with peripheral SR and SV. Some microtubules (arrows) are also present. M, mitochondrion.

From Somlyo and Somlyo 197
Figure 12. Figure 12.

Freeze‐fracture photo of several smooth muscle cells from small mesenteric artery of guinea pig, showing general longitudinal orientation of rows of surface vesicles (arrows). Typical planes of fracture through cell membrane are shown revealing P faces (with cytoplasm beneath membrane as viewed) and E faces (with extracellular space beneath membrane as viewed). Openings of surface vesicles can be seen as depressions on P face; whereas broken‐off necks of surface vesicles are present on E face. Fractured collagen fibrils (C) are present between smooth muscle cells. Unetched.

From Devine and Rayns 34
Figure 13. Figure 13.

a, Stereo pair of electron photomicrographs of 50‐nm thick longitudinal section of vascular smooth muscle cell showing actin filaments actually entering dense bodies rather than coursing above or beneath them. This point can only be observed when viewed in stereo. Thin filaments attach to 2 lower portions of dense bodies (DB), and there are several prominent intermediate filaments (arrows) around upper portions. b, Lighter print of lower portion of a. Arrowheads indicate points where parallax measurements were made: when viewed in stereo arrowheads to left indicate thickness of section; those to upper right indicate top and bottom of dense body; lower arrowheads show that the 2 thin filaments measured run into rather than above or below the dense body. Tannic acid 2% in glutaraldehyde. Section stained with 5% uranyl acetate in absolute ethanol and lead citrate. Stereo angle ± 20°; 150 kV.

From Ashton, Somlyo, and Somlyo 3
Figure 14. Figure 14.

Portions of 2 smooth muscle cells from chicken gizzard incubated before embedding in Epon‐Araldite with anti‐α‐actinin followed by sheep anti‐rabbit IgG conjugated with peroxidase (indirect method). Dark reaction product is located both at periphery of cell (double arrow), corresponding to surface dense bodies and within cytoplasm (single arrow), in regions of dense bodies, ecs, Extracellular space. This section counterstained with lead citrate.

From Schollmeyer et al. 176
Figure 15. Figure 15.

Transverse section from rabbit main pulmonary artery showing smooth muscle cells between elastic lamellae (el) and collagen (col). Note many cell processes and cell contacts (arrows) within lamellae but not across lamellae. Connective tissue staining is greatly enhanced by 2% tannic acid.

Figure 16. Figure 16.

Longitudinal section from rabbit mesotubarium stretched twice rest length in both directions. Cell‐to‐cell attachments (large arrows) and elastin microfibrils (ef, small arrows) appear to connect smooth muscle cells (see lower 2 cells). col, Collagen. Note prominent staining of basement membrane (bm) and connective tissue due to use of 2% tannic acid following fixation.

Figure 17. Figure 17.

Transverse section of a bundle of smooth muscle fibers of rabbit portal‐anterior mesenteric vein, illustrating regular spacing of thick filaments (large arrows) and the relatively large number of thin myofilaments (small arrows). Several groups of intermediate filaments (some shown by double arrows) associated with dense bodies are present. Elements of sarcoplasmic reticulum (SR), arrow‐heads, occur at periphery of cells. Smooth SR continuous with rough endoplasmic reticulum can be seen in cell in upper left quadrant.

From Somlyo et al. 194
Figure 18. Figure 18.

Transverse sections through peripheral portions of portal‐anterior mesenteric vein smooth muscle cells incubated for 90 min in Krebs solution containing ferritin. Ferritin is in extracellular space (ecs) and in the surface vesicles (v). No ferritin is in sarcoplasmic reticulum (SR), arrows, that lies between surface vesicles. m, Mitochondrion. Not lead stained.

From Somlyo and Somlyo 197
Figure 19. Figure 19.

Transverse sections through peripheral portions of portal‐anterior mesenteric vein smooth muscle cells incubated for 90 min in Krebs solution containing ferritin. Ferritin is in extracellular space (ecs) and in the surface vesicles (v). No ferritin is in sarcoplasmic reticulum (SR), arrows, that lies between surface vesicles. m, Mitochondrion. Not lead stained.

From Somlyo and Somlyo 197
Figure 20. Figure 20.

Section through portal‐anterior mesenteric vein smooth muscle fibers that were exposed to extracellular marker colloidal lanthanum during osmium fixation, after primary fixation with glutaraldehyde. Some lanthanum deposits are in free‐floating vesicles (arrows) not visibly connected to cell membrane; connections are out of plane of section. Sarcoplasmic reticulum does not contain lanthanum and is therefore not in direct communication with extracellular space.

From Somlyo and Somlyo 197
Figure 21. Figure 21.

Longitudinal sections showing couplings of sarcoplasmic reticulum (SR) with surface membrane. Dense periodic structures (bars) are present across 15–20‐nm junctional gap between SR and the plasma membrane. Tannic acid 2% post osmium; microtubule (arrow).

Figure 22. Figure 22.

Longitudinal sections showing couplings of sarcoplasmic reticulum (SR) with surface membrane. Dense periodic structures (bars) are present across 15–20‐nm junctional gap between SR and the plasma membrane. Tannic acid 2% post osmium; microtubule (arrow).

Figure 23. Figure 23.

High‐magnification view of longitudinal section of portal–anterior mesenteric vein, illustrating surface vesicle (SV) and sarcoplasmic reticulum (SR) relationship. SR forms fenestrated network running between and sometimes encircling (arrows) surface vesicles.

From Somlyo and Somlyo 197
Figure 24. Figure 24.

Transversely sectioned main pulmonary artery smooth muscle cell with elements of central and peripheral sarcoplasmic reticulum (SR), arrows. Compare more extensive SR in this artery with that of portal vein (Fig. 17). el, Elastin; col, collagen.

Figure 25. Figure 25.

Section through portion of smooth muscle cell surface membrane from vena cava of the diamondback turtle, showing several striated vesicles. In some longitudinally sectioned vesicles the striations extend completely across vesicle (arrows). ecs, Extracellular space.

From Somlyo et al. 193
Figure 26. Figure 26.

Longitudinal section of vascular smooth muscle showing flattened sacs and vesicles of normal Golgi apparatus (G). Rabbit main pulmonary artery incubated for 30 min in normal Krebs solution.

From Somlyo et al. 195
Figure 27. Figure 27.

Longitudinal section of vascular smooth muscle, showing marked swelling of Golgi system. Vacuolation is at nuclear pole. Rabbit main pulmonary artery incubated for 30 min in X537A, 5 μg/ml.

From Somlyo et al. 195
Figure 28. Figure 28.

Gap junction between 2 smooth muscle cells from rabbit portal‐anterior mesenteric vein. Gap is stained, giving rise to pentalayered structure. Note cytoplasmic densities in region of gap junction. Tannic acid 2% post osmium. Section stained with lead citrate.

Figure 29. Figure 29.

Gap junction between 2 longitudinally oriented portal‐anterior mesenteric vein smooth muscle cells. Long regions of cell membranes are closely apposed and form a gap junction in one region (arrow). Tannic acid 2% post osmium. Section stained with lead citrate.

Figure 30. Figure 30.

Model of vertebrate gap junction. A, cross‐sectional profile. B, profile after lanthanum staining (section). C, face view after lanthanum staining (section). D, freeze fracture. Junction is fractured in steps. E, diagram of path followed by fracture plane.

From Peracchia 148
Figure 31. Figure 31.

Interendothelial cleft (arrowhead) from rabbit main pulmonary artery. Tannic acid reacted with osmium has acted as extracellular marker and has penetrated surface vesicles, but has not permeated tight junction (inset, arrow). Both tight junctions and gap junctions (not shown) are found between neighboring endothelial cell membranes 91,184,185. sm.m., Smooth muscle; end., endothelial cell; e.c.s., extracellular space; el, elastin.



Figure 1.

Transverse (220 nm thick) section of rabbit portal‐anterior mesentric vein. Thick myosin filaments (large arrow) are surrounded by thin actin filaments (double‐headed arrow). Intermediate 10‐nm filaments (small arrows) are associated with dense bodies (DB) or are in bundles (lower left). 200 kV.

From Somlyo et al. 198


Figure 2.

Chicken gizzard myosin molecules.

From Elliott et al. 42


Figure 3.

Stereo pair of electron photomicrographs of 160‐nm thick longitudinal section cut near surface of vascular smooth muscle fiber. When three‐dimensional image is viewed in stereo viewer, a 2.3‐μm long myosin filament (ends marked by arrows) is completely included within the section. Note also, below upper arrow, dense body with associated 10‐nm filaments. Microtubule runs along right side of cell adjacent to surface vesicles. Tannic acid 8% in fixative; lead citrate‐stained section. Tilt ± 10°.

From Ashton, Somlyo, and Somlyo 3


Figure 4.

Stereo pairs of electron photomicrographs of portions of 4 from a series of 8 serial transverse sections 0.47 μm thick from rabbit portal‐anterior mesenteric veins. Thick filaments present in sections 1 labeled A–G. Group of thick filaments, labeled 1–9, starts in sections 2 and 3. Filaments complete in set of 8 sections, ending in sections 6 and 7. Dense body (II) found in sections 1 and 2. Actin filaments seen in subsequent sections in regions continuous with dense body II. Another dense body (III) continuous throughout 8 sections. Note, particularly in section 4, that, due to oblique orientation, the view on right gives appearance of short ribbons. Profile of filament D becomes very small in section 4 and is absent in subsequent section (not shown), showing taper of myosin filaments. Not stained with lead. View on left, tilt + 15°; view on right, tilt + 5°.

From Ashton, Somlyo, and Somlyo 3


Figure 5.

Six consecutive single (not stereo) serial 140‐nm thick transverse sections of vascular smooth muscle demonstrating tapering of ends of myosin filaments. Three filaments (B, C, D) appear in sections 2 and 3, and another, A, ends in section 5. Fifth filament, E, appears in section 5. Whereas shanks appear to be up to 20 nm wide (slightly obliquely running filaments presenting oversize profiles), ends taper down to approximately 12 nm (C and D) or smaller (B in section 2; A in section 5). Surface dense body (DB) is seen at top of each section. Tannic acid in fixative, 2%; sections stained with lead citrate.

From Ashton, Somlyo, and Somlyo 3


Figure 6.

Stereo electron photomicrograph of 100‐nm thick transverse section showing a thick filament surrounded by 12 thin filaments. When viewed in stereo 3 cross‐bridges in region of arrow occur at different levels and run between thick and thin filaments. There is suggestion of other cross‐bridges lying close to thick filament. Tannic acid 2% in glutaraldehyde. Section stained with aqueous uranyl acetate and lead citrate. 0°, −7°. 200 kV.

From Ashton, Somlyo, and Somlyo 3


Figure 7.

Tracing of smooth muscle cell from one transverse 0.47‐μm section from series where thick filaments were followed through 8 consecutive sections. Tracing shows only filaments that begin or end in this section. X, filament first appears; O, filament terminates. Note that filaments tend to appear or terminate in small groups. Shaded areas and dots represent, respectively, dense bodies and 10‐nm filaments.

From Ashton, Somlyo, and Somlyo 3


Figure 8.

gTransverse section of portion of smooth muscle cell from rabbit portal–anterior mesenteric vein. Muscle was fixed in 2% glutaraldehyde for 30 min, frozen in supercooled Freon 22, sectioned at −110°C, picked up from dry knife onto a drop of frozen sucrose solution, allowed to melt, and negatively stained with 3% ammonium molybdate. This technique excludes effects of osmium and dehydration. Rosettes of thick filaments surrounded by thin filaments are present, as well as a few 10‐nm intermediate filaments, large arrows.

A. V. Somlyo and F. T. Ashton, unpublished observations


Figure 9.

Three stereo pairs of electron photomicrographs of transverse sections of dense bodies from vascular smooth muscle cells, demonstrating association of actin with dense bodies. A and B, dense bodies with some substructure and amorphous material surrounded by 10‐nm filaments. When viewed in stereo, profiles approximately size of actin filaments are visible (small arrows). Sections 100 nm thick stained with aqueous uranyl acetate and lead citrate. Tilt ± 4°. C, dense body is shown with latticelike structure whose spacing is similar to that of actin filaments. Actin size profiles are visible (small arrow), as well as 10‐nm filaments (double arrow). Section 100 nm thick stained with lead citrate. Tilt ± 3.5°.

From Ashton, Somlyo, and Somlyo 3


Figure 10.

Photomicrograph of 80‐nm thick longitudinal section of 2 smooth muscle cells showing actin filaments (arrows) passing over surface vesicles and attaching to surface dense body (DB). Section stained with lead citrate.

From Ashton, Somlyo, and Somlyo 3


Figure 11.

Transverse section of part of smooth muscle cell from rabbit main pulmonary artery. Four portions of sarcoplasmic reticulum (SR) approach surface membrane associated with surface vesicles (SV). Dense bodies (DB) alternate with peripheral SR and SV. Some microtubules (arrows) are also present. M, mitochondrion.

From Somlyo and Somlyo 197


Figure 12.

Freeze‐fracture photo of several smooth muscle cells from small mesenteric artery of guinea pig, showing general longitudinal orientation of rows of surface vesicles (arrows). Typical planes of fracture through cell membrane are shown revealing P faces (with cytoplasm beneath membrane as viewed) and E faces (with extracellular space beneath membrane as viewed). Openings of surface vesicles can be seen as depressions on P face; whereas broken‐off necks of surface vesicles are present on E face. Fractured collagen fibrils (C) are present between smooth muscle cells. Unetched.

From Devine and Rayns 34


Figure 13.

a, Stereo pair of electron photomicrographs of 50‐nm thick longitudinal section of vascular smooth muscle cell showing actin filaments actually entering dense bodies rather than coursing above or beneath them. This point can only be observed when viewed in stereo. Thin filaments attach to 2 lower portions of dense bodies (DB), and there are several prominent intermediate filaments (arrows) around upper portions. b, Lighter print of lower portion of a. Arrowheads indicate points where parallax measurements were made: when viewed in stereo arrowheads to left indicate thickness of section; those to upper right indicate top and bottom of dense body; lower arrowheads show that the 2 thin filaments measured run into rather than above or below the dense body. Tannic acid 2% in glutaraldehyde. Section stained with 5% uranyl acetate in absolute ethanol and lead citrate. Stereo angle ± 20°; 150 kV.

From Ashton, Somlyo, and Somlyo 3


Figure 14.

Portions of 2 smooth muscle cells from chicken gizzard incubated before embedding in Epon‐Araldite with anti‐α‐actinin followed by sheep anti‐rabbit IgG conjugated with peroxidase (indirect method). Dark reaction product is located both at periphery of cell (double arrow), corresponding to surface dense bodies and within cytoplasm (single arrow), in regions of dense bodies, ecs, Extracellular space. This section counterstained with lead citrate.

From Schollmeyer et al. 176


Figure 15.

Transverse section from rabbit main pulmonary artery showing smooth muscle cells between elastic lamellae (el) and collagen (col). Note many cell processes and cell contacts (arrows) within lamellae but not across lamellae. Connective tissue staining is greatly enhanced by 2% tannic acid.



Figure 16.

Longitudinal section from rabbit mesotubarium stretched twice rest length in both directions. Cell‐to‐cell attachments (large arrows) and elastin microfibrils (ef, small arrows) appear to connect smooth muscle cells (see lower 2 cells). col, Collagen. Note prominent staining of basement membrane (bm) and connective tissue due to use of 2% tannic acid following fixation.



Figure 17.

Transverse section of a bundle of smooth muscle fibers of rabbit portal‐anterior mesenteric vein, illustrating regular spacing of thick filaments (large arrows) and the relatively large number of thin myofilaments (small arrows). Several groups of intermediate filaments (some shown by double arrows) associated with dense bodies are present. Elements of sarcoplasmic reticulum (SR), arrow‐heads, occur at periphery of cells. Smooth SR continuous with rough endoplasmic reticulum can be seen in cell in upper left quadrant.

From Somlyo et al. 194


Figure 18.

Transverse sections through peripheral portions of portal‐anterior mesenteric vein smooth muscle cells incubated for 90 min in Krebs solution containing ferritin. Ferritin is in extracellular space (ecs) and in the surface vesicles (v). No ferritin is in sarcoplasmic reticulum (SR), arrows, that lies between surface vesicles. m, Mitochondrion. Not lead stained.

From Somlyo and Somlyo 197


Figure 19.

Transverse sections through peripheral portions of portal‐anterior mesenteric vein smooth muscle cells incubated for 90 min in Krebs solution containing ferritin. Ferritin is in extracellular space (ecs) and in the surface vesicles (v). No ferritin is in sarcoplasmic reticulum (SR), arrows, that lies between surface vesicles. m, Mitochondrion. Not lead stained.

From Somlyo and Somlyo 197


Figure 20.

Section through portal‐anterior mesenteric vein smooth muscle fibers that were exposed to extracellular marker colloidal lanthanum during osmium fixation, after primary fixation with glutaraldehyde. Some lanthanum deposits are in free‐floating vesicles (arrows) not visibly connected to cell membrane; connections are out of plane of section. Sarcoplasmic reticulum does not contain lanthanum and is therefore not in direct communication with extracellular space.

From Somlyo and Somlyo 197


Figure 21.

Longitudinal sections showing couplings of sarcoplasmic reticulum (SR) with surface membrane. Dense periodic structures (bars) are present across 15–20‐nm junctional gap between SR and the plasma membrane. Tannic acid 2% post osmium; microtubule (arrow).



Figure 22.

Longitudinal sections showing couplings of sarcoplasmic reticulum (SR) with surface membrane. Dense periodic structures (bars) are present across 15–20‐nm junctional gap between SR and the plasma membrane. Tannic acid 2% post osmium; microtubule (arrow).



Figure 23.

High‐magnification view of longitudinal section of portal–anterior mesenteric vein, illustrating surface vesicle (SV) and sarcoplasmic reticulum (SR) relationship. SR forms fenestrated network running between and sometimes encircling (arrows) surface vesicles.

From Somlyo and Somlyo 197


Figure 24.

Transversely sectioned main pulmonary artery smooth muscle cell with elements of central and peripheral sarcoplasmic reticulum (SR), arrows. Compare more extensive SR in this artery with that of portal vein (Fig. 17). el, Elastin; col, collagen.



Figure 25.

Section through portion of smooth muscle cell surface membrane from vena cava of the diamondback turtle, showing several striated vesicles. In some longitudinally sectioned vesicles the striations extend completely across vesicle (arrows). ecs, Extracellular space.

From Somlyo et al. 193


Figure 26.

Longitudinal section of vascular smooth muscle showing flattened sacs and vesicles of normal Golgi apparatus (G). Rabbit main pulmonary artery incubated for 30 min in normal Krebs solution.

From Somlyo et al. 195


Figure 27.

Longitudinal section of vascular smooth muscle, showing marked swelling of Golgi system. Vacuolation is at nuclear pole. Rabbit main pulmonary artery incubated for 30 min in X537A, 5 μg/ml.

From Somlyo et al. 195


Figure 28.

Gap junction between 2 smooth muscle cells from rabbit portal‐anterior mesenteric vein. Gap is stained, giving rise to pentalayered structure. Note cytoplasmic densities in region of gap junction. Tannic acid 2% post osmium. Section stained with lead citrate.



Figure 29.

Gap junction between 2 longitudinally oriented portal‐anterior mesenteric vein smooth muscle cells. Long regions of cell membranes are closely apposed and form a gap junction in one region (arrow). Tannic acid 2% post osmium. Section stained with lead citrate.



Figure 30.

Model of vertebrate gap junction. A, cross‐sectional profile. B, profile after lanthanum staining (section). C, face view after lanthanum staining (section). D, freeze fracture. Junction is fractured in steps. E, diagram of path followed by fracture plane.

From Peracchia 148


Figure 31.

Interendothelial cleft (arrowhead) from rabbit main pulmonary artery. Tannic acid reacted with osmium has acted as extracellular marker and has penetrated surface vesicles, but has not permeated tight junction (inset, arrow). Both tight junctions and gap junctions (not shown) are found between neighboring endothelial cell membranes 91,184,185. sm.m., Smooth muscle; end., endothelial cell; e.c.s., extracellular space; el, elastin.

References
 1. Albertini, D. F., D. W. Fawcett, and P. J. Olds. Morphological variations in gap junctions of ovarian granulosa cells. Tissue Cell 7: 389–405, 1975.
 2. Asada, Y., and M. V. L. Bennett. Experimental alteration of coupling resistance at an electrotonic synapse. J. Cell Biol. 49: 159–172, 1971.
 3. Ashton, F. T., A. V. Somlyo, and A. P. Somlyo. The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy. J. Mol. Biol. 98: 17–29, 1975.
 4. Barany, M., K. Barany, E. Gaetijens, and G. Balin. Chicken gizzard myosin. Arch. Biochem. Biophys. 113: 205–222, 1966.
 5. Bardele, C. F. Structure, biochemistry and function of microtubules. Cytobiologie 7: 442–488, 1973.
 6. Barr, L., and M. M. Dewey. Electrotonus and electrical transmission in smooth muscle. In: Handbook of Physiology. Alimentary Canal, edited by C. F. Code. Washington, D.C.: Am. Physiol. Soc., 1968, sect. 6, vol. IV, chapt. 85, p. 1733–1742.
 7. Behrendt, H. Effect of anabolic steroids on rat heart muscle cells. I. Intermediate filaments. Cell Tissue Res. 180: 303–315, 1977.
 8. Bennett, G. S., J. M. Croop, J. J. Otto, S. A. Fellini, Y. Toyama, and H. Holtzer. Observations on intermediate sized or 100 Å filaments. In: John M. Marshall Symposium on Cell Biology, edited by F. Pepe, J. W. Sanger, and V. T. Nachmias. New York: Academic, 1979.
 9. Bennett, G. S., S. A. Fellini, J. M. Croop, J. J. Otto, J. Bryan, and H. Holtzer. Differences among 100 Å filament subunits from different cell types. Proc. Natl. Acad. Sci. US 75: 4364–4368, 1978.
 10. Bennett, M. V. L. Function of electrotonic junctions in embryonic and adult tissues. Federation Proc. 32: 65–75, 1973.
 11. Bennett, M. V. L., and A. A. Auerbach. Calculation of electrically coupling of cells separated by a gap. Anat. Record 163: 152, 1969.
 12. Bergman, R. Uterine smooth muscle fibers in castrate and estrogen‐treated rats. J. Cell Biol. 36: 639–648, 1968.
 13. Blobel, G. Synthesis and segregation of secretory proteins: the signal hypothesis. In: International Cell Biology, edited by B. R. Brinkley and K. R. Porter. New York: Rockefeller Univ. Press, 1976, p. 318–325.
 14. Blose, S. H., M. L. Shelanski, and S. Chacko. Localization of bovine brain filament antibody on intermediate (100Å) filaments in guinea pig vascular endothelial cells and chick cardiac muscle cells. Proc. Natl. Acad. Sci. US 74: 662–665, 1977.
 15. Bo, W. J., D. L. Odor, and M. Rothrock. The fine structure of uterine smooth muscle of the rat uterus at various time intervals following a single injection of estrogen. Am. J. Anat. 123: 369–384, 1968.
 16. Bremel, R. D., and A. Weber. Cooperative behavior within the functional unit of the actin filament in vertebrate striated muscle. Nature 238: 97, 1972.
 17. Brightman, M. W., and T. S. Reese. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40: 648–677, 1969.
 18. Bullard, B., and G. M. Sainsbury. The proteins in the Z line of insect flight muscle. Biochem. J. 161: 399–403, 1977.
 19. Bussow, H., and U. Wulfhekel. Ultrastructure of smooth muscle cells in muscle arteries of birds. Z. Zellforsch. Mikroskop. Anat. 125: 339–352, 1972.
 20. Campbell, G. R., and J. H. Chamley. Thick filaments in vertebrate smooth muscle. Cell Tissue Res. 156: 201–216, 1975.
 21. Campbell, G. R., Y. Uehara, G. Mark, and G. Burnstock. Fine structure of smooth muscle cells grown in tissue culture. J. Cell Biol. 49: 21–34, 1971.
 22. Chamley, J. H., V. Gröschel‐Stewart, G. R. Campbell, and G. Burnstock. Distinction between smooth muscle, fibroblasts and endothelial cells in culture by use of fluoresceinated antibodies against smooth muscle actin. Cell Tissue Res. 177: 445–457, 1977.
 23. Cobb, J. L. S., and T. Bennett. A study of nexuses in visceral smooth muscle. J. Cell Biol. 41: 287–297, 1969.
 24. Cooke, P. H. Filamentous aggregates of purified myosin from smooth muscle. Cytobiologie 11: 346–357, 1975.
 25. Cooke, P. H. A filamentous cytoskeleton in vertebrate smooth muscle fibers. J. Cell Biol. 68: 539–556, 1976.
 26. Cooke, P. H., and R. H. Chase. Potassium chloride insoluble myofilaments in vertebrate smooth muscle cells. Exptl. Cell Res. 66: 417–425, 1971.
 27. Cooke, P. H., and F. Fay. Correlation between fiber length, ultrastructure, and the length‐tension relationship of mammalian smooth muscle. J. Cell Biol. 52: 105–116, 1972.
 28. Craig, R., and J. Megerman. Assembly of smooth muscle myosin into side‐polar filaments. J. Cell Biol. 75: 990–996, 1977.
 29. Daniel, E. E., V. P. Saniel, G. Duchon, R. E. Garfield, M. Nichols, S. K. Malhotra, and M. Oki. Is the nexus necessary for cell‐to‐cell coupling of smooth muscle? J. Membrane Biol. 28: 207–239, 1976.
 30. Davies, P., P. Bechtel, and I. Pastan. Filamin inhibits actin activation of heavy meromyosin ATPase. FEBS Letters 77: 228–232, 1977.
 31. Davison, P. F., B. S. Hong, and P. Cooke. Classes of distinguishable 10 nm cytoplasmic filaments. Exptl. Cell Res. 109: 471–474, 1977.
 32. DeMello, W. C. Effect of intracellular injection of calcium and strontium on cell communication in heart. J. Physiol. London 250: 231–245, 1975.
 33. DeMello, W. C. Uncoupling of heart cells produced by intracellular sodium injection. Experientia 31: 460–461, 1975.
 34. Devine, C. E., and D. G. Rayns. Freeze fracture studies of membrane systems in vertebrate muscle. II. Smooth muscle. J. Ultrastruct. Res. 51: 293–306, 1975.
 35. Devine, C. E., F. O. Simpson, and W. S. Bertad. Surface feature of smooth muscle cells from the mesenteric artery and vas deferens. J. Cell Sci. 8: 427–443, 1971.
 36. Devine, C. E., and A. P. Somlyo. Thick filaments in vascular smooth muscle. J. Cell Biol. 49: 636–649, 1971.
 37. Devine, C. E., A. V. Somlyo, and A. P. Somlyo. Sarcoplasmic reticulum and excitation‐contraction coupling in mammalian smooth muscle. J. Cell Biol. 52: 690–718, 1972.
 38. Devine, C. E., A. V. Somlyo, and A. P. Somlyo. Sarcoplasmic reticulum and mitochondria as cation accumulating sites in smooth muscle. Phil. Trans. Roy. Soc. London Ser. B 265: 17–23, 1973.
 39. Dewey, M. M., and L. Barr. Intracellular connection between smooth muscle cells: the nexus. Science 137: 670, 1962.
 40. Driska, S. P., and R. A. Murphy. An estimate of cellular force generation in an arterial smooth muscle with a high actin: myosin ratio. Blood Vessels 15: 26–32, 1978.
 41. Dulhunty, A. F., and C. Franzini‐Armstrong. The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibers at different sarcomere lengths. J. Physiol. London 250: 513–539, 1975.
 42. Ebashi, S., H. Iwakura, H. Nakajima, R. Nakamura, and Y. Ooi. New structural proteins from dog heart and chicken gizzard. Biochem. Z. 345: 201–211, 1966.
 43. Ebashi, S., T. Mikawa, M. Hirata, and Y. Nonomura. The regulatory role of calcium in muscle. Ann. NY Acad. Sci. 307: 451–461, 1978.
 44. Elliott, A., G. Offer, and K. Burridge. Electron microscopy of myosin molecules from muscle and non‐muscle sources. Proc. Roy. Soc. London Ser. B 193: 45–53, 1976.
 45. Elliot, G. F., and J. Lowy. Organization of actin in a mammalian smooth muscle. Nature 219: 156–157, 1968.
 46. Elzinga, M., and J. H. Collins. The amino acid sequence of rabbit skeletal muscle actin. Cold Spring Harbor Symp. Quant. Biol. 37: 1–8, 1972.
 47. Epstein, M. L., and N. B. Gilula. A study of communications specificity between cells in culture. J. Cell Biol. 75: 769–787, 1977.
 48. Evans, D. H. L., and E. M. Evans. The membrane relationships of smooth muscles: an electron microscopic study. J. Anat. 98: 37–46, 1964.
 49. Farquhar, M. G., and G. E. Palade. Junctional complexes in various epithelia. J. Cell Biol. 17: 375–412, 1963.
 50. Fawcett, D. W., and N. S. McNutt. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42: 1–45, 1969.
 51. Fay, F. S. Isometric contractile properties of single isolated smooth muscle cells. Nature 265: 553–556, 1977.
 52. Fay, F. S., and C. M. Delise. Contraction of isolated smooth‐muscle cells—structural changes. Proc. Natl. Acad. Sci. US 70: 641–645, 1973.
 53. Ferrans, V. J., and W. C. Roberts. Intermyofibrillar and nucleomyofibrillar connections in human and canine myocardium. An ultrastructural study. J. Mol. Cellular Cardiol. 5: 247–257, 1973.
 54. Fisher, B. A., and R. M. Bagby. Reorientation of myofilaments during contraction of a vertebrate smooth muscle. Am. J. Physiol. 232: C5–C14, 1977 or
 55. Am. J. Physiol.: Cell Physiol. 1: C5–C14, 1977.
 56. Franzini‐Armstrong, C. Studies of the triad. I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47: 488–499, 1970.
 57. Franzini‐Armstrong, C., and A. F. Dulhunty. The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J. Physiol. London 250: 513–539, 1975.
 58. Fry, G. N., C. E. Devine, and G. Burnstock. Freeze‐fracture studies of nexuses between smooth muscle cells. Close relationship to sarcoplasmic reticulum. J. Cell Biol. 72: 26–34, 1977.
 59. Gabella, G. Intercellular junctions between circular and longitudinal intestinal muscle layers. Z. Zellforsch. Mikroskop. Anat. 125: 191–199, 1972.
 60. Gabella, G. Cellular structures and electrophysiological behavior. Fine structure of smooth muscle. Phil. Trans. Roy. Soc. London Ser. B 265: 7–16, 1973.
 61. Gabella, G. Structural changes in smooth muscle cells during isotonic contraction. Cell Tissue Res. 170: 187–201, 1976.
 62. Gabella, G. The force generated by a visceral smooth muscle. J. Physiol. London 263: 199–213, 1976.
 63. Gabella, G., and D. Blundell. Effect of stretch and contraction on caveolae of smooth muscle cells. Cell Tissue Res. 190: 255–271, 1978.
 64. Gabella, G., and L. Raeymaekers. Effect of collagenase on mechanical activity and fine structure of an intestinal smooth muscle. Cell Tissue Res. 173: 29–44, 1976.
 65. Garfield, R. E., S. Chacko, and S. Blose. Phagocytosis by muscle cells. Lab. Invest. 33: 418–427, 1975.
 66. Garfield, R. E., and E. E. Daniel. Relation of membrane vesicles to volume control and Na+ transport in smooth muscle: effect of metabolic and transport inhibition on fresh tissues. J. Mechanochemistry Cell Motility 4: 113–155, 1977.
 67. Garfield, R. E., S. Sims, and E. E. Daniel. Gap junctions: their presence and necessity in myometrium during parturition. Science 198: 958–959, 1977.
 68. Garfield, R. E., and A. P. Somlyo. Golgi apparatus and lectin‐binding sites: effects of lasalocid (X537A). Exptl. Cell Res. 109: 163–179, 1977.
 69. Geisweid, G., and G. Wermbter. The fine structure of the nexus between smooth muscle cells of the taenia coli in freezeetched replicas. Cytobiologie 9: 121–130, 1974.
 70. Gillis, J. M., and E. J. O'Brien. The effect of calcium ions on the structure of reconstituted muscle thin filaments. J. Mol. Biol. 99: 445–459, 1975.
 71. Gilula, N. B. Gap junctions and cell communication. In: International Cell Biology, edited by B. R. Brinkley and K. R. Porter. New York: Rockefeller Univ. Press, 1976, p. 61–69.
 72. Gilula, N. B., O. R. Reeves, and A. Steinbach. Metabolic coupling, ionic coupling and cell contacts. Nature 235: 262–265, 1972.
 73. Gilula, N. B., and P. Satir. Septate and gap junctions in molluscan gill epithelium. J. Cell Biol. 51: 869–872, 1971.
 74. Goldman, R., T. Pollard, and J. Rosenbaum In: Cell Motility, Microtubules and Related Proteins, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spr. Harbor Labs., 1976, vol. 3, book C. (Cold Spr. Harbor Conf. Cell Proliferation.)
 75. Goodenough, D. A., and W. Stoeckenius. The isolation of mouse hepatocyte gap junctions. Preliminary chemical characterization and x‐ray diffraction. J. Cell Biol. 54: 646–656, 1972.
 76. Goodford, P. J. The distribution and exchange of electrolytes in intestinal smooth muscle. In: Handbook of Physiology. Alimentary Canal, edited by C. F. Code. Washington, DC: Am. Physiol. Soc., 1968, sect. 6, vol. IV, chapt. 86, p. 1743–1766.
 77. Goodford, P. J., and M. W. Wolowyk. Localization of cation interactions in the smooth muscle of the guinea pig taenia coli. J. Physiol. London 224: 521–535, 1972.
 78. Hamoir, G. Biochemistry of the myometrium. In: Biology of the Uterus, edited by R. M. Wynn. New York: Plenum, 1977, p. 377–421.
 79. Hanak, H., and P. Böck. Die Feinstruktur der Muskel‐Sehnenverbindung von Skelett‐und Herzmuskel. J. Ultrastruct. Res. 36: 68–85, 1971.
 80. Hanson, J., V. Lednev, E. J. O'Brien, and P. M. Bennett. Structure of the actin‐containing filaments in vertebrate skeletal muscle. Cold Spring Harbor Symp. Quant. Biol. 37: 311–318, 1973.
 81. Hanson, J., and J. Lowy. The structure of F‐actin and of actin filaments isolated from muscle. J. Mol. Biol. 6: 46–60, 1963.
 82. Hanson, J., and J. Lowy. Discussion: The problem of the location of myosin in vertebrate smooth muscle. Proc. Roy. Soc. London Ser. B 160: 523–524, 1964.
 83. Hartshorne, D. J., and M. Askoy. Introduction: Biochemistry of the contractile proteins in smooth muscle: a survey of current knowledge. In: Biochemistry of Smooth Muscle, edited by N. L. Stephens. Baltimore: Univ. Park, 1977, p. 363–378.
 84. Haselgrove, J. C. X‐ray evidence for a conformational change in the actin‐containing filaments of vertebrate striated muscle. Cold Spring Harbor Symp. Quant. Biol. 37: 341–352, 1973.
 85. Hax, W. M. A., G. E. P. M. van Venrooji, J. J. Denier van der Gon, and P. F. Elbers. Cell communication induced by lysolecithin. J. Membrane Biol. 13: 61–78, 1973.
 86. Henderson, R. M. Cell‐to‐cell contacts. In: Methods in Pharmacology, edited by E. E. Daniel and D. M. Paton. New York: Plenum, 1975, vol. 3, p. 47–77.
 87. Henderson, R. M. Types of cell contacts in arterial smooth muscle. Experientia 31: 103–105, 1975.
 88. Henderson, R. M., G. Duchon, and E. E. Daniel. Cell contacts in duodenal smooth muscle layers. Am. J. Physiol. 221: 564–574, 1971.
 89. Heumann, H. G. Mechanism of smooth muscle contraction. An electron microscope study of the mouse large intestine. Cytobiologie 3: 259–281, 1971.
 90. Heuser, J. E., D. M. D. Landis, and T. S. Reese. Preservation of synaptic structure by rapid freezing. Cold Spring Harbor Symp. Quant. Biol. 40: 17–24, 1976.
 91. Hinssen, H., and J. D'Haese. Filament formation by slime mould myosin isolated at low ionic strength. J. Cell Sci. 15: 113–129, 1974.
 92. Holtzer, H., J. Croop, S. Dienstman, H. Ishikawa, and A. P. Somlyo. The effects of cytochalasin‐B and colcimide on myogenic cultures. Proc. Natl. Acad. Sci. US 72: 513–517, 1975.
 93. Holtzer, H., J. Croop, M. Gershon, and A. P. Somlyo. Effects of cytochalasin‐B and colcimide on cells in muscle cultures. Am. J. Anat. 141: 291–296, 1974.
 94. Holtzer, H., S. Fellini, N. Rubinstein, J. Chi, and K. Strahs In: Cell Motility. Cells, Myosins and 100Å Filaments, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spr. Harbor Labs., 1976, book B, p. 823–839. (Cold Spr. Harbor Conf. Cell Proliferation.)
 95. Huttner, I., M. Boutet, and R. H. More. Gap junctions in arterial endothelium. J. Cell Biol. 57: 247–252, 1973.
 96. Huxley, A. F. Muscle structure and theories of contraction. Progr. Biophys. Biophys. Chem. 7: 257–318, 1957.
 97. Huxley, H. E. Electron microscopic studies on the structure of natural and synthetic protein filaments from striated muscle. J. Mol. Biol. 7: 281–308, 1963.
 98. Huxley, H. E. Structural changes in the actin‐ and myosincontaining filaments during contraction. Cold Spring Harbor Symp. Quant. Biol. 37: 361–376, 1973.
 99. Imaizumi, M., and K. Hama. An electron microscopic study on the interstitial cells of the gizzard in the love bird (Uroloncha domestica). Z. Zellforsch. Mikroskop. Anat. 97: 351–357, 1969.
 100. Inoue, Shinya. Chromosome movement by reversible assembly of microtubules. In: Cell Motility, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spr. Harbor Labs., 1976, vol. 3, book A, p. 1317–1327. (Cold Spr. Harbor Conf. Cell Proliferation.)
 101. Ishikawa, H. Formation of elaborate networks of T‐system tubules in cultured skeletal muscle with special reference to the T‐system formation. J. Cell Biol. 38: 51–66, 1968.
 102. Ishikawa, H. Arrowhead complexes in a variety of cell types. Excerpta Med. Intern. Congr. Ser. 333: 37–50, 1973.
 103. Ishikawa, H., R. Bischoff, and H. Holtzer. Mitosis and intermediate‐sized filaments in developing skeletal muscle. J. Cell Biol. 38: 538–555, 1968.
 104. Ishikawa, H., R. Bischoff, and H. Holtzer. Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43: 312–328, 1969.
 105. Ishikawa, H., and E. Yamada. Electron microscopic observations on smooth muscles of cat nictitating membrane. In: Proc. Ann. Meeting Electron Microscopy Soc. Am., 30th, edited by C. J. Arcenaux. Los Angeles: Claitor's, 1972, p. 32–33.
 106. Ivanov, I. I., N. I. Mirovich, V. P. Moisseieva, E. A. Parshina, S. E. Tukachinski, V. A. Yuriev, Z. N. Zhakhova, and I. P. Zinovieva. About the correlation of function and the fractional composition of the proteins in the muscles of various types. Acta Physiol. Acad. Sci. Hung. 16: 7–16, 1959.
 107. Jamieson, J. D., and G. E. Palade. Production of secretory proteins in animal cells. In: International Cell Biology, edited by B. R. Brinkley and K. R. Porter. New York: Rockefeller Univ. Press, 1976, p. 308–317.
 108. Johnson, R., M. Hammer, J. Sheridan, and J. P. Revel. Gap junction formation between reaggregated Novikoff hepatoma cells. Proc. Natl. Acad. Sci. US 71: 4536–4540, 1974.
 109. Jones, A. W., A. P. Somlyo, and A. V. Somlyo. Potassium accumulation in smooth muscle and associated ultrastructural changes. J. Physiol. London 232: 247–273, 1973.
 110. Jongsma, J. J., and H. E. van Rijn. Electrotonic spread of current in monolayer cultures of neonatal rat heart cells. J. Membrane Biol. 9: 341–360, 1972.
 111. Junker, J., and J. R. Sommer. Anchorfibers and the topography of junctional sarcoplasmic reticulum. In: Proc. Ann. Meeting Electron Microscopy Soc. Am., 35th, edited by G. W. Bailey. Baton Rouge, LA: Claitor's, 1977, p. 582.
 112. Kalderon, N., M. L. Epstein, and N. B. Gilula. Cell‐to‐cell communication and myogenesis. J. Cell Biol. 75: 788–806, 1977.
 113. Kaminer, B. Synthetic myosin filaments from vertebrate smooth muscle. J. Mol. Biol. 39: 257–264, 1969.
 114. Kaminer, B., and A. L. Bell. Myosin filamentogenesis: effects of pH and ionic concentrations. J. Mol. Biol. 20: 391–401, 1966.
 115. Kannan, M. S., and E. E. Daniel. Induction of spontaneous contractions and gap junctions in a multi‐unit smooth muscle by K+ conductance blockers. Pharmacologist 19: 110, 1977.
 116. Laszt, L., and G. Hamoir. Étude par éléctrophorèse et ultracentrifugation de la composition protéinique de la couche musculaire des carotides de bovidé. Biochim. Biophys. Acta 50: 430–449, 1961.
 117. Lazarides, E. Two general classes of cytoplasmic actin filaments in tissue culture cells: The role of tropomyosin. J. Supramol. Struct. 5: 531–563, 1976.
 118. Lazarides, E., and D. R. Balzer, Jr.. Specificity of desmin to avian and mammalian muscle cells. Cell 14: 429–438, 1978.
 119. Leblond, C. P., and G. Bennett. Role of the Golgi apparatus in terminal glycosylation. In: International Cell Biology, edited by B. R. Brinkley and K. R. Porter. New York: Rockefeller Univ. Press, 1976, p. 326–336.
 120. Loewenstein, W. R. Permeability of the junctional membrane channel. In: International Cell Biology, edited by B. R. Brinkley and K. R. Porter. New York: Rockefeller Univ. Press, 1976, p. 70–82.
 121. Lowy, J., F. R. Poulsen, and P. J. Vibert. Myosin filaments in vertebrate smooth muscle. Nature 225: 1053–1054, 1970.
 122. Lowy, J., and J. V. Small. The organization of myosin and actin in vertebrate smooth muscle. Nature 227: 46–51, 1970.
 123. Luciano, L., E. Junger, and E. Reale. Glykogen in glatten Muskelzellen der Gefäßwand von Saugetieren. Histochemie 15: 219–228, 1968.
 124. MacLennan, D. H., and P. C. Holland. Calcium transport in sarcoplasmic reticulum. In: Annual Reviews of Biophysics and Bioengineering, edited by L. J. Mullins. Palo Alto, CA: Ann. Rev., 1975, vol. 4, p. 377–404.
 125. Maruyama, K., and S. Ebashi. Alpha‐actinin, a new structural protein from striated muscle. II. Action on actin. J. Biochem. Tokyo 58: 13–19, 1965.
 126. McNutt, N. S., R. A. Hershberg, and R. S. Weinstein. Further observations on the occurrence of nexuses in benign and malignant human cervical epithelium. J. Cell Biol. 51: 805–825, 1971.
 127. McNutt, N. S., and R. S. Weinstein. The ultrastructure of the nexus. A correlated thin section and freeze cleave study. J. Cell Biol. 47: 666–688, 1970.
 128. Miura, S., R. Takahashi, S. Sunano, and E. Miyazaki. Studies on the dense body in intestinal smooth muscle. Japan J. Smooth Muscle Res. 5: 197, 1969.
 129. Mobley, B. A., and B. R. Eisenberg. Size of components in frog skeletal muscle measured by methods of stereology. J. Gen. Physiol. 66: 31–45, 1975.
 130. Moore, P. B., H. E. Huxley, and D. J. DeRosier. Three‐dimensional reconstruction of F‐actin, thin filaments and decorated thin filaments. J. Mol. Biol. 50: 279–295, 1970.
 131. Moos, C. Interaction of C‐protein with myosin and light meromyosin. Cold Spring Harbor Symp. Quant. Biol. 37: 93–95, 1973.
 132. Muggli, R., and H. R. Baumgartner. Pattern of membrane invaginations at the surface of smooth muscle cells of rabbit arteries. Experientia 28: 1212–1214, 1972.
 133. Murphy, R. A. Contractile system function in mammalian smooth muscle. Blood Vessels 13: 1–23, 1976.
 134. Murphy, R. A., S. P. Driska, and D. M. Cohen. Variations in actin to myosin ratios and cellular force generation in vertebrate smooth muscles. In: Excitation‐Contraction Coupling in Smooth Muscle, edited by R. Casteels, T. Godfraind, and J. C. Rüegg. Amsterdam: Elsevier, 1977, p. 417–424.
 135. Murphy, R. A., J. T. Herlihy, and J. Megerman. Forcegenerating capacity and contractile protein content of arterial smooth muscle. J. Gen. Physiol. 64: 691–705, 1974.
 136. Nachmias, V. T. Filament formation by purified Physarum. Proc. Natl. Acad. Sci. US 69: 2011, 1972.
 137. Nachmias, V. T. Physarum myosin: two new properties. Cold Spring Harbor Symp. Quant. Biol. 37: 607–612, 1972.
 138. Nagasawa, J., and T. Susuki. Electron microscopic study on the cellular interrelationships in the smooth muscle. Tohoku J. Exptl. Med. 91: 299–313, 1967.
 139. Needham, D. M., and C. F. Shoenberg. Proteins of the contractile mechanism in vertebrate smooth muscle. In: Handbook of Physiology. Alimentary Canal, edited by C. F. Code. Washington, D.C.: Am. Physiol. Soc., 1968, sect. 6, vol. IV, chapt. 88, p. 1793–1810.
 140. Nonomura, Y., and S. Ebashi. Isolation and identification of smooth muscle contractile proteins. In: Methods in Pharmacology, edited by E. E. Daniel and D. M. Paton. New York: Plenum, 1975, vol. 3, p. 141–162.
 141. Novikoff, P. M., A. B. Novikoff, N. Quintana, and J. J. Hauw. Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J. Cell Biol. 50: 859–886, 1971.
 142. O'Brien, E. J., J. M. Gillis, and J. Couch. Symmetry and molecular arrangement in paracrystals of reconstituted muscle thin filaments. J. Mol. Biol. 99: 461–475, 1975.
 143. Page, S. G. Structure and some contractile properties of fast and slow muscles of the chicken. J. Physiol. London 205: 131–145, 1969.
 144. Panner, B. J., and C. R. Honig. Filament ultrastructure and organization in vertebrate smooth muscle. Contraction hypothesis based on localization of actin and myosin. J. Cell Biol. 35: 303–321, 1967.
 145. Pappas, G. D., Y. Asada, and M. V. L. Bennett. Morphological correlates of increased coupling resistance at an electrotonic synapse. J. Cell Biol. 49: 173–188, 1971.
 146. Payton, B. W., M. V. L. Bennett, and G. D. Pappas. Temperature‐dependence of resistance at an electrotonic synapse. Science 165: 594–597, 1969.
 147. Pease, D. C., and S. Molinari. Electron microscopy of muscular arteries; pial vessels of the cat and monkey. J. Ultrastruct. Res. 3: 447–468, 1960.
 148. Pepe, F. A. The myosin filament. I. Structural organization from antibody staining observed in electron microscopy. J. Mol. Biol. 27: 203–225, 1967.
 149. Pepe, F. A. The myosin filament: backbone structure. In: John M. Marshall Symposium on Cell Biology, edited by F. Pepe, J. W. Sanger, and V. T. Nachmias. New York: Academic, 1979.
 150. Peracchia, C. Gap junctions. Structural changes after uncoupling procedures. J. Cell Biol. 72: 628–641, 1977.
 151. Peracchia, C. Gap junction structure and function. Trends Biochem. Sci. 2: 26–30, 1977.
 152. Polinger, I. S., and N. S. McNutt. Intercellular junctions in freeze‐cleaved and etched chicken heart (Abstract). Meeting Am. Soc. Cell Biol., 11th Annual, New Orleans, 1971, p. 230.
 153. Pollard, T. D. Electron microscopy of synthetic myosin filaments. J. Cell Biol. 67: 93–104, 1975.
 154. Pollard, T. D., K. Fujiwara, R. Niederman, and P. Maupin‐Szamier. Evidence for the role of cytoplasmic actin and myosin in cellular structure and motility. In: Cell Motility, edited by R. D. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spr. Harbor Labs., 1976, book B, p. 689–724. (Cold Spr. Harbor Conf. Cell Proliferation.)
 155. Pollard, T. D., and R. R. Weihing. Actin and myosin and cell movement. CRC Critical Rev. Biochem. 2: 1–65, 1974.
 156. Prescott, L., and M. W. Brightman. The sarcolemma of Aplysia smooth muscle in freeze‐fracture preparations. Tissue Cell 8: 241–258, 1976.
 157. Prosser, C. L., G. Burnstock, and J. Kahn. Conduction in smooth muscle: comparative structural properties. Am. J. Physiol. 199: 545–552, 1960.
 158. Revel, J. P., L. Napolitano, and D. W. Fawcett. Identification of glycogen in electron micrographs of thin tissue sections. J. Biophys. Biochem. Cytol. 8: 575–589, 1960.
 159. Revel, J. P., W. Olson, and M. J. Karnovsky. A twenty‐angstrom gap junction with a hexagonal array of subunits in smooth muscle. J. Cell Biol. 35: 112A, 1967.
 160. Rhodin, J. A. G. Fine structure of vascular walls in mammals. With special reference to smooth muscle component. Physiol. Rev. 42: (Suppl. 5) 48–81, 1962.
 161. Rhodin, J. A. G. The ultrastructure of mammalian arterioles and precapillary sphincters. J. Ultrastruct. Res. 18: 181–223, 1967.
 162. Rhodin, J. A. G. Fine structure of elasmobranch arteries, capillaries and veins in the spiny dogfish, Squalus acanthias. Comp. Biochem. Physiol. 42: 59–64, 1972.
 163. Rice, R. V. Conformation of individual macromolecular particles from myosin solutions. Biochim. Biophys. Acta 52: 602–604, 1961.
 164. Rice, R. V., and A. C. Brady. Biochemical and ultrastructural studies on vertebrate smooth muscle. Cold Spring Harbor Symp. Quant. Biol. 37: 429–438, 1973.
 165. Rice, R. V., A. C. Brady, R. H. DePue, and R. E. Kelly. Morphology of individual macromolecules and their ordered aggregates by electron microscopy. Biochem. Z. 345: 370–394, 1966.
 166. Rice, R. V., G. M. McManus, C. E. Devine, and A. P. Somlyo. A regular organization of thick filaments in mammalian smooth muscle. Nature New Biol. 231: 242–243, 1971.
 167. Rice, R. V., J. A. Moses, G. M. McManus, A. C. Brady, and L. M. Blasik. The organization of contractile filaments in a mammalian smooth muscle. J. Cell. Biol. 47: 183–197, 1970.
 168. Rosenbluth, J. Smooth muscle: an ultrastructural basis for the dynamics of its contraction. Science 184: 1337–1339, 1965.
 169. Rosenbluth, J. Obliquely striated muscle. III. Contraction mechanism of Ascaris body muscle. J. Cell Biol. 34: 15–33, 1967.
 170. Rosenbluth, J. Myosin‐like aggregates in trypsin‐treated smooth muscle cells. J. Cell Biol. 48: 174–188, 1971.
 171. Ross, R. The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J. Cell Biol. 50: 172–186, 1971.
 172. Ross, R. Connective tissue cells, cell proliferation and synthesis of extracellular matrice—a review. Phil. Trans. Roy. Soc. London Ser. B 271: 247–259, 1975.
 173. Ross, R., and P. Bornstein. The elastic fiber. I. The separation and partial characterization of its macromolecular components. J. Cell Biol. 40: 366–381, 1969.
 174. Ross, R., and S. J. Klebanoff. Fine structural changes in uterine smooth muscle and fibroblasts in response to estrogen. J. Cell Biol. 32: 155–167, 1967.
 175. Ross, R., and S. J. Klebanoff. The smooth muscle cell. I. In vivo synthesis of connective tissue proteins. J. Cell Biol. 50: 159–171, 1971.
 176. Rüegg, J. C. Smooth muscle tone. Physiol. Rev. 51: 201–248, 1971.
 177. Sachs, E. S., and W. T. Daems. Microtubules in human aortic intimal cells. Z. Zellforsch. Mikroskop. Anat. 73: 553–558, 1966.
 178. Sanger, J. W. Formation of synthetic myosin filaments: influence of pH, ionic strength, cation substitution, dielectric constant and method of preparation. Cytobiologie 4: 450–466, 1971.
 179. Schollmeyer, J. E., L. T. Furcht, D. E. Goll, R. M. Robson, and M. H. Stromer. Localization of contractile proteins in smooth muscle cells and in normal and transformed fibroblasts. In: Cell Motility, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spr. Harbor Labs., 1976, vol. 3, book A, p. 361–388. (Cold Spr. Harbor Conf. Cell Proliferation.)
 180. Shelanski, M. L., S. H. Yen, and V. M. Lee. Neurofilaments and glial filaments. In: Cell Motility, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spring Harbor Labs., 1976, vol. 3, p. 1007–1020. (Cold Spr. Harbor Conf. Cell Proliferation.)
 181. Shizuta, Y., H. Shizuta, M. Gallo, P. Davies, I. Pastan, and M. S. Lewis. Purification and properties of filamin, an actin binding protein from chicken gizzard. J. Biol. Chem. 251: 6562–6567, 1976.
 182. Shoenberg, C. F. An electron microscopic study of smooth muscle in pregnant uterus of the rabbit. Biophys. Biochem. Cytol. 4: 609–614, 1958.
 183. Shoenberg, C. F. Contractile proteins of vertebrate smooth muscle. Nature 206: 526–527, 1965.
 184. Shoenberg, C. F., P. J. Goodford, M. W. Wolowyk, and G. S. Wootton. Ion changes during smooth muscle fixation for electron microscopy. J. Mechanochemistry Cell Motility 2: 69–82, 1973.
 185. Shoenberg, C. F., and J. C. Haselgrove. Filaments and ribbons in vertebrate smooth muscle. Nature 249: 152–154, 1974.
 186. Shoenberg, C. F., and D. M. Needham. A study of the mechanism of contraction in vertebrate smooth muscle. Biol. Rev. 51: 53–104, 1976.
 187. Simionescu, M., N. Simionescu, and G. E. Palade. Segmental differentiations of cell junctions in the vascular endothelium. The Microvasculature. J. Cell Biol. 67: 863–885, 1975.
 188. Simionescu, M., N. Simionescu, and G. E. Palade. Segmental differentiations of cell junctions in the vascular endothelium. Arteries and Veins. J. Cell Biol. 68: 705–723, 1976.
 189. Small, J. V. Contractile units in vertebrate smooth muscle cells. Nature 249: 325–327, 1974.
 190. Small, J. V., and A. Sobieszek. Studies on the function and composition of the 10 nm (100Å) filaments of vertebrate smooth muscle. J. Cell Sci. 23: 243–268, 1977.
 191. Small, J. V., and J. M. Squire. Structural basis of contraction in vertebrate smooth muscle. J. Mol. Biol. 67: 117–149, 1972.
 192. Sobieszek, A. Vertebrate smooth muscle myosin. Enzymatic and structural properties. In: Biochemistry of Smooth Muscle, edited by N. L. Stephens. Baltimore: Univ. Park, 1977, p. 413–443.
 193. Sobieszek, A., and R. D. Bremel. Preparation and properties of vertebrate smooth muscle myofibrils and actomyosin. European J. Biochem. 55: 49–60, 1975.
 194. Socolar, S. J., and A. L. Politoff. Uncoupling cell junctions in a glandular epithelium by depolarizing current. Science 172: 492–494, 1971.
 195. Somlyo, A. P., C. E. Devine, and A. V. Somlyo. Thick filaments in unstretched mammalian smooth muscle. Nature New Biol. 233: 218–219, 1971.
 196. Somlyo, A. P., C. E. Devine, A. V. Somlyo, and S. R. North. Sarcoplasmic reticulum and the temperature‐dependent contraction of smooth muscle in calcium‐free solutions. J. Cell Biol. 51: 722–741, 1971.
 197. Somlyo, A. P., C. E. Devine, A. V. Somlyo, and R. V. Rice. Filament organization in vertebrate smooth muscle. Phil. Trans. Roy. Soc. London Ser. B 265: 223–229, 1973.
 198. Somlyo, A. P., R. E. Garfield, S. Chacko, and A. V. Somlyo. Golgi organelle response to the antibiotic X537A. J. Cell. Biol. 66: 425–554, 1975.
 199. Somlyo, A. P., and A. V. Somlyo. Vascular smooth muscle. I. Normal structure, pathology, biochemistry and biophysics. Pharmacol. Rev. 20: 197–272, 1968.
 200. Somlyo, A. P., and A. V. Somlyo. Ultrastructure of smooth muscle. In: Methods in Pharmacology, edited by E. E. Daniel and D. M. Paton. New York: Plenum, 1975, vol. 3, p. 3–43.
 201. Somlyo, A. P., A. V. Somlyo, F. T. Ashton, and J. Vallieres. Vertebrate smooth muscle: ultrastructure and function. In: Cell Motility, edited by R. Goldman, T. Pollard, and J. Rosenbaum. Cold Spring Harbor, N.Y.: Cold Spring Harbor Labs., 1976, vol. 3, book A, p. 165–183. (Cold Spr. Harbor Conf. Cell Proliferation.)
 202. Somlyo, A. P., A. V. Somlyo, C. E. Devine, and R. V. Rice. Aggregation of thick filaments into ribbons in mammalian smooth muscle. Nature New Biol. 231: 243–246, 1971.
 203. Somlyo, A. P., A. V. Somlyo, C. E. Devine, P. D. Peters, and T. A. Hall. Electron microscopy and electron probe analysis of mitochondrial cation accumulation in smooth muscle. J. Cell Biol. 61: 723–742, 1974.
 204. Somlyo, A. V. The contractile apparatus of vascular smooth muscle. In: Mechanisms of Vasodilation, edited by P. M. Vanhoutte and I. Leusen. Basel: Karger, 1978, p. 12–20.
 205. Somlyo, A. V. Bridging structures spanning the junctional gap at the triad of skeletal muscle. J. Cell Biol. 80: 743–750, 1979.
 206. Somlyo, A. V., F. T. Ashton, L. Lemanski, J. Vallieres, and A. P. Somlyo. Filament organization and dense bodies in vertebrate smooth muscle. In: Biochemistry of Smooth Muscle, edited by N. L. Stephens. Baltimore: Univ. Park, 1977, p. 445–471.
 207. Somlyo, A. V., H. Shuman, and A. P. Somlyo. Elemental distribution in striated muscle and effects of hypertonicity: electron probe analysis of cryo sections. J. Cell Biol. 75: 828–857, 1977.
 208. Somlyo, A. V., and A. P. Somlyo. Strontium accumulation by sarcoplasmic reticulum and mitochondria in vascular smooth muscle. Science 174: 955–958, 1971.
 209. Sommer, J. R., and E. A. Johnson. Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. J. Cell Biol. 36: 497–526, 1968.
 210. Sparrow, M. P., L. C. Maxwell, J. C. Rüegg, and D. F. Bohr. Preparation and properties of a calcium ion‐sensitive actomyosin from vascular smooth muscle. Am. J. Physiol. 219: 1366–1372, 1970.
 211. Squire, J. M. Muscle filament structure and muscle contraction. In: Annual Reviews of Biophysics and Bioengineering, edited by L. J. Mullins. Palo Alto, CA: Ann. Rev., 1975, vol. 4, p. 137–163.
 212. Staehelin, L. A. Three types of gap junctions interconnecting intestinal epithelial cells visualized by freeze‐etching. Proc. Natl. Acad. Sci. US 69: 1318–1321, 1972.
 213. Staehelin, L. A., F. S. Chlapowski, and M. A. Bonneville. Lumenal plasma membrane of the urinary bladder. I. Three dimensional reconstruction from freeze‐etch images. J. Cell Biol. 53: 73–91, 1972.
 214. Stein, O., S. Eisenberg, and Y. Stein. Aging of aortic smooth muscle cells in rats and rabbits. Lab. Invest. 21: 386–397, 1969.
 215. Taylor, A. B., D. Kreulen, and C. L. Prosser. Electron microscopy of the connective tissues between longitudinal and circular muscle of small intestine of cat. Am. J. Anat. 150: 427–441, 1977.
 216. Tregear, R. T., and J. M. Squire. Myosin content and filament structure in smooth and striated muscle. J. Mol. Biol. 77: 279–290, 1973.
 217. Turin, L., and A. Warner. Carbon dioxide reversibly abolishes ionic communication between cells of early amphibian embryo. Nature 270: 56–57, 1977.
 218. Twarog, B. M., M. M. Dewey, and T. Hidaka. The structure of Mytilus smooth muscle and the electrical constants of the resting muscle. J. Gen. Physiol. 61: 207–221, 1973.
 219. Uehara, Y., and G. Burnstock. Demonstration of “gap junctions” between smooth muscle cells. J. Cell Biol. 44: 215–217, 1970.
 220. Uehara, Y., G. R. Campbell, and G. Burnstock. Cytoplasmic filaments in developing and adult vertebrate smooth muscle. J. Cell Biol. 50: 484–497, 1971.
 221. Vibert, P. J., J. C. Haselgrove, J. Lowy, and F. R. Poulsen. Structural changes in actin‐containing filament of muscle. J. Mol. Biol. 71: 757–767, 1972.
 222. Wachsberger, P. R., and F. A. Pepe. Purification of uterine myosin and synthetic filament formation. J. Mol. Biol. 88: 385–391, 1974.
 223. Wakabayashi, T., H. E. Huxley, L. A. Amos, and A. Klug. Three‐dimensional image reconstruction of actin‐tropomyosin complex and actin‐tropomyosin‐troponin T‐troponin I complex. J. Mol. Biol. 93: 477–497, 1975.
 224. Wang, K., and S. J. Singer. Interaction of filamin with F‐actin in solution. Proc. Natl. Acad. Sci. US 74: 2021–2025, 1977.
 225. Weingart, R. The actions of ouabain on intercellular coupling and conduction velocity in mammalian ventricular muscle. J. Physiol. London 264: 341–365, 1977.
 226. Wells, G. X., and M. W. Wolowyk. Freeze‐etch observations on membrane structure in the smooth muscle of guinea‐pig taenia coli. J. Physiol. London 218: 11P–13P, 1971.
 227. Whalen, R. G., G. S. Butler‐Browne, and F. Gros. Protein synthesis and actin heterogeneity in calf muscle cells in culture. Proc. Natl. Acad. Sci. US 73: 2018–2022, 1976.
 228. Whaley, W. G., M. Dauwalder, and J. E. Kephart. Golgi apparatus: influence on cell surfaces. Science 175: 596–599, 1972.
 229. Wight, T. N., and R. Ross. Proteoglycans in primate arteries. I. Ultrastructural localization and distribution in the intima. J. Cell Biol. 67: 660–674, 1975.
 230. Wootton, G. S., and P. J. Goodford. An association between mitochondria and vesicles in smooth muscle. Cell Tissue Res. 161: 119–132, 1975.
 231. Wuerker, R. B. Neurofilaments and glial filaments. Tissue Cell 2: 1–9, 1970.
 232. Yamamoto, M. Electron microscopic studies on the innervation of the smooth muscle and the interstitial cell of Cajal in the small intestine of the mouse and bat. Arch. Histol. Japan. Niigata, Japan 40: 171–201, 1977.
 233. Zachar, J., and D. Zacharova. Potassium contractures in single muscle fibres of the crayfish. J. Physiol. London 186: 596–618, 1966.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

Avril V. Somlyo. Ultrastructure of Vascular Smooth Muscle. Compr Physiol 2011, Supplement 7: Handbook of Physiology, The Cardiovascular System, Vascular Smooth Muscle: 33-67. First published in print 1980. doi: 10.1002/cphy.cp020202