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Three-dimensional architecture of sarcoplasmic reticulum and T-system in human skeletal muscle.

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THE ANATOMICAL RECORD 218~275-283(1987)
Three-Dimensional Architecture of Sarcoplasmic
Reticulum and T-System in Human Skeletal Muscle
KAZUKO HAYASHI, RODMAN G. MILLER, AND A. KEITH W. BROWNELL
Department ofAnatomy (K.H., R. G.M.) and Department of Clinical Neurosciences (A.K.W.B.),
Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4 N l
ABSTRACT
A modified Golgi method combined with stereoscopy has been used
to demonstrate the three-dimensional architecture of the sarcoplasmic reticulum
(SRI and the T-system in human skeletal muscle. SR formed a continuous repeating
network with a different structure dependent upon the sarcomere position. Intermyofibrillar SR contained three regions: 1)fenestrated collars overlying the M-band
region, 2) terminal cisternae overlying the A-I region, and 3) a three-dimensional
anastomosed tubular network overlying the Z-band region. Longitudinal andlor
transverse SR tubules connected these regions. Subsarcolemmal SR was also composed of three regions: 1)transversely oriented polygonal meshes overlying the Mband, 2) single-layered tubules overlying the Z-band region, and 3) a loose network
between the two. In the subsarcolemmal sarcoplasm, where mitochondria were
aggregated, SR anastomosed loosely and showed nonfenestrated cisternae beneath
the plasma membrane. The T-system was composed of transversely oriented networks overlying the A-I region with occasional longitudinal tubules connecting these
networks.
Extensive ultrastructural studies of human skeletal
muscle have been done, with thin sections, which describe the two-dimensional appearance of different fiber
types and pathological conditions. Less is known about
the three-dimensional architecture of the sarcoplasmic
reticulum (SRI and T-system in normal human muscle,
undoubtedly due to the sparsity of en face visualizations
of the SR and T-system in thin sections.
Selective SR staining techniques utilizing high-voltage electron microscopy have recently been developed to
study thick sections of frog muscle (Bailey and Peachey,
1975), and various staining methods using conventional
electron microscopy have been successfully applied to
obtain three-dimensional visualizations of the intermyofibrillar membrane systems in animal skeletal muscle
(Forbes and Sperelakis, 1980; Rambourg and Segretain,
1980; Scales and Yasumura, 1982; Yasumura and Scales,
1982).
In the present communication, we have used the modified Golgi black reaction (the Golgi method) initially
applied to skeletal muscle by Veratti (1902) and modified
for electron microscopy by Franzini-Armstrong and
Peachey (1982) to study the morphology of the SR and
the T-system in human skeletal muscle. Although tissue
treated by this method does not stain homogeneously,
adequate staining could be obtained to allow us to better
define the three-dimensional morphology of the SR and
the T-system in normal human skeletal muscle.
MATERIALS AND METHODS
The vastus lateralis biopsy specimens used in this
study were obtained from 31 subjects (ten males and 21
females, aged from 4 to 64 years, mean age 32 years)
who were undergoing testing for malignant hyperther0 1987 ALAN R. LISS, INC.
mia susceptibility but who turned out to be normal. In
addition, histological and histochemical examination of
these muscles also showed no abnormality.’
Muscle bundles, 20 mm in length and 2-3 mm in
diameter, were slightly stretched, tied to a wooden stick,
and fixed immediately in 2.5% glutaraldehyde in 0.1 M
cacodylate buffer pH 7.4 at 4°C for 1 day to 2 weeks. For
the Golgi method, the bundles were cut into pieces
(2 x 2 x 1 mm), rinsed three times for 20 min each in 0.1
M cacodylate buffer, washed twice for 30 min each in
3% K2Cr207, and incubated in a solution containing
0.2% Os04, 2.4% K2Cr207 for 8 days a t 4°C and then in
0.75% AgN03 a t 4°C for 5 days. Second infiltrations in
the same solutions (0.2% Os04 and 2.4% K2Cr207 and
0.75% AgN03) followed, with 3 and 2 days of incubation,
respectively. Specimens were then dehydrated in
ethanol, infiltrated with propylene oxide, and embedded
in Spurr’s plastic media (Spurr, 1969).
Thick sections (0.3-1.0 pm) were cut from the blocks
treated by the Golgi method and scanned light microscopically for adequately staining regions. The blocks
were trimmed to these regions and cut for EM observation. Sections were mounted on folding oyster grids
which were pressed firmly together and without further
staining were examined in a Philips 400 electron microscope at 100 kV. Stereo pairs of electron micrographs of
Received April 24, 1986; accepted January 27, 1987.
Address reprint requests to Dr. A.K.W. Brownell, Department of
Clinical Neurosciences, Faculty of Medicine, University of Calgary,
Foothills Hospital, 1403 29th Street NW, Calgary, Alberta, Canada
T2N 2T9.
‘These examinations were done in the Department of Pathology at
the Foothills Hospital in Calgary.
276
K. HAYASHI, R.G. MILLER, AND A.K.W. BROWNELL
the same field were made by tilting the specimen stage
a t +6-12" and viewed with a stereoscope.
For comparing SR morphology between fiber types, we
prepared serial thin and thick sections from specimens
treated by the Golgi method and identified fiber types
on the basis of the Z-band width and M-band appearance
(Sjostrom et al., 1982) in thin sections which were additionally stained with uranyl acetate and lead citrate
(Reynolds, 1963). The structure of the SR was then examined in the serial thick section. We also used a series
of thin and thick sections to confirm the identity of the
structures stained with the Golgi method.
Additional tissue was processed for conventional electron microscopy for examination of SR and T-tubule
morphology. Strips of the muscle fixed in glutaraldehyde were postfixed in 1% OsO4 in 0.1 M cacodylate
buffer, pH 7.4, a t 4°C for 1 hr, dehydrated in ethanol,
and embedded in Spurr's plastic media (1969). Th'in sections were cut on a n ultramicrotome and stained with
uranyl acetate and lead citrate (Reynolds, 1963).
RESULTS
In our Golgi preparations of human skeletal muscle,
both the SR and the T-system were frequently stained,
while in some regions only the T-system or the SR was
stained, and in other regions the staining was totally
lacking (Fig. 1). Occasionally, nuclear membranes and
mitochondria were also stained. In our comparative
study of fiber types, although morphometric differences
have been reported by Eisenberg (1983), we could not
find any predictable difference in the morphology of SR
(Fig. 1). We found variability of SR complexity between
subjects rather than between fiber types; however, no
quantitation of this variability was attempted. Therefore, we shall make no further distinction of structures
on the basis of fiber types.
Sarcoplasmic Reticulum
Sarcoplasmic reticulum (SR) in human skeletal muscle showed a different structure depending upon its relation both to the plasma membrane and to the adjacent
myofibrillar pattern; we have termed these the subsarcolemmal SR and the intermyofibrillar SR, respectively.
Between myofibrils, the SR was composed of longitudinally oriented repeating units whose morphology varied
according to its position within the sarcomere (Figs. 1,
2). Overlying the M-band region, SR formed patchlike
fenestrated collars of varying size and shape (Fig. 2).
Although these collars were usually transversely connected by thinner tubules, they were not always continuous around myofibrils (Fig. 2).
Overlying the A-I junction, SR associated with the Ttubule formed distended sacs, i.e., terminal cisternae
(Figs. 1, 2). These terminal cisternae were apposed to
the T-tubule, forming triads, occasionally dyads, and
rarely tetrads or pentads. These sacs of various sizes
were usually located perpendicular but also occasionally
parallel to the fiber axis. Adjacent terminal cisternae
were connected by one or two thinner transverse tubules
running parallel to but separate from the T-tubule (Figs.
1, 2), and the two terminal cisternae making a triad
were usually connected by small, longitudinally oriented tubules located at the lateral region of the triads
(Fig. 2b, double arrowheads). Longitudinal tubules provided connection between SR in the M-band region and
in the A-I junction region. SR overlying A-bands formed
a single layer between adjacent myofibrils, while SR
overlying I-bands had a more complex multilayered
structure (Figs. 1,2).
In the Z-band region, tubular forms of SR irregularly
anastomosed to form a three-dimensional network, encircling each myofibril and displaying horizontal continuity (Figs. 1, 2). The SR of this region also had
occasional fenestrations. The SR between the Z-band
and the A-I junction was connected by longitudinal SR
tubules (Figs. 1,2).
At the periphery of the fiber, the SR had a completely
different appearance (Figs. 3-5). Here, it was composed
of transversely oriented continuous polygonal meshes at
the M-band region, transverse tubules at the Z-band
region, and a loose network of SR connecting the two
(Fig. 3). These subsarcolemmal regions were continuous
with the intermyofibrillar regions (Fig. 3). Some parts of
the network were distended to form nonfenestrated cisternae which did not have any special association with
T-tubules, as was seen in the deeper portions of SR.
Other parts occasionally made triads with T-tubules.
Since these findings could only be clearly resolved in
fortuitous tangential thick sections in which the SR was
stained without extracellular staining (Figs. 3, 51, we
used the goniometer specimen stage to confirm these
findings in thick sections where plasma membranes
were not tangentially sectioned. We occasionally observed the subsarcolemmal network in tangential thin
sections prepared by conventional methods (Fig. 4a),
thus confirming our Golgi method observations.
In the subsarcolemmal mitochondria-rich region, tubular and occasionally focally bulged SR loosely anastomosed in all directions among other organelles (Fig. 5).
Beneath the plasma membrane, in addition to a tubular
appearance, the SR in this area also formed small, nonfenestrated cisternae without any specific orientation
(Fig. 5).T-tubules were usually not observed in this area
in Golgi preparations (not shown).
Although junctional feet located between a subsarcolemma1 vesicle and plasma membrane were not observed in Golgi preparations, they were occasionally
seen in conventionally prepared thin sections (Fig. 4b).
Therefore, nonfenestrated cisternae located beneath the
plasma membrane would form a peripheral coupling
with plasma membrane in human as in other skeletal
muscles (Forbes et al., 1977; Forbes and Sperelakis, 1980;
Spray et al., 1974).
T-System
In longitudinal sections stained by the Golgi method,
T-tubules were easily distinguished from SR; the T-tubules were much more electron dense (Figs. 1, 2) and
were located close to the A-I junction (Fig. 6a). We occasionally observed longitudinal T-tubule connecting two
transversely oriented T-tubule networks and sometimes being part of a longitudinally oriented triad (Fig.
6a). These longitudinally oriented T-tubules were not
evenly distributed throughout the fiber, but they were
common in regions of dislocation of cross-striations or in
the regions close to the plasma membrane. In cross
sections, T-tubules showed both flat ribbon and cylindrical shapes and formed a continuous transverse network
(Fig. 6b). Although the flat ribbon T-tubules typically
associated with the SR in the formation of triads were
SARCOPLASMIC RETICULUM IN HUMAN MUSCLE
Fig. 1. Electron micrograph of a thick section (0.5 pm in thickness)
prepared by the Golgi method includes three fibers; both left (A) and
right (C) fibers are type I1 and the middle one (B)is type I. The staining
is observed on sarcoplasmic reticulum (SR) in fiber A, SR and some
mitochondria in fiber B, both SR and T-tubule in fiber C, and extracellular spaces (EC) between fibers. SR shows repeating units depending
on myofibrillar pattern. Bar = 1 pm.
277
Fig. 2. Stereo pair (Za)and a higher magnification (2b) of the same
section in which SR and T-tubules are selectively stained. Intermyofibrillar SR shows a continuous network made up of repeating units:
patchlike fenestrated collars overlying the M-band (FC), terminal cisternae overlying the A-I region forming triads (arrows) with T-tubule,
and three-dimensionally anastomosed tubules overlying the Z-band
region. Longitudinal andor transverse tubules connect these regions
Figure 2b (arrowheads). Double arrowheads point to the small tubules
that connect the two terminal cisternae of a triad. Bar = 1 pm. Tilt
12".
+
278
K. HAYASHI, R.G. MILLER, AND A.K.W. BROWNELL
Fig. 3. a: Slightly oblique section (0.5 pm in thickness) prepared by
the Golgi method in which only SR is stained showing the structure of
the SR in the periphery of a fiber. The elaborate network of subsarcolemma1 SR can be easily observed in the upper region of the centre
fiber where there is no coarse precipitation in the extracellular space
(EC). Bar = 1 pm. b: Stereo pairs of the same section as above. The
three-dimensional architecture of the subsarcolemmal SR and conti-
nuity with the intermyofibrillar SR can be detected. Bar = 1 pm. Tilt
6". c: A higher magnification of the same section as 3b shows the
three regions of the sarcolemmal SR transversely oriented polygonal
mesh (arrows) overlying the M-band region, single-layered tubules
overlying the Z-band region (double arrowheads), and loose networks
between the former two which contain nonfenestrated cisternae (arrowheads). Bar = 0.5 pm.
SARCOPLASMIC RETICULUM IN HUMAN MUSCLE
Fig. 4. a: A tangential section prepared by conventional methods
and stained with uranyl acetate and lead citrate shows a region of the
subsarcolemmal SR network polygonal meshes overlying the M-band
region (arrow) and nonfenestrated cisternae (arrowheads). Double arrowheads indicate caveolae. EC: extracellular space. Z: Z-band. Bar =
279
0.1 pm. b: A longitudinal section prepared by conventional methods
and stained with uranyl acetate and lead citrate shows junctional feet
(arrowheads) between plasma membrane (Pm) and subsarcolemmal
cisternae. Z: Z-band. C: caveolae. EC: extracellular space. Bar = 0.1
pm.
Fig. 5. Stereo pair in which only SR is stained. This oblique section shows a loose network of SR in the
subsarcolemmal region where mitochondria (M) and lipid droplets
are aggregated. Beneath the plasma
membrane, SR contains nonfenestrated cisternae (arrowheads) in the tubular anastomosed network.
Arrows indicate bulged SR. Intermyofibrillar network of SR is seen in the upper left region and polygonal
meshes in the subsarcolemmal region are seen in the upper right region. Bar = 1pm. Tilt f 6".
a)
280
K. HAYASHI, R.G. MILLER, AND A.K.W. BROWNELL
Fig. 6. a: Longitudinal stereo pair in which only T-tubules are Bar = 1 pm. Tilt k 12". b Transverse stereo pair in which only Tstained, showing T-tubule networks located at the A-I region and tubules are stained, showing a continuous transverse network of Toccasional longitudinal tubules (arrowheads). Arrow shows flat, rib- tubules forming both flat ribbon and cylindrical shapes. Bar = 1 pm.
bon-shaped regions of T-tubules forming longitudinally oriented triads. Tilt k 12".
the commonest type of T-tubule, they were less frequent
than was seen in frog twitch muscle or rat white muscle
(Peachey and Franzini-Armstrong, 1983).
In the silver-stained preparations we could follow the
course of T-tubules close to the plasma membrane; however, we were unable to define connections between the
T-tubule and the plasma membrane due to the presence
of artifactual silver precipitate frequently seen in the
extracellular space and sometimes in the intracellular
space. Evidence of openings of the T-tubules to the extracellular space were only rarely seen in the conventionally prepared thin sections (Shafiqet al., 1966);T-tubules
SARCOPLASMIC RETICULUM IN HUMAN MUSCLE
281
d
Fig. 7. A diagrammatic presentation of a superficial portion of a
human skeletal myofiber demonstrating the structural characteristics
of subsarcolemmal and intermyofibrillar membrane systems. 1:plasma
membrane; 2: basal lamina; 3: endomysial collagen; 4: myofibril; 5:
terminal cisternae; 6: fenestrated collar; 7: continuous tubular anasto-
moses overlying the Z-band region; 8: longitudinal and/or transverse
tubules; 9: T-tubule; 10: subsarcolemmal polygonal mesh overlying the
M-band region; 11:single-layered tubules overlying the Z-band region;
12: a nonfenestrated cisternae; 13: mitochondria; A:A-band; 1:I-band;
MM-band Z:Z-band.
followed a sinuous course beneath the plasma membrane and appeared to open in the region where subsarcolemmal caveolae were found (Oguchi and Tsukagoshi,
1980). The disposition of the openings to the extracellular space is similar to that seen in other vertebrates
(Rayns et al., 1968; Zampighi et al., 1975). Our findings
are summarized and illustrated in Figure 7.
conventionally prepared thin sections. The complex geometry of the SR, dependent on its relation to the plasma
membrane and different parts of the contractile apparatus, has been demonstrated. These results are summarized and illustrated in Figure 7.
Our investigations indicate that SR and T-tubules in
human skeletal muscle are structurally similar to what
has already been described in other mammalian muscles (Landon, 1982). The intermyofibrillar SR in human
skeletal muscle shows three regions with respect to the
adjacent myofibril pattern: 1)fenestrated collars overlying the M-band region, 2) terminal cisternae at the A-I
region, and 3) three-dimensionally anastomosed tubular
SR in the Z-band region. Longitudinally and/or transverse SR tubules connect these regions. We also fre-
DISCUSSION
We report the first successful application of the Golgi
method in the study of human skeletal muscle to demonstrate the three-dimensional architecture of the SR
and the T-system. Thick sections from the Golgi method
demonstrated good structural preservation and detail of
the SR and T-system that could not be appreciated in
282
K. HAYASHI. R.G. MILLER, AND A.K.W. BROWNELL
quently found short longitudinal connections between
ACKNOWLEDGMENTS
opposite terminal cisternae forming a triad, a s has been
reported in earlier studies (Peachey, 1965; Luff and AtSupported by the Alberta Heritage Foundation for
wood, 1971; Franzini-Armstrong, 1973; Rambourg and Medical Research and the Muscular Dystrophy AssociaSegretain, 19801, though rarely demonstrated in conven- tion of Canada.
tional thin sections of human skeletal muscle. Overall
LITERATURE CITED
our findings indicate that the SR in human skeletal
muscle forms a continuous network made up of repeat- Bailey, C.H., and L.D. Peachey (1975) The sarcoplasmic reticulum of
frog slow and twitch muscle fibers as revealed by stereoscopic high
ing units throughout the fiber length, in agreement
voltage electron microscopy. In: Annu. Proc. Electron. Microsc. Soc.
with a n earlier study (Revel, 1962).
Am., 33rd. C.H. Bailey, ed. Claitor’s, Baton Rouge, Louisiana, pp.
Although the overall morphology of intermyofibrillar
552-553.
SR in human skeletal muscle is generally similar to Eisenberg, B.R. (1983)Quantitative ultrastructure of mammalian skeletal muscle. In: Handbook of Physiology, Section 10, Skeletal Musthat in mammalian muscle, we noted, for example, 1)
cle. L.D. Peachey, R.H. Adrian, and S.R. Geiger, eds. Am. Physiol.
that the fenestrations at the A-I region described in the
Soc., Bethesda, MD, pp. 73-112.
mouse diaphragm muscle (Waugh et al., 1973) were not Forbes,
M.S., B.A. Plantholt, and N. Sperelakis (1977) Cytochemical
observed in human skeletal muscle and 2) that in rat
staining procedures selective for sarcotubular systems of muscle:
diaphragm muscle, the SR overlying the M-band region
Modifications and applications. J. Ultrastruct. Res., 6Ot306-327.
showed tubular anastomoses containing few fenestra- Forbes, M.S., and N. Sperelakis (1980) Membrane systems in skeletal
muscle of the lizard Anolis carolinensis. J. Ultrastruct. Res., 73:245tions (Rambourg and Segretain, 1980) while in human
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muscle and rabbit skeletal muscle (Yasumura and Franzini-Armstrong, C. (1973) Membranous systems in muscle fibers.
In: The Structure and Function of Muscle. Vol. 2. G.H. Bourne, ed.
Scales, 1981) SR contains fenestrated collars overlying
Academic Press, New York and London, pp. 532-619.
the M-band region. Furthermore, in our preparations, Franzini-Armstrong,
C., and L.D. Peachey (1982) A modified Golgi
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chem. Cytochem., 3Ot99-105.
Jorgensen, A.O., A.C.-Y. Shen, K.P. Campbell, and D.H. MacLennan
varied.
(1983) Ultrastructural localization of calsequestrin in rat skeletal
The elaborate network of subsarcolemmal SR found
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during this study has not been emphasized in previous
Cell Biol., 97,1573-1581.
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