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Mitochondrial size and shape in equine skeletal muscleA three-dimensional reconstruction study.

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THE ANATOMICAL RECORD 222:333-339 (1988)
Mitochondria1 Size and Shape in Equine Skeletal
Muscle: A Three-Dimensional Reconstruction Study
S.R. KAYAR, H. HOPPELER, L. MERMOD, ANDE.R.WEIBEL
Institute of Anatomy, University of Bern, CH3000 Bern, Switzerland
ABSTRACT
Individual mitochondria were reconstructed from ultrathin serial
sections of selected muscle fibers in the M. semitendinosus of a horse, over a length
of nearly two sarcomeres. Mitochondria were found to be highly variable, with size
and complexity of single mitochondria increasing with the fractional part of a fiber
occupied by mitochondria. In fibers with a mitochondrial volume density of less than
4%, corresponding to the mitochondrial content of fast-twitch glycolytic fibers, mitochondria were generally rather simple cylindrical shapes, oriented parallel to the
myofibrils. In fibers with a mitochondrial volume density of more than 7%, corresponding to the mitochondrial content of slow-oxidative or fast-oxidative glycolytic
fibers, mitochondria were generally cylindrical at the A-band and Z-plate level of
the muscle sarcomeres. However, these mitochondria often had transverse extensions or interconnections that occurred a t the I-band level. Volumes of individual
mitochondria ranged from as small a s a few thousandths of a pm3 up to several pm3
for the incompletely reconstructed portions of the largest mitochondria. Mitochondrial profiles that one would classify from single sections as subsarcolemmal were
found to interconnect with other profiles deeper within the fiber. This suggests that
it is unlikely that subsarcolemmal and interfibrillar mitochondria are two structurally distinct populations. However, we found no evidence of a reticulum completely
interlinking all mitochondrial material in a muscle fiber.
The three-dimensional shape and volume of individual
muscle mitochondria have recently become important in
estimating oxygen gradients in muscle cells (Clark and
Clark, 1985; Hoofd, 1987). This has spurred interest in
analyzing skeletal muscle mitochondria either by serial
section reconstruction (Bakeeva et al., 1978, 19811, by
high-voltage electron microscopy (Kirkwood et al., 1986,
1987), or by scanning electron microscopy (Ogata and
Yamasaki, 1985)to obtain such information. It has long
been considered by researchers (Gauthier and Padykula,
1966) that these mitochondria may be rather complex
and variable in shape, despite the common textbook
image of simple spheroids or sausages (Tzagoloff, 1982).
Indeed it has been suggested that in some muscles all
mitochondrial material is interlinked into a complex
reticulum (Bakeeva et al., 1978; Kirkwood et al., 1986).
The distinction between discrete, spheroidal mitochondria and a mitochondrial reticulum is important if one
considers that extensive branching and interlinkage of
mitochondria may be significant to intracellular transport of substances involved in cellular respiration.
In the present study we analyzed the structure of
mitochondria in four fibers of horse semitendinosus by
serial section reconstruction, over a distance of approximately 2 sarcomeres, to determine mitochondrial connectivity. Horse semitendinosus was selected as a muscle
well suited to this work. Since horses are highly aerobic
athletes, their muscles are particularly interesting to
analyze biochemically and ultrastructurally, and the
semitendinosus is considered to have a typical function
0 1988 ALAN R. LISS, INC
in hindlimb movement (Straub et al., 1983). The fiber
type composition (Hoppeler et al., 19831, myoglobin content (Kayar et al., 1988a), and activities of several key
metabolic enzymes (Essen-Gustavsson et al., 1983; Kayar
et al., 1988a) have all been well characterized in horse
semitendinosus. The average distribution of mitochondrial particles in cross sections of muscle fibers has also
been analyzed in this muscle (Kayar et al., 1988a). The
present study extends our information on muscle mitochondria to include the third dimension.
MATERIALS AND METHODS
Tissue Fixation
One horse (Equus caballus, gelding, body weight 516
kg) was sedated, anesthetized, and euthanized by cardiac arrest. Within less than 1 hour of death, the M.
semitendinosus of one leg was exposed, and the limb
was held in a position that fully extended this muscle.
Using a fine needle, 10 ml of a fixative solution (6.25%
glutaraldehyde in 0.01 M sodium cacodylate buffer, adjusted with NaCl to 1,100 mOsm, pH 7.4) were injected
into the superficial portion of this muscle over a n area
of approximately 3 x 1cm and a depth of 1.5 cm. After
10-15 minutes, the injection-fixed portion of muscle was
cut out, immersed in glutaraldehyde fixative, and furReceived January 22, 1988; accepted June 22, 1988.
Address reprint requests to S.R. Kayar, Institute of Anatomy, Uni.
versity of Bern, Biihlstrasse 26, CH3000 Bern, Switzerland.
334
S.R. KAYAR ET AL.
ther processed for electron microscopy as described in
detail elsewhere (Hoppeler et al., 1981; Mermod et al.,
1988). This procedure was followed to ensure that the
muscle fibers were fixed a t a n extended sarcomere
length.
Mitochondrial Reconstruction
From one tissue block of the semitendinosus, four individual muscle fibers were selected for analysis of the
size and three-dimensional shape of the mitochondria
within them. These four fibers were chosen because
their small size ( < 120 pm2 in cross-sectional area) permitted a n entire fiber profile to appear in one electron
micrograph of 16,000-20,000 final magnification. For
each fiber, 50-70 ultrathin (90-nm) serial sections, which
spanned 1complete sarcomere and all or part of a second
sarcomere (sarcomere length = 3.00 pm) were cut with
an LKB ultramicrotome. A series of eight to ten sections
was then cut a t 50-pm intervals, and another series of
eight to ten sections was cut at 200-pm intervals. The
serial reconstruction was performed using the following
computer system configuration: a microcomputer (DEC,
PDP-l1/23) with a terminal (DEC, VT220) and a color
graphic display (Barco, CD233), with the program
SSRCON (Perkins and Green, 1984). Mitochondrial volume density in each of these fibers was calculated in a
subsample of 25 micrographs of all the serial sections.
The injection fixation technique, which we employed
to fix muscles a t an extended sarcomere length, rendered it impossible to perform definitive fiber typing;
this requires fresh-frozen tissue (Hoppeler et al., 1983).
However, in horse semitendinosus it has been demonstrated that there is a distinction between the mitochondrial volume density of type IIb fast glycolytic fibers,
versus the type I slow-oxidative and type IIa fast-oxidative glycolytic fibers. The type IIb fibers have mitochondrial volume densities of 1-5%, whereas the type I and
IIa fibers have mitochondrial volume densities from 5%
to more than 8%. There is no significant difference in
the mitochondrial content of type I and IIb fibers. Thus
while we cannot unequivocally demonstrate the histochemical types of fibers analyzed in this study, the range
of mitochondrial volume densities in the selected fibers
makes it probable that two were type IIb and two were
either type I or IIa.
RESULTS
The four individual fibers of semitendinosus selected
for three-dimensional reconstruction were of very small
cross-sectional area [a(f); Table 11, to make it practical
to reconstruct all the mitochondrial profiles found in the
serial sections. These fibers were also selected to span a
range of mitochondrial volume density [Vv(mt,fl;Table
11 from less than 2% to 996, and therefore to include at
least two fiber types (Hoppeler et al., 1983).
An electron micrograph of one section of fiber A appears in Figure l a , along with the fiber and mitochondrial profiles outlined for the serial reconstruction (Fig.
lb). This is probably either a type I or 1Ia fiber, given its
high volume density of mitochondria. Individual mitochondrial profiles appear to be either circular or relatively simple elongate ovoids. When this fiber was
reconstructed from 50 serial sections (spanning a vertical distance of 4.5 pm), a general cross-sectional view
shows many interconnections between the mitochon-
TABLE 1. Mean fiber cross-sectional area [a(D] and volume
density of mitochondria [V,(mt,D] in four selected fibers of
horse M. semitendinosus
Fiber
A
B
C
D
am
(urn2)
V,(mt,D
120 + 8
51 + _ 4
88 +_ 3
74 + 7
9.03 k 0.53
7.91 +_ 0.29
1.74 k 0.23
3.42 + 0.37
(5%)
drial profiles (Fig. lc). Two mitochondria in this fiber
have been selected for detailed reconstruction (Figs. Id
and 2). The first mitochondrion (Fig. 2a) is located near
the sarcolemma. In its lowest portion, which corresponds
to the A-band level of the muscle sarcomere, it consists
of unbranched cylinders. Farther up, corresponding to
the I-band level of the muscle, transverse connections
between cylinders can be seen not only along the sarcolemma, but also deeper into the fiber. Note the brief
interruption in the horizontal connections, which occurs
at the Z-disk level. At the top of the figure, corresponding to the next A-band of the muscle, the mitochondrion
returns to its cylindrical pattern. All profiles in Figure
2a appear interconnected and can be assumed to extend
beyond the upper and lower bounds of the series of
sections. The volume of the mitochondrion that is included in these sections is 6.73 pm3, with a n unknown
additional volume beyond the serial sections. It is particularly noteworthy in this reconstruction that a number
of mitochondrial profiles that would be counted as subsarcolemmal mitochondria are connected to what would
appear on single cross sections to be interfibrillar
mitochondria.
The second mitochondrion reconstructed from fiber A
(Fig. 2b) is strictly interfibrillar. The sarcomeres in this
fiber, a s expected (Peachey and Eisenberg, 19781, were
staggered across the fiber profile. Thus the second reconstruction happens to include I-bands in the upper and
lower portions of the figure, whereas the first mitochondrion (Fig. 2a) includes a n I-band in the center of the
reconstruction. Just as in the preceding mitochondrion,
a t the I-band level of the muscle there is extensive
transverse branching, with a short interruption in the
branching at the Z-disk. When it reaches the A-band
level, the network separates and forms cylindrical columns running parallel to the muscle fiber axis. The
estimated volume of the reconstructed portion of this
mitochondrion is 2.70 pm3.
Fig. 1 , Fiber A, horse M. semitendinosus. a: Electron micrograph of
a single ultrathin (90 nm) section. b: Profiles of fiber and mitochondrial
particles from this section, for computer reconstruction. Profiles marked
in red and blue are shown reconstructed in subsequent figures. c:
Computer reconstruction of 50 ultrathin serial sections (4.5 p m ) , viewed
from above. All mitochondrial profiles shown in red or blue are interconnected with each other. Outlined in white are all other mitochondria] profiles on the first and every tenth section. d: Same computer
reconstruction, viewed from a -60" rotation of the x axis.
336
S.R. KAYAR ET AL.
In fiber B (Fig. 3a), a general cross-sectional view
shows fewer transverse connections than in fiber A, and
mitochondrial volume density is slightly lower (Table 1).
It is probably a type I or IIa fiber (Hoppeler et al., 1983).
Two mitochondria, one subsarcolemmal and one interfibrillar, are shown reconstructed from 66 serial sections
(a vertical span of 6 pm; Fig. 3b). The subsarcolemmal
mitochondrion is a simple cylinder, with only a slight
enlargement a t the level of the I-band. The volume of
the portion illustrated is 0.361 pm3, but this mitochondrion presumably extends beyond the upper and lower
planes of sectioning. The interfibrillar mitochondrion is
composed of two cylindrical portions that are parallel to
the fiber axis in the A-band regions of the muscle. They
are interconnected in the center of the figure a t the level
of the I-bands within the muscle by two transverse portions, one otcurring just above and the other just below
the Z-disk. There is another transverse interconnection
at the top of the diagram, corresponding to the next Iband region. The volume included within these sections
is 1.56 pm3.
Fibers C and D have a very low mitochondrial content
(Table 1)and are therefore probably type IIb fibers (Hoppeler et al., 1983). There are very few connections between mitochondria in these fibers. In fiber C (Fig. 4),
approximately 30 individual mitochondria were identified from the reconstruction of 61 serial sections (vertical
span of 5.5 pm). Most of them appear as cylinders of
varying diameter, some of which begin andlor end within
the section series. Only eight mitochondria show transverse linkages, which occur invariably a t the level of
the I-band. For the single mitochondrion that begins and
ends within these sections, the estimated volume is 0.183
pm3. In fiber D, while individual sections show numerous small mitochondrial profiles as usual (Fig. 5a), there
were only ten mitochondria that actually began and
ended within the reconstruction of 61 sections (5.5 pm
vertical span; Fig. 5b). Volumes of these discrete mitochondria were between 0.004 and 0.083 pm3.
DISCUSSION
Skeletal muscle mitochondria seem to be functionally
similar among a wide variety of mammalian species and
muscles (Hoppeler et al., 1981).Biochemical studies have
indicated that the respiratory complexes and ATP synthetase enzymes are integrated in the mitochondrial
inner membrane a t a density set by the crystalline dimensions of the enzyme molecules and the concentration of lipid in the membranes (Tzagoloff, 1982). The
respiratory capacity of the mitochondria should therefore be. set by the surface density of the inner membranes. Morphometric analysis of mitochondria from a
variety of mammalian muscles has shown that this density of membranes is approximately constant (Hoppeler
et al., 1981). While horses have a high maximal oxygen
consumption rate during exercise, this rate can be accounted for by the high total volume of mitochondria in
the muscles (Kayar et al., 198813). Thus we expect that
this study of mitochondrial structure in horse muscle
will be applicable to other mammalian muscles as well.
Our primary finding in this study is that mitochondrial size and shape are far more variable and complex
than present models of muscle energetics allow. Despite
the variabilitv. there are some consistent features of
mitochondrial" shape relative to the muscle sarcomeres
adjacent to them; despite the complexity, discrete mitochondria can be found. In particular, we found that the
mitochondrial material in the muscle fibers we analyzed
did not exist as a continuous mitochondrial reticulum,
but that the degree of mitochondrial connectivity appeared to be related to mitochondrial volume density.
By using serial section reconstruction, we were able to
estimate the volume of individual mitochondria.
The conventional view of muscle mitochondrial structure is that they are discrete spheres or ellipsoids. Such
a view is easily reinforced by examining single micrographs of muscle in transverse or longitudinal section,
where circular and ovoid profiles are common. However,
in the muscle fibers examined in our study, only one
roughly spheroid mitochondrion was found (fiber D, Fig.
51, with a volume (0.004 pm3) the smallest of all those
we measured. At low volume density, i.e., low fractional
part of a fiber occupied by mitochondria, most mitochondria were discrete, unbranched cylindrical bodies, oriented parallel to the muscle fibers. As volume density
increased, many mitochondria became larger and more
complex in shape, with cylindrical portions a t the Aband and Z-disk levels of the sarcomeres, which intricately interconnected transversely at the I-band level of
the muscle.
Many studies of mitochondria in muscle cross sections
have noted that there are large accumulations of mitochondrial particles immediately beneath the sarcolemma. In some experiments, as for example with
endurance exercise training, it can be demonstrated that
there are greater changes in the volume density of these
subsarcolemmal mitochondria than in the mitochondrial profiles deeper within the fiber (Hoppeler, 1986).
However, in our reconstructions we found that in a fiber
with relatively high mitochondrial volume density, there
are numerous connections between mitochondrial particles that one would classify from single micrographs as
subsarcolemmal or interfibrillar (Fig. 1). A similar observation was made by Kirkwood et al. (1986, 1987) in
rat muscle. It does not seem to be justified on structural
grounds to divide mitochondria into two truly separate
populations, subsarcolemmal and interfibrillar, if their
outer membranes and hence presumably their inner
membranes and matrix space are continuous (Matlib et
al., 1981).
Mitochondria1 reticula in muscle have been described
previously. However, we did not find any evidence of a
continuous reticulum linking all mitochondrial material, as described by Bakeeva et al. (1978, 1981) and
Kirkwood et al. (1986, 1987) in rat muscle. The latter
group has suggested that mitochondria that appear to
be discrete particles within a limited range of sections
are in fact interconnected with the reticulum in another
plane. This does not appear to be the case in the muscle
fibers analyzed in our study, since in the fibers with low
mitochondrial volume density we found individual mitochondria that definitely began and terminated within
less than 2 sarcomeres. In the fibers with high mitochondrial volume density and branching mitochondria, these
did not all interconnect within the fiber portion reconstructed. There is little reason to think that these complex mitochondria are completely interconnected with
each other beyond the reconstructed region, since further sectioning of the same fibers from 50 pm up to
2,000 pm beyond the original region shows virtually
identical mitochondrial locations. One reason for the
different observations of our studv versus those of Bakeeva et al. (1978) and Kirkwoo$ et al. (1986) may be
that the horse muscle fibers of our study had a relatively
MITOCHONDRIAL SIZE AND SHAPE
337
Fig. 2. Detailed reconstruction of two portions of mitochondria as
viewed from 50 ultrathin serial sections of fiber A, horse M. semitendinosus. a: Primarily subsarcolemmal mitochondrion (also shown in
red in Fig. 1).b: Interfibrillar mitochondrion (also shown in blue in
Fig. 1).All profiles that appeared interconnected to those shown in
color in Figure l b are included in the illustrations, but both mitochondria extend beyond the first and last sections of this series. Approximate locations of the Z-band in the muscle sarcomeres are indicated
by the white arrows.
Fig. 3. Fiber B, horse M. semitendinosus. a: Overview of 66 ultrathin
serial sections (6 pm). Marked in green and yellow are two portions of
mitochondria selected for detailed reconstruction. Outlined in white
are the profiles of all other mitochondrial particles on the first and
every tenth section. b: Same reconstruction, viewed from a -60" rotation of the x axis. Green and yellow mitochondria illustrate all profiles
appearing interconnected to each other within these sections, but both
mitochondria extend beyond the first and last sections of this,series.
Outlined in white are all other mitochondrial profiles in the topmost
section. White arrows indicate approximate locations of Z-bands in the
muscle sarcomeres.
Fig. 4. Fiber C , horse M. semitendinosus. Reconstruction of 61 ultra- within these sections, only one (illustrated in red near the center of
thin serial sections (5.5 Gm), viewed from a -60" rotation of the x axis. the fiber) began and ended within this fiber volume.
Of the approximately 30 discrete portions of mitochondria appearing
338
S.R. KAYAR ET AL.
Fig. 5. Fiber D, horse M. semitendinosus. a: Single sections, numbers
1and 60, viewed from a -60" rotation of the x axis. All mitochondria1
profiles on these two sections are outlined. b: Reconstruction of 61
ultrathin serial sections (5.5 pni) viewed from a -60" rotation of the x
axis. Only the mitochondria that began and ended within this tissue
volume are illustrated. Note the yellow profile in the upper right
corner of the fiber, appearing on only one tissue section. It is the only
mitochondrion identified in this study that appears to have a spherical
form.
low volume density of mitochondria compared with rat
muscles. Bakeeva et al. (1978) have reported that in the
ontogeny of the diaphragm in rat, embryonic rats have
discrete mitochondria that merge into a continuous reticulum within the first 2 postnatal months as mitochondrial volume density increases. Mitochondrial volume
density in an adult rat diaphragm is reported to be
roughly 20% (Hoppeler et al., 1981). For comparison,
human skeletal muscle fibers are generally on the order
of 2 4 % mitochondria (Hoppeler, 1986).
One serious limitation to any structural study of mitochondria by three-dimensional reconstruction is that
the resolution is set by the thickness of the tissue sections. Mitochondrial projections that are vertically
aligned and approach each other within the plane of
sectioning may be incorrectly viewed as being continuous if the distance between their outer membranes is
less than the section thickness. Our sections were - 90
nm; those of Bakeeva et al. (1978,1981) were 60-70 nm,
and those of Kirkwood et al. (1986) were 500 nm. Technical limitations make it difficult to cut serial muscle
sections significantly thinner than 60-70 nm. On the
other hand, morphometry of particles the size of mitochondria is not possible €or sections of several hundred
339
MITOCHONDRIAL SIZE AND SHAPE
nm thickness because of overprojection (Weibel, 1979).
The effect of overprojection of irregularly shaped particles in thicksections is readily apparent in a n overview
such as in Figure lc, spanning 4,500 nm, or 50 thin
sections, compared with a single thin section (Fig. la,b).
The “thick section” view gives a n impression of mitochondrial content that is fallaciously high and cannot
be corrected. Examination of these figures also makes
clear the futility of trying to count mitochondrial number or size from individual sections, regardless of section
thickness.
There is a difference in the interpretation of the structural findings of Kirkwood et al. (1986) versus those of
our study, which is important for considering substrate
fluxes within muscle fibers. Our reconstructions show
that the primary axis of interconnections within mitochondria is parallel to muscle fibers and capillaries,
with a lesser degree of interconnections radially from
capillaries, whereas Kirkwood et al. (1986, Fig. 5) report
the contrary. It has been hypothesized (Longmuir, 1981)
that oxygen, given its 8 times greater solubility in lipids
than in cytosol, will diffuse through a cell more rapidly
by following a biological membrane than by traveling
freely through the cytosol. If mitochondria are completely transversely interconnected, one could envision
this as facilitating transport of oxygen and perhaps other
metabolically important substances radially from capillaries to mitochondria throughout the fiber (Kirkwood
et al., 1986). If mitochondria are relatively little interconnected transversely, it is not clear what effect longitudinal interconnections of mitochondria would have on
substrate flux.
The complexity and variability of mitochondrial shape
and size within a single muscle fiber suggests a definite
word of caution to modelers of oxygen transport to tissues: individual muscle mitochondria can differ in volume by at least three orders of magnitude. Any model
that is highly sensitive to this parameter must bracket
a n enormous range. A model that requires only mitochondrial volume density or total mitochondrial volume
in a muscle and average radial distribution will be subject to far smaller variance. A recent study in human
muscle (Kawai et al., 1987) has offered the provocative
observation that myoglobin is present in I-bands but not
A-bands, and seems to have a n affinity for mitochondrial outer membranes. The localization of myoglobin in
regions of muscle with relatively high concentrations of
mitochondria could seriously affect the modeling of oxygen transport in muscle. Thus we need more information, particularly including a quantitative estimate of
mitochondrial connectivity, before it is possible to construct a comprehensive model for cellular level aerobic
respiration.
ACKNOWLEDGMENTS
The animal used in this study was from a series of
experiments performed in the Department of Veterinary
Medicine of the Swedish School of Agricultural Sciences,
Uppsala, Sweden. We thank their faculty and staff for
support and facilities. We are especially grateful for the
excellent technical assistance of Ms. H. Claassen and
Mr. M. Diezi. This work was supported by Swiss National Science Foundation Grant 3.036.84.
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