SKELETAL MUSCLE MUSCLE STRUCTURE
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1 11 SKELETAL MUSCLE The goal of the material in this chapter is to provide a very brief introduction to skeletal muscle, its structure, and its electrophysiological and contractile properties MUSCLE STRUCTURE A whole muscle can be divided into separate bundles. Each bundle contains many individual fibers. The fiber is the basic (smallest) functional unit (it constitutes a single cell). It is bounded by a plasma membrane and a thin sheet of connective tissue, the endomysium. The bundles are also surrounded by a connective tissue sheet, the perimysium, which delineates specific fascicles. The whole muscle is encased in its connective tissue sheet, namely, the epimysium. Most skeletal muscles begin and end in tendons. Muscle fibers lie parallel to each other, so the force of contraction contributed by each is additive. The general features noted above are illustrated in Figure In this chapter attention will be primarily directed to the electromechanical properties of the single muscle fiber. Each muscle fiber is made up of many fibrils, each of which, in turn, is divisible into individual filaments. The filaments are composed of contractile proteins, essentially myosin, actin, tropomyosin, and troponin. Mature fibers may be as long as the muscle of which they are a part (tens of centimeters); they vary in diameter from 10 to 100 μm. As noted above, each fiber contains myofibrils, which are proteins and which lie in the cytoplasm. The cytoplasm also contains mitochondria, the SR and T systems, plus glycogen granules. When examined under light microscopy (LM), the myofilaments show characteristic cross-striations (banding), which are in register in all myofilaments (see Figure 11.1.) It is the latter property from which skeletal muscle derives the alternate name of striated (muscle). The overall physical features of a muscle fiber are shown in Figure This shows the dense packing of myofibrils, the transverse tubular system (TTS), and the sarcoplasm reticulum 341
2 342 CH. 11: SKELETAL MUSCLE Figure Structure of a Whole Muscle and Its Components. The cross-striations are visible under light microscopy. From Keynes RD, Aidley DL Nerve and muscle. Cambridge: Cambridge UP. Based on Schmidt-Nielsen K Animal physiology. Cambridge: Cambridge UP. Reprinted with the permission of Cambridge University Press. (SR). Both the bounding membrane and the TTS membrane are excitable and play an important part in the process whereby contraction is initiated MUSCLE CONTRACTION Each mammalian muscle fiber is contacted by a single nerve terminal. The muscle fiber is known as a twitch fiber, since the response to a single nerve stimulus is a twitch. The time to reach the peak of a typical twitch contraction is around 200 msec, while recovery requires an additional 600 msec. In normal activity a muscle will shorten as it develops force (tension). However, experiments are often carried out under conditions of constant muscle length (isometric) as well as under conditions of constant muscle load (isotonic). To study behavior under isometric conditions, a transducer is needed that converts force into an electrical signal while itself undergoing very little deflection. If a second stimulus is applied before the effect of the previous twitch has ended, then the second (twitch) response will build on the residual of the first and summation results. Corresponding to a long inter-stimulus interval, a bumpy response is seen. For increasing stimulus frequency, a value will be reached where the bumps disappear and a smooth buildup to a maximum steady level results, as illustrated in Figure The frequency is known as the fusion frequency, and the muscle is said to be in tetanus. The peak twitch tension to the maximum tetanus tension is the twitch/tetanus ratio, which is about 0.2 for mammalian muscle.
3 BIOELECTRICITY: A QUANTITATIVE APPROACH 343 Figure Magnified View of the Structure of a Single Muscle Fiber, with a cutaway view of the myofibrillar structure. Each fibril is surrounded by a sarcoplasmic reticulum (SR) and by the transverse tubules system (TTS), which opens to the exterior of the fiber. From Krstic RV Ultrastructure of the mammalian cell. Berlin: Springer-Verlag, with permission.
4 344 CH. 11: SKELETAL MUSCLE Figure Tension versus Time for a Single Stimulus (twitch response) and for a train of stimuli of increasing frequency b, c, d. From Keynes RD, Aidley DJ Nerve and muscle. Cambridge: Cambridge UP. Reprinted with the permission of Cambridge University Press. Mammalian muscle can be classified into fast glycolytic or type II fibers, and slow oxidative or type I muscle. 2 Fast (white) fibers contract and relax much more rapidly than slow (red) ones. The former are found where rapid movement is encountered (e.g., muscles involved in fast running and jumping), while the slow muscle is more involved in, for example, long-distance running or postural movement. The characteristics of the fast muscle include (1) larger diameter fibers, (2) greater developed tension, (3) mainly dependent on glycolytic and less on oxidative metabolism, (4) contractions of short duration, and (5) muscle fatigues rapidly and recovers slowly. Distinguishing the slow muscle is (1) a smaller diameter fiber, (2) lower tension, (3) primarily oxidative metabolism (hence more extensive vasculature and mitochondria), (4) long-duration twitch, and (5) fatigues slowly and recovers quickly. All muscles are actually some combination of the fast and slow muscle, each having their own particular characteristics. The length tension relation of skeletal muscle is illustrated in Figure Under isometric conditions, the total active (tetanus) tension depends on the (fixed) length of the fiber according to the plotted data. A passive tension is required to extend the muscle beyond its resting length (mainly because of the need to stretch the connective tissue associated with the muscle). The passive tension is measured on the muscle in the absence of stimulation. The difference between the total active tension and the passive tension is a measure of the contractile force derived from stimulation and is called the active increment. The latter quantity reaches a maximum at the resting length and is lower for either greater or lesser lengths. An explanation of this behavior is given in a subsequent section.
5 BIOELECTRICITY: A QUANTITATIVE APPROACH 345 Figure Length Tension Relationship for a Skeletal Muscle under Isometric Conditions. From Keynes RD, Aidley DJ Nerve and muscle. Cambridge: Cambridge UP. Reprinted with the permission of Cambridge University Press Structure of the Myofibril Each fiber contains a large number of cylindrical (protein) constituents called myofibrils. The banded structure seen for the fiber as a whole is, in fact, a consequence of the Saffie banding and alignment of the individual fibrils. The banding corresponds to the structure of the protein components of the myofibril, namely, the thick and thin filaments. The thick filaments are around 11 nanometers in diameter, while the thin filaments are around 5 nm in diameter. The arrangement of these filaments is shown in Figure 11.5a, where it is seen that in the crosssection they are interdigitated in a hexagonal array, while along the axis they lie in a recurring pattern of overlapping and non overlapping regions. When viewed lengthwise, the banding effect arises from the relative amounts of transmitted light permitted by the thick and thin filaments. In Figure 11.6 we show both the structural organization of the thin and thick filaments and the associated banding that would be observed in the LM. The two main bands are the dark A band and the lighter I band. The bands alternate regularly along the myofibril. In the middle of the I band is the Z line (dark line), while the middle of the A band has a lighter region, the H zone. The H zone is bisected by a darker M line surrounded by a lighter region, the L zone (not always seen). The repeating unit (Z Z distance) is the sarcomere. These characteristic bands of different light intensity derive from the underlying thin and thick filament structure, the major elements of which can be recognized in Figure The dark A band arises from the overlapping thin and thick filaments, while the lighter H zone reflects the presence of thick filaments alone. The M line and L zone derive from the structural details of the thick filament at its center, the M line from crosslinks at the center.
6 346 CH. 11: SKELETAL MUSCLE Figure Axial and Cross-Sectional View of a Portion of the Array of Thin and Thick Filaments that constitutes a single fibril. The cross-section at (a) registers the presence of both thin and thick filaments, while that at (b) thick filaments only, and at (c) thin filaments only. From Aidley DJ The physiology of excitable cells. Cambridge: Cambridge UP. Reprinted with the permission of Cambridge University Press. The L zone is due to the absence of projections on either side of the thick filament (to be described later); the L zone is around 0.15 μm in width. The Z line reflects the interconnection of the I filaments from the region to its left and its right. The above letters are derived from the German and reflect certain properties of their designated regions. They are A = anisotropic (polarizes light), I = isotropic, Z = zwischenscheibe, H = Henrens disc, and M = mittlemembrane The thick filament is made up of myosin, a complex protein. Trypsin splits it into light meromyosin (LMM) and heavy meromyosin (HMM). The latter has a short tail and two globular heads; it has an ATPase behavior (i.e., it hydrolyzes ATP into ADP + P with the release of large amounts of energy). The light meromyosin is rod-like and does not split ATP. The thin filament is actin, which is also a protein. There are two forms, but neither has ATPase behavior. (The important ATPase activity is actually confined only to the globular sub fragments.) The LMM and the tail of the HMM are composed of two α-helices that coil around each other. When combined in a solution, the actin and myosin form a complex called actomyosin (a quite viscous material). A description of the myosin structure is given in Figure Glycerol-extracted fibers are prepared by soaking muscle fibers in 50% glycerol for several weeks, a process that removes most sarcoplasmic material except for the contractile elements. The fibers are found to be in rigor (they are stiff and resist contraction, a result of the formation
7 BIOELECTRICITY: A QUANTITATIVE APPROACH 347 Figure Myofibrillar Structure and Associated Pattern Seen in a Light Microscope. The banding nomenclature is given. The observed pattern of light intensity in (a) can be explained by the underlying structure shown in (b). From Keynes RD, Aidley J Nerve and muscle. Cambridge University Press. (a) is based on a photograph by Dr. HE Huxley. Reprinted with the permission of Cambridge University Press. Figure Different Components of the Myosin Molecule. Proteolytic enzymes cleave the molecule into heavy meromyosin (HMM) and light meromyosin (LMM). The HMM comprises a short segment of the α-helical rod (S2) and the two globular heads (S1), to which the light chains are attached. The globular heads form the cross-bridges. Reprinted by permission from McComasAJ Skeletal muscle, Champaign, IL: Human Kinetics. Based on Vibert P, Cohen C Domains, motions, and regulation in the myosin head. J Muscle Res Cell Motility 9: , and Rayment I, et al Structure of the actin myosin complex and its implications for muscle contraction. Science 261: of cross-bridges between the actin and myosin). If ATP and magnesium are added, the fibers become readily extensible due to the breakage of crosslinks by the ATP. If Ca ++ is also added, then contraction takes place. In the transverse plane, the relative positions of the thin and thick filaments in a region of overlap is as illustrated in Figure One notes that each thick filament is surrounded by six thin filaments, while each thin filament is surrounded by three thick ones. Hence, there are twice as many thin as thick filaments.
8 348 CH. 11: SKELETAL MUSCLE Figure Transverse Plane View of the Thin and Thick Filament Structure in an axial plane in which they overlap (see Figure 11.6). In the ultrastructural studies of the myosin (thick) filament, one finds the occurrence of projection pairs at a regular interval of 14.3 nm; however, successive pairs are found to be rotated by 120. Consequently, when established, cross-bridges are then 14.3 nm apart, while an identical repetition occurs every 43 nm. An illustration of this is given in Figure 11.9a. One can derive the thick filament structure from an aggregation of myosin molecules, as illustrated in Figure Each projection is identified as a globular head pair of the myosin molecule. Note the necessarily projection-free region in the center, which is the explanation for the observed L zone. Note also the reversed orientation of molecules on either side of the center SLIDING FILAMENT THEORY The idea that muscular contraction is a consequence of the contraction of protein units patterned after that of a helical spring had to be abandoned when measurements revealed that the A band does not change length during contraction or lengthening. In fact, in frog muscle, as the sarcomere length is varied from 2.2 to 3.8 μm, the I filaments remain essentially at 2.05 μm in length and the A filaments at around 1.6 μm. (The Z line is 0.05 μm wide, and each side of the I filament has a length of 1.0 μm, to account for the total of 2.05 μm.) As a consequence of the above, the sliding-filament model was advanced. According to this idea, contraction involves the relative movement of the thin and thick filaments, as illustrated in Figure 11.11, where contraction yields a reduced sarcomere length while the filaments are unchanged in length.
9 BIOELECTRICITY: A QUANTITATIVE APPROACH 349 Figure Models of the Structure of the Thick and Thin Filaments: (a) myosin; (b) F- actin; (c) thin filament. In (a) the two globular heads of myosin, which split ATP, are shown (a more detailed view is given in Figure 11.11). From Keynes RD, Aidley DJ Nerve and muscle. Cambridge: Cambridge UP. Reprinted with the permission of Cambridge University Press. Based on Offer G The molecular basis of muscular contraction. In Companion to biochemistry, Ed AT Bull et al. London: Longman; Huxley HE, Brown W The low angle x-ray diagram of vertebrate striated muscle and its behavior during contraction and rigor. J Mol Biol 30: ; and Huxley HE Molecular basis of contraction in cross-striated muscles. In Structure and function of muscle, 2nd ed., pp Ed GH Bourne. New York: Academic Press. Figure Huxley s Suggestion as to How Myosin Molecules Aggregate to Form a Thick Filament. See also Figure 11.2 for details of myosin structure. From Huxley HE The structural basis of molecular contraction. Proc R Soc 178: Redrawn in Aidley DJ The physiology of excitable cells. Cambridge: Cambridge UP. The sliding itself is thought to be produced by reactions between the projections on the myosin filaments and active sites on the thin filament. Each projection first attaches itself to the actin filament to form a cross-bridge, then pulls on it, causing the sliding of the actin, then releases it, and finally moves to attach to another site which is further along the thin filament. The sliding filament theory is generally (though not universally) accepted. Accordingly, one expects isometric tension to depend on the degree of overlap in the thin and thick filaments. This
10 350 CH. 11: SKELETAL MUSCLE Figure This figure illustrates the sliding-filament model: (a) the muscle is elongated; (b) the muscle is contracted. In each case the lengths of the thick and thin filaments are unchanged. Figure Isometric Tension of a Frog Muscle Fiber, measured as a percentage of its maximum value at different sarcomere lengths. The numbers 1 6 refer to the myofilament positions illustrated in Figure Note that the general shape is anticipated in Figure From Gordon AM, Huxley AF, Julian FJ The variation in isometric tension with sarcomere length in vertebrate muscle fibers. J Physiol 184: Redrawn by Aidley DJ The physiology of excitable cells. Cambridge: Cambridge UP. result is supported by the study illustrated in Figures and and can be understood in the following discussion. Stage 1 (in Figures and 11.13) refers to full extension of the myofibril. Using the dimensions given above for the thin and thick filament lengths, the sarcomere length is
11 BIOELECTRICITY: A QUANTITATIVE APPROACH 351 Figure Myofilament Arrangements at Different Lengths. The numbers are the positions corresponding to the curve given in Figure a = thick filament length (1.6 μm); b = thin filament length including z line (2.05 μm); c = thick filament region base of projections (0.15 μm); and z = z line width (0.05 μm). From Gordon AM, Huxley AF, Julian FJ The variation in isometric tension with sarcomere length in vertebrate muscle fibers. J Physiol 184: Redrawn in Aidley DJ The physiology of excitable cells. Cambridge: Cambridge UP = 3.65 μm, which is the sum of the length of the thin plus thick filament. There can be no cross-bridges and the observed zero tension is explained on this account. As the myofibril shortens so that the sarcomere diminishes from 3.6 to μm (stage 2), the number of cross-bridges increases linearly with decreasing length. Therefore, the isometric tension should show a similar increase. In fact, such an increase in tension with decreased length is seen in Figure This linear behavior ends at stage 2, when the Z Z distance equals 2.05 μm plus the L zone width ( 0.15 μm), or 2.20 μm. With further shortening, the number of cross-bridges remains unchanged and a plateau in tension is both expected and observed. Stage 3 is reached when the thin filaments touch. The sarcomere equals the length of the thin filament, namely, 2.05 μm at this point. From stage 3 to stage 4 one anticipates some internal resistance to shortening to develop, since actin filaments now overlap. Beyond stage 4 this overlap not only constitutes a frictional impediment, but it also interferes with cross-bridge formation. When stage 5 (1.65 μm) is reached, the myosin filaments hit the Z line and a further increase in resistance is associated with the deformation that results beyond this point.
12 352 CH. 11: SKELETAL MUSCLE Figure Interaction of Actin and Myosin on a Molecular Level. From Huxley HE The structural basis for contraction and regulation in skeletal muscle. In Molecular basis of motility. Ed LMG Heilmeyer et al. Berlin: Springer. The curve in Figure shows a break point at stage 5 and a rapid decrease in tension with further shortening. Zero tension is reached at a sarcomere length of 1.3 μm, which designates stage 6. The actin structure is described in Figure 11.9b,c and in Figure as a double helix involving chains of monomers. The thin filament is made up of actin, troponin, and tropomyosin, as shown in Figure 11.9c. The thick filament is shown in Figure as containing an S 2 filament subunit and the S 1 (globular head) subunits. The S 1 subunits can rotate about their point of attachment with S 2. Together, S 1 and S 2 make up the heavy meromyosin (HMM) portion of the myosin molecule; the remainder of the molecule is filamentary and constitutes the light meromyosin (LMM) (see Figure 11.7). Sliding is accomplished by the rotation of S 1 about S 2, as noted earlier. In the upper portion of Figure 11.14, the left-hand cross-bridge has just attached while the S 1 subunit of the right-hand one has nearly completed its rotation. The lower diagram, which illustrates conditions a moment later, shows the S 1 subunit on the left-hand cross-bridge having rotated to cause the actin filament to slide leftward; the right-hand cross-bridge is now separated.
13 BIOELECTRICITY: A QUANTITATIVE APPROACH 353 There are two S 1 cross-bridges for each myosin molecule, and each cross-bridge is relatively independent of the other, though each behaves as described here. The biochemical events associated with these mechanical events can be described according to the following sequence: 1. Myosin is released from a cross-bridge with actin. This results from the action of ATP with which the myosin combines. That is, where A actin and M myosin). AM + ATP A+M ATP 2. ATP is split into ADP + P, while the myosin (S 2 ) repositions for reattachment with the thin filament. The products remain attached to the myosin, which now has a high affinity for actin. 3. Myosin cross-bridges attach to a new actin monomer. 4. This results in products being released and the energy so derived utilized as the power stroke (rotation of S 2 and linear movement of actin). At this point, return to step 1. While actin will react with pure myosin so as to split ATP in the absence of calcium ions, when tropomyosin and troponin are also present, calcium ions are required. In the case of muscle, the tropomyosin and troponin are, in fact, always present and appear to exert a regulatory (control) role EXCITATION CONTRACTION The details of the process, starting with propagation of an action potential along a muscle fiber and ending with contraction of the target muscle, can now be examined. The possibility that the influx of calcium ions, associated with the membrane depolarization, is the primary initiator of the contractile mechanism has to be discarded since only about a 0.2 picomole Ca ++ /cm 2 influx is observed (frog sartorius). This amount corresponds to an increase in internal calcium ion concentration of only 0.08 μmole (assuming a fiber diameter of 50 μm). To better understand contemporary ideas, one must include the presence of the sarcoplasmic reticulum (SR) and the transverse tubular system (TTS). The T-system lies transverse to the fiber axis and consists of tubules that are open to the extracellular space and form a meshwork shaped somewhat as the spokes of a wheel (described in Figure 11.2). The TTSs are located at the Z lines of frog muscle and the A I boundary in most other striated muscle. The SR is in close proximity to the T-system but extends in the axial direction, mainly. It constitutes a network of vesicular elements surrounding the myofibrils. It is not directly connected to the TTS and is otherwise isolated from extracellular space. Excitation propagating along the surface membrane of the muscle fiber passes the outside opening of each of the many T-tubules. It is believed that this excitation can propagate inward,
14 354 CH. 11: SKELETAL MUSCLE that the membranes defining the T-tubules are excitable in the usual way. The inward speed of conduction has, in fact, been measured and is about 7 cm/sec (in a fiber 100 μm in diameter a latency of 0.7 msec from outside to inside would consequently be observed). The SR, while not continuous with the TTS, in places, is in close proximity via a structure called feet. The SR sequesters Ca ++ (which is pumped into the SR vesicles by an ATP-driven calcium pump). This sequestration can reduce the calcium ion concentration in the muscle to a point below that necessary for contraction (i.e., it results in the relaxation of the muscle). Then activation results from the action potential propagating throughout the TTS, which in turn results in a movement of ions to open the calcium channels in the SR membrane. This results in a release of Ca ++ from the SR into the myoplasm. The consequent contractile process then arises as described earlier. We assumed in the above that in the presence of tropomyosin and troponin Ca ++ is required for ATP to be split. The tropomyosin and troponin appear, in fact, to be a structural component of the thin filament, as described in Figure 11.9c. The tropomyosin in the resting muscle is positioned to prevent the myosin heads combining with the actin monomers, but it can be moved out of the way by a conformational change in the troponin complex when calcium binds to troponin C NOTES 1. The interested reader can find further information in [1, 2, 3]. These works were the primary sources for the material of this chapter. 2. A continuum of fiber types actually exists and this classification describes those at each end of this spectrum. Other classification schemes have been proposed, but this choice identifies the basic differences that are found REFERENCES 1. Junge D Nerve and muscle excitation. Sunderland, MA: Sinauer Associates. 2. Katz B Nerve, muscle and synapse. New York: McGraw-Hill. 3. Kenes RD, Aidley DJ Nerve and muscle. Cambridge: Cambridge UP. Additional References Aidley DJ The physiology of excitable cells. Cambridge: Cambridge UP. Stein RB Nerve and muscle. New York: Plenum Press. Kenes RD, Aidley DJ Nerve and muscle, 2nd ed. Cambridge: Cambridge UP.
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