Skeletal muscle adaptability : Significance for metabolism and performance

The sections in this article are:


1
Motor Unit
1.1
Fibers per Motor Unit

1.2
Contractile Properties

1.3
Biochemical Basis for Differences in Twitch Properties

1.4
Histochemical Differentiation of Muscle Fibers

1.5
Ultrastructural Basis for Skeletal Muscle Fiber Typing

1.6
Maximal Contractile Force

1.7
Speed of Contraction

1.8
Fatigue Characteristics

1.9
Metabolic Characteristics

1.10
Ionic Composition of Skeletal Muscle

1.11
Summary




2
Muscle Fiber Composition in Human Skeletal Muscle

3
Motor-Unit Recruitment

4
Adaptive Response in Skeletal Muscle
4.1
Muscle Size

4.2
Metabolic Capacity




5
Connective Tissue

6
Capillaries
6.1
Methodology

6.2
Anatomy

6.3
Capillary Density

6.4
Capillary Length and Diameter

6.5
Use and Disuse

6.6
Regulation




7
Significance of Adaptation
7.1
Muscular Size

7.2
Substrate Stores

7.3
Enzyme Activities

7.4
Summary

Skeletal Muscle Adaptability: Significance for Metabolism and Performance

A number of studies have suggested that Z-disk degradation is a major factor contributing to postmortem tenderization. These conclusions seem to have been based largely on experimental findings showing that the calpain system has a major role in postmortem tenderization, and that when incubated with myofibrils or muscle strips, purified calpain removes Z-disks. Approximately 65 to 80% of all postmortem tenderization occurs during the first 3 or 4 d postmortem, however, and there is little or no ultrastructurally detectable Z-disk degradation during this period. Electron microscope studies described in this paper show that, during the first 3 or 4 d of postmortem storage at 4 degrees C, both costameres and N2 lines are degraded. Costameres link myofibrils to the sarcolemma, and N2 lines have been reported to be areas where titin and nebulin filaments, which form a cytoskeletal network linking thick and thin filaments, respectively, to the Z-disk, coalesce. Filamentous structures linking adjacent myofibrils laterally at the level of each Z-disk are also degraded during the first 3 or 4 d of postmortem storage at 4 degrees C, resulting in gaps between myofibrils in postmortem muscle. Degradation of these structures would have important effects on tenderness. The proteins constituting these structures, nebulin and titin (N2 lines); vinculin, desmin, and dystrophin (three of the six to eight proteins constituting costameres); and desmin (filaments linking adjacent myofibrils) are all excellent substrates for the calpains, and nebulin, titin, vinculin, and desmin are largely degraded within 3 d postmortem in semimembranosus muscle. Electron micrographs of myofibrils used in the myofibril fragmentation index assay show that these myofibrils, which have been assumed to be broken at their Z-disks, in fact have intact Z-disks and are broken in their I-bands.

Is Z-disk degradation responsible for postmortem tenderization?

Removal of rabbit psoas strips immediately after death and incubation in a saline solution containing 1 mM Ca2+ and 5 nM Mg2+ for 9 hr at 37°C and pH 7.1 causes complete Z-line removal but has no ultrastructurally detectable effect on other parts of the myofibril. Z lines remain ultrastructurally intact if 1 mM 1,2-bis-(2-dicarboxymethylaminoethoxy)-ethane (EGTA) is substituted for 1 mM Ca2+ and the other conditions remain unchanged. Z lines are broadened and amorphous but are still present after incubation for 9 hr at 37°C if 1 mM ethylenediaminetetraacetate (EDTA) is substituted for 1 mM Ca2+ and 5 mM Mg2+ in the saline solution. A protein fraction that causes Z-line removal from myofibrils in the presence of Ca2+ at pH 7.0 can be isolated by extraction of ground muscle with 4 mM EDTA at pH 7.0–7.6 followed by isoelectric precipitation and fractionation between 0 and 40% ammonium sulfate saturation. Z-line removal by this protein fraction requires Ca2+ levels higher than 0.1 mM, but Z lines are removed without causing any other ultrastructurally detectable degradation of the myofibril. This is the first report of a protein endogenous to muscle that is able to catalyze degradation of the myofibril. The very low level of unbound Ca2+ in muscle cells in vivo may regulate activity of this protein fraction, or alternatively, this protein fraction may be localized in lysosomes.

/pdf/ca2-specific-removal-of-z-lines-from-rabbit-skeletal-muscle-4ly81spkix.pdf

Ca2+-SPECIFIC REMOVAL OF Z LINES FROM RABBIT SKELETAL MUSCLE

Samples were removed from bovine longissimus (L), semitendinosus (ST) and psoas major (PM) muscles at 1, 2, 3, 6, 7, 10 or 13 days postmortem stored at 2°C or 25°C. Myofibril fragmentation index (MFI) and Warner-Bratzler (W-B) shear-force values were determined on steaks from each muscle. Myofibril fragmentation index (MFI) was determined quantitatively by measuring the absorbance of a myofibril suspension. It was observed that MFI increased during postmortem storage for L and ST, but increased only slightly for PM. These results paralleled those changes in myofibrils observed with phase and polarized light microscopy. Both MFI and W-B shear-force values changed greatly from 1 to 3 days postmortem with a lesser change occurring after 3 days in L and ST muscles. In PM muscle, however, only a slight change in MFI and W-B shear-force occurred during postmortem storage. Elevated storage temperature (25°C) caused an accelerated change in both MFI and W-B shear-force in L and ST muscles; however, storage temperature had little effect on PM muscle. L and ST muscles responded similarly to postmortem storage, but PM muscle was characteristically different from the L and ST muscles. These findings demonstrate the differences and similarities of muscles to postmortem storage and further elucidate the role of myofibrillar proteins in meat tenderness.

Myofibril fragmentation and shear resistance of three bovine muscles during postmortem storage

Ultrastructural changes in bovine, porcine, and rabbit muscle have been studied during the first 24 hours post-mortem. Samples were taken for phase and electron microscopy immediately after death, after 4, 8, and 24 hours of post-mortem storage at 2° and 37°C, and after 24 hours post-mortem at 16° and 25°C. The results show that two kinds of structural changes occur in muscle during the first 24 hours post-mortem: (a) a variable amount of shortening, this shortening occurring via a sliding of filaments in all species and at all post-mortem storage temperatures examined, and (b) degradation of the Z line, and at higher storage temperatures, of the M line also. Shortening of unrestrained muscle occurs soonest post-mortem at 37°C in all three species and is completed within four hours post-mortem in porcine and rabbit muscle and within eight hours post-mortem in bovine muscle. Post-mortem short-ening of unrestrained rabbit and porcine muscle is greatest at 37°C (sarcomere lengths of 1.5 μ); shortening of rabbit muscle is minimal at 2°C (sarcomere lenght of 1.7 μ), but shortening of porcine muscle is minimal at 25°C (sarcomere length of 1.8 μ) and is slightly greater at 2°C (sarcomere length of 1.6 μ) than at 16°C. Post-mortem shortening of bovine muscle is greatest at 2°C (sarcomere length of 1.3 μ), is minimal at 16–25°C (sarcomere length of 1.8 μ), and increases between 25–37°C (sarcomere length of 1.5 μ at 37°C). Sarcomere length measurements show that some variation occurs in the extent of post-mortem shortening within the same muscle.



Z line degradation occurs sooner post-mortem and to a greater extent at storage temperatures of 25°C or above than at temperatures of 16°C or below. Also, bovine muscle Z lines are clearly more resistant to post-mortem degradation than porcine or rabbit muscle Z lines. Loss of fibrillar structure in porcine or rabbit muscle Z lines occurs during the first four hours post-mortem at 37°C, but eight hours of post-mortem storage at 37°C are required to cause loss of fibrillar structure of bovine muscle Z lines. After 24 hours at 25 or 37°C, Z lines of rabbit and porcine muscle are usually completely absent; M lines are also frequently absent in this muscle.

A comparison of shortening and Z line degradation in post-mortem bovine, porcine, and rabbit muscle.

SUMMARY– Investigations were conducted on the effect of three storage temperatures, 2°, 16°, and 37°, on the changes and relationships of certain chemical and physical properties of post-mortem bovine semitendinosus and psoas muscle. Post-mortem muscle shortening was measured with the isometer. Isometric tension development was maximal at 2°, minimal at 16°, and at 37° tension was approximately one-half that developed at 2°. The large tension development at 2° very likely originates from the same events as those in “cold shortening.” Differences in isometric tension parameters were noted between muscles in that psoas muscle developed tension and lost the ability to maintain tension more quickly than did the semitendinosus. Loss of ability to maintain tension was observed only at 2°, and this could correspond to a “resolution” of rigor mortis. Adenosine triphosphate (ATP) degradation was measured by two methods, ammonia production and bioluminescent enzymic method; the bioluminescent method proved to be the more satisfactory. A common relationship was observed between pH and ATP for both muscles and the three temperatures studied. No direct relationship was found between ATP degradation and shear resistance with the possible exception of muscle stored at 37°. Isometric tension parameters and shear resistance were related somewhat at 2° in semitendinosus muscle, but no relationship existed at 16° and 37°. Although considerable tension developed in psoas and semitendinosus muscle at 37°, shear resistance values decreased continuously, indicating that factors other than shortening are more important at high temperature and that these factors are temperature-dependent.



The role of ATP degradation in tension development was difficult to interpret, since at 2°, only a small change occurred in ATP level during large tension development, and the level of ATP at 2° did not differ from ATP level in muscle stored at 16° which developed little tension.



Differences in post-mortem muscle shortening at 2 and 37 are discussed.

Molecular Properties of Post‐Mortem Muscle. 4. Effect of Temperature on Adenosine Triphosphate Degradation, Isometric Tension Parameters, and Shear Resistance of Bovine Muscle

Molecular properties of postmortem muscle.

SUMMARY— Post-mortem changes in nucleoside triphosphatase activity of bovine myosin B have been studied by using several different modifiers with either 5 mM ATP or 5 mM ITP as substrate at ionic strengths (r/2) of 0.09, 0.19, or 0.52. Enzymic activity was determined by measuring the release of inorganic phosphate. There was very little difference in enzymic activity between myosin B isolated from prerigor, rigor (24 hr post-mortem) or post-rigor (312 hr post-mortem) muscle stored at either 2° or 16°C except that the specific activity of myosin B prepared from muscle stored for 12–24, hr post-mortem was higher than activity of myosin B prepared immediately after death. This increase cannot be explained in terms of rigor shortening, but suggests that a change in myosin conformation or in the nature of the actin-myosin interaction occurs in post-mortem muscle. If an actin-myosin interaction occurs during rigor mortis and if this association remains unchanged during extraction of myosin B, then the very low Mg++-modified myosin B enzymic activities obtained at Γ/2 = 0.19 and 0.52 indicate that this interaction is not irreversible. Extraction in the absence of ATP produced a myosin B whose ATPase activity was markedly inhibited by trace amounts of Mg++. This may be due to the absence of a-actinin in these myosin B preparations. No consistent differences in activation energies were found either at Γ/2 = 0.19 or 0.52 among the NTPase reactions of myosin B samples prepared from muscle after various times of post-mortem storage.

Molecular Properties of Post-Mortem Muscle.

SUMMARY— A study was made of the fine structure of myofibril suspensions prepared from seven heifers immediately after death and after various times post-mortem. Studies on myofibrils sampled immediately after death showed that sucrose isolation gave the best structural preservation as indicated by maintenance of Z-line structure. Although the appearance of resting muscle was maintained in both sucrose and KCI preparations, several myofibrils from the KCI-treated preparations showed stretched sarcomeres. Glycerol-treated myofibrils usually had shorter sarcomere lengths than myofibrils prepared with the other two solvents. Although fibrillar preservation seemed adequate when glycerol was used, Z-line structure was seldom well-preserved with glycerol.



Myofibrils from muscle sampled 24 hr post-mortem at 2°C were supercontracted with thick filaments pushed against or through the Z-line, and no trace of l-bands remained. Myofibrils from muscle sampled 24 hr post-mortem at 16°C were contracted, but to a much lesser extent than 2°C-24 hr myofibrils. Storage at 2°C for 312 hr after death resulted in myofibrils that were contracted and that were structurally in a much poorer state of preservation than their 16°C counterparts. The 16°C-312 hr myofibrils were slightly contracted as indicated by the absence of H-zones and the presence of prominent, although narrowed, I-bands. All observations showed that shortening accompanying rigor mortis caused changes in banding patterns similar, and probably identical, to those predicted by Huxley's sliding filament model for contracting muscle.

Darrel E. Goll

Papers

A comparison of shortening and Z line degradation in post-mortem bovine, porcine, and rabbit muscle.

Molecular Properties of Post‐Mortem Muscle. 4. Effect of Temperature on Adenosine Triphosphate Degradation, Isometric Tension Parameters, and Shear Resistance of Bovine Muscle

Molecular properties of postmortem muscle.

Molecular Properties of Post-Mortem Muscle.

Molecular Properties of Post-Mortem Muscle. 3. Electron Microscopy of Myofibrils