Department of Cell Biology, University of Salzburg, A-5020 Salzburg, Austria
Submitted 25 May 2004 ; accepted in final form 7 August 2004
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ABSTRACT |
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isoform structure-function relationship; stretch activation; muscle mechanics
MHC isoform content determines the contractile properties of muscle fibers (for review see Ref. 4). The relation between MHC content, stretch activation kinetics, and unloaded shortening velocity (Vu) has been clearly established for rat, rabbit, and human skeletal muscle fibers (4, 7, 9, 17, 35). Although the mouse is the most important mammalian model for genetic manipulations, the skeletal muscle fibers of this species have been investigated to a much lesser degree. The relationship between shortening velocity and load has been determined in different mouse muscle fiber types. Furthermore, Vu was compared with the actin filament sliding propelled by the different myosin isoforms (28, 39). The kinetics of stretch activation has never been investigated in mouse skeletal muscle fibers, although a strong correlation of this parameter with the MHC isoforms has been found in other species (3, 12, 16, 17, 19, 24, 26, 33). This correlation most likely points to different kinetic properties of myosin heads of various MHC isoforms while generating force (1, 31, 34). Therefore, in the present study stretch activation experiments have been performed on mouse skeletal muscle fibers with known MHC isoform content. To investigate any dependence of stretch activation kinetics on body mass, we compared the results in mice with those of corresponding rat, rabbit, and human fiber types.
Comparisons between different animal species were also used to establish structure-function relationships on the molecular level. We tried to answer the question of which specific structural alterations of the myosin molecule are responsible for the functional differences of mammalian MHC isoforms. So far this problem has been addressed particularly in other animal phyla. In particular, two flexible loops of the myosin head were discussed as possible candidates for modulation of kinetic activities of myosin (22, 37): loop 1, which is the connection of the 25-kDa and 50-kDa domains of the myosin head, and loop 2, which is the connection between the 50-kDa and 20-kDa domains (20). Comparisons of MHC isoforms of striated and smooth muscles of two molluscan species (Argopecten, Placopecten) suggested that the differences in their ATPase activity are likely due to sequence variation of loop 1 (40). Further information about the influence of various myosin head regions on differences in function were provided by studies on chimeric MHC isoforms. In a study of Uyeda et al. (52), loop 2 of Dictyostelium was genetically modified by substitution of nine amino acids with those of myosins of other animal species. Significant changes of ATPase activity after the substitutions in loop 2 were observed. The ATPase activity of the chimeric myosins correlated well with that of myosin from which the substitution was derived. Similarly, in a study of Sweeney et al. (50), loop 1 of different myosin II isoforms was inserted into a smooth myosin backbone. Here a variation of functional properties depending on the substitutions of loop 1 was found. However, the properties of chimeric myosins did not correlate with those of myosins from which the loop was derived. In Drosophila, dramatic changes of kinetic properties were observed after genetic manipulations of the converter region (48).
In the present study, we correlated alterations of the amino acid sequence of the MHC isoforms with the stretch activation kinetics of corresponding fiber types. The correlations were carried out both within and between different animal species. Either whole amino acid sequences or fragments of amino acid sequences of various MHC isoforms were available. In a previous study (39), a similar approach was applied for identification of the structural correlate underlying the differences in filament sliding of mammalian muscle fiber types.
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MATERIALS AND METHODS |
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Solutions. The following solutions (05°C; Ref. 53) were used for sequential incubations: 1) skinning solution (in mM): 132 sodium propionate, 5 EGTA, 7 Na2H2ATP, 2 MgCl2, 10 MOPS, 1 dithioerythritol (DTE) adjusted to pH 6.9 with KOH; 2) skinning solution in which sodium propionate was replaced by potassium propionate; 3) solution 2 with 10% (vol/vol) glycerol; 4) solution 2 with 25% (vol/vol) glycerol; and 5) relaxation solution (for composition see Mechanical measurements; pH 6.9) with 50% (vol/vol) glycerol. The preparations were stored in this solution at about 25°C for up to 2 mo. Before the experiments, single fibers were dissected in this solution (around 5°C) and glued to the tips of the two needles of the apparatus.
Mechanical measurements.
The experimental apparatus and the method for mechanical measurements have been described previously (14). The attachment points for the muscle fibers (active length 0.82.5 mm, mean diameter 2555 µm) on the mechanical apparatus were two
2-mm-long vertically oriented epoxy carbon fiber needles of
100-µm tip diameter. The needles were connected to the apparatus by silicon plates from force transducer elements (AE 801; SensoNor). One element, the force sensor (resonance frequency
7.5 kHz), was connected mechanically to a micrometer screw and electrically to a force bridge amplifier. The other element was glued on the lever arm of a stepping motor. Rapid changes of the fiber length (
1 ms) were achieved by a feedback-controlled stepping motor based on a Ling vibrator. The ability to make rapid solution changes was provided by a cuvette transporting system. Laser diffractometry (He-Ne laser; 632.8 nm, 4 mW) was used for measuring the sarcomere length.
After attachment of the skinned fiber with the tissue glue Vetseal (Braun Melsungen) the fiber ends were fixed by superfusion with a fine, rapidly flowing, downward-directed stream of stained glutaraldehyde solutions (8% glutaraldehyde, 5% toluidine blue, fixative) for 23 s. For this purpose the fiber was bathed in a low-ionic-strength rigor solution (in mM: 10 imidazole, 2.5 EGTA, and 7.5 EDTA, 134 potassium propionate, pH 6.9) with a lower specific mass than the fixative. This procedure created a sharp boundary between the functional part of the fiber and the fixed ends. This method considerably improves the maintenance of sarcomere homogeneity and the stability of mechanical properties during prolonged activations (25).
The solutions used during the mechanical measurements had an ionic strength of 0.25 M and contained (in mM) 60 HEPES, 8 Na2H2ATP, 10 sodium creatine phosphate, 10 NaN3, 1 DTE, 40 g/l dextran T-500, 30 U/ml creatine phosphokinase, and 1 mM free Mg2+. The dextran was included in the solutions to prohibit swelling of the skinned muscle fibers (21). In addition, the relaxation solution [pCa > 9, pCa = log free Ca2+ concentration ([Ca2+])] contained 50 mM EGTA. The maximal activation solution (pCa 4.5) contained 50 mM Ca-EGTA, and the preactivation solution (low Ca2+-buffering capacity, pCa 7) contained 50 mM hexamethylenediamine-N,N,N',N'-tetraacetate (HDTA). pH was adjusted to 7.10 with KOH at 22°C. Free [Ca2+] and free [Mg2+] of the solutions were determined with ion-selective electrodes (13).
Before the experiment, the length of the fibers was adjusted to exactly the slack position (resting length) in relaxation solution, and both fiber dimensions and sarcomere length were recorded. The measurements were carried out at resting length to make them comparable with previous work on other species. Fiber cross-sectional area was calculated, using the largest and the smallest diameters and assuming an elliptical shape. After transfer of the fiber to the preactivating solution (1 min) and subsequently to the maximal activating solution, a steady force was reached. The maximal isometric tension was determined by dividing this force by the cross-sectional area. A number of quick (
1 ms) stretches of 0.10.2% of fiber length, lasting 14 s, were applied to induce force transients. The interval between individual stretches was 0.51 min. All experiments were carried out at 22°C. Results are expressed as means ± SD and were analyzed with the two-tailed Student's t-test. Data that did not exhibit a Gaussian distribution were tested with ANOVA.
Biochemical analysis.
After completion of the mechanical measurements, the muscle preparations were removed from the apparatus for biochemical analysis, which was described previously (19). The muscle fragments were dissolved in SDS lysis buffer [62 mM Tris·HCl, pH 6.8, 10% (vol/vol) glycerol, 5% (wt/vol) SDS, 5% (vol/vol) 2-mercaptoethanol] and heated at 65°C for 15 min. Subsequently, a part of this extract (0.1 µg protein) was applied to a SDS polyacrylamide gel system (4% polyacrylamide in stacking gel and 8% in separation gel). For electrophoresis (19), a SE 600 chamber (Hoefer, San Francisco, CA) with 16-cm-long glass plates was used. A constant voltage of 180 V was applied for 28 h. After electrophoresis, gels were silver stained and the relative amount of MHC isoforms was estimated using densitometry.
Comparison of amino acid sequence. For establishing the relationship between the measured kinetic parameters and the amino acid sequence of the MHC isoforms National Center for Biotechnological Information (NCBI) data were used. Sequences with the following GI numbers were compared: mouse: 16508127 (MHCI), 14250231 (MHCIIa), 20883346 (MHCIIx(d)), 38091417 (MHCIIb); rabbit: 2144825 (MHCI), 940233 (MHCIIx(d)); rat: 56657 (MHCI), 543418 (MHCIIa), 34870884 MHCIIx(d), 34870888 and 543419 (MHCIIb); human: 107137 (MHCI), 4808813 (MHCIIa), 4808815 (MHCIIx(d)), 4808811 (MHCIIb). Sequences were aligned with the CLUSTAL W program (Ref. 51; available at http://www.ebi.ac.uk). With this program, the sequence identity score index was determined for pairs of corresponding amino acid sequences.
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RESULTS AND DISCUSSION |
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In hybrid muscle fibers, a relationship between the t3 values and the densitometrically determined ratio of MHC isoform concentrations was established (Fig. 3). For type IIBX hybrids (Fig. 3A), it can be seen that the t3 values depend on the percent distribution of the two isoforms (r = 0.88). Conversely, in mouse type C hybrid fibers, the distribution of t3 was mainly dependent on the predominant MHC isoform (Fig. 3B). Fibers in which MHCIIa was predominant (MHCI-to-MHCIIa+MHCI concentration ratio: 0.100.45) exhibited a range of t3 (96190 ms) close to that of type IIA (91150 ms). Fibers in which MHCI was predominant (MHCI-to-MHCIIa+MHCI concentration ratio: 0.650.95) exhibited a range (568770 ms) close to that of type I (520980 ms). In IIBX rabbit fibers (17) and hybrid fibers of rabbit masseter muscle containing combinations of MHCIIa and -cardiac MHC (3), the t3 values were distributed in the same way as in mouse type IIBX fibers. Because stretch activation data of type C fibers of other mammalian species are scarce, no comparison is possible.
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Although the correlation between the kinetics of stretch activation and the MHC isoforms is strong, the influence of other myofibrillar protein isoforms is possible in principle. However, the following observations make this unlikely. No correlation was found between t3 and the essential myosin light chain (MLC) isoform content of rat and rabbit fibers (unpublished results). Furthermore, in rabbit and rat fast-twitch muscle fibers, essential MLC isoforms are correlated with Vu (5, 49), but stretch activation kinetics are not correlated with Vu (19). Regarding thin filament proteins, an earlier study (18) suggests that troponin T isoforms do not affect the stretch activation kinetics in rat fast-twitch skeletal muscle fibers.
Comparison of stretch activation kinetics in mouse, rat, rabbit, and human. Although the same relationship between stretch activation kinetics and MHC isoforms was found for mouse, rat, rabbit, and human fibers (3, 17, 19, 26), the t3 values of corresponding fiber types within different animal species are not identical in these mammalian species. Figure 4 shows a double logarithmic plot of the velocity parameter 1/t3 (mean ± SD) of mouse, rat, rabbit, and human fiber types against the corresponding body mass. A 1/t3 value for human type IIB fibers is missing because these fibers do not exist. The values originate from different studies executed under identical conditions (human, Ref. 26; rabbit, Ref. 3). For rat fibers, 1/t3 values of measurements more recent than those in Ref. 19 were taken to have absolutely identical conditions for all species. Although not significant in all cases (see Fig. 4), the 1/t3 values show a trend to decrease with increasing body mass. This trend is expressed by the (negative) slopes of the regression lines (scaling coefficients; Ref. 27). The scaling coefficients were similar for all fiber types (0.073 for type I, 0.079 for type IIA, 0.102 for type IIX(D), and 0.086 for type IIB). The same type of dependence on body mass was also observed for Vu and the actin filament sliding propelled by different myosins in vitro (8, 28, 39, 44, 47, 55). In type II fibers, the scaling coefficients of stretch activation kinetics were in the range of those of shortening velocity reported in the literature (39); however, in type I fibers, a much smaller scaling coefficient was found for stretch activation (0.073) than for Vu [0.175 (39), 0.180 (44)]. Vu is a measure that includes changes of the fiber length, whereas stretch activation kinetics (0.10.2% fiber length change) is a measure taken under almost isometric conditions. Thus, for type I fibers, it appears that the cross-bridge cycle steps limiting fiber shortening are more dependent on body mass than specific steps within the cross-bridge cycle during isometric force production.
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To obtain a quantitative measure of the structural variability the following procedure was undertaken. Pairs of amino acid sequences were aligned in the CLUSTAL W program (51). In short, this program detects identical, nonidentical, and missing amino acids of the two sequences and calculates a sequence identity score index. An index of 100 means 100% identity. Sequence identity score indexes of the following MHC regions were determined: whole MHC, myosin head, loop 1 (amino acids 199225 of chicken myosin), loop 2 (621647), loop 3 (567578) (considered in Refs. 54 and 39 for structure-functional comparisons), whole actin-binding region (487600 + loop 2), and converter region (712779). Not all sequences were available in the NCBI database. The GI numbers of the available sequences (Table 2) are mentioned in MATERIALS AND METHODS. For both intra- and interspecies comparisons all possible pairs of available MHC sequences were analyzed. Each isoform was compared with each other MHC isoform of the same species (mouse, rat, rabbit, and human). Likewise, each isoform was compared with each corresponding MHC isoform of the other species (i.e., isoforms with the same name). Thus a considerable number of sequence identity score indexes were obtained.
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In the intraspecies comparisons, the structure-function correlation revealed correlation coefficients near 0.7 for all MHC regions (Table 2). Because all correlation coefficients were similar, these comparisons were not useful to differentiate the importance of variability in different MHC regions. Therefore, the intraspecies comparisons were not considered for further analysis or reflections. In contrast, the interspecies comparisons revealed a range of correlation coefficients from 0.21 to 0.74. The highest correlation coefficients were found for the whole actin-binding region (r = 0.68; Fig. 5A) and for the combination of actin-binding loops 2 and 3 (r = 0.74; Fig. 5B). This suggests a contribution of these loops to the variation in kinetics (at least for corresponding MHC isoforms of different animal species). It is interesting that the structure-function correlation is less pronounced when sequences of loop 2 and loop 3 are individually correlated to the corresponding t3 ratios. It appears that simultaneous variations in both loops are necessary for contributing to differences in function. This requires a cooperative action of the two loops. The actin-binding loop 2 and loop 3 have also been mentioned as possible origins of the differences in the kinetics of unloaded filament sliding of different mammalian skeletal muscle fiber types (8, 39).
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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