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MUSCLE CELL BIOLOGY AND CELL MOTILITY
1Zentrum Biochemie and 2Zentrum Physiologie, Medizinische Hochschule Hannover, Hannover, Germany; and 3Edward A. Doisy Department of Biochemistry and Molecular Biology, Saint Louis University School of Medicine, St. Louis, Missouri
Submitted 1 June 2007 ; accepted in final form 13 November 2007
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ABSTRACT |
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sarcoplasmic reticulum; t-tubule; lactate transporter; ryanodine receptor; sarco(endo)plasmic reticulum Ca2+-ATPase
It has been proposed that a muscle CA associated with the SR membrane is involved in the kinetics of Ca2+ transport and consequentially in the kinetics of muscle contraction (3, 42, 43). Therefore, we studied isometric twitch and tetanic contractions of isolated fiber bundles from the fast-twitch extensor digitorum longus muscle (EDL) and from the slow-twitch soleus muscle (Sol) as well as their fatigue behavior. Muscle fibers either deficient for CA IV or deficient for CA IX did not show a muscle function different from wild-type (WT) fibers. Muscle function of CA IV/XIV double knockout (dKO) mice showed a decrease in rise and relaxation time and in force of single twitches. In contrast, acute exposure to the CA inhibitor dorzolamide (DZ) of either WT or CA IV/XIV dKO muscle fibers solely expressing CA IX led to an increase in rise time and peak force of single twitches. We conclude that the deficiency of one SR CA isoform does not, while inhibition of all three CAs does, affect muscle contraction.
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METHODS |
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Protein concentrations of SL and SR membrane vesicle fractions were measured according to the method of Lowry et al. (18). All animal experiments were reviewed and approved by the Bezirksregierung Hannover.
Enzyme Measurements Na+-K+-ATPase. Na+-K+-ATPase was measured as described by Seiler and Fleischer (32). To obtain maximal Na+-K+-ATPase activity, SL and SR membrane vesicles were preincubated in a medium containing 40 mM imidazole-HEPES (pH 7.3), 2 mM Tris EDTA, and 0.3 mg/ml SDS for 20 min at room temperature. The sample was diluted 50-fold into the assay medium containing (in mM) 120 NaCl, 20 KCl, 3 MgCl2, 3 Na2ATP, 0.5 EGTA, 5 NaN3, and 30 imidazole-HCl (pH 7.5) with or without 1 mM ouabain. The reaction proceeded for 5 min at 37°C before being stopped by the addition of trichloroacetic acid at a final concentration of 5% (wt/wt) and immediate placement on ice. Inorganic phosphate was measured according to the method of Ottolenghi (28). ATPase activity was calculated by the amount of inorganic phosphate produced during the reaction time. Ouabain-sensitive Na+-K+-ATPase was calculated as the difference between total Na+-K+-ATPase activity and the activity measured in the presence of 1 mM ouabain.
Ca2+- and Mg2+-ATPases. Ca2+- and Mg2+-ATPases were measured as described by Seiler and Fleischer (32). Mg2+-ATPase was determined in the presence of (in mM) 100 KCl, 3 MgCl2, 3 Tris-ATP, 30 imidazole (pH 7.2), and 1 Tris-EGTA, with 5 µg/ml ionophore A-23187 and protein sample. Total ATPase activity was determined in the presence of 50 µM CaCl2 instead of 1 mM Tris-EGTA. The reaction proceeded for 5 min at 25°C, and inorganic phosphate was determined. Ca2+-dependent ATPase activity is the difference between total and Mg2+-dependent ATPase activity.
Carbonic anhydrase. CA was measured as described by Bruns et al. (3). CO2 was applied at a flow rate of 360 ml/min. The final assay volume of 0.4 ml contained 200 µl of phenol red solution (12.5 mg phenol red dissolved in 1 liter of 2.6 mM NaHCO3), 130 µl of sample-H2O, 20 µl of 2% Triton X-100, and 50 µl of buffer solution (64 mM 5,5-diethylbarbituric acid Na-salt, adjusted to pH 9.0 with HCl). The temperature was 0°C. The reaction was started by quickly adding the buffer solution after a 2.5-min period of preincubation. The time interval between the start of the reaction and the color change of the indicator from red to yellow was determined. One unit of CA activity is defined as the concentration of enzyme required in the final assay volume to halve the uncatalyzed reaction time. The CA activity of membrane vesicles was determined in the presence of Triton X-100 to measure extra- as well as intravesicular CA activity. In the presence of 0.1% Triton X-100, CA was inhibited by 0.1 mM DZ.
Western Blot Analysis SL and SR membrane proteins were separated on 10% SDS-polyacrylamide gels under reducing conditions. After SDS-polyacrylamide gel electrophoresis, protein polypeptides were electrophoretically transferred on an Immobilon-P polyvinylidene difluoride membrane (Millipore, Billerica, MA) with a polyblot assembly (Trans-Blot SD semi-dry transfer cell, Bio-Rad Laboratories, Hercules, CA). After peptide transfer, membranes were subjected to immunostaining as described previously (47). The polypeptides for CA IV and CA XIV were detected with primary rabbit anti-mouse CA IV or CA XIV antibodies at a dilution of 1:3,000. The polypeptides for CA IX and CA XII were investigated with primary rabbit anti-human CA IX and rabbit anti-mouse CA XII antibodies at a dilution of 1:2,000. Goat anti-rabbit IgG antibody conjugated with peroxidase was used as secondary antibody (1 ng/ml; Calbiochem). The blots were developed with a luminol-peroxide buffer kit from Pierce Biotechnology (Supersignal West Femto, Rockford, IL). Low-molecular-mass standard proteins were from Bio-Rad Laboratories.
SL WT and SR WT bands of 39 and 43 kDa were also quantitatively analyzed in order to estimate the distribution of the CA IV and CA IX proteins, respectively, between SL and SR membranes. Therefore, amounts of SL WT and SR WT protein were chosen so that the SL WT and SR WT contained the same amount of CA enzyme units (EU), namely, 0.033 EU in the case of CA IV and 0.020 EU in the case of CA IX. In the case of CA IV 6.6 µg of SL WT protein and 71.8 µg of SR WT protein were used to give 0.033 EU, and in the case of CA IX 3.8 µg of SL WT protein and 43.0 µg of SR WT protein were used to give 0.020 EU. Quantitative analysis of the CA IV and IX protein bands was performed with ImageMaster 1D software (Pharmacia LKB Biotechnology, Uppsala, Sweden).
Immunofluorescence Staining EDL muscle fiber bundles of WT, CA IV KO, CA IX KO, and CA IV/XIV dKO mice were fixed with 3% paraformaldehyde and 100% methanol and permeabilized in 0.1% Triton X-100 for 5 min as described previously (24). Fibers were incubated with primary antibodies for 30 min. The primary rabbit anti-mouse CA IV and rabbit anti-human CA IX antibodies were diluted 1:400, and the primary goat anti-mouse monocarboxylate transporter (MCT)4, goat anti-mouse sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA)1, and goat anti-mouse ryanodine receptor (RyR) antibodies were diluted 1:200. Incubation with FITC-labeled anti-rabbit IgG secondary antibody and tetramethylrhodamine isothiocyanate (TRITC)-labeled anti-goat IgG secondary antibody was performed for a further 30 min. The subcellular localization of CA IV, CA IX, MCT4, SERCA1, and RyR was examined by CLSM (Leica DMIRBE, Wetzlar, Germany) and analyzed with Image Span software (Leica TCS-NT).
Measurements of Isometric Contractions
EDL and Sol muscles were dissected from killed WT, CA IV KO, CA IX KO, and CA IV/XIV dKO mice. Small intact muscle fiber bundles were prepared from tendon to tendon consisting of 
50 muscle cells. The muscle fiber bundles were directly stimulated with platinum wires, and isometric contraction signals were measured at 25.0 ± 0.2°C as described previously (1). The fiber bundles were superfused with Krebs-Henseleit solution containing (in mM) 120 NaCl, 3.3 KCl, 1.2 MgSO4, 1.2 KH2PO4, 1.3 CaCl2, and 25 NaHCO3. The Krebs-Henseleit solution was equilibrated with 95% O2-5% CO2 to give a pH of 7.4. Single twitches were stimulated by pulses of 1-ms duration and supramaximal voltage. Tetani of EDL fiber bundles were elicited by a 0.4-s train of 1-ms pulses at 100 Hz and tetani of Sol fiber bundles by a 1.5-s train of 1-ms pulses at 50 Hz. During the fatigue test, EDL fibers were stimulated with 0.2-s tetani at 55 Hz repeated every 12.5 s for 40 min or repeated every 2 s for 16 min, and Sol fibers were stimulated with 1.2-s tetani at 15 Hz repeated every 5 s also for 40 min. Single twitches were analyzed for time to peak (TTP), 50% relaxation time (t50) and peak force. TTP was defined as the time interval between initial baseline and peak force. t50 was defined as the time interval between peak force and 50% decayed force. Tetani were analyzed for maximum tetanic force and t50. All forces are given in normalized force (mN/mm2), correcting for the varying sizes of the fiber bundles.
Blood Parameters Blood samples of WT mice and CA IV/XIV dKO mice were analyzed with a blood gas and electrolyte system (ABL 505, Radiometer Medical, Copenhagen, Denmark). The values of pH, PCO2, PO2, and base excess (BE) as well as plasma HCO3– concentrations at PCO2 = 40 mmHg (= standard HCO3–) were determined at 37°C.
Intracellular pH Measurements
The membrane potential electrodes and the H+-sensitive electrodes were pulled from borosilicate glass tubing (GC 150T-7.5, Harvard Apparatus, Edenbridge, UK) as described previously (41). The membrane potential electrodes were filled with a solution containing 1.5 M KCl and 1.5 M potassium acetate (pH adjusted to 6.6–6.7 with HCl). Their resistance varied between 30 and 50 M
. The H+-sensitive electrodes were silanized with N,N-dimethyltrimethylsilylamine (Fluka) vapor and then backfilled with (in mM) 100 NaCl, 200 HEPES, and 100 NaOH. A short column of the H+ sensor Hydrogen Ionophore Cocktail A (Fluka) was sucked into the tip. The resistance of the H+-sensitive electrodes varied between 15 and 30 G. The average slope of the H+-sensitive electrode, which was used to measure intracellular pH (pHi), was 58 mV/
pH. The reference electrode was filled with 3 M KCl and 3% agar. The muscle fibers were superfused with Krebs-Henseleit solution containing (in mM) 120 NaCl, 3.3 KCl, 1.2 MgSO4, 1.3 CaCl2, and 25 NaHCO3. The solution was gassed with 95% O2-5% CO2. The PCO2 of the solution in the chamber was 32 ± 3 mmHg, and the pH was 7.37 ± 0.05 (n = 6 measurements). pHi measurements were performed at room temperature under resting conditions for the muscle fibers.
Antibodies and CA Inhibitor Dorzolamide The polyclonal rabbit anti-mouse CA IV and CA XIV antibodies were described previously (14, 30). Polyclonal rabbit anti-mouse CA XII antibody was characterized by Kyllönen et al. (15), and rabbit anti-human CA IX antibody was described by Scheibe et al. (31). Goat anti-mouse MCT4 antibody (sc-14934), goat anti-mouse SERCA1 antibody (sc-8093), and goat anti-mouse RyR antibody (sc-8170) as well as all secondary anti-rabbit IgG and anti-goat IgG antibodies were purchased from Santa Cruz Biotechnology (Santa Cruz, CA). DZ was a kind gift from Merck & Company (Rahway, NJ).
CA IV KO, CA IV/XIV dKO, and CA IX KO Mice CA IV KO and CA IV/XIV dKO mice were characterized by Shah et al. (34) and CA IX KO mice by Ortova Gut et al. (27).
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RESULTS |
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The double immunostaining of EDL WT fibers with anti-CA IV/FITC and anti-MCT4/TRITC is seen in Fig. 3, A–C. The immunohistochemical staining was examined by CLSM, and the light was focused on the plasma membrane. In fast-twitch skeletal muscle fibers, the lactate transporter MCT4 has been described to be located on plasma membranes as well as on t-tubular membranes (2). The distribution of anti-MCT4/TRITC fluorescence as seen in Fig. 3B confirms this subcellular localization of MCT4. CA IV is seen mainly in the form of spots of green fluorescence, which appear regularly in lines and indicate that CA IV is especially localized in the regions of t-tubular openings (Fig. 3A). A weaker green FITC fluorescence is seen in the regions between these spots, indicating that CA IV is present in the surface membrane. The merged image in Fig. 3C shows the colocalization of CA IV and MCT4 in the same membrane regions. Figure 3, D–F, show the double immunostaining of EDL WT fibers with anti-CA IX/FITC and anti-MCT4/TRITC. Here again, the light of the confocal microscope was focused on the level of the plasma membrane. It is seen that CA IX is not expressed in the plasma membrane (Fig. 3D). Weak spots of anti-CA IX/FITC fluorescence as seen in Fig. 3D are unspecific, as confirmed by anti-CA IX/FITC staining of EDL-CA IX KO fibers (Fig. 3, G–I).
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25% compared with the activity of the SL WT fraction and the activity of the SL CA IV/XIV dKO fraction by 80% compared with the CA activity of SL WT. Because of the positive staining of CA IX in the SL CA IV/XIV dKO fraction as shown in Fig. 2, it is concluded that CA IX contributes to the CA activity found in the SL CA IV/XIV dKO fraction. DZ, a CA inhibitor that does not distinguish among the different CA isoforms, causes complete CA inhibition in every SL fraction (Fig. 6A). The SR CA IV KO fraction displays a lower CA activity than the SR WT membrane fraction, but this difference is not significant (Fig. 6B). The CA activity of the SR CA IV/XIV dKO fraction is significantly reduced by 40% compared with the activity of the SR WT fraction. The remaining activity of SR CA IV/XIV dKO is probably caused by the activity of CA IX (see Fig. 2). DZ (0.1 mM) leads to nearly complete CA inhibition in all SR CA fractions (Fig. 6B).
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30% compared with force of CA IV/XIV WT fibers. Compared with the forces of CA IX WT fibers from mice that had the same genetic background as the CA IX KO mice, forces of EDL-CA IX KO fibers are unaffected. Values of peak force from Sol CA IV KO fiber bundles are comparable to those of Sol CA IV/XIV WT fiber bundles, and values of force from Sol CA IV/XIV dKO fibers are 60% greater than those of CA IV/XIV WT fibers (Fig. 7A). Peak force of Sol CA IX KO fibers does not differ from peak force of their corresponding WT fibers. Figure 7B shows that the values of TTP and t50 are not different between CA IV/XIV WT and CA IV KO fiber bundles. However, values of TTP and t50 from CA IV/XIV dKO fibers are significantly shorter than the values from CA IV/XIV WT fibers. Values of TTP and t50 from CA IX WT and CA IX KO fibers are comparable. This holds for EDL as well as for Sol.
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25% (Fig. 10A) and the values of peak force by 50 (Fig. 10C); t50 is unaffected by DZ (Fig. 10B). It is seen that the inhibitory effects on EDL CA IV/XIV WT and EDL CA IV/XIV dKO fibers by DZ are comparable. In Sol CA IV/XIV WT and Sol CA IV/XIV dKO fiber bundles, DZ significantly prolongs TTP by 20% and t50 by 10% and increases peak force by 20% (data not shown). Also in Sol, the effects of DZ are expressed to the same extent in CA IV/XIV WT and CA IV/XIV dKO fibers.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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SR-Associated CAs and Isometric Contractions of Skeletal Muscle Fibers It has been predicted that SR-associated CAs are involved in excitation-contraction coupling (3, 42). Several studies provided evidence that H+ in addition to Mg2+, K+, and Cl– (21, 35) are transported into the SR during Ca2+ release (13, 29, 35). This is possible because of the extremely high H+ permeability of the SR membrane (23, 26). Ca2+ uptake into the SR is also accompanied by H+ transport (4, 20, 21, 36, 37, 45, 46). Bruns et al. (3) postulated that a SR CA catalyzes the hydration of CO2 to form the H+ ions, which are transported across the SR membrane. We previously showed that inhibition of SR CAs by various membrane-permeant CA inhibitors such as chlorzolamide, L-645,151, and DZ prolongs Ca2+ release as well as Ca2+ uptake, probably by slowing down the rate of H+ transport. The prolonged Ca2+ release and the prolonged Ca2+ uptake are accompanied by prolongation of TTP and t50 of twitches and by an increase in peak force (42, 43). In these studies isolated muscle fibers of rat EDL and Sol were used. As seen in Fig. 10, in EDL WT fibers of mouse DZ significantly increases TTP and peak force of twitches but does not affect t50. This might be explained by the higher concentration of parvalbumin in the EDL of mouse compared with the EDL of rat (9). Ca2+ binding to parvalbumin as well as Ca2+ pumping by SERCA accelerate the decay in free cytoplasmic Ca2+ concentration, and by this muscle relaxation. Because of the higher concentration of parvalbumin in mouse compared with rat, it seems possible that in mouse Ca2+ binding to parvalbumin is more important than Ca2+ pumping by SERCA in determining the kinetics of Ca2+ decay. Ca2+ pumping by SERCA requires a H+ antiport, which is dependent on the presence of a SR CA. If the latter mechanism is less important in mouse than in rat, it is plausible that CA inhibitors exert only a minor or no effect on t50 of twitches in mouse EDL.
Contrary to these earlier data, values of peak force from mouse EDL CA IV/XIV dKO fibers as well as values of TTP and t50 from both EDL and Sol CA IV/XIV dKO fibers are significantly reduced compared with those of mouse WT fibers (Figs. 7 and 8). Acidosis occurring in the muscle fibers, which would affect the function of actin-myosin filaments, might have caused the effects observed in the CA IV/XIV dKO mice. Because of the lack of CA IV and CA XIV, the CA IV/XIV dKO mice may have a reduced rate of renal HCO3– reabsorption resulting in renal acidosis and consequently in acidosis of the muscle fibers. However, CA IV/XIV dKO mice show normal values of BE and normal concentrations of standard HCO3– (Table 2). It has been shown that SL CA activity improves interstitial buffering in muscle (8, 10, 41) and that impaired interstitial buffering will impair pHi regulation (see, e.g., Ref. 39). Since the total SL CA activity of CA IV/XIV dKO muscle cells is reduced by 80% (Fig. 6A), it might have been assumed that the pHi of the CA IV/XIV dKO muscle fibers is more acidic than the pHi of WT fibers. Table 3 shows that under resting conditions for the muscle fibers pHi of neither EDL CA IV/XIV dKO nor Sol CA IV/XIV dKO is altered compared with pHi of WT fibers. Thus the effects on contraction parameters of CA IV/XIV dKO fibers can be explained neither by a more acidic pHi under resting conditions of muscle cells nor by a renal acidosis. It cannot be excluded that the lack of CA IV and XIV activities inside the SR might have caused pH changes within the intra-SR environment. Because of the phosphoinositol-glycan anchor of CA IV, it is predicted that CA IV will be catalytically active inside the SR, whereas the membrane orientation of SR CA XIV is not known so far. It can thus be assumed that the fast buffering of the H+ ions, which are transported into the SR during Ca2+ release, is impaired because of the lack of SR CA IV. Therefore, during the release of Ca2+, pH within the SR will become more acidic than under normal conditions. A more acidic intra-SR pH will reduce the open probability of the RyR (16, 19) and by this possibly abbreviate the interval of Ca2+ release and reduces TTP and peak force of twitches.
In CA IV single KO muscles as well as in CA IX single KO muscles, the contraction parameters of twitches and tetani are affected neither in EDL nor in Sol compared with WT fibers. Two possibilities may be discussed as to why CA IV KO and CA IX KO muscle fibers are not affected in the manner in which WT fibers are affected by CA inhibitors. 1) CA IV contributes 20% and CA IX 60% to the total SR CA activity (Fig. 6B). The remaining SR CA activity of 80% or 40%, respectively, may be still sufficient to maintain a normal SR function and consequently a normal muscle function. 2) On the other hand, it cannot be excluded that the transport rates of Mg2+, K+, and Cl–, which can also function as counterions for Ca2+ at the SR membrane, are upregulated in CA IV KO and CA IX KO mice in order to compensate for the reduced H+ transport rates.
Only the acute inhibition of all CA activity by DZ led to a prolongation of TTP and to an increase in force of twitches in WT fibers as well as in CA IV/XIV dKO fibers (Fig. 10). CA IX is the sole known membrane-associated CA isoform present in the CA IV/XIV dKO fibers. We show here that CA IX is very likely localized in the terminal SR. If we assume that CA IX is catalytically active at the cytoplasmic side of the terminal SR membrane, then on inhibition by DZ pH at the cytoplasmic side of the SR membrane will become more alkaline during the release of Ca2+. This is known to increase Ca2+ release (6, 22, 25) and by this increase TTP and force of twitches (36). Studies with muscle fibers of CA IV, IX, and XIV triple KO mice will be helpful in further exploring this concept.
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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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, EDL CA IV/XIV WT, n = 5 bundles; 
, EDL CA IV/XIV dKO, n = 6 bundles. Values are means ± SD. Values at time 0 min are set to 100%. At time 0 min, 0.5 mM DZ was added to the superfusion solution. Significance of differences between the mean values of each time course was calculated by repeated measures 1-way ANOVA followed by Dunnett's post test, control = mean value at time 0 min. *Significant differences between mean values (P < 0.01). In the presence of DZ, values of TTP and peak force are significantly increased to the same extent in WT and CA IV/XIV dKO fibers.