Key words: Branched-chain c~-keto acid dehydrogenase complex, branched-chain c~-keto acid
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1 Vol. 44, No. 6, May 1998 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL Pages BRANCHED-CHAIN cx-keto ACID DEHYDROGENASE KINASE CONTENT IN RAT SKELETAL MUSCLE IS DECREASED BY ENDURANCE TRAINING Hisao Fujii 1, u Shimomura 2., Taro Murakami 2, Naoya Nakai 2, Tasuku Sato 1, Masashige Suzuki 3, and Robert A. Harris 4 1Department of Sport Science, Scndai College, Miyagi , Japan; 2Department of Bioscience, Nagoya Institute of Technology, Nagoya 466, Japan; 3Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba 305, Japan; and ~Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN , USA Received October 30, 1997 Received after revision, December 16, 1997 Summary: The activity slate of branched-chain a-keto acid dehydrogenase complex in skeletal muscle was elevated by running exercise in trained and untrained rats, but level of this elevation was significantly greater in the former than in the latter. To elucidate the mechanism of the training effect on the exercise-induced activation of the complex, a protein amount of branchedchain c~-keto acid dehydrogenase kinase, which is responsible for inactivation of the complex by phosphorylation, in the muscle was measured by the Western blot analysis. Endurance training decreased the content of the kinase protein in the muscle by ~30%, suggesting that this decrease is involved in the mechanisms for greater activation of the complex by exercise in trained rats. Key words: Branched-chain c~-keto acid dehydrogenase complex, branched-chain c~-keto acid dehydrogenase kinase, skeletal muscle, endurance training, acute exercise, rat. Introduction Branched-chain c~-keto acid dehydrogenase (BCKDH) complex (c~-ketoisovalerate decarboxylase (Elc~+EII3), dihydrolipoamido acyltransferase (E2), and dihydrofipoamido dehydrogenase (E3)) is an intramitoehondrial multienzyme complex and catalyzes the ratelimiting step in the catabolism of branched-chain amino acids (leucine, isoleucine, and valine) (1). This enzyme complex is subject to regulation by covalent modification. BCKDH kinase (EC ) is responsible for phosphorylation and inactivation of the Elc~ component of the enzyme complex (2-5). It has been reported that acute exercise causes activation of BCKDH complex in rat skeletal muscle (6-10). In our previous study, it was suggested that the activation of muscle BCKDH complex during muscle contractions may be induced by inhibition of BCKDH kinase by branched-chain c~-keto acids accumulated in the muscle (11). Furthermore, we reported that endurance training not only increased the activity state and the total activity of the enzyme complex but also sensitized BCKDH kinasc to the inhibitors branched-chain c~-keto acids in rat *To whom correspondence should be addressed /98/ /0 Copyright by Acctdemic Press Australia. All rights of reproduction in any form reserved,
2 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL skeletal muscle (12,13). The mechanisms for modulation of the activity of the enzyme complex by endurance training remained to be elucidated. In the present study, we measured the protein amount and the mrna abundance of BCKDH kinase in skeletal muscle of trained and untrained rats and showed that endurance training decreased the protein amount, but not the mrna abundance, in the muscle. Materials and Methods Materials: Thirty-two female Sprague-Dawley rats weighing g (5 weeks old) were obtained from CLEA Japan, Tokyo. Purified BCKDH kinase (3) and antiserum against the kinase (4) were prepared as described previously, c~-keto[1-zac]isocaproate, [c~-32p]dctp and 125I-labeled protein A were purchased from Amersham Japan, Tokyo. Other chemicals were of reagent grade. Animal care and endurance training: All procedures involving animals were approved by the experimental animal care committee of Sendai College. The rats were housed at 23~ with light from 07:00 to 19:00 h and with free access to laboratory diet (CE-2, CLEA Japan, Tokyo) and water. The rats (at 7 weeks old) were randomly divided into two groups; trained (n=16) and untrained (n=16) group. The former group of rats was trained by treadmill running for 5 weeks. The training program was as described previously (13). On the final day of the experiment, a half of rats in each trained and untrained group was run on the treadmill at 26 m/rain (up an 8 ~ incline) for 1 h. Immediately after running, the rats were killed by cervical dislocation and gastrocnemius muscles were rapidly removed and freeze-clamped at liquid nitrogen temperature, and stocked at -70~C until use. Another half of rats in each group was successively treated in the same manner without running exercise. Extraction and assay of BCKDH complex: Extraction of BCKDH complex from rat skeletal muscle and assay of the enzyme activity using a-keto[1-1*c]isocaproate as a substrate were performed as described previously (10). The basal activity of the enzyme complex (an estimate of in vivo activity) was determined using the muscle extract directly in the assay. For measurements of total enzyme activity, the preparations were activated before assay by dephosphorylation of the enzyme complex using MgSO 4 and broad specificity phosphoprotein phosphatase as described previously (10). The activity state of BCKDH complex was determined as the ratio of basal activity to total activity. Western blot analysis of BCKDH kinase: Western blot analysis of BCKDH kinase was performed as described previously (13). The standard curve of the kinase protein was prepared using the purified BCKDH ldnase in this quantitative analysis. Northern blot analysis of BCKDH kinase mrna : Total cellular RNA was isolated by the procedure described by Chomczynski and Sacchi (14). The concentration of the total cellular RNA extracted was spectrophotometrically determined (15). Northern blotting of the total cellular RNA (10 ~tg) was conducted by a standard protocol using rat BCKDH kinase and 13- actin (for internal standard) cdna probes as described previously (13). Statistical analysis: Results are expressed as mean _+ SE. Data were analyzed by two-way analysis of variance (ANOVA) and subsequently by unpaired Student's t-test of multiple comparison. Values were considered to be significantly different at P<0.05. Results Effects of endurance training on the activity of BCKDH complex in rat skeletal muscle: The basal activity of BCKDH complex was ~8% and -12% of the total activity in untrained and trained rats, respectively, and the enzyme activities were significantly increased to ~14% and ~23%, respectively, by acute running exercise for i h on the final day of the experiment (Fig. 1). Both the basal activity and the elevated activity were significantly higher in 1212
3 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL v X 30 I I I ] 7." [ - - I [ - - I E o O -I- 20 nn "6 10 >,m < L I L ] Untrained Trained Fig. 1. Effects of endurance training on the activity state of BCKDH complex in rat skeletal muscle. Exercised rats in both untrained and trained groups were run on the treadmill at 26 m/min (up an 8 ~ incline) for 1 h before killed, and sedentary rats in both groups were killed without running exercise on the final day of the experiment. Values are means +_ SE for 8 rats. *P<0.05. trained rats than in untrained rats. On the other hand, the total activity of BCKDH complex was not significantly different among all the groups (data not shown). Effects of endurance training on the protein amount of BCKDH kinase in rat skeletal muscle: The protein amounts of BCKDH kinase in skeletal muscle of untrained and trained rats were ~40 and ~28 ~tg/g tissue, respectively, indicating that the kinase content was decreased to ~0.7 fold by endurance training for 5 weeks (Fig. 2). On the other hand, the kinase content was not affected by acute running exercise for I h in either trained or untrained rats (Fig. 2). Effects of endurance training on BCKDH kinase mrna abundance in rat skeletal muscle: The mrna level for BCKDH kinase in skeletal muscle was only slightly increased by endurance training for 5 weeks but was not affected by acute running exercise for 1 h in either trained or untrained rats (Fig. 3). Discussion We found in the present study that skeletal muscle of untrained rats contained ~40 ~g of BCKDH kinase protein/g tissue. This amount of the kinase is greater than those of the 1213
4 BIOCHEMISTRY and MOLECULAR BIOLOGY INTERNATIONAL 50 "~ 40 e'- o I I 1 I "~ ~ m 4 I I I Untrained Trained Fig. 2. Effects of endurance training on a protein content of BCKDH kinase in rat skeletal muscle. Values are means _+ SE for 8 rats. *P< mg of gastrocnemius muscle tissue was analyzed by the Western blot analysis. The kinase protein in the tissue was quantitated using the standard curve of the purified BCKDH kinase. components of BCKDH complex reported before (13). This high content of the kinase relative to BCKDH complex in rat skeletal muscle may be responsible for markedly low activity state of the BCKDH complex in skeletal muscle of rats under the rested conditions. In our previous study, it was found that activation of BCKDH complex in skeletal muscle by starvation and leucine administration was greater in trained rats than in untrained rats (12). Since the activity of the enzyme complex is regulated by the phosphorylation and dephosphorylation cycle and branched-chain ec-keto acids, especially c~-ketoisocaproate from leucine, are reported to be potent inhibitors of BCKDH kinase (2), it was suggested that BCKDH kinase in skeletal muscle is sensitized by endurance training for 5 weeks to the inhibitors (12). Furthermore, it was found in the present study that activation of muscle BCKDH complex by acute running exercise was greater in trained rats than in untrained rats. These findings suggest that BCKDH kinase in skeletal muscle might be modulated by endurance training. Actually, it was found that the protein amount of BCKDH kinase in skeletal muscle was decreased by training for 5 weeks, suggesting that the mechanisms of greater activation of muscle BCKDH complex by acute exercise in trained rats involves an adaptive decrease in the BCKDH kinase content in response to the endurance training for 5 weeks. These results may be 1214
5 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL z~ h- E o 40 < z 30 f I ;p. 1 ~ "- 20 r- r" 0 v ~ m ~_ 10.1:1 < v [ J L I Untrained Trained Fig. 3. Effects of endurance training on the mrna abundance of BCKDH kinase in rat skeletal muscle. Values are means _+ SE for 8 rats. *P< ~tg of total RNA extracted from gastrocnemius muscle was analyzed by the Northern blot analysis. supported by the findings of Espinal et al. (17) and Harris et al. (18), who have reported that the decrease in rat liver BCKDH complex activity caused by the protein starvation was associated with an adaptive increase in the BCKDH kinase activity. Endurance training for 5 weeks resulted in divergent pattern of expression of the mrna for BCKDH kinase in rat skeletal muscle. The mrna abundance of BCKDH kinase in rat skeletal muscle was slightly increased by endurance training for 5 weeks, although the protein amount was decreased by the training. These results suggest that the level of protein expression of BCKDH kinase in response to endurance training is regulated by translational and/or posttranslational steps. On the other hand, Popovet al. (19) observed that an increase of BCKDH kinase content in response to dietary protein starvation in rat liver was associated with an increase in the abundance of the mrna, suggesting that gene expression of the BCKDH kinase might be regulated in an organ specific manner. References 1. Harper, A. E., Miller, R. H., and Block, K. P. (1984) Annu. Rev. Nutr. 4, Paxton, R., and Harris, R. A. (1982) J. Biol. Chem. 257, Shimomura, Y., Nanaumi, N., Suzuki, M., Popov, K. M., and Harris., R. A. (1990) Arch. Biochem. Biophys. 283, Shimomura, Y., Nanaumi, N., Suzuki, M., and Harris, R. A. (1991) FEBS Lett. 288,
6 BIOCHEMISTRYand MOLECULAR BIOLOGY INTERNATIONAL 5. Popov, K. M., Zhao, Y., Shimomura, Y., Kuntz, M. J., and Harris, R. A. (1992) J. Biol. Chem. 267, Wagenmakers, A. J. M., Schepens, J. T. G., and Veerkamp, J. H. (1984) Biochem. J. 223, Kasperek, G. J., Dohm, G. L., and Snider, R. D. (1985) Am. J. Physiol. 248, (Regulatory Integrative Comp. Physiol. 17), R166-R Aftring, R. P., Block, K. P., and Buse, M. G. (1986) Am. J. Physiol. 250, (Endocrinol. Metab. 13), E599-E Kasperek, G. J., and Snider, R. D. (1987) Am. J. Physiol. 252 (Endocrinol. Metab. 15), E33-E Shimornura, Y., Suzuki, T., Saitoh, S., Tasaki, Y., Harris, R. A., and Suzuki, M. (1990) J. Appl. Physiol. 68(1), Shimomura, Y., Fujii, H., Suzuki, M., Fujitsuka, N., Naoi, M., Sugiyama, S., and Harris, R. A. (1993) Biochim. Biophys. Aeta 1157, Fujii, H., Shimomura, Y., Tokuyama, K., and Suzuki, M. (1994) Biochim. Biophys. Acta 1199, Fujii, H., Tokuyama, K. Suzuki, M. Popov, K. M., Zhao, Y., Harris, R. A., Nakai, N., Murakami, T., and Shimomura, Y. (1995) Biochim. Biophys. Acta 1243, Chomczynski, P., and Sacchi, N. (1987) Anal. Biochem. 162, Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: Plainview, Corld Spring Harbor, New York. 16. Williams, R. S., Salmons, S., Newsholme, E. A., Kaufman, R. E., and Mellor, J. (1986) J. Biol. Chem. 261, Espinal, J., Beggs, M., Patel, H., and Randle, P. J. (1986) Biochem. J. 237, Harris, R. A., Paxton, R., Powell, S. M., Goodwin, G. W., Kuntz, M. J., and Hart, A. C. (1986) Adv. Enzyme Regul. 25, Popov, K. M., Zhao, Y., Shimomura, Y., Jaskiewicz, J., Kedishvili, N. Y., Irwin, J., Goodwin, G. W., and Harris, R. A. (1995)Arch. Biochem. Biophys. 316,
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