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1 Laboratory of Muscle Physiology, Faculty of Education, Kumamoto University, Kumamoto 860-8555; 2 Laboratory of Neurochemistry, Faculty of Integrated Human Studies, Kyoto University, Kyoto 606-8316; 3 School of Health and Sport Sciences, Osaka University, Osaka 560-0043, Japan; and 4 Brain Research Institute, University of California, Los Angeles, California 90095
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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An original method to induce heat stress was used to clarify the time course of changes in heat shock proteins (HSPs) in rat skeletal muscles during recovery after a single bout of heat stress. One hindlimb was inserted into a stainless steel can and directly heated by raising the air temperature inside the can via a flexible heater twisted around the steel can. Muscle temperature was increased gradually and maintained at 42°C for 60 min. Core rectal and contralateral muscle temperatures were increased <1.5°C during the heat stress. HSP60, HSP72, and heat shock cognate (HSC) 73 content in the slow soleus and fast plantaris in both limbs were determined immediately (0 h) and 2, 4 , 8, 12, 24, 36, 48, or 60 h after heat stress. Within 0-4 h, all HSPs were ~1.5- to 2.2-fold higher in heat-stressed than contralateral soleus. Compared with the contralateral plantaris, the heat-stressed plantaris had a higher (1.5-fold) HSP60 content immediately and 2 h after heat stress and a higher (2.5- to 6.8-fold) HSP72 content between 24 and 48 h after heat stress. Plantaris HSC73 content was not affected by heat stress. This unique heat-stress method provides advantages over existing systems; muscle temperature can be controlled precisely during heating and the HSP response can be compared between muscles in heat-stressed and contralateral limbs of individual rats. Results show a differential response of HSPs in the soleus and plantaris during recovery after heat stress; soleus demonstrated a more rapid and broader HSP response to heat stress than plantaris.
heat shock proteins; heat stress; rat; soleus; plantaris
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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HEAT SHOCK PROTEINS (HSPs) are induced in cells by heat or several other types of stresses and are often used as markers of stress and adaptation in a variety of physiological systems. The most stress-inducible type of HSPs belong to the HSP70 family, which have a molecular mass of 70 kDa (37). Several studies show that HSPs protect mammalian cardiac muscle from ischemic injury (14, 25), but the precise functions or mechanisms for the induction of HSPs in mammalian skeletal muscles are unclear (21). In the hindlimb musculature of sedentary unstressed rats, the levels of HSP72 are significantly different among individual muscles, whereas the levels of heat shock cognate (HSC) 73 are similar among the muscles (8). In addition, the levels of HSP72 appear to be related to the percentage of slow oxidative fibers of individual muscles in sedentary animals (23). Both HSP72 and HSC73 are located in the cytosol and/or nuclei of the cell, whereas HSP60, one of the mitochondrial HSPs having a molecular mass of 60 kDa, is synthesized in the cytoplasm, migrates to the mitochondria, and functions to facilitate polypeptide maturation (14, 37).
Exposure to heat is a traditional and often-used method to induce the expression of HSPs. HSPs, especially HSP72, are increased significantly in a variety of cells and/or organs, including skeletal muscles, when the organism is exposed to heat stress (12, 22). There are no studies, however, comparing HSP levels in muscles of a heat-stressed vs. a non-heat-stressed limb within the same animal. In addition, the response of HSP60 in skeletal muscles of varying fiber-type compositions to heat stress has not been investigated. Furthermore, few studies have investigated the time course of the response of specific HSPs in rodent skeletal muscles after heat stress. These seem to be important issues because the time course for changes in the levels of specific HSPs can be significantly different among body organs after heat stress (9) or between slow and fast muscles after denervation or tenotomy (11).
In the present study, therefore, we developed a method to expose one hindlimb of rats to heat stress for 1 h and used the contralateral limb as an internal control to determine the responses of HSP60, HSP72, and HSC73 proteins in the slow soleus and fast plantaris muscles. These muscles were selected for study because they are both plantar flexors and thus allow for a comparison of the response to heat stress of synergists having different fiber-type distributions and contrasting mechanical and biochemical properties. We also determined the time course of the changes in HSPs during 60 h of recovery after exposure to this single bout of heat stress. On the basis of previous results suggesting a muscle (fiber)-specific response to HSP induction associated with other perturbations such as exercise, denervation, and tenotomy (8, 11, 23), we hypothesized that the initial response to and recovery from heat stress would be different for slow and fast muscles and that the temporal modulation would be different for each HSP studied. Our results were consistent with these hypotheses and showed both muscle type- and a HSP-specific responses during recovery after heat stress.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. Adult male Wistar rats (n = 45) were used in this study. Soleus and plantaris muscles of the left hindlimb served as the experimental heat-stressed group and those of the right hindlimb served as the contralateral control group. All experimental procedures and animal care procedures were approved by the Committee on Animal Care and Use at Kumamoto University and followed the Guiding Principles for the Care and Use of Animals in the Field of Physiological Sciences established by the Physiological Society of Japan and the American Physiological Society animal care guidelines.
Heat-stress procedures. Rats were anesthetized deeply (20% ethyl carbamate, 500 µl/100 g body wt) and placed in a supine position on a soft foam pad. The limbs were extended and secured with surgical tape. A thermistor probe (type PI, Shibaura Electronics) was inserted into the rectum to monitor core temperature and secured to the tail with the use of surgical tape. Standard lead II recordings of the electrocardiograms were obtained by using small, steel safety pins as electrodes. The electrodes were inserted subcutaneously into the proximal, ventral region of both arms and the right leg to monitor heart rate.
A small skin incision (~10 mm) was made at the rostral, medial surface of each thigh, and a copper-constantan thermocouple temperature sensor (T-6F, Ninomiya Dennsen) was tunneled subcutaneously to the surface of the medial gastrocnemius muscle. The left hindlimb then was inserted carefully into a stainless steel can (50-mm diameter and 90-mm length) such that the hindlimb did not contact the inner wall of the steel can. Soft cotton was used to cushion the leg. The left hindlimb was heat stressed by raising the air temperature inside the steel can with the use of a flexible heater (FH-1, Masuda Rika Kogyo), which was coiled and secured around the steel can. Air temperature inside the steel can was raised to 56 ± 2°C, monitored via a thermal sensor (T-6F), and controlled by an automatic temperature-controlling unit (REX C100FK-V, Rika Kogyo) connected to the sensor. The muscle temperature of the heat-stressed limb was gradually increased and reached 42°C during the first 10 min of heating. Muscle temperature then was maintained at 42°C for the next 60 min (Fig. 1). This temperature was selected because several previous studies have used whole body hyperthermia at 42°C as the heat stress (4, 5, 10) and the average temperature of the rat hindlimb musculature can reach at least 42°C after exhaustive exercise sessions (2). Temperature in the contralateral hindlimb, core body temperature (rectum), and heart rate were monitored during the entire heat-stress period. Room temperature and humidity were controlled at 22 ± 1°C and 60%, respectively, throughout the study.
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Muscle preparation.
Soleus and plantaris muscles (5 rats/time point) were removed
bilaterally either immediately or 2, 4, 8, 12, 24, 36, 48, or 60 h
after the 1-h heat-stress period. Muscles were cleaned of excess fat
and connective tissue, wet weighed, quickly frozen in isopentane cooled
by liquid nitrogen, and stored at 
85°C. Muscle samples were
homogenized with 10 vol of buffer containing (in mM) 10 Tris, 10 NaCl,
0.1 EDTA, and 15 mercaptoethanol (pH 7.6), according to the procedures
of Kilgore et al. (13). After centrifugation at 12,000 g for 20 min, the supernatants were boiled in sample buffer
(19) for 2 min at a final protein concentration of 1 µg/µl, according to the method of Bradford (1), and
then subjected to HSP analysis.
SDS-PAGE. HSP proteins were separated by using 10% acrylamide separating and 4% stacking minigels by standard electrophoretic methods (19). Electrophoresis was continued at 30 mA (constant current/gel) for ~60 min until the dye front migrated to the bottom of the gel, at which time the gel was subjected immediately to Western blotting.
Western blotting. Gels were transferred to nitrocellulose sheets by using a semidry blotting unit (model FB-SDB-2020, Fisher Biotech) at 50 mA (constant current/gel) for 2 h, as described previously (32). After the transfer, blots were blocked with 2.5% BSA in Tris-buffered saline (TBS) with Tween 20 (TTBS; 100 mM Tris · HCl, pH 7.5, 0.9% NaCl, and 0.1% Tween-20) for 1 h at room temperature. After being washed twice in TTBS for 10 min each, blots were incubated in the primary anti-HSP60 (SPA-807, StressGen, Victoria, BC, Canada), anti-HSP70 (SPA-810, StressGen), and anti-HSC70 (SPA-815, StressGen) antibodies diluted 1:1,000 in TTBS for overnight at 4°C. After being washed twice with TTBS for 10 min each, blots were incubated with horseradish peroxidase-conjugated rabbit anti-mouse IgG or anti-rat IgG (A-9044 or A-5795 diluted 1:1,000 in TTBS, Sigma Chemical) for 2 h at room temperature. Blots then were washed in TTBS and TBS (100 mM Tris · HCl, pH 7.5, and 0.9% NaCl) for 15 min each and reacted for ~10 min with H2O2 solution (diluted 1:1,000 with TBS) by using 3,3-diaminobenzidine (D5637, Sigma Chemical) as a substrate. Quantification of the HSP proteins was performed by using the National Institutes of Health Image system, and the data were expressed as a percentage of the content in contralateral control muscles. To ensure uniformity, only bands within the same blot were used to compare the relative amounts of each protein among groups.
Statistical analyses. All data are presented as means ± SE. Differences between groups were determined by using one-way ANOVA followed by Fisher's paired least-significant difference post hoc tests. All differences were assumed to be significant at P < 0.05.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Body and muscle masses. The overall mean body mass of the rats was 355 ± 4 g (n = 45). Mean soleus and plantaris masses were similar in control and heat-stressed limbs at each time point. The muscle masses of the heat-stressed limb relative to the contralateral control limb ranged from 0.96 to 1.02 g for the soleus and from 0.97 to 1.02 g for the plantaris.
Core and muscle temperatures. Figure 1 shows the time course of the changes in temperature for the core (rectum), and right (control) and left (heat-stressed) hindlimbs (medial gastrocnemius) in one experimental rat during 1 h of heat stress. All rats showed a similar response. The temperature of the muscle surface in the heat-stressed hindlimb gradually reached ~42°C about 10 min after the onset of the heat stress and was maintained at 42°C for 60 min (Fig. 1). The core temperature and the temperature of the contralateral hindlimb (medial gastrocnemius) increased slightly from 35.5 ± 0.1 and 34.5 ± 0.2°C to 36.6 and 35.8°C, respectively, during the same period.
Relative content of HSPs.
Representative expression patterns of the HSP60, HSP72, and HSC73
proteins in the soleus and plantaris muscles at several recovery time
points after 1 h of heat stress are shown in Fig. 2. HSP60 content was significantly
greater in heat-stressed than control soleus immediately (161 ± 16%) and 2 h (189 ± 19%) after heat stress (Fig.
3). Similarly, HSP60 content in the
plantaris was increased significantly immediately (159 ± 16%)
and 2 h (141 ± 22%) after heat stress (Fig.
4). Thereafter, the levels of HSP60 were
similar to control in both muscles.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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A novel method for inducing heat stress in a single rat hindlimb
was used in the present study. Restricting the heat stress to one limb
made it possible to compare the responses of various HSPs in the
muscles of a heat-stressed and a non-heat-stressed (contralateral
control) hindlimb of the same rat. This is an important technical
advancement in that previous studies have compared the HSP responses in
heat-stressed animals and age-matched controls (3, 4, 5, 8, 10,
15, 16, 27, 30, 33, 35). The small increases in the core and
contralateral limb muscle temperatures did not affect the HSP levels:
HSP levels were similar in the contralateral control soleus or
plantaris muscles of heat-stressed rats and in age-matched sedentary
controls. These data are consistent with the observation that whole
body heating until the rectal temperature is raised 
3°C has no
effect on the HSP72 levels in the rat left ventricle (10).
Combined, these results indicate that the muscles in the contralateral
hindlimb are valid controls for determining the HSP responses in
muscles of the heat-stressed hindlimb.
The major findings in the present study were 1) the patterns of the response to heat stress for the three HSPs studied were similar in the soleus but different in the plantaris; and 2) the pattern of adaptation of HSP60 was similar in the soleus and plantaris, whereas HSP72 and HSC73 showed muscle-specific responses. In the soleus, all HSPs showed a rapid and transient elevation to the heat stress; i.e., there was a significant increase (~1.5- to 2.2-fold) between 0 and 4 h after the heat stress and then a return to baseline levels. In the plantaris, HSP60 showed a rapid and transient increase (~1.4- to 1.6-fold increase immediately and 2 h after the heat stress), HSP72 showed a later and larger increase (~2.5- to 3-fold increase at 24 and 36 h and 7-fold increase at 48 h after the heat stress), and HSC73 was not affected by heat stress. In general, these data support our hypotheses for both an HSP-specific and a muscle type-specific response during recovery after heat stress.
Muscle-specific and HSP-specific responses to heat or other stresses
also have been reported. Flanagan et al. (4) reported that
an elevation of core temperature in rats to ~40 to 42°C for 24 min
enhanced the HSP72 levels in the liver, small intestine, or kidney but
not in the brain or quadriceps muscles. Skidmore et al.
(35) reported that heat stress (colonic temperature
elevated to 41°C for 1 h) or a single bout of treadmill running
(17 m/min for 1 h) significantly enhanced the HSP72 levels by
approximately three- to fourfold in the rat soleus and gastrocnemius
muscles but not in the extensor digitorum longus muscle. Treadmill
training concomitant with body hyperthermia enhanced HSP72, but not
HSC73, by greater than fourfold in the rat cardiac muscle
(30). Electrical stimulation of skeletal muscles also
induced HSP-specific responses. For example, Neufer and colleagues
(28, 29) reported the time course for changes of several
HSPs in the rabbit tibialis anterior muscle during continuous
electrical stimulation for 21 days. The stimulated tibialis anterior
muscles were analyzed after 4 or 8 h or after 1, 3, 7, 14, or 21 days of stimulation. The levels of HSP72 increased by 3- to 9-fold
after 1-7 days of stimulation and by 4- to 20-fold after 14-21
days of stimulation. In contrast, the levels of HSP60 were unchanged
after up to 7 days of stimulation but then increased fivefold after
14-21 days of stimulation (29). In addition, the
smaller HSPs (i.e., HSP27 and 
B-crystallin) were increased by 1.8- and 2.5- to 4-fold, respectively, after 1-21 days of continuous
electrical stimulation (28). All of these results indicate
that the adaptations of HSPs in skeletal muscle or other organs to a
stressor are dependent on a number of factors to include the type of
stress, the specific muscle or organ being analyzed, and the specific
HSP being measured.
As described above, the magnitude of increase in HSPs associated with exercise (30, 35) or electrical stimulation (28, 29) is somewhat larger than that observed with heat stress in the present study. This was not unexpected, since both electrical stimulation and exercise increase the levels of muscular activity. Elevated muscle activity, in turn, most likely enhances free radical and/or lactate production, muscle (fiber/membrane) injury, humoral/hormonal factors, ATP consumption, and the metabolic rate, all of which appear to be related to the synthesis of HSPs in muscles. For example, recent studies have reported a close relationship between the duration and/or intensity of exercise and the level of enhancement of HSPs (3, 21, 30). In addition, an increase in muscle temperature during electrical stimulation (29) or body temperature during exercise (35) is not necessary to increase muscle HSP levels, suggesting that non-heat-stress factors associated with muscle contractile activity are important determinants of HSP induction under these conditions.
In the present study, the transient induction of HSPs in the rat soleus or plantaris muscles had different time courses and were HSP specific. Some data for the time course of induction of HSPs after heat stress are consistent with these observations. For example, HSP72 was induced in IEC-18 cells, a cultured cell derived from rat small intestine, by heat stress at 42°C for 20 min, and this induction continued 1-5 h after heat stress (26). Hotchkiss et al. (9) reported a temporal increase in HSP72 after heat stress; i.e., HSP72 levels were increased in the intestine, kidney, lung, heart, liver, and brain at 8 h and peaked at 12 h after the mice core temperature was raised to 42.5°C for 20 min. Thereafter, the levels gradually decreased and reached control values ~24 to 48 h after the heat stress.
The present results indicate that mitochondrial HSP60 is a heat stress-inducible protein and that its level and early time course of induction in the slow soleus and fast plantaris muscles are similar (Figs. 3 and 4). Recent studies, however, have reported muscle-specific adaptations in the levels of HSP60 and another mitochondrial HSP, i.e., glucose-regulated protein (GRP) 75, in rat skeletal muscles after prolonged endurance training. For example, Mattoson et al. (24) reported that 8 wk of treadmill running (27 m/min, 60 min/day, 10% incline, 6 days/wk; Wistar rats) increased HSP60 and GRP75 levels by 103 and 105%, respectively, in the plantaris, whereas the soleus muscle was unaffected. In contrast, Samelman (34) reported that 16-20 wk of treadmill running (15 m/min, 60 min/day, 10% incline, 5 days/wk; Fischer 344 rats) resulted in a 70% increase in HSP60 in the soleus and no change in the lateral portion of the gastrocnemius muscle, a synergist of the plantaris. GRP75 levels also have been reported to increase in the soleus (1.8-fold) and extensor digitorum longus (2.3-fold) muscles after 3, but not 1 or 2, mo of an incremental program of treadmill running (20-30 m/min, 30-85 min/day, 0-8% incline, 5 days/wk; Wistar rats) (7). All of the results indicate that mitochondrial HSPs in skeletal muscle are responsive to both heat and exercise stress, although the response to prolonged training appears to be somewhat variable.
What is the role(s) of HSPs in skeletal muscles? Several lines of evidence indicate that an elevation in HSPs (especially HSP72) induced by pretreatment with a heat stress has a protective effect against subsequent stresses (14). For example, the survival rate of mice administered a lethal dose of endotoxin was higher in mice pretreated with a heat stress than in non-heat-stressed animals at various time points after the heat stress (9). In addition, the survival rate was greatest if the endotoxin was administered 12 h after the heat stress, i.e., the time when the expression level of HSP72 was highest. Naito et al. (27) reported that heat stress (elevation of the colonic temperature to 42°C for 60 min and a concomitant increase in HSP72) before an 8-day period of hindlimb unloading in rats attenuated atrophy of the soleus muscle. Compared with sedentary cage control rats, hindlimb unloading resulted in a 25% atrophy of the soleus muscle and a 40% decrease in the level of HSP72. When pretreated with heat stress, the soleus atrophied by 17% and had >20% higher HSP72 levels than control after 8 days of unloading. It was postulated that the elevated levels of HSP72 could have retarded muscle atrophy by both maintaining protein synthesis and decreasing the rate of protein breakdown via its known functions in determining the elongation rates of nascent polypeptides (17, 18).
Similarly, preheating rats in a warm water bath for 20 min to attain a core temperature of 42.5°C protected the gastrocnemius muscle from ischemic injury (wrapping a rubber band tightly 8 times around the proximal thigh for 90 min) as assessed by electron microscopy (6). The recent study by Lepore et al. (20) also indicates that prior heat stress to rat skeletal muscles induces the expression of HSP72 and protects the muscle against subsequent ischemia-reperfusion injury. Furthermore, Smolka et al. (36) have suggested that HSP72 may have a complimentary protective role against exercise-induced oxidative stress in the rat soleus muscle. These authors suggest that HSP72 is part of a secondary defense system acting to provide fast additional protection when the main system (antioxidant enzymatic activity) is attacked by exercise-induced oxidative stress.
In the present study, the more rapid response in HSP72 synthesis in the soleus than in the plantaris muscle suggests that slow muscles may be more responsive to stressful conditions than fast muscles. This differential response, however, also could be related to the fact that slow muscles have a higher protein turnover rate than fast muscles (29). In addition, because slow muscles have higher levels of HSP72 than fast muscles even under the sedentary control conditions (7, 8), the soleus may have an innate ability to synthesize HSP72 more rapidly than fast muscles when a stress is added.
Perspective. It is well known that exercise and heat stress induce muscle fiber injury or protein degradation. Because HSPs function to maintain the homeostasis or preserve cellular function under stressful conditions in other tissues (14, 37), it is speculated that HSPs are involved with the repair of injured or denatured proteins and the maintenance of a homeostatic state in skeletal muscles exposed to stress. Skeletal muscle is a highly adaptive tissue; its response to alterations in functional demands can include changes in muscle fiber morphological, phenotype, metabolic, and mechanical properties. The role that HSP induction may play in skeletal muscle plasticity needs to be studied further.
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ACKNOWLEDGEMENTS |
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The authors are grateful to S. Yamaguchi and K. Okadera for technical assistance in performing the present experiment.
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FOOTNOTES |
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A portion of this study was supported by grants from the Ministry of Education, Science, Sports, and Culture of Japan, National Space Development Agency of Japan, Japan Space Forum (Ground Research for Space Utilization), and the Institute of Space and Astronautical Science, Japan.
Address for reprint requests and other correspondence: Y. Oishi, Laboratory of Muscle Physiology, Faculty of Education, Kumamoto Univ., Kumamoto 860-8555, Japan (E-mail: oishi{at}gpo.kumamoto-u.ac.jp).
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.
10.1152/japplphysiol.00739.2001
Received 17 July 2001; accepted in final form 5 November 2001.
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METHODS
RESULTS
DISCUSSION
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