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School of Kinesiology, Faculty of Health Sciences, and Lawson Health Research Institute, University of Western Ontario, London, Ontario, Canada N6A 3K7
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Exercise induces expression of the protective heat shock protein, HSP70, in striated muscle. To characterize the relationship between induction of this protein and exercise intensity in muscles exhibiting different recruitment patterns, male Sprague-Dawley rats were assigned to a sedentary control or one of seven exercise groups for which treadmill running speed varied between 15 and 33 m/min (n = 8/group). Twenty-four hours after a single 60-min exercise bout, hearts, red and white portions of the vastus (RV and WV, respectively) muscles, and soleus (Sol) muscles were harvested and analyzed for both relative and absolute HSP70 content. Cardiac HSP70 was significantly elevated only when animals were exercised at 24 m/min and beyond. Similarly, HSP70 was elevated in RV at running speeds above 24 m/min but did not increase in WV until 27 m/min. In contrast, HSP70 content was initially elevated in the Sol but subsequently declined at the highest running speeds. The observed patterns of HSP70 expression in skeletal muscle were in general accordance with known muscle recruitment patterns and suggest that alterations in muscle loading, resulting from changes in exercise intensity, are an important component of exercise-induced increases in HSP70 content.
heart; skeletal muscle; rat; treadmill running; stress proteins; heat shock protein 70
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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CELLS OVEREXPRESSING THE inducible member of the 70-kDa family of heat shock proteins (HSP70) become resistant to otherwise lethal levels of stress (for review see Ref. 11). In mammals, HSP70 is associated with the protection of striated muscle from ischemia-reperfusion injury (14, 20, 21, 29, 31) and the attenuation of skeletal muscle atrophy during hindlimb unweighting (25). Moreover, transgenic mice overexpressing HSP70 show enhanced contractile and metabolic myocardial recovery postischemia, providing evidence for the vital role of HSP70 in this protection (21, 31). Not surprisingly then, the exposure of cells to various sublethal stresses results in an adaptive increase in HSP70 as a survival mechanism (11). Exercise is one such stressor that increases the content of HSP70 in cardiac and skeletal muscle (26) and may represent a powerful therapeutic agent against ischemia-reperfusion injury (29). The relative exercise intensity required to elicit this potentially beneficial increase in HSP70 is not well known, however. Recently, Noble et al. (27) found that rats allowed to exercise voluntarily on a free wheel (low-intensity exercise) for 8 wk did not exhibit significant increases in cardiac HSP70 content. This contrasted with the elevated levels found in animals trained to run on a treadmill at a speed of 30 m/min (high-intensity exercise). Even when animals that trained at low intensity ran for similar or greater weekly distances than did their high-intensity-trained counterparts, only high-intensity exercise was able to induce significant increases in HSP70 (27). Similarly, Liu et al. (16) found that exercise-induced elevations of HSP70 in the vastus of male rowers were more dependent on the intensity of each exercise bout rather than exercise duration during a multiweek training protocol. Because these studies suggested a relationship between intensity-dependent changes in muscle loading and HSP70 expression, we set out to characterize this association by examining HSP70 content in cardiac tissue and hindlimb muscles from rats acutely exercised at several running speeds. It was hypothesized that not only would the increase in muscle HSP70 content exhibit an intensity-dependent threshold but also the threshold in individual skeletal muscles would be related to their known recruitment patterns.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals
Use and treatment of laboratory animals was approved by the University of Western Ontario Council on Animal Care according to the guidelines of the Canadian Council on Animal Care. Adult male Sprague-Dawley rats (~220 g and 8 wk of age) were obtained from Charles River Laboratories and housed in triplicate in standard shoe box rat cages. The vivarium was maintained at constant temperature and humidity with a 12:12-h light-dark cycle. All rats were fed LabDiet 5P00 standard rat chow and water ad libitum.Acute-Exercise Protocol
After being housed for 1 wk, the rats were randomly assigned to either a sedentary control group (Con; n = 8) or one of seven exercise groups (15, 18, 21, 24, 27, 30, and 33 m/min on a 2% incline; n = 8 /group). All rats were familiarized with treadmill running for 10 min on 3 alternating days in the week leading up to the acute exercise bout. Familiarization consisted of 2 min running at 15 m/min, 4 min at 24 m/min, 2 min at 30 m/min, and 2 min at 15 m/min, all at a 2% incline. Rats were encouraged to run with a gentle air blast that blew on their hindquarters when the rats broke a photosensor beam near the rear of the treadmill. Although the air blast was generally sufficient to keep the rats running, if they stopped on the grid at the back of the treadmill, they were further encouraged to run by the administration of a brief electric shock. Neither the familiarization nor the stimuli used to encourage running elicit a significant heat shock or stress response (Noble EG, Ho R, and Dzialoszynski T, unpublished observations). Each exercise bout consisted of continuous treadmill running at room temperature (~21°C) at one of the designated speeds for a period of 60 min. Animals were weighed, and rectal temperature was measured immediately before the exercise bout by using a thermometer inserted 5 cm into the rectum. Rectal temperature was then measured every 15 min during the exercise bout and immediately after the run. Con rats were handled similarly to their exercising counterparts without being placed on the treadmill. All animals completed the full hour of their respective exercise bouts.Blood Collection
Blood was collected by tail clipping exactly 5 min after each rat had finished its exercise bout. Whole blood was centrifuged at 17,000 g for 10 min, after which the serum was carefully pipetted out and transferred to microcentrifuge tubes for later analysis. Blood was taken from Con rats at similar times during the day and treated as indicated. Duplicate measurements of serum lactate were made on a Yellow Springs Instruments 2300 STAT Plus glucose and lactate analyzer and expressed as millimoles per liter.Heart Rate Measurements
A separate group of animals, of comparable weight and age to those above (n = 3), was used to determine resting, maximum, and exercise heart rates at various running speeds. These animals were given a surgical dose of pentobarbital sodium (65 mg/kg), and then an electrode was implanted under the skin at the nape of the neck. One week after surgery, resting and exercise heart rates were determined. Heart rates were measured at rest while the animals stood on the nonmoving treadmill. Exercise heart rates were measured by running the animals for 2 min intervals (at which point heart rates had stabilized) at progressively increasing speeds. Maximum heart rate was determined when a plateau in HR was reached even after running speed was increased.Tissue Collection
Twenty-four hours after the acute exercise bout, animals were anesthetized (65 mg/kg pentobarbitol sodium) and weighed, and the heart, red and white portions of the vastus (RV and WV, respectively), and soleus (Sol) were harvested, rapidly frozen in liquid nitrogen, and stored at
70°C until further analysis. The heart represents an
organ that may particularly benefit from increased HSP70 content (37), and the RV, WV, and Sol represent muscles that
exhibit different fiber-type profiles and recruitment patterns
(1, 2, 13). Sol is a posturally active muscle, rich in
slow oxidative (SO) fibers [87% SO and 13% fast oxidative glycolytic
(FOG) fibers]. In contrast, RV and WV are composed of 9 and 0% SO, 56 and 3% FOG, and 35 and 97% fast glycolytic (FG) fibers, respectively (1), and are sequentially recruited at increasing running
speeds (13).
SDS-PAGE
Approximately 70 mg of tissue were cut from the midbelly of frozen muscle samples or from the apex of the heart and immediately homogenized in 19 vol of homogenizing buffer (600 mM NaCl and 15 mM Tris base, pH 7.5). Sample homogenates were then stored at70°C
until the time of total protein concentration determination and
electrophoresis. Total protein concentration was accomplished with the
use of the bicinchoninic acid protein assay (36).
Muscle homogenates were mixed with an equal volume of sample buffer
(0.5 M Tris base, 13% glycerol, 0.05% SDS, 13%
2-
-mercaptoethanol, and bromophenol blue) and heated for 3 min at
100°C in boiling water. Samples were then cooled to room
temperature and spun at 20,000 g for ~20 s. Equal amounts
of protein (RV, SOL = 40 µg/well; heart = 50 µg/well; and
WV = 100 µg/well) from each sample were loaded into the wells
and then separated according to their molecular weights by running the
gel for 2 h at a constant 110 V in running buffer (25 mM Tris
base, 200 mM glycine, and 0.1% SDS, pH ~8.3). A sample known to
express HSP70 in high levels (male rat Sol) and a broadband molecular
weight standard (Bio-Rad Kaleidoscope prestained standard) were run
concurrently on each gel for accurate determination of HSP70. The gels
consisted of a 4% acrylamide stacking gel overlaying a 12% acrylamide
separating gel (12).
HSP70 Western Blotting
After electrophoresis, the proteins were transferred overnight at constant voltage to nitrocellulose membranes in transfer buffer (10% running buffer, 20% methanol in doubly distilled H2O). The membranes were blocked in a 5% nonfat dry milk (Blotto) powder solution in Tris-buffered saline (TBS; 80 mM Tris base and 0.5 M NaCl) for 6 h and then washed three times in TTBS (0.05% Tween 20 in TBS). Membranes were then incubated in primary antibody specific to HSP70 (anti-HSP70 polyclonal antibody, StressGen SPA-812) diluted 1:4,000 in TTBS with 2% Blotto powder overnight. Membranes were washed again in TTBS and then incubated in secondary antibody (goat anti-rabbit alkaline phosphatase conjugate antibody, Bio-Rad 170-6518) diluted 1:3,000 in TTBS with 2% Blotto for 2 h. After washes in TTBS and TBS, the blots were developed by using 5-bromo-4-chloro-3-indolyl phosphate/nitro blue tetrazolium color-developing reagents (Bio-Rad 170-653) in 100 ml of bicarbonate buffer. The blots were dried and scanned, and then Scion image blot analysis software was used for densitometric quantification.HSP70 ELISA
To complement and compare the observations made with Western blotting, changes in HSP70 content were also assessed by using a competitive ELISA as per Gutierrez and Guerriero (6). Briefly, 25 ng/well of purified HSP70 (StressGen SPP-755) in a carbonate buffer (15 mM Na2CO3, 35 mM NaHCO3, and 30 mM NaN3, pH 9.6) were added to 96-well microtiter styrene plates and allowed to incubate overnight at 4°C. Serially diluted standards (from 12.5 to 800 ng/100 µl) and homogenates used for Western blotting (27-35 µl) were brought to a final concentration of 1% SDS and boiled for 3 min. An adequate amount of antibody buffer [10 mM Tris (pH 7.4), 0.15 M NaCl, 30 mM NaN3, and 1% Triton X-100] to bring the samples to a final volume of 200 µl was then added. Samples without homogenate served as controls. Two hundred microliters of HSP70 antibody (StressGen SPA-812 diluted 1:1,000) were added to both standards and unknown samples, which were then incubated overnight at 4°C.The next day, wells were blocked for 15 min in 10 mM Tris (pH 7.4), 0.15M NaCl, 30 mM NaN3, and 0.25% Tween 20, and 100 µl each of standards and samples were subsequently added to blocked wells and incubated for 3 h at room temperature. After three washes with cold blocking buffer, 100 µl of the secondary antibody (goat anti-rabbit alkaline phosphatase conjugate diluted 1:2,500) were added to each well and incubated at room temperature for 2 h. Plates were then washed three times with TBS and 100 µl of freshly made p-nitrophenyl phosphate (1 mg/ml) in developing buffer (100 mM triethanolamine, 1 mM MgCl2, and 30 mM NaN3, pH 9.8) and incubated at 37°C until absorbance, measured at 405 nm, in wells without competitor reached 1.0. Amount of HSP70 in samples was calculated from a curve of absorbance vs. log of the standards.
Statistics
Statistical analysis was performed by using Sigma Stat for Windows Version 2.03. For the comparision of HSP70 levels among treatment groups, a one-way analysis of variance was used. On the finding of a significant F-ratio (P < 0.05), Dunnett's post hoc test was employed to determine significant differences from the Con group.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Heart Rate
In a separate group of animals, heart rates were measured to provide estimates of the exercise intensities at the different running speeds (Table 1). These data are similar to those previously recorded (3) and show that, from the lowest intensity of 15 m/min to the highest at 33 m/min, the animals were exercising at ~87-94% of their maximum heart rate.
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Serum Lactate
Serum lactate data are presented in Fig. 1. Lactate values were similar after exercise at all intensities except 33 m/min, indicating that at most treadmill speeds the animals were exercising below the lactate threshold.
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Animal Weight and Temperature Measurements
Animal weight and temperature measurements are presented in Table 2. Peak temperature (Tp) was approached by the 15th minute of exercise and was then maintained throughout. Increasing the intensity of exercise tended to result in lower postexercise body weights and higher Tp.
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HSP70 Expression
Both Western blotting and ELISA protocols generated similar results with regard to HSP70 expression, although in some instances the ELISA assay proved more sensitive and had the additional advantage of allowing absolute quantification of changes in HSP70 content.Cardiac muscle.
In cardiac tissue, HSP70 levels were similar between Con and exercise
groups up to a running speed of 21 m/min (Fig.
2). At speeds of 24 m/min and greater,
myocardial HSP70 content (ELISA data in Fig. 2) of exercised animals
was significantly increased (P < 0.05). This increase
became especially pronounced after exercise at 33 m/min, an exercise
intensity that exceeded the lactate threshold (Fig. 2).
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Skeletal muscle.
Like the heart, the RV (Fig. 3), a mixed
muscle high in FOG fibers (1), demonstrated a progressive
rise in HSP70 content from the slowest speed of 15 m/min. This increase
achieved significance at exercise intensities of 24 m/min and above
(P < 0.05). When assessed with use of ELISA, HSP70
levels rose to approximately sixfold those of nonexercised values at
the highest intensity (P < 0.05). In contrast, the WV
(Fig. 3), a muscle previously shown to have a majority of FG fibers
(1), exhibited similar HSP70 values between Con and all
exercise groups up to 24 m/min, inclusive. Exercise at 27 m/min caused
a 2.5-fold increase in HSP70 (P < 0.05), an increase
that was further enhanced (to almost 6 times that of Con values), after
running at 33 m/min (P < 0.05).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Exercise is associated with several mechanisms that may afford cardioprotection (7, 38, 40). However, recent observations that specific antisense oligonucleotide ablation of exercise-induced elevations in cardiac HSP70 resulted in loss of protection against ischemia-reperfusion injury (29), coupled with the positive effects of HSP70 overexpression in transgenic (21, 31) and chronically exercised models (8) on this condition, suggest that the HSP70 plays a prominent role in exercise-induced myocardial protection. In a recent study in which Noble et al. (27) employed intense treadmill training vs. voluntary free wheel running, only treadmill running resulted in an increase in cardiac HSP70. At the time, these investigators speculated that the induction of myocardial HSP70 may exhibit an intensity-related threshold. The findings of the present investigation confirm this speculation and extend the previous observations of Liu et al. (16) with regard to skeletal muscle.
The heart operates as a functional syncytium, whereby all fibers are recruited with each beat, but during exercise, the work of the heart is linearly increased with exercise intensity because of increases in both cardiac contractility and frequency. Cardiac HSP70 induction, however, does not exhibit this linear response; rather, it demonstrates an intensity-related threshold with significant increases in HSP70 being first noted at a speed of 24 m/min, corresponding to a heart rate of over 90% of maximum. A further dramatic increase in HSP70 is observed after exercise at 33 m/min when HSP70 content rose to nearly 22 times Con levels. Lactate concentrations obtained at various running speeds in the present study are in general agreement with the findings of Pilis et al. (30) and indicate that the largest increase in myocardial HSP70 content occurred when animals were exercising near or above their lactate threshold. Hence, it appears, that simply undertaking exercise per se is insufficient to induce this stress protein. To garner the potential cardioprotective effects of HSP70 (21, 29, 31), relatively intense exercise is required. These findings could help explain observations that the cardioprotective effect of exercise is more influenced by the intensity of the exercise rather than the total amount of physical activity (22, 23, 39), although total exercise volume (17, 34) and other factors such as temperature (7, 38) and gender (28, 29) may modulate the response.
Unlike the myocardium, skeletal muscle fibers do not function as one distinct unit but operate as motor units that are sequentially recruited as required. Therefore, to further evaluate the role of exercise intensity in eliciting HSP70 expression, we examined a variety of skeletal muscle types in the rat hindlimb known to vary with respect to fiber-type composition and recruitment patterns during treadmill running. In the vastus, the progressive recruitment of FOG fibers at all exercise intensities is contrasted by the recruitment of FG fibers only at high intensities. For example, by using periodic acid-Schiff staining of rat muscle cross sections, Armstrong et al. (2) observed lower glycogen content in FOG and SO fibers after treadmill running at 22.5 m/min, 0% grade, whereas glycogen content in FG fibers only decreased after exercise at 38.9 m/min, 0% grade. Blood flow observations in the rat hindlimb confirmed these recruitment patterns (13). Similarly, although observing progressively larger increases in cytochrome c concentration in rodent RV after exercise training at low to moderate intensities, Dudley et al. (4) reported that the WV exhibited a training response threshold at and above 30 m/min. In the present study, HSP70 expression in the RV and WV closely mimicked these recruitment and adaptive patterns (Fig. 3).
The Sol, a postural muscle composed predominantly of SO fibers (1) and extensively recruited in rats during normal locomotion and standing (32), demonstrated a different pattern of HSP70 expression than that observed in the other skeletal muscles. The Sol showed modest exercise-induced changes in HSP70; nonetheless, when assessed via Western blots, HSP70 content in the Sol increased slightly at the lowest exercise intensity (15 m/min), but at speeds above 27 m/min, HSP70 content actually declined (Fig. 3). This response is reminiscent of observations by Dudley et al. (4), who found that the Sol demonstrated an increase in cytochrome c concentration as the intensity of an 8-wk treadmill running regimen was increased to ~80% maximal O2 uptake, but at intensities greater than this, cytochrome c activity returned toward Con levels. This is also in keeping with observations made by Roy et al. (32), who found that with faster treadmill speeds, the total amount of activation of the rat Sol remained relatively constant and even exhibited a slight decrease as measured by electromyogram. It is likely that these observations reflect a functional unloading of the slower contracting Sol muscle when surrounding, faster contracting muscles are recruited at the higher running speeds.
The fiber-type differences in the constitutive or basal expression of HSP70 observed in the present study (Fig. 4) have been noted previously (9, 18). It has also been reported that the exercise-induced increase in HSP70 is inversely related to the basal levels of this protein in skeletal muscle. Hence, those muscles with the lowest constitutive expression of HSP70 demonstrate the greatest relative increases in response to exercise training (5, 10). A similar trend was observed in the present study, with the WV demonstrating a 6-fold increase in HSP70 and the Sol exhibiting only a 1.5-fold rise (Fig. 3). However, when data were normalized for the total amount of protein loaded on each gel during SDS-PAGE (see MATERIALS AND METHODS) and the change in HSP70 content between Con, a low exercise intensity (18 m/min), and the highest exercise intensity (33 m/min) was examined, the magnitude of the maximal absolute increase in HSP70 followed the pattern of Sol > RV > WV (Fig. 4). This expression pattern, which could result from the more frequent recruitment of muscles with higher oxidative capacity, is in accord with observations that heat shock results in greater and more rapid DNA binding of the factor responsible for HSP70 transcription (heat shock factor-1) in the Sol as opposed to the less oxidative white portion of the gastrocnemius muscle (19). It is interesting to speculate that the more robust response of the oxidative fibers may also be a factor in the reduced damage they experience after eccentric muscle contractions (15).
During exercise, a number of physiological and metabolic events occur within muscle cells. These include but are not limited to an increase in core and muscle temperature, oxidative stress, altered pH, and structural damage to muscle proteins. Many of these events are known to induce HSP70 (for review see Ref. 26). Although we do not provide evidence for a specific exercise stimulus that will elevate HSP70, it is likely that the previously mentioned factors, and possibly others, all contribute to the observed stress response to some degree. Increased body temperatures accompanying exercise are clearly a factor in the cardiac induction of HSP70 (7, 38); nonetheless, in the present study, the substantial increase in myocardial HSP70 content when the exercise intensity was increased from 30 to 33 m/min (Fig. 2), despite a similar elevation in core temperature (Table 2), suggests that other factors are also important. A whole body inflammatory or stress response may be involved (24); however, local conditions and indeed actual muscle loading plays a major role. If this were not the case, we would not expect to see the markedly different patterns of HSP70 expression after exercise in muscles in such close proximity to each other. In this regard, the observations that the Sol demonstrated a return toward Con HSP70 expression at the most intense workloads, despite these workloads resulting in the greatest elevations in body temperature, strongly suggests that factors associated with muscle recruitment are critical to eliciting a stress response. Whether individual motor units increase their expression of HSP70 on initial activation, or like cardiac tissue exhibit a threshold related to the frequency of activation, cannot be ascertained from this study.
In conclusion, the present results demonstrate that the exercise-induced increase in HSP70 exhibits an intensity-dependent threshold that in skeletal muscles is related to their known recruitment patterns. Because HSP70 has been demonstrated to protect striated muscle against a variety of insults, these observations may have implications regarding exercise prescription and the relative exercise intensity required to gain these benefits.
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ACKNOWLEDGEMENTS |
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We are grateful to members of the Exercise Biochemistry laboratory at the University of Western Ontario for help in the care and running of the animals employed in this study. We thank G. Ouellet for preparation of electrocardiograph electrodes.
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FOOTNOTES |
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This study was supported by grants from the Heart and Stroke Foundation of Ontario (NA-4445) and the National Science and Engineering Research Council of Canada (OPG0008170) to E. G. Noble.
Address for reprint requests and other correspondence: E. G. Noble, School of Kinesiology, Faculty of Health Sciences, Univ. of Western Ontario, London, Ontario, Canada N6A 3K7 (E-mail: enoble{at}uwo.ca).
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.
May 3, 2002;10.1152/japplphysiol.00528.2001
Received 29 May 2001; accepted in final form 2 May 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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1.
Armstrong, RB,
and
Phelps RO.
Muscle fiber type composition of the rat hindlimb.
Am J Anat
171:
259-272,
1984.
2.
Armstrong, RB,
Saubert CW,
Sembrowich WL,
Shepherd RE,
and
Gollnick PD.
Glycogen depletion in rat skeletal muscle fibers at different intensities and durations of exercise.
Pflügers Arch
352:
243-256,
1974.
3.
Barnard, RJ,
Duncan HW,
and
Thorstensson AT.
Heart rate responses of young and old rats to various levels of exercise.
J Appl Physiol
36:
472-474,
1974.
4.
Dudley, GA,
Abraham WM,
and
Terjung RL.
Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle.
J Appl Physiol
53:
844-850,
1982.
5.
Gonzalez, B,
Hernando R,
and
Manso R.
Stress proteins of 70 kDa in chronically exercised skeletal muscle.
Pflügers Arch
440:
42-49,
2000.
6.
Gutierrez, JA,
and
Guerriero V, Jr.
Quantitation of Hsp70 in tissues using a competitive enzyme-linked immunosorbent assay.
J Immunol Methods
143:
81-88,
1991.
7.
Hamilton, KL,
Powers SK,
Sugiura T,
Kim S,
Lennon S,
Tumer N,
and
Mehta JL.
Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins.
Am J Physiol Heart Circ Physiol
281:
H1346-H1352,
2001.
8.
Harris, MB,
and
Starnes JW.
Effects of body temperature during exercise training on myocardial adaptations.
Am J Physiol Heart Circ Physiol
280:
H2271-H2280,
2001.
9.
Hernando, R,
and
Manso R.
Muscle fibre stress in response to exercise: synthesis, accumulation and isoform transitions of 70-kDa heat-shock proteins.
Eur J Biochem
243:
460-467,
1997.
10.
Kelly, DA,
Tiidus PM,
Houston ME,
and
Noble EG.
Effect of vitamin E deprivation and exercise training on induction of HSP70.
J Appl Physiol
81:
2379-2385,
1996.
11.
Kiang, JG,
and
Tsokos GC.
Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology.
Pharmacol Ther
80:
183-201,
1998.
12.
Laemmli, UK.
Cleavage of structural proteins during the assembly of the head of the baceriophage T4.
Nature
227:
680-685,
1970.
13.
Laughlin, MH,
and
Armstrong RB.
Muscular blood flow distribution patterns as a function of running speed in rats.
Am J Physiol Heart Circ Physiol
243:
H296-H306,
1982.
14.
Lepore, DA,
Hurley JV,
Stewart AG,
Morrison WA,
and
Anderson RL.
Prior heat stress improves survival of ischemic-reperfused skeletal muscle in vivo.
Muscle Nerve
23:
1847-1855,
2000.
15.
Lieber, RL,
and
Friden J.
Selective damage of fast glycolytic muscle fibres with eccentric contraction of the rabbit tibialis anterior.
Acta Physiol Scand
133:
587-588,
1988.
16.
Liu, Y,
Lormes W,
Baur C,
Opitz-Gress A,
Altenburg D,
Lehmann M,
and
Steinacker JM.
Human skeletal muscle HSP70 response to physical training depends on exercise intensity.
Int J Sports Med
21:
351-355,
2000.
17.
Liu, Y,
Mayr S,
Opitz-Gress A,
Zeller C,
Lormes W,
Baur S,
Lehmann M,
and
Steinacker JM.
Human skeletal muscle HSP70 response to training in highly trained rowers.
J Appl Physiol
86:
101-104,
1999.
18.
Locke, M,
Noble EG,
and
Atkinson BG.
Inducible isoform of HSP70 is constitutively expressed in a muscle fiber type specific pattern.
Am J Physiol Cell Physiol
261:
C774-C779,
1991.
19.
Locke, M,
and
Tanguay RM.
Increased HSF activation in muscles with a high constitutive Hsp70 expression.
Cell Stress Chaperones
1:
189-196,
1996.
20.
Locke, M,
Tanguay RM,
Klabunde RE,
and
Ianuzzo CD.
Enhanced postischemic myocardial recovery following exercise induction of HSP 72.
Am J Physiol Heart Circ Physiol
269:
H320-H325,
1995.
21.
Marber, MS,
Mestril R,
Chi SH,
Sayen MR,
Yellon DM,
and
Dillmann WH.
Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury.
J Clin Invest
95:
1446-1456,
1995.
22.
Morris, JN,
Chave SPW,
Adam C,
Sirey C,
Epstein L,
and
Sheehan DJ.
Vigorous exercise in leisure time and the incidence of coronary heart-disease.
Lancet
1:
333-339,
1973.
23.
Morris, JN,
Everitt MG,
Pollard R,
Chave SPW,
and
Semmence AM.
Vigorous exercise in leisure-time: protection against coronary heart disease.
Lancet
2:
1207-1210,
1980.
24.
Moseley, PL.
Exercise, stress, and the immune conversation.
Exerc Sport Sci Rev
28:
128-132,
2000.
25.
Naito, H,
Powers SK,
Demirel HA,
Sugiura T,
Dodd SL,
and
Aoki J.
Heat stress attenuates skeletal muscle atrophy in hindlimb-unweighted rats.
J Appl Physiol
88:
359-363,
2000.
26.
Noble, EG.
Heat shock proteins and their induction with exercise.
In: Exercise and Stress Response: The Role of Stress Proteins, edited by Locke M,
and Noble EG.. Boca Raton, FL: CRC, 2002, p. 43-78.
27.
Noble, EG,
Moraska A,
Mazzeo RS,
Roth DA,
Olsson MC,
Moore RL,
and
Fleshner M.
Differential expression of stress proteins in rat myocardium after free wheel or treadmill run training.
J Appl Physiol
86:
1696-1701,
1999.
28.
Paroo, Z,
Dipchand ES,
and
Noble EG.
Estrogen attenuates postexercise HSP70 expression in skeletal muscle.
Am J Physiol Cell Physiol
282:
C245-C251,
2002.
29.
Paroo, Z,
Haist JV,
Karmazyn M,
and
Noble EG.
Exercise improves post-ischemic cardiac function in males but not females: consequences of a novel gender-specific Hsp70 response.
Circ Res
90:
911-917,
2002.
30.
Pilis, W,
Zarzeczny R,
Langfort J,
Kaciuba-Uscilko H,
Nazar K,
and
Wojtyna J.
Anaerobic threshold in rats.
Comp Biochem Physiol Comp Physiol
106:
285-289,
1993.
31.
Plumier, JCL,
Ross BM,
Currie RW,
Angelidis CE,
Kazalaris H,
Kollias G,
and
Pagoulatos GN.
Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery.
J Clin Invest
95:
1854-1860,
1995.
32.
Roy, RR,
Hutchison DL,
Pierotti DJ,
Hodgson JA,
and
Edgerton VR.
EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming.
J Appl Physiol
70:
2522-2529,
1991.
33.
Salo, DC,
Donovan CM,
and
Davies KJ.
HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise.
Free Radic Biol Med
11:
239-246,
1991.
34.
Samelman, TR.
Heat shock protein expression is increased in cardiac and skeletal muscles of Fischer 344 rats after endurance training.
Exp Physiol
85:
92-102,
2000.
35.
Skidmore, R,
Gutierrez JA,
Guerriero VJ,
and
Kregel KC.
HSP70 induction during exercise and heat stress in rats: role of internal temperature.
Am J Physiol Regul Integr Comp Physiol
268:
R92-R97,
1995.
36.
Smith, PK,
Krohn RI,
Hermanson GT,
Mallia AK,
Gartner FH,
Provenzano MD,
Fujimoto EK,
Goeke NM,
Olson BJ,
and
Klenk DC.
Measurement of protein using bicinchoninic acid.
Anal Biochem
150:
76-85,
1985. [Corrigenda. Anal Biochem 163: May 1987 p. 279.]
37.
Snoeckx, LH,
Cornelussen RN,
van Nieuwenhoven FA,
Reneman RS,
and
van der Vusse GJ.
Heat shock proteins and cardiovascular pathophysiology.
Physiol Rev
81:
1461-1497,
2001.
38.
Taylor, RP,
Harris MB,
and
Starnes JW.
Acute exercise can improve cardioprotection without increasing heat shock protein content.
Am J Physiol Heart Circ Physiol
276:
H1098-H1102,
1999.
39.
Williams, PT.
Physical fitness and activity as separate heart disease risk factors: a meta-analysis.
Med Sci Sports Exerc
33:
754-761,
2001.
40.
Yamashita, N,
Hoshida S,
Otsu K,
Asahi M,
Kuzuya T,
and
Hori M.
Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation.
J Exp Med
189:
1699-1706,
1999.
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