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1 Department of Physiology, National Cheng-Kung University Medical College, Tainan, Taiwan 701; and 2 Department of Physiology, National Yang-Ming University, Medical College, Taipei, Taiwan 11221
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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This study attempted to ascertain whether the ischemic damage to neurons and monoamine overload in brain that occur during rat heatstroke can be attenuated by heat shock protein (HSP) 72 induction. Effects of heatstroke on mean arterial pressure (MAP), cerebral blood flow (CBF), brain dopamine (DA) and serotonin (5-HT) release, and neural damage score were assayed in rats 0, 16, or 48 h after heat shock (42°C for 15 min) or chemical stress (5 mg/kg sodium arsenite ip). Brain HSP 72 in rats after heat shock or chemical stress was detected by Western blot, and brain monoamine was determined by a microdialysis probe combined with high-performance liquid chromatography. Heatstroke was induced by exposing the animal to a high ambient temperature (43°C); the moment at which MAP and CBF decreased from their peak values was taken as the time of heatstroke onset. Prior heat shock or chemical stress conferred significant protection against heatstroke-induced hyperthermia, arterial hypotension, cerebral ischemia, cerebral DA and 5-HT overload, and neural damage and correlated with expression of HSP 72 in brain at 16 h. However, at 48 h, when HSP 72 expression returned to basal values, the above responses that occurred during the onset of heatstroke were indistinguishable between the two groups (0 h vs. 48 h). These results lead to the hypothesis that the brain can be preconditioned by thermal or chemical injury, that this preconditioning will induce HSP 72, and that HSP 72 induction will correlate quite well with anatomic, histochemical, and hemodynamic protection in rat heatstroke.
microdialysis; heat shock; chemical stress; dopamine; serotonin
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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HEATSTROKE, a very serious disease in medical emergency, has been studied extensively by many investigators (34). Our previous studies (8, 14, 33) demonstrated that cerebral ischemia rather than hyperthermia is the main reason for the central nervous system dysfunction that occurs during heatstroke. Evidence has also accumulated to suggest that marked activation of the nigrostriatal dopaminergic (8, 16) or serotoninergic (5, 9) systems is associated with ischemic neuronal damage during heatstroke. Destruction of brain dopaminergic (16) or serotoninergic (9) pathways protects against ischemic neuronal injury in heatstroke in rats.
There is mounting evidence that neurons produce heat shock protein (HSP) in response to a variety of environmental stresses, resulting in protection from subsequent lethal damage (29, 32, 36-38). HSP 72 induction increases the number of surviving neurons in rat hippocampal neuron primary culture as well as the tolerance of hippocampal neurons to ischemic injury (10, 19, 30). This raises the possibility that pretreatment that increases brain HSP 72 content before heatstroke may limit the development of arterial hypotension, cerebral ischemia, cerebral monoamine overload, and neuronal damage that occur during the onset of heatstroke (12).
To address the question properly, in the present study we compared the temporal profiles of mean arterial pressure (MAP), cerebral blood flow (CBF), cerebral dopamine (DA) and serotonin (5-HT) release, and neuron damage score in rats with or without brain HSP 72 expression in heatstroke.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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HSP 72 induction. HSP expression was induced in male Wistar rats (Animal Resource Center, National Science Council, Taipei, Taiwan, ROC) weighing 250-300 g by either heat shock (39) or chemical stress (28). For heat shock treatment, rats under general anesthesia (1 h after 40 mg/kg pentobarbital sodium ip) were heated gently with an electric pad. The colonic temperature of the heated animals was kept at 42 ± 0.5°C for 15 min. They were returned to room temperature during the recovery period. For chemical stress treatment, the unanesthetized rats were treated with sodium arsenite (5 mg/kg ip). These groups of animals were subjected to heatstroke experiments at 0, 4, 8, 16, or 48 h after the start of heat shock or chemical stress treatment.
HSP 72 detection. The animals were killed by decapitation at the end of the experiment for detection of HSP 72. The brains were quickly removed and stored at 0°C. The corpus striatum was dissected from the brain and placed into Eppendorf tubes. For protein extraction, the samples were weighed, rapidly thawed in 6 vols of homogenizing buffer consisting of 20 mM Tris · HCl (pH 7.6), 100 mM KCl, 5 mM NaCl, 2 mM EDTA, 1 mM EGTA, 0.25 M sucrose, 2 mM dithiothreitol, and 2 mM phenylmethylsulfonyl fluoride at pH 7.2, and then homogenized by a sonicator. After centrifugation at 5,000 g for 15 min at 4°C, the protein assay was carried out by the Bradford method. The samples (40 µg/lane) were incubated for 5 min at 95°C in Laemmli buffer, separated on 10% SDS-polyacrylamide discontinuous gel, and then electrophoretically transferred to a polyvinylidine difluoride membrane. The membrane was blocked for 1 h at room temperature with PBS containing 10% skim milk. Mouse monoclonal antibodies against HSP 72 (Oncogene Science) were used as primary antibodies (1:1,000 dilution). Incubation time with the primary antibody at room temperature was 1 h. Band detection was performed with an enhanced chemiluminescence Western blotting analysis system (RPN 2108; Amersham International, Amersham, UK).
Heatstroke induction. Six groups of animals were used: 1) rats 0 h after heat shock; 2) rats 16 h after heat shock; 3) rats 48 h after heat shock; 4) rats 0 h after chemical stress; 5) rats 16 h after chemical stress; and 6) rats 48 h after chemical stress. Under urethan (1.4 g/kg ip) anesthesia, the femoral artery of these animals was cannulated with polyethylene tubing (PE-50) for measurement of systemic arterial blood pressure and heart rate. Pulsatile arterial pressure, MAP, and heart rate were monitored continuously with a pressure transducer and a chart recorder (model 2400, Gould). The animals were then placed in a Kopf stereotaxic frame (Grass) in the flat skull position. A flow probe was implanted into the right corpus striatum using the atlas and coordinates of Paxinos and Watson (24) for measurement of CBF. At the same time, for measurement of extracellular monoamine release a microdialysis probe was implanted stereotaxically into the left corpus striatum. Heatstroke was induced by exposing these groups of animals to an ambient temperature of 43°C; the moment in which MAP and CBF began to decrease from their peak levels was taken as the onset of heatstroke (8, 16; see Fig. 2). All experimental protocols were approved by the Animal Research Committee of the Yang-Ming University School of Medicine. Adequate anesthesia was maintained in the animals after administration of urethan (1.4 g/kg ip). At the end of the experiments, the animals were killed for evaluation of neuron damage, HSP 72 detection, or histological verification of the path of the probes.
CBF measurement. CBF was monitored with a Laserflo BPM2 laser-Doppler flowmeter (Vasamedic, St. Paul, MN). A 24-gauge stainless steel needle probe (diameter 0.58 mm, length 40 mm) was implanted into the corpus striatum as indicated in Heatstroke induction. The Laserflo BPM2 records at a bandwidth of 30 Hz and a low band pass of 20 KHz. The display is digital only, collects eight data points per second, and was set to give a moving average of data every 0.3 s. Blood perfusion was recorded until the flux value leveled off at a stable reading, which usually occurred after ~1 min. That value was then recorded and used as the flux measurement for the period.
In addition, an autoradiographic technique was used to quantify CBF in the corpus striatum (31). Approximately 50 µCi of iodo[14C]antipyrine in 1 ml of normal saline were infused at a constant rate via the femoral venous catheter for a period of 1 min, during which time arterial samples were collected on filter paper disks for assay of arterial concentration. At exactly 1 min, the animal was decapitated and the brain was removed, frozen, and assayed for 14C concentration by the autoradiographic technique. Autoradiographs of sections of rat brain and a calibrated plastic 14C standard were used to determine tissue concentrations of 14C by densitometric measurements.Measurement of extracellular monoamine release. After a microdialysis probe (active length 3.5 mm) was inserted into the left corpus striatum, it was perfused with artificial cerebrospinal fluid (in mM: 149 NaCl2, 2.8 KCl, 1.2 CaCl2, 1.2 MgCl2, 0.125 ascorbic acid, and 5.4 D-glucose, pH 7.2-7.4) using microliter syringe pumps (model SJ-3206, Harvard) at a flow rate of 1.35 µl/min. After 2 h of stabilization, dialysate samples from the corpus striatum were collected into 700-µl Eppendorf tubes at 20-min intervals. Samples were assayed by an HPLC system. Extracellular monoamine concentrations were assayed by HPLC combined with an electrochemical detection system as described previously (13). The HPLC system comprised a Beckman 126 pump (Beckman Instruments) and a CMA-200 microautosampler (CMA/Microdialysis, Stockholm, Sweden), and a microbore reversed-phase column was filled with Inertsil ODS-2 (GSK-C18, 5-mm OD, 150 × 1.0-mm ID). The performance of each microdialysis probe was calibrated by dialysis of a known amount of the standard mixture, and recovery of all analyses was then determined. Brain concentrations of 5-HT and other monoamines were calculated by determining each peak height ratio relative to the internal standard and were also corrected by each probe performance. The internal standard 3-methoxytyramine and standard mixtures were prepared fresh daily. The mobile phase was prepared by adding 60 ml of acetonitrile, 0.42 g of SDS (2.2 mM), 200 g of sodium citrate (30 mM), 10 mg of EDTA (0.027 mM), and 1 ml of diethylamine in double-distilled water. The solution was adjusted to pH 3.5 by concentrated orthophosphoric acid, and its final volume was adjusted to 1 liter. We filtered the mixture with a 0.22-µm nylon filter under reduced pressure and degassed it by pumping helium gas for 20 min. The flow rate was 0.05-0.06 ml/min, maintaining column pressure at ~7.6 mPa.
In vitro tests were run to determine the recovery of 5-HT or other monoamines in the dialysis solution at the flow rate used. At room temperature, dialysis probes were immersed in dialysis solution containing 5-HT or DA. At a flow rate of 1.35 µl/min, the relative recovery was 14 ± 1.4% (n = 8). Basal monoamine levels were considered stable after observation of four consecutive samples with no upward or downward trend. These basal values were averaged, and all samples were expressed as a percentage of the mean baseline to avoid large variations in the absolute values.Evaluation of neuron damage and probe placement. In separate experiments, 5 min after the onset of heatstroke rats were killed, and brains were perfused, fixed in 10% neutral Formalin, and embedded in paraffin blocks. Coronal sections (6 µm) through the striatum were stained with hematoxylin and eosin for microscope evaluation. Neuronal damage was graded from the grading system of Pulsinelli et al. (26, 27) in which 0 = normal, 1 = few neurons damaged, 2 = many neurons damaged, and 3 = all neurons damaged. All probe placements were in the regions of the corpus striatum as verified by microscopic evaluation.
Statistics. The numerical values cited are means ± SE. Repeated-measures analysis of variance was used for factorial experiments, whereas Duncan's multiple-range test (multi-time point experiments) was used for post hoc multiple comparisons among means. Student's t-test was used when only two groups were compared. The criterion for statistical significance was set at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Figure 1,
top, shows that heat shock (42°C
body temperature for 15 min), in the presence of an increase in body
temperature, induced HSP 72 expression in the striatum that was
detected 4 h after treatment, peaked between 8 and 16 h, and returned
to baseline by 48 h. In this series of experiments, heat shock was conducted in rats 1 h after intraperitoneal administration of pentobarbital sodium. Normothermic control rats receiving the same dose
of pentobarbital sodium did not express HSP 72 in the corpus striatum.
Chemical stress (sodium arsenite injection), in the absence of an
increase in body temperature, also induced HSP 72 expression in the
corpus striatum that was detected 4 h after injection, peaked between 8 and 16 h, and returned to baseline by 48 h (Fig. 1,
bottom). Every animal in the
treatment groups showed a consistent HSP 72 response to the priming
insults as shown in Fig. 1.
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Tables 1 and
2 summarize means ± SE values for all
groups of animals. Heatstroke was induced by exposing the animals to an
ambient temperature of 43°C. Heatstroke rats without striatal HSP
72 expression showed higher colon temperature, heart rate, and striatal
DA and 5-HT release but lower mean arterial pressure, striatal blood
flow, and survival time compared with those of normothermic control
rats. Figure 2 shows typical examples of the effects of heatstroke on colon temperature, mean arterial pressure,
heart rate, striatal DA and 5-HT release, striatal blood flow, and
survival time. Induction of striatal HSP 72 expression, 16 h after heat
shock or chemical stress, significantly reduced the hyperthermia,
arterial hypotension, striatal accumulation of both DA and 5-HT, and
striatal ischemia that occurred after the onset of heatstroke.
However, with the loss of HSP observed at 48 h, no further protection
was induced.
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In separate experiments, 5 min after the onset of heatstroke, animals
were killed for determination of both local CBF and neuronal damage
score. The data are summarized in Table 3.
After the onset of heatstroke, animals with no HSP 72 expression
displayed higher values of striatal neuronal damage score but lower
values of striatal blood flow compared with those of normothermic
control rats. In addition, histopathological verification revealed that heatstroke caused cell body shrinkage, pyknosis of the nucleus, loss of
Nissl substance, and disappearance of the nucleolus in the corpus
striatum (Fig.
3B).
However, with the expression of HSP 72 in the corpus striatum observed
at 16 h neuroprotection was ensured (Fig.
3C).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In the present study using a well-described rat model (12), we induced thermal or chemical preconditioning and clearly demonstrated production of HSP 72 in the brain at 16 h that returned to baseline at 48 h. Using preconditioned animals, we induced heatstroke to find that prior heat shock or chemical stress conferred significant protection against heatstroke-induced hyperthermia, arterial hypotension, striatal ischemia, striatal DA and 5-HT overload, and striatal neuronal damage. These results are consistent with previous findings that HSP 70 expression can alter the resistance of the heart (42) and the brain (4) to subsequent ischemic or nonischemic injury. With the loss of HSP 72 observed at 48 h, no further protection was induced in the present studies. It should be stated that there are many consequences of hyperthermic insults, including the induction of other HSP as well as diverse physiological changes (32). Because the thermal insult is attenuated in the preconditioned animals in our studies, this raises the possibility that the resulting pathology would be less. Although tissue injury was formerly attributed to hyperthermia itself, it has recently been observed that normal volunteers heated passively and cancer patients treated with whole body hyperthermia can endure a rectal temperature of 41-42°C with no, or minimal, tissue injury (3, 25). Heatstroke can occur when the rectal temperature increases to only 40°C (1, 2); moreover, tissue injury continues to develop after cooling to normal body temperature in 25% of heatstroke patients (2, 7, 20, 34). Our previous results (5, 8, 9, 12, 14, 16, 33) further demonstrated that cerebral ischemia and overloading of DA and 5-HT in the brain, rather than hyperthermia, is the main reason for heatstroke formation in animals.
It has been shown that both intracranial hypertension (because of cerebral edema and cerebral vascular congestion) and arterial hypotension result in a reduction in cerebral perfusion pressure in animals with heatstroke (15, 33). Reduction of cerebral perfusion pressure to below the autoregulatory level will induce cerebral ischemia in animals with heatstroke (14). Our recent results (15) also showed that a decline in stroke volume or ventricular depolarization resulting from an increased plasma level of interleukin-1 is an important mechanism signaling arterial hypotension in rat heatstroke. Indeed, the heatstroke-induced arterial hypotension, intracranial hypertension, cerebral ischemia, cerebral DA and 5-HT overload, and cerebral neuronal damage were significantly attenuated by blockade of interleukin-1 receptors in rats (12, 18). Other lines of evidence showed that heat shock and chemical stress with heavy metal salts or sulfhydryl reagents, all of which induce the expression of HSP 70, concomitantly inhibit the production of interleukin and other cytokines in human monocytes and mouse macrophages activated by lipopolysaccharide (6). Putting these observations together, it seems that induction of brain HSP 72 by prior heat shock or chemical stress reduces the augmented production of interleukin-1 and other cytokines in the plasma and results in protection against heatstroke-induced arterial hypotension, cerebral ischemia, cerebral monoamine overload, and cerebral neuronal damage in rats.
It should be stated that, after the onset of heatstroke, ischemic injury or monoamine overload was observed to occur in different brain structures including the corpus striatum, hypothalamus, cortex, and thalamus (8, 9, 17). In addition, prior heat shock was shown to induce HSP 72 induction in different brain structures (including corpus striatum, hypothalamus, cortex, and thalamus), liver, heart, and kidney (39, 40). In the present study, the corpus striatum was chosen as a representative region for measurement of HSP 72 induction, blood flow, and neuronal damage in rat heatstroke. However, it can be inferred from the present results that in addition to the corpus striatum, the mechanisms existing in other brain structures (such as the hypothalamus, cortex and thalamus) and vital organs are also responsible for these physiological consequences of preconditioning.
In fact, the processes involved in cell injury during ischemia and reperfusion are complex. The generation of free radicals, hydrogen peroxide, and cellular calcium overload are implicated in the process of ischemic neuronal damage (11, 23, 41). In this regard, many investigators demonstrated that HSP 70 induction by either heat shock or immobilization protects the rat or rabbit heart against the calcium overload triggered by calcium depletion-repletion (21, 22, 35). In a rat myocyte culture model, heat shock is capable of inducing acquired thermotolerance and limiting myocyte injury on subsequent H2O2 exposure (35). However, it is not known whether the same mechanisms can be applied to explain the neuroprotective action exerted by HSP expression in brain during heatstroke.
In summary, the present results show that heat shock and chemical stress, which induce the expression of HSP 72 in the brain, concomitantly inhibit the arterial hypotension, cerebral ischemia, cerebral DA and 5-HT overload, and cerebral cell injury that occur during the onset of heatstroke in rats. This leads to the hypothesis that the brain can be preconditioned by thermal or chemical injury, that this preconditioning will induce HSP 72, and that HSP 72 induction will correlate well with anatomic, biochemical, and hemodynamic protection in rat heatstroke.
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ACKNOWLEDGEMENTS |
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This work was supported by grants from the National Science Council of the Republic of China (NSC86-2745-B-010-005) and the Veterans' General Hospital-National Yang-Ming University joint research program (VTY 88-p5-43), Tsou's Foundation, Republic of China.
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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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: M.-T. Lin, Dept. of Physiology, National Yang-Ming University Medical College, Taipei, Taiwan 11221 [E-mail: mtlin{at}ym.edu.tw].
Received 21 September 1998; accepted in final form 25 January 1999.
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REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Austin, M. G.,
and
J. W. Berry.
Observation of a hundred cases of heatstroke.
JAMA
161:
1525-1529,
1956.
2.
Bouchama, A.,
A. Cafege,
E. B. Deval,
O. Labdi,
K. El-Assil,
and
M. Seraj.
Ineffectiveness of dantrolene sodium in the treatment of heatstroke.
Crit. Care Med.
19:
176-180,
1991[Medline].
3.
Bynum, G. D.,
K. B. Pandolf,
W. H. Schuette,
R. F. Goldman,
D. E. Lees,
J. Whang-Peng,
E. R. Atkinson,
and
J. M. Bull.
Induced hyperthermia in sedated humans and the concept of critical thermal maximum.
Am. J. Physiol.
235 (Regulatory Integrative Comp. Physiol. 4):
R228-R236,
1978.
4.
Chen, J.,
S. H. Graham,
R. I. Zhu,
and
R. P. Simon.
Stress proteins and tolerance to focal cerebral ischemia.
J. Cereb. Blood Flow Metab.
16:
566-577,
1996[Medline].
5.
Chiu, W. T.,
T. Y. Kao,
and
M. T. Lin.
Interleukin-1 receptor antagonist increases survival in rat heatstroke by reducing hypothalamic serotonin release.
Neurosci. Lett.
202:
33-36,
1995[Medline].
6.
Hall, T. J.
Role of HSP70 in cytokine production.
Experientia
50:
1048-1053,
1994[Medline].
7.
Hart, G. R,
R. J. Anderson,
C. P. Crumpler,
A. Shulkin,
G. Reed,
and
J. P. Knochel.
Epidemic classical heatstroke: clinical characteristics and course of 28 patients.
Medicine (Baltimore)
61:
189-197,
1982[Medline].
8.
Kao, T. Y.,
C. C. Chio,
and
M. T. Lin.
Hypothalamic dopamine release and local cerebral blood flow during onset of heatstroke in rats.
Stroke
25:
2483-2487,
1994[Abstract].
9.
Kao, T. Y.,
and
M. T. Lin.
Brain serotonin depletion attenuates heatstroke-induced cerebral ischemia and cell death in rats.
J. Appl. Physiol.
80:
680-684,
1996
10.
Kirino, T.,
Y. Tsujita,
and
A. Tamura.
Induced tolerance to ischemia in gerbil hippocampal neurons.
J. Cereb. Blood Flow Metab.
11:
299-307,
1991[Medline].
11.
Kukreja, R. C.,
and
M. L. Hess.
The oxygen free radical system: from equations through membrane protein interactions to cardiovascular injury and protection.
Cardiovasc. Res.
26:
641-655,
1992
12.
Lin, M. T.
Heatstroke-induced cerebral ischemia and neuronal damage: involvement of cytokines and monoamines.
Ann. NY Acad. Sci.
813:
572-580,
1997[Medline].
13.
Lin, M. T.,
F. Y. Chueh,
M. T. Hsieh,
and
C. F. Chen.
Antihypertensive effects of dl-tetrahydropalmatine: an active principle isolated from Corydalis.
Clin. Exp. Pharmacol. Physiol.
23:
738-742,
1996[Medline].
14.
Lin, M. T.,
and
S. Z. Lin.
Cerebral ischemia is the main cause for heat stroke syndrome in rabbits.
Experientia
48:
225-227,
1992[Medline].
15.
Lin, M. T.,
H. H. Liu,
and
Y. L. Yang.
Involvement of interleukin-1 receptor mechanism in development of arterial hypotension in rat heatstroke.
Am. J. Physiol.
273 (Heart Circ. Physiol. 42):
H2072-H2077,
1997
16.
Lin, M. T.,
T. Y. Kao,
C. C. Chio,
and
Y. T. Jin.
Dopamine depletion protects striatal neurons from heatstroke-induced ischemia and cell death in rats.
Am. J. Physiol.
269 (Heart Circ. Physiol. 38):
H487-H490,
1995
17.
Lin, M. T.,
T. Y. Kao,
Y. T. Jin,
and
C. F. Chen.
Interleukin-1 receptor antagonist attenuates the heat stroke-induced neuronal damage by reducing the cerebral ischemia in rats.
Brain Res. Bull.
37:
595-598,
1995[Medline].
18.
Lin, M. T.,
T. Y. Kao,
C. F. Su,
and
S. F. Hsu.
Interleukin-l
production during the onset of heat stroke in rabbits.
Neurosci. Lett.
174:
17-20,
1994[Medline].
19.
Lowenstein, D. H.,
P. H. Chan,
and
M. F. Miles.
The stress protein response in cultured neurons: characterization and evidence for a protective role in excitoxicity.
Neuron
7:
1053-1060,
1991[Medline].
20.
Malamud, N.,
W. Hagmaker,
and
R. P. Custer.
Heat stroke: a clinico-pathologic study of 125 fatal cases.
Mil. Surg.
99:
397-449,
1946.
21.
Marber, M. S.,
J. M. Walker,
and
D. M. Yellon.
Heat stress attenuates a submaximal calcium paradox.
J. Mol. Cell. Cardiol.
25:
1119-1126,
1993[Medline].
22.
Meerson, F. Z.,
I. H. Malyshev,
Y. V. Arkkipenks,
and
V. I. Vovk.
Adaptive increase in the resistance of the heart to calcium paradox (Abstract).
J. Mol. Cell Cardiol.
23, Suppl. V:
162,
1991.
23.
Opie, L. H.
Reperfusion injury and its pharmacological modification.
Circulation
80:
1049-1062,
1989
24.
Paxinos, G.,
and
C. Watson.
The Rat Brain in Stereotaxic Coordinates. New York: Academic, 1982.
25.
Petigrew, R. T.,
J. M. Galt,
C. M. Ludge,
D. B. Horn,
and
A. N. Smith.
Circulatory and biochemical effects of whole body hyperthermia.
Br. J. Surg.
61:
727-730,
1974[Medline].
26.
Pulsinelli, W. A.,
and
J. B. Brierley.
A new model of bilateral hemispheric ischemia in the unanesthetized rat.
Stroke
10:
267-272,
1979
27.
Pulsinelli, W. A.,
J. B. Brierley,
and
F. Plum.
Temporal profile of neuronal damage in a model of transient forebrain ischemia.
Ann. Neurol.
11:
491-498,
1982[Medline].
28.
Ribeiro, S. P.,
J. Villar,
G. P. Downey,
J. D. Edelson,
and
A. S. Slutsky.
Sodium arsenite induces heat shock protein-72 kilodalton expression in the lungs and protects rats against sepsis.
Crit. Care Med.
22:
922-929,
1994[Medline].
29.
Ritossa, F.
A new puffing pattern induced by temperature shock and DNP in Drosophila.
Experientia
18:
571-573,
1962.
30.
Rodorf, G.,
W. J. Koroshetz,
and
J. V. Bonventre.
Heat shock protects cultured neurons from glutamate toxicity.
Neuron
7:
1043-1051,
1991[Medline].
31.
Sakurada, O.,
C. Kennedy,
J. Jehle,
J. D. Brown,
G. L. Carbin,
and
L. Sokoloff.
Measurement of local cerebral blood flow with iodo[14C]antipyrine.
Am. J. Physiol.
234 (Heart Circ. Physiol. 3):
H59-H66,
1978
32.
Sato, K.,
H. Saito,
and
N. Matsuli.
HSP70 is essential to the neuroprotective effect of heat-shock.
Brain Res.
740:
117-123,
1996[Medline].
33.
Shih, C. J.,
M. T. Lin,
and
S. H. Tsai.
Experimental study on the pathogenesis of heat stroke.
J. Neurosurg.
60:
1246-1252,
1984[Medline].
34.
Simon, H. B.
Hyperthermia.
N. Engl. J. Med.
329:
483-487,
1993
35.
Su, C. Y.,
W. H. Dillman,
W. T. Wood,
and
O. K. Owen.
Heat shock induced oxidative tolerance in muscle cells (Abstract).
Circulation
83, Suppl. I:
I-33,
1992.
36.
Subjeck, J. R,
and
T.-T. Shyy.
Stress protein systems of mammalian cells.
Am. J. Physiol.
250 (Cell Physiol. 19):
C1-C17,
1986
37.
Welch, W. J.
Mammalian stress response: cell physiology structure/function of stress proteins, and implications for medicine and disease.
Physiol. Rev.
72:
1063-1081,
1992
38.
Welch, W. J.,
and
J. P. Suhan.
Cellular and biochemical events in mammalian cells during and after recovery from physiological stress.
J. Cell Biol.
103:
20352052,
1986.
39.
Yang, S. L.,
S. H. Jing,
S. S. Chen,
J. J. Chen,
and
R. C. Yang.
The effects of hyperthermic treatment on electroencephalographic recovery after interruption of respiration in rats.
Exp. Brain Res.
19:
431434,
1994.
40.
Yang, Y. L.,
K. T. Lu,
H. J. Tsay,
C. H. Lin,
and
M. T. Lin.
Heat shock protein expression protects against death following exposure to heatstroke in rats.
Neurosci. Lett.
252:
9-12,
1998[Medline].
41.
Yellon, D. M.,
and
J. M. Downey.
Current research views on myocardial reperfusion and reperfusion injury.
Cardioscience
1:
89-98,
1990[Medline].
42.
Yellon, D. M.,
and
M. S. Marber.
Hsp70 in myocardial ischemia.
Experientia
50:
1075-1083,
1994[Medline].
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  W. C. Lee, H. C. Wen, C. P. Chang, M. Y. Chen, and M. T. Lin Heat shock protein 72 overexpression protects against hyperthermia, circulatory shock, and cerebral ischemia during heatstroke J Appl Physiol, June 1, 2006; 100(6): 2073 - 2082. [Abstract] [Full Text] [PDF]
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 J. Campisi, T. H. Leem, B. N. Greenwood, M. K. Hansen, A. Moraska, K. Higgins, T. P. Smith, and M. Fleshner Habitual physical activity facilitates stress-induced HSP72 induction in brain, peripheral, and immune tissues Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2003; 284(2): R520 - R530. [Abstract] [Full Text] [PDF]
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 S. H. H. Chan, K.-F. Chang, C.-C. Ou, and J. Y. H. Chan Up-Regulation of Glutamate Receptors in Nucleus Tractus Solitarii Underlies Potentiation of Baroreceptor Reflex by Heat Shock Protein 70 Mol. Pharmacol., May 1, 2002; 61(5): 1097 - 1104. [Abstract] [Full Text] [PDF]
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 P.-L. Li, Y.-M. Chao, S. H. H. Chan, and J. Y. H. Chan Potentiation of Baroreceptor Reflex Response by Heat Shock Protein 70 in Nucleus Tractus Solitarii Confers Cardiovascular Protection During Heatstroke Circulation, April 24, 2001; 103(16): 2114 - 2119. [Abstract] [Full Text] [PDF]
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 J. D. Kelty, P. A. Noseworthy, M. E. Feder, R. M. Robertson, and J.-M. Ramirez Thermal Preconditioning and Heat-Shock Protein 72 Preserve Synaptic Transmission during Thermal Stress J. Neurosci., January 1, 2002; 22(1): RC193 - RC193. [Abstract] [Full Text] [PDF]
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) or 0 (
) h after heat shock. The former displays
striatal HSP 72 expression, whereas the latter has none.
