| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Department of Physiology, The
responses of inbred heat-tolerant FOK rats to cold were compared with
those of Wistar King A/H (WKAH) and Std:Wistar (WSTR) strains. The fall
of colonic temperature during cold exposure was unexpectedly smaller in
FOK than in other groups, but the onset of shivering was delayed in
FOK. Norepinephrine (NE)-induced in vivo oxygen consumption and the
mitochondrial uncoupling protein 1 level of brown adipose tissue (BAT)
were not different among the groups, but the cold-induced increases in
in vivo oxygen consumption as well as plasma glycerol and free fatty
acids were higher in FOK than in other groups. In vitro NE-induced
oxygen consumption of BAT was less in FOK than WSTR, but not WKAH. The
magnitude of the NE-induced increase in blood flow through BAT was
higher in FOK than in other groups. These results suggest that FOK
paradoxically have a high capacity for nonshivering thermogenesis in
spite of their high capacity for heat tolerance, probably due to an
increased lipid utilization and improved circulation of BAT.
brown adipose tissue; blood flow through brown adipose tissue; cold
tolerance; nonshivering thermogenesis; oxygen consumption
IT IS WELL ESTABLISHED that cold adaptability of
homeothermic animals is based on the capacities of suppression of heat
dissipation and enhancement of thermogenesis, especially nonshivering
thermogenesis (NST). The required capacities for cold tolerance
and for heat tolerance are opposite, and it is thus probable that
there exists a negative cross-adaptation between heat and cold
tolerance (3). Indeed, heat-acclimated Std:Wistar (WSTR) rats have been
shown to be less tolerant to cold compared with warm-acclimated ones (13). It was also shown that Fischer 344, a less heat-tolerant strain
(5), was more resistant to cold than Sprague-Dawley (10), a moderately
heat-tolerant strain (5). Moreover, the thermogenic response of brown
adipose tissue (BAT) to ventromedial hypothalamus stimulation was less
in Sprague-Dawley rats than in Long-Evans rats (20), one of the least
heat-tolerant strains (5).
The FOK rat (FOK), a genetically heat-tolerant strain with a capacity
for enhanced heat loss, has been developed recently. It was selected
for heat tolerance from an outbred colony of several rat strains such
as Wistar/MK, Jcl:Wistar, Wistar/MS, HOS:Wistar, and WSTR, and was
sib-mated for over 30 generations (7). Survival time at
42.5°C is two times as long in FOK as in the Sprague-Dawley rat,
which has one of the longest survival times among the other rat strains
previously investigated (5, 7). The enhanced heat loss of FOK depends
mainly on the ability to mobilize and evaporate body fluid efficiently
(6), although the weaker response of BAT to mild sympathetic
stimulation under higher body temperature may also participate in the
enhanced heat tolerance of this strain, as the thermogenic response of
BAT to a low dose of isoproterenol at high temperature is claimed to be
less in FOK than Wistar King A/H (WKAH; see Ref. 19), one of the least
heat-tolerant Wistar strains (8). It was also recently shown that FOK
prefers cooler conditions than WKAH and that both the resting body
temperature and the threshold core temperatures for tail skin
vasodilation and cold-induced thermogenesis under body warming or
cooling are lower in FOK compared with those in WKAH (18). These
results imply that the cold tolerance of FOK could be somewhat
different from what is expected according to the viewpoint of negative
cross-adaptation between heat and cold.
We have a special interest in the cold tolerance of FOK, a model animal
of genotypic heat adaptation, and have used this strain to gather
evidence for a further understanding of the thermal regulatory
mechanisms of animals. In the present study, the responses to cold and
the thermogenic activity of FOK were compared with those of WKAH and
WSTR, a moderately heat-tolerant counterpart of the parent strain, to
determine differences in acute cold tolerance between the strains and
to evaluate thermoregulatory mechanism of FOK to cold.
Animals. The FOK strain used was
FOK/Ncu of 33-35 generations, raised in Nagoya City University
Medical School. In every generation except with the last three, the
animals received a heat tolerance test. WKAH and WSTR were purchased
from SLC (Hamamatsu, Tokyo, Japan). Experiments were done on male rats
13-14 wk of age to see the strain difference in cold tolerance of
the above groups. These rats were kept in groups of five in metal cages
at 25 ± 1°C under artificial lighting from 700 to 1900 for
5-6 wk before experiments. They were allowed free access to
standard laboratory chow (Oriental MF; Oriental Yeast, Tokyo, Japan)
and tap water.
Evaluation of cold tolerance. Cold
tolerance of the rats was evaluated from the fall of colonic
temperature (Tcol) under acute cold exposure. Overnight-fasted rats were sheared of hair, and Tcol was measured by a thermistor
thermometer (Takara Kogyo, Tokyo, Japan) inserted 5 cm into the anus
during exposure to 0°C for 3 h.
In vivo NST activity. The capacity for
in vivo NST was evaluated from the increase in oxygen consumption at
25°C induced by the maximum effective dose of norepinephrine (NE)
with an open circuit system. Rats were familiarized with a metabolic
chamber with a volume of 1.5 liters for 3 days (30-60 min/day)
before the experiment. For the experiment, the chamber was immersed in temperature-controlled water to keep the inside temperature of the
chamber at 25 ± 1°C. Air was drawn with a pump via a drying tube containing silica gel and a water trap. The flow rate after drying
was 0.5 l/min. The air was analyzed by an oxygen analyzer (Expired Gas
Monitor 1H21A; NEC-Sanei, Tokyo, Japan), which was calibrated with a
standard gas mixture of 16%
O2-5%
CO2 in
N2. The resting metabolic rate was
estimated from the level of oxygen consumption maintained for the last
10 min of a 2-h habituation period. The rats were injected
intraperitoneally with NE [0.75 mg ( For the measurement of in vivo oxygen consumption under cold exposure,
the chamber was immersed for 1 h, after the 2-h habituation at 25°C
to measure the resting metabolism, in a cooled bath containing an
ethanol-water mixture (1:1 by volume) that lowered the chamber's inside temperature and maintained it at 5°C. The inside temperature of the chamber dropped to 5°C after 15 min of cooling.
Determination of thermogenic indexes of
BAT. BAT composition was determined by the method of
Folch et al. (3a). Interscapular BAT was dissected, cleaned of adhesive
tissue, and minced. The minced BAT (ca. 100 mg) was shaken in a
chloroform-methanol (2:1 by volume) solution for 4 h to extract lipid.
The extract was dried for 1 h at 60°C and then was weighed for
lipid. The tissue residue was dried at 110°C for 4 h and then
weighed for fat-free dry matter (FFDM).
DNA content of the BAT was measured fluorometrically with
bisbenzimidazole (Hoechst 33258; Polyscience) after defatting. About 30 mg of interscapular BAT was homogenized in cold ( Estimation of the mitochondrial uncoupling protein (UCP) 1 of
interscapular BAT was performed as follows: 50 µg of BAT proteins were subjected to reducing SDS-PAGE, transferred to a nylon membrane, and made to react with anti-rat UCP1 serum. Bound antibody was visualized with the chemiluminescence system as recommended by the
manufacturer (Renaisance Kit; New England Nuclear).
In vitro thermogenic activity of BAT.
The in vitro thermogenic capacity of BAT was evaluated by the
NE-induced increase in oxygen consumption of tissue blocks.
Interscapular BAT was dissected from the untreated animal and cleaned
of adhesive tissue, and 50-100 mg of tissue samples were carefully
cut into fine blocks of 0.5-1
mm3. The tissue blocks were
preincubated for 2-3 h at 37°C under slow shaking in
Krebs-Ringer phosphate buffer (pH 7.4), containing half the recommended
concentration of CaCl2, 5 mM
glucose, and 4% BSA (Armour; fraction V, dialyzed for 24 h through
cellulose membrane against the above phosphate buffer). About 20 mg of
the preincubated tissue blocks were transferred and stirred gently in 2 ml of the same buffer, supplemented with oxygen, in a Clark oxygen
electrode measurement chamber (Rank Brothers, Cambridge, UK) at
37°C for ~20 min until a stable respiratory rate was obtained. Next, NE (1 µg/ml) was added, and the changes in oxygen consumption were measured for 20 min. The oxygen electrode was calibrated with
distilled water containing 217 nmol
O2/ml.
Blood flow through BAT and tissue
temperatures. The changes in the blood flow through
interscapular BAT induced by NE (2 µg · 5 µl Plasma lipid contents.
Overnight-fasted rats were sheared of hair, exposed to 0°C for 60 min, and then killed by decapitation. Trunk blood was collected in a
heparinized beaker and centrifuged at 0°C for isolation of plasma.
Plasma samples were frozen at Shivering activity. Shivering activity
was assessed by the amplitude of the electromyogram in
urethan-anesthetized animals (1 g/kg body weight ip) at 5°C for 90 min, using bipolar platinum electrodes, 4 mm apart, inserted in the
neck muscles. During the cold exposure,
Tcol and
Ttail were continuously measured
as noted above.
Statistics. Results are expressed as
means ± SE. Data were analyzed by ANOVA, which was followed by
Sheffé's post hoc multiple comparison and Student's
t-test. A
P value of <0.05 was considered statistically significant.
Cold tolerance. The body weight of FOK
was the same as that of WSTR but less than that of WKAH
(P < 0.01). The BAT weight of FOK
was also the same as that of WSTR but less than that of WKAH
(P < 0.001), whereas the mass of
epididymal white adipose tissue was smaller in FOK compared with WSTR
and WKAH (P < 0.001; Table
1).
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
)-arterenol bitartate
salt (Sigma) · ml
saline
1 · kg
body weight1, resulting in
0.4 mg NE base/kg body weight]. The specific metabolic rate was
expressed in ml
O2 · h1 · kg
body weight0.75.
20°C)
acetone with a high-speed disintegrator (ultra-disperser, model LK-21; Janke and Kunkel) followed by shaking (10 min) and centrifugation (1,800 g, 10 min). The defatted
pellets were homogenized in 10 ml of 1% SDS with a Teflon-glass tissue
grinder and incubated at 37°C for 1 h. Twenty microliters of the
homogenate were separated into aliquots in the cuvette and mixed with
1,980 µl of dye solution (0.1 mg Hoechst 33258/ml TNE buffer
consisting of 10 mM Tris, 0.1 mM EDTA, and 0.1 M NaCl), and the
fluorescence at an excitation wavelength of 365 nm and emission
wavelength of 460 nm was measured using a spectrofluorometer (Hitachi
650-40 fluorescence spectrophotometer; Hitachi, Tokyo, Japan).
Calf thymus DNA (Sigma Chemical, St. Louis, MO) in TNE buffer was used
as a standard.
1 · min1
iv infusion) were measured. The animals were anesthetized with urethan
(1.2 g/kg body weight ip) at a room temperature of 25-28°C. Left and right external jugular cannulas, consisting of an injection needle connected to a PE-50 tube (Cray Adams), were inserted ~1 cm in
vessels to inject a drug or saline solution. For the measurement of BAT
blood flow, laser-Doppler flowmetry (LDF) was performed using an
Advance Flowmeter (AFL21; Advance). The LDF probe (tip diameter 10 mm)
was positioned above the left lobe surface of the BAT. The analog
output of the flowmeter was fed into a multipen recorder TI-106 (Tokai
Irika). Changes in BAT blood flow were calculated as a percentage of
the basal value. The probes of the thermistor thermometer (Takara
Kogyo) were inserted 5 cm into the colon for measuring
Tcol, attached to the proximal
tail skin for skin temperature
(Ttail), and placed beneath the
interscapular BAT for BAT temperature
(TBAT). These temperatures were
recorded continuously with a Takara thermistor thermometer.
70°C until measurement of
lipid contents. Glycerol and free fatty acid (FFA) levels were measured
with commercial kits (F-kit glycerol from Boehringer Mannheim and NEFA
C-test from Wako Pure Chemical Industries, respectively).
RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
Table 1.
Body and adipose tissue weights
The resting Tcol of the rats did
not differ among the three groups, although it was significantly lower
in FOK (P < 0.05) than in other
groups when two groups were compared. They were 37.1 ± 0.12, 37.5 ± 0.08, and 37.5 ± 0.04°C in FOK, WSTR, and WKAH,
respectively. During acute cold exposure,
Tcol significantly dropped in all
groups, but the magnitude of the decrease in
Tcol during cold exposure was
smaller in FOK compared with other groups (P < 0.001). The decrease in
Tcol after 3 h of cold exposure
was 1.5 ± 0.17, 5.4 ± 0.51, and 6.3 ± 0.33°C
in FOK, WSTR, and WKAH, respectively (Fig.
1).
|
In vivo thermogenic activity. The
resting oxygen consumption of WKAH (1,131 ± 31.4 ml · kg0.75 · h1)
was significantly higher (P < 0.01)
than that of other rats, but there was no difference between FOK (1,021 ± 27.5 ml · kg0.75 · h1)
and WSTR (977 ± 28.8 ml · kg0.75 · h1). NE increased
the oxygen consumption in all groups, and the NE-induced increase in
oxygen consumption of FOK did not differ from that of other rats. The
increase in oxygen consumption at 30 min after NE administration was
707 ± 162.1, 397 ± 54.1, and 534 ± 60.8 ml · kg0.75 · h1
in FOK, WSTR, and WKAH, respectively (Fig.
2).
|
Cold exposure also increased the oxygen consumption in all rats, but
the increase was significantly higher in FOK than in the other two
groups (P < 0.001). The increase at
30 min after cold exposure was 2,225 ± 51.7, 1,713 ± 52.1, and
1,485 ± 79.3 ml · kg0.75 · h1
in FOK, WSTR, and WKAH, respectively (Fig.
3).
|
Thermogenic indexes and in vitro thermogenic response
of BAT. DNA content (P < 0.05) and the percentage of FFDM
(P < 0.01) as well as the protein
content (P < 0.001) of BAT in FOK
were larger than those in other groups. Conversely, the percentage of
lipid was lower in FOK compared with that of other groups
(P < 0.001), and there was no
difference among the groups in the content of mitochondrial UCP1 of BAT
(Table 2).
|
The in vitro basal oxygen consumption of BAT was 93.7 ± 12.3, 146.5 ± 20.9, and 99.1 ± 6.1 pmol
O2/µg DNA in FOK, WSTR, and WKAH, respectively, with that of WSTR being higher than that of the
other two groups (P < 0.05). The in
vitro thermogenic response to NE was also higher in WSTR compared with
FOK and WKAH (P < 0.05). NE-induced
maximum increases were 126 ± 13.8, 304 ± 67.5, and 135 ± 22.0 pmol O2/µg DNA in FOK,
WSTR, and WKAH, respectively (Fig. 4).
|
NE-induced changes in blood flow through BAT and in
the body and tissue temperatures. The blood flow
through BAT was not changed by saline infusion. NE infusion
significantly increased the blood flow through BAT in all groups, but
the magnitude of increase was greater in FOK (1,083 ± 60.2%;
P < 0.05) than in WSTR (710 ± 54.7%) and WKAH (825 ± 41.7%; Fig.
5).
|
The initial Tcol and
TBAT did not differ among the
groups, but the Ttail of FOK was
higher than that of WSTR and WKAH (P < 0.01 and 0.05, respectively). NE-induced rises of
Tcol and
Ttail in FOK were higher
(P < 0.05-0.001) than
those in WSTR and WKAH. The increase in
TBAT of FOK was also higher
(P < 0.01) than that of WSTR but not
of WKAH (Table 3).
|
Shivering activity. The initial
Tcol of FOK, WSTR, and WKAH at
25°C under anesthesia were 37.6 ± 0.18, 37.6 ± 0.06, and
37.9 ± 0.24°C, and initial
Ttail were 29.5 ± 0.64, 30.3 ± 0.55, and 30.2 ± 0.27°C, respectively. The initial
Tcol and
Ttail did not differ among the
groups. During cold exposure, the fall in
Tcol was smaller in FOK than in
WSTR and WKAH (P < 0.01), as shown in the cold tolerance experiment, whereas the
Ttail dropped in the same time
course in all groups. The final
Tcol of FOK, WSTR, and WKAH were
33.3 ± 0.21, 29.3 ± 0.20, and 30.2 ± 0.34°C, and final
Ttail were 7.8 ± 0.21, 7.7 ± 0.12, and 7.9 ± 0.19°C, respectively. Nevertheless, the onset of shivering in FOK was delayed
(P < 0.01-0.001), and the
Ttail, but not
Tcol, at the onset of shivering
was lower (P < 0.01-0.001) than
in the other two groups (Table 4).
Furthermore, the shivering activity in FOK was less during the early
part of the 60-min cold exposure than in other groups (data not shown).
|
Changes in plasma lipids in cold. The
plasma levels of glycerol and FFA did not differ among the groups in
warm conditions. Cold exposure increased markedly the plasma glycerol
and FFA levels (P < 0.01) in all
groups. The plasma glycerol and FFA levels after cold exposure were
higher in FOK than in the other groups
(P < 0.05; Table 5).
|
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The present results demonstrate that heat-tolerant FOK rats also have
an enhanced tolerance to cold as a result of successive heat selection.
The cold adaptability of homeotherms depends on a capacity for
suppression of heat loss and for enhancement of heat production. It is,
thus, unexpected that FOK, being genetically tolerant to heat, have a
high capacity for cold tolerance. Indeed, it has been demonstrated that
heat acclimation reduces cold tolerance in rats (13). However, it was
noted that guinea pigs exposed alternatively to warm and cold could
tolerate the wide changes in core temperature by means of extending the
interthreshold zone, that is, decreasing the shivering threshold
but retaining the heat polypnea threshold (2). Gerbils, with low
resting and high peak metabolic rate, can tolerate a wide range of
ambient temperatures from 20 to 38°C (17).
A large-sized animal with a relatively small body surface has an advantage in the cold because of less heat loss from the body, and more subcutaneous fat lessens the heat loss by increasing insulation. However, these factors are not likely to contribute to the improved cold tolerance of FOK, because neither body size nor epididymal white adipose tissue, a representative body fat, was larger in FOK compared with other groups. Suppression of heat loss from the tail skin is also unlikely to contribute to the higher cold tolerance of FOK, as the time course of changes in Ttail during cold exposure did not differ among the groups.
The comparison of the increase in oxygen consumption during acute cold exposure clearly indicated that FOK had a greater thermogenic activity compared with the other strains. It is therefore surmised that the enhancement of heat production, especially NST, plays a significant role in the improved cold tolerance observed in FOK because the onset of shivering is delayed and the shivering activity during acute cold exposure was less in FOK than in the other groups. Furthermore, it is interesting to note that the significantly greater increases in the plasma levels of FFA and glycerol after cold exposure in FOK imply an increase of lipolysis and a greater supply of energy sources for NST.
BAT is the major site of NST (9) in small mammals such as rats, and the thermogenic capacity of BAT is evaluated by the content of mitochondrial UCP1, an indicator of proton conductance pathways (16), and the rate of increase in oxygen consumption induced by NE, the major stimulator of NST (9). However, the mitochondrial UCP1 content and the in vitro response of BAT to NE were not greater in FOK than in the comparison groups, although relatively large amounts of DNA and protein and a high percentage of FFDM in BAT suggest a higher thermogenic activity of BAT in FOK. Determination of the levels of unmasked-state UCP1 and UCP2, a subtype of UCP, which is suggested to increase in heart, skeletal muscle, and BAT during cold exposure (1), should be useful for further evaluation of thermogenic activity of BAT in FOK. Contrary to expectations, it was shown that the increase in blood flow through BAT induced by NE was significantly higher in FOK than other groups. The rate of blood flow through BAT is an important factor contributing to the thermogenic activity of BAT (4). Therefore, it is likely that the marked response to NE in the blood flow through BAT compensates for the low in vitro thermogenic activity of this tissue in FOK and that it contributes, at least in part, to an enhancement of NST. It should be also noted that the ability of BAT to vasodilate to dissipate the generated heat to the periphery to maintain core body temperature might be enhanced, causing the high capacity for cold tolerance in FOK. It was demonstrated that nitric oxide contributes to the increase in blood flow through BAT (15). Thus it is possible that nitric oxide plays a significant role in the increase in blood flow through BAT in FOK.
It still remains to be clarified why FOK does not exhibit an improved in vivo response to NE under warm conditions, in spite of the enhanced NST under cold exposure. Glucagon might be involved in the enhanced cold-induced NST because glucagon is a potent stimulator of BAT thermogenic activity in rats (14) and has been demonstrated to stimulate lipolysis in BAT and to increase heat production in brown adipocytes (11) as well as oxygen consumption in BAT tissue blocks (22). Furthermore, both cold and immobilization stress greatly elevate not only the plasma but also the BAT glucagon levels in rats (21), and NE significantly elevates the plasma and BAT glucagon levels (12). The significance of glucagon in NST of FOK should be elucidated in a further study.
In any event, the present results seem to indicate that an enhanced NST activity is involved in the high capacity for cold tolerance of FOK. In this context, it is interesting to note that a great adaptability of BAT mitochondria could cause a low resting metabolic rate and a high peak metabolic rate, making it possible for gerbils to tolerate a wide range of ambient temperatures (17). It was recently shown that the core body temperature under warm conditions and both threshold core temperatures for tail skin vasodilation and cold-induced thermogenesis under body warming or cooling were lower in FOK compared with those in WKAH (18). The lower resting Tcol of FOK was also observed in the present study, and this result could imply the improved cold tolerance of this rat. It hence may be concluded that FOK has a high capacity for NST through an improved circulation in BAT, at least in part, and that factor(s) other than NE, such as glucagon, contribute to the activation of BAT in FOK.
The present results indicate that the inbred heat-tolerant FOK has paradoxically a high capacity for NST. It is probably due to an improved circulation in BAT because the NE-induced increase in blood flow through BAT was greater in FOK than in the compared rats. However, the thermogenic responses of FOK to NE were not higher, unexpectedly, compared with those of the other rats in both the in vivo experiment and the in vitro experiment on BAT. These results suggest the possibilities that blood vessel sensitivity to NE is different in FOK than in other strains of rat, that the ability of BAT in FOK to vasodilate to dissipate the generated heat to the periphery to maintain core temperature is enhanced, and that factor(s) other than NE contribute to the activation of BAT. It is also suggested that the enhancement of NST in tissue(s) other than BAT contributes to the improvement of cold tolerance in FOK. In this context, it would be worthwhile to examine the role of glucagon in NST in this rat. In any event, it is probable that the genetic selection procedure of FOK led to improved heat tolerance but did not necessarily select the traits associated with heat acclimation and that elucidating the above problems may give clues for a further understanding of the thermal regulatory mechanisms of animals.
| |
ACKNOWLEDGEMENTS |
|---|
We are grateful to Professor H. Sakamoto, Asahikawa Medical College, for advice and kind arrangements for the measurement of electromyogram.
| |
FOOTNOTES |
|---|
This study was partly supported by a Grant-in-Aid no. 07557190 from the Ministry of Education, Science, Sports and Culture of Japan.
Present address of T. Yahata: Department of Nursing, Nayoro City College, Nayoro 096-8641, Japan.
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: T. Yahata, Dept. of Nursing, Nayoro City College, W2-N8 Nayoro 096-8641, Japan (E-mail: hryahata{at}snow.hokkai.or.jp).
Received 6 November 1998; accepted in final form 16 April 1999.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Boss, O.,
S. Samec,
A. Dulloo,
J. Seydoux,
P. Muzzin,
and
J.-P. Giacobino.
Tissue-dependent upregulation of rat uncoupling protein-2 expression in response to fasting or cold.
FEBS Lett.
412:
111-114,
1997[Medline].
2.
Brück, K.,
W. Wünnenberg,
H. Gallmeier,
and
B. Ziehm.
Shift of threshold temperature for shivering and heat polypnea as a mode of thermal adaptation.
Pflügers Arch.
321:
159-172,
1970[Medline].
3.
Fleischner, J. R.,
and
F. Sergent II.
Effects of heat and cold on the albino rat: crossed resistance or crossed sensitization?
J. Appl. Physiol.
114:
789-797,
1959.
3a.
Folch, J.,
I. Ascoli,
M. Lees,
J. Meath,
and
F. N. LeBaron.
Preparation of lipid extracts from brain tissue.
J. Biol. Chem.
191:
833-841,
1951
4.
Foster, D. O.,
F. Depocas,
G. Zaror-Behrens,
M. L. Frydman,
and
S. Lacelle.
Effects of rate of blood flow on fractional extraction and on uptake of infused noradrenaline by brown adipose tissue in vivo.
Can. J. Physiol. Pharmacol.
58:
1212-1220,
1980[Medline].
5.
Furuyama, F.
Strain difference in thermoregulation of rats surviving extreme heat.
J. Appl. Physiol. Respir. Environ. Exercise Physiol.
52:
410-415,
1982
6.
Furuyama, F.,
M. Murakami,
T. Oiwa,
and
H. Nishino.
Differences in thermal salivation between the FOK rat (a model of genotypic heat adaptation) and three other rat strains.
Physiol. Behav.
63:
787-793,
1998[Medline].
7.
Furuyama, F.,
and
K. Ohara.
Genetic development of an inbred rat strain with increased resistance adaptation to a hot environment.
Am. J. Physiol.
265 (Regulatory Integrative Comp. Physiol. 34):
R957-R962,
1993
8.
Furuyama, F.,
T. Yoshida,
M. Kumazaki,
and
K. Ohara.
Thermal salivation and body water economics among Wistar strains.
Jpn. J. Vet. Res.
50:
415-423,
1988.
9.
Janský, L.
Non-shivering thermogenesis and its thermoregulatory significance.
Biol. Rev..
48:
85-132,
1973[Medline].
10.
Kiang-Ulrich, M.,
and
S. M. Horvath.
Metabolic responses to tyramine and cold in young male Sprague-Dawley and Fischer 344 rats.
Am. J. Physiol.
246 (Endocrinol. Metab. 9):
E141-E144,
1984
11.
Kuroshima, A.,
and
T. Yahata.
Thermogenic responses of brown adipocytes to noradrenaline and glucagon in heat-acclimated and cold-acclimated rats.
Jpn. J. Physiol.
29:
683-690,
1979[Medline].
12.
Kuroshima, A.,
and
T. Yahata.
Noradrenaline-induced changes in rat brown adipose tissue glucagon.
Jpn. J. Physiol.
39:
311-315,
1989[Medline].
13.
Kuroshima, A.,
T. Yahata,
K. Doi,
and
T. Ohno.
Thermal and metabolic responses of temperature-acclimated rats during cold and heat exposures.
Jpn. J. Physiol.
32:
561-571,
1982[Medline].
14.
Kuroshima, A.,
T. Yahata,
Y. Habara,
and
T. Ohno.
Hormonal regulation of brown adipose tissue
with special reference to the participation of endocrine pancreas.
J. Therm. Biol.
9:
81-85,
1984.
15.
Nagashima, T.,
H. Ohinata,
and
A. Kuroshima.
Involvement of nitric oxide in noradrenaline-induced increase in blood flow through brown adipose tissue.
Life Sci.
54:
17-25,
1994[Medline].
16.
Nedergaard, J.,
and
B. Cannon.
[3H]GDP binding and thermogenin amount in brown adipose tissue mitochondria from cold-exposed rats.
Am. J. Physiol.
248 (Cell Physiol. 17):
C365-C371,
1985
17.
Oufara, S.,
H. Barré,
J.-L. Rouanet,
and
Y. Minaire.
Great adaptability of brown adipose tissue mitochondria to extreme ambient temperatures in control and cold-acclimated gerbils as compared with mice.
Comp. Biochem. Physiol.
90B:
209-214,
1988.
18.
Shido, O.,
S. Sakurada,
N. Sugimoto,
F. Furuyama,
and
T. Nagasaka.
Thermoeffector thresholds and preferred ambient temperature of the FOK rats.
Am. J. Physiol.
274 (Regulatory Integrative Comp. Physiol. 43):
R604-R609,
1998
19.
Tanaka, E.,
A. Yamakawa,
K. Ito,
M. Yamamura,
and
F. Furuyama.
Heat production by brown adipocytes of FOK rats genetically resistant to a hot environment.
J. Vet. Med. Sci.
59:
1157-1159,
1997[Medline].
20.
Thornhill, J.,
and
I. Halvorson.
Differences in brown adipose tissue thermogenic responses between Long-Evans and Sprague-Dawley rats.
Am. J. Physiol.
263 (Regulatory Integrative Comp. Physiol. 32):
R59-R69,
1992
21.
Yahata, T.,
and
A. Kuroshima.
Cold-induced changes in glucagon of brown adipose tissue.
Jpn. J. Physiol.
37:
773-782,
1987[Medline].
22.
Yahata, T.,
and
A. Kuroshima.
In vitro thermogenic activity of rat brown adipose tissue in neonatal period.
Biol. Neonate
64:
53-61,
1993[Medline].
This article has been cited by other articles:
|
|
 |
|
  Y. Masuda, S. Haramizu, K. Oki, K. Ohnuki, T. Watanabe, S. Yazawa, T. Kawada, S.-i. Hashizume, and T. Fushiki Upregulation of uncoupling proteins by oral administration of capsiate, a nonpungent capsaicin analog J Appl Physiol, December 1, 2003; 95(6): 2408 - 2415. [Abstract] [Full Text]
|
|
|
|
 |
|
 F. Furuyama, M. Murakami, E. Tanaka, H. Hida, D. Miyazawa, T. Oiwa, Y. Isobe, and H. Nishino Regulation mode of evaporative cooling underlying a strategy of the heat-tolerant FOK rat for enduring ambient heat Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2003; 285(6): R1439 - R1445. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
, FOK; 
, Wistar (WSTR); 
, Wistar King A/H (WKAH).
Number of rats was 8 (FOK), 5 (WSTR), and 6 (WKAH).
*** Significantly different from WSTR and WKAH,
P < 0.001.
O2) of conscious rats during
cold exposure (5°C). Data are means ± SE. 
