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First published online January 17, 2007
Journal of Experimental Biology 210, 512-521 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02659
Thermogenesis, food intake and serum leptin in cold-exposed lactating Brandt's voles Lasiopodomys brandtii
1 State Key Laboratory of Integrated Management of Pest Insects and Rodents,
Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuan Xilu,
Zhongguancun, Haidian, Beijing 100080, China
2 Graduate School of the Chinese Academy of Sciences, Beijing 100049,
China
* Author for correspondence (e-mail: wangdh{at}ioz.ac.cn)
Accepted 21 November 2006
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Key words: Brandt's vole, Lasiopodomys brandtii, cold exposure, food intake, lactation, serum leptin, uncoupling protein 1 (UCP1)
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Barber et al., 1997). The
increased energy requirements are usually met primarily by an increase in food
intake (Wade and Schneider,
1992; Scantlebury et al.,
2000). For example, food intake increased by fourfold in rats
(Wade and Schneider, 1992) and
threefold in Siberian hamster Phodopus sungorus
(Bartness, 1997) at peak
lactation. Although rodents increased food intake with the time of lactation,
the sustained energy intake reached a plateau in late lactation
(Johnson et al., 2001a). It
has been suggested that the sustained energy intakes in lactation are limited
either by the central machinery involved in acquisition, processing and
allocation of energy, resources and waste products, or by the capacity of
peripheral mammary glands (Hammond and
Diamond, 1997; Bacigalupe and
Bozinovic, 2001; Speakman and
Król, 2005). Many studies have been performed to test
between these two hypotheses; however, the evidence available at present does
not unambiguously support either of them
(Speakman and Król,
2005). The suppression of thermogenesis in brown adipose tissue
(BAT), as shown by tissue hypotrophy, a decrease in mitochondrial biogenesis,
and an impaired expression of genes encoding uncoupling protein 1 (UCP1)
(Trayhurn et al., 1982;
Wade et al., 1986;
Schneider and Wade, 1987;
Li and Wang, 2005a), is an
important thermogenic characteristic during lactation. This adjustment has
been considered as an energy-sparing mechanism to facilitate conversion of
available energy for milk production
(Smith and Grove, 2002). In
addition, use of maternal reserves, which was thought to be a strategy during
lactation only in large mammals (Oftedal,
2000), was also found in some rodents, such as laboratory rats
(Barber et al., 1997), Siberian
hamsters (Schneider and Wade,
1987), Syrian hamsters Mesocricetus auratus
(Wade et al., 1986), mice
(Johnson et al., 2001b), and
Brandt's voles (Lasiopodomys brandtii, formerly Microtus
brandti) (Liu et al.,
2003).
A growing body of evidence indicates that leptin, primarily secreted by
adipocytes, acting on the leptin receptor OB-Rb in the hypothalamus, plays
important roles in regulating both food intake and energy expenditure
(Halaas et al., 1995;
Friedman and Halaas, 1998;
Schwartz et al., 2000).
Circulating leptin concentrations are positively correlated with adiposity and
positive energy balance (Halaas et al.,
1995). During lactation, the daytime serum leptin concentration
decreased by 20–75% and the nocturnal rise in serum leptin was
attenuated in the rats (Woodside et al.,
2000; Denis et al.,
2003). The decrease in serum leptin acted as a starvation signal
(Flier, 1998), and induced
hyperphagia and suppression of thermogenesis during lactation
(Xiao et al., 2004).
Brandt's voles Lasiopodomys brandtii are nonhibernating herbivores
that mainly inhabit the grasslands of Inner Mongolia of China, Mongolia, and
the region of Beigaer in Russia, where the winter lasts for more than 5 months
and average annual temperature is 0–4°C. It has been demonstrated
that Brandt's voles, in common with other small rodents, meet most of the
energy demands for lactation by increasing food intake, using body reserves
(Liu et al., 2003), and also
by decreasing thermogenic capacity in BAT
(Li and Wang, 2005a). In the
wild, voles face combined stresses of lactation and cold exposure. It is well
known that the development of large thermogenic capacities during cold
exposure is an important mechanism to maintain body temperature in rodents
(Cannon and Nedergaard, 2004),
and the increase in food intake compensates for the added energy expenditure
for thermogenesis (Bing et al.,
1998). However, the rodents suppress thermogenic capacity in BAT
(Trayhurn et al., 1982;
Wade et al., 1986;
Schneider and Wade, 1987;
Li and Wang, 2005a) and
increase food intake (Johnson et al.,
2001a; Liu et al.,
2003) during lactation. Thus the adjustment in thermogenesis and
food intake is an interesting question during lactation and simultaneous cold
stress. Some studies showed that in mice, food intake and resting metabolic
rate (RMR) increased during lactation
(Hammond et al., 1994;
Johnson et al., 2001a;
Johnson et al., 2001b), and
food intake further significantly increased when the lactating mice were
exposed to cold (Hammond and Kristan,
2000; Król and
Speakman, 2003). No available data for integrated studies of the
regulation of thermogenesis, food intake and serum leptin levels for wild
rodents have been found, hence the present study aimed to examine whether
Brandt's voles have the ability to adjust energy intake and thermogenesis to
accommodate simultaneous lactation and cold exposure.
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The females were paired with males for 4 days to allow insemination, and then the males were removed. On the day of parturition, the females (lactating in the cold, LC: N=8) and their litters were transferred to a room at 5±1°C with the same photoperiod for 2 weeks, and provided with a small amount of cotton bedding (approximately 3 g) for nest material. Other lactating females (lactating in the warm, LW: N=8) remained at 23±1°C and 12 h:12 h L:D photoperiod. Non-reproductive females were kept either at 23±1°C (non-reproductive females in the warm, NW: N=8) or 5±1°C (non-reproductive females in the cold, NC: N=8) for the same period as the lactating ones. All the groups were given the same amount of cotton bedding. All animal procedures were licensed under the Institutional Animal Care and Use Committee of Institute of Zoology, Chinese Academy of Sciences.
Metabolic trials
Between 09:00 h and 17:00 h on day 11 of lactation or cold exposure, RMR
was measured by using an established closed-circuit respirometer at
30±0.5°C (within the animals' thermal neutral zone) as described
previously (Li and Wang,
2005b). Briefly, the metabolic chamber volume was 3.6 l and the
temperature inside the chamber was maintained by a water bath. KOH and silica
gel were used to absorb carbon dioxide and water, respectively, in the
metabolic chamber. The voles were weighed before and after each test. After 60
min stabilization in the chamber, oxygen consumption was recorded for another
60 min at 5 min intervals. Two stable consecutive lowest readings were taken
to calculate RMR and corrected to standard temperature and pressure (STP)
(Li and Wang, 2005b).
Energy intake
Dry food intake (DFI) was measured for the consecutive 3 days from days 12
to 14 of lactation, as described previously
(Liu et al., 2003). During the
test, voles were housed individually in stainless steel mesh metabolic cage
(24 cmx24 cmx24 cm), in which food and water were provided ad
libitum. Uneaten food and feces were collected after the 3-day test,
oven-dried at 60°C to constant mass, and separated manually. The caloric
value of food and feces were determined by Parr1281 oxygen bomb calorimetry
(Parr Instrument USA). Gross energy intake (GEI, kJ day–1),
digestible energy intake (DEI, kJ day–1) and digestibility
(%) were calculated (Grodzinski and
Wunder, 1975; Liu et al.,
2003) as follows:
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Measurements of cytochrome c oxidase (COX) activity and UCP1 content
All voles were sacrificed between 09:00 h and 11:00 h by puncture of the
posterior vena cava. Serum was collected and stored at –80°C. The
interscapular BAT was carefully dissected, weighed and stored at
–80°C. For measuring total mitochondrial protein content, COX
activity and UCP1 content, BAT was homogenized as described previously
(Zhao and Wang, 2005). The COX
activity of BAT was measured by the polarographic method using oxygen
electrode units (Hansatech Instruments Ltd, Norfolk, England)
(Sundin et al., 1987). The
mitochondrial protein content of BAT was measured with Folin phenol method
using bovine serum albumin as standards
(Lowry et al., 1951).
BAT mitochondrial protein (12 µg per lane) was separated in a
discontinuous SDS-polyacylamide gel (12.5% running gel and 3% stacking gel)
and blotted to a nitrocellulose membrane (Hybond-C, Amersham Biosciences,
Buckinghamshire, UK). Efficiency of protein transfer was checked by staining
gels and nitrocellulose membranes with Commassie Brilliant Blue and Ponceau
Red, respectively. Unspecific binding sites were saturated with 5% non-fat dry
milk in phosphate-buffered saline (PBS). UCP1 was detected using a polyclonal
rabbit anti-hamster UCP1 (1:5000) (supplied by Dr M. Klingenspor, Department
of Biology, Philipps University, Marburg, Germany) as a primary antibody and
peroxidase-conjugated goat anti-rabbit IgG (1:5000) (Jackson Immuno. Inc.,
USA, Baltimore, PA, USA) as the secondary antibody. Enhanced chemoluminescence
(ECL; Amersham Biosciences) was used for detection. UCP1 concentration was
expressed as relative units (RU), determined by using Scion Image Software
(Scion Corporation, Frederick, MA, USA)
(Li and Wang, 2005a;
Li and Wang, 2005b;
Zhao and Wang, 2005;
Zhang and Wang, 2006).
Serum leptin assays
Serum leptin levels were determined by radioimmunoassay (RIA) with a
125I multi-species kit (Cat. No. XL-85K, Linco Research Inc.,
Missouri, USA) (Li and Wang,
2005b; Zhang and Wang,
2006). The lowest level of leptin that could be detected by this
assay was 1.0 ng ml–1 when using a 100 µl sample (see
manufacturer's instructions for multi-species leptin RIA Kit). Inter- and
intra-assay variability for leptin RIA were <3.6% and 8.7%,
respectively.
Morphology
After collecting trunk blood, the visceral organs, including heart, lung,
liver, kidneys, spleen, uterus and gastrointestinal tract (stomach, small
intestine, cecum, proximal colon and distal colon), were extracted and weighed
(±1 mg). The stomach and intestines were rinsed with saline to
eliminate all the gut contents, before being dried and weighed. The remaining
carcass and all the organs were dried in an oven at 60°C to constant mass
(at least 72 h), and then weighed again to obtain the dry mass. The difference
between the wet carcass mass and dry carcass mass was the water mass of
carcass. Total body fat was extracted from the dried carcass by ether
extraction in a Soxhlet apparatus.
Statistics
Data were analyzed using SPSS software (SPSS 1998). Prior to all
statistical analyses, data were examined for assumptions of normality and
homogeneity of variance, using Kolmogorov–Smirnov and Levene tests,
respectively. The differences in body mass of the mother and pups during the
experimental course were analyzed by repeated measures, followed by
Least-Significant Difference (LSD) post-hoc tests. Group differences
in RMR, energy intake (DFI, GEI, DEI), and morphological parameters were
analyzed by a two-way analysis of covariance (ANCOVA) (temperature and
lactation) with body mass as a covariate. Group differences in body mass of
the mother, COX activity, UCP1 content and serum leptin levels were analyzed
by a two-way analysis of variance (ANOVA). Data were further analyzed by
one-way ANOVA or ANCOVA followed by LSD post-hoc tests. Group
differences in the litter and pup masses were analyzed by Independent-samples
t-test. Finally, linear regression analysis was performed to
determine the correlation between residual serum leptin levels and residual
GEI, and UCP1 content. Results are presented as means ± s.e.m.;
P<0.05 was considered to be statistically significant.
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Morphology
Lactating females had higher water mass content of the carcass
(F1,27=30.2, P<0.001), liver and
gastrointestinal tract (Tables
2 and
3), but lower dry carcass mass
(F1,27=34.4, P<0.001), fat mass
(F1,27=26.5, P<0.001) and body fat content
(F1,27=17.2, P<0.001;
Table 1) than did NR females.
Cold-exposed females had lower wet carcass mass
(F1,27=10.0, P<0.01), but higher values in
kidney, small intestine and caudal colon (Table
2 and
3) compared to females in the
warm. Fat free dry mass of the carcass was not affected by either lactation
(F1,27=0.14, P>0.05) or cold exposure
(F1,27=1.92, P>0.05;
Table 1). The masses of kidney,
stomach and small intestine were increased by the interactions of cold
exposure and lactation (Table 2
and 3).
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Energy intake
Cold-exposed females significantly increased their DFI (by 2.6 g
day–1 or 16% in the lactating voles, and by 2.7 g
day–1 or 36% in the NR voles; F1,27=27.7,
P<0.001), DEI (by 18.5 kJ day–1 or 10% in the
lactating voles, and by 31.5 kJ day–1 or 42% in the NR voles;
F1,27=20.5, P<0.001;
Table 4), compared to those in
the warm. The lactating females increased DFI and GEI (by 8.6 g
day–1 or 117% in the warm, and by 8.6 g
day–1 or 86% in the cold; F1,27=106.9,
P<0.001), DEI (by 103.2 kJ day–1 or 136% in the
warm, and by 90.2 kJ day–1 or 84% in the cold;
F1,27=96.1, P<0.001) compared to the NR
females. Digestibility, however, was not changed during cold exposure
(F1,28=0.07, P>0.05) or lactation
(F1,28=3.42, P=0.075). The interaction of cold
exposure and lactation was significant on DEI (F1,27=4.69,
P<0.05) and digestibility (F1,28=6.15,
P<0.05), but not on DFI or GEI (F1,27=2.34,
P>0.05; Table
4).
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RMR and sustained energy intake
As expected, RMR was higher in voles exposed to cold than warm
(F1,27=21.1, P<0.001;
Fig. 3). The lactating voles
(Warm: 148.2±9.6 ml O2 h–1; Cold:
163.6±4.0 ml O2 h–1) had a higher RMR than
NR voles (Warm: 96.6±4.5 ml O2 h–1; Cold:
126.2±5.4 ml O2 h–1)
(F1,27=20.0, P<0.001). There was no
interaction of cold and lactation on RMR (F1,27=2.55,
P>0.05). Body mass was positively correlated with RMR
(R2=0.328, F1,30=14.6,
P<0.001). The sustained daily energy intake at peak lactation was
3.8 times of RMR in the warm, and 4.0 times in the cold.
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Cold exposure increased mitochondrial protein content (F1,28=42.5, P<0.001) and COX activities in BAT expressed per mg mitochondrial protein (F1,28=13.5, P<0.001), per g BAT (F1,28=13.0, P<0.001) and in whole BAT (F1,28=19.1, P<0.001; Table 5) in both the non-reproductive and lactating voles. Lactation also significantly influenced BAT mitochondrial protein content (F1,28=11.0, P<0.01) and COX activity per g BAT (F1,28=13.9, P<0.001; Table 5). Moreover, the mitochondrial protein content in BAT was influenced by the interaction of cold exposure and lactation (F1,28=37.3, P<0.001; Table 5).
UCP1 content in the cold was higher than that in warm (F1,28=37.4, P<0.001; Fig. 4) both in the non-reproductive (by 16%) and lactating voles (by 75%). UCP1 content was also influenced by lactation (F1,28=5.92, P<0.05; Fig. 4), such that the lactating voles decreased UCP1 content by 31% compared with NR in the warm (P<0.05), but there was no difference between these two groups in the cold (P>0.05). There was a significant interaction of cold and lactation on UCP1 content (F1,28=10.5, P<0.01; Fig. 4). The lactating voles in the warm had the lowest UCP1 contents (F3,28=17.9, P<0.001).
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), our data further support the notion that thermogenic
capacity increased for the rodents to respond to the cold. Moreover, lactating
Brandt's voles increased UCP1 content in the cold, to the same level as the
cold-exposed NR females. Energy intake in the cold-exposed lactating females
at peak lactation was increased, to compensate for the added energy demands of
cold exposure. Serum leptin levels decreased in response to lactation, and
were negatively correlated with energy intake, but not with UCP1 content. Our
data suggest that the voles could respond to simultaneous cold and lactation
by increasing their thermogenic capacity and energy intake. Serum leptin may
be involved in the regulation of energy intake, but thermoregulation by leptin
was complicated under different conditions.
Changes in body mass and body compositions
During pregnancy and lactation, nutritional requirements in small mammals
are increased and the maintenance of body mass is critical to the survival and
reproduction (Amico et al.,
1998). The changes in body mass during pregnancy and lactation are
species-specific. For example, laboratory rats
(Leshner et al., 1972) and
mice (Richard and Trayhurn,
1985; Johnson et al.,
2001a) increased body mass and body fat during pregnancy and
lactation. Siberian hamsters (Schneider
and Wade, 1987; Bartness,
1997) and Syrian hamsters
(Fleming, 1978;
Wade et al., 1986) increased
body mass, but decreased body fat mass during pregnancy and lactation. In the
present study, Brandt's voles decreased body mass and body fat mass during
lactation, consistent with the previous findings in the same species
(Liu et al., 2003). These data
suggest that mobilizing body fat may be one of metabolic compensations to meet
the high nutrition (energy) requirements during lactation in some rodent
species. In addition, modification of digestive organs, to meet the high
energy intake and digestion, suggests that the sustained energy intake during
lactation is not limited by the central machinery in Brandt's voles.
We also found that the litter mass decreased during cold exposure. This was
supported by the findings in the cold-exposed lactating mice
(Hammond and Kristan, 2000;
Johnson and Speakman, 2001).
The decrease in the litter mass may be the result of the decreased milk
production or the greater daily energy expenditure of the pups in the cold.
Johnson and Speakman found that cold-exposed lactating mice increased the
volume of milk production and energy content, indicating that it was not the
decrease in milk production that resulted in the decreased litter mass
(Johnson and Speakman, 2001).
Since we did not measure milk production and litter daily energy expenditure,
however, we could not establish the factors that resulted in the decreased
litter mass gains during cold exposure in Brandt's voles.
Changes in RMR and energy intake in response to cold exposure and lactation
The decrease in body mass during lactation was associated with changes in
energy expenditure and intake. The lactating Brandt's voles increased RMR by
53%, as seen in other rodent species
(Harder et al., 1996;
Johnson and Speakman, 2001),
and further increased it by 10% when exposed to cold. The increase in RMR was
consistent with the increases in body mass, organ mass and the decomposition
of fat reserves (Johnstone et al.,
2005). The increased energy demand during lactation and/or cold
exposure is met by the increase in food intake, as also shown for other small
mammals (Wade and Schneider,
1992; Hammond et al.,
1994; Bartness,
1997; Hammond and Kristan,
2000; Scantlebury et al.,
2000; Johnson and Speakman,
2001).
The sustained gross energy intake at peak lactation was 4 times the
measured RMR in cold-exposed female voles, which was similar to the previously
suggested limitation on sustained metabolic rate
(Drent and Dann, 1980), but
was lower compared to the postulated limit of 7xRMR
(Peterson et al., 1990;
Hammond and Diamond, 1997). In
the cold-exposed lactating MF1 mice, however, the sustained energy intake
during late lactation was 9.4xRMR
(Johnson and Speakman, 2001).
This difference between Brandt's voles and MF1 mice may be related to their
different litter sizes, as the former has a mean litter size of around 7
(Liu et al., 2003), while the
latter is around 11 (Johnson and Speakman,
2001). Moreover, MF1 lactating mice in the cold increased food
intake by 6.9 g compared with an average of 2.7 g increase in the
non-reproductive females (Johnson and
Speakman, 2001), while lactating Brandt's voles in the cold
increased by the same amount of food as did the non-reproductive voles.
Additionally, the cold-exposed lactating mice did not increase RMR, while the
lactating Brandt's voles did, which may also result in the lower sustained
metabolic rate in the voles.
Changes of thermogenesis in response to cold exposure and lactation
Thermogenic capacity in small mammals is enhanced in the cold
(Cannon and Nedergaard, 2004),
but suppressed during lactation (Trayhurn
et al., 1982). In the present study, we found that the lactating
voles decreased COX activity and UCP1 content, as shown in the previous study
in Brandt's voles (Li and Wang,
2005a), and also decreased the absolute and relative BAT mass.
These results have also been found in other wild rodents
(Wade et al., 1986;
Schneider and Wade, 1987;
Nizielski et al., 1993).
Inhibition of BAT thermogenesis has a significant energy-sparing effect on
lactating (Trayhurn et al.,
1982) and fasting animals
(Sivitz et al., 1999).
Alternatively, it can avoid overheating due to processing food and producing
milk during lactation (Król and
Speakman, 2003). We also found both non-reproductive and lactating
voles increased BAT thermogenic capacity during cold exposure. These data
suggest that cold-induced BAT thermogenesis is important for Brandt's voles to
survive the cold early spring.
Roles of leptin in regulating energy intake and thermogenesis during cold exposure and lactation
It has been suggested that leptin, positively correlated with body fat
content, plays roles in inducing hyperphagia and inhibiting thermogenesis
during lactation (Schneider et al.,
1998; Stocker et al.,
2004; Xiao et al.,
2004). Serum leptin levels in the lactating voles decreased
significantly, coupled with higher energy expenditure (RMR), compared with the
non-reproductive females. Similar results in the warm were found in rats
(Amico et al., 1998;
Woodside et al., 2000;
Denis et al., 2003) and also
in insectivorous bats Eptesicus fuscus
(Kunz et al., 1999). These
data support the hypothesis that the negative energy state results in the
decrease in serum leptin during lactation
(Vernon et al., 2002).
Interestingly, in rats low leptin levels occur in the presence of large body
fat stores (Brogan et al.,
1999), which suggests that leptin synthesis and/or secretion was
actively inhibited during lactation. Furthermore, our results show that after
correcting for the effects of body mass, residual serum leptin was negatively
related to residual energy intake. Similar results were also found in
seasonally acclimatized Brandt's voles (Li
and Wang, 2005b) and photoperiod acclimated root voles
Microtus oeconomus (Wang et al.,
2006). Other results have indicated that leptin administration to
lactating mice or rats reduced their food intake
(Woodside et al., 2000;
Mistry and Romsos, 2002;
Stocker et al., 2004).
Together, these data may further support the hypothesis
(Flier, 1998) that leptin acts
as a `starvation signal' to increase food intake during negative energy
balance states such as fasting, cold exposure and/or lactation. It should be
noted that, although serum leptin levels decrease little in lactating voles
exposed to cold, food intake was further increased compared with that in the
warm, which may suggest that the lactating voles were much sensitive to the
levels of leptin. Compared with cold-active mammals, hibernators ignore
`satiety signal' of leptin to allow extreme fat deposition during
prehibernatory period (Kronfeld-Schor et
al., 2000).
Although leptin is involved in regulating energy balance, the relationship
between leptin and energy expenditure is still ambiguous. Leptin
administration to mice or rats increased oxygen consumption, UCP1 mRNA and
protein expression (Hwa et al.,
1997; Scarpace and Metheny,
1998; Xiao et al.,
2004). However, BAT thermogenesis was reduced in cold-acclimated
rats when they were injected with exogenous leptin
(Abelenda et al., 2003). Leptin
administration to post-hibernatory Arctic ground squirrels did not alter RMR,
BAT UCP1 mRNA and protein levels, but reduced food intake and weight gain
(Boyer et al., 1997). The
present study showed that serum leptin levels were negatively correlated with
RMR (corrected for body mass) during lactation and cold exposure, in contrast
to the proposed relationship between leptin and energy expenditure
(Hwa et al., 1997). In
previous studies on the cold-acclimated or seasonally acclimatized Brandt's
voles (Li and Wang, 2005b;
Zhang and Wang, 2006), the
decreased serum leptin levels were also associated with increased RMR and
thermogenesis. Moreover, we found that serum leptin levels (corrected for body
mass) were positively correlated with UCP1 content only in the warm-acclimated
voles, but not in the cold. These data suggest that in warm-acclimated voles,
leptin may be involved in decreasing energy expenditure by inducing the
thermogenesis, while in the cold, the increase in thermogenesis activated by
the sympathetic nerve may conceal the reduction of thermogenesis by decreased
serum leptin. Although the exact relationship between leptin and energy
expenditure could not be determined just by the correlation analysis, the
recent finding that a leptin antagonist blocked leptin-mediated anorexic
effects as well as the increase in BAT UCP1 protein
(Zhang et al., 2006), confirms
that leptin plays roles in regulating not only food intake but also
thermogenesis.
Brandt's voles can suppress thermogenesis during lactation. The conserved
available energy might be used for milk production and/or to avoid overheating
during lactation (Johnson et al.,
2001a; Król and
Speakman, 2003). During simultaneous cold exposure and lactation,
however, the voles can increase thermogenesis. Serum leptin, secreted
according to the body status and circumstances, was negatively related to the
energy intake and RMR. These data suggest that Brandt's voles can adjust
energy intake and thermogenesis to accommodate simultaneous lactation and cold
exposure, and serum leptin may potentially be involved in the regulation of
energy intake and thermogenesis, but the thermoregulation in the cold may be
mainly mediated by other factors.
List of abbreviations
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Acknowledgments |
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References |
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