Stress Research Unit, Department of Animal Science, University of California, Davis, California 95616
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ABSTRACT |
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There is a cost of stress that may result in the loss of normal biological function (e.g., growth). Repeated, and even single, applications of stressors have been shown to induce negative energy balance in rodents. However, here we addressed whether this energetic response changes during multiple stress exposure and whether there is complete recovery subsequent to the cessation of stress exposure. These questions were addressed in growing C57Bl/6 mice (31 day) by determining at different times the energetic and endocrine responses after the exposure to restraint (R) stress for 4 h applied once (R1), repeatedly over 3 days (R3), or repeatedly over 7 days (R7). Compared with control values, R elevated (P < 0.05) plasma corticosterone and reduced plasma insulin-like growth factor I on all days of exposure to the stressor. Seven days, but not 1 or 3 days of R, decreased the net growth (126%, P < 0.05) and deposition of fat (71%, P < 0.05) and lean (60%, P < 0.05) energy over the 7 days. Only R7 depressed the 7-day metabolizable energy intake (P < 0.05), and R7, but not R1 or R3, increased the overall energy expenditure (10%, P < 0.05). Our results demonstrate that repeated episodes of stress are energetically costly to the rapidly growing animal, but compensatory mechanisms mitigate this cost of repeated stress exposure and permit complete recovery of energy balance after the cessation of stress application.
growth; energy partitioning; feed intake; corticosterone
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INTRODUCTION |
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STRESS CAUSES A SHIFT in biological function, a shift that comes at a biological cost to the individual (47). During stress, changes in metabolism help support the biological defenses an individual uses to maintain homeostasis (13, 21, 48, 57). These metabolic alterations during stress often result in the mobilization of energy away from energy-sensitive functions, such as growth in adolescents and maintenance of body weight in adults (12, 21, 57). As a result, stress can cause negative energy balance. For example, stress characteristically results in depressed body weight and food intake in rodents (16, 27, 36).
Previous reports have demonstrated that the stress-induced depression in body weight is maintained over time, even after the exposure to stress has ceased (27, 52). Although repeated stress (3 daily episodes) was reported to reduce food intake during and subsequent to the last day of stress exposure, one episode only of the stressor depressed food consumption on the day of stress. When the three daily episodes of restraint were applied to young (3-wk-old) rats, reductions in food intake and especially body weight were not as marked or as persistent as those observed in adult rats exposed to the repeated stressor. Results from a study by Marty et al. (42) suggest that chronic, intermittent restraint and immobilization maintain their inhibitory effects on growth and food intake in adult rats over the entire 4-wk experiment.
These findings, and previous results from studies conducted in our laboratory (39), raise two interesting questions about rapidly growing mice: 1) is the energetic response altered over the course of daily exposure to restraint stress? and 2) is there recovery of energy and body weight after the stress-induced depression of growth? To address these questions, we evaluated the energetic response to repeated restraint stress and poststress recovery in young, postweanling mice.
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MATERIALS AND METHODS |
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Male C57Bl/6 mice (B&K Universal, Fremont, CA) were individually housed in hanging wire mesh cages in a room maintained at 23 ± 2°C on a 14:10-h lighting schedule. Before each experiment, mice were acclimated for 1 wk, and all experiments began when mice were 31 days of age. Each experiment lasted 7 days, beginning at 0700 on day 1 and ending at 0700 on day 8. Each day at 0700, body weight was recorded, feed was removed, and feed intake (corrected for spillage) was measured. All mice were then returned to their home cage.
On day 1 of each experiment, all mice were weighed and the treated group was exposed to 4 h of restraint stress by placing each mouse into a well-ventilated restraint tube. During the 4-h restraint period, both experimental and control (nonrestrained) mice had no access to food or water. The restraint tube was a well-ventilated 50-ml plastic centrifuge tube. The tube was tied to the bottom of the cage with Silastic tubing, which was not accessible to the mouse. Several hole punches were evenly distributed throughout the length of each tube, and a bottom section of each tube was removed to allow free drainage of urine and feces. Once the tube had been fastened to the cage, the mouse was placed in the tube and a paper towel plug was used to prevent the mouse from escaping. Mice could move freely back and forth but could not turn around while in the tube. After the 4 h of restraint, mice were removed from the tube, and the tube was removed from the cage.
Immediately after the 4-h restraint period, both restrained and control mice were fed a semipurified test diet (PMI AIN-76A, PMI Feeds, St. Louis, MO) having a guaranteed analysis of 18.4% protein, 5.0% fat, 65.0% carbohydrate, and 5.0% fiber. With the exception of the 4-h restraint period, all mice had ad libitum access to feed and water. All experiments were approved by the University of California, Davis Animal Care and Use Committee.
Experiment 1a: Effect of repeated behavioral stress on growth and
energetics.
To evaluate the cost of repeated behavioral stress, we quantified
growth and energetics of growing mice repeatedly exposed (R,
n = 6) once/day for 7 days, or not exposed (Con,
n = 8) to restraint stress. A comparative slaughter
experimental design was employed to quantify any changes in 7-day
protein (lean) and fat tissue energy. On the 1st day of experimentation
and before the initiation of treatment, an initial group of mice (31 day) was decapitated and dissected into eviscerated carcass (C),
gastrointestinal tract (contents removed) + liver (G), and
remaining viscera (V). These components were analyzed for water
(freeze-drying to constant weight), fat (difference in weight of dried
component before and after ether-acetone extraction), and protein
(Kjeldahl N × 6.25) content. Carcass lean energy (CLE),
GI/Liver lean energy (GLE), and viscera lean energy (VLE) were
determined by multiplying the dry gram protein content by the energy
content of protein (assumed to be 5.4 kcal/g). Carcass fat energy
(CFE), GI/Liver fat energy (GFE), and viscera fat energy (VFE) were
determined by multiplying the dry gram content by the energy content of
fat (assumed to be 9.0 kcal/g). Regression equations were generated
from these data to express C, G, and V water, FE (fat energy), and LE
(lean energy) as linear functions of body weight at age 31 days (Table 1). These regression equations were used
to predict the initial state (i.e., FE, LE) of experimental mice.
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Experiment 1b: Effect of repeated behavioral stress on
corticosterone and insulin-like growth factor I.
To obtain sufficient blood for hormone analyses and to avoid any stress
associated with blood collection, it was necessary to kill mice by
decapitation (within 30 s of removal from their home cage).
Therefore, this experiment paralleled experiment 1a to
examine the effects of repeated behavioral stress on circulating corticosterone and insulin-like growth factor I (IGF-I) over the 7-day
experimental period. In experiment 1b, mice were randomly assigned to 1 of 8 day/treatment combinations, and blood was collected 4 h after the initiation of restraint on days 1, 3, 6, and 7. On each day of blood collection, four mice from each
treatment group were decapitated. Restraint was initiated as described
for experiment 1a, and at the selected times, a
predetermined group of mice was decapitated for the collection of trunk
blood into heparinized (15 U/ml blood) tubes kept on ice until plasma
was separated by centrifugation at 1,000 g at 4°C for 30 min. After centrifugation, plasma was collected and stored at 70°C
until assayed for corticosterone and IGF-I.
Experiment 2a: Growth and energetics of poststress recovery. In this experiment, we examined our young mice to determine if they were capable of recovering from the stress-induced inhibition of growth. To address this question, we first compared the effect of 1 (n = 9), 3 (n = 10), or 7 (n = 11) daily episodes of restraint stress only on growth over 7 days. Controls (n = 10) were not exposed to restraint. Subsequently, we replicated this experiment in a parallel study to quantify the effects of these three stressors on energy partitioning among energy expenditure and lean and fat tissues, as described in experiment 1a. With the exception of R7 (n = 6), each of the Con, R1, and R3 treatment groups represented an n of 5 in this parallel study of energy partitioning.
Experiment 2b: Effect of 1, 3, or 7 episodes of behavioral stress on corticosterone and IGF-I. To address the possibility of a prolonged or carryover effect of 1, 3, or 7 daily episodes of restraint on circulating corticosterone and IGF-I, we examined the plasma concentration of these hormones at 4, 28, 76, and 168 h after the initiation (0700, day 1) of restraint. At the selected times, mice from each treatment group were decapitated, and their trunk blood was collected for the analyses of corticosterone and IGF-I. On each of the selected times, five or six animals from each treatment group were decapitated for blood collection.
Hormone assays. Plasma corticosterone concentrations were determined by RIA with a corticosterone 125I system (ICN, Costa Mesa, CA). Samples were run in duplicate, and the intra- and interassay coefficients of variation were determined as 3.1 and 8.1%, respectively. Plasma IGF-I was extracted using an acid-ethanol procedure with cryoprecipitation (10). Human recombinant IGF-I (R&D Systems, Minneapolis, MN) was iodinated and purified as described by Hodgkinson et al. (29). IGF-I concentrations were determined by a nonequilibrium RIA (10). The polyclonal IGF-I antiserum (UB3-189), kindly provided by Drs. J. J. Van Wyk and L. Underwood, was obtained through the NIDDK National Hormone and Pituitary Program. Samples were run in duplicate, and the intra- and interassay coefficients of variation were determined as 4.2 and 8.2%, respectively.
Statistical analyses.
All data were analyzed using least squares ANOVA procedures (SAS/STAT
User's Guide, 1990). Comparisons between treatment groups for 7-day
MEI, changes in body weight, lean energy (LE), fat energy (FE
),
body energy (BE
), and energy expenditure were analyzed in a
statistical model that included the effect of treatment. For hormone
data, differences between treatment groups were analyzed in a model
that included the effects of treatment, day of collection, and their
interaction. Where indicated, as a means of adjusting energetic
responses to a common MEI, analysis of covariance was employed. Data
from experiments evaluating daily body weight, daily body weight gain,
daily relative body weight gain [body wt gain (g)/body wt (g) or body
wt (g.75)], feed intake, daily relative feed intake
[feed intake/body wt (g) or body wt (g.75)], and
daily feed conversion [body wt gain (g)/feed intake (g)] were
evaluated using a repeated-measures model (22). If a
significant treatment × day interaction was present in the
repeated-measures analysis, data were stratified by day and differences
between treatment groups were analyzed using least squares procedures (SAS/STAT User's Guide, 1990) in a statistical model that included the
effect of treatment. For all analyses, differences in means were
determined with the PDIFF option in PROC GLM (SAS/STAT User's Guide,
1990), and a level of P < 0.05 was considered
statistically significant. A P < 0.10 was considered
to indicate tendencies.
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RESULTS |
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Experiment 1a: Effect of repeated behavioral stress on growth and
energetics.
Although the initial body weights did not differ before the initiation
of treatment (P > 0.10), repeated restraint stress significantly (P < 0.0002) depressed final body weight
and total body weight gain over the 7 days of repeated restraint (Fig.
1A). The repeated
behavioral stressor also reduced (P < 0.0005) daily body weight, daily body weight gain (Fig. 1B), and daily
feed intake (Fig. 1C). However, the effects of repeated
restraint on daily body weight and daily body weight gain were
dependent on the day (Pstress × day
interaction < 0.0001). Relative body weight gain and relative
feed intake were also reduced by repeated restraint stress
(P < 0.0001). Although repeated restraint stress
suppressed absolute feed intake on all 7 days, this stressor reduced
absolute and relative body weight gain and relative feed intake only on
days 1-4. To determine whether the stress-induced reduction in daily body weight was strictly due to differences in feed
intake between stressed and nonstressed mice, daily feed conversion was
calculated. Repeated restraint stress depressed (P < 0.0001) daily feed conversion on only the first 2 days (Fig. 1D).
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Experiment 1b: Effect of repeated behavioral stress on
corticosterone and IGF-I.
On each day of determination, restraint stress increased
(P < 0.0001) circulating corticosterone (Fig.
4A) and reduced
(P < 0.0001) circulating IGF-I (Fig. 4B).
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Experiment 2a: Growth and energetics of poststress recovery.
Initial body weights did not differ (P > 0.10) between
treatment groups. One, three, or seven episodes of restraint stress initially depressed body weight (P < 0.0001), body
weight gain (P < 0.0001), and feed intake
(P < 0.0001) in all animals (Fig. 5). R1, R3, and R7 equally depressed each
of these parameters from day 1 to day 2 (P > 0.1). Likewise, R3 and R7 depressed body weight,
weight gain, and feed intake to the same degree over the first 3 days
(P > 0.1). As in experiment 1, only those
mice that were exposed to 7 days of repeated restraint stress had
depressed final body weight (P < 0.0001) and total
body weight gain (P < 0.0001) over the 7-day
experiment. However, body weight was restored to control levels by
day 3 in animals exposed to one episode of restraint and by
day 7 in mice exposed to three episodes of the stressor.
Mice exposed to one or three daily episodes of restraint stress
appeared to respond with enhanced feed intake, feed conversion, and
growth after the last episode of restraint. To answer this question,
the growth and feed intake data were analyzed from day 2 to
day 8 for those animals that experienced one episode of
restraint and from day 4 to day 8 for mice
exposed to three episodes of restraint. From day 2 to
day 8, separate analyses were made between control mice and
mice exposed to a single episode of restraint and between mice exposed
to one or seven episodes of restraint. From day 4 to
day 8, we compared the data, in two separate analyses, between control mice and mice exposed to three episodes of restraint and between mice exposed to three or seven episodes of restraint.
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Experiment 2b: Effect of one, three, or seven daily episodes of
behavioral stress on corticosterone and IGF-I.
The behavioral stressor elevated (P < 0.0001)
circulating corticosterone on each of the designated sampling days,
when sampling occurred 4 h after the initiation of the stressor
(Fig. 7). The corticosterone
concentrations of mice experiencing a single episode of restraint
stress on day 1 did not differ from control levels on
days 2, 4, and 8. Likewise, the plasma
concentrations of corticosterone in mice exposed to only three episodes
of the stressor did not differ from control concentrations on
days 4 and 8.
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DISCUSSION |
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We found that repeated exposure to an acute episode of restraint stress induced a cost that significantly suppressed normal growth in the growing mouse. This cost to normal growth resulted, at least in part, from altered deposition of energy into lean and fat tissues. Although the overall effect of the repeated stressor was inhibitory, the energetic response to daily restraint was not constant over the 7-day study. Interestingly, although there was an attenuated energetic response to repeated restraint, there were comparable and repeated increases in circulating corticosterone and decreases in IGF-I each time mice were exposed to the stressor. These results support the view that stress can lead to a shift of energy from growth to those functions that prepare the individual for survival (12, 21, 25, 53, 58). Furthermore, our results demonstrate that there is a shift in the energetic response to repeated stress from energy mobilization to energy preservation in young, rapidly growing mice.
Although the body weights of mice exposed to one or three episodes of restraint were initially depressed, the body weights returned to control levels because of a rapid enhancement of growth after the last exposure to stress. In fact, mice exposed to only one or three episodes of the stressor failed to show any net impairment of lean and fat energy deposition, which was in contrast to the animals exposed to seven daily episodes of stress. We previously found (40) that a single episode of restraint significantly reduced the energy deposited into lean and fat tissue 24 h after the initiation of restraint. Therefore, those results and our present work suggest that 1 or 3 days of restraint stress initially impaired energy deposition, but during the poststress period, this energy was replenished by increased rates of energy deposition into both lean and fat tissues. As a result, the mice overcame the inhibitory effects of stress on growth by a period of compensatory growth that enabled them to fully recover energy and normal body weight.
Although other investigators (27, 52) have demonstrated a sustained reduction of body weight after 3 days of restraint stress, this very interesting finding was in adult rats. The drive for growth and the attainment of a mature body weight may have been so great in our mice that compensatory mechanisms to ensure such a body weight, after stress, are intact in such young animals. In contrast, repeated exposure to behavioral stress on all 7 days prevented any compensatory growth, recovery of energy, or the recovery of normal body weight by the final day after seven daily episodes of stress. It is quite possible that, given a recovery period after the 7 days of repeated stress, these mice would also have recovered. However, the longer an individual is incapable of reaching normal stature, the greater that individual is at risk for developing pathologies related to abnormal growth. For example, psychosocial short stature resulting from chronic stress is related to delayed puberty, eating disorders, and/or vulnerability to disease (58).
Although determining the mechanisms that lead to altered energy deposition and growth was not the primary focus of this study, we did evaluate factors known to influence these functions. Feed and metabolizable energy consumption were significantly reduced by repeated behavioral stress, and this response is consistent with the reduced feed or energy intake that results from other types of stress (18, 33, 34, 37). On the other hand, feeding was enhanced during the recovery period after either one or three episodes of stress. Growth depends on nutrient and energy availability, as dictated by intake and its partitioning among tissues (25). Therefore, it is possible that, in this study, the stress-induced reduction in feed and energy intake was responsible for impaired growth, whereas increased intake may have stimulated catch-up growth seen in recovering mice. However, the depressed feed conversion in mice repeatedly exposed to seven episodes of behavioral stress and the enhanced feed conversion in recovering mice indicate that some factor(s) other than altered feed intake affected growth. However, the total effect of the repeated stress was not completely independent from this altered feed consumption, as suggested by the treatment × day interaction effect on daily feed conversion in repeatedly stressed mice and mice recovering from one episode of restraint. Daily feed conversion in mice recovering from three episodes of stress was, however, significantly enhanced on each of the 4 days after the last day of stress, suggesting that mechanisms controlling the efficiency of energy deposition were necessary for rapid recovery of a normal body weight.
Changes in energy expenditure may also explain the altered growth and energy deposition in our repeatedly stressed and recovering mice. In this study, both MEI and total heat energy production were reduced by the repeated exposure to stress. However, this does not preclude the possibility that stress increased basal heat energy production (1, 20, 24, 51, 59). In fact, when differences in MEI between stressed and control mice were removed, only repeated exposure to seven episodes of restraint caused significantly higher net energy expenditure. Thus, although the total energy expenditure may have been suppressed by the significant reduction in MEI (7, 8, 17, 20, 35), the examination of energy expenditure, independent from the effects of MEI, suggests that mice repeatedly exposed to stress had an elevated basal energy expenditure. This stress-induced increase in basal energy expenditure probably caused the overall expenditure to be higher than one would expect from an equivalent reduction of MEI in nonstressed mice. Therefore, the stress-induced elevation in basal expenditure of energy is a cost that increases the quantity of energy partitioned into heat as opposed to growth, and may, in part, have accounted for the impaired growth in the repeatedly stressed mice.
Whereas increased basal energy expenditure may have inhibited normal energy deposition in mice exposed to seven episodes of restraint, mice recovering from stress may have incurred a greater capacity for energy deposition because of lowered basal energy expenditure over the period of recovery. Although our measure of energy expenditure reflects the net sum of all 7 days, the energy expended over the specific period of recovery may have been reduced. A reduced expenditure of energy has been shown to occur in animals experiencing compensatory growth after a period of nutritional stress (19). Because, for a given intake, a lower basal energy expenditure can lead to a greater efficiciency of energy deposition (4), the enhanced feed conversion in our recovering mice may reflect a depressed energy expenditure during the recovery period.
Finally, the hormonal status of an individual dictates energy partitioning, and thus growth capacity (21, 25, 53). Thus stress-induced alterations in hormones known to affect this partitioning may affect growth. We measured circulating concentrations of corticosterone and IGF-I in the present study. IGF-I is an important growth factor (41, 50, 55), and its circulating levels are positively correlated with body size and growth (5, 6, 45, 46). Therefore, repeated inhibition of this growth factor may have contributed to the impaired growth in mice exposed repeatedly to the behavioral stress. Additionally, it has been reported that elevated circulating corticosterone, as seen in this study, has catabolic effects on both protein and fat tissue (30) and inhibits growth and feed efficiency (15, 16, 56). Therefore, the repeated increases in circulating corticosterone in mice exposed repeatedly to restraint stress may have contributed to the alterations in energy partitioning and growth in these behaviorally stressed mice.
It remains uncertain whether changes in the growth hormone/IGF-I and adrenal-cortical systems play a role in stimulating compensatory growth. Our results showed that circulating concentrations of corticosterone and IGF-I in mice exposed to restraint only on day 1 were similar to the concentrations of experimental controls on day 2, and mice exposed to restraint on days 1-3 had circulating concentrations of corticosterone and IGF-I similar to those in experimental controls when the levels of these hormones were determined on day 4. However, our morning determination of corticosterone and IGF-I is not necessarily indicative of the animal's hormonal status at any given time throughout the period of recovery, and thus we cannot exclude these hormones from those factors regulating the enhanced growth of our recovering mice. Furthermore, other factors, such as the receptors and binding proteins for corticosterone and IGF-I, may alter the impact of these circulating hormones on growth-related processes.
We demonstrated that repeated episodes of stress are energetically costly to the rapidly growing animal. However, the results suggest that there are counterregulatory mechanisms that become engaged to attenuate the detrimental effects of repeated stress on growth. Furthermore, there exist poststress mechanisms that induce rapid recovery of energy in young mice. Thus there appear to be mechanisms that serve to preserve excessive energy loss during repeated stress and to enhance poststress recovery of body weight in the young, rapidly growing animal.
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ACKNOWLEDGEMENTS |
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We thank Dr. Chris Calvert for expert advice on growth and energetics and guidance in many areas of the experimentation. Our thanks go to Dr. Anita M. Oberbauer for help with the IGF-I assay and to Dr. Edward J. DePeters and Scott Taylor for technical help with nutritional analyses.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. D. Laugero, Department of Physiology, University of California, San Francisco, CA 94143-0444 (E-mail: laugero{at}itsa.ucsf.edu).
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.
Received 11 May 1999; accepted in final form 22 February 2000.
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