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Physical Fitness Research Laboratory, Department of Kinesiology, University of Illinois, Urbana, Illinois 61801
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study
determined the effects of exercise on the ability of macrophages (M
)
to present antigen to T cells. Pathogen-free male Balb/c mice (8 ± 2 wk of age) were randomly assigned to either home cage control, moderate exercise (Mod; 18 m/min, 5% grade, 0.5 h/day), exhaustive exercise (Exh, 18-30 m/min, 3 h/day), or treadmill control groups. The mice underwent treatments for 4 days
during peritoneal thioglycolate inflammation. Peritoneal M were
harvested, purified, and incubated with chicken ovalbumin (C-OVA;
0-10 mg/ml) for 18 h. M were then cocultured with
C-OVA-specific T cells for 48 h, and the supernatants were analyzed via
ELISA for interleukin-2 as an indication of M antigen presentation (AP). Exh exhibited suppressed (~25-34%) M AP across a wide
range of C-OVA doses when measured immediately, 3, and 24 h
postexercise. In contrast, Mod had reduced M AP only at 3 h
postexercise. M AP was also lower in the treadmill control
(4-27%) compared with the home cage control group, but was
significantly higher than Exh. The reduction in M AP was not due to
exercise-induced differences in M number, percentage, or expression
of intercellular adhesion molecule-1, B7-2, or major
histocompatability complex II, molecules important in AP. In
conclusion, our data lend evidence that may help explain the increased
incidence of infection observed after prolonged exhaustive exercise or overtraining.
immunity; stress; T lymphocytes; interleukin-2; mice; intercellular adhesion molecule-1
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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MACROPHAGES (M) are a first line of defense against
microbial invaders and malignancies by nature of their phagocytic,
cytotoxic, and intracellular killing capacities. They are ubiquitously
located within the body and are involved in the initiation of immune
responses by acting as inflammatory and antigen-presenting cells (APCs) (1). In the antigen presentation (AP) process, M engulf
microorganisms into phagosomes, which then fuse with acidic lysosomes
containing a variety of proteases that digest and process foreign
proteins into antigenic peptides (17). These peptides then associate with major histocompatability complex (MHC) II and are translocated to
the M cell surface where they interact with
CD4+ T lymphocytes (1). The
interactions between M and T cells lead to the generation of
antigen-specific T-cell clones that will eventually recognize and
eradicate the invading microorganism, providing long-lasting immunity.
The ability of the M to present antigen is crucial to immune
function, and, when this ability is compromised, there is an increased
risk of morbidity and mortality due to infection (5, 23).
Several studies have independently examined the effects of exercise on
components of M AP, but none has considered the process as a whole.
These studies, utilizing various modes of exhaustive exercise, have
been shown to increase peritoneal M chemotaxis toward antigenic
stimuli (11, 22), increase phagocytosis of opsonized
Candida albicans (7, 10, 18, 22),
alter metabolic and lysosomal enzyme activity (10), and increase
microbicidal activity as measured by nitro blue tetrazolium reduction
(6). In contrast, we demonstrated that exhaustive, but not moderate, exercise reduced bacterially stimulated expression of MHC II on the
surface of peritoneal M (28). It was hypothesized that this
reduction in MHC II may lead to a reduction in M AP. Unfortunately, the ability of M to present antigens to T lymphocytes has not been
directly measured. Therefore, the purpose of this study was to
determine the effects of different doses of exercise on M AP
ability. An additional purpose was to determine whether any exercise-induced changes in M AP were due to differences in M number or expression of various surface molecules involved in M-T-cell interactions.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals.
A murine model was employed to test the research objectives proposed in
this study. This model was selected to satisfy the need for
experimental manipulation and control and to obtain fully differentiated tissue M that are difficult to obtain from human donors. Balb/cByJ inbred male mice (8 ± 2 wk of age) were used in
this study because of the MHC compatibility
(I-Ad) with the T-cell hybridoma
and our previous experience with this strain. Mice were
housed in a specific-pathogen-free animal containment facility three to
five per cage (12 × 17 × 28 cm) on a 12:12-h light-dark
cycle (0600-1800 light) at 23°C. Mice were provided autoclaved
food (8640 Harlan Teklad 22-5, Harlan, Madison, WI) and water ad
libitum. All experiments were performed at the beginning of the light
cycle (0600-0900). The animal treatments were approved by the
Laboratory Animal Care Advisory Committee at the University of Illinois
at Urbana-Champaign and were within National Institutes of Health guidelines.
Exercise protocol.
The exercise protocol consisted of treadmill running. This mode of
exercise was chosen because exercise intensity and duration can be
experimentally manipulated and quantified (unlike voluntary wheels or
swimming). Mice (3-5 per group in 
3 experiments) were randomly
assigned to one of the following four groups: home cage control (HCC),
moderate exercise (Mod), exhaustive exercise (Exh), or treadmill
control (TC). The HCC group served as temporal controls and remained sedentary in their cages during the 4-day treatment period. The TC group served as isolation and environmental stress controls and were exposed to handling, treadmill noise, and vibration and were deprived of food during the exhaustive exercise bouts but did
not exercise. This group was killed immediately after treadmill
exposure and was included to control for extraneous stressors (i.e.,
handling, noise, and vibrations) that may have been associated with
exhaustive treadmill exercise. The Mod group exercised for 30 min at 18 m/min, 5% grade, and the Exh group exercised for 2.5-3 h at
gradually increasing speeds (18-40 m/min), 5% grade. In past
studies, moderate exercise has been defined as brief (usually
15-60 min) bouts of treadmill running at 50-75% maximum
O2 consumption or ~15-22
m/min (25). Electric shock or prodding was never used in these
experiments, as the mice ran well without extrinsic motivation. The
animals exercised for 4 consecutive days during the time necessary for
thioglycolate (TG) to recruit M to the peritoneal cavity. TG was
injected intraperitoneally (1 ml/mouse) on day
1 immediately after the first exercise session. TG was
employed as a M-eliciting agent for two reasons:
1) it resembled an inflammation,
making it possible to study the effects of exercise on an inflammatory
response, and 2) it provided
increased numbers of M necessary to perform the AP and other assays.
Tissue collection and processing.
Immediately or 3 or 24 h after the final exercise session
(day 4), the mice were killed by
rapid CO2 asphyxiation and
weighed, and the tissues were extracted and processed. The peritoneal
cavity was aseptically lavaged with 10 ml of RPMI-1640 (GIBCO, Grand Island, NY) containing 1 U/ml of sterile heparin to obtain peritoneal exudate cells (PECs). PECs from three to five mice were pooled in each
experiment to obtain enough cells for analysis, and each experiment was
performed multiple (3) times. The PECs were washed (190 g, 5 min, 4°C) twice, counted, and
stained with trypan blue (>95% viable). The cells were adjusted to a
concentration of 2 × 106
cells/ml in RPMI containing 5% heat-inactivated, low-endotoxin (<0.01 ng/ml) fetal bovine serum (FBS; Sigma Chemical, St. Louis, MO), 10
5 M
2-mercaptoethanol, penicillin (100 U/ml), streptomycin (100 U/ml), and
glutamine (20 mM) for use in the M AP and flow cytometric analysis.
M AP assay.
The M AP protocol was adapted from previously published works (13,
16). Briefly, 4 × 105 PECs
per well were plated onto 96-well flat-bottom microtiter plates and
incubated at 37°C, 5% CO2,
and 95% humidity for 3 h to allow the M to adhere to the plate.
After the incubation, the plates were washed four times with RPMI to
remove all nonadherent cells, and, in initial experiments, various
concentrations (0, 0.25, 0.5, 1.0, 2.5, 5, and 10 mg/ml) of chicken
ovalbumin (C-OVA; Sigma Chemical) were added to the plates. The plates
were incubated for 18 h, washed four times with RPMI to remove any
residual C-OVA, and 2 × 105
T hybridoma cells per well were added. The plates were then incubated at 37°C, 5% CO2, and 95%
humidity for 48 h, after which time the supernatants were harvested and
stored at 
80°C until determination of interleukin-2 (IL-2).
Based on initial dose-response studies, we chose antigen concentrations
that reflected suboptimal (2.5 mg/ml) and optimal (10 mg/ml) AP.
(16). Therefore, IL-2 production in this in vitro system
is directly proportional to M AP. The T-cell hybridoma line was
maintained in media consisting of RPMI-1640 with 10% FBS,
105 M 2-mercaptoethanol,
and 100 U/ml of penicillin and streptomycin, and
L-glutamine (20 mM) at 37°C with 5% humidified
CO2. The cells were seeded at a
density of 1 × 104 cells/ml
and were passed every 3 days. Cells were used in all experiments on the
third day of growth. Frozen lots were rederived monthly, and all
experiments used cells that had grown for the same amount of time to
ensure accurate and reliable results.
IL-2 ELISA.
An IL-2 ELISA was developed by using an IL-2 anticytokine capture
antibody (Ab; Pharmingen, San Diego, CA) and a biotinylated IL-2
anticytokine detection Ab (Pharmingen). Briefly, the capture Ab was
diluted to 2 µg/ml in coating buffer, and 50 µl/well were added to
the ELISA plates and incubated at 4°C overnight. The plates were
blocked with PBS containing 10% FBS to reduce nonspecific binding.
Serial dilutions of IL-2 standards (0-2,000 pg/ml; Sigma Chemical)
and the M AP supernatants were added to the appropriate wells and
incubated overnight at 4°C. After the second incubation, 100 µl
of 1 µg/ml detection Ab were added, and the plates were incubated at
room temperature for 45 min. After this incubation, 100 µl of 2.5 µg/ml strepavidin-peroxidase (Sigma Chemical) were added, and the
plates were incubated at room temperature for 30 min. Finally, 100 µl
of 2,2'-azino-bis (3-ethylbenz-thiazoline-6-sulfonic acid) (Sigma
Chemical) substrate were added, and the plates were allowed to develop
at room temperature for 60 min. Color change was quantified by light
absorbency on a microplate reader at 405 nm.
Determination of M number.
To determine whether exercise-induced changes in M AP were due to
changes in M numbers in the culture wells, the number of M in
parallel cultures was assessed by staining postadherent cells removed
with a Teflon cell scraper. The PECs and postadherent samples were
analyzed by flow cytometry with FITC-conjugated monoclonal Ab against
Mac-3 (clone M3/84; Pharmingen), a surface glycoprotein found on mature
TG-elicited M but not on lymphocytes, monocytes, or neutrophils
(14). The cells were centrifuged and resuspended in RPMI with 5% FBS
at 1 × 106 cells/ml and then
incubated on ice for 5 min. FITC-conjugated anti-Mac-3 and the
FITC-conjugated isotypic control Ab were diluted to 2 µg per 1 × 106 cells in PBS with 2%
neonatal calf serum, added to appropriately labeled tubes, and
incubated for 45 min at 4°C. Cells containing only PBS with
neonatal calf serum were used as a control for autofluorescence. The
cells were washed twice with PBS (0.01% sodium azide) and resuspended
in 4% paraformaldehyde, and 1 × 105 cells were analyzed via flow
cytometry. The gating for percent positive and mean fluorescence was
set and adjusted by using the isotypic control and autofluorescence.
Expression of intercellular adhesion molecule-1 (ICAM-1),
B7-2, and MHC II.
To determine whether exercise-induced changes in M AP were due to
differences in M accessory molecule expression, the percentage and
mean fluorescence intensity (MFI) signal of ICAM-1, B7-2, and MHC
II were assessed by staining both the pre- and postadherent PECs with
immunofluorescent monoclonal Ab. These three accessory molecules were
analyzed because of their documented importance in M AP (1, 15, 20)
and because they (i.e., MHC II and ICAM-1) have been shown to be
affected by exercise (3, 28). Two-color analysis was performed on
postadherent M cultured with suboptimal and optimal doses of C-OVA
for 18 h. The M were stained by using FITC anti-Mac-3 and either
anti-ICAM-1, anti-B7-2, or anti-MHC II Ab conjugated to
R-phycoerythrin for analysis. Appropriate isotypic controls and
autofluorescence were run with each sample.
Data analysis. All data are reported as means ± SE. Significant differences among groups were determined by two-way (group × dose or time) ANOVA or one-way ANOVA, depending on the variable. Significance levels were set at P < 0.05. Student-Newman-Keuls contrast procedures were performed when significant main effects existed.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Effects of different doses of exercise on M AP.
Previous studies have shown that the T-cell hybridoma (AO-40.10AG1)
used in this study does not produce IL-2 unless C-OVA antigenic
peptides are presented in the context of MHC II on the surface of an
APC (16, 26). However, because the influence of exercise
on M-T-cell interactions and IL-2 production is unknown, preliminary
experiments were done to determine whether exercise affected the
ability of M to influence T-cell IL-2 production in the absence of
coculture with C-OVA. No T-cell IL-2 production was found in any group
at any time in the absence of M coculture with C-OVA (Fig.
1), thereby ruling out an effect of
exercise on any extraneous M-T-cell interactions leading to T-cell
IL-2 production. In addition, experiments were performed with a related but nonidentical protein (turkey ovalbumin), and no IL-2 production was
found (data not shown), thus demonstrating the specificity of the
response.
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AP at three different times postexercise (immediately, 3, and 24 h) across a wide range (0-10 mg/ml) of C-OVA doses. The data in
the figure represent the means ± SE of duplicate culture wells. In
these representative experiments, at the immediate postexercise time,
both exercise groups were run in the same experiment with one HCC group
(Fig. 1A), whereas at 3 and 24 h
postexercise only one exercise group (Mod or Exh) was run with a HCC
group (Fig. 1, B and
C). Results indicated that
exhaustive exercise suppressed M AP across all C-OVA doses when
measured immediately postexercise, whereas moderate exercise had no
appreciable effect (Fig. 1A). At 3 h postexercise, both moderate and exhaustive exercise significantly reduced M-dependent T-cell IL-2 production at all C-OVA
concentrations (Fig. 1B). Whereas
this suppression continued at the 24-h postexercise time point in both
groups, high concentrations of C-OVA overcame the suppression in the
Mod, but not Exh, group (Fig. 1C).
Even though care was taken to treat the T hybridoma cells consistently
across all experiments (i.e., similar passage and culture conditions),
inherent interassay variability common in bioassays of this type
prohibited the use of all of the raw IL-2 data in one statistical
analysis. This is demonstrated by the differences in IL-2 production in
the HCC group in the different experiments illustrated in Fig. 1.
Therefore, an analysis of all experiments expressed as a percent
difference from HCC {e.g., [(Exh HCC)/HCC] × 100} was performed for data collected at suboptimal (2.5 mg/ml; Fig.
2A) and
optimal (10 mg/ml; Fig. 2B) doses of
C-OVA at all postexercise times.
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AP immediately and 3 h postexercise.
In contrast, there was a small (~10%) suppression in M AP
immediately postexercise in Mod that was significantly less than
that in Exh. Both groups exhibited significant exercise-induced suppression 3 h postexercise. There was a trend
(P = 0.08) toward suppression at 24 h
postexercise in the Exh and Mod groups compared with HCC. There was
also a significant
[F(4, 44) = 4.73, P = 0.004] interaction
effect at the optimal C-OVA dose (Fig. 2B). Contrast procedures revealed
significant suppression (~24-37%) in M AP relative to HCC in
the Exh group immediately and 3 and 24 h postexercise. In contrast,
M AP was suppressed (45%) only at the 3-h postexercise time point
in the Mod group and not immediately or 24 h postexercise. The small
suppression immediately postexercise in Mod and the ability of high
(i.e., 10 mg/ml) concentrations of C-OVA to overcome the suppressive
effect suggest a more robust suppressive effect in M AP in response
to exhaustive exercise compared with moderate exercise.
To determine the independent effects of exercise vs. environmental
stress (i.e., treadmill noise and vibration, handling, isolation) on
M AP, a group of mice (TC) were exposed to the same environment (3 h
of treadmill exposure) as the Exh group but did not exercise. We
measured M AP in this group immediately after treadmill exposure
only (Fig. 2, A and
B). The TC group exhibited
~4-27% reduction in M AP immediately postexposure at the
suboptimal C-OVA dose, which was significantly
(P < 0.05) lower than that in the
HCC group, but significantly (P < 0.05) greater than that in the Exh group (Fig.
2A). At the optimal C-OVA dose,
there was no significant suppression in M AP in the TC group (Fig.
2B). Thus the exhaustive
exercise-induced suppression of M AP was significantly greater than
that observed as a result of environmental stress alone. In other
words, the suppression induced by exhaustive exercise could not be
explained solely by environmental stress.
Effects of exercise on M number and adherence.
The number and percentage of M in the culture wells were quantified,
because a reduction in the number or percentage of M per well could
possibly affect AP (19) and because previous studies have shown that
exercise may affect the adherence capacities of M (6). No
significant differences among treatment groups at any time point were
found by using a one-way ANOVA in which total PEC number
[F(5, 58) = 0.86, P = 0.53], percentage of
Mac-3+ cells pre-
[F(5, 52) = 0.32, P = 0.90] or postadherence [F(5, 43) = 0.52, P = 0.79], and M cell
number pre- [F(5,
58) = 0.10, P = 0.43] or postadherence
[F(5, 43) = 0.52, P = 0.79] were used as
dependent variables (Table 1). Therefore, the reduction in AP observed in the Exh group immediately, 3, and 24 h
postexercise was not a result of differences in M number or
percentage.
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Effects of exercise on M accessory molecule
expression.
Expression of ICAM-1, B7-2, and MHC II are important in M AP to
T cells (1, 15). Because similar numbers and percentages of M among
treatment groups were observed, but there was an exhaustive exercise-induced decrease in M AP, it was hypothesized that M expression of ICAM-1, B7-2, and MHC II might be affected by
exercise. A one-way ANOVA with the use of percent positive or MFI as
the dependent variable and treatment group as the independent variable revealed no significant differences among the groups immediately postexercise for the percentage of M expressing ICAM-1
[F(3, 11) = 1.44, P = 0.30], B7-2
[F(3, 13) = 0.61, P = 0.62], or MHC II
[F(3, 13) = 0.71, P = 0.57] (Table
2). In addition, no significant differences
were found among the groups immediately postexercise for M MFI of
ICAM-1
[F(3, 13) = 3.20, P = 0.08], B7-2
[F(3, 11) = 1.28, P = 0.34], or MHC II
[F(3, 13) = 2.68, P = 0.10]. Therefore,
the reduction in AP observed immediately postexercise was not a result
of either a lower percentage of M expressing these accessory
molecules or a lower amount (i.e., MFI) of these accessory molecules
expressed on the M surface.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The effects of moderate and exhaustive exercise on the ability of
TG-elicited peritoneal M to present antigen to T hybridoma cells at
three different postexercise time points were examined. Exhaustive
exercise was found to suppress M AP across a wide range of C-OVA
doses when measured immediately, 3, and 24 h postexercise. The degree
of suppression was not related to the dose of C-OVA, as the percent
suppression across all doses was similar (data not shown). In contrast,
the effects of moderate exercise on M AP varied, depending on the
time point measured and the dose of C-OVA. Unlike exhaustive exercise,
moderate exercise had little effect on M AP immediately
postexercise. However, moderate exercise suppressed M AP at 3 and
24 h postexercise at a suboptimal dose of C-OVA. At an
optimal C-OVA dose, moderate exercise suppressed M AP only at 3 h
postexercise and not immediately or 24 h postexercise. These data
suggest that the suppressive effect of exhaustive exercise was more
robust than that of moderate exercise.
The exhaustive exercise-induced suppression of M AP could not be
entirely explained by environmental stress and handling. Our data
indicated that M AP in the Exh group was significantly lower than
that exhibited in the TC group, which was exposed to the treadmill for
a period similar to that of the Exh group without running. Therefore,
exhaustive exercise caused a significant suppression of M AP beyond
that observed as a result of changes in the environmental setting.
No studies have examined the effects of exercise stress on M AP.
However, other studies have demonstrated that other types of chronic
stress, such as chronic ethanol consumption (19, 27), dietary protein
deprivation (5, 24), chemical hypotension (9), chronic viral infection
(4), human immunodeficiency virus (23), trauma (2), and old age (12),
suppress AP in a variety of cell types including M, dendritic cells,
and B cells. In contrast, other studies have found that an acute bout
of restraint stress either enhanced (8) or had no effect (29) on M
AP. Taken together, the data would indicate that multiple bouts of prolonged stress are necessary to suppress AP in a variety of APCs.
Preliminary data support this contention because 1 day of exhaustive
exercise (on day 4 after TG injection,
data not shown) did not suppress M AP, whereas 4 consecutive days did.
The results indicated that the effect of exhaustive exercise on M AP
was not due to differences in M number or adherence. Therefore, it
was suspected that M expression of surface molecules important to
M-T-cell interactions was altered by exercise. Indeed, it has been
shown that the expression of these molecules (i.e., MHC II and ICAM-1)
can be affected by exercise (3, 28). In a previous study, we documented
that exhaustive, but not moderate, exercise decreased the ability of
Propioniebacterium acnes to increase
the expression of MHC II on peritoneal M (28). In the present study,
we found no exercise-induced differences in M expression of ICAM-1,
B7-2, or MHC II molecules immediately postexercise. Direct
comparisons between the two studies are made difficult by the fact
that, in the present study, we did not stimulate MHC II expression with
cytokines or bacteria. Even though our data suggest that surface
expression of ICAM-1, B7-2, or MHC II is not responsible for
exercise-induced suppression in M AP, our data do not preclude the
possibility that other surface molecules (i.e., CD40 or B7-1)
associated with M AP were altered in response to exercise. Moreover,
expression of these molecules at 3 and 24 h postexercise was not
measured, and, therefore, we cannot say with confidence that they did
not contribute to suppressed M AP at these later times. Last, only
total surface expression of MHC II, and not MHC II containing C-OVA
peptide, was measured; therefore, it is possible that there could have
been a difference among the groups with respect to the expression of
MHC II containing C-OVA on the M surface. Future studies are
required to determine the intracellular mechanism(s) responsible for
the exercise-induced suppression in M AP.
In conclusion, our results are the first to demonstrate that exercise
suppresses M AP. Four consecutive days of exhaustive exercise
resulted in a marked and prolonged (at least 24 h) depression in the
ability of M to present antigen to T cells. Moderate exercise also
suppressed M AP, although this effect was less pronounced. Thus it
is possible that at least some of the previously reported immune
suppression after repeated exhaustive exercise (21) may be due in part
to a decrease in M AP to T lymphocytes.
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ACKNOWLEDGEMENTS |
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This study was supported in part by National Institute on Aging Grant AG-13928 (to J. A. Woods).
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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: J. A. Woods, 906 S. Goodwin Ave., Univ. of Illinois, Urbana, IL 61801 (E-mail: Woods1{at}uiuc.edu)
Received 12 February 1999; accepted in final form 26 July 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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