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1 Department of Immunology, Juntendo University School of Medicine, Tokyo 113-8421; and 2 Department of Health Science, Meiji University School of Business Administration, Tokyo 168-0064, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The change of plasma
catecholamine concentration correlates with the change of natural
killer (NK) activity and NK cell number in peripheral blood mononuclear
cells (PBMC) during and after moderate exercise. We studied the
causal relation between exercise-induced catecholamine and expression
of adhesion molecules on NK cells during and after exercise. The
expression of CD44 and CD18 on CD3
CD56+ NK
cells was significantly reduced during exercise (P < 0.01). When PBMC were stimulated with 108M norepinephrine
in vitro, the expression of these adhesion molecules on
CD3CD56+ NK cells was downmodulated within 30 min. The binding capacity of NK cells to a CD44 ligand, hyaluronate,
was reduced by the stimulation with norepinephrine (P < 0.01). The intravenous injection of norepinephrine in mice decreased
the expression of CD44 and CD18 on CD3NK1.1+
cells (P < 0.01) and increased the number of
CD3NK1.1+ cells in PBMC (P < 0.01). These findings suggest that exercise-induced catecholamines
modulate the expression of adhesion molecules on NK cells, resulting in
the mobilization of NK cells into the circulation.
natural killer activity; norepinephrine; CD44 expression
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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DURING
EXERCISE natural killer (NK) cell activity and NK cell
number are increased, and after exercise they are suppressed (8,
11, 12, 15, 16, 18-20, 26). It has been suggested that the
exercise-induced modulation of NK activity is mainly caused by a
mobilization of NK cells into the blood (5, 14, 23, 24).
In response to physical exercise, the blood concentrations of stress
hormones increase, including epinephrine and norepinephrine. These
exercise-induced catecholamines have been implicated in a selective
increase in circulating NK cells that express 
-adrenergic receptors
(9, 17, 21, 22, 25). However, the molecular mechanisms for
the catecholamine-induced mobilization of NK cells remain elusive.
We hypothesized that the exercise-induced catecholamines stimulate the
-adrenergic receptors on NK cells, which might modulate the
expression level of adhesion molecules critical for migration of NK
cells. In this study, we investigated the causal association between
the exercise-induced catecholamines and the change in the expression of
adhesion molecules on NK cells during and after exercise. We found that
norepinephrine rapidly downmodulates CD44 expression on NK cells, which
appears to be relevant to the mobilization of NK cells during exercise.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Eight healthy, nonsmoking males (19.6 ± 0.5 yr old, maximal oxygen consumption = 47.8 ± 6.6 ml · kg1 · min1) were used
in this study. Exercise was performed with a cycle ergometer for 30 min
at 110% of ventilation threshold (VT)
O2. Blood samples were obtained 10 min
before, immediately after, and 5, 15, 30, and 60 min after exercise for
determination of NK activity,
CD3CD16+CD56+ NK cell number, and
plasma epinephrine, norepinephrine, dopamine, -endorphin,
PGE2, and cortisol concentrations.
NK Activity
Isolation of peripheral blood mononuclear cells. Peripheral blood mononuclear cells (PBMC) were separated by Ficoll-Hypaque density-gradient centrifugation, washed twice with PBS, and suspended in RPMI 1640 medium containing 10% (vol/vol) fetal bovine serum and penicillin-streptomycin (complete medium).
Cell lines. The K562 erythroleukemic cell line was used as a target cell in the assay. The cells were maintained in the complete medium and used in the early and mid-log phases for NK assay.
Labeling of target cells with europium. K562 target cells were labeled with nonradioactive europium-diethylenetriaminepentaacetic acid (Eu-DTPA). The labeling procedure used was the same as previously described (4, 13). Before labeling, K562 cells were washed twice with buffer A (in mM: 50 HEPES, 93 NaCl, 5 KCl, and 2 MgCl2). K562 cells were then incubated in a labeling buffer (in mM: 40 Eu, 125 DTPA, and 250 dextran sulfate) for 20 min at 4°C. After labeling, the cells were washed seven times with buffer B (in mM: 50 HEPES, 93 NaCl, 5 KCl, 2 MgCl2, 2 CaCl2, and 10 dextrose) and twice with the complete medium and resuspended at a concentration of 1 × 105 cells/ml.
NK assay.
One hundred microliters of target cells labeled with Eu-DTPA were
pipetted into the wells of a 96-well round-bottom microplate. An equal
volume of effector cells was added to give effector-to-target cell
ratios of 5:1, 10:1, and 20:1. The plate was centrifuged for 1 min at
1,000 g and then incubated for 2 h in a humidified 5%
CO2 atmosphere at 37°C. Twenty microliters of supernatant
and one hundred microliters of enhancement solution (Pharmacia) were added into each well of a 96-well flat-bottom microplate (immunoassay plate, Nunc). The released Eu3+ was detected by measuring
the fluorescence on a time-resolved fluorometer (Arcus 1232 Delphia
fluorometer, Pharmacia). The spontaneous release was determined from
the well with target cells alone. The maximum release was determined by
lysing the target cells with 10 µl of 10% Triton X-100. The
percentage of the Eu3+ release was calculated according to
the formula
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Phenotypic Analyses
Aliquots (1 × 106) of PBMC were stained with FITC-labeled anti-CD16 (Leu-11a, Becton Dickinson, San Jose, CA), phycoerythrin (PE)-labeled anti-CD56 (NKH1, Coulter), and perpridinin-chlorophyll (PerCP)-labeled anti-CD3 (Leu-4, Becton Dickinson) monoclonal antibodies (MAbs) for 15 min at 4°C. After being washed twice with PBS, the cells were subjected to three-color flow cytometric analysis on a FACScan (Becton Dickinson). NK cell number in PBMC was determined as a percentage of CD3CD16+CD56+ cells.
Hormonal Measurement
Epinephrine, norepinephrine, and dopamine in plasma were measured by HPLC. Plasma prostaglandin E2, cortisol, and-endorphin concentrations were determined by RIA.
Expression of Adhesion Molecules
FITC-labeled MAbs against CD31, CD44, CD49d, CD18, and CD62L were obtained from PharMingen (San Diego, CA). Aliquots of cells (1 × 106) were stained with one of these FITC-labeled MAbs, PE-labeled anti-CD56 MAb, and PerCP-labeled anti-CD3 MAb at a concentration of 1 µg/100 µl for 15 min at 4°C. After being washed twice with PBS, the cells were subjected to three-color flow cytometric analysis on a FACScan. The expression levels of each adhesion molecule were determined by mean fluorescence intensity (MFI) of FITC fluorescence on CD3CD56+ cells.
Binding Assay
Coating. Tissue culture dishes (Becton Dickinson) were coated with 0.1% sodium hyaluronate (Wako, Osaka, Japan) in PBS for 1 h at 37°C. Control dishes were incubated with PBS for 1 h at 37°C.
Stimulation of PBMC with norepinephrine.
PBMC were resuspended at 1 × 106/ ml in RPMI 1640 medium containing 1% BSA. After 108 M norepinephrine was
added to 5 ml of the PBMC suspension, the mixture was incubated for 30 min at 37°C. Another 5 ml of PBMC suspension did not receive
norepinephrine as a control and was similarly incubated at 37°C for
30 min.
Binding assay procedure.
After precoated dishes were washed twice with PBS, PBMC incubated with
or without norepinephrine were added to the dishes. The cells were
incubated to adhere for 1 h in a humidified 5% CO2
atmosphere at 37°C. Nonadherent cells were carefully removed with a
pipette after gentle agitation. The plates were then gently washed
three times with prewarmed RPMI 1640 containing 1% BSA, and the
remaining nonadherent cells were added to the former nonadherent cells.
Adherent cells were then detached from the plates using Cell Scraper L
(Sumilon, Tokyo, Japan) and collected with a pipette. After cells were
counted, the nonadherent or adherent cells were stained with
FITC-labeled anti-CD14 MAb (PharMingen), PE-labeled anti-CD56 MAb, and
PerCP-labeled anti-CD3 mAb. The content of CD3CD14CD56+ NK cells was then
analyzed by flow cytometry. The percent adherence of NK cells was
calculated as
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In Vivo Analyses in Mice
Experimental design. Six-week-old male C57BL/6 mice were purchased from Charles River (Shizuoka, Japan). Five mice in each group were intravenously injected with 3 ng of norepinephrine in 100 µl of PBS or with PBS alone. After 10 min, PBMC were prepared from each mouse and analyzed for the frequency of NK cells and expression of CD44 and CD18 on NK cells.
Isolation of PBMC. PBMC were isolated by density-gradient centrifugation by using mouse-sodium meharizoate ficoll (M-SMF, JIMRD, Gunma, Japan), washed twice, and suspended in the complete medium.
Phenotypic analysis.
Aliquots (1 × 106) of PBMC were stained with
FITC-labeled anti-CD3 (145-2C11, PharMingen) and PE-labeled
anti-NK1.1 (PK136, PharMingen) MAbs for 15 min at 4°C. After being
washed twice with PBS, the cells were analyzed for frequency of
CD3NK1.1+ cells by flow cytometry.
Expression of CD44 and CD18 on NK cells.
Aliquots (1 × 106) of PBMC were stained with
FITC-labeled anti-CD44 (IM7, PharMingen) or FITC-labeled anti-CD18
(C71/16, PharMingen) MAb, PE-labeled anti-NK1.1 MAb, and
cytochrome-labeled anti-CD3 MAb (145-2C11, PharMingen) for 15 min at 4°C. The cells were then analyzed by
three-color flow cytometry. The expression levels of CD44 and
CD18 were determined by MFI of FITC fluorescence on CD3NK1.1+ cells.
Statistical Analyses
Data from the exercise experiments in vivo were analyzed using one-factor ANOVA. When a significant F ratio was demonstrated, differences between time points were determined by Bonferroni post hoc analysis. Student's t-tests were carried out for the data from the experiments in vitro and in vivo for mice. Linear regressions were calculated by Pearson's method. All statistical calculations were performed using StatView program for Macintosh (Abacus Concepts, Berkeley, CA), with statistical significance set at P < 0.05.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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PBMC were prepared from venous blood drawn at 10 min before and 0, 10, 20, 30, and 60 min after an exercise (110% VT). NK activity was
tested against K562 target cells by the Eu release assay, and the
frequency of CD3CD16+CD56+ NK
cells was determined by flow cytometry. Figure
1 represents means ± SD of eight
individuals tested. NK activity was significantly increased during
exercise (P < 0.01) and then suppressed after exercise
(P < 0.05). The change in NK activity (Fig.
1A) was well correlated with the change in frequency of
CD3CD16+CD56+ NK cells in PBMC
(Fig. 1B) (r > 0.623 at 6 different time
points, P < 0.05), suggesting that the change in NK
activity of PBMC during and after the exercise is predominantly
determined by the NK cell contents in PBMC.
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Simultaneously, we measured the blood concentrations of epinephrine and
norepinephrine (Fig. 2). Dopamine,
cortisol, -endorphin, and PGE2 were also measured,
because these hormones have been known to affect NK activity (6,
7, 10, 17). The concentrations of epinephrine, norepinephrine,
and dopamine were significantly increased during exercise
(P < 0.001 or P < 0.01) and returned to basal levels after exercise. These transitions correlated closely with the change in NK activity (r > 0.624 at 4 time
points and r > 0.320 at another 2 time points,
P < 0.05) and the frequency of
CD3CD16+CD56+ cells
(r > 0.301 at 4 time points, P < 0.05). On the other hand, the concentrations of cortisol,
-endorphin, and PGE2 did not change.
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We also examined the changes in expression of various adhesion
molecules (CD31, CD44, CD49d, CD18, and CD62L) on
CD3CD56+ NK cells during and after exercise
(Fig. 3). The expression of CD44 and CD18
was significantly decreased during exercise. The change in CD44 and
CD62L expression on NK cells during the time course showed a reverse
pattern to the NK activity and the frequency of NK cells. On the other
hand, the expression of CD31 or CD49d on
CD3CD56+ NK cells did not change.
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We next examined the effect of catecholamines on the expression of
these adhesion molecules on NK cells in vitro. PBMC were incubated with
108 M (1.69 ng/ml) norepinephrine for 10, 30, or 60 min
at 37°C, and the expression of CD44, CD18, CD31, or CD49d on
CD3CD56+ cells was analyzed by flow
cytometry. We selected this concentration because the serum
norepinephrine level after exercise was ~7 × 109
M, as shown in Fig. 2. As shown in Fig.
4, expression of CD44 was gradually
downmodulated by norepinephrine. Expression of CD18 was decreased at 10 min but then recovered at 30 min. On the other hand, expression of CD31
and CD49d did not change.
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It is known that the CD44 molecules on lymphocytes bind to hyaluronic
acid on blood vessels. We next examined the effect of catecholamines on
binding of NK cells to hyaluronic acid. After PBMC were stimulated with
108 M norepinephrine at 37°C for 30 min, the binding of CD3CD56+ NK cells to
hyaluronic acid-coated plates was measured. As shown in Fig.
5, NK cells exhibited significantly
higher binding to hyaluronate-coated plates than to uncoated
plates (P < 0.01) in the absence of norepinephrine.
However, in the presence of norepinephrine, the binding of NK cells to
hyaluronate-coated plates was significantly inhibited
(P < 0.01). These results suggested that
norepinephrine inhibits binding of NK cells to hyaluronic acid by
downmodulating CD44.
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Finally, we verified the in vivo effect of catecholamines on the
mobilization of NK cells and the expression of adhesion molecules on NK
cells in the murine system. Mice were intravenously injected with 3 ng
of norepinephrine per mouse, and the peripheral blood was taken after
10 min. The frequency of CD3NK1.1+ NK cells
in PBMC and the expression of CD44 and CD18 on NK cells were analyzed
by flow cytometry. As shown in Fig.
6A, the frequency of
CD3NK1.1+ NK cells in PBMC was significantly
increased by norepinephrine administration (P < 0.01).
Concomitantly, the expression of CD44 and CD18 on
CD3NK1.1+ NK cells was significantly
decreased in norepinephrine-treated mice (P < 0.01;
Fig. 6B).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In this study, we demonstrated that the dynamic change in peripheral blood NK activity during and after an exercise is associated with mobilization of NK cells, which appears to result from modulation of adhesion molecules such as CD44 on NK cells by exercise-induced catecholamines. In support of this notion, an intravenous injection of norepinephrine into mice induced a rapid mobilization of NK cells into circulation in association with downmodulation of adhesion molecules on NK cells.
Some previous studies have characterized the effect of catecholamines
on mobilization of NK cells. Schedlowski et al. (21, 22)
reported that catecholamines modulate human NK cell circulation and
function by -adrenergic mechanisms. They showed that NK cell numbers
in PBMC were increased 6 times by epinephrine infusion and 1.3 times by
norepinephrine infusion. Although the increased serum catecholamines
during exercise seem to be mainly derived from the adrenal medulla, the
lymphoid organs such as spleen that contain NK cells are heavily
innervated by the sympathetic nerves, and the neural norepinephrine may
also affect NK cells in these organs, as described by Benschop et al.
(3).
Benschop et al. (1, 2) showed that epinephrine and norepinephrine cause detachment of NK cells from cultured endothelium and might induce recruitment of NK cells from the marginating pool to the circulation. Our present observations that norepinephrine downmodulates CD44 on NK cells and inhibits NK cell binding to hyaluronic acid appear to be relevant to the detachment of NK cells from endothelium. Thus it is likely that the catecholamine-induced mobilization of NK cells during exercise is primarily caused by the downmodulation of adhesion molecules on NK cells.
The downmodulation of adhesion molecules by catecholamines appears to
be a unique feature of NK cells. The expression of CD44, CD62L, and
CD18 on CD3+CD56 T cells did not change
during and after exercise or by in vitro stimulation with
norepinephrine (data not shown). This is consistent with the previous
report that the change in T cell numbers is less than that of NK cells
during exercise (8, 22). This appears to result from
higher expression of -adrenergic receptors on NK cells than on T
cells (27).
Our present study suggests that the mobilization of NK cells during exercise is caused by downmodulation of NK cell surface adhesion molecules by catecholamines. In contrast to mobilization of NK cells during exercise, circulating NK cells rapidly decreased below the resting level after the exercise (Fig. 1). This decrease of NK cells might be associated with upregulation of CD44 and CD62L expression on NK cells, although the change was not statistically significant in the present study because of large individual differences. Further studies are needed to explain the decrease of circulating NK cells after exercise.
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ACKNOWLEDGEMENTS |
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The authors thank Dr. T. Kodama and Dr. T. Tsukada for experimental assistance and Dr. T. Muto and Dr. H. Kimura for statistical analyses.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Okumura, Juntendo Univ. School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan (E-mail: kokumura{at}med.juntendo.ac.jp).
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. Section 1734 solely to indicate this fact.
Received 20 September 1999; accepted in final form 3 May 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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