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Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Sports Medicine & Doping Studies
Liu et al., J Sports Med Doping Stud 2012, 2:6
http://dx.doi.org/10.4172/2161-0673.1000119
Research Article Open Access
Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly
Women
Jing Liu1,2*, Peijie Chen3, Ru Wang3, Yonghong Yuan4, and Chunying Li5*
1Department of Martial Arts, Shanghai University of Sport, Shanghai 200438, China
2Department of Psychology, School of Kinesiology, University of Michigan, Ann Arbor, MI, 48109, USA
3Department of Sports Medicine, Shanghai University of Sport, Shanghai 200438, China
4Department of Sports Leisure, Shanghai University of Sport, Shanghai 200438, China
5Department of Biochemistry & Molecular Biology, Wayne State University School of Medicine, Detroit, Michigan 48201, USA
Abstract
Objective: The purpose of this study was to investigate the effect of Tai Chi (TC) exercise on immune functions
among middle-aged and elderly women, and to evaluate the relationship between immune modulation of Natural Killer
T (NKT) cells and Dendritic Cells (DCs) and T Helper (Th) 1 /Th2 immune response.
Methods: Sixty healthy middle-aged and elderly women were randomly assigned into 2 groups: Tai Chi (TC)
group (n=30) and control (CON) group (n=30). Subjects in TC group participated in TC exercise for 6 months, 60
minutes a day, four times a week. Meanwhile, subjects in CON group maintained their normal physical activity levels
during the whole study period. Peripheral blood samples were collected right before, and after 4 and 6 months of the
exercise program, and the sampled were analyzed within 24 hours after collection.
Results: After the 6-month TC exercise program, the percentage of CD4+ T lymphocytes, the CD4+:CD8+ ratio,
and the percentage of NK and NKT cells in TC group signicantly increased (p<0.05). The percentage of interferon-γ
(IFN-γ) producing T cells increased signicantly after 4 months (p<0.01) and 6 months (p<0.05) of exercise. The
percentage of interleukin-4 (IL-4) producing T lymphocytes also demonstrated an increase after 4 months (p<0.05)
and 6 months (p>0.05) of exercise. The percentage of CD123+ DCs and CD11c+ DCs also signicantly increased after
the 6-month program (p<0.01), with the percentage of CD11c+ cells increasing much more dramatically than CD123+
DCs. However, the CON group did not show any signicant changes in these parameters.
Conclusion: Regular TC exercise favors the development of Th1 immune responses in middle-aged and elderly
women. TC-induced changes in Th1 and Th2 immune responses are associated with the immune modulation of NKT
cells and DCs and their reciprocal interactions.
*Corresponding authors: Jing Liu, Ph.D., Department of Martial Arts, Shanghai
University of Sport, 588 Qing Yuan Huan Road, Shanghai 200438, China, E-mail:
liujing_j3@163.com
Chunying Li, Ph.D., Department of Biochemistry & Molecular Biology, Wayne State
University School of Medicine, 540 E. Caneld, 5312 Scott, Detroit, MI 48201,
USA, Tel: (313) 577-4182; Fax: (313) 577-2765; E-mail: cl@med.wayne.edu,
cl@med.wayne.edu
Received September 27, 2012; Accepted November 09, 2012; Published
November 11, 2012
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on
Immune Function in Middle-aged and Elderly Women. J Sports Med Doping Stud
2:119. doi:10.4172/2161-0673.1000119
Copyright: © 2012 Liu J, et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and
source are credited.
Keywords: Physical activity; Immunology; Immunosenescence;
Aging; Female
Introduction
Immunosenescence is the steady degeneration of the immune
system that occurs with age in humans and animals [1]. Multiple
aspects of the immune response are severely disregulated by aging,
among which the T cell immune response is the most dramatically
aected. T cell-mediated production of cytokines Interleukin (IL)-2
and Interferon (IFN)-γ decreases signicantly with age. e amount of
IFN-γ decreases along with the activity of T Helper 1 (1) cells and the
amount of IL-4 and IL-10 increases along with the activity of T Helper
2 (2) cells [2,3], resulting in a decreasing ratio of 1/2 in elderly
people. e decrease in the numbers of Natural Killer (NK) cells and
Natural Killer T (NKT) cells contributes to the deleterious immune
response in the elderly, and the number of myeloid Dendritic Cells
(DCs) also progressively declines with age [4].
Aging is also associated with decreased physical activity. Exercise
can profoundly inuence health, and there is mounting evidence that
the mechanisms behind these eects are related, in part, to the impact
of exercise on immune function [5]. It has been shown that the numbers
of circulating T cells and their functions are inuenced by brief periods
of exercise [6,7]. Hinton et al. [8] reported signicant changes in the
composition of the total lymphocyte cultures immediately post-
exercise: increased numbers of CD56+ NK cells and CD8+ T cells
and decreased numbers of T-helper cells (CD4+), in male endurance-
trained runners aer an interval running session of 15×1-min intervals
at 95% VO2 max. A decrease in mitogen-stimulated T cell proliferation
and T cell production of IL-2 and IFN-γ was reported immediately
aer acute, intensive exercise [9]. In fact, the volume of exercise has
been shown to be a critical element in inducing a positive or negative
eect on the immune response [5,10]. It has been shown that moderate
exercise enhances T cell function and decreases respiratory infections
[11]. Although many components of the immune system are known to
exhibit various changes depending on the stage and type of exercise, the
long-term eects of regular moderate exercise on immune responses
remain incompletely understood.
Tai Chi (TC) is a traditional Chinese martial art with a long history.
It usually consists of TC Chuan and TC Weapon (for example, TC
Sword, TC Spear, TC Broa dsword). TC has gained popularity in
Western countries in recent years for its recognized positive eects on
health in the elderly [12]. TC incorporates slow-moving, gentle physical
activity, balance, and weight shiing, with meditation, relaxation, deep
Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly Women. J Sports
Med Doping Stud 2:119. doi:10.4172/2161-0673.1000119
Page 2 of 7
breathing, and imagination. Reported benets of TC include increased
balance and decreased incidence of falls, increased strength and
exibility, reduced pain and anxiety, improved self-ecacy, improved
sleep, and enhanced cardiopulmonary function [12]. TC has also been
shown to signicantly increase the ratio of CD4+ vs. CD8+, signicantly
increase CD4+/CD25+ regulatory T cell number [13] reduce the levels
of HbA1c in type II diabetes and enhance the 1 response [14] and
increase varicella-zoster virus specic cell-mediated immunity [15],
signicantly increased the numbers and activity of natural killer cells
in the peripheral blood [3]. To our knowledge, there haven’t been any
studies as to whether TC could promote the amelioration of the age-
induced 1/2 immune imbalance.
e purpose of this study was to investigate the eect of TC on the
subsets of T cells, NK cells, NKT cells and DCs, and the cytokines IFN-γ
and IL-4 producing T cells, in aged 50–65 women who had practiced TC
for six months. Our hypothesis was that TC induces a 1-type immune
response in elderly people, ameliorating the age-induced immune
imbalance. By evaluating the relationships between TC exercise and T
lymphocyte immune function, we sought to elucidate the role that TC
exercise plays in reversing the age-associated imunosenescence.
Materials and Methods
Subjects
Sixty women, aged 50–65, were recruited by advertising for the
study, and randomly divided into 2 groups: Tai Chi (TC) exercise
group (n=30) and non-exercise control (CON) group (n=30). Table
1 shows the physical characteristics of the study subjects, and both
groups were of similar age and body composition. Body mass and Body
Mass Index (BMI) did not demonstrate any signicant changes during
the whole study period in either TC group or CON group. Exclusion
criteria included angiocardiopathy (cardiopulmonary illness),
autoimmune disorder, metabolic disorder, malignancies actively being
treated with chemotherapy, hormone replacements (such as the use of
corticosteroids), and acute illness from infection, and major surgery
during the preceding 6 months. All subjects had no TC training
experience before. Written informed consent was obtained from all
participants upon enrollment, and the protocol was reviewed and
approved by the institutional review board of Shanghai University of
Sport. e subjects in the CON group were instructed not to participate
in any formal exercise but simply to maintain their normal levels of
physical activity as usual for the whole 6-month study period, and they
kept diaries to record their daily activities.
TC exercise program
All subjects in TC group participated in TC Chuan (24 forms;
CON group (N=30) TC group (N=30)
Pre Post Pre Post
Age (yr)
Body Weight (kg)
Height (cm)
BMI (kg/m2)
Body Fat (%)
55 ± 2.74
62.14 ± 12.77
165.28 ± 1.95
23.96 ± 0.87
28.82 ± 7.61
-
62.33 ± 11.86
165.42 ± 1.87
23.34 ± 0.93
28.72 ± 6.34
54 ± 3.54
64.41 ± 10.09
164.33 ± 2.09
24.19 ± 0.79
29.07 ± 6.33
-
63.93 ± 11.26
164.97 ± 1.77
23.99 ± 0.68
29.02 ± 5.69
Table 1: Characteristics of all subjects in both CON and TC groups before and after
6 months of TC exercise training. CON group: control group; TC group: Tai Chi
exercise group; Pre: pre-exercise program; Post: 6-month after exercise program;
BMI: body mass index.
Figure 1: Comparison of the percentages of T lymphocyte CD3+ (A), and their subsets CD4+ (B) and CD8+ (C) in the peripheral blood, as well as CD4+/CD8+ ratio
(D) at the onset, 4 months and 6 months during the study period in control (CON) group and Tai Chi (TC) exercise group. Data are presented as Mean ± SEM.
P values were analyzed by Student’s paired t-test (n=3subjects per group). * p<0.05 as compared with onset of the same grou▲p;p<0.05 as compared with 4
months of the same group.
Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly Women. J Sports
Med Doping Stud 2:119. doi:10.4172/2161-0673.1000119
Page 3 of 7
Supplementary gure 1 for TC techniques) and TC Sword (42 forms)
exercise for 6 months, 4 sessions a week. ey were supervised and
instructed by an experienced TC teacher who has practiced TC for 18
years. Each TC session lasted 60 minutes consisting of a 10 minutes
warm up, a 40 minutes practice, and a 10 minutes cool down. e
subjects in TC group spent 3 months in learning and practicing all
forms of TC Chuan and TC Sword, and then continued to practice for
another 3 months. All TC subjects kept diaries to record details.
Blood sampling and analysis
Blood sampling: At the onset, 4-month, and 6-month during the
study period, peripheral venous blood (5 ml) of each subject in both
groups was collected in an anticoagulant heparin tube. Blood samples
were analyzed within 24 hours of collection. Blood was collected
between 7 am–9 am in the morning aer a 12 hours overnight fast (only
water was allowed). On the day of blood collection, subjects did not
carry out any TC exercise. All subjects refrained from any exercise for
at least 24 hours before the blood collection/sampling.
Analysis of T cell subset, NKT cells, and NK cells
Flow cytometric analysis for T cells: Peripheral blood (100 l) was
incubated with anti-human CD4-uorescein isothiocyanate (FITC),
anti-human CD8-phycoerythrin (PE), as well as anti-human CD3-
peridinin chlorophyll protein (PerCP)-Cy5 antibodies (Immunotech
Co.) in the dark for 15 minutes. en haemolysis xative agent (0.5
ml) (Beckman Coulter) was added for another 10 minutes, followed
by the addition of Isoton II diluent (0.5 ml) (Beckman Coulter). CD3+,
CD4+, and CD8+ cells were measured using uorescence detection by
ow cytometry.
Flow aytometric analysis for NK/NKT cells: Peripheral blood (100
µl) was stained with anti-human CD3-FITC, anti-human CD16-PE,
and anti-human CD56-PE antibodies (Beckman Coulter, California,
USA). Aer staining, red blood cells were lysed with OptiLyse C
Lysing Solution (Beckman Coulter). Finally, cells were analyzed using
a Coulter EPICS XL Flow Cytometer (Beckman Coulter) with System
IITM soware. NK cells were dened as CD3–CD16+CD56+ cells, and
NKT as CD3+CD16+CD56+ cells [16].
Analysis of IFN-γ and IL-4 producing CD3+CD4+ T cells
Ten µl of PMA (1 µg/ml), 8 µl of ionomycin (50 µg/ml) and 6.8
µl of monensin uid (0.1 mg/ml; Sigma Chemical Co.) were added
to peripheral blood (200 µl) along with RPMI-1640 media (200
µl), and incubated for 4 to 6 hours at 37°C in a 5% CO2 incubator.
Monoclonal anti-CD3-PerCP (20 µl) and anti-CD4-FITC antibodies
(20 µl; Beckman Coulter) were then added and the mixture was
incubated for another 15 minutes. Aer the incubation, cell suspension
of each sample was divided into three 100-l aliquots, and all samples
were treated with xation/permeabilization reagents according to the
manufacturer’s instructions (Beckman Coulter). Intracellular cytokines
in each aliquot were stained using PE-conjugated mAbs against IL-4,
IFN-γ, or an isotype control (Beckman Coulter) for 30 minutes. e
samples were washed with PBS and the supernatant was discarded. e
cell pellet was resuspended in PBS and analyzed by ow cytometry. All
incubations (except PMA-activation and incubation) were performed
at room temperature in the dark.
Analysis of CD123+ and CD11c+ dendritic cells by direct
immunouorescence staining of whole blood
Monoclonal antibodies: PE-conjugated anti–IL-3 receptor α chain
(CD123), PE-conjugated anti-CD11c, PerCP-conjugated anti–HLA-
DR, and FITC-conjugated lineage cocktail 1 (lin 1), as well as PE- and
PerCP-conjugated isotype control murine mAbs were obtained from BD
(San Jose, CA). e lin 1 contains monoclonal antibody clones against
CD3 (T cells), CD14 (monocytes/macrophages), CD16 (natural killer
cells), CD19 (B cells), CD20 (B cells), and CD56 (natural killer cells).
Sensitive detection of DCs was achieved by exclusion of cells positive
for CD3, CD14, CD16, CD19, CD20, or CD56 using Lineage Cocktail 1
(FITC-conjugated Ab mixture against CD3, CD14, CD16, CD19, CD20,
and CD56). ereaer, myeloid and lymphoid DCs (DC1s and DC2s,
respectively) were detected using PE-conjugated Ab against CD11c and
CD123, respectively.
Flow cytometric analysis: Peripheral blood cells obtained from
the subjects were analyzed by three-color ow cytometry. To minimize
selective cell loss during the preparation procedure, the cells were rst
stained with mAbs followed by lysing the erythrocytes. Briey, aliquots
(100 µl) of peripheral blood were incubated with a mixture of anti-
lin mAbs (BD Biosciences), a PerCP-conjugated anti-HLA-DR mAb,
and either a PE-conjugated anti-CD11c mAb to detect myeloid DC
or a PE-conjugated anti-CD123 mAb to detect plasmacytoid DC, or
a PE-conjugated isotype control (BD Biosciences) in the dark at room
temperature for 15 min (Supplementary table 1). en 2 ml of FACS
lysing solution (BD) was added, vortexed, and incubated for 10 minutes
to lyse the erythrocytes. e mixture was centrifuged at 300×g for 5
minutes, and the supernatant was discarded. e mixture was then
vortexed gently with 1 ml of wash buer, centrifuged again as described
above, and the supernatant was discarded. ereaer, the mixture
was vortexed and resuspended in 300 µl of 1% paraformaldehyde
for 10 min, and then washed and analyzed on a ow cytometer.
Identical ow cytometric settings were used for the acquisition of all
samples enabling the expression of cell surface molecules on dierent
samples to be directly compared. All incubations were performed at
room temperature in the dark. DCs were dened as the cells positive
for PerCP-conjugated anti-HLA-DR mAb and negative for FITC-
conjugated lin 1. Anti-CD11c or anti-CD123 mAb conjugated with PE
was used for further identication of the mDC and pDC subsets.
Statistical analysis
All data were expressed as means ± SEMs, and p<0.05 was set as
the criterion for signicance. e Statistical Package for Social Sciences
(SPSS Inc, USA; version 12.0) was used for statistical analysis. Data
were analyzed using one-way Analysis Of Variance (ANOVA), and the
independent samples t-tests were applied to assess dierences between
control group and TC group before exercise program. Paired-samples
t-tests were only used to assess dierences of variables between pre-
exercise and 4-month, as well as between pre-exercise and 6-month.
Results
Eect of TC exercise on T lymphocytes and their subsets
As shown in Figure 1, the percentages of T lymphocytes (CD3+) and
their subsets (CD4+ and CD8+) in the peripheral blood before exercise
program (at onset) did not show any signicant inter-group dierences
between CON and TC groups. Six-month TC exercise program
signicantly increased the percentage of CD4+ T () lymphocytes and
the CD4+:CD8+ ratio (p<0.05; Figures 1B and 1D), while no signicant
change in the percentages of CD3+ or CD8+ T cells was observed
(Figures 1A and 1C). Within the TC exercise group, the dierence
was signicant in the CD4+:CD8+ ratio at 6-month of TC exercise
compared with the ratio at the onset (p<0.05; Figure 1D). ere was
also a signicant dierence in the percentage of CD4+ T lymphocytes at
Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly Women. J Sports
Med Doping Stud 2:119. doi:10.4172/2161-0673.1000119
Page 4 of 7
6-month compared with at 4-month of TC exercise (p<0.05; Figure 1B).
However, the percentages of T lymphocytes (CD3+) and their subsets
(CD4+ and CD8+) in CON group did not demonstrate any changes
during the whole study period (onset; 4 months; and 6 months).
Eect of TC exercise on NK and NKT cells
Figure 2 shows the changes in the percentages of NK cells and
NKT cells in the peripheral blood in both CON and TC groups. e
percentages of NK cells and NKT cells before exercise program (at
onset) did not show any inter-group dierences between CON and
TC groups. Following TC exercise program, the percentages of both
NK and NKT cells signicantly increased at 4 months compared with
at the onset (p<0.05; Figures 2A and 2B). At 6 months of TC exercise
program, the percentages of both NK and NKT cell decreased slightly
compared with at 4-month, but the percentage of NKT cells at 6-month
was still signicantly higher than at the onset (p<0.05; Figure 2B).
e percentages of NK cells and NKT cells in CON group did not
demonstrate any signicant changes during the whole study period
(onset; 4 months; and 6 months).
Eect of TC exercise on cytokines IL-4 and IFN-γ producing
CD4+ T cells
Figure 3 shows the changes in the percentages of IFN-γ producing
CD4+ T cells (1) and IL-4 producing CD4+ T cells (2) in both CON
and TC groups. e percentages of both IFN-γ and IL-4 producing
CD4+ T cells before exercise program (at onset) were not signicantly
dierent between CON and TC groups (Figure 3). However, TC exercise
program signicantly increased both IFN-γ and IL-4 producing CD4+
T cells (Figure 3). ere was signicant dierence in the proportion
of IFN-γ (p<0.01; Figure 3A) and IL-4 (p<0.05; Figure 3B) producing
T cells at 4-month of TC exercise compared with at the onset. IFN-γ
producing T cells also demonstrated a signicantly higher percentage
at 6-month than at the onset (p<0.05; Figure 3A). e percentages of
IFN-γ and IL-4 producing CD4+ T cells in CON group did not show
any signicant changes during the whole study period (onset; 4 months;
and 6 months).
Eect of TC exercise on CD123+ DCs and CD11c+ dendritic
cells
As shown in gure 4, the percentages of both CD123+
(plasmacytoid) DCs and CD11c+ (myeloid) DCs before TC exercise
program (at onset) were not signicantly dierent between CON and
TC groups. However, aer the 6 months of TC exercise program, the
percentage of both CD123+ (plasmacytoid) DCs and CD11c+ (myeloid)
DCs signicantly increased (Figure 4). ere was signicant increase
in the percentages of CD11c+ DCs (p<0.01; Figure 4 A) and CD123+
DCs (p<0.01; Figure 4B) at 6 months of TC exercise compared with
at the onset. ere was also signicant increase in the percentage of
CD11c+ DCs (p<0.01; Figure 4A) and CD123+ DCs (p<0.01; Figure 4B)
at 6-month compared with at 4-month of TC exercise. e number of
CD11c+ DCs (myeloid) (Figure 4A) increased much more dramatically
than that of CD123+ DCs (plasmacytoid) (Figure 4B). e percentages
of both CD123+ (plasmacytoid) DCs and CD11c+ (myeloid) DCs in
CON group did not show any changes during the study period (onset;
4 months; and 6 months).
Figure 2: Comparison of NK (A) and NKT (B) cell percentages in the
peripheral blood at the onset, 4 months and 6 months during the study
period in control (CON) group and Tai Chi (TC) exercise group. Data are
presented as Mean ± SEM. * p<0.05 as compared with onset of the
same group.
Figure 3: Comparison of the percentages of cytokines IFN-γ (A) and IL-4 (B)
producing CD4
+ T cells in the peripheral blood at the onset, 4 months and
6 months during the study period in control (CON) group and Tai Chi (TC)
exercise group. Data are presented as Mean ± SEM. * p<0.05, ** p<0.01 as
compared with onset of the same group.
Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly Women. J Sports
Med Doping Stud 2:119. doi:10.4172/2161-0673.1000119
Page 5 of 7
Discussion
e human immune system demonstrates degenerative changes
with advancing age [17], especially T cells which demonstrate
prominent age-related alterations in distribution and function, such as
declined number of circulating cells, NKT cells, and DCs, decreased
production of 1 cytokines (IFN-γ) and increased production of
2 cytokines (IL-4) with aging [2,4,3]. However, the ndings of our
present study demonstrated that aer a 6-month TC exercise program,
the percentages of CD4+ T lymphocytes, NK cells, NKT cells, and
DCs, along with the CD4+:CD8+ ratio and cytokines IFN-γ and IL-4
producing T cells, signicantly increased in middle-aged and elderly
women.
Many studies have reported exercise-induced changes in the
immune function [5]. Changes in exercise-induced immune functions
are associated with the exercise type, intensity, and the duration of both
the exercise and any intermissions [5]. It was observed that the number
of CD4+ T cells decreased while the number of CD8+ T cells signicantly
increased, resulting in a decreased CD4+:CD8+ ratio, in seven middle-
and long-distance runners undergoing four-week intensive training aer
36 hours of rest [18]. Aer a bout of strenuous and prolonged exercise
(>1.5 h), the number of circulating T lymphocytes decreased below pre-
exercise levels for several hours aer exercise, with a decreased CD4+/
CD8+ ratio [19]. Excessive training can cause signicant drop in NK
cell number, leading to immune suppression [20]. However, our present
work and some previously published studies showed that moderate
physical exercise improved immune function [21,22]. A 6-month
supervised exercise training program led to nominal increases in some
aspects of immune function in previously sedentary elderly [22]. While
others reported that NK cell activity increased by 33% aer moderate
intensity training for 16 weeks in the elderly population [23], and
increased by 57% in a group of middle-aged women aer six weeks of
moderate intensity exercise training (60% VO2 max) [24]. Yeh et al. [14]
reported that aer 12 weeks of TC exercise, transcription factor T-bet
as well as expression of 1/2/T regulatory (Treg) cells signicantly
increased in type 2 diabetes patients. So far, there have been no studies
reporting changes in the age-induced 1/2 immune imbalance aer
regular long-term Tai Chi exercise. e results of our present study
demonstrated for the rst time that regular TC exercise appears to favor
improvement of 1 immune responses in middle-aged and elderly
women and the percentage of NKT cells and CD11c+ DCs signicantly
increased aer 6-month regular TC exercise as compared to the control
group.
1 cytokines, of which IFN-γ is typical, support cell-mediated
inammatory reactions by activating cytotoxic and inammatory
functions; while 2 cytokines, of which IL-4 is typical, support
humoral immune responses [25]. 1 and 2 cytokines are mutually
inhibitory for the dierentiation and eector functions of the reciprocal
phenotype [26]. IFN-γ selectively inhibits proliferation of 2 cells, and
IL-4 and IL-10 inhibit cytokine synthesis by 1 cells [26]. A number of
studies have shown that physical exercise aects 1 and 2 immune
responses as well as the balance between these responses. Excessive
or exhaustive exercise has been reported to induce exercise-related
immunosuppression via altering the 1/2 balance by decreasing the
percentage of circulating 1 lymphocytes, with increase or no change
in 2 cells; and also by decreasing IFN-γ production and increasing
IL-4 production resulting in a decreased IFN-γ/IL-4 ratio [6,27-29].
However, 2-month endurance training of moderate intensity promoted
IFN-γ production in moderately trained athletes [30], and 6 months
of moderate combined (endurance and resistance) training increased
spontaneously CD28 expressing cells and mitogen-stimulated
IFN-γ producing 1 cells in elderly subjects [31]. Consistent with
these ndings, our present study showed that aer 6-month regular
TC exercise, the percentages of IL-4 and IFN-γ producing T cells
signicantly increased, and IFN-γ producing T cells were up-modulated
more dramatically than IL-4 producing T cells. ese results suggest
that long-term TC exercise can up-regulate cell-mediated immune
responses and promote the switch of the focus of the immune system
from humoral immunity to cell immunity, resulting in a higher 1-
type immune response (1 dominance) and therefore enhancing anti-
viral function. However, the mechanism by which TC modulates the
immune responses and the 1/2 balance remains unclear.
CD1d-restricted NKT cells expressing both invariant T-cell
receptors and NK cell receptors are an important immunoregulatory
subset of T lymphocytes, and they play an important role not only in
immune defense and surveillance, but also in regulating the immune
balance [16]. Activated NKT cells are involved in immune dierentiation
of 1 and 2 cells, and in the switch of the immune response in the
opposite direction, i.e., towards a 1-type response [16]. Most recently,
we investigated the relationship between NKT cells and the 1/2
lymphocyte imbalance aer overtraining and excessive exercise, and
showed that -galactosylceramide played an important modulatory
role in the exercise-induced 1/2 lymphocyte imbalance, which
may correlate with NKT immunoregulatory cells [32]. It was reported
that not only the NKT cell function depends on stimulation and the
microenvironment in the initial stages of the immune response, but
also the NKT activation signal is transmitted by the specic type of
APCs, such as DCs [33].
DCs are the most important and potent APCs, priming the primary
Figure 4: Comparison of the percentages of CD11c+ (A) dendritic cells
(DCs) and CD123+ (B) DCs in the peripheral blood at the onset, 4 months
and 6 months during the study period in control (CON) group and Tai
Chi (TC) exercise group. Data are presented as Mean ± SEM. ** p<0.01
as compared with onset of the same group; ▲▲ p<0.01 as compared with
4 months.
Volume 2 • Issue 6 • 1000119
J Sports Med Doping Stud
ISSN: 2161-0673 JSMDS, an open access journal
Citation: Liu J, Chen P, Wang R, Yuan Y, Li C (2012) Effect of Tai Chi Exercise on Immune Function in Middle-aged and Elderly Women. J Sports
Med Doping Stud 2:119. doi:10.4172/2161-0673.1000119
Page 6 of 7
immune response [34]. Two distinct DC subsets, myeloid DCs (mDC,
also called Type 1 DCs, DC1), and plasmacytoid DCs (pDC, also
called Type 2 DCs, DC2) that may produce dierent outcomes aer
their interaction with T lymphocytes, have been identied in humans
[34,35], DC1 (identied as CD11c+CD123–) subsets induce 1 cell
dierentiation by the secretion of IL-12. DC2 (identied as CD11c–
CD123+) subsets secrete mainly IL-10, which induces initial T cells to
dierentiate into 2 cells, resulting in immune tolerance. On the basis
of these distinct properties of the DC subtypes, mDCs and pDCs are
considered to be specialized APCs inducing a 1 and 2 response,
respectively. Exercise has been reported to induce a signicant
increase in DC numbers and modulate myeloid DC dierentiation
and maturation in rats [36,37]. e ndings of our present study
demonstrated that TC exercise promotes CD11c+ DCs and CD123+
DCs, with the change in CD11c+ DCs being more dramatic, suggesting
that TC exercise facilitates the induction of 1 cell dierentiation.
As the most powerful APCs, DCs can activate resting NKT cells
in vivo, present antigen peptide and provide a co-stimulus signal for
NKT cell sensitization, activation and amplication [38]. It was shown
that DCs produce high levels of co-stimulus molecules to activate T
cells, aer combining DCs and T cells to mediate the 1 response
by secreting large amounts of IL-12, helping to eliminate tumors
[39]. Others reported that exogenous or endogenous IL-12 induces a
progressive decrease in the number of liver NKT cells producing IL-
4, thus supporting the development of 1 immune responses [38].
However, immature DCs do not induce cell dierentiation, and
IFN-γ mainly induces immature DC dierentiation to DC1 cells.
e increased percentage of NKT cells enhanced IFN-γ secretion,
promoting DC1 production and possibly favoring the development of
1 immune responses. erefore, NKT cells and DCs demonstrate
reciprocal interactions and cooperatively regulate immune
dierentiation. Our results suggested that TC-induced changes in the
1 and 2 immune responses were related to immune modulation of
NKT cells and DCs, and their reciprocal interactions with each other.
In conclusion, our present study has shown that a six-month
regular TC exercise program signicantly improved immune function
in middle-aged and elderly women. e CD4+:CD8+ ratio showed a
signicant increase, and the percentages of NKT cells, CD11c+ DCs and
CD123+ DCs, as well as the percentages of cytokine IFN-γ producing
T cells were also signicantly increased. e percentage of CD11c+ DC
was increased more dramatically than that of CD123+ DC. We conclude
that regular TC exercise can improve age-associated immune imbalance
and promote the development of 1 immune responses, and these
changes may be related to the immune modulation of NKT cells and
DCs and their reciprocal interactions with each other. erefore,
regular TC exercise has benecial eects of reversing the age-associated
immunosenescence in middle-aged and elderly people.
Acknowledgements
The authors thank Dr. Lai Wei (National Eye Institute, and National Center
for Complementary and Alternative Medicine, National Institutes of Health, USA)
for critically reading the manuscript. This study was supported by grants from
the Shanghai Pujiang Program, the Shanghai Natural Science Foundation (No.
07ZR14103) and the Shanghai Leading Academic Discipline Project (No. T0902).
Appreciation is also extended to all participating staff and subjects, whose
cooperation made this study possible.
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