Corticosterone administration induces oxidative injury in skeletal muscle of broiler chickens

Corticosterone administration induces oxidative injury in skeletal muscle of broiler chickens H. Lin,1 J. Gao, Z. G. Song, and H. C. Jiao Lab of Animal Econutrition, Department of Animal Science, Shandong Agricultural University, Taian, Shandong 271018, P. R. China by CORT administration. The preslaughter level of TBARS could be increased by CORT administration in pectoralis major. In contrast, although the preslaughter level of TBARS was not significantly changed by CORT administration in BF, the augmented TBARS level was detected at 48 h postmortem in BF of CORT chickens. During the period of storage, the concentrations of TBARS increased, whereas ferric reducing-antioxidant power level decreased over time regardless of treatment. In conclusion, the data suggest that elevated CORT due to preslaughter stress would affect the redox balance in skeletal muscle. The result suggested that the oxidative stability during storage of meat is associated with the alteration in muscle physiology induced by CORT administration.

Key words: stress, corticosterone, lipid peroxidation, meat quality, broiler 2009 Poultry Science 88:1044–1051 doi:10.3382/ps.2008-00312

INTRODUCTION Preslaughter stressors such as heat stress, feed withdrawal, catching, crating, transport, and stunning may cause undesirable changes in meat quality (Ali et al., 1999; Sams, 1999). For example, preslaughter heat stress could accelerate rigor mortis development, reduce water-holding capacity, and increase paleness of breast meat (Northcutt et al., 1994; McKee and Sams, 1997). Previous studies have shown that broiler chickens subjected to preslaughter stress had increased plasma concentrations of corticosterone (CORT, Kannan et al., 1997, 1998; Nijdam et al., 2006; Bedanova et al., 2007), and such an upregulation of CORT can cause a deterioration of meat quality (Gao et al., 2008). Therefore, the physiological status of the individual animal and, as a result, the muscle cells, at the moment of slaughter,

©2009 Poultry Science Association Inc. Received July 31, 2008. Accepted January 12, 2009. 1 Corresponding author: [email protected]

may play a role in the process of rigor mortis and, in turn, have an effect on meat quality. The redox balance is gently maintained by the enzymatic and nonenzymatic systems in organisms. Heat stress could induce augmented lipid peroxidation in either broiler or laying hens (Lin et al., 2006, 2008). Mujahid et al. (2005, 2006) reported that superoxide anion production was enhanced in the skeletal muscle mitochondria of meat-type chickens in response to acute heat stress. Similar to mammals, the upregulated circulating glucocorticoids have been proved to be involved in the induction of oxidative stress (Lin et al., 2004a,b). The drip loss, lipid peroxidation, and warmed-over flavor development in broiler meat were decreased by dietary supplementation of antioxidant such as α-tocopherol (O’Neill et al., 1998; Goñi et al., 2007). Moreover, the lipid peroxidation in homogenized, cooked, and stored samples of pectoralis major (PM) and iliotibialis of stressed broilers (transport and shackling) was decreased by the supplementation of ascorbic acid and α-tocopherol (Young et al., 2003b). Hence, we hypothesize that the oxidative stress induced by pre-

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ABSTRACT The present study had been conducted to explore the effect of corticosterone (CORT) on the induction of lipid peroxidation in skeletal muscle. The experimental chickens were subjected to 1 single s.c. injection of CORT (4 mg/kg of BW). Blood samples were obtained at the beginning and end of a 3-h experimental period. Muscle samples were obtained from musculus pectoralis major and musculus biceps femoris (BF) before and immediately after slaughter, and at 24- and 48-h time points postmortem. The result showed that plasma level of TBA reacting substances (TBARS) was significantly increased, whereas the activity of superoxide dismutase was decreased after CORT injection. Plasma level of total antioxidant power, as reflected by the ferric reducing-antioxidant power, was increased

CORTICOSTERONE INDUCES OXIDATIVE INJURY IN SKELETAL MUSCLE

slaughter stress may contribute to the altered oxidative stability in skeletal muscles. In the present study, 3 experiments had been conducted to explore the effect of CORT on the induction of oxidative injury in skeletal muscle. The objective of the present study was to determine the effect of 1 single administration of CORT on lipid peroxidation in breast and thigh meat of broiler chickens. The effect of CORT during the exsanguination process was estimated by the difference between the muscle biopsies and corresponding muscle samples obtained immediately after slaughter (Lin et al., 2007).

MATERIALS AND METHODS Broiler chicks (Arbor Acres) were obtained from a local hatchery (Taiyu Broiler Company, Taian, Shandong, China) at 1 d of age and reared in an environmentally controlled room. The brooding temperature was maintained at 35°C for the first 2 d and then decreased gradually to 21°C (45% RH) until 28 d and thereafter maintained as such to the end of the experiment. In experiment 1, the broilers received a commercial starter diet (12.10 MJ of ME/kg and 22.2% CP) until 7 d of age, after which a commercial grower diet (12.68 MJ/kg, 21.4% CP) was provided until the end of the experiment. In experiment 2 and 3, all chicks received a starter diet with 21.5% CP and 3,000 kcal of ME/kg from d 1 to 21 and were fed with a grower diet with 19.5% CP and 3,100 kcal of ME/kg after d 21. Feed and water were supplied ad libitum, and continuous light was provided during the entire rearing period. The present study was approved by the university and was carried out in accordance with the Guidelines for Experimental Animal of Ministry of Science and Technology, Beijing, China.

Experiment Design In experiment 1, at 40 d of age, 2 groups of 6 broiler chickens of both sexes with similar BW were used and injected s.c. with CORT (4 mg/kg of BW, dissolved in 0.5 mL of corn oil, Lin et al., 2004b) or 0.5 mL of corn oil (sham control group), respectively. The effect of CORT administration on plasma parameters was investigated. The concentrations of plasma glucose, urate, and CORT and the activities of creatine kinase (CK) were measured to evaluate the effect of stress responses. The redox status of chickens was determined by the measurement of plasma concentrations of TBA reacting substances (TBARS) and ferric reducing-antioxidant power (FRAP). In experiment 2, twenty-four chickens of both sexes with similar BW were selected. The chickens were assigned to 2 groups of 12 chickens (6 males and 6 females) and were randomly subjected to 1 of the 2 treatments (CORT and control) as that in experiment

1. Food was withdrawn before the experiment began and water was kept available during the whole experimental period. The effect of CORT administration on the redox status was investigated. The concentrations of TBARS and FRAP in plasma and skeletal muscles were determined. Experiment 3 was conducted to further clarify the effect of CORT on the redox status in plasma and muscle. The experiment chickens were subjected to the same treatments as that of experiment 2 except that more plasma parameters were included and muscle sampling time range was expanded. The plasma activities of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) as well as the concentrations of TBARS and FRAP were measured. Muscle levels of TBARS and FRAP were determined up to 48-h postmortem.

Sampling In all 3 experiments, a blood sample was respectively obtained before and at 3 h after CORT administration from a wing vein of each chicken by using a heparinized syringe and was collected in iced tubes. Plasma was obtained after centrifugation at 400 × g for 10 min at 4°C and was stored at −20°C for further analysis. In experiment 2 and 3, all of the chickens were killed by exsanguination immediately after the muscle biopsies were obtained from the left musculus PM and musculus biceps femoris (BF) muscles of all the chickens according to the description of Quentin et al. (2003). Immediately postmortem (0 h), a 3- to 4-g muscle sample was respectively obtained from right PM and BF muscles and immediately cooled down in liquid nitrogen and stored at −80°C for further analysis. The eviscerated carcasses were chilled overnight (24 h) in a cold cell at 4°C. Meat samples were obtained again at 24 h postmortem in experiment 2 and at 24 and 48 h postmortem, respectively, in experiment 3 for further analysis of meat quality characteristics. After each sampling, skin was kept to fully cover the site of cutting and the next sample was cut again at 10 mm apart from the previous sample area.

Measurement The concentrations of plasma glucose, urate, and the activities of CK, SOD, and GSH-Px were measured by commercial diagnostic kits (Jiancheng Bioengineering Institute, Nanjing, China), which have been successfully used in poultry study (Zhang et al., 2007). Plasma lipid peroxidation was estimated by spectrophotometric determination of TBARS and was expressed as nanomoles of malondialdehyde per milliliter of plasma (Lin et al., 2004b). The FRAP was determined to estimate the total plasma antioxidant activity as described by Benzie and Strain (1996, 1999). The measurement was conducted at room temperature and a 5-min time window was used.

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Experimental Chickens and Diets

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Lin et al. Table 1. Effect of s.c. administration of corticosterone (4 mg/kg of body mass) on plasma metabolite and redox parameters of broiler chickens in experiment 11 Item2

Control

16.9 ± 7.9y 374.5 ± 40.2a,x

12.8 ± 4.9 13.9 ± 2.5b

4,370 ± 1,024 5,255 ± 1,066

6,315 ± 1,551 6,598 ± 1,864

238 ± 5y 274 ± 8a,x

240 ± 6x 216 ± 7b,y

3.6 ± 0.3y 10.3 ± 0.8a,x

4.2 ± 0.4 4.6 ± 1.1b

0.74 ± 0.06 0.62 ± 0.10

0.56 ± 0.05 0.59 ± 0.08

0.90 ± 0.03y 1.91 ± 0.11a,x

1.04 ± 0.08 1.02 ± 0.13b

Probabilities Treatment (Treat): <0.0001 Time: <0.0001 Treat × time: <0.0001 Treat: NS Time: <0.0001 Treat × time: 0.0070 Treat: 0.0042 Time: NS Treat × time: <0.0001 Treat: 0.0014 Time: 0.0004 Treat × time: 0.0011 Treat: NS Time: NS Treat × time: NS Treat: 0.0011 Time: 0.0010 Treat × time: 0.0009

a,b

Means with different superscripts within the same time point differ significantly (P < 0.05). Means with different superscripts within the same treatment differ significantly (P < 0.05). 1 Values are means ± SEM (n = 6). 2 CK = creatine kinase; FRAP = ferric reducing-antioxidant power; TBARS = TBA reacting substances; 0 h and 3 h = blood samples obtained immediately before and at 3 h after treatment, respectively. x,y

Corticosterone was only measured in experiment 1 by using a sensitive and highly specific RIA kit (IDS Inc., Boldon, UK), with a sensitivity of 0.39 ng/mL, and low cross-reaction with aldosterone (0.20%), cortisol (0.40%), and deoxycorticosterone (3.30%), which have been used in previous study (Malheiros et al., 2003). The intraassay variability was 3.8%. Before as-

say, plasma samples were heated at 80°C for 10 min to inactivate CORT-binding proteins. Tissue samples were homogenized in 9 volumes of 10 mM sodium phosphate buffer (pH 7.4) containing 1.15% potassium chloride. The concentrations of TBARS in skeletal muscle tissues were measured according to the description by Lin et al. (2004b). After

Table 2. Effect of corticosterone administration (4 mg/kg of body mass) on plasma concentrations of TBA reacting substances (TBARS) and ferric reducing-antioxidant power (FRAP) of broiler chickens in experiment 2 and experiment 31 Corticosterone Item2 Experiment 2   TBARS, nmol/mL   FRAP, mmol/L Experiment 3   TBARS, nmol/mL   FRAP, mmol/L   SOD, U/mL   GSH-Px, U/mL

Source of variation   Experiment 2    Corticosterone    Time    Corticosterone × time   Experiment 3    Corticosterone    Time    Corticosterone × time a,b

Control

0h 1.80 ± 0.15y 1.08 ± 0.03y 0.79 0.98 98.3 3,465

± ± ± ±

0.11y 0.09y 13.3x 190x

TBARS

3h

0h

3.98 ± 0.37a,x 1.77 ± 0.12a,x

1.89 ± 0.18 1.10 ± 0.05x

1.39 1.76 83.6 2,732

± ± ± ±

0.17a,x 0.17a,x 16.9y 178y

0.66 0.87 115.2 3,387 Probabilities

± ± ± ±

0.09 0.04x 14.5 173x

3h 1.40 ± 0.21b 0.91 ± 0.04b,y 0.81 0.70 114.5 2,838

± ± ± ±

0.13b 0.05b,y 13.8 174y

FRAP

SOD

GSH-Px

0.0003 0.0017 <0.0001

NS <0.0001 <0.0001

— — —

— — —

0.0294 0.0010 0.0342

0.0001 <0.0001 <0.0001

NS NS NS

NS <0.0001 0.0068

Means with different superscripts within the same time point differ significantly (P < 0.05). Means with different superscripts within the same treatment differ significantly (P < 0.05). 1 Values are means ± SEM (n = 12). 2 GSH-Px = glutathionine peroxidase; SOD = superoxide dismutase; 0 h and 3 h = blood samples obtained immediately before and at 3 h after treatment, respectively. x,y

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Corticosterone, ng/mL  0 h  3 h CK, IU/L  0 h  3 h Glucose, mg/dL  0 h  3 h Urate, mg/dL  0 h  3 h TBARS, nmol/mL  0 h  3 h FRAP, mmol/L  0 h  3 h

Corticosterone

CORTICOSTERONE INDUCES OXIDATIVE INJURY IN SKELETAL MUSCLE

the homogenates were centrifuged (400 × g, for 10 min at 4°C), the supernatant was used for the measurement of FRAPS, with the same methods as for plasma. All samples in 1 experiment were run in the same assay to avoid interassay variability.

Statistical Analysis For the statistical analyses of all the plasma and tissue variables, the repeated measurement analysis (SAS Institute, 1998) was conducted to evaluate the main effects of CORT and time, as well as their interaction. The time effect within treatment was evaluated with post-hoc analysis (Tukey). Means were considered significantly different at P < 0.05.

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FRAP level decreased (P < 0.0001) with time regardless of treatment. Muscle concentrations of TBARS in BF were not significantly affected by CORT treatment (Figure 1A, Table 3). Regardless of treatment, TBARS level was increased along with time (P < 0.0001). In contrast, the level of FRAP in BF was significantly (P < 0.01) increased by CORT treatment at all the time points (Figure 1B, Table 3). Meanwhile, FRAP level signifi-

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RESULTS Experiment 1 At 3 h after CORT injection, plasma concentrations of CORT, glucose, urate, and FRAP were all significantly (P < 0.01) elevated in CORT chickens, compared with the basal levels (Table 1). In the control chickens, however, all the plasma parameters were not significantly (P > 0.05) changed compared with the basal levels, except that the concentration of plasma glucose was decreased with time (P < 0.05). There were significant interactions between treatment and time for glucose (P < 0.001), urate (P < 0.01), FRAP (P < 0.001), CORT (P < 0.0001), and CK (P < 0.01). At 3 h after CORT injection, plasma levels of CORT (P < 0.0001), glucose (P < 0.01), urate (P < 0.01), and FRAP (P < 0.01) in CORT chickens were significantly higher than that of control chickens.

Experiment 2 Corticosterone injection significantly (P < 0.05) increased BW loss compared with control chickens (control, 35.3 g, 1.50% initial BW vs. CORT, 72.6 g, 3.04% initial BW) during the 3-h experimental period. In CORT treatment, plasma concentrations of TBARS and FRAP were all significantly (P < 0.05) higher after 3 h, compared with either their initial basal levels or control chickens (Table 2). In contrast, the levels of FRAP decreased (P < 0.05) with time in control chickens, whereas there was a trend suggesting that TBARS decreased over time (P = 0.0988). The preslaughter level of TBARS in PM was higher (P < 0.01) in CORT chickens compared with control chickens. However, this phenomenon was not observed immediately after slaughter and at 24-h postmortem (Figure 1A, Table 3). Compared with control chickens, muscle content of FRAP was higher (P < 0.0001) in PM of CORT chickens immediately before or after slaughter and, however, no obvious difference could be detected at 24 h postmortem (Figure 1B). The concentrations of TBARS increased (P < 0.0001), whereas

Figure 1. Effect of corticosterone (CORT) administration (4 mg/ kg of body mass) on the levels of TBA reacting substances (TBARS, A) and ferric reducing-antioxidant power (FRAP, B) in musculus pectoralis major (PM) and biceps femoris (BF) of broilers in experiment 2. Values are means ± SEM (n = 12). Pre-slaughter = muscle biopsies obtained immediately before slaughter; 0 h and 24 h = muscle samples obtained immediately after slaughter and at 24 h postmortem, respectively. a,b, a′–c′, x,y, x′–z′Means with different superscript within the same treatment differ significantly (P < 0.05). †Means at the same time point in PM differ significantly between treatment (P < 0.05). ‡ Means at the same time point in BF differ significantly between treatment (P < 0.05).

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cantly (P < 0.01) decreased with time and the lowest value was observed at 24 h postmortem in both control and CORT groups.

Experiment 3

DISCUSSION Plasma concentration of CORT was only measured in experiment 1 and was significantly elevated to a pharmacological level at 3 h after CORT administration. The result indicated that a single s.c. injection of CORT (4 mg/kg of BW) could induce the hypercorticosterone status in CORT chickens, which was in line with a previous report (Lin et al., 2004b). The altered physiological responses of CORT chickens were characterized by the elevated plasma concentrations of glucose and urate. In the present study, the augmented plasma lipid peroxidation was observed in CORT chickens, indicating that acute upregulation of CORT could induce oxidative stress in broiler chickens. The induction of plasma lipid peroxidation seemed to be related to the adverse responses in nonenzymatic and enzymatic antioxidant systems. In our previous work, the enhanced lipid peroxidation was not detected in CORT-challenged chickens when plasma SOD activity was not affected (Lin et al., 2004b). In contrast, concurrently with the increased plasma concentrations of TBARS, plasma activity of SOD was significantly decreased and the GSH-Px was depressed to a more severe extent (CORT, 21.1% vs. control, 16.2%). The result may imply that short-term

Table 3. The probabilities of the effect of corticosterone administration (4 mg/kg of body mass) on the levels of TBA reacting substances (TBARS) and ferric reducing-antioxidant power (FRAP) in musculus pectoralis major (PM) and biceps femoris (BF) of broilers in experiment 2 and 3 Item Experiment 2   PM    TBARS, nmol/g of wet tissue    FRAP, μmol/g of wet tissue   BF    TBARS, nmol/g of wet tissue    FRAP, μmol/g of wet tissue Experiment 3   PM    TBARS, nmol/g of wet tissue    FRAP, μmol/g of wet tissue   BF    TBARS, nmol/g of wet tissue    FRAP, μmol/g of wet tissue 1

P > 0.05.

Corticosterone

Time

Corticosterone × time

NS1 <0.0001

<0.0001 <0.0001

0.0913 <0.0001

NS <0.0001

<0.0001 <0.0001

NS <0.0001

NS <0.0001

<0.0001 <0.0001

NS 0.0002

0.0968 0.0502

0.0006 0.0019

NS NS

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Compared with control chickens, 1 single CORT administration resulted in enhanced (P < 0.05) BW loss in CORT treatment (CORT, 58.7 g or 2.37% initial BW vs. control, 32.3 g or 1.26% initial BW). Plasma levels of TBARS and FRAP were all significantly (P < 0.05) increased in CORT chickens compared with the control group (P < 0.05, P < 0.0001) or their initial levels (P < 0.01, P < 0.0001; Table 2). The interaction of time and CORT was significant for either TBARS (P < 0.05) or FRAP (P < 0.0001). In control chickens, TBARS levels were not changed (P > 0.05), whereas FRAP level was decreased (P < 0.001) at 3 h after treatment. Neither SOD nor GSH-Px activity was affected by CORT treatment (P > 0.05). In CORT chickens, however, SOD activity was lower (P < 0.05) after 3 h of treatment. There was an obvious time effect (P < 0.0001) on the activity of GHS-Px, which declined with time in either control or CORT treatment (Table 2). The interaction of time and treatment was significant (P < 0.01) for GSH-Px, which had more decline in CORT chickens compared with control ones (CORT, 21.1% vs. control, 16.2%). The concentrations of TBARS in PM were not obviously affected by CORT treatment (Figure 2A, Table 3). However, there was a significant (P < 0.0001) time effect and TBARS levels increased with time regardless of treatment. Muscle FRAP level was significantly (P < 0.0001) affected by either CORT or time. The FRAP level was higher (P < 0.05) in CORT chickens at all time points except the 48-h postmortem time point, when there was no obvious difference (P > 0.05) between 2 treatments (Figure 2B, Table 3). In the control group, muscle FRAP increased after slaughter and then decreased at 48 h postmortem, compared with the ini-

tial preslaughter level. In contrast, there was no obvious decline until 48 h postmortem in CORT chickens. The TBARS levels in BF tended (P = 0.0968) to be increased by CORT treatment and the obvious effect (P < 0.05) was detected at 48 h postmortem (Figure 2A, Table 3). The time effect was only observed in CORT chickens, in which TBARS levels significantly (P < 0.01) increased with time. Muscle FRAP content was affected (P = 0.0502) by CORT treatment (Figure 2B, Table 3). Regardless of treatment, FRAP levels increased (P < 0.05) at 24 h postmortem compared with the initial postmortem levels and then restored to the initial values.

CORTICOSTERONE INDUCES OXIDATIVE INJURY IN SKELETAL MUSCLE

upregulation of circulating CORT could induce oxidative stress. In CORT chickens, the significant elevated plasma total antioxidant power was found in all 3 experiments, which should be ascribed to the increased concentration of urate (Lin et al., 2006). Urate was significantly elevated by CORT administration, which is the result of enhanced proteolysis (Dong et al., 2007). As a powerful antioxidant, urate could extinguish reactive oxygen species in poultry (Simoyi et al., 2002, 2003). Although we can assume that a CORT-induced increase in plasma total antioxidant power did not prevent the occurrence of lipid peroxidation, further re-

search is required to reach the conclusion because we did not measure the oxidation product of urate. The increased plasma concentration of urate and in turn the elevated total antioxidant power cannot solely illustrate the status of antioxidant substrates. In the present study, the different change in plasma activity of CK was observed in CORT treatment compared with control chickens, indicating the skeletal muscle damage in CORT chickens. Moreover, shortterm challenge of CORT could induce the oxidative injury in skeletal muscles, as seen in mammals in which a high dose of CORT administration (100 mg/kg of BW) led to lipid peroxidation in the gastrocnemius muscle of rats (Ohtsuka et al., 1998). Young et al. (2003b) reported that preslaughter stress (transport and shackling) increased lipid peroxidation in PM. Thus, it can be concluded that acute CORT challenge induces altered redox status of skeletal muscles. Moreover, in the present study, although the effect of CORT on the preslaughter TBARS level in BF was not significant, the TBARS level at 48 h postmortem was significantly higher in CORT chickens compared with control ones. This result was in line with previous studies on pork meat (Juncher et al., 2001, 2003), suggesting that the oxidative stability during storage of meat is affected by the preslaughter physiological state of muscle tissue. Because this effect was not observed in PM, the tissue specificity in the oxidative stability should be related to the difference in the numbers of mitochondria and myoglobin between red and white meat. In broiler chickens, exposure of synthetic glucocorticoid (dexamethasone) could induce the oxidative stress in seminal plasma reflected by the high lipid peroxidation and reduced activity of GSH-Px, resulting in decreased sperm count and motility and increased percentage of dead sperm (Eid et al., 2006). Preslaughter stress modifies the characteristics of the antioxidant system as evident through altered activities of antioxidant enzymes in porcine meat (Young et al., 2003a). It was postulated that the impaired muscle cell membrane integrity is associated with the reduced meat quality caused by stress (Sandercock et al., 2001; Malheiros et al., 2003). Therefore, if lipid peroxidation caused deteriorated meat quality through exudative water loss resulting from stress, new research needs to focus on this problem. During the development of rigor mortis, muscle cells experience a variety of metabolic processes, such as anaerobic metabolism and energy depletion. During these processes, muscle cells maintain the capacity to metabolically respond to their changing environment. However, the information about the development of lipid peroxidation during the process of rigor mortis is limited. The components of the antioxidant substances are complex, consisting either of substances with both high activity but in low amount, such as vitamins E and C, or substances in high amount and low activity, such as proteins, peptides, and amino acids (Dröge, 2002). The work of Young et al. (2003a) indicates that the

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Figure 2. Effect of corticosterone (CORT) administration (4 mg/ kg of body mass) on the levels of TBA reacting substances (TBARS, A) and ferric reducing-antioxidant power (FRAP) in musculus pectoralis major (PM) and biceps femoris (BF, B) of broilers in experiment 3. Values are means ± SEM (n = 12). Pre-slaughter = muscle biopsies obtained immediately before slaughter; 0 h, 24 h, and 48 h = muscle samples obtained immediately after slaughter and at 24 h postmortem, respectively. a,b, a′,b′, x,y, x′–z′Means with different superscript within the same treatment differ significantly (P < 0.05). †Means at the same time point in PM differ significantly between treatment (P < 0.05).

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ACKNOWLEDGMENTS This work was supported by grants from National Basic Research Program of China (2004CB117507) and New Century Excellent Talents in University and sponsored by Scientific Research Foundation for the Returned Oversea Chinese Scholars, State Education Ministry. The project was supported by National Key Project of Scientific and Technical Supporting Programs Funded by Ministry of Science & Technology of China (2006BAD14B01).

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