Seyed Morteza Tayebi1, Karsten Krüger2, Farahnaz Ebrahimi3, Abbas Izadi3, Maryam Roushan3, Anna V. Nenasheva4
1Allameh Tabataba’i University, Faculty of Sport Science, Department of Exercise Physiology, Tehran, Iran
2Justus-Liebig-Universität Gießen, Department of Exercise Physiology and Sports Therapy, Gießen, Germany
3Islamic Azad University, Kerman Branch, Faculty of Humanity, Department of Exercise Physiology, Kerman, Iran
4South Ural State University (National Research University), Institute of Sport, Tourism and Service, Athletic Performance Enhancement Department, Chelyabinsk, Russia
Supplementation with Ziziphus Jujuba Suppresses Apoptosis Signals in Neutrophils after Acute Exercise
Monten. J. Sports Sci. Med. 2021, 10(2), 31-39 | DOI: 10.26773/mjssm.210905
Abstract
It is suggested that jujube might benefit exercise-induced immune fluctuations, specifically on neutrophils’ apoptosis
regulation, but its cellular mechanism is unclear. This study aimed to investigate the effect of one-week supplemen-
tation with Ziziphus jujuba on pro- and anti-apoptotic protein levels of neutrophils in response to a session of circuit
resistance exercise. Fourteen young, healthy male students completed a session of circuit resistance exercise (75% 1RM,
nine exercises, three sets) in two groups (n=7). While one group received a placebo, the other group was supplemented
with jujube (0.5 g/kg body weight suspended in 2.5 cc distilled water) started a weekday before the exercise session.
Blood samples were collected 30 minutes before, immediately, and two hours after the exercise. Neutrophils were col-
lected and pro- (Calpain-1, Bax, Caspase-3) and anti-apoptotic (Calpastatin, XIAP) proteins measured with ELISA. In-
tracellular calcium ([Ca 2+ ]i) was assessed using the Atomic Absorption/ Flame Emission method. Repeated-Measures
ANOVA was used for the interaction effects of TIME×GROUP (3×2) at the significance level (p) of 0.05. The SPSS software
was used for analyses. Levels of ([Ca 2+ ]i), ex
Keywords
exercise, resistance exercise, ziziphus jujuba, neutrophil cell, cell apoptosis, intracellular calcium
View full article
(PDF – 651KB)
References
Afroz, R., Tanvir, E. M., Islam, M. A., Alam, F., Gan, S. H., & Khalil, M. I. (2014). Potential Antioxidant and Antibacterial Properties of a Popular Jujube Fruit: Apple Kul (Zizyphus mauritiana). Journal of Food Biochemistry, 38(6), 592-601. https://doi.org/10.1111/jfbc.12100
Afzalpour, M. E., Abtahi Eivari, H., Rezazadeh, A., & Soluki, A. (2015). Effect of Ziziphus jujuba Supplementation before One Session of Acute Resistance Exercise on the Serum Glutathione Peroxidase and Superoxide Dismutase Activity. Horizon of Medical Sciences, 21(2), 97-104.
Afzalpour, M. E., Rezazadeh, A., & Abtahi, S. H. (2014). Effects of Jujube fruit on total antioxidant capacity and lipid peroxidation in young women after an intensive resistance exercise session. Journal of Sport and Biomotor Sciences, 6(11), 16-26.
Altznauer, F., Conus, S., Cavalli, A., Folkers, G., & Simon, H. U. (2004). Calpain-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. Journal of Biological Chemistry, 279(7), 5947-5957. https://doi.org/10.1074/jbc.M308576200
Borges, L., Passos, M. E. P., Silva, M. B. B., Santos, V. C., Momesso, C. M., Pithon-Curi, T. C., . . . Hatanaka, E. (2019). Dance Training Improves Cytokine Secretion and Viability of Neutrophils in Diabetic Patients. Mediators of Inflammation, 2019, 2924818. https://doi.org/10.1155/2019/2924818
Chen, J., Li, Z., Maiwulanjiang, M., Zhang, W. L., Zhan, J. Y. X., Lam, C. T. W., . . . Tsim, K. W. K. (2013). Chemical and Biological Assessment of Ziziphus jujuba Fruits from China: Different Geographical Sources and Developmental Stages. Journal of Agricultural and Food Chemistry, 61(30), 7315-7324. https://doi.org/10.1021/jf402379u
Chen, Y.-C., Chou, W.-Y., Fu, T.-C., & Wang, J.-S. (2018). Effects of normoxic and hypoxic exercise training on the bactericidal capacity and subsequent apoptosis of neutrophils in sedentary men. European Journal of Applied Physiology, 118(9), 1985-1995. https://doi.org/10.1007/s00421-018-3935-7
Cheng, D., Zhu, C., Cao, J., & Jiang, W. (2012). The protective effects of polyphenols from jujube peel (Ziziphus Jujube Mill) on isoproterenol-induced myocardial ischemia and aluminum-induced oxidative damage in rats. Food and Chemical Toxicology, 50(5), 1302-1308. https://doi.org/10.1016/j.fct.2012.01.026
Choi, S. H., Ahn, J. B., Kozukue, N., Levin, C. E., & Friedman, M. (2011). Distribution of free amino acids, flavonoids, total phenolics, and anti-oxidative activities of Jujube (Ziziphus jujuba) fruits and seeds harvested from plants grown in Korea. Journal of Agricultural and Food Chemistry, 59(12), 6594-6604. https://doi.org/10.1021/jf200371r
Chuong, P., Wysoczynski, M., & Hellmann, J. (2019). Do Changes in Innate Immunity Underlie the Cardiovascular Benefits of Exercise? Frontiers in Cardiovascular Medicine, 6(70). https://doi.org/10.3389/fcvm.2019.00070
Curi, T. C., De Melo, M. P., De Azevedo, R. B., Zorn, T. M., & Curi, R. (1997). Glutamine utilization by rat neutrophils: presence of phosphate-dependent glutaminase. American Journal of Physiology, 273(4 Pt 1), C1124-1129.
Cury-Boaventura, M. F., Levada-Pires, A. C., Folador, A., Gorjao, R., Alba-Loureiro, T. C., Hirabara, S. M., . . . Pithon-Curi, T. C. (2008). Effects of exercise on leukocyte death: prevention by hydrolyzed whey protein enriched with glutamine dipeptide. European Journal of Applied Physiology, 103(3), 289-294. https://doi.org/10.1007/s00421-008-0702-1
Du, L.-J., Gao, Q.-H., Ji, X.-L., Ma, Y.-J., Xu, F.-Y., & Wang, M. (2013). Comparison of Flavonoids, Phenolic Acids, and Antioxidant Activity of Explosion-Puffed and Sun-Dried Jujubes (Ziziphus jujuba Mill.). Journal of Agricultural and Food Chemistry, 61(48), 11840-11847. https://doi.org/10.1021/jf401744c
Ermert, D., Niemiec, M. J., Röhm, M., Glenthøj, A., Borregaard, N., & Urban, C. F. (2013). Candida albicans escapes from mouse neutrophils. Journal of Leukocyte Biology, 94(2), 223-236. https://doi.org/10.1189/jlb.0213063
Gao, Q. H., Wu, C. S., Yu, J. G., Wang, M., Ma, Y. J., & Li, C. L. (2012). Textural characteristic, antioxidant activity, sugar, organic acid, and phenolic profiles of 10 promising jujube (Ziziphus jujuba Mill.) selections. Journal of Food Science, 77(11), C1218-C1225.
Gao, Q.-H., Wu, P.-T., Liu, J.-R., Wu, C.-S., Parry, J. W., & Wang, M. (2011). Physico-chemical properties and antioxidant capacity of different jujube (Ziziphus jujuba Mill.) cultivars grown in loess plateau of China. Scientia Horticulturae, 130(1), 67-72. https://doi.org/10.1016/j.scienta.2011.06.005
Geering, B., & Simon, H. U. (2011). Peculiarities of cell death mechanisms in neutrophils. Cell Death & Differentiation, 18(9), 1457-1469.
Ghanbari Niaki, A., Hosseini, F., Rooadbari, F., Rahmati Ahmadabad, S., & Rooadbari, M. (2013). Effects of Aerobic Training, with or without Zizyphus Jujuba Water Extraction, on Fundus Nesfatin-1, ATP, HDL-C, and LDL-C Concentrations in Female Rats. Iranian Journal of Health and Physical Activity, 4(1), 9-16.
Ghanbari Niaki, A., Mohammadi Joojadeh, F., Zare Kookandeh, N., Najafi, S., Chaichi, M. J., Rodbari, F., & Bayat, H. (2013). Liver and plasma nesfatin-1 responses to 6 weeks of treadmill running with or without zizyphus jujuba liquid extract in female rat. International Journal of Endocrinology and Metabolism, 11(2), 95-101. https://doi.org/10.5812/ijem.8438
Guo, S., Duan, J.-a., Qian, D., Tang, Y., Qian, Y., Wu, D., . . . Shang, E. (2013). Rapid Determination of Amino Acids in Fruits of Ziziphus jujubaby Hydrophilic Interaction Ultra-High-Performance Liquid Chromatography Coupled with Triple-Quadrupole Mass Spectrometry. Journal of Agricultural and Food Chemistry, 61(11), 2709-2719. https://doi.org/10.1021/jf305497r
Guo, S., Duan, J.-a., Qian, D., Wang, H., Tang, Y., Qian, Y., . . . Shang, E. (2013). Hydrophilic interaction ultra-high performance liquid chromatography coupled with triple quadrupole mass spectrometry for determination of nucleotides, nucleosides and nucleobases in Ziziphus plants. Journal of Chromatography A, 1301, 147-155. https://doi.org/10.1016/j.chroma.2013.05.074
Jacobs, L., Nawrot, T. S., de Geus, B., Meeusen, R., Degraeuwe, B., Bernard, A., . . . Panis, L. I. (2010). Subclinical responses in healthy cyclists briefly exposed to traffic-related air pollution: an intervention study. Environmental Health, 9(1), 64. https://doi.org/10.1186/1476-069x-9-64
Kroemer, G., Dallaporta, B., & Resche-Rigon, M. (1998). The mitochondrial death/life regulator in apoptosis and necrosis. Annual Review of Physiology, 60, 619-642. https://doi.org/10.1146/annurev.physiol.60.1.619
Kruger, K., & Mooren, F. C. (2014). Exercise-induced leukocyte apoptosis. Exercise Immunology Review, 20, 117-134.
Lagranha, C. J., deLima, T. M., Senna, S. M., Doi, S. Q., Curi, R., & Pithon-Curi, T. C. (2005). The effect of glutamine supplementation on the function of neutrophils from exercised rats. Cell Biochemistry & Function, 23(2), 101-107. https://doi.org/10.1002/cbf.1192
Lagranha, C. J., Hirabara, S. M., Curi, R., & Pithon-Curi, T. C. (2007). Glutamine supplementation prevents exercise-induced neutrophil apoptosis and reduces p38 MAPK and JNK phosphorylation and p53 and caspase 3 ex
Lagranha, C. J., Levada-Pires, A. C., Sellitti, D. F., Procopio, J., Curi, R., & Pithon-Curi, T. C. (2008). The effect of glutamine supplementation and physical exercise on neutrophil function. Amino Acids, 34(3), 337-346. https://doi.org/10.1007/s00726-007-0560-x
Lagranha, C. J., Senna, S. M., De Lima, T. M., Silva, É. P. P., Doi, S. Q., Curi, R. U. I., & Pithon-Curi, T. C. (2004). Beneficial Effect of Glutamine on Exercise-Induced Apoptosis of Rat Neutrophils. Medicine & Science in Sports & Exercise, 36(2), 210-217.
Lee, S. M., Min, B. S., Lee, C. G., Kim, K. S., & Kho, Y. H. (2003). Cytotoxic Triterpenoids from the Fruits of Zizyphus jujuba. Planta Medica, 69(11), 1051-1054. https://doi.org/10.1055/s-2003-45155
Li, J., Ai, L., Yang, Q., Liu, Y., & Shan, L. (2013). Isolation and structural characterization of a polysaccharide from fruits of Zizyphus jujuba cv. Junzao. International Journal of Biological Macromolecules, 55, 83-87. https://doi.org/10.1016/j.ijbiomac.2012.12.017
Liang, S., & Juan, J. (2011). Effect of jujube extract on oxidative injury in heart muscles of exhausted training rats. African Journal of Microbiology Research, 5(14), 1896-1899.
Mooren, F. C., Völker, K., Klocke, R., Nikol, S., Waltenberger, J., & Krüger, K. (2012). Exercise delays neutrophil apoptosis by a G-CSF-dependent mechanism. Journal of Applied Physiology, 113(7), 1082-1090. https://doi.org/10.1152/japplphysiol.00797.2012
Plastina, P. (2016). Pharmacological Aspects of Jujubes. Pharmacologia, 7(5), 243-255. https://doi.org/10.5567/pharmacologia.2016.243.255
Presbitero, A., Mancini, E., Castiglione, F., Krzhizhanovskaya, V. V., & Quax, R. (2019). Game of neutrophils: modeling the balance between apoptosis and necrosis. BMC Bioinformatics, 20(6), 475. https://doi.org/10.1186/s12859-019-3044-6
Rodríguez Villanueva, J., & Rodríguez Villanueva, L. (2017). Experimental and Clinical Pharmacology of Ziziphus jujuba Mills. Phytotherapy Research, n/a-n/a. https://doi.org/10.1002/ptr.5759
Syu, G. D., Chen, H. I., & Jen, C. J. (2011). Severe Exercise and Exercise Training Exert Opposite Effects on Human Neutrophil Apoptosis via Altering the Redox Status. PLoS One, 6(9), e24385. https://doi.org/10.1371/journal.pone.0024385
Tayebi, S. M., Agha-Alinejad, H., Shafaee, S., Gharakhanlou, R., & Asouri, M. (2014). Short-Term Effects of Oral Feeding Jujube Ziziphus Solution before a Single Session of Circuit Resistance Exercise on Apoptosis of Human Neutrophil. Annals of Applied Sport Science, 2(1), 53-68.
Tayebi, S. M., Ghorban-alizadeh, F., Ghaziani., & Mohamadi, H., Bazneshin. (2012). Oral glucose administration after circuit resistance exercise induced plasma ghrelin suppression. European Journal of Experimental Biology, 2(5), 1616-1624.
Tayebi, S. M., Saeidi, A., Gharahcholo, L., Haghshenas Gatabi, R., & Radmehr, L. (2016). Acute and Short-Term Effects of Oral Jujube Solution on White Blood Cell and its Differential count in Response to Circuit Resistance Exercise. International Journal of Applied Exercise Physiology, 5(2), 1-10.
Tayebi, S. M., Saeidi, A., Mahmoudi, A. A., Gharahcholo, L., & Radmehr, L. (2015). Acute and Short-Term Effects of Oral Feeding of Jujube Solution on Blood Platelets and its Morphological Indices in Response to a Circuit Resistance Exercise. Annals of Applied Sport Science, 3(3), 67-82. https://doi.org/10.18869/acadpub.aassjournal.3.3.67
Vahedi, F., Fathi Najafi, M., & Bozari, K. (2008). Evaluation of inhibitory effect and apoptosis induction of Zyzyphus Jujube on tumor cell lines, an in vitro preliminary study. Cytotechnology, 56(2), 105-111. https://doi.org/10.1007/s10616-008-9131-6
van Raam, B. J., Drewniak, A., Groenewold, V., van den Berg, T. K., & Kuijpers, T. W. (2008). Granulocyte colony-stimulating factor delays neutrophil apoptosis by inhibition of calpains upstream of caspase-3. Blood, 112(5), 2046-2054. https://doi.org/10.1182/blood-2008-04-149575
Wang, B.-N., Liu, H. F., Zheng, J. B., Fan, M. T., & Cao, W. (2011). Distribution of Phenolic Acids in Different Tissues of Jujube and Their Antioxidant Activity. Journal of Agricultural and Food Chemistry, 59(4), 1288-1292. https://doi.org/10.1021/jf103982q