ARTICLE INFO

Article Type

Original Research

Authors

Hosseini   M (1)
Bambaeichi   E (*)
Sarir   H (2)
Kargarfard   M (1)
Mogharnasi   M (3)






(*) Department of Exercise Physiology, Faculty of Sport Sciences, University of Isfahan, Isfahan, Iran
(1) Department of Exercise Physiology, Faculty of Sport Sciences, University of Isfahan, Isfahan, Iran
(2) 2 Department of Animal Science, Faculty of Agriculture, University of Birjand, Birjand, Iran
(3) Department of Exercise Physiology, Faculty of Sport Sciences, University of Birjand, Birjand, Iran

Correspondence

Address: Department of Exercise Physiology, Faculty of Sport Sciences, University of I sfahan, Isfahan, Iran
Phone: +98 (56) 32405471
Fax: +98 (56) 32405471

Article History

Received:  September  30, 2017
Accepted:  May 23, 2018
ePublished:  July 23, 2018

BRIEF TEXT


Cardiovascular diseases are the most common cause of death in most countries of the world [1]. … [2-15]. Due to having compounds such as tannins and flavonoids, jujube has antioxidant and anti-inflammatory properties and protects the body against oxidative stress [16]. … [17-22]. High intensity periodic exercises can effectively increase the angiogenesis factors and improve cardiac function in mice after myocardial infarction [23].

Some reports have shown that long-term endurance exercises after myocardial ischemia (MI) significantly increase the hypertrophy of cardiac myocytes [21] and prevent the structural deformity of the left ventricle due to isoprenaline injection [22]. High intensity periodic exercises have also been effective in increasing angiogenesis factors and improving cardiac function in mice after myocardial infarction [23]. On the other hand, some studies have shown that short-term endurance exercises after myocardial infarction can exacerbate tissue damage in the heart of mice [24].

The aim of this study was to investigate the effect of 6-week continuous exercise along with jujube consumption on lipocalin-2 and adiponectin levels in cardiac plasma and heart tissue in rats with myocardial infarction.

This applied research is an experimental study.

This research was carried out on Wistar rats at Animal Laboratory, Faculty of Agriculture, University of Birjand, in the winter of 2016.

Samples included 30 Wistar rats weighing 180-320 g in the range of 2-3 months. An infarction induction was performed randomly on 24 rats. They were randomly assigned to 4 groups, including infarction control, infarction + jujube extract, continuous aerobic exercise + infarction, as well as continuous aerobic exercise + infarction + jujube extract. It should be noted that a healthy control group (including 6 rats) was also considered.

Induced infarction with intraperitoneal injection of isoprenalin (85 mg/kg) as normal saline solution (per 1 ml of isophoraline dosage, 1 ml of normal saline) was injected intraperitoneally to the mice for 2 consecutive days with a 24-hour interval in the peritoneum area to cause myocardial infarction [25]. … [26, 27]. One week after infarction induction, aerobic exercise protocol running on treadmill was performed, including of 2 stages of adjustment (1 week) and a main exercise program (6 weeks) [28]. In the adjustment phase, running speed and exercise duration gradually increased as treadmill speed ranged from 5-10 m/min and exercise duration ranged from 5 minutes per session to 10 minutes. Then, the intervention of exercise activity began. Continuous exercise groups started the main exercise program at the first week at speed of 10 m/min for 10 minutes per day and the zero slope of treadmill for 5 sessions per week. The speed and duration of the exercise gradually increased, so that at the end of the 6th week, the mice were able to run with a speed of 16 m/min and 40 minutes per day [29]. During this period, the control group was placed under the standard environmental conditions of the laboratory (without activity). Jujube extract groups used jujube supplement according to the program. After 6 weeks of intervention and jujube extract consumption, 2 days after the last exercise session, each rat was anesthetized by injecting anesthetics (ketamine combination of 70 mg/kg and xylocaine 10 mg/kg) [30] and, then, the chests of the rats were split and blood samples were taken directly from the rats’ hearts. Then, the heart muscle was isolated and washed in the physiologic serum and immediately frozen with liquid nitrogen and transported to a freezer at 80°C for further measurements. Blood samples were centrifuged after mixing the falcon tube with EDTA saturation solution for 15 minutes at 3200 rpm, and the obtained plasma was frozen in a freezer at 80°C. The heart tissue was homogenized by liquid nitrogen, and, then, a buffer containing a protease inhibitor pill, made in the United States, St. Louis Sigma, was added to each sample. The soluble proteins was determined by Bradford test and for left ventricular extraction of the heart, the tissue was weighed out of liquid nitrogen; it was 5 times that of the weight of the Lysis buffer, and also a little powder PMSF was added [31]. Lipocalin-2 and adiponectin levels in plasma and heart tissue were evaluated, using a German lipocalin-2 rats kit made by the Zelbio company, with a sensitivity of 0.2 ng/ml and adiponectin with a sensitivity of 28 pg/ml in ELISA. The data were analyzed by SPSS 22, using Shapiro Wilco test and to examine the data distribution, One-way ANOVA and Tukey's test were used to determine the difference between pair groups.

6 weeks of continuous exercise with jujube supplementation did not significantly affect lipoparticulin-2 levels and plasma adiponectin, as well as lipocalin-2 of heart tissue in rats with myocardial infarction. On the other hand, the lipocalin-2 levels of heart tissue in the control group of infarction showed a significant increase compared to the healthy control group. There was also a slight increase in lipocalin-2 plasma levels in continuous exercise + infarction + jujube extract, continuous exercise + infarction, and infarction + extract compared to the control group of infarction, but this increase was not significant. On the other hand, continuous exercise along with jujube extracts had a significant effect on adiponectin levels in the heart tissue of rats in continuous exercise + infarction + jujube extract compared to the control group of infarction (p<0.05). However, plasma adiponectin levels did not change significantly in continuous exercise + infarction + jujube extract and continuous + infarction group compared to control group of infarction (Table 1).

…. [32]. The findings of this study were consistent with a number of studies. Jafarzadeh et al. stated that after 8 weeks of moderate-intensity aerobic exercise, changes in lipociline-2 levels and plasma glucose levels were not significant [33]. Hosseini et al. reported that there was no significant difference between the lipocalin-2 levels in the 5 groups and the use of Pistacia atlantica extract, which is probably due to the low level of exercise duration and the dosage of Pistacia atlantica extract [34]. Ghorbanian et al. have shown the lack of significant effect of exercise on lipocalin-2 with investigating the effect of extended resistance exercise course on lipocalin-2 levels and lipid profiles in passive men, although resistance exercises significantly reduced some lipid profile [35]. …. [36-46]. The results of adiponectin were consistent with some studies. Abdi et al. investigated the effect of 8 weeks of cardiac rehabilitation on serum adiponectin and plasma lipoprotein levels in men with coronary artery disease, and the results have shown an increase in adiponectin levels and no change in subjects' weight [47]. Dehghani et al. studied the effects of 10 weeks aerobic exercise on plasma adiponectin levels and concluded that regular aerobic exercise (55-85% of maximum heart rate) significantly increased plasma adiponectin in non-athletic male students and after 4 weeks without exercise, the reduction of adiponectin levels was observed [48]. … [49-51].

It is suggested that surgical infarction induction methods should be considered with longer rest periods after infarction induction and the implementation of long-term practice protocols, as well as the use of different doses of jujube extracts on animal samples of myocardial infarction.

It seems that a week for the normal rehabilitation of the rats and the starting the exercise after infarction induction is short, and the combination of exercise and gavage in one day and a lack of time for rest is considered as a stressor for the mice.

6 weeks of continuous exercise and jujube consumption improves cardiac damage from infarction in rats by increasing the amount of adiponectin in the heart tissue.

The authors express their gratitude to the sincere cooperation of the colleagues at the library of faculty of agriculture of the University of Birjand, and in particular, Dr. Sarir, as well as all the dear people who helped us with this plan.

There is no conflict of interest between the authors.

None declared by the authors.

The present study was funded by the research department of Isfahan University.

TABLES and CHARTS

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CITIATION LINKS

[1]Hatmi ZN, Tahvildari S, GafarzadehMotlag A, Sabouri Kashani A. Prevalence of coronary artery disease risk factors in Iran: A population based survey. BMC Cardiovasc Disord. 2007;7:32-7.
[2]Feijóo-Bandín S, Rodríguez-Penas D, García-Rúa V, Mosquera-Leal A, González-Juanatey JR, Lago F. Adipokines at the cardiovascular system: Role in health and disease. SM J Endocrinol Metab. 2016;2(1):1009-17.
[3]Soylu K, Aksan G, Nar G, Özdemir M, Gülel O, İnci S, et al. Serum neutrophil gelatinase-associated lipocalin levels are correlated with the complexity and the severity of atherosclerosis in acute coronary syndrome. Anatol J Cardiol. 2015;15(6):450-55.
[4]Cowland JB, Sørensen OE, Sehested M, Borregaard N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol. 2003;171(12):6630-9.
[5]Yndestad A, Landrø L, Ueland T, Dahl CP, Flo TH, Vinge LE, et al. Increased systemic and myocardial expression of neutrophil gelatinase-associated lipocalin in clinical and experimental heart failure. Eur Heart J. 2009;30(10):1229-36.
[6]Choi KM, Lee JS, Kim EJ, Baik SH, Seo HS, Choi DS, et al. Implication of lipocalin-2 and visfatin levels inpatients with coronary heart disease. Eur J Endocrinol. 2008;158(2):203-7.
[7]Bu DX , Hemdahl AL, Gabrielsen A, Fuxe J, Zhu Ch, Eriksson P, et al. Induction of neutrophil gelatinase-associated lipocalin in vascular injury via activation of nuclear factor-κB. Am J Pathol. 2006;169(6):2245-53.
[8]Aigner F, Maier HT, Schwelberger HG, Wallnöfer EA, Amberger A, Obrist P, et al. Lipocalin-2 regulates the inflammatory response during ischemia and reperfusion of the transplanted heart. Am J Transplant. 2007;7(4):779-88.
[9]Shibata R, Ouchi N, Murohara T. Adiponectin and cardiovascular disease. Circ J. 2009;73(4):608-14.
[10]Ding G, Qin Q, He N, David SCF, Hou J, Liu J, et al. Adiponectin and its receptors are expressed in adult ventricular cardiomyocytes and upregulated by activation of peroxisome proliferator-activated receptor gamma. J Mol Cell Cardiol. 2007;43(1):73-84.
[11]De Roeck L, Vandamme S, Everaert BR, Hoymans V, Haine S, Vandendriessche T, et al. Adiponectin and ischemia reperfusion injury in ST segment elevation myocardial infarction. Eur Heart J Acute Cardiovasc Care. 2016;5(1):71-6.
[12]Shibata R, Izumiya Y, Sato K, Papanicolaou K, Kihara S, Colucci WS, et al. Adiponectin protects against the development of systolic dysfunction following myocardial infarction. J Mol Cell Cardiol. 2007;42(6):1065-74.
[13]Ren J, Xu X, Wang Q, Ren SY, Dong M, Zhang Y. Permissive role of AMPK and autophagy in adiponectindeficiency-accentuated myocardial injury and inflammation in endotoxemia. J Mol Cell Cardiol. 2016;93:18-31.
[14]Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA. 2007;297(8):842-57.
[15]Esteki T, Urooj A. Phytochemical Profile and antioxidant potential of different tissues of Zizyphus Jujuba mill. Int J Food Nutr Saf. 2012;1(3):144-57.
[16]Taati M, Alirezaei M, Meshkatalsadat M H, Rasoulian B, Dezfolian O, Neamati S. Antioxidant effects of aqueous fruit extract of Ziziphus jujuba on ethanol-induced oxidative stress in the liver and kidney of male rats. J Lorestan Univ Med Sci (Yafte). 2011;13(2):54-68. [Persian]
[17]Zhang H, Jiang L, Ye S, Ye Y, Ren F. Systematic evaluation of antioxidant capacities of the ethanolic extract of different tissues of jujube (Ziziphus jujuba Mill.) from China. Food Chem Toxicol. 2010;48(6):1461-65.
[18]Zhang S, Li N. Effects of carbon monoxide on quality, nutrients and antioxidant activity of post-harvest jujube. J Sci Food Agric. 2014;94(5):1013-9.
[19]Cheng D, Zhu C, Cao J, Jiang W. The protective effects of polyphenols from jujube peel (Ziziphus Jujube Mill) on isoproterenol-induced myocardial ischemia and aluminum-induced oxidative damage in rats. Food Chem Toxicol. 2012;50(5):1302-8.
[20]Liang S, Juan J. Effect of jujube extract on oxidative injury in heart muscles of exhausted training rats. Afr J Microbiol Res. 2011;5(14):1896-9.
[21]Bito V, de Waard MC, Biesmans L, Lenaerts I, Ozdemir S, van Deel E, et al. Early exercise training after myocardial infarction prevents contractile, but not electrical remodeling or hypertrophy. Cardiovasc Res. 2009;86(1):72-81.
[22]Serra AJ, Santos MH, Bocalini DS, Antônio EL, Levy RF, Santos AA, et al. Exercise training inhibits inflammatory cytokines and more than prevents myocardial dysfunction in rats with sustained β-adrenergic hyperactivity. J Physiol. 2010;588(Pt 13):2431-42.
[23]Karbalaeifar S, Gaeini AA, Kordi MR, Nuri R, Ghorbani P. The effect of 6-week high intensity interval training on the VEGF/COL-18 ratio and some echocardiographic indices in rats with myocardial infarction. J Kermanshah Univ Med Sci. 2016;20(3):94-8. [Persian]
[24]Azamian Jazi A, Abdi H, Haffezi Ahmadi M R, Cheraghi J. Effect of endurance exercise training on morphological changes in rat heart tissue following experimental myocardial infarction. J Basic Res Med Sci. 2017;4(1):8-16.
[25]Kesarwani N, Azmi L. Evaluation of cardioprotective effect of Tinospora cordifolia against isoprenaline induced myocardial infarction in rats. Int J Curr Microbiol App Sci. 2014;3(3):543-55.
[26]Dashtban M, Sarir H, Omidi A. The effect of Prosopis farcta beans extract on blood biochemical parameters in streptozotocin-induced diabetic male rats. Adv Biomed Res. 2016;5:116.
[27]Ebrahimi S, Sadeghi H, Pourmahmoudi A, Askariyan S, Askari S. Protective effect of Zizphus vulgaris extract, on liver toxicity in laboratory rats. Armaghane Danesh. 2011;16(2):172-80. [Persian]
[28]Ghanbari Niaki A, Hosseini F, Rooadbari F, Rahmati Ahmadabad S, Rooadbari M. 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. Iran J Health Phys Act. 2013;4(1):9-16.
[29]Xu X, Zhao W, Lao S, Wilson BS, Erikson JM, Zhang JQ. Effects of exercise and L-arginine on ventricular remodeling and oxidative stress. Med Sci Sports Exerc. 2010;42(2):346-54.
[30]Yang YL, Chen CL, Chen CM, Ko WC. Hesperetin-5,7,3'-O-triacetate suppresses airway hyperresponsiveness in ovalbumin-sensitized and challenged mice without reversing xylazine/ketamine-induced anesthesia in normal mice. BMC Pharmacol Toxicol. 2017;18(1):39.
[31]Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54.
[32]Siri-Angkul N, Chattipakorn SC, Chattipakorn N. Roles of lipocalin 2 and adiponectin in iron overload cardiomyopathy. J Cell Physiol. 2018:233(7):5104-11.
[33]Jafarzadeh M, Shemshaki A, Kordi MR, Hedayati M. The effect of 8 week aerobic interval training on the plasma levels of Lipocalin 2, insulin, glucose and insulin resistance in obese women. Exer Phys Act. 2015;8(1):1157-66. [Persian]
[34]Hosseini M, Shemshaki A, Saghebjoo M, Gharari Arefi R. Effect of aerobic training and Pistacia atlantica extract consumption on plasma levels of Lipocalin-2 and insulin resistance index in Streptozotocin-induced diabetic rats. Q Horiz Med Sci. 2016;22(1):27-33. [Persian]
[35]Ghorbanian B, Esmaeilzadeh D. Effect of progressive resistance training on serum Lipocalin-2 and lipid profiles in in-active men. Iran J Endocrinol Metab. 2017;18(5):378-85. [Persian]
[36]Sung HK, Chan YK, Han M, Jahng JWS, Song E, Danielson E, et al. Lipocalin‐2 (NGAL) attenuates autophagy to exacerbate cardiac apoptosis induced by myocardial ischemia. J Cell Physiol. 2017;232(8):2125-34.
[37]Song E, Ramos SV, Huang X, Liu Y, Botta A, Sung H, et al. Holo-lipocalin-2-derived siderophores increase mitochondrial ROS and impair oxidative phosphorylation in rat cardiomyocytes. Proc Natl Acad Sci U S A. 2018;115(7):1576-81.
[38]Xu G, Ahn J, Chang S, Eguchi M, Ogier A, Han S, et al. Lipocalin-2 induces cardiomyocyte apoptosis by increasing intracellular iron accumulation. J Biol Chem. 2012;287(7):4808-17.
[39]Corripio R, Gónzalez-Clemente JM, Pérez-Sánchez J, Näf S, Gallart L, Nosàs R, Vendrell J, et al. Weight loss in prepubertal obese children is associated with a decrease in adipocyte fatty-acid-binding protein without changes in lipocalin-2: A 2-year longitudinal study. Eur J Endocrinol. 2010;163(6):887-93.
[40]Talebi-garakani E, Hoseini-Andargoli M, Fathi R, Safarzade AR. Changes of adipose tissue lipocalin-2 gene expression in response to one session exercise in the streptozotocin-induced diabetic rats. Iran J Endocrin Metab. 2012;14(2):178-84. [Persian]
[41]Moghadasi M, Mohammadi Domieh A. Effects of resistance versus endurance training on plasma Lipocalin-2 in young men. Asian J Sports Med. 2014;5(2):108-14.
[42]Aigner F, Maier HT, Schwelberger HG, Wallnöfer EA, Amberger A, Obrist P, et al. Lipocalin-2 regulates the inflammatory response during ischemia and reperfusion of the transplanted heart. Am J Transplant. 2007;7(4):779-88.
[43]Shemshaki A, Hosseini M, Saghebjoo M, Gharari Arefi R. The effect of 6 weeks of aerobic training on plasma levels of lipocalin-2, insulin and insulin resistance in streptozotocin-induced diabetic male rats. Sport Physiol Manag Investig. 2011;8(1):51-61. [Persian]
[44]Damirchi A, Rahmani-Nia F, Mehrabani J. Lipocalin-2: Response to a short-term treadmill protocol in obese and normal-weight men. J Human Sport Exercise. 2011;6(1):59-67.
[45]Kehrer JP. Lipocalin-2: Pro-or anti-apoptotic? ‏Cell Biol Toxicol. 2010;26(2):83-9.
[46]Zhu XJ, Chen LH, Li JH. The effects of aerobic exercise on plasma adiponectin level and adiponectin-related protein expression in myocardial tissue of ApoE-/- Mice. J Sports Sci Med. 2015;14(4):877-82.
[47]Abdi M, Marefati H, Moazenzadeh M. The effect of cardiac rehabilitation on the serum levels of adiponectin and lipoproteins in male atherosclerotic patients. J Kerman Uni Med Sci. 2012;19(4):317-25. [Persian]
[48]Dehghani K, Mogharnasi M. Effects of ten weeks of aerobic interval training and four weeks detraining on plasma adiponectin level in male student non-athletes. Zahedan Res Med Sci. 2015;17(10):29-34.
[49]Nunes RB, Alves JP, Kessler LP, Dornelles AZ, Stefani GP, Lago PD. Interval and continuous exercise enhances aerobic capacity and hemodynamic function in CHF rats. Brazilian J Phys Therap. 2015;19(4):257-63.
[50]Ranjbar K, Nazm F, Nazari A, Golami MR. Effect of 10 weeks aerobic exercise training on left ventricular systolic function, Caspase-3 and infarction size in myocardial infarction rat. J Knowl Health. 2015;10(3):16-23. [Persian]
[51]Hemmati M, Asghari S, Zohoori E, Karamian M. Hypoglycemic effects of three Iranian edible plants: Jujube, barberry and saffron: Correlation with serum adiponectin level. Pak J Pharm Sci. 2015;28(6):2095-99. [Persian]