@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(3):193-202
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(3):193-202
The Effect of Six Weeks of Continuous Training with Ziziphus Jujube Extract Consumption on Lipocalin-2 and Adiponectin Levels in Plasma and Heart Tissue of Rats with Myocardial Infraction (MI)
ARTICLE INFO
Article Type
Original ResearchAuthors
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, IranPhone: +98 (56) 32405471
Fax: +98 (56) 32405471
Article History
Received: September 30, 2017Accepted: May 23, 2018
ePublished: July 23, 2018
ABSTRACT
Aims
Exercise training is one of the methods used in cardiac rehab.The aim of this
study was to determine the effect of six weeks of continuous training with Ziziphus
Jujube extract consumption on lipocalin-2 and adiponectin levels in plasma and
heart tissue in rats with myocardial infraction.
Materials & Methods 30 male Wistar rats weighing 180 - 320 gr, aged 2-3 months, were randomly divided into 5 groups of 6 each: 1. Healthy control, 2. Infarction control, 3. Infarction + Jujube extract, 4. Infarction +Continuous aerobic exercise, 5. Infarction +Continuous aerobic exercise + Jujube extract. The training program lasted for 5 days per week for 6 weeks and speed of 16 m/min for 40 min per day. The Ziziphus jujube extract was gavaged 400 mg / kg for 6 weeks. In the end, the rats were anesthetized and blood samples were taken from heart tissue. The levels of lipocalin 2 and adiponectin were measured using the appropriate kits and ELISA method and the statistical analysis was conducted using one way ANOVA and Tukey post hoc test at a significant level of p<0.05.
Findings Adiponectin values in heart tissue of rats increased significantly (p<0.05) after six weeks of continuous training with Ziziphus Jujube extract consumption. While levels of plasma and heart tissue lipocalin-2 and plasma adiponectin did not change significantly (p>0.05).
Conclusion Six weeks of continuous training with Ziziphus Jujube extract consumption can improve cardiac damage caused by infarction through increasing adiponectin levels in the heart tissue.
Materials & Methods 30 male Wistar rats weighing 180 - 320 gr, aged 2-3 months, were randomly divided into 5 groups of 6 each: 1. Healthy control, 2. Infarction control, 3. Infarction + Jujube extract, 4. Infarction +Continuous aerobic exercise, 5. Infarction +Continuous aerobic exercise + Jujube extract. The training program lasted for 5 days per week for 6 weeks and speed of 16 m/min for 40 min per day. The Ziziphus jujube extract was gavaged 400 mg / kg for 6 weeks. In the end, the rats were anesthetized and blood samples were taken from heart tissue. The levels of lipocalin 2 and adiponectin were measured using the appropriate kits and ELISA method and the statistical analysis was conducted using one way ANOVA and Tukey post hoc test at a significant level of p<0.05.
Findings Adiponectin values in heart tissue of rats increased significantly (p<0.05) after six weeks of continuous training with Ziziphus Jujube extract consumption. While levels of plasma and heart tissue lipocalin-2 and plasma adiponectin did not change significantly (p>0.05).
Conclusion Six weeks of continuous training with Ziziphus Jujube extract consumption can improve cardiac damage caused by infarction through increasing adiponectin levels in the heart tissue.
CITATION LINKS
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[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]
[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]