Modern Care Journal
Modern Care Journal

article information

Modern Care Journal: Vol.17, issue 2; e100003
published online: March 11, 2020
article type: Research Article
received: December 7, 2019
revised: January 5, 2020
accepted: January 19, 2020
DOI: https://doi.org/10.5812/modernc.100003
Crossmark

Effect of Endurance Training with Coriander Seed Consumption on Caspase-3 and Cytochrome-C in the Heart Tissue of H2O2-Poisoned Rats

authors:

avatar Zahra Mardani ORCID 1 , avatar Seyed Ali Hosseini ORCID 2 , * , avatar Hassan Matinhomaee ORCID 1 , avatar Saleh Rahmati-Ahmadabad ORCID 3

Department of Sport Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
Department of Sport Physiology, Marvdasht Branch, Islamic Azad University, Marvdasht, Iran
Department of Physical Education, Pardis Branch, Islamic Azad University, Pardis, Iran

how to cite: Mardani Z, Hosseini S A, Matinhomaee H, Rahmati-Ahmadabad S. Effect of Endurance Training with Coriander Seed Consumption on Caspase-3 and Cytochrome-C in the Heart Tissue of H2O2-Poisoned Rats. Mod Care J. 2020;17(2):e100003. https://doi.org/10.5812/modernc.100003.

Abstract

Background:

Oxidative stress is a process created by free radicals at the cellular level and can lead to structural damage in different parts of the cell. However, training (T) and medicinal plants with antioxidant effects can prevent these damages.

Objectives:

The aim of present study was to investigate the effect of T with coriander seed (CS) consumption on caspase-3 and cytochrome-C in the heart tissue of hydrogen peroxide (H2O2)-poisoned rats.

Methods:

In this experimental study, 35 male Wistar rats were divided into 7 groups of 5 rats, including: 1) healthy control, 2) sham, 3) T, 4) 500 mg/kg CS, 5) 1000 mg/kg CS, 6) T+500 mg/kg CS, and 7) T+1000 mg/kg CS. During eight weeks, groups 2 - 7 received 1 mmol/kg H2O2 peritoneally for three times per week; groups 4 - 7 received CS at given doses. Also, groups 3, 6 and 7 performed T three days per week. Data analysis was performed using independent sample t-test, two-way analysis of variance and Bonferroni’s post-hoc tests. Significance level was set at 0.05.

Results:

H2O2 poisoning significantly increased caspase-3 and cytochrome-C compared to the sham group (P = 0.001); T and CS significantly decreased caspase-3 and cytochrome-C (P = 0.001), and interactive effects of T and CS were significant compared to the sham group (P ≥ 0.05). In addition, 1000 mg/kg CS had more effect on decrease of caspase-3 and cytochrome-C than 500 mg/kg CS (P ≥ 0.05).

Discussion:

T and CS consumption appear to have interactive effects on decrease of caspase-3 and cytochrome-C in the heart tissue of rats poisoned with H2O2; also effects of CS can be dose-dependent.

1. Background

Free radicals and their role in the incidence of various diseases have attracted the attention of many researchers (1). The animal body naturally responds to destructive effects of incoming free radicals in various ways. One of these methods is the use of antioxidants to neutralize the degrading nature of free radicals. The disruption of balance between the production of free radicals and antioxidant mechanisms leads to destructive conditions in the body known as oxidative stress (2). Previous studies have shown that oxidative stress can severely damage various body biomolecules, including carbohydrates, lipids, proteins, and DNA of living cells (3). Up to the present, various reasons have been reported to be causes behind increased oxidative stress in the human body. Stressful working conditions, smoking, inadequate nutrition and physical activity and training (T) are among the causes of increased oxidative stress in the blood. For example, it has been shown that the oxidative stress level in the blood of firefighters, military personnel and police officers is above normal as a result of their working conditions and therefore they are more prone to cardiovascular diseases (4). Apoptosis is a physiological process in the body to remove old and worn-out cells or cells whose DNA is irreparably damaged (5). Signals of apoptosis initiation in the cell include activation of a group of cysteine hydrolyzing enzymes known as caspases. Apart from apoptosis, caspases are a group of proteases that are involved in many other cell processes, such as cell differentiation (6). One sign of increased oxidative stress in living cells is an increase in apoptosis-related signals such as caspase-3 and release of cytochrome-C from mitochondria in stressed cells (7). Release of cytochrome-C from mitochondria activates caspase-9, resulting in caspase-3 activation and eventually apoptosis. Thus, increased oxidative stress indirectly induces apoptosis in healthy cells (8). Despite numerous benefits of exercise in the prevention of neurological and cardiovascular diseases, it has been found that oxidative stress increases in the body after exercise (9). Mitochondrial activity, when using muscles to supply the required energy, is the major cause of increased oxidative stress during exercise (10). It should be noted, however, that the amount of oxidative stress produced is directly proportional to the intensity of pressure applied to the muscles and the duration of exercise (11). In this vein, adding different antioxidants to the diet is recommended by many researchers for the maintenance of balance between free radicals and antioxidants and also due to the ability of cells to counter these dangerous compounds (12). Given obstacles and difficulties associated with existing therapeutic and control methods, the need for new and effective treatments is quite evident. Coriander, known as Coriandrum sativum, belongs to the Apiaceae family (13). The therapeutic potential of coriander seed (CS) extracts has been investigated in different studies. CS has been shown to have antimicrobial (14), anti-cancer (15) and rich antioxidant properties (16). These therapeutic properties of CS are thought to be related to essential fatty acids extracted from different parts of the plant (17). Previous studies have also shown that the extract of CS has a significant effect on the reduction of oxidative stress in the brain and testis of rats (18).

In previous studies, effects of T and CS consumption have been separately examined on apoptosis-related factors and various results have been reported. However, no study has been found to investigate the simultaneous effects of T and CS. Thus, the present study aimed to investigate the effects of T with CS consumption on caspase-3 and cytochrome-C in the heart tissue of hydrogen peroxide (H2O2) - poisoned rats.

2. Methods

In this experimental study, according to previous studies (18, 19), 35 male Wistar rats with the mean age of 10 - 12 weeks, weighing 200 - 220 g, were purchased and transferred to the laboratory. After one week of laboratory adaptation, the rats were divided into 7 groups of 5 rats including: (1) healthy control, (2) sham, (3) T, (4) 500 mg/kg CS, (5) 1000 mg/kg CS, (6) T+500 mg/kg CS, and (7) T+1000 mg/kg CS. During eight weeks, the groups 2 - 7 received 1 mmol/kg H2O2 (Sigma Aldrich) peritoneally three times per week (19) and the groups 4 - 7 received CS extracts at given doses (20). Moreover, the groups 3, 6, and 7 performed T three days per week (21).

For preparation of the CS extract, 400 g CS powder was macerated with 2160 mL of EtOH-H20 (80:20) for 24 hours. The extract was then shaken, filtered and evaporated in a rotary evaporator under reduced pressure until a semisolid extract was obtained. Moreover, the concentrated extract was freeze-dried to obtain a dry powdered extract with a yield value of 10/85% (W/W) (20).

To perform T, the rats ran on a treadmill at a speed of 8 m/min and slope of 10° for 30 minutes in the first week, at a speed of 12 m/min with the same slope for 30 minutes in the second week, at a speed of 16 m/min with the same slope for 45 minutes in the third week, and at a speed of 20 m/min with the same slope for 45 minutes in the fourth week. During the fifth to eighth weeks, the rats were trained at a speed of 20 m/min and slope of 10° for 60 minutes each session (21). Forty eight hours after the last T session and CS extract consumption, to collect heart tissue specimens, the rats were anesthetized with ketamine 10% (50 mg/kg dose) and xylazine 2% (10 mg/kg dose) and heart tissues were extracted. After weighing and washing the extracted heart tissues, they were frozen in liquid nitrogen and stored at -80° C for subsequent measurement. The tissues were then incubated for evaluation of the research variables. After homogenization of the solution, it was centrifuged at 9000 rpm for 10 minutes at 4°C and supernatants were separated.

Caspase-3 and cytochrome-C were measured by ELISA using CUSABIO laboratory kits with catalog numbers CSB-E08857r and CSB-E14281r, respectively.

2.1. Statistical Analysis

Independent-sample t-test was used to evaluate the effects of H2O2 poisoning on caspase-3 and cytochrome-C between the healthy control and sham groups. Furthermore, two-way ANOVA with Bonferroni’s post hoc tests were used to review the effects of T and CS on caspase-3 and cytochrome-C by SPSS (version 21) software (P ≤ 0.05).

3. Results

Levels of caspase-3 and cytochrome-C in the heart tissues of the rats in the seven research groups are presented in Figures 1 and 2, respectively. The results of the Independent-sample t-test showed that caspase-3 and cytochrome-C levels were significantly higher in the sham group than in the healthy control group (P = 0.001) (Figures 1 and 2). According to the two-way ANOVA results, T (P = 0.001) as well as 500 mg/kg and 1000 mg/kg CS (P = 0.001) significantly decreased caspase-3 compared to the sham group. In addition, interactive effects of T and CS were significant on caspase-3 decrease compared to the sham group (P = 0.04). Bonferroni’s post hoc test results revealed that 500 mg/kg and 1000 mg/kg CS consumption had a significant effect on decrease of caspase-3 compared to the sham group (P = 0.001), with 1000 mg/kg CS having a greater effect in this regard compared to 500 mg/kg CS (P = 0.009) (Figure 1).

Caspase-3 levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were performed using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; ++, P < 0.01 and +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed, HC, healthy control, S, sham, T, training.
Caspase-3 levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were performed using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; ++, P < 0.01 and +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed, HC, healthy control, S, sham, T, training.
Figure 1.

Caspase-3 levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were performed using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; ++, P < 0.01 and +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed, HC, healthy control, S, sham, T, training.

The results of two-way ANOVA also indicated that T (P = 0.001) along with 500 mg/kg and 1000 mg/kg CS (P = 0.001) significantly decreased cytochrome-C compared to the sham group. Further, interactive effects of T and CS were significant on decrease of cytochrome-C compared to the sham group (P = 0.001). Based on the Bonferroni’s post hoc test results, consumption of 1000 mg/kg and 500 mg/kg CS had a significant effect on decrease of cytochrome-C compared to the sham group (P = 0.001), with 1000 mg/kg CS having a higher effect in this regard compared to 500 mg/kg CS (P = 0.001) (Figure 2).

Cytochrome-C levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were carried out using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed; HC, healthy control; S, sham, T, training.
Cytochrome-C levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were carried out using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed; HC, healthy control; S, sham, T, training.
Figure 2.

Cytochrome-C levels in the heart tissues of the seven groups of rats. Data are presented as mean ± SEM. Statistical analyses were carried out using two-way ANOVA with Bonferroni’s post hoc tests. ***, P < 0.001 comparison of the sham group with the healthy control group; $$$, P < 0.001 comparison of the training group with the sham group; +++, P < 0.001 comparison of the treatment group with the sham group; #, P < 0.05 comparison of T+500 mg/kg CS with T+1000 mg/kg CS. CS, coriander seed; HC, healthy control; S, sham, T, training.

4. Discussion

In the present study, H2O2 poisoning significantly increased caspase-3 and cytochrome-C in the heart tissues of the rats. In fact, H2O2 in the study was used as an oxidative stress enhancer. The results showed that the gene expression levels of caspase-3 and cytochrome-C significantly increased in the heart tissues of rats receiving H2O2 compared to the healthy control rats. As a result, the heart tissues of rats exposed to H2O2 were destroyed. Previous studies have also shown an increase in oxidative stress after exposure of human cells to H2O2 (22). Consistent with the present study, Pirooz et al. showed that eight weeks of H2O2 administration at doses of 1 and 2 mmol/kg led to a significant increase in apoptotic factors (23). Several mechanisms have been implicated in the induction of apoptosis in the myocardial tissue of the heart, including the role of oxidative stress. Oxygen free radicals resulting from oxidative stress along with inactivation of ERK1-2 kinase and inactivation of another kinase enzyme called C-juN/C-juN/AP-1 may indicate apoptosis following oxidative stress (23).

In this study, eight weeks of T resulted in a significant decrease in caspase-3 and cytochrome-C in the heart tissues of rats poisoned with H2O2. Consistent with the findings of the present study, it was observed that low-intensity endurance training could affect oxidative stress factors and that oxidative stress would be significantly reduced if T continued for at least 12 weeks (24). Eight weeks of continuous endurance training resulted in improved citrate oxidase activity and oxidative stress in the rats (25). Exercise activity appears to be directly hemoligomerized by increasing levels of Bcl-2 that acts directly on the mitochondrial outer membrane and plays a critical role in mitochondrial outer membrane permeability. Moreover, increased Bcl-2 following T adaptation inhibits the Bax/Bcl-2 ratio. This, subsequently, alters the mitochondrial membrane potential and release of cytochrome-C and Smac/DIABLO, which eventually inhibits caspase-9. However, the major role of mitochondria in inhibiting apoptosis following T is associated with inhibition of cytochrome-C release into cytosol, which leads to increased mitochondrial membrane potential. This potential is essential for the production of ATP and the maintenance of cellular homeostasis. Finally, a decrease in cytochrome-C inhibits apoptosis by decreasing caspase-9 production and induces proteolytic inhibition of effector caspases (26). In addition to exercise activities, the role of medicinal plants in reducing oxidative stress has been investigated in various studies (13, 15, 27, 28).

The results of the present study showed that eight weeks of CS consumption significantly decreased caspase-3 and cytochrome-C in the heart tissues of rats poisoned with H2O2. In addition, consumption of 1000 mg/kg CS had a greater effect on the decrease of caspase-3 and cytochrome-C compared to 500 mg/kg CS consumption. These findings suggest dose-dependent effects of CS, which is known as a medicinal plant with many properties. Consistent with the findings of the present study, the heated extract of coriander leaves significantly reduced the amount of oxidative stress-related factors in the kidney tissue of mice (27). CSs have also been reported to be rich in phenolic compounds with antioxidant properties and CS consumption can be effective in reducing the levels of oxidative stress (28). Various studies have reported that anti-toxic effects of coriander can be due to its phenolic compounds and antioxidants (29). Phenol contained in coriander can reduce H2O2 production and prevent oxidative stress (29).

The results of our study also demonstrated that T along with CS consumption had an interactive effect on decrease of caspase-3 and cytochrome-C in the heart tissues of rats poisoned with H2O2. In this regard, T and 1000 mg/kg CS consumption together had a greater effect on the decrease of caspase-3 and cytochrome-C compared to simultaneous T and 500 mg/kg CS consumption. Lack of sufficient information on the effect of T and CS consumption on caspase-3 and cytochrome-C in the heart tissues in H2O2 toxicity status and lack of access to cell death assay methods appear to be limitations of the present research. Therefore, it is suggested in future studies to investigate the effect of T with different intensities along with CS consumption on apoptosis indices and also to use hematoxylin-eosin (H&E) and tunnel techniques.

4.1. Conclusions

Considering the results of the present study, it appears that in the context of H2O2 poisoning, caspase-3 and cytochrome-C increase in heart tissues of rats. However, T and CS consumption, both together and alone, can prevent an increase incaspase-3 and cytochrome-C in heart tissues of rats poisoned with H2O2. Moreover, effects on CS consumption can be dose-dependent.

Acknowledgements

References

  • 1.

    Dasuri K, Zhang L, Keller JN. Oxidative stress, neurodegeneration, and the balance of protein degradation and protein synthesis. Free Radic Biol Med. 2013;62:170-85. [PubMed ID: 23000246]. https://doi.org/10.1016/j.freeradbiomed.2012.09.016.

  • 2.

    Pena-Bautista C, Baquero M, Vento M, Chafer-Pericas C. Free radicals in Alzheimer's disease: Lipid peroxidation biomarkers. Clin Chim Acta. 2019;491:85-90. [PubMed ID: 30685358]. https://doi.org/10.1016/j.cca.2019.01.021.

  • 3.

    Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem. 2017;86:715-48. [PubMed ID: 28441057]. https://doi.org/10.1146/annurev-biochem-061516-045037.

  • 4.

    Huang CJ, Webb HE, Zourdos MC, Acevedo EO. Cardiovascular reactivity, stress, and physical activity. Front Physiol. 2013;4:314. [PubMed ID: 24223557]. [PubMed Central ID: PMC3819592]. https://doi.org/10.3389/fphys.2013.00314.

  • 5.

    Streck EL, Goncalves CL, Furlanetto CB, Scaini G, Dal-Pizzol F, Quevedo J. Mitochondria and the central nervous system: Searching for a pathophysiological basis of psychiatric disorders. Braz J Psychiatry. 2014;36(2):156-67. [PubMed ID: 24845118]. https://doi.org/10.1590/1516-4446-2013-1224.

  • 6.

    Yagami T, Yamamoto Y, Koma H. Pathophysiological roles of intracellular proteases in neuronal development and neurological diseases. Mol Neurobiol. 2019;56(5):3090-112. [PubMed ID: 30097848]. https://doi.org/10.1007/s12035-018-1277-4.

  • 7.

    Redza-Dutordoir M, Averill-Bates DA. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta. 2016;1863(12):2977-92. [PubMed ID: 27646922]. https://doi.org/10.1016/j.bbamcr.2016.09.012.

  • 8.

    Oh Y, Ahn CB, Nam KH, Kim YK, Yoon NY, Je JY. Amino acid composition, antioxidant, and cytoprotective effect of blue mussel (Mytilus edulis) hydrolysate through the inhibition of caspase-3 activation in oxidative stress-mediated endothelial cell injury. Mar Drugs. 2019;17(2):135. [PubMed ID: 30823522]. [PubMed Central ID: PMC6409750]. https://doi.org/10.3390/md17020135.

  • 9.

    Melo KP, Silva CM, Almeida MF, Chaves RS, Marcourakis T, Cardoso SM, et al. Mild exercise differently affects proteostasis and oxidative stress on motor areas during neurodegeneration: A comparative study of three treadmill running protocols. Neurotox Res. 2019;35(2):410-20. [PubMed ID: 30276717]. https://doi.org/10.1007/s12640-018-9966-3.

  • 10.

    McAllister MJ, Basham SA, Waldman HS, Smith JW, Mettler JA, Butawan MB, et al. Effects of psychological stress during exercise on markers of oxidative stress in young healthy, trained men. Physiol Behav. 2019;198:90-5. [PubMed ID: 30342058]. https://doi.org/10.1016/j.physbeh.2018.10.013.

  • 11.

    Bloomer RJ, Davis PG, Consitt LA, Wideman L. Plasma protein carbonyl response to increasing exercise duration in aerobically trained men and women. Int J Sports Med. 2007;28(1):21-5. [PubMed ID: 17024638]. https://doi.org/10.1055/s-2006-924140.

  • 12.

    Chen Y, Zhang G, Liu H, Qu J. Confining free radicals in close vicinity to contaminants enables ultrafast fenton-like processes in the interspacing of MoS2 membranes. Angew Chem Int Ed Engl. 2019;58(24):8134-8. [PubMed ID: 31020744]. https://doi.org/10.1002/anie.201903531.

  • 13.

    Abdelkader MAI, Gendy ASH, Bardisi IA, Elakkad HA. The impact of NPK fertilization level and Lithovit concentration on productivity and active ingredients of Coriandrum sativum plants. Middle East J Appl Sci. 2018;8(3):827-36.

  • 14.

    Salamon I, Kryvtsova M, Bucko D, Tarawneh AH. Chemical characterization and antimicrobial activity of some essential oils after their industrial large-scale distillation. J Microbiol Biotechnol Food Sci. 2019;8(4):984-8. https://doi.org/10.15414/jmbfs.2019.8.4.984-988.

  • 15.

    Caputo L, Souza LF, Alloisio S, Cornara L, De Feo V. Coriandrum sativum and lavandula angustifolia essential oils: Chemical composition and activity on central nervous system. Int J Mol Sci. 2016;17(12):1999. [PubMed ID: 27916876]. [PubMed Central ID: PMC5187799]. https://doi.org/10.3390/ijms17121999.

  • 16.

    Dos Santos MDV, De Carvalho Neto MF, De Melo ACGR, Takahashi JA, Ferraz VP, Chagas EA, et al. Chemical composition of essential oil of Coriander seeds (Coriandrum sativum) cultivated in the Amazon Savannah, Brazil. Chem Eng Transac. 2019;75:409-14.

  • 17.

    De Melo ACGR, Dos Santos MDV, De Carvalho Neto MF, Takahashi JA, Ferraz VP, Chagas EA, et al. Phytochemical trial and bioactivity of the essential oil from Coriander leaves (Coriandrum sativum) on pathogenic microorganisms. Chem Eng Transac. 2019;75:403-8.

  • 18.

    Velaga MK, Yallapragada PR, Williams D, Rajanna S, Bettaiya R. Hydroalcoholic seed extract of Coriandrum sativum (Coriander) alleviates lead-induced oxidative stress in different regions of rat brain. Biol Trace Elem Res. 2014;159(1-3):351-63. [PubMed ID: 24793421]. https://doi.org/10.1007/s12011-014-9989-4.

  • 19.

    Radak Z, Sasvari M, Nyakas C, Pucsok J, Nakamoto H, Goto S. Exercise preconditioning against hydrogen peroxide-induced oxidative damage in proteins of rat myocardium. Arch Biochem Biophys. 2000;376(2):248-51. [PubMed ID: 10775409]. https://doi.org/10.1006/abbi.2000.1719.

  • 20.

    Heidari B, Sajjadi SE, Minaiyan M. Effect of Coriandrum sativum hydroalcoholic extract and its essential oil on acetic acid- induced acute colitis in rats. Avicenna J Phytomed. 2016;6(2):205-14. [PubMed ID: 27222834]. [PubMed Central ID: PMC4877963].

  • 21.

    Husain K, Hazelrigg SR. Oxidative injury due to chronic nitric oxide synthase inhibition in rat: Effect of regular exercise on the heart. Biochim Biophys Acta. 2002;1587(1):75-82. [PubMed ID: 12009427]. https://doi.org/10.1016/s0925-4439(02)00070-4.

  • 22.

    Bader R, Ibrahim JN, Moussa M, Mourad A, Azoury J, Azoury J, et al. In vitro effect of autologous platelet-rich plasma on H2 O2 -induced oxidative stress in human spermatozoa. Andrology. 2020;8(1):191-200. [PubMed ID: 31079423]. https://doi.org/10.1111/andr.12648.

  • 23.

    Pirooz M, Azarbayjani MA, Hosseini SA, Peeri M. [The simultaneous effect of regular exercise and vitamin d on apoptosis level and antioxidant enzymes of heart tissue of male rats exposed to oxygenated water]. J Knowledge Health. 2018;13(2):29-42. Persian.

  • 24.

    Vezzoli A, Mrakic-Sposta S, Montorsi M, Porcelli S, Vago P, Cereda F, et al. Moderate intensity resistive training reduces oxidative stress and improves muscle mass and function in older individuals. Antioxidants (Basel). 2019;8(10):431. [PubMed ID: 31561586]. [PubMed Central ID: PMC6826968]. https://doi.org/10.3390/antiox8100431.

  • 25.

    Gouraud E, Charrin E, Dube JJ, Ofori-Acquah SF, Martin C, Skinner S, et al. Effects of individualized treadmill endurance training on oxidative stress in skeletal muscles of transgenic sickle mice. Oxid Med Cell Longev. 2019;2019:3765643. [PubMed ID: 31428225]. [PubMed Central ID: PMC6681588]. https://doi.org/10.1155/2019/3765643.

  • 26.

    Ghajari H, Hosseini SA, Farsi S. The effect of endurance training along with cadmium consumption on bcl-2 and bax gene expressions in heart tissue of rats. Annu Mil Health Sci Res. 2019;17(1). e86795. https://doi.org/10.5812/amh.86795.

  • 27.

    Nishio R, Tamano H, Morioka H, Takeuchi A, Takeda A. Intake of heated leaf extract of Coriandrum sativum contributes to resistance to oxidative stress via decreases in heavy metal concentrations in the kidney. Plant Foods Hum Nutr. 2019;74(2):204-9. [PubMed ID: 30783906]. https://doi.org/10.1007/s11130-019-00720-2.

  • 28.

    Hameed S, Imran A, Nisa M, Arshad MS, Saeed F, Arshad MU, et al. Characterization of extracted phenolics from black cumin (Nigella sativa linn), coriander seed (Coriandrum sativum L.), and fenugreek seed (Trigonella foenum-graecum). International Journal of Food Properties. 2019;22(1):714-26. https://doi.org/10.1080/10942912.2019.1599390.

  • 29.

    Jayakumar R, Kanthimathi MS. Dietary spices protect against hydrogen peroxide-induced DNA damage and inhibit nicotine-induced cancer cell migration. Food Chem. 2012;134(3):1580-4. [PubMed ID: 25005983]. https://doi.org/10.1016/j.foodchem.2012.03.101.