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Lotf, F., Ziamajidi, N., Abbasalipourkabir, R., Taghi Goodarzi, M., & Soleimani Asl, S. (2021). Impacts of garlic extract on testicular oxidative stress and sperm characteristics in type 1 and 2 diabetic rats: An experimental study. International Journal of Reproductive BioMedicine (IJRM), 19(10), 929-942. https://doi.org/10.18502/ijrm.v19i10.9825
https://doi.org/10.18502/ijrm.v19i10.9825
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- Cited by 2 articles
authors
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Fatemeh Lotf
Fatemeh Lotf
Department of Clinical Biochemistry, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran.
-
Nasrin Ziamajidi
Nasrin Ziamajidi
Department of Clinical Biochemistry, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran.
-
Roghayeh Abbasalipourkabir
Roghayeh Abbasalipourkabir
Department of Clinical Biochemistry, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran.
-
Mohammad Taghi Goodarzi
Mohammad Taghi Goodarzi
Molecular Medicine Research Center, Hamadan University of Medical Sciences, Hamadan, Iran.
-
Sara Soleimani Asl
Sara Soleimani Asl
Department of Anatomy, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran.
Published Date
- Nov 4, 2021
Impacts of garlic extract on testicular oxidative stress and sperm characteristics in type 1 and 2 diabetic rats: An experimental study
Abstract
Background: Hyperglycemia damages various tissues such as the testes through oxidative stress and inflammation, which can eventually lead to infertility.
Objective: Garlic extract effects on the testicular tissue of diabetic rats were investigated.
Materials and Methods: In this experimental study, 36 male Wistar rats (8-wk old, weighing 230-300 gr) were randomly divided into 6 groups (n = 6/each) including; C: control rats, G: received 0.4 gr of garlic extract/100 gr body weight, D1: Streptozotocin-induced-diabetic rats or type 1, D1+G: D1 rats that were treated with garlic, D2: Streptozotocin + nicotinamide-induced-diabetic rats or type 2, D2+G: D2 rats treated with garlic. At the end of the study, serum testosterone was assayed by ELISA. Also, sperm quality and quantity were evaluated. For determination of oxidative stress status, total antioxidant capacity, total oxidative status, lipid peroxidation, and thiol groups were assayed in the testis tissues of the rats by colorimetric methods. Also, inducible nitric oxide synthase (iNOS) gene expression and the protein level of interleukin-1-1β (IL-1β) were determined by quantitative real-time polymerase chain reaction and enzyme-linked immunosorbent assay, respectively.
Results: In diabetic rats, glucose, total oxidative status and lipid peroxidation, iNOS gene expression, and IL-1β were higher than in non-diabetic rats, whereas testosterone, total antioxidant capacity and thiol groups, and sperm quality were significantly lower compared with control rats. These alterations were normalized by garlic intervention.
Conclusion: In diabetic rats, garlic was associated with reduced glucose, oxidative stress, IL-1β, and iNOS gene expression and increased testosterone and sperm quality. So, the results suggest that garlic can reduce the severity of damage in testicular tissues of diabetic rats through its hypoglycemic, antioxidant, and anti-inflammatory properties.
Key words: Diabetes mellitus, Garlic, Oxidative stress, Inflammation, Testis.
References
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[5] Choudhury H, Pandey M, Hua CK, Mun CS, Jing JK, Kong L, et al. An update on natural compounds in the remedy of diabetes mellitus: A systematic review. J Trad Complement Med 2018; 8: 361–376.
[6] Bayan L, Koulivand PH, Gorji A. Garlic: A review of potential therapeutic effects. Avicenna J Phytomed 2014; 4: 1–14.
[7] Wang J, Zhu H, Lin S, Wang K, Wang H, Liu Z. Protective effect of naringenin against cadmium-induced testicular toxicity in male SD rats. J Inorgan Biochem 2020; 214: 111310.
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[10] Kielkopf CL, Bauer W, Urbatsch IL. Bradford assay for determining protein concentration. Cold Spring Harb Protoc 2020; 2020: 136–138.
[11] Benzie IFF, Devaki M. The ferric reducing/antioxidant power (FRAP) assay for non−enzymatic antioxidant capacity: Concepts, procedures, limitations and applications. Measurement of Antioxidant Activity & Capacity 2018: 77–106.
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[13] Kurokawa Y, Takamura N, Matsuoka C, Imazawa T, Matsushima Y, Onodera H, et al. Comparative studies on lipid peroxidation in the kidney of rats, mice, and hamsters and on the effect of cysteine, glutathione, and diethyl maleate treatment on mortality and nephrotoxicity after administration of potassium bromate. J Am College Toxicol 1987; 6: 489–501.
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[15] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔCT method. Methods 2001; 25: 402–408.
[16] Abey NO, Ebuehi OAT. Semen analysis and morphological study of two subsequent generations of dietary protein deficient sprague dawley rats. Int Ann Sci 2020; 10: 85– 91.
[17] Mahmoud ARH, Shalaby NMM. Ameliorative effect of zinc oxide nanoparticles on nicotine induced testicular dysfunction; Biochemical and histological study. J Toxicol Environ Health Sci 2019; 11: 104–113.
[18] Roy S, Rahaman N, Ahmed F, Metya S, Sannigrahi S. Naringenin attenuates testicular damage, germ cell death and oxidative stress in streptozotocin induced diabetic rats: Naringenin prevents diabetic rat testicular damage. J Appl Biomed 2013; 11: 195–208.
[19] Nna VU, Bakar A, Bahiyah A, Ahmad A, Eleazu CO, Mohamed M. Oxidative stress, NF-κb-mediated inflammation and apoptosis in the testes of streptozotocininduced diabetic rats: Combined protective effects of malaysian propolis and metformin. Antioxidants 2019; 8: 465–487.
[20] Asadi N, Bahmani M, Kheradmand A, Rafieian-Kopaei M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: A review. J Clin Diagn Res 2017; 11: IE01–IE5.
[21] Li C, Miao X, Li F, Wang S, Liu Q, Wang Y, et al. Oxidative stress-related mechanisms and antioxidant therapy in diabetic retinopathy. Oxid Med Cell Longev 2017; 2017: 1– 15.
[22] Zhou Y, Olatunji OJ, Chen H. Ameliorative effects of Lycium chinensis on male sexual dysfunction and testicular oxidative damage in streptozotocin-induced diabetic rats. Food Sci Biotechnol 2019; 28: 1217–1223.
[23] Jaiballah ZA, Lji NM, Alamyel FB. Effect of Moringa oleifera extract on some sperm parameters and testis in diabetic rats. J Pure Appl Sci 2020; 19: 18–22.
[24] Ola-Mudathir KF, Suru SM, Fafunso MA, Obioha UE, Faremi TY. Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food Chem Toxicol 2008; 46: 3604–3611.
[25] Kaur G, Padiya R, Adela R, Putcha UK, Reddy G, Reddy B, et al. Garlic and resveratrol attenuate diabetic complications, loss of β-cells, pancreatic and hepatic oxidative stress in streptozotocin-induced diabetic rats. Front Pharmacol 2016; 7: 1–15.
[26] Hfaiedh N, Murat JC, Elfeki A. Compared ability of garlic (Allium sativum) extract or α−tocopherol+ magnesium association to reduce metabolic disorders and oxidative stress in diabetic rats. Phytother Res 2011; 25: 821–827.
[27] El-Demerdash F, Yousef MI, El-Naga NA. Biochemical study on the hypoglycemic effects of onion and garlic in alloxan-induced diabetic rats. Food Chem Toxicol 2005; 43: 57–63.
[28] Thomson M, Al-Amin ZM, Al-Qattan KK, Shaban LH, Ali M. Anti-diabetic and hypolipidaemic properties of garlic (Allium sativum) in streptozotocin-induced diabetic rats. Int J Diabetes Metab 2007; 15: 108–115.
[29] Sayem ASM, Arya A, Karimian H, Krishnasamy N, Ashok Hasamnis A, Hossain CF. Action of phytochemicals on insulin signaling pathways accelerating glucose transporter (GLUT4) protein translocation. Molecules 2018; 23: 258–272.
[30] Sajadi E, Dadras S, Bayat M, Abdi S, Nazarian H, Ziaeipour S, et al. Impaired spermatogenesis associated with changes in spatial arrangement of Sertoli and spermatogonial cells following induced diabetes. J Cell Bioche 2019; 120: 17312–17325.
[31] Ballester J, Muñoz MC, Domínguez J, Rigau T, Guinovart JJ, Rodríguez−Gil JE. Insulin−dependent diabetes affects testicular function by FSH−and LH−linked mechanisms. J Androl 2004; 25: 706–719.
[32] Gautam D, Misro M, Chaki S, Sehgal N. H2O2 at physiological concentrations modulates Leydig cell function inducing oxidative stress and apoptosis. Apoptosis 2006; 11: 39–46.
[33] Al-brakati AY. Protective effect of garlic against diabetic retinopathy in adult albino rats. Res J Pharm Biol Chem Sci 2016; 7: 2748–2749.
[34] Anwar MM, Meki ARM. Oxidative stress in streptozotocin-induced diabetic rats: Effects of garlic oil and melatonin. Comparat Biochem Physiol Part A 2003; 135: 539–547.
[35] Bayan L, Koulivand PH, Gorji A. Garlic: A review of potential therapeutic effects. Avicenna J Phytomed 2014; 4: 1–14.
[36] Drobiova H, Thomson M, Al-Qattan K, Peltonen-Shalaby R, Al-Amin Z, Ali M. Garlic increases antioxidant levels in diabetic and hypertensive rats determined by a modified peroxidase method. Evid Based Complement Alternat Med 2011; 2011: 1–8.
[37] Cao L, Leers-Sucheta S, Azhar S. Aging alters the functional expression of enzymatic and non-enzymatic anti-oxidant defense systems in testicular rat Leydig cells. J Steroid Biochem Mol Biol 2004; 88: 61–67.
[38] Sönmez MF, Kiliç E, Karabulut D, Çilenk K, Deligönül E, Dündar M. Nitric oxide synthase in diabetic rat testicular tissue and the effects of pentoxifylline therapy. Syst Biol Reprod Med 2016; 62: 22–30.
[39] Tirmenstein M, Nicholls-Grzemski F, Schmittgen T, Zakrajsek B, Fariss M. Glutathione-dependent regulation of nitric oxide production in isolated rat hepatocyte suspensions. Antioxid Redox Signal 2000; 2: 767–777.
[40] Arivazhagan S, Balasenthil S, Nagini S. Garlic and neem leaf extracts enhance hepatic glutathione and glutathione dependent enzymes during N−methyl−N’−nitro−N−nitrosoguanidine (MNNG)−induced gastric carcinogenesis in rats. Phytother Res 2000; 14: 291–293.
[41] Liu T, Zhang L, Joo D, Sun SC. NF-κB signaling in inflammation. Signal Transduct Target Ther 2017; 2: 1–9.
[2] Alves MG, Martins AD, Cavaco JE, Socorro S, Oliveira PF. Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function. Tissue Barriers 2013; 1: e23992.
[3] Maresch CC, Stute DC, Alves MG, Oliveira PF, de Kretser DM, Linn T. Diabetes-induced hyperglycemia impairs male reproductive function: A systematic review. Hum Reprod Update 2018; 24: 86–105.
[4] Lingappan K. NF-κB in oxidative stress. Curr Opin Toxicol 2018; 7: 81–86.
[5] Choudhury H, Pandey M, Hua CK, Mun CS, Jing JK, Kong L, et al. An update on natural compounds in the remedy of diabetes mellitus: A systematic review. J Trad Complement Med 2018; 8: 361–376.
[6] Bayan L, Koulivand PH, Gorji A. Garlic: A review of potential therapeutic effects. Avicenna J Phytomed 2014; 4: 1–14.
[7] Wang J, Zhu H, Lin S, Wang K, Wang H, Liu Z. Protective effect of naringenin against cadmium-induced testicular toxicity in male SD rats. J Inorgan Biochem 2020; 214: 111310.
[8] Hakemi SG, Sharififar F, Haghpanah T, Babaee A, EftekharVaghefi SH. The effects of olive leaf extract on the testis, sperm quality and testicular germ cell apoptosis in male rats exposed to busulfan. Int J Fertil Steril 2019; 13: 57.
[9] Oguntibeju OO, Aboua Y, Kachepe P. Possible therapeutic effects of vindoline on testicular and epididymal function in diabetes-induced oxidative stress male Wistar rats. Heliyon 2020; 6: e03817–e3826.
[10] Kielkopf CL, Bauer W, Urbatsch IL. Bradford assay for determining protein concentration. Cold Spring Harb Protoc 2020; 2020: 136–138.
[11] Benzie IFF, Devaki M. The ferric reducing/antioxidant power (FRAP) assay for non−enzymatic antioxidant capacity: Concepts, procedures, limitations and applications. Measurement of Antioxidant Activity & Capacity 2018: 77–106.
[12] Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem 2005; 38: 1103–1111.
[13] Kurokawa Y, Takamura N, Matsuoka C, Imazawa T, Matsushima Y, Onodera H, et al. Comparative studies on lipid peroxidation in the kidney of rats, mice, and hamsters and on the effect of cysteine, glutathione, and diethyl maleate treatment on mortality and nephrotoxicity after administration of potassium bromate. J Am College Toxicol 1987; 6: 489–501.
[14] Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968; 25: 192–205.
[15] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 −ΔΔCT method. Methods 2001; 25: 402–408.
[16] Abey NO, Ebuehi OAT. Semen analysis and morphological study of two subsequent generations of dietary protein deficient sprague dawley rats. Int Ann Sci 2020; 10: 85– 91.
[17] Mahmoud ARH, Shalaby NMM. Ameliorative effect of zinc oxide nanoparticles on nicotine induced testicular dysfunction; Biochemical and histological study. J Toxicol Environ Health Sci 2019; 11: 104–113.
[18] Roy S, Rahaman N, Ahmed F, Metya S, Sannigrahi S. Naringenin attenuates testicular damage, germ cell death and oxidative stress in streptozotocin induced diabetic rats: Naringenin prevents diabetic rat testicular damage. J Appl Biomed 2013; 11: 195–208.
[19] Nna VU, Bakar A, Bahiyah A, Ahmad A, Eleazu CO, Mohamed M. Oxidative stress, NF-κb-mediated inflammation and apoptosis in the testes of streptozotocininduced diabetic rats: Combined protective effects of malaysian propolis and metformin. Antioxidants 2019; 8: 465–487.
[20] Asadi N, Bahmani M, Kheradmand A, Rafieian-Kopaei M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: A review. J Clin Diagn Res 2017; 11: IE01–IE5.
[21] Li C, Miao X, Li F, Wang S, Liu Q, Wang Y, et al. Oxidative stress-related mechanisms and antioxidant therapy in diabetic retinopathy. Oxid Med Cell Longev 2017; 2017: 1– 15.
[22] Zhou Y, Olatunji OJ, Chen H. Ameliorative effects of Lycium chinensis on male sexual dysfunction and testicular oxidative damage in streptozotocin-induced diabetic rats. Food Sci Biotechnol 2019; 28: 1217–1223.
[23] Jaiballah ZA, Lji NM, Alamyel FB. Effect of Moringa oleifera extract on some sperm parameters and testis in diabetic rats. J Pure Appl Sci 2020; 19: 18–22.
[24] Ola-Mudathir KF, Suru SM, Fafunso MA, Obioha UE, Faremi TY. Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food Chem Toxicol 2008; 46: 3604–3611.
[25] Kaur G, Padiya R, Adela R, Putcha UK, Reddy G, Reddy B, et al. Garlic and resveratrol attenuate diabetic complications, loss of β-cells, pancreatic and hepatic oxidative stress in streptozotocin-induced diabetic rats. Front Pharmacol 2016; 7: 1–15.
[26] Hfaiedh N, Murat JC, Elfeki A. Compared ability of garlic (Allium sativum) extract or α−tocopherol+ magnesium association to reduce metabolic disorders and oxidative stress in diabetic rats. Phytother Res 2011; 25: 821–827.
[27] El-Demerdash F, Yousef MI, El-Naga NA. Biochemical study on the hypoglycemic effects of onion and garlic in alloxan-induced diabetic rats. Food Chem Toxicol 2005; 43: 57–63.
[28] Thomson M, Al-Amin ZM, Al-Qattan KK, Shaban LH, Ali M. Anti-diabetic and hypolipidaemic properties of garlic (Allium sativum) in streptozotocin-induced diabetic rats. Int J Diabetes Metab 2007; 15: 108–115.
[29] Sayem ASM, Arya A, Karimian H, Krishnasamy N, Ashok Hasamnis A, Hossain CF. Action of phytochemicals on insulin signaling pathways accelerating glucose transporter (GLUT4) protein translocation. Molecules 2018; 23: 258–272.
[30] Sajadi E, Dadras S, Bayat M, Abdi S, Nazarian H, Ziaeipour S, et al. Impaired spermatogenesis associated with changes in spatial arrangement of Sertoli and spermatogonial cells following induced diabetes. J Cell Bioche 2019; 120: 17312–17325.
[31] Ballester J, Muñoz MC, Domínguez J, Rigau T, Guinovart JJ, Rodríguez−Gil JE. Insulin−dependent diabetes affects testicular function by FSH−and LH−linked mechanisms. J Androl 2004; 25: 706–719.
[32] Gautam D, Misro M, Chaki S, Sehgal N. H2O2 at physiological concentrations modulates Leydig cell function inducing oxidative stress and apoptosis. Apoptosis 2006; 11: 39–46.
[33] Al-brakati AY. Protective effect of garlic against diabetic retinopathy in adult albino rats. Res J Pharm Biol Chem Sci 2016; 7: 2748–2749.
[34] Anwar MM, Meki ARM. Oxidative stress in streptozotocin-induced diabetic rats: Effects of garlic oil and melatonin. Comparat Biochem Physiol Part A 2003; 135: 539–547.
[35] Bayan L, Koulivand PH, Gorji A. Garlic: A review of potential therapeutic effects. Avicenna J Phytomed 2014; 4: 1–14.
[36] Drobiova H, Thomson M, Al-Qattan K, Peltonen-Shalaby R, Al-Amin Z, Ali M. Garlic increases antioxidant levels in diabetic and hypertensive rats determined by a modified peroxidase method. Evid Based Complement Alternat Med 2011; 2011: 1–8.
[37] Cao L, Leers-Sucheta S, Azhar S. Aging alters the functional expression of enzymatic and non-enzymatic anti-oxidant defense systems in testicular rat Leydig cells. J Steroid Biochem Mol Biol 2004; 88: 61–67.
[38] Sönmez MF, Kiliç E, Karabulut D, Çilenk K, Deligönül E, Dündar M. Nitric oxide synthase in diabetic rat testicular tissue and the effects of pentoxifylline therapy. Syst Biol Reprod Med 2016; 62: 22–30.
[39] Tirmenstein M, Nicholls-Grzemski F, Schmittgen T, Zakrajsek B, Fariss M. Glutathione-dependent regulation of nitric oxide production in isolated rat hepatocyte suspensions. Antioxid Redox Signal 2000; 2: 767–777.
[40] Arivazhagan S, Balasenthil S, Nagini S. Garlic and neem leaf extracts enhance hepatic glutathione and glutathione dependent enzymes during N−methyl−N’−nitro−N−nitrosoguanidine (MNNG)−induced gastric carcinogenesis in rats. Phytother Res 2000; 14: 291–293.
[41] Liu T, Zhang L, Joo D, Sun SC. NF-κB signaling in inflammation. Signal Transduct Target Ther 2017; 2: 1–9.