Toxic Effects of Chronic Exposure to High-Fat Diet and Arsenic on the Reproductive System of the Male Mouse
,
Abstract
Objective: Obesity is associated with reproductive disorders. Arsenic disrupts male reproduction by direct effects on the male gonads or androgens secretion. So, the present study was conducted to evaluate the toxic effects of chronic concomitant administration of high-fat diet (HF) and arsenic on the reproductive system of the male mouse.
Materials and methods: In this experimental study, 72 adult male mice were randomly divided into 6 groups: low-fat diet (LF0), LF+arsenic 25 ppm, LF+arsenic 50ppm, HF0, HF+arsenic 25 ppm and, HF+arsenic 50 ppm. 24 hours after the last experimental day, plasma samples, the cauda of epididymis and testis were prepared and removed for hormonal, sperm count and histopathological assessments.
Results: Testis weight and volume increased in HF0 than other groups except for LF0. Plasma LH and testosterone levels decreased in LF50, HF0, HF25, and HF50 compared to LF0. A similar effect was observed in plasma FSH levels of HF0, HF25 and HF50 groups compared with LF0. Plasma level of estradiol increased in LF50 versus to other groups. Testosterone to estradiol ratio and sperm count decreased in all groups compared to LF0. Reduced interstitial cells and large numbers of vacuoles were observed in germinal epithelium of HF0 group, that these changes were more intense in both concentrations of arsenic-treated mice.
Conclusion: Present study indicated that chronic exposure to HF and arsenic-induced hypogonadotropic hypogonadism concomitant with sperm count reduction and testicular damage.
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2. Campos-Silva P, Furriel A, Costa WS, Sampaio FJ, Gregório BM. Metabolic and testicular effects of the long-term administration of different high-fat diets in adult rats. Int Braz J Urol 2015; 41: 569-75.
3. Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U. Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol reprod 2010; 82: 96-104.
4. Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT. Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril 2008; 90: 897-904.
5. Olivares A, Méndez JP, Zambrano E, Cárdenas M, Tovar A, Perera-Marín G, et al. Reproductive axis function and gonadotropin microheterogeneity in a male rat model of diet-induced obesity. Gen Comp Endocrinol 2010; 166: 356-64.
6. Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, et al. Selenium-enriched probiotics improves murine male fertility compromised by high fat diet. Biol Trace Elem Res 2012; 147:251-60.
7. Reddy MVB, Sudheer SD, Sasikala P, Reddy PS, Reddy SH, Karthik A. Transplacental and Lactational Exposure of Mice to Arsenic: Effect on Body and Organ Weights with Special Reference to Male Reproductive Organs. J Rep Infert 2012; 3: 17-21.
8. Pant N, Kumar R, Murthy RC, Srivastava SP. Male reproductive effect of arsenic in mice. Biometals 2001; 14: 113-7.
9. Jahan S, Rehman S, Ullah H, Munawar A, Ain QU, Iqbal T. Ameliorative effect of quercetin against arsenic-induced sperm DNA damage and daily sperm production in adult male rats. Drug chem toxicol 2016; 39: 290-6.
10. Pizent A, Tariba B, Živković T. Reproductive toxicity of metals in men. Arh Hig Rada Toksikol 2012; 63 Suppl 1: 35-45.
11. Ning Y, Xu M, Cao X, Chen X, Luo X. Inactivation of AKT, ERK and NF-kappaB by genistein derivative, 7-difluoromethoxyl-5,4'-di-n-octylygenistein, reduces ovarian carcinoma oncogenicity. Oncol Rep 2017; 38: 949-58.
12. Afolabi OK, Wusu AD, Ogunrinola OO, Abam EO, Babayemi DO, Dosumu OA, et al. Arsenic-induced dyslipidemia in male albino rats: comparison between trivalent and pentavalent inorganic arsenic in drinking water. BMC Pharmacology and Toxicology 2015;
16: 15.
13. Ahangarpour A, Alboghobeish S, Rezaei M, Khodayar MJ, Oroojan AA, Zainvand M. Evaluation of diabetogenic mechanism of high fat diet in combination with Arsenic exposure in male mice. Iran J Pharm Res 2018; 17: 164-83.
14. Ahangarpour A, Alboghobeish S, Oroojan AA, Zeidooni L, Samimi A, Afshari G. Effects of Combined Exposure to Chronic High-Fat Diet and Arsenic on Thyroid Function and Lipid Profile in Male Mouse. Biol Trace Elem Res 2018; 182: 37-48.
15. Paul DS, Walton FS, Saunders RJ, Stýblo M. Characterization of the impaired glucose homeostasis produced in C57BL/6 mice by chronic exposure to arsenic and high-fat diet. Environ Health Perspect 2011; 119: 1104-9.
16. Han Y, Liang C, Manthari RK, Yu Y, Gao Y, Liu Y,
et al. Arsenic influences spermatogenesis by disorganizing the elongation of spermatids in adult male mice. Chemosphere 2020; 238: 124650.
17. Ahangarpour A, Oroojan A, Aliakbari FR. Effects of C-peptide and nicotinamide on serum LH, FSH, testosterone levels and sperm count in nicotinamide/streptozotocin-induced-diabetes in mice. Acta Endocrinologica 2014; 10: 588-94.
18. Ahangarpour A, Oroojan AA, Radan M. Effect of aqueous and hydro-alcoholic extracts of lettuce (Lactuca sativa) seed on testosterone level and spermatogenesis in NMRI mice. Iran J Reprod Med 2014; 12: 65-72.
19. Khorsandi LS, Hashemitabar M, Orazizadeh M, Albughobeish N. Dexamethasone effects on fas ligand expression in mouse testicular germ cells. Pak J Biol Sci 2008; 11: 2231-6.
20. Orazizadeh M, Khorsandi L, Absalan F, Hashemitabar M, Daneshi E. Effect of beta-carotene on titanium oxide nanoparticles-induced testicular toxicity in mice. J Assist Reprod Genet 2014; 31: 561-8.
21. Khorsandi L, Orazizadeh M, Mansouri E, Hemadi M, Moradi-Gharibvand N. Morphometric and stereological assessment of the effects of titanium dioxide nanoparticles on the mouse testicular tissue. Bratisl Lek Listy 2016; 117: 659-64.
22. BB, Uygur R, Caglar V, Aktas C, Aydin M, Ozen O. Protective effects of quercetin against arsenic‐induced testicular damage in rats. Andrologia 2016; 48: 1202-13.
23. Li SG, Ding YS, Niu Q, Xu SZ, Pang LJ, Ma RL, et al. Grape Seed Proanthocyanidin Extract Alleviates Arsenic-induced Oxidative Reproductive Toxicity in Male Mice. Biomed Environ Sci 2015; 28: 272-80.
24. Lenzi A, Balercia G, Bellastella A, Colao A, Fabbri A, Foresta C, et al. Epidemiology; diagnosis, and treatment of male hypogonadotropic hypogonadism. J Endocrinol Invest 2009; 32: 934-8.
25. Sakurai T, Himeno S. Endocrine disruptive effects of inorganic arsenicals. Environ Sci 2006;13:101-6.
26. Xu Y, Tokar EJ, Waalkes MP. Arsenic-induced cancer cell phenotype in human breast epithelia is estrogen receptor-independent but involves aromatase activation. Arch Toxicol 2014; 88: 263-74.
27. Cano P, Jiménez-Ortega V, Larrad A, Reyes Toso CF, Cardinali DP, Esquifino AI.Effect of a high-fat diet on 24-h pattern of circulating levels of prolactin,luteinizing hormone, testosterone, corticosterone, thyroid-stimulating hormone and glucose, and pineal melatonin content, in rats. Endocrine 2008; 33: 118-25.
28. Ibrahim MH, Selim SA, Abd-Alaleem DI, Al-sayed RM. Effect of Obestatin on Gonadal Functions in High Fat-fed Albino Rats. Basic Sciences of Medicine 2014; 3: 43-59.
29. Cabler S, Agarwal A, Flint M, Du Plessis SS. Obesity: modern man's fertility nemesis. Asian J Androl 2010; 12: 480-9.
30. Fan Y, Liu Y, Xue K, Gu G, Fan W, Xu Y, et al. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PloS one 2015; 10: e0120775.
31. Akingbemi BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol 2005; 3: 51.
32. Holdcraft RW, Braun RE. Hormonal regulation of spermatogenesis. Int J Androl 2004; 27: 335-42.
33. Kim YJ, Kim JM. Arsenic Toxicity in Male Reproduction and Development. Dev Reprod 2015; 19: 167-80.
34. Galaly SR, Hozayen WG, Amin KA, Ramadan SM. Effects of Orlistat and herbal mixture extract on brain, testes functions and oxidative stress biomarkers in a rat model of high fat diet. Beni-Suef University Journal of Basic and Applied Sciences 2014; 3: 93-105.
35. Souza ACF, Marchesi SC, Domingues de Almeida Lima G, Ferraz RP, Santos FC, da Matta SLP, et al. Effects of Sodium Arsenite and Arsenate in Testicular Histomorphometry and Antioxidants Enzymes Activities in Rats. Biol Trace Elem Res 2016; 171: 354-62.
2. Campos-Silva P, Furriel A, Costa WS, Sampaio FJ, Gregório BM. Metabolic and testicular effects of the long-term administration of different high-fat diets in adult rats. Int Braz J Urol 2015; 41: 569-75.
3. Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U. Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol reprod 2010; 82: 96-104.
4. Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT. Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril 2008; 90: 897-904.
5. Olivares A, Méndez JP, Zambrano E, Cárdenas M, Tovar A, Perera-Marín G, et al. Reproductive axis function and gonadotropin microheterogeneity in a male rat model of diet-induced obesity. Gen Comp Endocrinol 2010; 166: 356-64.
6. Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, et al. Selenium-enriched probiotics improves murine male fertility compromised by high fat diet. Biol Trace Elem Res 2012; 147:251-60.
7. Reddy MVB, Sudheer SD, Sasikala P, Reddy PS, Reddy SH, Karthik A. Transplacental and Lactational Exposure of Mice to Arsenic: Effect on Body and Organ Weights with Special Reference to Male Reproductive Organs. J Rep Infert 2012; 3: 17-21.
8. Pant N, Kumar R, Murthy RC, Srivastava SP. Male reproductive effect of arsenic in mice. Biometals 2001; 14: 113-7.
9. Jahan S, Rehman S, Ullah H, Munawar A, Ain QU, Iqbal T. Ameliorative effect of quercetin against arsenic-induced sperm DNA damage and daily sperm production in adult male rats. Drug chem toxicol 2016; 39: 290-6.
10. Pizent A, Tariba B, Živković T. Reproductive toxicity of metals in men. Arh Hig Rada Toksikol 2012; 63 Suppl 1: 35-45.
11. Ning Y, Xu M, Cao X, Chen X, Luo X. Inactivation of AKT, ERK and NF-kappaB by genistein derivative, 7-difluoromethoxyl-5,4'-di-n-octylygenistein, reduces ovarian carcinoma oncogenicity. Oncol Rep 2017; 38: 949-58.
12. Afolabi OK, Wusu AD, Ogunrinola OO, Abam EO, Babayemi DO, Dosumu OA, et al. Arsenic-induced dyslipidemia in male albino rats: comparison between trivalent and pentavalent inorganic arsenic in drinking water. BMC Pharmacology and Toxicology 2015;
16: 15.
13. Ahangarpour A, Alboghobeish S, Rezaei M, Khodayar MJ, Oroojan AA, Zainvand M. Evaluation of diabetogenic mechanism of high fat diet in combination with Arsenic exposure in male mice. Iran J Pharm Res 2018; 17: 164-83.
14. Ahangarpour A, Alboghobeish S, Oroojan AA, Zeidooni L, Samimi A, Afshari G. Effects of Combined Exposure to Chronic High-Fat Diet and Arsenic on Thyroid Function and Lipid Profile in Male Mouse. Biol Trace Elem Res 2018; 182: 37-48.
15. Paul DS, Walton FS, Saunders RJ, Stýblo M. Characterization of the impaired glucose homeostasis produced in C57BL/6 mice by chronic exposure to arsenic and high-fat diet. Environ Health Perspect 2011; 119: 1104-9.
16. Han Y, Liang C, Manthari RK, Yu Y, Gao Y, Liu Y,
et al. Arsenic influences spermatogenesis by disorganizing the elongation of spermatids in adult male mice. Chemosphere 2020; 238: 124650.
17. Ahangarpour A, Oroojan A, Aliakbari FR. Effects of C-peptide and nicotinamide on serum LH, FSH, testosterone levels and sperm count in nicotinamide/streptozotocin-induced-diabetes in mice. Acta Endocrinologica 2014; 10: 588-94.
18. Ahangarpour A, Oroojan AA, Radan M. Effect of aqueous and hydro-alcoholic extracts of lettuce (Lactuca sativa) seed on testosterone level and spermatogenesis in NMRI mice. Iran J Reprod Med 2014; 12: 65-72.
19. Khorsandi LS, Hashemitabar M, Orazizadeh M, Albughobeish N. Dexamethasone effects on fas ligand expression in mouse testicular germ cells. Pak J Biol Sci 2008; 11: 2231-6.
20. Orazizadeh M, Khorsandi L, Absalan F, Hashemitabar M, Daneshi E. Effect of beta-carotene on titanium oxide nanoparticles-induced testicular toxicity in mice. J Assist Reprod Genet 2014; 31: 561-8.
21. Khorsandi L, Orazizadeh M, Mansouri E, Hemadi M, Moradi-Gharibvand N. Morphometric and stereological assessment of the effects of titanium dioxide nanoparticles on the mouse testicular tissue. Bratisl Lek Listy 2016; 117: 659-64.
22. BB, Uygur R, Caglar V, Aktas C, Aydin M, Ozen O. Protective effects of quercetin against arsenic‐induced testicular damage in rats. Andrologia 2016; 48: 1202-13.
23. Li SG, Ding YS, Niu Q, Xu SZ, Pang LJ, Ma RL, et al. Grape Seed Proanthocyanidin Extract Alleviates Arsenic-induced Oxidative Reproductive Toxicity in Male Mice. Biomed Environ Sci 2015; 28: 272-80.
24. Lenzi A, Balercia G, Bellastella A, Colao A, Fabbri A, Foresta C, et al. Epidemiology; diagnosis, and treatment of male hypogonadotropic hypogonadism. J Endocrinol Invest 2009; 32: 934-8.
25. Sakurai T, Himeno S. Endocrine disruptive effects of inorganic arsenicals. Environ Sci 2006;13:101-6.
26. Xu Y, Tokar EJ, Waalkes MP. Arsenic-induced cancer cell phenotype in human breast epithelia is estrogen receptor-independent but involves aromatase activation. Arch Toxicol 2014; 88: 263-74.
27. Cano P, Jiménez-Ortega V, Larrad A, Reyes Toso CF, Cardinali DP, Esquifino AI.Effect of a high-fat diet on 24-h pattern of circulating levels of prolactin,luteinizing hormone, testosterone, corticosterone, thyroid-stimulating hormone and glucose, and pineal melatonin content, in rats. Endocrine 2008; 33: 118-25.
28. Ibrahim MH, Selim SA, Abd-Alaleem DI, Al-sayed RM. Effect of Obestatin on Gonadal Functions in High Fat-fed Albino Rats. Basic Sciences of Medicine 2014; 3: 43-59.
29. Cabler S, Agarwal A, Flint M, Du Plessis SS. Obesity: modern man's fertility nemesis. Asian J Androl 2010; 12: 480-9.
30. Fan Y, Liu Y, Xue K, Gu G, Fan W, Xu Y, et al. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PloS one 2015; 10: e0120775.
31. Akingbemi BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol 2005; 3: 51.
32. Holdcraft RW, Braun RE. Hormonal regulation of spermatogenesis. Int J Androl 2004; 27: 335-42.
33. Kim YJ, Kim JM. Arsenic Toxicity in Male Reproduction and Development. Dev Reprod 2015; 19: 167-80.
34. Galaly SR, Hozayen WG, Amin KA, Ramadan SM. Effects of Orlistat and herbal mixture extract on brain, testes functions and oxidative stress biomarkers in a rat model of high fat diet. Beni-Suef University Journal of Basic and Applied Sciences 2014; 3: 93-105.
35. Souza ACF, Marchesi SC, Domingues de Almeida Lima G, Ferraz RP, Santos FC, da Matta SLP, et al. Effects of Sodium Arsenite and Arsenate in Testicular Histomorphometry and Antioxidants Enzymes Activities in Rats. Biol Trace Elem Res 2016; 171: 354-62.
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| Issue | Vol 13, No 4 (December 2019) | |
| Section | Original Articles | |
| DOI | https://doi.org/10.18502/jfrh.v13i4.2645 | |
| Keywords | ||
| Arsenic High Fat Diet Gonadotropin Sperm Testis | ||
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How to Cite
1.
Ahangarpour A, Oroojan AA, Alboghobeish S, Khorsandi L, Moradi M. Toxic Effects of Chronic Exposure to High-Fat Diet and Arsenic on the Reproductive System of the Male Mouse. J Family Reprod Health. 2019;13(4):181-190.
