Fertility enhancing efficacy of Cicer arietinum in male albino mice

Amany A Sayed; Atef A. Ali; Hanan R. H. Mohamed

doi:10.14715/cmb/2018.64.4.6

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Vol. 64 No. 4: Issue 4

Issue Published : April 2, 2018

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Fertility enhancing efficacy of Cicer arietinum in male albino mice

https://doi.org/10.14715/cmb/2018.64.4.6

Amany A Sayed

Zoology Department Faculty of Science Cairo University, Giza, Egypt

Atef A. Ali

Zoology Department Faculty of Science Cairo University, Giza, Egypt

Hanan R. H. Mohamed

Zoology Department Faculty of Science Cairo University, Giza, Egypt

Corresponding Author(s) : Hanan R. H. Mohamed

hananesresm@yahoo.com

Cellular and Molecular Biology, Vol. 64 No. 4: Issue 4
Article Published : March 31, 2018

Abstract

The present study was conducted to investigate the effect of incorporating Cicer arietinum in the diet on the testicular functions of the male mice. Seventy-two mice were divided equally into four groups that were daily fed a diet containing 0, 20, 30 and 50% of C. arietinum seeds, respectively. After 7, 14 and 21 days of starting the experiments, the mice were anesthetized and euthanized to collect the blood, testes, epididymis and seminal vesicles. The present results showed that the increased percentage of C. arietinum in the diet caused significant elevations in the serum levels of testosterone and luteinizing hormone (LH), sperm concentration, sperm motility as well as the testicular levels of antioxidants including glutathione (GSH), glutathione peroxidase (GPx) and catalase (CAT), in comparison to the controls. On the other hand, marked reductions in the sperm abnormality, testicular levels of malondialdehyde (MDA), the percentage of DNA damage in tail and tail moment (TM) were observed in the mice that received a diet containing C. arietinum as compared to the controls. Both the sperms and testes of the mice fed a diet containing C. arietinum in the diet showed a normal intact appearance of the electrophoresed genomic DNA on agarose, as those of the controls. In conclusion, C. arietinum is not only a safe ingredient in the fast-food but also an enhancer of the testicular functions.

Keywords

Cicer arietinum Mice Fertility Testis Antioxidants Genetic safety.

Sayed, A. A., Ali, A. A., & Mohamed, H. R. H. (2018). Fertility enhancing efficacy of Cicer arietinum in male albino mice. Cellular and Molecular Biology, 64(4), 29–38. https://doi.org/10.14715/cmb/2018.64.4.6

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References

References
(1) Kashani HH, Faraji Z, Nikzad H, Parivar K, Sharrif M. The effect of aqueous extract of Salep prepared from root- tubers of Dactylorhiza maculate (Orchidaceae) on the testes and sexual hormones of immature male mice. J Med Plants 2012; 6:4102–4106.
(2) Hess R. A., Carnes K. The role of estrogen in testis and the male reproductive tract: a review and species comparison. Anim. Reprod. 2004; 1, 5–30
(3) Atanassova NN, Walker M, McKinnell C, Fisher JS & Sharpe RM. Evidence that androgens and oestrogens, as well as folliclestimulating hormone, can alter Sertoli cell number in the neonatal rat. Journal of Endocrinology, 2005, Vol.184, pp107–117.
(4) Akondi RB, Akula A, Challa SR. Influence of high phytoestrogen diet on rat male reproductive system. Int.Journal of Pharmacy&Technology December 2009 | Vol. 1 | Issue No.1 | 1-20
(5) Ekaluo UB1, Udoh PB, Ikpeme EV, Udensi O. Effect of soybean (Glycine max L.) on the hormonal milieu of male rats. Pak J Biol Sci. 2011 Jul 15;14(14):752-4.
(6) Harris DM, Besselink E, Henning SM, Go VL, Heber D. Phytoestrogens induce differential estrogen receptor alpha- or Beta mediated responses in transfected breast cancer cells. Exp Biol Med (Maywood) 2005; 230: 558–568.
(7) Robertson KM, O'Donnell L, Simpson ER & Jones MME. The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology, 2002, Vol.143, pp2913–2921.
(8) Modaresi M, Messripour M and Khorami H. Effect of soybean on male reproductive physiology in mice. International Conference on Life Science and Technology. vol.3 (2011) 15-18
(9) Glover A & Assinder SJ. Acute exposure of adult male rats to dietary phytoestrogens reduces fecundity and alters epididymal steroid hormone receptor expression. Journal of Endocrinology 2006 ; 189: 565–573.
(10) Sharmaa P, Parmar J, Vermaa P, Goyal P.K. Radiation induced oxidative stress and its toxicity in testes of mice and their prevention by Tinospora cordifolia extract. Journal of reproductive health and medicine 2015; 1: 64–75
(11) Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev. 2008; 1:15–24.
(12) Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction. 2001; 122:497–506.
(13) El Din, S., Batta, H., Abdul, E. and Abdul, E.F.. Effect of Soybean on Fertility of Male and Female Albino Rats. J. American Science, 2011; 7(6), 872-883.
(14) Zeriouh IF, Addou S, Bouferkas Y, Kheroua O, Saidi D. Effect of the consumption of milk of soya on the male fertility of swiss mice. International Journal of Pharmacy and Pharmaceutical Sciences. Vol 6, Issue 4, 2014: 669-676
(15) Singh, R.J., Chung, G.H., Nelson, R.L. (2007). Landmark research in legumes. Genome, 2007, 50(6): 525-537.
(16) Ahmad M, Qureshi R, Arshad M, Khan Ma, Zafar M. Traditional herbal remedies used for the treatment of diabetes from district Attock (Pakistan). Pak. J. Bot., 2009; 41(6): 2777-2782
(17) Fahmy SR, Soliman AM, Sayed AA, Marzouk M. Possible antiosteoporotic mechanism of Cicer arietinum extract in ovariectomized rats. Int J Clin Exp Pathol 2015; 8(4):3477-3490
(18) Sajja RB, Venkatesh V, Suneetha B, Srinivas N. Evaluation of aphrodisiac activity of methanolic extract of cicer arietinum seeds in sexually sluggish male albino rats. Int J Pharm 2014; 4(4): 309-313.
(19) Das S, Parveen S, Kundra CP, Pereira BMJ. Reproduction in male rats is vulnerable to treatment with the flavonoid-rich seed extracts of Vitex negundo. Phytother. Res. 2004; 18:8-13
(20) Yousef MI, Esmail AM & Baghdadi HH. Effect of isoflavones on reproductive performance, testosterone levels, lipid peroxidation, and seminal plasma biochemisty of male rabbits. Journal of Environmental Science and Health. Part. B 2005; 39 819–833.
(21) Oyedeji KO, Bolarinwana AF. Evaluation of antifertility and teratogenic effects of crude extracts of Portulaca oleracea in male and female albino rats. Asian J Pharm Clin Res 2013; 6: 217-220
(22) AOAC - Association of Official Analytical Chemists. Official methods of analysis of the Association of Analytical Chemist. 1995. 16th ed. AOAC International, Washington, DC.
(23) Watanabe T, Endo A. Effects of selenium deficiency on sperm morphology and spermatocyte chromosomes in mice. Mutat Res. 1991 Feb; 262(2):93-99.
(24) Foreman D, Gaylor L, Evans E, Trella C. A modification of the Roe procedure for the determination of fructose in tissues with increased specificity. Anal Biochem 1973; 56: 584-590.
(25) Okhawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem. 1979; 95:351–358.
(26) Harris LJ, Ray SN. Vitamin C and the suprarenal cortex: Loss of potency of guinea-pig suprarenals in scurvy. With notes on a method for determining antiscorbutic activity (hexuronic acid) by chemical means. Biochem J. 1933; 27(1):303–310.
(27) Beutler, E., Duron, O., Kelly, B.M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 1963; 61, 882–888.
(28) Nishikimi M, Appaji N, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazinemethosulfate and molecular oxygen. Biochem. Bioph. Res. Common. 1972; 46:849-854.
(28) Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase, J. Lab. Clin. Med. 70 (1) (1967) 158–169.
(30) Aebi H., Catalase in vitro, Methods Enzymol. 1984; 105: 121–126.
(31) Tice R.R., Agurell E., Anerson D., Burlinson B., Hartmann A., Kobayashi H., Miyamae Y., Rojas E., Ryu J.C., Sasaki Y.F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing, Environ. Mol. Mutagen. 2000; 35 (3): 206–221
(32) Sriram, M.I., Kanth, S.B.M., Kalishwaralal, K., Gurunathan, S.,. Antitumor activity of silver nanoparticles in Dalton's lymphoma ascites tumor model. Int. J. Nanomed. 2010; 5, 753-762
(33) Razali, N. M., & Wah, Y. B. Power Comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling Tests. Journal of Statistical Modeling and Anlytics, 2011; 2, 21-33.
(34) Agrawal SS, Kumar A, Gullaiya S, Dubey V, Nagar A, Tiwari P, Dhar P, Singh V. Antifertility activity of methanolic bark extract of Aegle marmelos (l.) in male wistar rats. Daru. 2012; 20:94
(35) Li Z, Lin Q, Liu R, Xiao W, Liu W. Protective Effects of Ascorbate and Catalase on Human Spermatozoa During Cryopreservation. Journal of Andrology, 2010; 31(5) September/October
(36) Ebrahim M, Pool EJ. The effect of Tulbaghia violacea extracts on testosterone secretion by testicular cell cultures. Journal of Ethnopharmacology 2010; 132: 359–361
(37) Mohan Vr, Balamurugan K, Sakthidevi G. Fertility enhancement of polycarpaea corymbosa (L.) Lam (caryophyllaceae) whole plant on male albino rats. Asian J Pharm Clin Res, Vol 6 Suppl 5, 2013, 151-155
(38) El-Kholy WM, Hemieda FAE, El-Zarif NA. Protective effect of aqueous extract of Anacyclus pyrethrum root on atrazine-induced male reproductive disorders in rats. International Journal of Advanced Research (2015), Volume 3, Issue 10, 1701 – 1715
(39) Gauthaman K, Adaikan PG & Prasad RNY. Aphrodisiac properties of Tribulus Terrestris extract (Protodioscin) in normal and castrated rats. Life Sciences 2002; 71: 1385–1396.
(40) Gupta RS, Kachhawa JB, Chaudhary R. Antifertility effects of methanolic pod extract of Albizzia lebbeck (L.) Benth in male rats. Asian J Androl 2004; 6:155e9.
(41) Kianifard D. Protective Effects of Morus alba (M.alba) Extract on the Alteration of Testicular Tissue and Spermatogenesis in Adult Rats Treated with Monosodium Glutamate. Medicine Science 2015; 4(1):1947-1958
(42) Oliveira JS, Silva AA, Silva VA Junior. Phytotherapy in reducing glycemic index and testicular oxidative stress resulting from induced diabetes: a review. Braz J Biol. 2016 Jul 11;0:0. doi: 10.1590/1519-6984.09915
(43) Singh S, Lata S, Tiwari KN. Antioxidant potential of Phyllanthus fraternus Webster on cyclophosphamide induced changes in sperm characteristics and testicular oxidative damage in mice. Indian J Exp Biol. 2015 Oct; 53(10):647-656.
(44) Desai KR, Moid N, Patel PB, Highland HN. Evaluation of Deltamethrin induced reproductive toxicity in male Swiss Albino mice. Asian Pacific Journal of Reproduction 2016; 5(1): 24–30
(45) Lewis SE, Agbaje IM. Using the alkaline comet assay in prognostic tests for male infertility and assisted reproductive technology outcomes. Mutagenesis. 2008 May; 23(3):163-170.
(46) Zhang J, Ren L, Zou Y, Zhang L, Wei J, Li Y, Wang J, Suna Z, Zhou X. Silica nanoparticles induce start inhibition of meiosis and cell cycle arrest via down-regulating meiotic relevant factors. Toxicol. Res., 2016, 5, 1453–1464
(47) Fortes MR, Satake N, Corbet DH, Corbet NJ, Burns BM, Moore SS, Boe-Hansen GB. Sperm protamine deficiency correlates with sperm DNA damage in Bos indicus bulls. Andrology. 2014 May; 2(3):370-378.

References

(1) Kashani HH, Faraji Z, Nikzad H, Parivar K, Sharrif M. The effect of aqueous extract of Salep prepared from root- tubers of Dactylorhiza maculate (Orchidaceae) on the testes and sexual hormones of immature male mice. J Med Plants 2012; 6:4102–4106.

(2) Hess R. A., Carnes K. The role of estrogen in testis and the male reproductive tract: a review and species comparison. Anim. Reprod. 2004; 1, 5–30

(3) Atanassova NN, Walker M, McKinnell C, Fisher JS & Sharpe RM. Evidence that androgens and oestrogens, as well as folliclestimulating hormone, can alter Sertoli cell number in the neonatal rat. Journal of Endocrinology, 2005, Vol.184, pp107–117.

(4) Akondi RB, Akula A, Challa SR. Influence of high phytoestrogen diet on rat male reproductive system. Int.Journal of Pharmacy&Technology December 2009 | Vol. 1 | Issue No.1 | 1-20

(5) Ekaluo UB1, Udoh PB, Ikpeme EV, Udensi O. Effect of soybean (Glycine max L.) on the hormonal milieu of male rats. Pak J Biol Sci. 2011 Jul 15;14(14):752-4.

(6) Harris DM, Besselink E, Henning SM, Go VL, Heber D. Phytoestrogens induce differential estrogen receptor alpha- or Beta mediated responses in transfected breast cancer cells. Exp Biol Med (Maywood) 2005; 230: 558–568.

(7) Robertson KM, O'Donnell L, Simpson ER & Jones MME. The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function. Endocrinology, 2002, Vol.143, pp2913–2921.

(8) Modaresi M, Messripour M and Khorami H. Effect of soybean on male reproductive physiology in mice. International Conference on Life Science and Technology. vol.3 (2011) 15-18

(9) Glover A & Assinder SJ. Acute exposure of adult male rats to dietary phytoestrogens reduces fecundity and alters epididymal steroid hormone receptor expression. Journal of Endocrinology 2006 ; 189: 565–573.

(10) Sharmaa P, Parmar J, Vermaa P, Goyal P.K. Radiation induced oxidative stress and its toxicity in testes of mice and their prevention by Tinospora cordifolia extract. Journal of reproductive health and medicine 2015; 1: 64–75

(11) Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev. 2008; 1:15–24.

(12) Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction. 2001; 122:497–506.

(13) El Din, S., Batta, H., Abdul, E. and Abdul, E.F.. Effect of Soybean on Fertility of Male and Female Albino Rats. J. American Science, 2011; 7(6), 872-883.

(14) Zeriouh IF, Addou S, Bouferkas Y, Kheroua O, Saidi D. Effect of the consumption of milk of soya on the male fertility of swiss mice. International Journal of Pharmacy and Pharmaceutical Sciences. Vol 6, Issue 4, 2014: 669-676

(15) Singh, R.J., Chung, G.H., Nelson, R.L. (2007). Landmark research in legumes. Genome, 2007, 50(6): 525-537.

(16) Ahmad M, Qureshi R, Arshad M, Khan Ma, Zafar M. Traditional herbal remedies used for the treatment of diabetes from district Attock (Pakistan). Pak. J. Bot., 2009; 41(6): 2777-2782

(17) Fahmy SR, Soliman AM, Sayed AA, Marzouk M. Possible antiosteoporotic mechanism of Cicer arietinum extract in ovariectomized rats. Int J Clin Exp Pathol 2015; 8(4):3477-3490

(18) Sajja RB, Venkatesh V, Suneetha B, Srinivas N. Evaluation of aphrodisiac activity of methanolic extract of cicer arietinum seeds in sexually sluggish male albino rats. Int J Pharm 2014; 4(4): 309-313.

(19) Das S, Parveen S, Kundra CP, Pereira BMJ. Reproduction in male rats is vulnerable to treatment with the flavonoid-rich seed extracts of Vitex negundo. Phytother. Res. 2004; 18:8-13

(20) Yousef MI, Esmail AM & Baghdadi HH. Effect of isoflavones on reproductive performance, testosterone levels, lipid peroxidation, and seminal plasma biochemisty of male rabbits. Journal of Environmental Science and Health. Part. B 2005; 39 819–833.

(21) Oyedeji KO, Bolarinwana AF. Evaluation of antifertility and teratogenic effects of crude extracts of Portulaca oleracea in male and female albino rats. Asian J Pharm Clin Res 2013; 6: 217-220

(22) AOAC - Association of Official Analytical Chemists. Official methods of analysis of the Association of Analytical Chemist. 1995. 16th ed. AOAC International, Washington, DC.

(23) Watanabe T, Endo A. Effects of selenium deficiency on sperm morphology and spermatocyte chromosomes in mice. Mutat Res. 1991 Feb; 262(2):93-99.

(24) Foreman D, Gaylor L, Evans E, Trella C. A modification of the Roe procedure for the determination of fructose in tissues with increased specificity. Anal Biochem 1973; 56: 584-590.

(25) Okhawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem. 1979; 95:351–358.

(26) Harris LJ, Ray SN. Vitamin C and the suprarenal cortex: Loss of potency of guinea-pig suprarenals in scurvy. With notes on a method for determining antiscorbutic activity (hexuronic acid) by chemical means. Biochem J. 1933; 27(1):303–310.

(27) Beutler, E., Duron, O., Kelly, B.M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 1963; 61, 882–888.

(28) Nishikimi M, Appaji N, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazinemethosulfate and molecular oxygen. Biochem. Bioph. Res. Common. 1972; 46:849-854.

(28) Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase, J. Lab. Clin. Med. 70 (1) (1967) 158–169.

(30) Aebi H., Catalase in vitro, Methods Enzymol. 1984; 105: 121–126.

(31) Tice R.R., Agurell E., Anerson D., Burlinson B., Hartmann A., Kobayashi H., Miyamae Y., Rojas E., Ryu J.C., Sasaki Y.F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing, Environ. Mol. Mutagen. 2000; 35 (3): 206–221

(32) Sriram, M.I., Kanth, S.B.M., Kalishwaralal, K., Gurunathan, S.,. Antitumor activity of silver nanoparticles in Dalton's lymphoma ascites tumor model. Int. J. Nanomed. 2010; 5, 753-762

(33) Razali, N. M., & Wah, Y. B. Power Comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling Tests. Journal of Statistical Modeling and Anlytics, 2011; 2, 21-33.

(34) Agrawal SS, Kumar A, Gullaiya S, Dubey V, Nagar A, Tiwari P, Dhar P, Singh V. Antifertility activity of methanolic bark extract of Aegle marmelos (l.) in male wistar rats. Daru. 2012; 20:94

(35) Li Z, Lin Q, Liu R, Xiao W, Liu W. Protective Effects of Ascorbate and Catalase on Human Spermatozoa During Cryopreservation. Journal of Andrology, 2010; 31(5) September/October

(36) Ebrahim M, Pool EJ. The effect of Tulbaghia violacea extracts on testosterone secretion by testicular cell cultures. Journal of Ethnopharmacology 2010; 132: 359–361

(37) Mohan Vr, Balamurugan K, Sakthidevi G. Fertility enhancement of polycarpaea corymbosa (L.) Lam (caryophyllaceae) whole plant on male albino rats. Asian J Pharm Clin Res, Vol 6 Suppl 5, 2013, 151-155

(38) El-Kholy WM, Hemieda FAE, El-Zarif NA. Protective effect of aqueous extract of Anacyclus pyrethrum root on atrazine-induced male reproductive disorders in rats. International Journal of Advanced Research (2015), Volume 3, Issue 10, 1701 – 1715

(39) Gauthaman K, Adaikan PG & Prasad RNY. Aphrodisiac properties of Tribulus Terrestris extract (Protodioscin) in normal and castrated rats. Life Sciences 2002; 71: 1385–1396.

(40) Gupta RS, Kachhawa JB, Chaudhary R. Antifertility effects of methanolic pod extract of Albizzia lebbeck (L.) Benth in male rats. Asian J Androl 2004; 6:155e9.

(41) Kianifard D. Protective Effects of Morus alba (M.alba) Extract on the Alteration of Testicular Tissue and Spermatogenesis in Adult Rats Treated with Monosodium Glutamate. Medicine Science 2015; 4(1):1947-1958

(42) Oliveira JS, Silva AA, Silva VA Junior. Phytotherapy in reducing glycemic index and testicular oxidative stress resulting from induced diabetes: a review. Braz J Biol. 2016 Jul 11;0:0. doi: 10.1590/1519-6984.09915

(43) Singh S, Lata S, Tiwari KN. Antioxidant potential of Phyllanthus fraternus Webster on cyclophosphamide induced changes in sperm characteristics and testicular oxidative damage in mice. Indian J Exp Biol. 2015 Oct; 53(10):647-656.

(44) Desai KR, Moid N, Patel PB, Highland HN. Evaluation of Deltamethrin induced reproductive toxicity in male Swiss Albino mice. Asian Pacific Journal of Reproduction 2016; 5(1): 24–30

(45) Lewis SE, Agbaje IM. Using the alkaline comet assay in prognostic tests for male infertility and assisted reproductive technology outcomes. Mutagenesis. 2008 May; 23(3):163-170.

(46) Zhang J, Ren L, Zou Y, Zhang L, Wei J, Li Y, Wang J, Suna Z, Zhou X. Silica nanoparticles induce start inhibition of meiosis and cell cycle arrest via down-regulating meiotic relevant factors. Toxicol. Res., 2016, 5, 1453–1464

(47) Fortes MR, Satake N, Corbet DH, Corbet NJ, Burns BM, Moore SS, Boe-Hansen GB. Sperm protamine deficiency correlates with sperm DNA damage in Bos indicus bulls. Andrology. 2014 May; 2(3):370-378.