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Karimipour, M., Dibayi, Z., Ahmadi, A., Zirak Javanmard, M., & Hosseinalipour, E. (2019). The protective effect of vitamin C on phenylhydrazine-induced hemolytic anemia on sperm quality and in-vitro embryo development in mice. International Journal of Reproductive BioMedicine (IJRM), 16(12), 791–800. https://doi.org/10.18502/ijrm.v16i12.3685
https://doi.org/10.18502/ijrm.v16i12.3685
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authors
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Mojtaba Karimipour
No author data available.
-
Zahra Dibayi
No author data available.
-
Abass Ahmadi
No author data available.
-
Masoumeh Zirak Javanmard
No author data available.
-
Elnaz Hosseinalipour
No author data available.
Published Date
- Jan 27, 2019
The protective effect of vitamin C on phenylhydrazine-induced hemolytic anemia on sperm quality and in-vitro embryo development in mice
Abstract
Background: Phenylhydrazine (PHZ) induced anemia and was shown to have harmful effects on the male reproductive system.
Objective: To investigate the protective effect of vitamin C (Vit C) on sperm parameters quality, in vitro fertilization potential and embryonic development in a mouse model of hemolytic anemia induced by PHZ.
Materials and Methods: Thirty-two NMRI adult male mice (n = 8/each) were randomly classified into four groups. Group I (control) received normal saline, Group II (PHZ) received 8 mg/100 gr body weight PHZ as initial dose, continued by 6 mg/100 gr intraperitoneally every 48 hr, Group III (Vit C) received Vit C (10 mg/kg, daily, intraperitoneally), and group IV (PHZ + Vit C) received PHZ and Vit C. After 35 days, sperm quality parameters, the percentage of sperm with DNA damage and in vitro fertilization outcomes up to blastocyst stage were evaluated.
Results: A significant (p < 0.001) reduction in all of the sperm parameters (count, motility, viability and normal morphology) were observed in group II (PHZ) compared with group I (control). In group IV (PHZ ± Vit C), these parameters and sperm DNA damage (p < 0.001) improved significantly when compared with PHZ-treated mice. Furthermore, PHZ caused a significant (p < 0.001) decrease in the fertilization rate and the percentage of pre implantation embryos’ (two cell embryo and blastocyst) formation in comparison to group I (control), and Vit C supplementation in mice of group IV improved significantly the fertilization rate (p = 0.002), but it could not improve the percentage of two cell embryos and blastocyst production.
Conclusion: The data from this study indicated that Vit C decreased the adverse effects of PHZ on the quality of sperm parameters and in vitro fertilization rate, but it is insufficient to restore the in-vitro embryonic development and fertility potential.
Key words: Vitamin C, Phenylhydrazine, Sperm, Fertilization, Mice.
References
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Justicia carnea leaves extract in phenylhydrazine inducedanemia in albino rats. Acta Sci Pol Technol Aliment 2017;
16: 217–230.
[2] Berger J. Phenylhydrazine haematotoxicity. J Appl Biomed 2007; 5: 125–130.
[3] Ashour TH. Hematinic and anti-anemic effect of thymoquinone against phenylhydrazine-induced hemolytic
anemia in rats. Res J Med Sci 2014; 8: 67–72.
[4] Mozafari AA, Shahrooz R, Ahmadi A, Malekinjad H, Mardani K. Protective effect of ethyl pyruvate on mice sperm parameters in phenylhydrazine induced hemolytic anemia. Vet Res Forum 2016; 7: 63–68.
[5] Amer J, Goldfarb A, Fibach E. Flow cytometric analysis of the oxidative status of normal and thalassemic red blood cells. Cytometry A 2004; 60: 73–80.
[6] Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 1987; 81: 459–469.
[7] Köksal IT, Tefekli A, Usta M, Erol H, Abbasoglu S, Kadioglu A. The role of reactive oxygen species in testicular
dysfunction associated with varicocele. BJU Int 2000; 86:549–552.
[8] Fraga CG, Motchnik PA, Shigenaga MK, Helbock HJ, Jacob RA, Ames BN. Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 1991; 88: 11003–11006.
[9] Fernandes GS, Fernandez CD, Campos KE, Damasceno DC, Anselmo-Franci JA, Kempinas WD. Vitamin C partially attenuates male reproductive deficits in hyperglycemic rats. Reprod Biol Endocrinol 2011; 9: 100.
[10] Chen N, Su P, Wang M, Li YM. Ascorbic acid inhibits cadmium-induced disruption of the blood-testis barrier by regulating oxidative stress-mediated p38 MAPK pathways. Environ Sci Pollut Res Int 2018; 25: 21713–21720.
[11] Talebi AR, Mangoli E, Nahangi H, Anvari M, Pourentezari M, Halvaei I. Vitamin C attenuates detrimental effects of diabetes mellitus on sperm parameters, chromatin quality and rate of apoptosis in mice. Eur J Obstet Gynecol Reprod Biol 2014; 181: 32–36.
[12] Sapra M, Sharma P, Kothari LK. Effect of vitamin C deficiency on testicular structure in the guinea pig. J
Postgrad Med 1987; 33: 69–73.
[13] Hess RA, Chen P. Computer tracking of germ cells in the cycle of the seminiferous epithelium and prediction of changes in cycle duration in animals commonly used in reproductive biology and toxicology. J Androl 1992; 13: 185–190.
[14] Orazizadeh M, Daneshi E, Hashemitmar M, Absalan F, Khorsandi L. Protective effect of beta-carotene against
titanium dioxide nanoparticles induced apoptosis in mouse testicular tissue. Andrologia 2015; 47: 816–825.
[15] Badkoobeh P, Parivar K, Kalantar SM, Hosseini SD, Salabat A. Effect of nano-zinc oxide on doxorubicin- induced oxidative stress and sperm disorders in adult male Wistar rats. Iran J Reprod Med 2013; 11: 355–364.
[16] Leite GAA, Figueiredo TM, Guerra MT, Borges CDS, Fernandes FH, Anselmo-Franci JA, et al. Ascorbic acid
co-administered with rosuvastatin reduces reproductive impairment in the male offspring from male rats exposed to the statin at pre-puberty. Food Chem Toxicol 2018; 118:416–429.
[17] Arabi M. Nicotinic infertility: assessing DNA and plasma membrane integrity of human spermatozoa. Andrologia 2004; 36: 305–310.
[18] Auger J, Eustache F, Andersen AG, Irvine DS, Jørgensen N, Skakkebaek NE, et al. Sperm morphological defects related to environment, lifestyle and medical history of 1001 male partners of pregnant women from four European cities.Hum Reprod 2001; 16: 2710–2717
[19] Kaur P, Bansal MP. Effect of experimental oxidative stress on steroidogenesis and DNA damage in mouse testis. JBiomed Sci 2004; 11: 391–397.
[20] Alvarez JG, Touchstone JC, Blasco L, Storey BT. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl 1987; 8: 338–348.
[21] Liu W, Gong F, Luo K, Lu G. Comparing the pregnancy rates of one versus two intrauterine inseminations (IUIs) in male factor and idiopathic infertility. J Assist Reprod Genet 2006; 23: 75–79.
[22] Chauhan SP, Sheth NR, Suhagia BN. Hematinic effect of fruits of Opuntia elatior Mill. on phenylhydrazine-induced anemia in rats. Ayu 2015; 36: 208–213.
[23] Unami A, Nishina N, Terai T, Sato S, Tamura T, Noda K, et al. Effects of cisplatin on erythropoietin production in rats. J Toxicol Sci 1996; 21: 157–165.
[24] Zarei L, Shahrooz R, Sadrkhanlou R, Malekinejad H, Ahmadi A, Bakhtiary Z. Protective effects of cornus mas extract on in vitro fertilization potential in methotrexate treated male mice. Vet Res Forum 2015; 6: 55–61.
[25] Agarwal A, Ikemoto I, Loughlin KR. Relationship of sperm parameters with levels of reactive oxygen species in semen specimens. J Urol 1994; 152: 107–110.
[26] Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L. Evaluation of antioxidant effects of crocin on sperm quality in
cyclophosphamide treated adult mice. Vet Res Forum 2014;5: 213–218.
[27] Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction.Fertil Steril 2003; 79: 829–843.
[28] Aguirre-Arias MV, Velarde V, Moreno RD. Effects of ascorbic acid on spermatogenesis and sperm parameters in diabetic rats. Cell Tissue Res 2017; 370: 305–317.
[29] Gil-Guzman E, Ollero M, Lopez MC, Sharma RK, Alvarez JG, Thomas AJ Jr, et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 2001; 16:1922–1930.
[30] Huszar G, Sbracia M, Vigue L, Miller DJ, Shur BD. Sperm plasma membrane remodeling during spermiogenetic maturation in men: relationship among plasma Membrane β 1, 4galactosyltransferase,cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. Biol
Reprod 1997; 56: 1020–1024.
[31] Mangoli E, Talebi AR, Anvari M, Taheri F, Vatanparast M, Rahiminia T, et al. Vitamin C attenuates negative effects of vitrification on sperm parameters, chromatin quality, apoptosis and acrosome reaction in neat and prepared normozoospermic samples. Taiwan J Obstet Gynecol 2018;57: 200–204.
[32] Silver EW, Eskenazi B, Evenson DP, Block G, Young S, Wyrobek AJ. Effect of antioxidant intake on sperm
chromatin stability in healthy nonsmoking men. J Androl 2005; 26: 550–556.
[33] Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am
J Reprod Immunol 2008; 59: 2–11.
[34] Lim CC, Lewis SE, Kennedy M, Donnelly ET, Thompson W. Human sperm morphology and in vitro fertilization: sperm tail defects are prognostic for fertilization failure. Andrologia 1998; 30: 43–47.
[35] Angulo C, Maldonado R, Pulgar E, Mancilla H, Córdova A, Villarroel F, et al. Vitamin C and oxidative stress in the seminiferous epithelium. Biol Res 2011; 44: 169–180.
[36] Augustine LM, Markelewicz RJ Jr, Boekelheide K, Cherrington NJ. Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab Dispos 2005; 33: 182–189.
[37] Angulo C, Castro MA, Rivas CI, Segretain D, Maldonado R, Yañez AJ, et al. Molecular identification and functional characterization of the vitamin C transporters expressed by Sertoli cells. J Cell Physiol 2008; 217: 708–716.
Justicia carnea leaves extract in phenylhydrazine inducedanemia in albino rats. Acta Sci Pol Technol Aliment 2017;
16: 217–230.
[2] Berger J. Phenylhydrazine haematotoxicity. J Appl Biomed 2007; 5: 125–130.
[3] Ashour TH. Hematinic and anti-anemic effect of thymoquinone against phenylhydrazine-induced hemolytic
anemia in rats. Res J Med Sci 2014; 8: 67–72.
[4] Mozafari AA, Shahrooz R, Ahmadi A, Malekinjad H, Mardani K. Protective effect of ethyl pyruvate on mice sperm parameters in phenylhydrazine induced hemolytic anemia. Vet Res Forum 2016; 7: 63–68.
[5] Amer J, Goldfarb A, Fibach E. Flow cytometric analysis of the oxidative status of normal and thalassemic red blood cells. Cytometry A 2004; 60: 73–80.
[6] Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 1987; 81: 459–469.
[7] Köksal IT, Tefekli A, Usta M, Erol H, Abbasoglu S, Kadioglu A. The role of reactive oxygen species in testicular
dysfunction associated with varicocele. BJU Int 2000; 86:549–552.
[8] Fraga CG, Motchnik PA, Shigenaga MK, Helbock HJ, Jacob RA, Ames BN. Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 1991; 88: 11003–11006.
[9] Fernandes GS, Fernandez CD, Campos KE, Damasceno DC, Anselmo-Franci JA, Kempinas WD. Vitamin C partially attenuates male reproductive deficits in hyperglycemic rats. Reprod Biol Endocrinol 2011; 9: 100.
[10] Chen N, Su P, Wang M, Li YM. Ascorbic acid inhibits cadmium-induced disruption of the blood-testis barrier by regulating oxidative stress-mediated p38 MAPK pathways. Environ Sci Pollut Res Int 2018; 25: 21713–21720.
[11] Talebi AR, Mangoli E, Nahangi H, Anvari M, Pourentezari M, Halvaei I. Vitamin C attenuates detrimental effects of diabetes mellitus on sperm parameters, chromatin quality and rate of apoptosis in mice. Eur J Obstet Gynecol Reprod Biol 2014; 181: 32–36.
[12] Sapra M, Sharma P, Kothari LK. Effect of vitamin C deficiency on testicular structure in the guinea pig. J
Postgrad Med 1987; 33: 69–73.
[13] Hess RA, Chen P. Computer tracking of germ cells in the cycle of the seminiferous epithelium and prediction of changes in cycle duration in animals commonly used in reproductive biology and toxicology. J Androl 1992; 13: 185–190.
[14] Orazizadeh M, Daneshi E, Hashemitmar M, Absalan F, Khorsandi L. Protective effect of beta-carotene against
titanium dioxide nanoparticles induced apoptosis in mouse testicular tissue. Andrologia 2015; 47: 816–825.
[15] Badkoobeh P, Parivar K, Kalantar SM, Hosseini SD, Salabat A. Effect of nano-zinc oxide on doxorubicin- induced oxidative stress and sperm disorders in adult male Wistar rats. Iran J Reprod Med 2013; 11: 355–364.
[16] Leite GAA, Figueiredo TM, Guerra MT, Borges CDS, Fernandes FH, Anselmo-Franci JA, et al. Ascorbic acid
co-administered with rosuvastatin reduces reproductive impairment in the male offspring from male rats exposed to the statin at pre-puberty. Food Chem Toxicol 2018; 118:416–429.
[17] Arabi M. Nicotinic infertility: assessing DNA and plasma membrane integrity of human spermatozoa. Andrologia 2004; 36: 305–310.
[18] Auger J, Eustache F, Andersen AG, Irvine DS, Jørgensen N, Skakkebaek NE, et al. Sperm morphological defects related to environment, lifestyle and medical history of 1001 male partners of pregnant women from four European cities.Hum Reprod 2001; 16: 2710–2717
[19] Kaur P, Bansal MP. Effect of experimental oxidative stress on steroidogenesis and DNA damage in mouse testis. JBiomed Sci 2004; 11: 391–397.
[20] Alvarez JG, Touchstone JC, Blasco L, Storey BT. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl 1987; 8: 338–348.
[21] Liu W, Gong F, Luo K, Lu G. Comparing the pregnancy rates of one versus two intrauterine inseminations (IUIs) in male factor and idiopathic infertility. J Assist Reprod Genet 2006; 23: 75–79.
[22] Chauhan SP, Sheth NR, Suhagia BN. Hematinic effect of fruits of Opuntia elatior Mill. on phenylhydrazine-induced anemia in rats. Ayu 2015; 36: 208–213.
[23] Unami A, Nishina N, Terai T, Sato S, Tamura T, Noda K, et al. Effects of cisplatin on erythropoietin production in rats. J Toxicol Sci 1996; 21: 157–165.
[24] Zarei L, Shahrooz R, Sadrkhanlou R, Malekinejad H, Ahmadi A, Bakhtiary Z. Protective effects of cornus mas extract on in vitro fertilization potential in methotrexate treated male mice. Vet Res Forum 2015; 6: 55–61.
[25] Agarwal A, Ikemoto I, Loughlin KR. Relationship of sperm parameters with levels of reactive oxygen species in semen specimens. J Urol 1994; 152: 107–110.
[26] Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L. Evaluation of antioxidant effects of crocin on sperm quality in
cyclophosphamide treated adult mice. Vet Res Forum 2014;5: 213–218.
[27] Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction.Fertil Steril 2003; 79: 829–843.
[28] Aguirre-Arias MV, Velarde V, Moreno RD. Effects of ascorbic acid on spermatogenesis and sperm parameters in diabetic rats. Cell Tissue Res 2017; 370: 305–317.
[29] Gil-Guzman E, Ollero M, Lopez MC, Sharma RK, Alvarez JG, Thomas AJ Jr, et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 2001; 16:1922–1930.
[30] Huszar G, Sbracia M, Vigue L, Miller DJ, Shur BD. Sperm plasma membrane remodeling during spermiogenetic maturation in men: relationship among plasma Membrane β 1, 4galactosyltransferase,cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. Biol
Reprod 1997; 56: 1020–1024.
[31] Mangoli E, Talebi AR, Anvari M, Taheri F, Vatanparast M, Rahiminia T, et al. Vitamin C attenuates negative effects of vitrification on sperm parameters, chromatin quality, apoptosis and acrosome reaction in neat and prepared normozoospermic samples. Taiwan J Obstet Gynecol 2018;57: 200–204.
[32] Silver EW, Eskenazi B, Evenson DP, Block G, Young S, Wyrobek AJ. Effect of antioxidant intake on sperm
chromatin stability in healthy nonsmoking men. J Androl 2005; 26: 550–556.
[33] Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am
J Reprod Immunol 2008; 59: 2–11.
[34] Lim CC, Lewis SE, Kennedy M, Donnelly ET, Thompson W. Human sperm morphology and in vitro fertilization: sperm tail defects are prognostic for fertilization failure. Andrologia 1998; 30: 43–47.
[35] Angulo C, Maldonado R, Pulgar E, Mancilla H, Córdova A, Villarroel F, et al. Vitamin C and oxidative stress in the seminiferous epithelium. Biol Res 2011; 44: 169–180.
[36] Augustine LM, Markelewicz RJ Jr, Boekelheide K, Cherrington NJ. Xenobiotic and endobiotic transporter mRNA expression in the blood-testis barrier. Drug Metab Dispos 2005; 33: 182–189.
[37] Angulo C, Castro MA, Rivas CI, Segretain D, Maldonado R, Yañez AJ, et al. Molecular identification and functional characterization of the vitamin C transporters expressed by Sertoli cells. J Cell Physiol 2008; 217: 708–716.