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The importance of trace minerals copper, manganese, selenium and zinc in bovine sperm–zona pellucida binding

Published online by Cambridge University Press:  15 March 2019

Juan Patricio Anchordoquy ,
Juan Mateo Anchordoquy ,
Raúl Martín Lizarraga ,
Noelia Nikoloff ,
Ana Malen Pascua  and
Cecilia Cristina Furnus Open the ORCID record for Cecilia Cristina Furnus [Opens in a new window]
Juan Patricio Anchordoquy
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina Cátedra de Fisiología, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina
Juan Mateo Anchordoquy
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina Cátedra de Fisiología, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina
Raúl Martín Lizarraga
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina
Noelia Nikoloff
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina
Ana Malen Pascua
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina
Cecilia Cristina Furnus*
Affiliation:
Igevet e Instituto de Genética Veterinaria ‘Prof. Fernando N. Dulout’ (UNLP-Conicet La Plata), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP 1900, La Plata, Buenos Aires, Argentina Cátedra de Citología, Histología y Embriología ‘A’ Facultad de Ciencias Médicas, Universidad Nacional de La Plata, calle 60 y 120 s/n, CP1900, La Plata, Buenos Aires, Argentina
*
Address for correspondence: Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET, UNLP-CONICET La Plata). Facultad de Ciencias Veterinarias. Universidad Nacional de La Plata, Calle 60 y 118 s/n CP (1900), La Plata, Buenos Aires, Argentina. Tel: +54 0221 5221488. E-mail: [email protected]
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Summary

Sperm–zona pellucida (ZP) binding is a necessary event for successful fertilization. The aim of this study was to determine the effect of trace minerals such as copper (Cu), manganese (Mn), selenium (Se) and zinc (Zn) on bovine spermatozoa binding to ZP. Sperm viability, functional membrane integrity, acrosomal status (AS), total antioxidant capacity (TAC) and sperm lipid peroxidation (LPO) were also evaluated. For the present study, in vitro fertilization (IVF) medium was supplemented with Cu (0.4 µg/ml Cu), Mn (5 ng/ml Mn), Se (100 ng/ml Se), Zn (0.8 µg/ml Zn), all minerals (Cu+Mn+Se+Zn), or tested without supplement (Control). Considerably more sperm bound to ZP when Cu, Se or Zn were added to the IVF medium, but there were no difference compared with the Control, Mn and Cu+Mn+Se+Zn groups. After 1 h of incubation, viability was increased by the addition of Cu, Mn and Se with respect to the Control but, after 2 h, viability was higher only with the addition of Mn to IVF medium. Functional membrane integrity improved in sperm treated with Cu. Acrosome integrity was higher in sperm treated with Zn after 1 h of incubation. LPO was significantly higher in sperm treated with Cu or Cu+Mn+Se+Zn. The mean TACs of sperm treated with Cu, Mn, Zn or Cu+Mn+Se+Zn were lower than in the Control. In conclusion, the results obtained in the present study determined that the presence of Cu, Se and Zn in the IVF medium increased the number of spermatozoa bound to the ZP, highlighting the importance of these minerals in the fertilization process.

Keywords

Lipid peroxidationMTT assayOxidative statusSperm qualityTrace element
Type
Research Article
Information
Zygote , Volume 27 , Issue 2 , April 2019 , pp. 89 - 96
Copyright
© Cambridge University Press 2019 

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References

Ahsan, U, Kamran, Z, Raza, I and Iqbal, Z (2014) Role of selenium in male reproduction—a review. Anim Reprod Sci 146, 55–62.Google Scholar
Aitken, RJ (1997) Molecular mechanisms regulating human sperm function. Mol Hum Reprod 3, 169–173.Google Scholar
Aitken, RJ and Baker, MA (2004) Oxidative stress and male reproductive biology. Reprod Fertil Dev 16, 581–588.Google Scholar
Aitken, RJ and Curry, BJ (2011) Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal 14, 367–381.Google Scholar
Aitken, RJ, Clarkson, JS and Fishel, S (1989) Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 41, 183–197.Google Scholar
Aitken, RJ, Jones, KT and Robertson, SA (2012) Reactive oxygen species and sperm function – in sickness and in health. J Androl 33, 1096–1106.Google Scholar
Aitken, RJ, Baker, MA and Nixon, B (2015) Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress? Asian J Androl 17, 633–639.Google Scholar
Anchordoquy, JP, Anchordoquy, JM, Pascua, AM, Nikoloff, N, Peral-García, P and Furnus, CC (2017) The copper transporter (SLC31A1/CTR1) is expressed in bovine spermatozoa and oocytes: copper in IVF medium improves sperm quality. Theriogenology 97, 124–133.Google Scholar
Aziz, DM (2006) Assessment of bovine sperm viability by MTT reduction assay. Anim Reprod Sci, 92(1–2), 1–8.Google Scholar
Barroso, G, Morshedi, M and Oehninger, S (2000) Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 15, 1338–1344.Google Scholar
Basim, J Mackenzie-Bell, AM and Buhr, MM (2009) Reactive oxygen species and boar sperm function. Biol Reprod 81, 553–561.Google Scholar
Baumber, J, Sabeur, K, Vo, A and Ball, BA (2003) Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 60, 1239–1247.Google Scholar
Cheema, RS, Bansal, AK and Bilaspuri, GS (2009) Manganese provides antioxidant protection for sperm cryopreservation that may offer new consideration for clinical fertility. Oxid Med Cell Longev 2, 152–159.Google Scholar
Chia, SE, Ong, CN, Chua, LH, Ho, LM and Tay, SK (2000) Comparison of zinc concentrations in blood and seminal plasma and the various sperm parameters between fertile and infertile men. J Androl 21, 53–57.Google Scholar
Chihuailaf, RH, Contreras, PA and Wittwer, FG (2002) Patogénesis del estrés oxidativo: Consecuencias y evaluación en salud animal pathogenesis of oxidative stress: consequences and evaluation in animal health. Vet Méx 33, 265.Google Scholar
Chiu, PCN, Chung, M-K, Koistinen, R and Yeung, WSB (2007) Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa–zona pellucida binding. J Cell Sci 120(Pt 1), 33–44.Google Scholar
Coassin, M, Ursini, F and Bindoli, A (1992) Antioxidant effect of manganese. Arch Biochem Biophys 299, 330–333.Google Scholar
Colagar, AH, Marzony, ET and Chaichi, MJ (2009) Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 29, 82–88.Google Scholar
Cornwall, GA, Tulsiani, DR and Orgebin-Crist, MC (1991) Inhibition of the mouse sperm surface alpha-d-mannosidase inhibits sperm-egg binding in vitro . Biol Reprod 44, 913–921.Google Scholar
Coutinho da Silva, MA, Seidel, GE, Squires, EL, Graham, JK and Carnevale, EM (2012) Effects of components of semen extenders on the binding of stallion spermatozoa to bovine or equine zonae pellucidae. Reproduction 143, 577–585.Google Scholar
Denizot, F and Lang, R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods, 89, 271–277.Google Scholar
Dorostkar, K, Alavi-Shoushtari, SM and Mokarizadeh, A (2012) Effects of in vitro selenium addition to the semen extender on the spermatozoa characteristics before and after freezing in water buffaloes (Bubalus bubalis). Vet Res Forum 3, 263–268.Google Scholar
Dorostkar, K, Alavi Shoushtari, SM and Khaki, A (2014) Effects of in vitro zinc sulphate additive to the semen extender on water buffalo (Bubalus bubalis) spermatozoa before and after freezing. Int J Fertil Steril 8, 325–332.Google Scholar
Ecroyd, HW, Jones, RC and Aitken, RJ (2003) Endogenous redox activity in mouse spermatozoa and its role in regulating the tyrosine phosphorylation events associated with sperm capacitation. Biol Reprod 69, 347–354.Google Scholar
El-Sharawy, M, Eid, E, Darwish, S, Abdel-Razek, I, Islam, MR, Kubota, K, Yamauchi, N and El-Shamaa, I (2017) Effect of organic and inorganic selenium supplementation on semen quality and blood enzymes in buffalo bulls: selenium effects on buffalo semen quality. Anim Sci J 88, 999–1005.Google Scholar
Fazeli, AR, Steenweg, W, Bevers Mvan den Broek, J, Bracher, V, Parlevliet, J and Colenbrander, B (1995) Relation between stallion sperm binding to homologous hemizonae and fertility. Theriogenology 44, 751–760.Google Scholar
Gavella, M and Lipovac, V (1998) In vitro effect of zinc on oxidative changes in human semen. Andrologia, 30, 317–323.Google Scholar
Gil-Guzman, E, Ollero, M, Lopez, MC, Sharma, RK, Alvarez, JG, Thomas, AJ Jr and Agarwal, A (2001) Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 16, 1922–1930.Google Scholar
Gonçalves, FS, Barretto, LS, Arruda, RP, Perri, SH and Mingoti, GZ (2010) Effect of antioxidants during bovine in vitro fertilization procedures on spermatozoa and embryo development. Reprod Domest Anim, 45, 129–135.Google Scholar
Gong, X, Dubois, DH, Miller, DJ and Shur, BD (1995) Activation of a G protein complex by aggregation of beta-1,4-galactosyltransferase on the surface of sperm. Science 269(5231), 1718–1721.Google Scholar
Hoodbhoy, T and Dean, J (2004) Insights into the molecular basis of sperm-egg recognition in mammals. Reproduction 127, 417–422.Google Scholar
Ivanova, M and Mollova, M (1993) Zona-penetration in vitro test for evaluating boar sperm fertility. Theriogenology 40 397–410.Google Scholar
Jones, R, Mann, T and Sherins, R (1979) Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril 31, 531–537.Google Scholar
Kasimanickam, R, Kasimanickam, V, Thatcher, CD, Nebel, RL and Cassell, BG (2007) Relationships among lipid peroxidation, glutathione peroxidase, superoxide dismutase, sperm parameters, and competitive index in dairy bulls. Theriogenology 67, 1004–1012.Google Scholar
Kaushik, K, Mittal, PK and Kalla, NR (2015) Antioxidant potential of Mn2+ in the human ejaculated spermatozoa under oxidative stress. Int J Pharm Sci Res 42, 2153–2162.Google Scholar
Kincaid, RL (1999) Assessment of trace mineral status of ruminants: a review. J Anim Sci 77(E-Suppl), 1–10.Google Scholar
Kiziler, AR, Aydemir, B, Onaran, I, Alici, B, Ozkara, H, Gulyasar, T and Akyolcu, MC (2007) High levels of cadmium and lead in seminal fluid and blood of smoking men are associated with high oxidative stress and damage in infertile subjects. Biol Trace Elem Res 120(1–3), 82–91.Google Scholar
Kodama, H, Kuribayashi, Y and Gagnon, C (1996) Effect of sperm lipid peroxidation on fertilization. J Androl 17, 151–157.Google Scholar
Lapointe, S, Ahmad, I, Buhr, MM and Sirard, MA (1996) Modulation of postthaw motility, survival, calcium uptake, and fertility of bovine sperm by magnesium and manganese. J Dairy Sci 79, 2163–2169.Google Scholar
Liu, D-Y, Sie, B-S, Liu, M-L, Agresta, F and Baker, HWG (2009) Relationship between seminal plasma zinc concentration and spermatozoa–zona pellucida binding and the ZP-induced acrosome reaction in subfertile men. Asian J Androl 11, 499–507.Google Scholar
Marai, IFM, El-Darawany, A-HA, Ismail, E-SA-F and Abdel-Hafez, MAM (2009) Reproductive and physiological traits of Egyptian Suffolk rams as affected by selenium dietary supplementation and housing heat radiation effects during winter of the sub-tropical environment of Egypt. Arch Anim Breed 52, 402–409.Google Scholar
Mendoza, C, Carreras, A, Moos, J and Tesarik, J (1992) Distinction between true acrosome reaction and degenerative acrosome loss by a one-step staining method using Pisum sativum agglutinin. J Reprod Fertil 95, 755–763.Google Scholar
Michailov, Y, Ickowicz, D and Breitbart, H (2014) Zn2+-stimulation of sperm capacitation and of the acrosome reaction is mediated by EGFR activation. Dev Biol 396, 246–255.Google Scholar
Miller, DJ, Macek, MB and Shur, BD (1992) Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357(6379), 589–593.Google Scholar
Mosmann, T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1–2), 55–63.Google Scholar
Nair, SJ, Brar, AS, Ahuja, CS, Sangha, SP and Chaudhary, KC (2006) A comparative study on lipid peroxidation, activities of antioxidant enzymes and viability of cattle and buffalo bull spermatozoa during storage at refrigeration temperature. Anim Reprod Sci 96(1–2), 21–29.Google Scholar
Oehninger, S, Mahony, M, Ozgür, K, Kolm, P, Kruger, T and Franken, D (1997) Clinical significance of human sperm–zona pellucida binding. Fertil Steril 67, 1121–1127.Google Scholar
Overstreet, JW, Yanagimachi, R, Katz, DF, Hayashi, K and Hanson, FW (1980) Penetration of human spermatozoa into the human zona pellucida and the zona-free hamster egg: a study of fertile donors and infertile patients. Fertil Steril 33, 534–542.Google Scholar
Parrish, JJ, Susko-Parrish, JL, Leibfried-Rutledge, ML, Critser, ES, Eyestone, WH and First, NL (1986) Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.Google Scholar
Reid, AT, Redgrove, K, Aitken, RJ and Nixon, B (2011) Cellular mechanisms regulating sperm–zona pellucida interaction. Asian J Androl 13, 88–96.Google Scholar
Reis, LSLS, Ramos, AA, Camargos, AS and Oba, E (2014) Effect of manganese supplementation on the membrane integrity and the mitochondrial potential of the sperm of grazing Nellore bulls. Anim Reprod Sci 150(1–2), 1–6.Google Scholar
Revell, SG and Mrode, RA (1994) An osmotic resistance test for bovine semen. Anim Reprod Sci 36, 77–86.Google Scholar
Rivlin, J, Mendel, J, Rubinstein, S, Etkovitz, N and Breitbart, H (2004) Role of hydrogen peroxide in sperm capacitation and acrosome reaction. Biol Reprod 70, 518–522.Google Scholar
Roblero, L, Guadarrama, A, Lopez, T and Zegers-Hochschild, F (1996) Effect of copper ion on the motility, viability, acrosome reaction and fertilizing capacity of human spermatozoa in vitro . Reprod Fertil Dev 8, 871–874.Google Scholar
Roy, SC and Atreja, SK (2008) Effect of reactive oxygen species on capacitation and associated protein tyrosine phosphorylation in buffalo (Bubalus bubalis) spermatozoa. Anim Reprod Sci 107(1–2), 68–84.Google Scholar
Shamsi, MB, Kumar, R and Dada, R (2008) Evaluation of nuclear DNA damage in human spermatozoa in men opting for assisted reproduction. Indian J Med Res 127, 115–123.Google Scholar
Shur, BD and Neely, CA (1988) Plasma membrane association, purification, and partial characterization of mouse sperm beta-1,4-galactosyltransferase. J Biol Chem 263(33), 17706–17714.Google Scholar
Sikka, SC (1996) Oxidative stress and role of antioxidants in normal and abnormal sperm function. Front Biosci 1, e78–e86.Google Scholar
Sinowatz, F, Töpfer‐Petersen, E, Kölle, S and Palma, G (2001) Functional morphology of the zona pellucida. Anat Histol Embryol 30, 257–263.Google Scholar
Slater, TF, Sawyer, B and Sträuli, U (1963) Studies on succinate-tetrazolium reductase systems. Biochim Biophys Acta 77, 383–393.Google Scholar
Storey, BT (2008) Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52(5–6), 427–437.Google Scholar
Tosic, J and Walton, A (1946) Formation of hydrogen peroxide by spermatozoa and its inhibitory effect of respiration. Nature 158, 485.Google Scholar
Underwood, EJ and Suttle, NF (1999) The Mineral Nutrition of Livestock, 3rd edn. Wallingford: CABI.Google Scholar
Ursini, F, Heim, S, Kiess, M and Flohé, L (1999) Dual function of the selenoprotein PHGPx during sperm maturation. Science 285(5432), 1393–1396.Google Scholar
Varghese, AC Sinha, B and Bhattacharyya, AK (2005) Current trends in evaluation of sperm function: in vitro selection and manipulation of male gametes for assisted conception. Indian J Exp Biol 43, 1023–1031.Google Scholar
Wassarman, PM (1990) Regulation of mammalian fertilization by zona pellucida glycoproteins. J Reprod Fertil Suppl 42, 79–87.Google Scholar
Wassarman, PM and Litscher, ES (2008) Mammalian fertilization: the egg’s multifunctional zona pellucida. Int J Dev Biol 52(5–6), 665–676.Google Scholar
Zhang, BR, Larsson, B, Lundeheim, N, Håård, MG and Rodriguez-Martinez, H (1999) Prediction of bull fertility by combined in vitro assessments of frozen–thawed semen from young dairy bulls entering an AI-programme. Int J Androl 22, 253–260.Google Scholar