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Absence of beneficial effects on rabbit sperm cell cryopreservation by several antioxidant agents

Published online by Cambridge University Press:  22 August 2013

M.J. Maya-Soriano ,
E. Taberner ,
M. Sabés-Alsina ,
M. Piles  and
M. Lopez-Bejar
M.J. Maya-Soriano
Affiliation:
Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Autònoma de Barcelona, Barcelona, Spain.
E. Taberner
Affiliation:
Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Autònoma de Barcelona, Barcelona, Spain.
M. Sabés-Alsina
Affiliation:
Department of Animal Health and Anatomy, Veterinary Faculty, Universitat Autònoma de Barcelona, Barcelona, Spain.
M. Piles
Affiliation:
Unitat de Cunicultura, Institut de Recerca i Tecnologia Agroalimentàries, Torre Marimón s/n, 08182’ Caldes de Montbui, Barcelona, Spain.
M. Lopez-Bejar*
Affiliation:
Department of Animal Health and Anatomy Faculty of Veterinary, Universitat Autònoma de Barcelona, Edifici V, Campus UAB, 08193 Barcelona, Spain.
*
All correspondence to: M. Lopez-Bejar. Department of Animal Health and Anatomy Faculty of Veterinary, Universitat Autònoma de Barcelona, Edifici V, Campus UAB, 08193 Barcelona, Spain. Tel: +34 93 5814615. Fax: +34 93 5812006. e-mail: manel.lopez.bejar@uab.cat or mj.maya.soriano@gmail.com
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Summary

The generation of reactive oxygen species associated with cryopreservation could be responsible for mammalian sperm damage and the limitable value of stored semen in artificial insemination. The aim of this study was to assess several antioxidant agents supplemented in a commercial freezing extender (Gent B®) in order to improve post-thaw rabbit sperm quality. Ejaculates of 26 New Zealand White rabbit bucks were collected, evaluated and frozen using a conventional protocol. Antioxidant agents were tested at different concentrations: bovine serum albumin (BSA; 5, 30 or 60 mg/ml), retinol (RO; 50, 100 or 200 μM) and retinyl (RI; 0.282 or 2.82 μg/ml). Per cent viability, morphological abnormalities and intact acrosomes were determined using eosin–nigrosin staining. Motility and progressivity were analyzed by computer-assisted sperm analysis (CASA). In general, all sperm quality parameters were negatively affected by the cryopreservation process, the largest effect seen was for total motility. The addition of antioxidant agents did not improve thaw sperm quality. Furthermore, for RI groups a significant decrease in sperm quality parameters was recorded. In conclusion, rabbit sperm quality is negatively affected by the cryopreservation process. To our knowledge this report is the first using these antioxidants to supplement rabbit freezing extender. BSA and RO at concentrations used in the study did not improve sperm quality parameters after thawing, whereas RI supplementation appeared to be toxic. More studies are required to find the appropriate antioxidants necessary and their most effective concentrations to improve rabbit post-thaw sperm quality.

Keywords

Bovine serum albuminRabbitRetinolRetinylSpermatozoa
Type
Research Article
Information
Zygote , Volume 23 , Issue 1 , February 2015 , pp. 1 - 10
Copyright
Copyright © Cambridge University Press 2013 

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References

Agarwal, A., Prahakaran, S.A. & Said, T.M. (2005). Prevention of oxidative stress injury to sperm. J. Androl. 26, 653–60.Google Scholar
Agarwal, A., Prabakaran, S. & Allamaneni, S. (2006). What an andrologist/urologist should know about free radicals and why. Urology 67, 2–8.CrossRefGoogle ScholarPubMed
Aitken, R.J. & Fisher, H. (1994). Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. Bio-assays 16, 259–67.Google Scholar
Aitken, R.J., Gordon, E., Harkiss, D., Twigg, J.P.I., Milne, P., Jennigs, Z. & Irvine, D.S. (1998). Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol. Reprod. 59, 1037–46.Google Scholar
Aitken, R.J., Ryan, A.L., Baker, M.A. & McLaughlin, E.A. (2004). Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic. Biol. Med. 36, 994–1010.Google Scholar
Alvarez, J.G. & Storey, B.T. (1989). Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res. 23, 77–90.Google Scholar
Anghel, A., Zamfirescu, S., Coprean, D. & Sogorescu, E. (2009). The effects of cysteine, bovine serum albumin and vitamin E on the qualitative parameters of frozen–thawed ram semen. Annals RSCB 14, 97–103.Google Scholar
Aurich, J.E., Schonherr, U., Hoppe, H. & Aurich, C. (1997). Effect of antioxidants on motility and membrane integrity of chilled-stored stallion semen. Theriogenology 48, 185–92.Google Scholar
Bailey, J.L., Bilodeau, J.F. & Cormier, N. (2000). Semen cryopreservation in minireview domestic animals: a damaging and capacitating phenomenon. J. Androl. 21, 1–7.Google Scholar
Bamba, K. (1988). Evaluation of acrosomal integrity of boar spermatozoa by bright field microscopy using an eosin–nigrosin stain. Theriogenology 29, 1245–51.Google Scholar
Baumber, J., Ball, B.A., Gravance, C.G., Medina, V. & Davies-Morel, M.C.G. (2000). The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential and membrane lipid peroxidation. J. Androl. 21, 895–902.Google Scholar
Baumber, J., Ball, B.A. & Linfor, J.J. (2005). Assessment of the cryopreservation of equine spermatozoa in the presence of enzyme scavengers and antioxidants. Am. J. Vet. Res. 66, 772–9.Google Scholar
Beconi, M.T., Affranchino, M.A., Schang, L.M. & Beorlegui, N.B. (1991). Influence of antioxidants on SOD activity in bovine sperm. Biochem. Int. 23, 545–53.Google Scholar
Beconi, M.T., Francia, C.R., Mora, N.G. & Affranchino, M.A. (1993). Effect of natural antioxidants on frozen bovine semen preservation. Theriogenology 40, 841–51.Google Scholar
Bennetts, L.E. & Aitken, J.R. (2005). A comparative study of oxidative DNA damage in mammalian spermatozoa. Mol. Reprod. Dev. 71, 77–87.CrossRefGoogle ScholarPubMed
Bilodeau, J.F., Chatterjee, S., Sirard, M.A. & Gagnon, C. (2000). Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing. Mol. Reprod. Dev. 55, 282–8.Google Scholar
Bilodeau, J.F., Blanchette, S., Gagnon, I.C. & Sirard, M.A. (2001). Thiols prevent H2O2-mediated loss of sperm motility in cryopreserved bull semen. Theriogenology 56, 275–86.Google Scholar
Bolet, G., Brun, J.M., Monnerot, M., Abeni, F., Arnal, C., Arnold, J., et al. (2000). Evaluation and conservation of European rabbit (Oryctolagus cuniculus) genetic resources. First results and inferences. World Rabbit Sci. 8(A), 281–315.Google Scholar
Bucak, M.N., Atessahin, A. & Yüce, A. (2008). Effect of anti-oxidants and oxidative stress parameters on ram semen after the freeze–thawing process. Small Rumin. Res. 77, 128–34.Google Scholar
Bucak, M.N., Tuncer, P.B., Sanözkan, S., Baspinar, N., Taspinar, M., Coyan, K., Bilgili, A., Akalin, P.P., Büyükleblebici, S., Aydos, S., Ilgaz, S., Sunguroglu, A. & Oztuna, D. (2010). Effects of antioxidants on post-thawed bovine sperm and oxidative stress parameters. Cryobiology 61, 248–53.Google Scholar
Buhr, M.M., Curtis, E.F. & Kakuda, N. (1994). Effect of boar sperm cryopreservation on the composition and behaviour of head membrane lipids. Cryobiology 31, 224–38.Google Scholar
Calamera, J.C., Fernandez, P.J., Buffone, M.G., Acosta, A.A. & Doncel, G.F. (2001). Effects of long-term in vitro incubation of human spermatozoa: functional parameters and catalase effect. Andrologia. 33, 79–86.Google Scholar
Castellini, C., Lattaioli, P., Bernardini, M. & Dal Bosco, A. (2000). Effect of dietary α-tocopheryl acetate and ascorbic acid on rabbit semen stored at 5°C. Theriogenology 54, 523–5.Google Scholar
Castellini, C., Cardinali, R., Dal Bosco, A., Minelli, A. & Camici, O. (2006). Lipid composition of the main fractions of rabbit semen. Theriogenology 65, 703–12.CrossRefGoogle ScholarPubMed
Chatterjee, S. & Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing and thawing. Mol. Reprod. Dev. 59, 452–8.CrossRefGoogle ScholarPubMed
Chen, Y., Foote, R.H. & Brockett, C.C. (1993). Effect of sucrose, trehalose, hypotaurine, taurine, and blood serum on survival of frozen bull sperm. Cryobiology 30, 423–31.Google Scholar
Darin-Bennet, A. & White, I.G. (1977). Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold shock. Cryobiology 14, 466–70.CrossRefGoogle Scholar
De Lamirande, E. & Gagnon, C. (1992). Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J. Androl. 13, 379–86.Google Scholar
Denniston, D.J., Squires, E.L., Bruemmer, J.E., Brinsko, S.P., McCue, P.M. & Graham, J.K. (2000). Effect of antioxidants on the motility and viability of cooled stallion spermatozoa. J. Reprod. Fertil. Suppl. 56, 121–6.Google Scholar
Di Mascio, P., Kaiser, S. & Sies, H. (1989). Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch. Biochem. Biophys. 274, 532–8.Google Scholar
El-Kon, I. (2011). Testing usability of bovine serum albumin (BSA) for preservation of Egyptian buffalo semen. American–Eurasian J. Agric. Environ. Sci. 11, 495–502.Google Scholar
Eulenberger, K., Schäfer-Somi, S. & Aurich, C. (2009). Effect of different concentrations of ascorbic acid on motility, membrane integrity and chromatin status of frozen–thawed canine spermatozoa within six hours of storage at 37°C. Reprod. Dom. Anim. 44(Suppl. 2), 354–8.CrossRefGoogle Scholar
Foote, R.H. & Carney, E.W. (2000). The rabbit as a model for reproductive and developmental toxicity studies. Reprod. Toxicol. 14, 477–93.CrossRefGoogle Scholar
Foote, R.H., Chen, Y., Brockett, C.C. & Kaproth, M.T. (1993). Fertility of bull spermatozoa frozen in whole milk extender with trehalose, taurine, or blood serum. J. Dairy Sci. 76, 1908–13.Google Scholar
Ford, W.C.L. (2004). Regulation of sperm function by reactive oxygen species. Hum. Reprod. Update 10, 387–99.Google Scholar
Funahashi, H. & Sano, T. (2005). Select antioxidants improve the function of extended boar semen stored at 10°C. Theriogenology 6, 1605–16.Google Scholar
Griveau, J.F. & Le Lannou, D. (1997). Reactive oxygen species and human spermatozoa: physiology and pathology. Int. J. Androl. 20, 61–9.Google Scholar
Gómez, E.A., Rafel, O. & Ramon, J. (2002). The Caldes strain (Spain). Options Méditerr. B Études et Rech. 38, 193–8.Google Scholar
Guthrie, H.D. & Welch, G.R. (2006). Determination of intracellular reactive oxygen species and high mitochondrial membrane potential in Percoll-treated viable boar sperm using fluorescence-activated flow cytometry. J. Anim. Sci. 84, 2089–100.Google Scholar
Hajializadeh, N., Babaei, H., Nematollahi-Mahani, S.N. & Azizollahi, S. (2008). The development of mouse early embryos in vitro in fibroblasts and cumulus cells co-cultures supplemented with retinoic acid. Iranian J. Vet. Res. 9, 1–8.Google Scholar
Hammerstedt, R.H., Graham, J.K. & Nolan, J.P. (1990). Cryopreservation of mammalian sperm: what we ask them to survive. J. Androl. 11, 73–88.Google Scholar
Holt, W.V. (2000). Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 53, 47–58.Google Scholar
Holt, W.V. & North, R.D. (1994). Effects of temperature and restoration of osmotic equilibrium during thawing on the induction of plasma membrane damage in cryopreserved ram spermatozoa. Biol. Reprod. 51, 414–24.Google Scholar
La Falci, V.S.N., Yrjo-Koskinen, A.E., Fazeli, A., Holt, W.V. & Watson, P.F. (2011). Antioxidant combinations are no more beneficial than individual components in combating ram sperm oxidative stress during storage at 5°C. Anim. Reprod. Sci. 129, 180–7.Google Scholar
Lasso, J.L., Noiles, E.E., Alvarez, J.G. & Storey, B.T. (1994). Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation. J. Androl. 15, 255–65.Google Scholar
Lewis, S.E.M., Sterling, E.S.L., Young, I.S. & Thompson, W. (1997). Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil. Steril. 67, 142–7.CrossRefGoogle ScholarPubMed
Lima, P.F., Oliveira, M.A., Gonçalves, P.B., Montagner, M.M., Reichenbach, H.D., Weppert, M., Neto, C.C., Pina, V.M. & Santos, M.H. (2004). Effects of retinol on the in vitro development of Bos indicus embryos to blastocysts in two different culture systems. Reprod. Domest. Anim. 39, 356–60.Google Scholar
Liu, E., Kitajima, S., Wiese, E., Reifenberg, K., Morimoto, M., Watanabe, T. & Fan, J. (2007). Re-establishment of complement C6-deficient rabbit colony by cryopreserved sperm transported from abroad. Exp. Anim. 56, 167–71.Google Scholar
Livingston, T., Eberhardt, D., Edwards, J.L. & Godkin, J. (2004). Retinol improves bovine embryonic development in vitro. Reprod. Biol. Endocrinol. 2, 83.Google Scholar
Lopez-Gatius, F., Sances, G., Sancho, M., Yaniz, J., Santolaria, P., Gutierrez, R., Nuñez, M., Nuñez, J. & Soler, C. (2005). Effect of solid storage at 15 °C on the subsequent motility and fertility of rabbit semen. Theriogenology 64, 252–60.Google Scholar
Maia, M. da S., Bicudo, S.D., Sicherle, C.C., Rodello, L. & Gallego, I.C. (2010). Lipid peroxidation and generation of hydrogen peroxide in frozen–thawed ram semen cryopreserved in extenders with antioxidants. Anim. Reprod. Sci. 122 (1–2), 118–23.Google Scholar
Marco-Jiménez, F., Lavara, R., Vicente, J.S. & Viudes-de-Castro, M.P. (2006). Cryopreservation of rabbit spermatozoa with freezing media supplemented with reduced and oxidised glutathione. Cryoletters 27, 261–8.Google Scholar
Martí, E., Marti, J.I., Muiño-Blanco, T. & Cebrián-Pérez, J.A. (2008). Effect of the cryopreservation process on the activity and immunolocalization of antioxidant enzymes in ram spermatozoa. J. Androl. 29, 459–67.Google Scholar
Matsuoka, T., Imai, H., Kohno, H. & Fukui, Y. (2006). Effects of bovine serum albumine and trehalose in semen diluents for improvement of frozen–thawed ram spermatozoa. J. Reprod. Dev. 52, 675–83.Google Scholar
Maxwell, W.M.C. & Stojanov, T. (1996). Liquid storage of ram semen in the absence or presence of some antioxidants. Reprod. Fert. Dev. 32, 353–60.Google Scholar
Medeiros, C.M., Forell, F., Oliveira, A.T. & Rodrigues, J.L. (2002). Current status of sperm cryopreservation: why isn't it better? Theriogenology 57, 327–44.Google Scholar
Michael, A., Alexopoulos, C., Pontiki, E., Hadjipavlou-Litina, D., Saratsis, P. & Boscos, C. (2007). Effect of antioxidant supplementation on semen quality and reactive oxygen species of frozen–thawed canine spermatozoa. Theriogenology 68, 204–12.Google Scholar
Moce, E. & Vicente, J.S. (2009). Rabbit sperm cryopreservation: a review. Anim. Reprod. Sci. 110, 1–24.Google Scholar
Neagu, V.R., García, B.M., Sandoval, C.S., Rodríguez, A.M., Ferrusola, C.O., Fernández, L.G., Tapia, J.A. & Peña, F.J. (2010). Freezing dog semen in presence of the antioxidant butylated hydroxytoluene improves postthaw sperm membrane integrity. Theriogenology 73, 645–50.Google Scholar
Neild, D.M., Gabella, B.M., Chaves, M.G., Miragaya, M.H., Colenbrander, B. & Aguero, A. (2003). Membrane changes during different stages of a freeze–thaw protocol for equine semen cryopreservation. Theriogenology 59, 1693–705.Google Scholar
Parks, J.E. & Graham, J.K. (1992). Effects of cryopreservation procedures on sperm membranes. Theriogenology 38, 209–22.Google Scholar
Parks, J.E. & Lynch, D.V. (1992). Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology 29, 255–66.Google Scholar
Prathalingam, N.S., Holt, W.V., Revell, S.G., Mirczuk, S., Fleck, R.A. & Watson, P.F. (2006). Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology 66, 1894–900.Google Scholar
Rajesh, N., Shankar, M.B. & Deecaraman, M. (2010). Effect of vitamin A supplementation at different gaseous environments on in vitro development of pre-implantation sheep embryos to the blastocyst stage. Animal 4, 1884–90.Google Scholar
Roca, J., Martinez, S., Vazquez, J.M., Lucas, X., Parrilla, I. & Martinez, E.A. (2000). Viability and fertility of rabbit spermatozoa diluted in Tris-buffer extenders and stored at 15°C. Anim. Reprod. Sci. 64, 103–12.Google Scholar
Saleh, R.A. & Agarwal, A. (2002). Oxidative stress and male infertility: from research bench to clinical practise. J. Androl. 23, 737–52.Google Scholar
Sanocka, D.M. & Kurpisz, M. (2004). Reactive oxygen species and sperm cells. Reprod. Biol. Endocrinol. 2, 12–8.Google Scholar
Sinclair, S. (2000). Male infertility: nutritional and environmental considerations. Alternatives Med. Rev. 5, 28–38.Google Scholar
Sinha, M.P., Sinha, A.K., Singh, B.K. & Prasad, P.L. (1996). The effect of glutathione on the motility, enzyme leakage and fertility of frozen goat semen. Theriogenology 41, 237–243.Google Scholar
Storey, B.T. (1997). Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol. Hum. Reprod. 3, 203–13.Google Scholar
Szczesniak-Fabianczyk, B., Bochenek, M., Smorag, Z. & Silvestre, M.A. (2006). Effect of antioxidants added to boar semen extender on the semen survival time and sperm chromatin structure. Reprod. Biol. 3, 81–7.Google Scholar
Tuncer, P.B., Bucak, M.N., Büyükleblebici, S., Sarýözkan, S., Yeni, D., Eken, A., Akalýn, P.P., Kinet, H., Avdatek, F., Fidan, A.F. & Gündoðan, M. (2010). The effect of cysteine and glutathione on sperm and oxidative stress parameters of post-thawed bull semen. Cryobiology 61, 303–7.Google Scholar
Upreti, G.C., Jensen, K., Munday, R., Duganzich, D.M., Vishwanath, R. & Smith, J.F. (1998). Studies on aromatic amino acid oxidase activity in ram spermatozoa: role of pyruvate as an antioxidant. Anim. Reprod. Sci. 51, 275–87.Google Scholar
Uysal, O. & Bucak, N. (2007). Effects of oxidized glutathione, bovine serum albumin, cysteine and lycopene on the quality of frozen–thawed ram semen. Acta Vet. Brno. 76, 383–90.Google Scholar
Uysal, O., Korkmaz, T. & Tosun, H. (2005). Effect of bovine serum albumine on freezing of canine semen. Indian Vet. J. 82, 97–8.Google Scholar
Vahedi, V., Zeinoaldini, S., Kohram, H. & Farahavar, A. (2009). Retinoic acid effects on nuclear maturation of bovine oocytes in vitro. African J. Biotechnol. 8, 3974–8.Google Scholar
Vishwanath, R. & Shannon, P. (2000). Storage of bovine semen in liquid and frozen state, Anim. Reprod. Sci. 62, 23–53.Google Scholar
Viudes-de-Castro, M.P., Vicente, J.S. & Lavara, R. (1999). Effet du nombre de spermatozoides sur la fertilite de la semence conserve 24 heures chez le lapin. Ann. Zootech. 48, 407–12.Google Scholar
Waterhouse, K.E., Hofmo, P.O.Tverdal, A. & Miller, R.R. Jr. (2006). Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 131, 887–94.Google Scholar
Watson, P.F. (1995). Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7, 871–91.Google Scholar
Watson, P.F. (2000). The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60–61, 481–92.Google Scholar
White, I.G. (1993). Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod. Fertil. Dev. 5, 639–58.Google Scholar
Yousef, M.I., Abdallah, G.A. & Kamel, K.I. (2003). Effect of ascorbic acid and vitamin E supplementation on semen quality and biochemical parameters of male rabbits. Anim. Reprod. Sci. 76, 99–111.Google Scholar