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The addition of docosahexaenoic acid (DHA) and antioxidants (glutathione peroxidase and superoxide dismutase) in extenders to epididymal sperm cryopreservation in bulls

Published online by Cambridge University Press:  21 May 2018

João D.A. Losano ,
Daniel S.R. Angrimani ,
Bruno R. Rui ,
Luana C. Bicudo ,
Andressa Dalmazzo ,
Bárbara C.S. Silva ,
Carlos H.C. Viana ,
Camilla M. Mendes ,
Mayra E.O.A. Assumpção  and
Valquiria H. Barnabe
...Show all authors
João D.A. Losano
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Daniel S.R. Angrimani*
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Bruno R. Rui
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Luana C. Bicudo
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Andressa Dalmazzo
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Bárbara C.S. Silva
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Carlos H.C. Viana
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Camilla M. Mendes
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Mayra E.O.A. Assumpção
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Valquiria H. Barnabe
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
Marcilio Nichi
Affiliation:
Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil
*
All correspondence to: Daniel S.R. Angrimani. Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Orlando Marques de Paiva, 87-05508-270, São Paulo, Brazil. Tel: +55 11 30917914. Fax: +55 11 30917914. E-mail: angrimani@gmail.com
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Summary

The cryopreservation of epididymal sperm is an important technique that allows genetic material to be preserved, even post mortem. However, cryopreservation leads to increased oxidative stress and impaired sperm viability. Polyunsaturated fatty acid (PUFA) supplementation may improve certain sperm characteristics, but it also makes sperm more susceptible to oxidative stress, therefore adding antioxidants that counteract oxidative stress has become an option. In this context, this study aimed to evaluate the effect of the interaction between docosahexaenoic acid (DHA) and antioxidants on the quality after the cryopreservation of epididymal bull sperm. Twenty epididymides were collected after slaughter, and epididymal sperm was cryopreserved with bovine extender supplemented with docosahexaenoic acid (DHA), glutathione peroxidase (GPx) and superoxide dismutase (SOD). We verified an improvement in motility in the group that was treated only with DHA 5 µM and a concentration-dependent effect on susceptibility to lipid peroxidation that was associated with DHA concentration (1 µM, 5 µM or 10 µM). Moreover, treatment with DHA (5 µM) and SOD (20 IU/ml) resulted in higher sperm motility. Thus, the association between DHA (5 µM) and SOD (20 IU/ml) appears to be an option for increased epididymal sperm features in bulls.

Keywords

Bovine spermEpididymisLipid oxidationReactive oxygen species
Type
Research Article
Information
Zygote , Volume 26 , Issue 3 , June 2018 , pp. 199 - 206
Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

These authors contributed equally to this work.

References

Agarwal, A., Saleh, R.A. & Bedaiwy, M.A. (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79, 829–43.CrossRefGoogle ScholarPubMed
Aitken, R.J., Wingate, J.K., De Iuliis, G.N., Koppers, A.J. & McLaughlin, E.A. (2006). Cis-unsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J. Clin. Endocrinol. Metab. 91, 4154–63.Google Scholar
Aitken, R.J., Jones, K.T. & Robertson, S.A. (2012). Reactive oxygen species and sperm function-in sickness and in health. J. Androl. 33, 1096–106.Google Scholar
Angrimani, D.S.R., Lucio, C.F., Veiga, G.A.L., Silva, L.C.G., Regazzi, F.M., Nichi, M. & Vannucchi, C.I. (2014). Sperm maturation in dogs: sperm profile and enzymatic antioxidant status in ejaculated and epididymal spermatozoa. Andrologia 46, 814–9.CrossRefGoogle ScholarPubMed
Birben, E., Sahiner, U.M., Sackesen, C., Erzurum, S. & Kalayci. (2012). Oxidative stress and antioxidant defense. World Allergy Org. J. 5, 9–19.Google Scholar
Buege, J.A. & Aust, S.D. (1978). Microsomal lipid peroxidation. Methods Enzymol. 52, 302–10.Google Scholar
Ehling, C., Rath, D., Struckmann, C., Frenzel, A., Schindler, L. & Niemann, H. (2006). Utilization of frozen–thawed epididymal ram semen to preserve genetic diversity in Scrapie susceptible sheep breeds. Theriogenology 66, 2160–4.Google Scholar
Evenson, D. & Jost, L. (2000). Sperm chromatin structure assay is useful for fertility assessment. Methods Cell Sci. 22, 169–89.Google Scholar
Gomez, E., Irvine, D.S. & Aitken, R.J. (1998). Evaluation of a spectrophotometric assay for the measurement of malondialdehyde and 4-hydroxyalkenals in human spermatozoa: relationships with semen quality and sperm function. Int. J. Androl. 21, 81–94.CrossRefGoogle ScholarPubMed
Gurler, H., Calisici, O. & Bollwein, H. (2015). Inter- and intra-individual variability of total antioxidant capacity of bovine seminal plasma and relationships with sperm quality before and after cryopreservation. Anim. Reprod. Sci. 155, 99–105.Google Scholar
Halliwell, B. (1991). Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 91, S14–22.CrossRefGoogle ScholarPubMed
Hrudka, F. (1987). Cytochemical and ultracytochemical demonstration of cytochrome c oxidase in spermatozoa and dynamics of its changes accompanying ageing or induced by stress. Int. J. Androl. 10, 809– 28.Google Scholar
Jow, W.W., Schlegel, P.N., Cichon, Z., Phillips, D., Goldstein, M. & Bardin, C.W. (1993). Identification and localization of copper-zinc superoxide dismutase gene expression in rat testicular development. J. Androl. 14, 439–47.Google Scholar
Kaabi, M., Paz, P., Alvarez, M., Anel, E., Boixo, J.C., Rouissi, H., Herraez, P. & Anel, L. (2003). Effect of epididymis handling conditions on the quality of ram spermatozoa recovered post-mortem. Theriogenology 60, 1249– 59.CrossRefGoogle ScholarPubMed
Kaka, A., Haron, W., Yusoff, R., Yimer, N., Khumran, A.M., Sarsaifi, K., Behan, A.A., Kaka, U., Memon, A.A. & Ebrahimi, M. (2015). Effect of docosahexanoic acid on quality of frozen–thawed bull semen in BioXcell extender. Reprod. Fertil. Dev. 8, 2015.Google Scholar
Kobayashi, T., Miyazaki, T., Natori, M. & Nozawa, S. (1991). Protective role of superoxide dismutase in human sperm motility: superoxide dismutase activity and lipid peroxide in human seminal plasma and spermatozoa. Hum. Reprod. 6, 987–91.CrossRefGoogle ScholarPubMed
Lagergren, C.G. (1953). On the eosin-nigrosin stain and some other methods for the appraisal of sperm vitality with special reference to practical application. Annali di ostetricia e ginecologia 75, 998–1005.Google Scholar
Lenzi, A., Gandini, L., Lombardo, F., Picardo, M., Maresca, V., Panfili, E., Tramer, F., Boitani, C. & Dondero, F. (2002). Polyunsaturated fatty acids of germ cell membranes, glutathione and glutathione-dependent enzyme-PHGPx: from basic to clinic. Contraception 65, 301–4.CrossRefGoogle ScholarPubMed
Lenzi, A., Picardo, M., Gandini, L., Lombardo, F., Terminali, O., Passi, S. & Dondero, F. (1994). Glutathione treatment of dyspermia: effect on the lipoperoxidation process. Hum. Reprod. 9, 2044–50.Google Scholar
Lenzi, A., Gandini, L., Maresca, V., Rago, R., Sgro, P., Dondero, F. & Picardo, M. (2000a). Fatty acid composition of spermatozoa and immature germ cells. Mol. Hum. Reprod. 6, 226–31.Google Scholar
Lenzi, A., Gandini, L., Picardo, M., Tramer, F., Sandri, G. & Panfili, E. (2000b). Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids. (PUFA): scavenger mechanisms and possible scavenger therapies. Front. Biosci. 5, 1–15.Google Scholar
Losano, J.D.A., Padín, J.F., Méndez-Lópes, I., Angrimani, D.S.R., García, A.G., Barnabe, V.H. & Nichi, M. (2017). The stimulated glycolytic pathway is able to maintain ATP levels and kinetic patterns of bovine epididymal sperm subjected to mitochondrial uncoupling. Oxid. Med. Cell. Longev. 2017, 1–8.Google Scholar
Lucio, C.F., Silva, L.C., Regazzi, F.M., Angrimani, D.S.R., Nichi, M., Assumpcao, M.E.O.A. & Vannucchi, C.I. (2016). Effect of reduced glutathione (GSH) in canine sperm cryopreservation: in vitro and in vivo evaluation. Cryobiology 72, 135–40.Google Scholar
Mandal, R., Badyakar, D. & Chakrabarty, J. (2014). Role of membrane lipid fatty acids in sperm cryopreservation. Adv. Androl. 2014, Article ID 190542, 9 pp. doi.org/10.1155/2014/190542Google Scholar
Minervini, F., Guastamacchia, R., Pizzi, F., Dell'Aquila, M.E. & Barile, V.L. (2013). Assessment of different functional parameters of frozen–thawed buffalo spermatozoa by using cytofluorimetric determinations. Reprod. Domest. Anim. 48, 317–24.Google Scholar
Monton, A., Gil, L., Malo, C., Olaciregui, M., Gonzalez, N. & de Blas, I. (2015). Sage (Salvia officinalis) and fennel (Foeniculum vulgare) improve cryopreserved boar epididymal semen quality study. Cryoletters 36, 83–90.Google Scholar
Nair, S.J., Brar, A.S., Ahuja, C.S., Sangha, S.P. & Chaudhary, K.C. (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, 21–9.Google Scholar
Nasiri, A.H., Towhidi, A. & Zeinoaldini, S. (2012). Combined effect of DHA and alpha-tocopherol supplementation during bull semen cryopreservation on sperm characteristics and fatty acid composition. Andrologia 44 (Suppl. 1), 550–5.Google Scholar
Neagu, V.R., García, B.M., Rodriguez, A.M., Ferrusola, C.O., Bolanos, J.M., Fernandez, L.G., Tapia, J.A. & Pena, F.J. (2011). Determination of glutation peroxidase and superoxide dismutase activities in canine seminal plasma and its relation with sperm quality and lipid peroxidation post thaw. Theriogenology 75, 10–6.CrossRefGoogle ScholarPubMed
Nichi, M., Goovaerts, I.G., Cortada, C.N., Barnabe, V.H., De Clercq, J.B. & Bols, P.E. (2007). Roles of lipid peroxidation and cytoplasmic droplets on in vitro fertilization capacity of sperm collected from bovine epididymides stored at 4 and 34°C. Theriogenology 67, 334–40.CrossRefGoogle Scholar
Nichitailo, M.E. & Furmanov, I.A. (2007). [Aleksandr Alekseevich Shalimov–surgeon, scientist, prominent figure]. Klinichna khirurhiia/Ministerstvo okhorony zdorov'ia Ukrainy. Naukove tovarystvo khirurhiv Ukrainy pp. 3–5.Google Scholar
Nissen, H.P. & Kreysel, H.W. (1983). Polyunsaturated fatty acids in relation to sperm motility. Andrologia 15, 264–9.Google Scholar
Ohkawa, H., Ohishi, N., Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351–8.Google Scholar
Pope, C.E., Zhang, Y.Z. & Dresser, B.L. (1991). A simple staining method for evaluating acrosomal status of cat spermatozoa. J. Zoo. Wildlife. Med. 22, 87–95.Google Scholar
Roca, J., Rodriguez, M.J., Gil, M.A., Carvajal, G., Garcia, E.M., Cuello, C., Vazquez, J.M. & Martinez, E.A. (2005). Survival and in vitro fertility of boar spermatozoa frozen in the presence of superoxide dismutase and/or catalase. J. Androl. 26, 15–24.Google Scholar
Rooke, J.A., Shao, C.C. & Speake, B.K. (2001). Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 121, 315–22.Google Scholar
Sharma, P., Jha, A.B., Dubey, R.S. & Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, Article ID 217037, 26 pp. doi.org/10.1155/2012/217037Google Scholar
Simoes, R., Feitosa, W.B., Siqueira, A.F., Nichi, M., Paula-Lopes, F.F., Marques, M.G., Peres, M.A., Barnabe, V.H., Visintin, J.A. & Assumpcao, M.E. (2013). Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome. Reproduction 146, 433–41.CrossRefGoogle ScholarPubMed
Vernet, P., Aitken, R.J. & Drevet, J.R. (2004). Antioxidant strategies in the epididymis. Mol. Cell. Endocrinol. 216, 31–9.Google Scholar