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Kinematic, bioenergetic and oxidative evaluations of donkey sperm preserved at +4°C

Published online by Cambridge University Press:  14 April 2020

Tommaso Di Palma ,
Stefano Cecchini ,
Giuseppe Macchia ,
Maria Pia Pasolini ,
Natascia Cocchia  and
Raffaele Boni Open the ORCID record for Raffaele Boni [Opens in a new window]
Tommaso Di Palma
Affiliation:
Department of Sciences, University of Basilicata, 85100Potenza, Italy Department of Veterinary Medicine and Animal Production, University of Naples Federico II, 80137Naples, Italy
Stefano Cecchini
Affiliation:
Department of Sciences, University of Basilicata, 85100Potenza, Italy
Giuseppe Macchia*
Affiliation:
Department of Sciences, University of Basilicata, 85100Potenza, Italy Department of Veterinary Medicine and Animal Production, University of Naples Federico II, 80137Naples, Italy
Maria Pia Pasolini
Affiliation:
Department of Veterinary Medicine and Animal Production, University of Naples Federico II, 80137Naples, Italy
Natascia Cocchia
Affiliation:
Department of Veterinary Medicine and Animal Production, University of Naples Federico II, 80137Naples, Italy
Raffaele Boni
Affiliation:
Department of Sciences, University of Basilicata, 85100Potenza, Italy
*
Address for correspondence: R. Boni. Campus di Macchia Romana, Via dell’Ateneo Lucano, 10 – 85100Potenza, Italy. E-mail: [email protected]
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Summary

Information on donkey sperm bioenergetics, kinetics and oxidative status is scarce even though crucial for development of reproductive technologies and germplasm conservation. For these reasons, it is interesting to monitor sperm kinetics, bioenergetics, and oxidative status during sperm storage at +4°C and with several sperm extenders and concentrations. Donkey semen was collected from three jackasses, three times each. It was diluted with four extenders (Kenney, Equiplus, INRA96 or Hippex), set at three sperm concentrations (30, 50 or 70 × 106 spermatozoa/ml) and evaluated for its functionality after 0, 3, 24, 48 and 72 h storage at +4°C. Sperm kinetics was analyzed by Sperm Computer Analysis; sperm bioenergetics was assessed by mitochondrial membrane potential (MMP); sperm oxidative status was evaluated by lipid peroxidation (LPO), anti-LPO potential and nitroblue tetrazolium (NBT) assays. Incubation produced a progressive (P < 0.01) decline in sperm kinetics and MMP, whereas parameters related to oxidative status either increased (LPO, NBT) or decreased (anti-LPO). The anti-LPO potential was the index better related to sperm motility and kinetics. Extenders proved to be differently (P < 0.01) effective in preserving sperm kinetics, MMP, and oxidative status. The concentration of 30 × 106 spermatozoa/ml provided an optimum preservation of sperm functions. Significant correlations emerged between most parameters examined. This study identified reference criteria for storing donkey spermatozoa at +4°C. A low sperm concentration together with a proper extender are crucial requirements for optimum sperm cryopreservation efficiency. Field trials are, however, required to validate these findings, making them operational in practice.

Keywords

DonkeyCryopreservationMitochondrial membrane potentialOxidative stressSpermatozoa
Type
Research Article
Information
Zygote , Volume 28 , Issue 4 , August 2020 , pp. 300 - 307
Copyright
© Cambridge University Press 2020

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References

Aitken, RJ (2018) Nitroblue tetrazolium (NBT) assay. Reprod Biomed Online 36, 90–1.CrossRefGoogle ScholarPubMed
Ali, SS, Marcondes, M-CG, Bajova, H, Dugan, LL and Conti, B (2010) Metabolic depression and increased reactive oxygen species production by isolated mitochondria at moderately lower temperatures. J Biol Chem 285, 32522–8.CrossRefGoogle ScholarPubMed
Alonso, C, Castañeira, C, Castex, CB, Ferrante, A, Arraztoa, C, Flores, A, Gambarotta, M, Miragaya, M and Losinno, L (2017) Effects of extenders and centrifugation on viability of donkey cooled semen. Preliminary results. In Proceedings of 1st International Symposium on Donkey Science, pp. 196–200.Google Scholar
Alvarez, A, Serres, C, Crespo, F, Santiago, I, Mateos, E and Gómez-Cuétara, C (2004) Natural service and artificial insemination with cooled semen of Zamorano-Leonés donkey. In Proceedings of the 15th International Congress. Anim Reprod 2, 393.Google Scholar
Aurich, C (2005) Factors affecting the plasma membrane function of cooled-stored stallion spermatozoa. Anim Reprod Sci 89, 65–75.CrossRefGoogle ScholarPubMed
Baehner, RL, Boxer, LA and Davis, J (1976) The biochemical basis of nitroblue tetrazolium reduction in normal human and chronic granulomatous disease polymorphonuclear leukocytes. Blood 48, 309–13.CrossRefGoogle ScholarPubMed
Ball, BA (2008) Oxidative stress, osmotic stress and apoptosis: impacts on sperm function and preservation in the horse. Anim Reprod Sci 107, 257–67.CrossRefGoogle Scholar
Ball, B and Anthony, V (2002) Detection of lipid peroxidation in equine spermatozoa based upon the lipophilic fluorescent dye C11-BODIPY581/591. J Androl 23, 259–69.Google Scholar
Ball, B, Medina, V, Gravance, C and Baumber, J (2001) Effect of antioxidants on preservation of motility, viability and acrosomal integrity of equine spermatozoa during storage at 5°C. Theriogenology 56, 577–89.CrossRefGoogle ScholarPubMed
Baumber, J and Ball, BA (2005) Determination of glutathione peroxidase and superoxide dismutase-like activities in equine spermatozoa, seminal plasma, and reproductive tissues. Am J Vet Res 66, 1415–19.CrossRefGoogle ScholarPubMed
Baumber, J, Ball, BA, Gravace, CG, Medina, V and Davies-Morel, MC (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 ScholarPubMed
Boni, R, Gallo, A and Cecchini, S (2017) Kinetic activity, membrane mitochondrial potential, lipid peroxidation, intracellular pH and calcium of frozen/thawed bovine spermatozoa treated with metabolic enhancers. Andrology 5, 133–45.CrossRefGoogle ScholarPubMed
Brinsko, S, Crockett, E and Squires, E (2000) Effect of centrifugation and partial removal of seminal plasma on equine spermatozoal motility after cooling and storage. Theriogenology 54, 129–36.CrossRefGoogle ScholarPubMed
Camillo, F, Rota, A, Biagini, L, Tesi, M, Fanelli, D and Panzani, D (2018) The current situation and trend of donkey industry in Europe. J Equine Vet Sci 65, 44–9.CrossRefGoogle Scholar
Cocchia, N, Pasolini, M, Mancini, R, Petrazzuolo, O, Cristofaro, I, Rosapane, I, Sica, A, Tortora, G, Lorizio, R and Paraggio, G (2011) Effect of sod (superoxide dismutase) protein supplementation in semen extenders on motility, viability, acrosome status and ERK (extracellular signal-regulated kinase) protein phosphorylation of chilled stallion spermatozoa. Theriogenology 75, 1201–10.CrossRefGoogle ScholarPubMed
Cochran, J, Amann, R, Froman, D and Pickett, B (1984) Effects of centrifugation, glycerol level, cooling to 5 C, freezing rate and thawing rate on the post-thaw motility of equine sperm. Theriogenology 22, 25–38.CrossRefGoogle ScholarPubMed
Contri, A, De Amicis, I, Veronesi, MC, Faustini, M, Robbe, D and Carluccio, A (2010) Efficiency of different extenders on cooled semen collected during long and short day length seasons in Martina Franca donkey. Anim Reprod Sci 120, 136–41.CrossRefGoogle ScholarPubMed
Contri, A, De Amicis, I, Molinari, A, Faustini, M, Gramenzi, A, Robbe, D and Carluccio, A (2011) Effect of dietary antioxidant supplementation on fresh semen quality in stallion. Theriogenology 75, 1319–26.CrossRefGoogle ScholarPubMed
Cortés-Gutiérrez, E, Crespo, F, Gosalvez, A, Davila-Rodriguez, M, López-Fernández, C and Gosalvez, J (2008) DNA fragmentation in frozen sperm of Equus asinus: Zamorano-Leonés, a breed at risk of extinction. Theriogenology 69, 1022–32.CrossRefGoogle Scholar
Cottorello, A, Amancio, R, Henry, M and Borges, I (2002) Effect of storage temperature and extenders on in vitro activity of donkey spermatozoa. Theriogenology 58, 325–8.Google Scholar
Darr, CR, Cortopassi, GA, Datta, S, Varner, DD and Meyers, SA (2016) Mitochondrial oxygen consumption is a unique indicator of stallion spermatozoal health and varies with cryopreservation media. Theriogenology 86, 1382–92.CrossRefGoogle ScholarPubMed
Darr, CR, Moraes, LE, Scanlan, TN, Baumber-Skaife, J, Loomis, PR, Cortopassi, GA and Meyers, SA (2017) Sperm mitochondrial function is affected by stallion age and predicts post-thaw motility. J Equine Vet Sci 50, 52–61.CrossRefGoogle Scholar
Del Prete, C, Tafuri, S, Ciani, F, Pasolini, M, Ciotola, F, Albarella, S, Carotenuto, D, Peretti, V and Cocchia, N (2018) Influences of dietary supplementation with Lepidium meyenii (Maca) on stallion sperm production and on preservation of sperm quality during storage at 5C. Andrology 6, 351–61.CrossRefGoogle Scholar
Demyda-Peyras, S, Bottrel, M, Acha, D, Ortiz, I, Hidalgo, M, Carrasco, J, Gómez-Arrones, V, Gosalvez, J and Dorado, J (2018) Effect of cooling rate on sperm quality of cryopreserved Andalusian donkey spermatozoa. Anim Reprod Sci 193, 201–8.CrossRefGoogle ScholarPubMed
Dorado, J, Acha, D, Ortiz, I, Gálvez, M, Carrasco, J, Díaz, B, Gómez-Arrones, V, Calero-Carretero, R and Hidalgo, M (2013) Relationship between conventional semen characteristics, sperm motility patterns and fertility of Andalusian donkeys (Equus asinus). Anim Reprod Sci 143, 64–71.CrossRefGoogle Scholar
Gallo, A, Menezo, Y, Dale, B, Coppola, G, Dattilo, M, Tosti, E and Boni, R (2018) Metabolic enhancers supporting 1-carbon cycle affect sperm functionality: an in vitro comparative study. Sci Rep 8, 11769.CrossRefGoogle Scholar
Gibb, Z, Lambourne, SR and Aitken, RJ (2014) The paradoxical relationship between stallion fertility and oxidative stress. Biol Reprod 91, 77.CrossRefGoogle ScholarPubMed
Gloria, A, Contri, A, De Amicis, I, Robbe, D and Carluccio, A (2011) Differences between epididymal and ejaculated sperm characteristics in donkey. Anim Reprod Sci 128, 117–22.CrossRefGoogle ScholarPubMed
Johannisson, A, Figueiredo, M, Al-Kass, Z and Morrell, J (2018) Simultaneous evaluation of superoxide content and mitochondrial membrane potential in stallion semen samples provides additional information about sperm quality. Anim Reprod Sci 192, 290–7.CrossRefGoogle ScholarPubMed
Kenney, R (1975) Minimal contamination techniques for breeding mares: techniques and preliminary findings. Proceedings of the American Association of Equine Practitioners, pp. 327–36.Google Scholar
Orhan, H, Gurer-Orhan, H, Vriese, E, Vermeulen, N and Meerman, J (2006) Application of lipid peroxidation and protein oxidation biomarkers for oxidative damage in mammalian cells. A comparison with two fluorescent probes. Toxicol In Vitro 20, 1005–13.CrossRefGoogle Scholar
Quartuccio, M, Marino, G, Zanghì, A, Garufi, G and Cristarella, S (2011) Testicular volume and daily sperm output in Ragusano donkeys. J Equine Vet Sci 31, 143–6.CrossRefGoogle Scholar
Restrepo, G, Varela, E, Duque, JE, Gómez, JE and Rojas, M (2019) Freezing, vitrification, and freeze-drying of equine spermatozoa: impact on mitochondrial membrane potential, lipid peroxidation, and DNA integrity. J Equine Vet Sci 72, 8–15.CrossRefGoogle ScholarPubMed
Rook, G, Steele, J, Umar, S and Dockrell, H (1985) A simple method for the solubilisation of reduced NBT, and its use as a colorimetric assay for activation of human macrophages by γ-interferon. J Immunol Methods 82, 161–7.CrossRefGoogle ScholarPubMed
Rota, A, Magelli, C, Impeduglia, R, Panzani, D and Camillo, F (2005) Effect of extender and method of preservation on motility of cooled stallion spermatozoa. Anim Reprod Sci 89, 281.Google ScholarPubMed
Rota, A, Magelli, C, Panzani, D and Camillo, F (2008) Effect of extender, centrifugation and removal of seminal plasma on cooled-preserved Amiata donkey spermatozoa. Theriogenology 69, 176–85.CrossRefGoogle ScholarPubMed
Rota, A, Sgorbini, M, Panzani, D, Bonelli, F, Baragli, P, Ille, N, Gatta, D, Sighieri, C, Casini, L and Maggiorelli, M (2018) Effect of housing system on reproductive behaviour and on some endocrinological and seminal parameters of donkey stallions. Reprod Dom Anim 53, 40–7.CrossRefGoogle ScholarPubMed
Sabeur, K and Ball, BA (2006) Detection of superoxide anion generation by equine spermatozoa. Am J Vet Res 67, 701–6.CrossRefGoogle ScholarPubMed
Santos, G, Henry, M, Sampaio, I and Gastal, E (1995) Effect of cooling system and rate of cooling on sperm quality of donkey semen preserved at 5°C. Biol Reprod 52, 761–7.CrossRefGoogle Scholar
Serres, C, Rodriguez, A, Alvarez, A, Santiago, I, Gabriel, J, Gómez-Cuétara, C and Mateos, E (2002) Effect of centrifugation and temperature on the motility and plasma membrane integrity of Zamorano-Leonés donkey semen. Theriogenology 58, 329–32.Google Scholar
Sim Choi, H, Woo Kim, J, Cha, YN and Kim, C (2006) A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoassay Immunochem 27, 31–44.CrossRefGoogle Scholar
Starkey, P and Starkey, M (2000) Regional and world trends in donkey populations. (eds) P Starkey and D Fielding, pp. 10–21.Google Scholar
Tunc, O, Thompson, J and Tremellen, K (2010) Development of the NBT assay as a marker of sperm oxidative stress. Int J Androl 33, 13–21.CrossRefGoogle ScholarPubMed
Vidament, M, Vincent, P, Martin, F-X, Magistrini, M and Blesbois, E (2009) Differences in ability of jennies and mares to conceive with cooled and frozen semen containing glycerol or not. Anim Reprod Sci 112, 22–35.CrossRefGoogle ScholarPubMed
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