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Lipid peroxidation in bull semen influences sperm traits and oxidative potential of Percoll®-selected sperm

Published online by Cambridge University Press:  05 April 2021

Vivian Cardoso Castiglioni Open the ORCID record for Vivian Cardoso Castiglioni [Opens in a new window] ,
Adriano Felipe Perez Siqueira ,
Luana de Cássia Bicudo ,
Tamie Guibu de Almeida ,
Thais Rose dos Santos Hamilton Open the ORCID record for Thais Rose dos Santos Hamilton [Opens in a new window] ,
Leticia Signori de Castro ,
Camilla Mota Mendes ,
Marcílio Nichi ,
João Diego de Agostini Losano Open the ORCID record for João Diego de Agostini Losano [Opens in a new window]  and
José Antônio Visitin
...Show all authors
Vivian Cardoso Castiglioni
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Adriano Felipe Perez Siqueira
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Luana de Cássia Bicudo
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Tamie Guibu de Almeida
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Thais Rose dos Santos Hamilton
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Leticia Signori de Castro
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Camilla Mota Mendes
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Marcílio Nichi
Affiliation:
Laboratory of Andrology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
João Diego de Agostini Losano
Affiliation:
Laboratory of Andrology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
José Antônio Visitin
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
Mayra Elena Ortiz D´Ávila Assumpção*
Affiliation:
Laboratory of Sperm Biology, Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
*
Author for correspondence: Mayra Elena Ortiz D´Ávila Assumpção Department of Animal Reproduction, College 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 30917665. Fax: +55 11 30917412. Email: [email protected]
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Summary

Although bovine embryo in vitro production (IVP) is a common assisted reproductive technology, critical points warrant further study, including sperm traits and oxidative status of sperm for in vitro fertilization (IVF). Our aim was to evaluate whether the lipid peroxidation index of commercial bull semen is influenced by sperm traits and oxidative status of sperm populations selected using Percoll® gradient. Semen straws from 48 batches from 14 Nelore bulls were thawed individually, analyzed for motility and subjected to Percoll selection. After Percoll, the lipid peroxidation index of the extender was evaluated, whereas selected sperm were analyzed for motility, acrosome and membrane integrity, mitochondrial membrane potential, chromatin resistance and oxidative potential under IVF conditions. Batches were divided retrospectively in four groups according to lipid peroxidation index. Sperm from Group 4 with the lowest index of lipid peroxidation had, after Percoll selection, greater plasma membrane integrity (81.3%; P = 0.004), higher mitochondrial potential (81.1%; P = 0.009) and lower oxidative potential (135.3 ng thiobarbituric acid reactive substances (TBARS)/ml; P = 0.026) compared with Group 1 with highest lipid peroxidation index (74.3%, 73% and 213.1 ng TBARS/ml, respectively). Furthermore, we observed negative correlations for the lipid peroxidation index with motility, membrane integrity and mitochondrial potential, and positive correlations with oxidative potential. In conclusion, oxidative stress in semen straws, as determined using lipid peroxidation in the extender, is associated with sperm traits and their oxidative potential under IVF conditions. These results provided further insights regarding the importance of preventing oxidative stress during semen handling and cryopreservation, as this could affect sperm selected for IVF. Finally, Percoll selection did not completely remove sperm with oxidative markers.

Keywords

Bull spermOxidative stressSperm traitsTBARS
Type
Research Article
Information
Zygote , Volume 29 , Issue 6 , December 2021 , pp. 476 - 483
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors have contributed equally to this work.

References

Agarwal, A, Virk, G, Ong, C and Plessis, SS (2014). Effect of oxidative stress on male reproduction. World J Mens Health 32, 1–17.CrossRefGoogle ScholarPubMed
Aitken, RJ, Clarkson, JS and Fishel, S (1989). Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 40, 183–97.CrossRefGoogle Scholar
Aitken, RJ, Gordon, E, Harkiss, D, Twigg, JP, Milne, P, Jennings, Z and Irvine, DS (1998). Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 59, 1037–46.CrossRefGoogle ScholarPubMed
Aitken, RJ, Jones, KT and Robertson, SA (2012). Reactive oxygen species and sperm function-in sickness and in health. J Androl 33, 1096–106.CrossRefGoogle ScholarPubMed
Alomar, M, Mahieu, J, Verhaeghe, B, Defoin, L and Donnay, I (2006). Assessment of sperm quality parameters of six bulls showing different abilities to promote embryo development in vitro . Reprod Fertil Dev 18, 395–402.CrossRefGoogle ScholarPubMed
Alomar, M, Tasiaux, H, Remacle, S, George, F, Paul, D and Donnay, I (2008). Kinetics of fertilization and development, and sex ratio of bovine embryos produced using the semen of different bulls. Anim Reprod Sci 107(1–2), 48–61.CrossRefGoogle ScholarPubMed
Alvarez, C, Storey, T and Touchstone, C (1978). Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. J Androl 8, 338–48.CrossRefGoogle Scholar
Alvarez, JG and Storey, B.T (1992). Evidence for increased lipid peroxidation damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J Androl 13, 232–41.Google ScholarPubMed
Blondin, P (2017). Logistics of large scale commercial IVF embryo production. Reprod Fertil Dev 29, 32–6.CrossRefGoogle Scholar
Castro, LS, Siqueira, AFP, Hamilton, TRS, Mendes, CM, Visintin, JA and Assumpção, MEOA (2018). Effect of bovine sperm chromatin integrity evaluated using three different methods on in vitro fertility. Theriogenology, 107, 142–8.CrossRefGoogle ScholarPubMed
Chatterjee, S and Gagnon, C (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Mol Reprod Dev 59, 451–8.CrossRefGoogle ScholarPubMed
de Castro, LS, de Assis, PM, Siqueira, AF, Hamilton, TR, Mendes, CM, Losano, JD, Nichi, M, Visintin, JA and Assumpção, ME (2016). Sperm oxidative stress is detrimental to embryo development: a dose-dependent study model and a new and more sensitive oxidative status evaluation. Oxid Med Cell Longev 2016, 8213071.CrossRefGoogle Scholar
Del Valle, I, Casao, A, Pérez-Pé, R, Holt, WV Cebrián-Pérez, JÁ and Muiño-Blanco, T(2017). Seminal plasma proteins prevent detrimental effects of ram sperm cryopreservation and enhance the protective effect of lecithin. Biochem Anal Biochem 6, 1–11.CrossRefGoogle Scholar
Evenson, DP, Larson, KL and Jost, L.K (2002). Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23, 25–43.CrossRefGoogle ScholarPubMed
Fischer, B and Bavister, B.D (1993). Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. Reproduction 99, 673–9.CrossRefGoogle ScholarPubMed
Ford, WCLF (2001). Reactive oxygen species and sperm. Hum Fertil 4, 77–8.CrossRefGoogle ScholarPubMed
Goto, Y, Noda, Y, Mori, T and Nakano, M (1993). Increased generation of reactive oxygen species in embryos cultured in vitro . Free Radic Biol Med 15, 69–75.CrossRefGoogle ScholarPubMed
Hamilton, TR, de Castro, LS, Delgado Jde, C, de Assis, PM, Siqueira, AF, Mendes, CM, Goissis, MD, Muiño-Blanco, T, Cebrián-Pérez, JÁ, Nichi, M, Visintin, JA and D'Ávila Assumpção, ME (2016). Induced lipid peroxidation in ram sperm: semen profile, DNA fragmentation and antioxidant status. Reproduction, 151, 379–90.CrossRefGoogle ScholarPubMed
Henkel, RR and Schill, WB (2003). Sperm preparation for ART. Reprod Biol Endocrinol 1, 1–22.CrossRefGoogle ScholarPubMed
Kadirvel, G, Kumar, S and Kumaresan, A (2009). Lipid peroxidation, mitochondrial membrane potential and DNA integrity of spermatozoa in relation to intracellular reactive oxygen species in liquid and frozen–thawed buffalo semen. Anim Reprod Sci 114, 125–34.CrossRefGoogle ScholarPubMed
Lane, M, McPherson, NO, Fullston, T, Spillane, M, Sandeman, L, Kang, WX and Zander-Fox, DL (2014). Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PLoS One 9, e100832.CrossRefGoogle ScholarPubMed
Leite, TG, do Vale Filho, VR, de Arruda, RP, de Andrade, AF, Emerick, LL, Zaffalon, FG, Martins, JA, de Andrade, VJ(2010). Effects of extender and equilibration time on post-thaw motility and membrane integrity of cryopreserved Gyr bull semen evaluated by CASA and flow cytometry. Anim Reprod Sci 120, 31–8.CrossRefGoogle ScholarPubMed
Lenzi, A, Gandini, L, Picardo, M, Tramer, F, Sandri, G and Panfili, E (2000). Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies. Front Biosci 5, 1–15.Google ScholarPubMed
Machado, GM, Carvalho, JO, Filho, ES, Caixeta, ES, Franco, MM, Rumpf, R and Dode, MA (2009). Effect of Percoll volume, duration and force of centrifugation, on in vitro production and sex ratio of bovine embryos. Theriogenology 71, 1289–97.CrossRefGoogle ScholarPubMed
Martinez-Alborcia, MJ, Morrell, JM, Gil, MA, Barranco, I, Maside, C, Alkmin, DV, Parrilla, I, Martinez, EA and Roca, J (2013). Suitability and effectiveness of single layer centrifugation using Androcoll-P in the cryopreservation protocol for boar spermatozoa. Anim Reprod Sci 140, 173–9.CrossRefGoogle ScholarPubMed
Medeiros, CMO, Forell, F, Oliveira, ATD and Rodrigues, JL (2002). Current status of sperm cryopreservation: Why isn’t it better? Theriogenology 52, 327–44.CrossRefGoogle Scholar
Morrell, JM, Lagerqvist, A, Humblot, P and Johannisson, A (2017). Effect of single layer centrifugation on reactive oxygen species and sperm mitochondrial membrane potential in cooled stallion semen. Reprod Fertil Dev 29, 1039–45.CrossRefGoogle Scholar
Nongbua, T, Johannisson, A, Edman, A and Morrell, JM (2017). Effects of single layer centrifugation (SLC) on bull spermatozoa prior to freezing on post-thaw semen characteristics. Reprod Domest Anim 52, 596–602.CrossRefGoogle ScholarPubMed
Otoi, T, Tachikawa, S, Kondo, S and T S (1993). Effects of different lots from the same bull on in vitro development of bovine oocytes fertilized in vitro . Theriogenology 39, 713–8.CrossRefGoogle ScholarPubMed
Palma, GA and Sinowatz, F (2004). Male and female effects on the in vitro production of bovine embryos. Anat Histol Embryol 33, 257–62.CrossRefGoogle ScholarPubMed
Parrish, JJ, Susko-Parrish, J, Winer, MA and First, N.L (1988). Capacitation of bovine sperm by heparin. Biol Reprod 38, 1171–80.CrossRefGoogle ScholarPubMed
Pontes, JH, Nonato-Junior, I, Sanches, BV, Ereno-Junior, JC, Uvo, S, Barreiros, TR, Oliveira, JA, Hasler, JF and Seneda, MM (2009). Comparison of embryo yield and pregnancy rate between in vivo and in vitro methods in the same Nelore (Bos indicus) donor cows. Theriogenology, 71, 690–7.CrossRefGoogle ScholarPubMed
Ramos-Deus, P, Santos Nascimento, P, Vieira, JIT, Chaves, MS, Albuquerque, KA, Ferreira-Silva, JC, Grázia, JGV, Santos Filho, AS, Batista, AM, Teixeira, VW, Oliveira, MAL (2020) Application of platelet-rich plasma in the in vitro production of bovine embryos. Trop Anim Health Prod 52, 2931–6.CrossRefGoogle ScholarPubMed
Ricci, JE, Muñoz-Pinedo, C, Fitzgerald, P, Bailly-Maitre, B, Perkins, GA, Yadava, N, Scheffler, IE, Ellisman, MH and Green, DR (2004). Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117, 773–86.CrossRefGoogle ScholarPubMed
Samardzija, M, Karadjole, M, Matkovic, M, Cergolj, M, Getz, I, Dobranic, T, Tomaskovic, A, Petric, J, Surina, J, Grizelj, J and Karadjole, T (2006). A comparison of BoviPure and Percoll on bull sperm separation protocols for IVF. Anim Reprod Sci 91, 237–47.CrossRefGoogle ScholarPubMed
Sikka, SC, Rajasekaran, M and Hellstrom, WJ (1995). Role of oxidative stress and antioxidants in male infertility. J Androl 16, 464–8.Google ScholarPubMed
Silva, PFN, Gadella, BM, Colenbrander, B and Roelen, BAJ (2007). Exposure of bovine sperm to pro-oxidants impairs the developmental competence of the embryo after the first cleavage. Theriogenology 67, 609–19.CrossRefGoogle ScholarPubMed
Simões, R, Feitosa, WB, Siqueira, AF, Nichi, M, Paula-Lopes, FF, Marques, MG, Peres, MA, Barnabe, VH, Visintin, JA and Assumpção, ME (2013). Influence of bovine sperm DNA fragmentation and oxidative stress on early embryo in vitro development outcome. Reproduction 146, 433–41.CrossRefGoogle ScholarPubMed
Siqueira, AFP, de Castro, LS, de Assis, PM, Bicudo, LC, Mendes, CM, Nichi, M, Visintin, JA and Assumpção, MEOD (2018). Sperm traits on in vitro production (IVP) of bovine embryos: too much of anything is good for nothing. PLoS One 13, e0200273.CrossRefGoogle Scholar
Suzuki, K, Geshi, M, Yamauchi, N and Nagai, T (2003). Functional changes and motility characteristics of Japanese Black bull spermatozoa separated by Percoll. Anim Reprod Sci 77, 157–72.CrossRefGoogle ScholarPubMed
Takahashi, M (2012). Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 58, 1–9.CrossRefGoogle ScholarPubMed
Tanghe, S, Van Soom, A, Sterckx, V, Maes, D and De Kruif, A (2002). Assessment of different sperm quality parameters to predict in vitro fertility of bulls. Reprod Domest Anim 37, 127–32.CrossRefGoogle ScholarPubMed
Tartaglione, CM and Ritta, MN (2004). Prognostic value of spermatological parameters as predictors of in vitro fertility of frozen–thawed bull semen. Theriogenology 62, 1245–52.CrossRefGoogle ScholarPubMed
Uribe, P, Villegas, JV, Boguen, R, Treulen, F, Sánchez, R, Mallmann, P, Isachenko, V, Rahimi, G and Isachenko, E (2017). Use of the fluorescent dye tetramethylrhodamine methyl ester perchlorate for mitochondrial membrane potential assessment in human spermatozoa. Andrologia 49, doi: 10.1111/and.12753.CrossRefGoogle Scholar
Viana, J (2019). 2018 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter-IETS, 36, 1–26.Google Scholar
Vieira, LM, Rodrigues, CA, Castro Netto, A, Guerreiro, BM, Silveira, CRA, Freitas, BG, Bragança, LGM, Marques, KNG, Sá Filho, MF, Bó, GA, Mapletoft, RJ and Baruselli, PS (2016). Efficacy of a single intramuscular injection of porcine FSH in hyaluronan prior to ovum pick-up in Holstein cattle. Theriogenology 85, 877–86.CrossRefGoogle ScholarPubMed
Vishwanath, R and Shannon, P (2000). Storage of bovine semen in liquid and frozen state. Anim Reprod Sci 62, 23–53.CrossRefGoogle ScholarPubMed