Analyze Diet
Antioxidants (Basel, Switzerland)2022; 11(2); 417; doi: 10.3390/antiox11020417

Impact of Seminal Plasma Antioxidants on Donkey Sperm Cryotolerance.

Abstract: This study investigated whether the activities of the antioxidant components of donkey seminal plasma (SP)-both enzymatic (superoxide dismutase (SOD), catalase-like (CAT), glutathione peroxidase-like (GPX), and paraoxonase type 1 (PON1)) and non-enzymatic (measured in terms of total thiol, copper-reducing antioxidant capacity (CUPRAC), ferric-reducing ability of plasma (FRAP), and Trolox equivalent antioxidant capacity (TEAC))-and oxidative stress index (OSI) are related to sperm cryotolerance. For this purpose, 15 ejaculates from jackasses (one per individual) were collected and split into two aliquots. The first one was used for measuring the activities levels of enzymatic and non-enzymatic antioxidants and OSI in SP, whereas the other aliquot was cryopreserved. Before cryopreservation, sperm quality parameters (concentration, motility, and viability) were evaluated. After thawing, sperm motility, plasma membrane integrity, lipid disorder, mitochondrial membrane potential, reactive oxygen species (ROS), and calcium intracellular levels were also determined. Based on the percentages of total motility (TM) and of sperm with an intact plasma membrane (SYBR14/PI) after thawing, samples were classified as good-freezability (GFE) or poor-freezability (PFE) ejaculates through cluster analyses. The SP activity levels of enzymatic (SOD and PON1) and non-enzymatic antioxidants (CUPRAC, FRAP, and TEAC) were higher ( < 0.05) in GFE than in PFE, whereas SP-OSI was higher ( < 0.05) in PFE than in GFE. In addition, the activity levels of SOD, PON1, GPX, CUPRAC, FRAP, and TEAC were positively ( < 0.05) related to post-thaw sperm motility and plasma membrane integrity and negatively to intracellular ROS levels. The SP-OSI was negatively correlated ( < 0.05) to post-thaw sperm quality parameters and positively to intracellular ROS levels. It can thus be concluded that donkey SP antioxidants are related to sperm cryotolerance and that measurements of antioxidants PON1, SOD, CUPRAC, FRAP, and TEAC, as well as SP-OSI, could be used as markers of sperm cryotolerance. Further research addressing the relationship of these antioxidants and SP-OSI with sperm cryotolerance and their potential use as freezing markers is warranted.
Publication Date: 2022-02-18 PubMed ID: 35204299PubMed Central: PMC8869541DOI: 10.3390/antiox11020417Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article examined the link between antioxidant activity in donkey sperm and its ability to endure freezing and thawing processes. The article highlights the potential value of antioxidants as indicators of sperm freeze-tolerance, suggesting that measurements of specific antioxidants, alongside an oxidative stress index, could help predict the viability of preserved sperm samples.

Overview of the Research & Methodology

  • The study set out to understand the relationship between the antioxidant activity in donkey seminal plasma (SP) and sperm’s ability to tolerate freezing and thawing, a process known as cryotolerance.
  • Both enzymatic antioxidants (super oxide dismutase, catalase-like, glutathione peroxidase-like, and paraoxonase type 1) and non-enzymatic antioxidants (total thiol, copper-reducing antioxidant capacity, ferric-reducing ability of plasma and Trolox equivalent antioxidant capacity) were assessed.
  • The team used 15 ejaculates from separate donkeys; each sample was split into two portions. One portion was used to measure antioxidant activity and the oxidative stress index in SP, while the other was frozen and thawed.
  • Quality parameters like sperm concentration, motility, and viability were evaluated before freezing. Post-thaw, measures such as sperm motility, plasma membrane integrity, lipid disorder, mitochondrial membrane potential, reactive oxygen species, and calcium intracellular levels were determined.

Results and Findings

  • The ejaculates were classified as good-freezability (GFE) or poor-freezability (PFE) based on post-thaw sperm motility and plasma membrane integrity.
  • In GFE samples, levels of both enzymatic and non-enzymatic antioxidants were higher compared to PFE samples, while the oxidative stress index was lower.
  • There was a positive correlation between the levels of enzymatic and non-enzymatic antioxidants and the post-thaw quality of the sperm. Inversely, there was a negative relationship between these antioxidant levels and intracellular reactive oxygen species levels.
  • The stress index showed a negative relationship with post-thaw sperm motility and a positive relationship with increased reactive oxygen species.

Conclusions

  • The researchers conclude that there’s a notable relationship between donkey SP antioxidants and sperm cryotolerance. Antioxidants such as SOD, PON1, CUPRAC, FRAP, and TEAC, along with the oxidative stress index, could serve as potential markers for sperm freeze-tolerance.
  • The research suggests further investigation into these antioxidant markers and their effectiveness in successful sperm freezing and thawing. This could be a significant contribution to fertility treatments and animal breeding programs.

Cite This Article

APA
Catalán J, Yánez-Ortiz I, Tvarijonaviciute A, González-Arostegui LG, Rubio CP, Yeste M, Miró J, Barranco I. (2022). Impact of Seminal Plasma Antioxidants on Donkey Sperm Cryotolerance. Antioxidants (Basel), 11(2), 417. https://doi.org/10.3390/antiox11020417

Publication

ISSN: 2076-3921
NlmUniqueID: 101668981
Country: Switzerland
Language: English
Volume: 11
Issue: 2
PII: 417

Researcher Affiliations

Catalán, Jaime
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Cerdanyola del Vallès, Spain.
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, E-17003 Girona, Spain.
  • Faculty of Veterinary Medicine, University of Teramo, Loc. Piano d'Accio, IT-64100 Teramo, Italy.
Yánez-Ortiz, Iván
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Cerdanyola del Vallès, Spain.
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, E-17003 Girona, Spain.
Tvarijonaviciute, Asta
  • Department of Medicine and Animal Surgery, Faculty of Veterinary Medicine, University of Murcia, ES-30100 Murcia, Spain.
  • Interdisciplinary Laboratory of Clinical Analysis Interlab-UMU, Faculty of Veterinary Medicine, Regional Campus of International Excellence 'Campus Mare Nostrum', University of Murcia, ES-30100 Murcia, Spain.
González-Arostegui, Luis Guillermo
  • Department of Medicine and Animal Surgery, Faculty of Veterinary Medicine, University of Murcia, ES-30100 Murcia, Spain.
  • Interdisciplinary Laboratory of Clinical Analysis Interlab-UMU, Faculty of Veterinary Medicine, Regional Campus of International Excellence 'Campus Mare Nostrum', University of Murcia, ES-30100 Murcia, Spain.
Rubio, Camila P
  • Interdisciplinary Laboratory of Clinical Analysis Interlab-UMU, Faculty of Veterinary Medicine, Regional Campus of International Excellence 'Campus Mare Nostrum', University of Murcia, ES-30100 Murcia, Spain.
  • Department of Animal and Food Science, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Cerdanyola del Vallès, Spain.
Yeste, Marc
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, E-17003 Girona, Spain.
Miró, Jordi
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Cerdanyola del Vallès, Spain.
Barranco, Isabel
  • Department of Veterinary Medical Sciences, University of Bologna, IT-40064 Ozzano dell'Emilia, Italy.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 103 references
  1. Camillo F, Rota A, Biagini L, Tesi M, Fanelli D, Panzani D. The current situation and trend of donkey industry in Europe.. J. Equine Vet. Sci. 2018;65:44–49.
  2. Canisso IF, Panzani D, Miró J, Ellerbrock RE. Key Aspects of Donkey and Mule Reproduction.. Vet Clin North Am Equine Pract 2019 Dec;35(3):607-642.
    doi: 10.1016/j.cveq.2019.08.014pubmed: 31672204google scholar: lookup
  3. Di Palma T, Cecchini S, Macchia G, Pasolini MP, Cocchia N, Boni R. Kinematic, bioenergetic and oxidative evaluations of donkey sperm preserved at +4°C.. Zygote 2020 Aug;28(4):300-307.
    doi: 10.1017/S096719942000012Xpubmed: 32285764google scholar: lookup
  4. Martini M, Altomonte I, Licitra R, Salari F. Nutritional and nutraceutical quality of donkey milk.. J. Equine Vet. Sci. 2018;65:33–37.
  5. Miró J, Marín H, Catalán J, Papas M, Gacem S, Yeste M. Seminal Plasma, Sperm Concentration, and Sperm-PMN Interaction in the Donkey: An In Vitro Model to Study Endometrial Inflammation at Post-Insemination.. Int J Mol Sci 2020 May 14;21(10).
    doi: 10.3390/ijms21103478pmc: PMC7278951pubmed: 32423134google scholar: lookup
  6. Papas M, Catalan J, Barranco I, Arroyo L, Bassols A, Yeste M, Miró J. Total and specific activities of superoxide dismutase (SOD) in seminal plasma are related with the cryotolerance of jackass spermatozoa.. Cryobiology 2020 Feb 1;92:109-116.
  7. Álvarez C, González N, Luño V, Martínez F, Gil L. Alternatives in Donkey semen cryopreservation: Mare vs. Jenny Colostrum.. Reprod Domest Anim 2019 Oct;54 Suppl 4:94-97.
    doi: 10.1111/rda.13516pubmed: 31625242google scholar: lookup
  8. Vidament M, Vincent P, Martin FX, Magistrini M, Blesbois E. Differences in ability of jennies and mares to conceive with cooled and frozen semen containing glycerol or not.. Anim Reprod Sci 2009 May;112(1-2):22-35.
  9. Canisso IF, Carvalho GR, Morel MD, Ker PG, Rodrigues AL, Silva EC, Coutinho Da Silva MA. Seminal parameters and field fertility of cryopreserved donkey jack semen after insemination of horse mares.. Equine Vet J 2011 Mar;43(2):179-83.
  10. Oliveira J.V, Papa F.O, Melo-Oña C.M, Monteiro G.A, Puoli-Filho J.N.P, Alvarenga M.A. New procedures to freeze donkey semen and its influence on mares and jennies fertility.. J. Equine Vet. Sci. 2012;32:503–504.
  11. Vilés K, Rabanal R, Rodríguez-Prado M, Miró J. Effect of ketoprofen treatment on the uterine inflammatory response after AI of jennies with frozen semen.. Theriogenology 2013 Apr 15;79(7):1019-26.
  12. Miró J, Papas M. Post–artificial insemination endometrial inflammation and its control in donkeys.. J. Equine Vet. Sci. 2018;65:38–43.
  13. Mateo-Otero Y, Zambrano F, Catalán J, Sánchez R, Yeste M, Miro J, Fernandez-Fuertes B. Seminal plasma, and not sperm, induces time and concentration-dependent neutrophil extracellular trap release in donkeys.. Equine Vet J 2022 Mar;54(2):415-426.
    doi: 10.1111/evj.13457pubmed: 33908643google scholar: lookup
  14. Yeste M, Estrada E, Rocha LG, Marín H, Rodríguez-Gil JE, Miró J. Cryotolerance of stallion spermatozoa is related to ROS production and mitochondrial membrane potential rather than to the integrity of sperm nucleus.. Andrology 2015 Mar;3(2):395-407.
    doi: 10.1111/andr.291pubmed: 25294093google scholar: lookup
  15. Holt WV. Basic aspects of frozen storage of semen.. Anim Reprod Sci 2000 Aug 18;62(1-3):3-22.
    doi: 10.1016/S0378-4320(00)00152-4pubmed: 10924818google scholar: lookup
  16. Watson PF. The causes of reduced fertility with cryopreserved semen.. Anim Reprod Sci 2000 Jul 2;60-61:481-92.
    doi: 10.1016/S0378-4320(00)00099-3pubmed: 10844218google scholar: lookup
  17. Papas M, Catalán J, Fernandez-Fuertes B, Arroyo L, Bassols A, Miró J, Yeste M. Specific Activity of Superoxide Dismutase in Stallion Seminal Plasma Is Related to Sperm Cryotolerance.. Antioxidants (Basel) 2019 Nov 9;8(11).
    doi: 10.3390/antiox8110539pmc: PMC6912747pubmed: 31717586google scholar: lookup
  18. Yeste M. Sperm cryopreservation update: Cryodamage, markers, and factors affecting the sperm freezability in pigs.. Theriogenology 2016 Jan 1;85(1):47-64.
  19. Sieme H, Oldenhof H, Wolkers WF. Sperm Membrane Behaviour during Cooling and Cryopreservation.. Reprod Domest Anim 2015 Sep;50 Suppl 3:20-6.
    doi: 10.1111/rda.12594pubmed: 26382025google scholar: lookup
  20. Amidi F, Pazhohan A, Shabani Nashtaei M, Khodarahmian M, Nekoonam S. The role of antioxidants in sperm freezing: a review.. Cell Tissue Bank 2016 Dec;17(4):745-756.
    doi: 10.1007/s10561-016-9566-5pubmed: 27342905google scholar: lookup
  21. Aitken R.J, De Iuliis G.N, Drevet J.R. Oxidants, Antioxidants, and Impact of the Oxidative Status in Male Reproduction.. Elsevier London, UK: 2018. Role of Oxidative Stress in the Etiology of Male Infertility and the Potential Therapeutic Value of Antioxidants; pp. 91–100.
  22. Papas M, Arroyo L, Bassols A, Catalán J, Bonilla-Correal S, Gacem S, Yeste M, Miró J. Activities of antioxidant seminal plasma enzymes (SOD, CAT, GPX and GSR) are higher in jackasses than in stallions and are correlated with sperm motility in jackasses.. Theriogenology 2019 Dec;140:180-187.
  23. Muiño-Blanco T, Pérez-Pé R, Cebrián-Pérez JA. Seminal plasma proteins and sperm resistance to stress.. Reprod Domest Anim 2008 Oct;43 Suppl 4:18-31.
  24. Oliveira R.A, Wolf C.A, Viu M.A.O, Gambarini M.L. Addition of glutathione to an extender for frozen equine semen.. J. Equine Vet. Sci. 2013;33:1148–1152.
  25. Gadea J, García-Vazquez F, Matás C, Gardón JC, Cánovas S, Gumbao D. Cooling and freezing of boar spermatozoa: supplementation of the freezing media with reduced glutathione preserves sperm function.. J Androl 2005 May-Jun;26(3):396-404.
    doi: 10.2164/jandrol.04155pubmed: 15867008google scholar: lookup
  26. Silva SV, Soares AT, Batista AM, Almeida FC, Nunes JF, Peixoto CA, Guerra MM. In vitro and in vivo evaluation of ram sperm frozen in tris egg-yolk and supplemented with superoxide dismutase and reduced glutathione.. Reprod Domest Anim 2011 Oct;46(5):874-81.
  27. Gangwar C, Saxena A, Patel A, Singh SP, Yadav S, Kumar R, Singh V. Effect of reduced glutathione supplementation on cryopreservation induced sperm cryoinjuries in Murrah bull semen.. Anim Reprod Sci 2018 May;192:171-178.
  28. Ogata K, Sasaki A, Kato Y, Takeda A, Wakabayashi M, Sarentonglaga B, Yamaguchi M, Hara A, Fukumori R, Nagao Y. Glutathione supplementation to semen extender improves the quality of frozen-thawed canine spermatozoa for transcervical insemination.. J Reprod Dev 2015;61(2):116-22.
    doi: 10.1262/jrd.2014-130pmc: PMC4410309pubmed: 25736550google scholar: lookup
  29. Dowsett KF, Knott LM. The influence of age and breed on stallion semen.. Theriogenology 1996 Aug;46(3):397-412.
    doi: 10.1016/0093-691X(96)00162-8pubmed: 16727908google scholar: lookup
  30. Sieme H, Harrison RA, Petrunkina AM. Cryobiological determinants of frozen semen quality, with special reference to stallion.. Anim Reprod Sci 2008 Sep;107(3-4):276-92.
  31. Loomis PR, Graham JK. Commercial semen freezing: individual male variation in cryosurvival and the response of stallion sperm to customized freezing protocols.. Anim Reprod Sci 2008 Apr;105(1-2):119-28.
  32. Mari G, Castagnetti C, Rizzato G, Mislei B, Iacono E, Merlo B. Density gradient centrifugation of sperm from a subfertile stallion and effect of seminal plasma addition on fertility.. Anim Reprod Sci 2011 Jun;126(1-2):96-100.
  33. Cabrera P, Sánchez R, Risopatrón J. Selección espermática en semen congelado/descongelado de equino: Evaluación de las membranas plasmática, acrosomal y potencial de membrana mitocondrial.. Int. J. Morphol. 2014;32:725–731.
  34. Neuhauser S, Gösele P, Handler J. Postthaw Addition of Autologous Seminal Plasma Improves Sperm Motion Characteristics in Fair and Poor Freezer Stallions.. J Equine Vet Sci 2019 Jan;72:117-123.
    doi: 10.1016/j.jevs.2018.10.028pubmed: 30929775google scholar: lookup
  35. Aurich JE, Kühne A, Hoppe H, Aurich C. Seminal plasma affects membrane integrity and motility of equine spermatozoa after cryopreservation.. Theriogenology 1996 Oct 1;46(5):791-7.
    doi: 10.1016/S0093-691X(96)00237-3pubmed: 16727943google scholar: lookup
  36. Brinsko SP, Crockett EC, Squires EL. Effect of centrifugation and partial removal of seminal plasma on equine spermatozoal motility after cooling and storage.. Theriogenology 2000 Jul 1;54(1):129-36.
    doi: 10.1016/S0093-691X(00)00331-9pubmed: 10990354google scholar: lookup
  37. Bromfield JJ. A role for seminal plasma in modulating pregnancy outcomes in domestic species.. Reproduction 2016 Dec;152(6):R223-R232.
    doi: 10.1530/REP-16-0313pubmed: 27601714google scholar: lookup
  38. Mogielnicka-Brzozowska M, Kordan W. Characteristics of selected seminal plasma proteins and their application in the improvement of the reproductive processes in mammals.. Pol J Vet Sci 2011;14(3):489-99.
    doi: 10.2478/v10181-011-0074-zpubmed: 21957748google scholar: lookup
  39. Li J, Barranco I, Tvarijonaviciute A, Molina MF, Martinez EA, Rodriguez-Martinez H, Parrilla I, Roca J. Seminal plasma antioxidants are directly involved in boar sperm cryotolerance.. Theriogenology 2018 Feb;107:27-35.
  40. Kenney R.M, Bergman R.V, Cooper W.L, Morse G.W. Minimal contamination techniques for breeding mares: Technique and preliminary findings.. Proc. Am. Assoc. Equine Pract. 1975;21:327–336.
  41. Bamba K. Evaluation of acrosomal integrity of boar spermatozoa by bright field microscopy using an eosin-nigrosin stain.. Theriogenology 1988;29:1245–1251.
  42. Jocelyn PC. Spectrophotometric assay of thiols.. Methods Enzymol 1987;143:44-67.
    doi: 10.1016/0076-6879(87)43013-9pubmed: 3657559google scholar: lookup
  43. Da Costa C.M, Dos Santos R.C.C, Lima E.S. A simple automated procedure for thiol measurement in human serum samples.. J. Bras. Patol. Med. Lab. 2006;42:345–350.
  44. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation.. Clin Biochem 2004 Apr;37(4):277-85.
  45. Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay.. Anal Biochem 1996 Jul 15;239(1):70-6.
    doi: 10.1006/abio.1996.0292pubmed: 8660627google scholar: lookup
  46. Campos C, Guzmán R, López-Fernández E, Casado A. Evaluation of the copper(II) reduction assay using bathocuproinedisulfonic acid disodium salt for the total antioxidant capacity assessment: the CUPRAC-BCS assay.. Anal Biochem 2009 Sep 1;392(1):37-44.
    doi: 10.1016/j.ab.2009.05.024pubmed: 19464250google scholar: lookup
  47. Barranco I, Roca J, Tvarijonaviciute A, Rubér M, Vicente-Carrillo A, Atikuzzaman M, Ceron JJ, Martinez EA, Rodriguez-Martinez H. Measurement of activity and concentration of paraoxonase 1 (PON-1) in seminal plasma and identification of PON-2 in the sperm of boar ejaculates.. Mol Reprod Dev 2015 Jan;82(1):58-65.
    doi: 10.1002/mrd.22444pubmed: 25487823google scholar: lookup
  48. Erel O. A new automated colorimetric method for measuring total oxidant status.. Clin Biochem 2005 Dec;38(12):1103-11.
  49. Wu R, Feng J, Yang Y, Dai C, Lu A, Li J, Liao Y, Xiang M, Huang Q, Wang D, Du XB. Significance of Serum Total Oxidant/Antioxidant Status in Patients with Colorectal Cancer.. PLoS One 2017;12(1):e0170003.
  50. Flores E, Taberner E, Rivera MM, Peña A, Rigau T, Miró J, Rodríguez-Gil JE. Effects of freezing/thawing on motile sperm subpopulations of boar and donkey ejaculates.. Theriogenology 2008 Oct 1;70(6):936-45.
  51. Lee JA, Spidlen J, Boyce K, Cai J, Crosbie N, Dalphin M, Furlong J, Gasparetto M, Goldberg M, Goralczyk EM, Hyun B, Jansen K, Kollmann T, Kong M, Leif R, McWeeney S, Moloshok TD, Moore W, Nolan G, Nolan J, Nikolich-Zugich J, Parrish D, Purcell B, Qian Y, Selvaraj B, Smith C, Tchuvatkina O, Wertheimer A, Wilkinson P, Wilson C, Wood J, Zigon R, Scheuermann RH, Brinkman RR. MIFlowCyt: the minimum information about a Flow Cytometry Experiment.. Cytometry A 2008 Oct;73(10):926-30.
    doi: 10.1002/cyto.a.20623pmc: PMC2773297pubmed: 18752282google scholar: lookup
  52. Petrunkina AM, Waberski D, Bollwein H, Sieme H. Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach.. Theriogenology 2010 Apr 15;73(7):995-1000.
  53. Garner DL, Johnson LA. Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.. Biol Reprod 1995 Aug;53(2):276-84.
    doi: 10.1095/biolreprod53.2.276pubmed: 7492679google scholar: lookup
  54. Harrison RA, Ashworth PJ, Miller NG. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes.. Mol Reprod Dev 1996 Nov;45(3):378-91.
  55. Catalán J, Papas M, Trujillo-Rojas L, Blanco-Prieto O, Bonilla-Correal S, Rodríguez-Gil JE, Miró J, Yeste M. Red LED Light Acts on the Mitochondrial Electron Chain of Donkey Sperm and Its Effects Depend on the Time of Exposure to Light.. Front Cell Dev Biol 2020;8:588621.
    doi: 10.3389/fcell.2020.588621pmc: PMC7750462pubmed: 33365309google scholar: lookup
  56. Guthrie HD, Welch GR. 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 2006 Aug;84(8):2089-100.
    doi: 10.2527/jas.2005-766pubmed: 16864869google scholar: lookup
  57. Yeste M, Fernández-Novell JM, Ramió-Lluch L, Estrada E, Rocha LG, Cebrián-Pérez JA, Muiño-Blanco T, Concha II, Ramírez A, Rodríguez-Gil JE. Intracellular calcium movements of boar spermatozoa during 'in vitro' capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model.. Andrology 2015 Jul;3(4):729-47.
    doi: 10.1111/andr.12054pubmed: 26097097google scholar: lookup
  58. Kadirvel G, Kumar S, Kumaresan A, Kathiravan P. Capacitation status of fresh and frozen-thawed buffalo spermatozoa in relation to cholesterol level, membrane fluidity and intracellular calcium.. Anim Reprod Sci 2009 Dec;116(3-4):244-53.
  59. Morató R, Prieto-Martínez N, Muiño R, Hidalgo CO, Rodríguez-Gil JE, Bonet S, Yeste M. Aquaporin 11 is related to cryotolerance and fertilising ability of frozen-thawed bull spermatozoa.. Reprod Fertil Dev 2018 Jul;30(8):1099-1108.
    doi: 10.1071/RD17340pubmed: 29365310google scholar: lookup
  60. Szczykutowicz J, Kałuża A, Kaźmierowska-Niemczuk M, Ferens-Sieczkowska M. The Potential Role of Seminal Plasma in the Fertilization Outcomes.. Biomed Res Int 2019;2019:5397804.
    doi: 10.1155/2019/5397804pmc: PMC6720062pubmed: 31531356google scholar: lookup
  61. Carretero M.I, Fumuso F.G, Giuliano M.S. Effect of seminal plasma in the conservation of semen in zootechnical species.. Spermova 2016;6:93–98.
    doi: 10.18548/aspe/0004.01google scholar: lookup
  62. Troedsson MH, Desvousges A, Alghamdi AS, Dahms B, Dow CA, Hayna J, Valesco R, Collahan PT, Macpherson ML, Pozor M, Buhi WC. Components in seminal plasma regulating sperm transport and elimination.. Anim Reprod Sci 2005 Oct;89(1-4):171-86.
  63. Jonakova V, Jonak J, Ticha M. Reproductive Genomics in Domestic Animals.. Wiley-Blackwell Oxford, UK: 2010. Proteomics of Male Seminal Plasma; pp. 339–366.
  64. Barranco I, Padilla L, Tvarijonaviciute A, Parrilla I, Martínez EA, Rodriguez-Martinez H, Yeste M, Roca J. Levels of activity of superoxide dismutase in seminal plasma do not predict fertility of pig AI-semen doses.. Theriogenology 2019 Dec;140:18-24.
  65. Yánez-Ortiz I, Catalán J, Mateo-Otero Y, Dordas-Perpinyà M, Gacem S, Yeste N, Bassols A, Yeste M, Miró J. Extracellular Reactive Oxygen Species (ROS) Production in Fresh Donkey Sperm Exposed to Reductive Stress, Oxidative Stress and NETosis.. Antioxidants (Basel) 2021 Aug 27;10(9).
    doi: 10.3390/antiox10091367pmc: PMC8470534pubmed: 34572999google scholar: lookup
  66. Baumber J, Ball BA. Determination of glutathione peroxidase and superoxide dismutase-like activities in equine spermatozoa, seminal plasma, and reproductive tissues.. Am J Vet Res 2005 Aug;66(8):1415-9.
    doi: 10.2460/ajvr.2005.66.1415pubmed: 16173486google scholar: lookup
  67. Waheed MM, Gouda EM, Khalifa TA. Impact of seminal plasma superoxide dismutase and glutathione peroxidase on cryopreserved buffalo spermatozoa.. Anim Reprod Sci 2013 Nov 30;142(3-4):126-30.
  68. Buffone MG, Calamera JC, Brugo-Olmedo S, De Vincentiis S, Calamera MM, Storey BT, Doncel GF, Alvarez JG. Superoxide dismutase content in sperm correlates with motility recovery after thawing of cryopreserved human spermatozoa.. Fertil Steril 2012 Feb;97(2):293-8.
  69. Kowalowka M, Wysocki P, Fraser L, Strzezek J. Extracellular superoxide dismutase of boar seminal plasma.. Reprod Domest Anim 2008 Aug;43(4):490-6.
  70. Silvestre MA, Yániz JL, Peña FJ, Santolaria P, Castelló-Ruiz M. Role of Antioxidants in Cooled Liquid Storage of Mammal Spermatozoa.. Antioxidants (Basel) 2021 Jul 8;10(7).
    doi: 10.3390/antiox10071096pmc: PMC8301105pubmed: 34356329google scholar: lookup
  71. Kehrer JP. The Haber-Weiss reaction and mechanisms of toxicity.. Toxicology 2000 Aug 14;149(1):43-50.
    doi: 10.1016/S0300-483X(00)00231-6pubmed: 10963860google scholar: lookup
  72. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa.. J Clin Endocrinol Metab 2008 Aug;93(8):3199-207.
    doi: 10.1210/jc.2007-2616pubmed: 18492763google scholar: lookup
  73. Ghaleno LR, Valojerdi MR, Janzamin E, Chehrazi M, Sharbatoghli M, Yazdi RS. Evaluation of conventional semen parameters, intracellular reactive oxygen species, DNA fragmentation and dysfunction of mitochondrial membrane potential after semen preparation techniques: a flow cytometric study.. Arch Gynecol Obstet 2014 Jan;289(1):173-80.
    doi: 10.1007/s00404-013-2946-1pubmed: 23846620google scholar: lookup
  74. Robinson KM, Janes MS, Pehar M, Monette JS, Ross MF, Hagen TM, Murphy MP, Beckman JS. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes.. Proc Natl Acad Sci U S A 2006 Oct 10;103(41):15038-43.
    doi: 10.1073/pnas.0601945103pmc: PMC1586181pubmed: 17015830google scholar: lookup
  75. Gallo A, Boni R, Buia MC, Monfrecola V, Esposito MC, Tosti E. Ocean acidification impact on ascidian Ciona robusta spermatozoa: New evidence for stress resilience.. Sci Total Environ 2019 Dec 20;697:134100.
  76. De Iuliis GN, Wingate JK, Koppers AJ, McLaughlin EA, Aitken RJ. Definitive evidence for the nonmitochondrial production of superoxide anion by human spermatozoa.. J Clin Endocrinol Metab 2006 May;91(5):1968-75.
    doi: 10.1210/jc.2005-2711pubmed: 16507629google scholar: lookup
  77. Aitken R.J, Iuliis G.N. Sperm Chromatin.. Springer New York, NY, USA: 2011. De Role of Oxidative Stress in the Etiology of Sperm DNA Damage; pp. 277–293.
  78. Ighodaro O.M, Akinloye O.A. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid.. Alex. J. Med. 2019;54:287–293.
  79. Kasimanickam R, Pelzer KD, Kasimanickam V, Swecker WS, Thatcher CD. Association of classical semen parameters, sperm DNA fragmentation index, lipid peroxidation and antioxidant enzymatic activity of semen in ram-lambs.. Theriogenology 2006 Apr 15;65(7):1407-21.
  80. Rubio-Riquelme N, Huerta-Retamal N, Gómez-Torres MJ, Martínez-Espinosa RM. Catalase as a Molecular Target for Male Infertility Diagnosis and Monitoring: An Overview.. Antioxidants (Basel) 2020 Jan 16;9(1).
    doi: 10.3390/antiox9010078pmc: PMC7022443pubmed: 31963256google scholar: lookup
  81. Aitken RJ, Buckingham D, Harkiss D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa.. J Reprod Fertil 1993 Mar;97(2):441-50.
    doi: 10.1530/jrf.0.0970441pubmed: 8388958google scholar: lookup
  82. Aitken RJ, Drevet JR. The Importance of Oxidative Stress in Determining the Functionality of Mammalian Spermatozoa: A Two-Edged Sword.. Antioxidants (Basel) 2020 Jan 27;9(2).
    doi: 10.3390/antiox9020111pmc: PMC7070991pubmed: 32012712google scholar: lookup
  83. Baiardi G, Ruiz RD, Fiol de Cuneo M, Ponce AA, Lacuara JL, Vincenti L. Differential effects of pharmacologically generated reactive oxygen species upon functional activity of epididymal mouse spermatozoa.. Can J Physiol Pharmacol 1997 Mar;75(3):173-8.
    doi: 10.1139/y97-015pubmed: 9164698google scholar: lookup
  84. Baumber J, Ball BA, Gravance CG, Medina V, Davies-Morel MC. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation.. J Androl 2000 Nov-Dec;21(6):895-902.
    pubmed: 11105916
  85. Maxwell WM, Stojanov T. Liquid storage of ram semen in the absence or presence of some antioxidants.. Reprod Fertil Dev 1996;8(6):1013-20.
    doi: 10.1071/RD9961013pubmed: 8896037google scholar: lookup
  86. Peruma P, Chamuah J.K, Rajkhowa C. Effect of catalase on the liquid storage of mithun (Bos frontalis) semen.. Asian Pac. J. Reprod. 2013;2:209–214.
  87. Michael AJ, Alexopoulos C, Pontiki EA, Hadjipavlou-Litina DJ, Saratsis P, Ververidis HN, Boscos CM. Effect of antioxidant supplementation in semen extenders on semen quality and reactive oxygen species of chilled canine spermatozoa.. Anim Reprod Sci 2009 May;112(1-2):119-35.
  88. Barranco I, Tvarijonaviciute A, Perez-Patiño C, Alkmin DV, Ceron JJ, Martinez EA, Rodriguez-Martinez H, Roca J. The activity of paraoxonase type 1 (PON-1) in boar seminal plasma and its relationship with sperm quality, functionality, and in vivo fertility.. Andrology 2015 Mar;3(2):315-20.
    doi: 10.1111/andr.309pubmed: 25598515google scholar: lookup
  89. Verit FF, Verit A, Ciftci H, Erel O, Celik H. Paraoxonase-1 activity in subfertile men and relationship to sperm parameters.. J Androl 2009 Mar-Apr;30(2):183-9.
    doi: 10.2164/jandrol.108.004929pubmed: 18930907google scholar: lookup
  90. Camps J, Marsillach J, Joven J. The paraoxonases: role in human diseases and methodological difficulties in measurement.. Crit Rev Clin Lab Sci 2009;46(2):83-106.
    doi: 10.1080/10408360802610878pubmed: 19255916google scholar: lookup
  91. Mackness MI, Arrol S, Abbott C, Durrington PN. Protection of low-density lipoprotein against oxidative modification by high-density lipoprotein associated paraoxonase.. Atherosclerosis 1993 Dec;104(1-2):129-35.
    doi: 10.1016/0021-9150(93)90183-Upubmed: 8141836google scholar: lookup
  92. Aviram M, Rosenblat M, Billecke S, Erogul J, Sorenson R, Bisgaier CL, Newton RS, La Du B. Human serum paraoxonase (PON 1) is inactivated by oxidized low density lipoprotein and preserved by antioxidants.. Free Radic Biol Med 1999 Apr;26(7-8):892-904.
    doi: 10.1016/S0891-5849(98)00272-Xpubmed: 10232833google scholar: lookup
  93. Lazaros LA, Xita NV, Hatzi EG, Kaponis AI, Stefos TJ, Plachouras NI, Makrydimas GV, Sofikitis NV, Zikopoulos KA, Georgiou IA. Association of paraoxonase gene polymorphisms with sperm parameters.. J Androl 2011 Jul-Aug;32(4):394-401.
    doi: 10.2164/jandrol.110.010348pubmed: 21127310google scholar: lookup
  94. Cecchini Gualandi S, Giangaspero B, Di Palma T, Macchia G, Carluccio A, Boni R. Oxidative profile and protease regulator potential to predict sperm functionality in donkey (Equus asinus).. Sci Rep 2021 Oct 15;11(1):20551.
    doi: 10.1038/s41598-021-99972-9pmc: PMC8521582pubmed: 34654898google scholar: lookup
  95. Rubio CP, Martínez-Subiela S, Hernández-Ruiz J, Tvarijonaviciute A, Cerón JJ, Allenspach K. Serum biomarkers of oxidative stress in dogs with idiopathic inflammatory bowel disease.. Vet J 2017 Mar;221:56-61.
    doi: 10.1016/j.tvjl.2017.02.003pubmed: 28283081google scholar: lookup
  96. Niki E. Assessment of antioxidant capacity of natural products.. Curr Pharm Biotechnol 2010 Dec;11(8):801-9.
    doi: 10.2174/138920110793262097pubmed: 20874689google scholar: lookup
  97. Bathgate R. Antioxidant mechanisms and their benefit on post-thaw boar sperm quality.. Reprod Domest Anim 2011 Sep;46 Suppl 2:23-5.
  98. López-Rodriguez G, Suárez-Dieguez T. Albumin and transferrin are antioxidants that prevent lipoperoxidation in vitro.. Rev. Latinoam. Quím. 2010;38:159–167.
  99. Roche M, Rondeau P, Singh NR, Tarnus E, Bourdon E. The antioxidant properties of serum albumin.. FEBS Lett 2008 Jun 11;582(13):1783-7.
    doi: 10.1016/j.febslet.2008.04.057pubmed: 18474236google scholar: lookup
  100. Bansal AK, Bilaspuri GS. Impacts of oxidative stress and antioxidants on semen functions.. Vet Med Int 2010 Sep 7;2010.
    doi: 10.4061/2011/686137pmc: PMC2943128pubmed: 20871827google scholar: lookup
  101. Abuelo A, Hernández J, Benedito JL, Castillo C. Oxidative stress index (OSi) as a new tool to assess redox status in dairy cattle during the transition period.. Animal 2013 Aug;7(8):1374-8.
    doi: 10.1017/S1751731113000396pubmed: 23510791google scholar: lookup
  102. Barranco I, Rubio CP, Tvarijonaviciute A, Rodriguez-Martinez H, Roca J. Measurement of Oxidative Stress Index in Seminal Plasma Can Predict In Vivo Fertility of Liquid-Stored Porcine Artificial Insemination Semen Doses.. Antioxidants (Basel) 2021 Jul 27;10(8).
    doi: 10.3390/antiox10081203pmc: PMC8388916pubmed: 34439450google scholar: lookup
  103. Contri A, Gloria A, Robbe D, Sfirro MP, Carluccio A. Effect of sperm concentration on characteristics of frozen-thawed semen in donkeys.. Anim Reprod Sci 2012 Dec;136(1-2):74-80.

Citations

This article has been cited 9 times.
  1. Gardela J, Ruiz-Conca M, Palomares A, Olvera-Maneu S, García-Calvo L, López-Béjar M, Martínez-Pastor F, Álvarez-Rodríguez M. Effect of Honey, Coenzyme Q10, and β-Carotene/α-Tocopherol as Novel Additives in Rabbit-Sperm Cryopreservation Extender. Animals (Basel) 2023 Jul 24;13(14).
    doi: 10.3390/ani13142392pubmed: 37508170google scholar: lookup
  2. Ďuračka M, Benko F, Tvrdá E. Molecular Markers: A New Paradigm in the Prediction of Sperm Freezability. Int J Mol Sci 2023 Feb 8;24(4).
    doi: 10.3390/ijms24043379pubmed: 36834790google scholar: lookup
  3. Gobato MLM, Segabinazzi LGTM, Scheeren VFC, Bandeira RS, Freitas-Dell'Aqua CP, Dell'Aqua JA Jr, Papa FO. Ability of donkey sperm to tolerate cooling: Effect of extender base and removal of seminal plasma on sperm parameters and fertility rates in mares. Front Vet Sci 2022;9:1011899.
    doi: 10.3389/fvets.2022.1011899pubmed: 36225802google scholar: lookup
  4. Catalán J, Yánez-Ortiz I, Tvarijonaviciute A, González-Aróstegui LG, Rubio CP, Barranco I, Yeste M, Miró J. Seminal Plasma Antioxidants Are Related to Sperm Cryotolerance in the Horse. Antioxidants (Basel) 2022 Jun 28;11(7).
    doi: 10.3390/antiox11071279pubmed: 35883774google scholar: lookup
  5. Wang S, Shi L, Zhang Z, Liu J, Xing J, Yang J, Duan J, Li B, Cao G. NT5C1B Improves Fertility of Boar Spermatozoa by Enhancing Quality and Cryotolerance During Cryopreservation. Animals (Basel) 2025 Dec 8;15(24).
    doi: 10.3390/ani15243530pubmed: 41463814google scholar: lookup
  6. Deng S, Yang L, Gao L, Ning C, Wang S, Zhang W. The effect of combined cryoprotectants on the cryotolerance of boar sperm. Anim Biosci 2025 Oct;38(10):2111-2124.
    doi: 10.5713/ab.24.0915pubmed: 40302671google scholar: lookup
  7. Udoekong EC, Ramirez-Lopez CJ, Silva Okano D, Barros E, Pereira Vidigal PM, Ribeiro IM, Rodrigues Carvalho RP, Machado-Neves M, Guimarães JD, Facioni Guimarães SE. Proteomic Alterations and Oxidative Stress in Seminal Plasma of Nellore Bulls Under Sexual Rest. Int J Mol Sci 2025 Mar 10;26(6).
    doi: 10.3390/ijms26062457pubmed: 40141101google scholar: lookup
  8. Catalán J, Padilla L, Maside C, Martínez-Hernández J, Yánez-Ortiz I, Tvarijonaviciute A, Barranco I, Bonet S, Miró J, Yeste M. Redox profiling of preovulatory follicular fluid in the donkey is species-specific, and contributes to modulate sperm function. Sci Rep 2025 Feb 23;15(1):6522.
    doi: 10.1038/s41598-025-91422-0pubmed: 39988588google scholar: lookup
  9. Catalán J, Yánez-Ortiz I, Torres-Garrido M, Ribas-Maynou J, Llavanera M, Barranco I, Yeste M, Miró J. Impact of Seminal Plasma Antioxidants on DNA Fragmentation and Lipid Peroxidation of Frozen-Thawed Horse Sperm. Antioxidants (Basel) 2024 Mar 6;13(3).
    doi: 10.3390/antiox13030322pubmed: 38539855google scholar: lookup