Biology of reproduction2014; 91(3); 77; doi: 10.1095/biolreprod.114.118539

The paradoxical relationship between stallion fertility and oxidative stress.

Abstract: The relationship between stallion fertility and oxidative stress remains poorly understood. The purpose of this study was to identify criteria for thoroughbred fertility assessment by performing a logistical regression analysis using "dismount" sperm parameters as predictors and weekly per-cycle conception rate as the dependent variable. Paradoxically, positive relationships between fertility and oxidative stress were revealed, such that samples that produced pregnancies exhibited higher rates of 8-hydroxy-2'-deoxyguanosine release (1490.2% vs. 705.5 pg/ml/24 h) and lower vitality (60.5% vs. 69.6%) and acrosome integrity (40.2% vs. 50.1%) than those that did not. We hypothesized that the most fertile spermatozoa exhibited the highest levels of oxidative phosphorylation (OXPHOS), with oxidative stress simply being a by-product of intense mitochondrial activity. Accordingly, an experiment to investigate the relationship between oxidative stress and motility was conducted and revealed positive correlations between mitochondrial ROS and total motility (R² = 0.90), rapid motility (R² = 0.89), average path velocity (VAP; R² = 0.59), and curvilinear velocity (VCL; R² = 0.66). Similarly, lipid peroxidation was positively correlated with total motility (R² = 0.46), rapid motility (R² = 0.51), average path velocity (R² = 0.62), and VCL (R² = 0.56), supporting the aforementioned hypothesis. The relative importance of OXPHOS in supporting the motility of equine spermatozoa was contrasted with human spermatozoa, which primarily utilize glycolysis. In this study, mitochondrial inhibition significantly reduced the velocity (P < 0.01) and ATP (P < 0.05) content of equine, but not human, spermatozoa, emphasizing the former's relative dependence on OXPHOS. The equine is the first mammal in which such a positive relationship between oxidative stress and functionality has been observed, with implications for the management of stallion fertility in vitro and in vivo.
Publication Date: 2014-07-30 PubMed ID: 25078685DOI: 10.1095/biolreprod.114.118539Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

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This is a research study investigating the relationship between fertility in stallions and oxidative stress. Surprisingly, the study discovered a positive connection between the two, speculating that the fertility might be due to a heightened level of oxidative stress being a result of strong mitochondrial activity in the most fertile spermatozoa.

Understanding the Research Focus

  • The subject of this research is the relationship between stallion fertility and oxidative stress. The objective of the study was to create evaluation standards for thoroughbred fertility.
  • The researchers carried out a logistic regression analysis, using sperm parameters as predictors and the weekly conception rate per cycle as the dependent variable.

Key Findings

  • Unexpectedly, the study found positive relationships between fertility and oxidative stress. Specifically, samples that resulted in pregnancies showed higher levels of 8-hydroxy-2′-deoxyguanosine release and lower vitality and acrosome integrity as compared to those that did not.
  • The study hypothesizes that the most fertile sperm cells exhibit the highest levels of oxidative phosphorylation (OXPHOS), and oxidative stress is merely a result of strong mitochondrial activity.

More Experiments and Results

  • An additional experiment investigating the relationship between oxidative stress and motility was conducted, which revealed a positive correlation between mitochondrial reactive oxygen species (ROS) and various measures of motility (total, rapid, average path velocity, curvilinear velocity).
  • Lipid peroxidation also positively correlated with these measures of motility, supporting the hypothesis of a key role for OXPHOS in equine sperm function.

Comparative Results and Implications

  • The study underscored the importance of OXPHOS relative to glycolysis in equine sperm motility, as compared to human sperm which primarily relies on glycolysis.
  • The inhibition of the mitochondria significantly reduced the velocity and ATP content in horse sperm, but not in human sperm, emphasizing the former’s relative dependence on OXPHOS.
  • The horse is the first mammal where a positive relationship between oxidative stress and functionality has been observed. These results have implications for the management of stallion fertility both in vitro and in vivo.

Cite This Article

APA
Gibb Z, Lambourne SR, Aitken RJ. (2014). The paradoxical relationship between stallion fertility and oxidative stress. Biol Reprod, 91(3), 77. https://doi.org/10.1095/biolreprod.114.118539

Publication

ISSN: 1529-7268
NlmUniqueID: 0207224
Country: United States
Language: English
Volume: 91
Issue: 3
Pages: 77

Researcher Affiliations

Gibb, Zamira
  • Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia zamira.gibb@newcastle.edu.au.
Lambourne, Sarah R
  • Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia.
Aitken, Robert J
  • Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia.

MeSH Terms

  • Animals
  • Animals, Inbred Strains
  • Biomarkers / metabolism
  • Fertility
  • Horse Diseases / diagnosis
  • Horse Diseases / metabolism
  • Horse Diseases / physiopathology
  • Horses / physiology
  • Infertility, Male / diagnosis
  • Infertility, Male / metabolism
  • Infertility, Male / physiopathology
  • Infertility, Male / veterinary
  • Lipid Peroxidation / drug effects
  • Logistic Models
  • Male
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • New South Wales
  • Oxidative Phosphorylation / drug effects
  • Oxidative Stress
  • Reactive Oxygen Species / metabolism
  • Semen Analysis / veterinary
  • Species Specificity
  • Sperm Motility / drug effects
  • Spermatozoa / drug effects
  • Spermatozoa / metabolism
  • Uncoupling Agents / pharmacology

Citations

This article has been cited 34 times.
  1. Medica AJ, Lambourne S, Aitken RJ. Predicting the Outcome of Equine Artificial Inseminations Using Chilled Semen.. Animals (Basel) 2023 Mar 30;13(7).
    doi: 10.3390/ani13071203pubmed: 37048459google scholar: lookup
  2. Mancini A, Oliva A, Vergani E, Festa R, Silvestrini A. The Dual Role of Oxidants in Male (In)fertility: Every ROSe Has a Thorn.. Int J Mol Sci 2023 Mar 5;24(5).
    doi: 10.3390/ijms24054994pubmed: 36902424google scholar: lookup
  3. Moustakli E, Zikopoulos A, Sakaloglou P, Bouba I, Sofikitis N, Georgiou I. Functional association between telomeres, oxidation and mitochondria.. Front Reprod Health 2023;5:1107215.
    doi: 10.3389/frph.2023.1107215pubmed: 36890798google scholar: lookup
  4. Bucci D, Spinaci M, Bustamante-Filho IC, Nesci S. The sperm mitochondria: clues and challenges.. Anim Reprod 2022;19(4):e20220131.
    doi: 10.1590/1984-3143-AR2022-0131pubmed: 36819482google scholar: lookup
  5. Van de Hoek M, Rickard JP, de Graaf SP. Motility Assessment of Ram Spermatozoa.. Biology (Basel) 2022 Nov 26;11(12).
    doi: 10.3390/biology11121715pubmed: 36552225google scholar: lookup
  6. Aitken RJ, Lambourne S, Medica AJ. Predicting the outcome of Thoroughbred stallion matings on the basis of dismount semen sample analyses.. Reproduction 2023 Mar 1;165(3):281-288.
    doi: 10.1530/REP-22-0309pubmed: 36538652google scholar: lookup
  7. Nikitkina E, Shapiev I, Musidray A, Krutikova A, Plemyashov K, Bogdanova S, Leibova V, Shiryaev G, Turlova J. Assessment of Semen Respiratory Activity of Domesticated Species before and after Cryopreservation: Boars, Bulls, Stallions, Reindeers and Roosters.. Vet Sci 2022 Sep 21;9(10).
    doi: 10.3390/vetsci9100513pubmed: 36288126google scholar: lookup
  8. Vigolo V, Giaretta E, Da Dalt L, Damiani J, Gabai G, Bertuzzo F, Falomo ME. Relationships between Biomarkers of Oxidative Stress in Seminal Plasma and Sperm Motility in Bulls before and after Cryopreservation.. Animals (Basel) 2022 Sep 22;12(19).
    doi: 10.3390/ani12192534pubmed: 36230273google scholar: lookup
  9. 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
  10. Al-Khaldi K, Yimer N, Sadiq MB, Firdaus Jesse Bin Abdullah F, Salam Babji A, Al-Bulushi S. Edible bird's nest supplementation in chilled and cryopreserved Arabian stallion semen.. Saudi J Biol Sci 2022 Mar;29(3):1577-1584.
    doi: 10.1016/j.sjbs.2021.11.009pubmed: 35280569google scholar: lookup
  11. Aitken RJ, Drevet JR, Moazamian A, Gharagozloo P. Male Infertility and Oxidative Stress: A Focus on the Underlying Mechanisms.. Antioxidants (Basel) 2022 Feb 2;11(2).
    doi: 10.3390/antiox11020306pubmed: 35204189google scholar: lookup
  12. Orsolini MF, Meyers SA, Dini P. An Update on Semen Physiology, Technologies, and Selection Techniques for the Advancement of In Vitro Equine Embryo Production: Section I.. Animals (Basel) 2021 Nov 13;11(11).
    doi: 10.3390/ani11113248pubmed: 34827983google scholar: lookup
  13. 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/s41598-021-99972-9pubmed: 34654898google scholar: lookup
  14. Yu00e1nez-Ortiz I, Catalu00e1n J, Mateo-Otero Y, Dordas-Perpinyu00e0 M, Gacem S, Yeste N, Bassols A, Yeste M, Miru00f3 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/antiox10091367pubmed: 34572999google scholar: lookup
  15. Pintus E, Ros-Santaella JL. Impact of Oxidative Stress on Male Reproduction in Domestic and Wild Animals.. Antioxidants (Basel) 2021 Jul 20;10(7).
    doi: 10.3390/antiox10071154pubmed: 34356386google scholar: lookup
  16. Gallo A, Esposito MC, Tosti E, Boni R. Sperm Motility, Oxidative Status, and Mitochondrial Activity: Exploring Correlation in Different Species.. Antioxidants (Basel) 2021 Jul 16;10(7).
    doi: 10.3390/antiox10071131pubmed: 34356364google scholar: lookup
  17. Lanu00e7oni R, Celeghini ECC, Giuli V, de Carvalho CPT, Zoca GB, Garcia-Oliveros LN, Batissaco L, Oliveira LZ, de Arruda RP. Coenzyme Q-10 improves preservation of mitochondrial functionality and actin structure of cryopreserved stallion sperm.. Anim Reprod 2021 Mar 31;18(1):e20200218.
    doi: 10.1590/1984-3143-AR2020-0218pubmed: 33936294google scholar: lookup
  18. Bazzano M, Laus F, Spaterna A, Marchegiani A. Use of nutraceuticals in the stallion: Effects on semen quality and preservation.. Reprod Domest Anim 2021 Jul;56(7):951-957.
    doi: 10.1111/rda.13934pubmed: 33772909google scholar: lookup
  19. Bucci D, Spinaci M, Galeati G, Tamanini C. Different approaches for assessing sperm function.. Anim Reprod 2020 May 22;16(1):72-80.
    doi: 10.21451/1984-3143-AR2018-122pubmed: 33299480google scholar: lookup
  20. Nikitkina E, Musidray A, Krutikova A, Anipchenko P, Plemyashov K, Shiryaev G. Efficiency of Tris-Based Extender Steridyl for Semen Cryopreservation in Stallions.. Animals (Basel) 2020 Oct 4;10(10).
    doi: 10.3390/ani10101801pubmed: 33020383google scholar: lookup
  21. Sotgia S, Taras A, Zinellu A, Cherchi R, Mangoni AA, Carru C, Bogliolo L. Hercynine, Ergothioneine and Redox State in Stallion's Seminal Plasma.. Antioxidants (Basel) 2020 Sep 13;9(9).
    doi: 10.3390/antiox9090855pubmed: 32933136google scholar: lookup
  22. Bubenickova F, Postlerova P, Simonik O, Sirohi J, Sichtar J. Effect of Seminal Plasma Protein Fractions on Stallion Sperm Cryopreservation.. Int J Mol Sci 2020 Sep 3;21(17).
    doi: 10.3390/ijms21176415pubmed: 32899253google scholar: lookup
  23. F Riesco M, Anel-Lopez L, Neila-Montero M, Palacin-Martinez C, Montes-Garrido R, Alvarez M, de Paz P, Anel L. ProAKAP4 as Novel Molecular Marker of Sperm Quality in Ram: An Integrative Study in Fresh, Cooled and Cryopreserved Sperm.. Biomolecules 2020 Jul 14;10(7).
    doi: 10.3390/biom10071046pubmed: 32674525google scholar: lookup
  24. Marzano G, Moscatelli N, Di Giacomo M, Martino NA, Lacalandra GM, Dell'Aquila ME, Maruccio G, Primiceri E, Chiriacu00f2 MS, Zara V, Ferramosca A. Centrifugation Force and Time Alter CASA Parameters and Oxidative Status of Cryopreserved Stallion Sperm.. Biology (Basel) 2020 Jan 27;9(2).
    doi: 10.3390/biology9020022pubmed: 32012799google scholar: lookup
  25. Wetzker C, Reinhardt K. Distinct metabolic profiles in Drosophila sperm and somatic tissues revealed by two-photon NAD(P)H and FAD autofluorescence lifetime imaging.. Sci Rep 2019 Dec 20;9(1):19534.
    doi: 10.1038/s41598-019-56067-wpubmed: 31862926google scholar: lookup
  26. Villaverde AISB, Netherton J, Baker MA. From Past to Present: The Link Between Reactive Oxygen Species in Sperm and Male Infertility.. Antioxidants (Basel) 2019 Dec 3;8(12).
    doi: 10.3390/antiox8120616pubmed: 31817049google scholar: lookup
  27. Peu00f1a FJ, O'Flaherty C, Ortiz Rodru00edguez JM, Martu00edn Cano FE, Gaitskell-Phillips GL, Gil MC, Ortega Ferrusola C. Redox Regulation and Oxidative Stress: The Particular Case of the Stallion Spermatozoa.. Antioxidants (Basel) 2019 Nov 19;8(11).
    doi: 10.3390/antiox8110567pubmed: 31752408google scholar: lookup
  28. Aouane N, Nasri A, Bekara MAA, Metref AK, Kaidi R. Retrospective study of the reproductive performance of Barb and Thoroughbred stallions in Algeria.. Vet World 2019 Jul;12(7):1132-1139.
  29. Ortiz-Rodriguez JM, Balao da Silva C, Masot J, Redondo E, Gazquez A, Tapia JA, Gil C, Ortega-Ferrusola C, Peu00f1a FJ. Rosiglitazone in the thawing medium improves mitochondrial function in stallion spermatozoa through regulating Akt phosphorylation and reduction of caspase 3.. PLoS One 2019;14(7):e0211994.
    doi: 10.1371/journal.pone.0211994pubmed: 31276504google scholar: lookup
  30. Valcarce DG, Robles V. Evaluation of Intracellular Location of Reactive Oxygen Species in Solea Senegalensis Spermatozoa.. J Vis Exp 2018 Mar 11;(133).
    doi: 10.3791/55323pubmed: 29578498google scholar: lookup
  31. Jeannerat E, Janett F, Sieme H, Wedekind C, Burger D. Quality of seminal fluids varies with type of stimulus at ejaculation.. Sci Rep 2017 Mar 13;7:44339.
    doi: 10.1038/srep44339pubmed: 28287188google scholar: lookup
  32. Gibb Z, Aitken RJ. The Impact of Sperm Metabolism during In Vitro Storage: The Stallion as a Model.. Biomed Res Int 2016;2016:9380609.
    doi: 10.1155/2016/9380609pubmed: 26881234google scholar: lookup
  33. Plaza Davila M, Martin Muu00f1oz P, Tapia JA, Ortega Ferrusola C, Balao da Silva C C, Peu00f1a FJ. Inhibition of Mitochondrial Complex I Leads to Decreased Motility and Membrane Integrity Related to Increased Hydrogen Peroxide and Reduced ATP Production, while the Inhibition of Glycolysis Has Less Impact on Sperm Motility.. PLoS One 2015;10(9):e0138777.
    doi: 10.1371/journal.pone.0138777pubmed: 26407142google scholar: lookup
  34. Varner DD. Odyssey of the spermatozoon.. Asian J Androl 2015 Jul-Aug;17(4):522-8.
    doi: 10.4103/1008-682X.153544pubmed: 25926611google scholar: lookup