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The mitochondria of stallion spermatozoa are more sensitive than the plasmalemma to osmotic-induced stress: role of c-Jun N-terminal kinase (JNK) pathway.
Abstract: Cryopreservation introduces extreme temperature and osmolality changes that impart lethal and sublethal effects on spermatozoa. Additionally, there is evidence that the osmotic stress induced by cryopreservation causes oxidative stress to spermatozoa. The main sources of reactive oxygen species in mammalian sperm are the mitochondria. In view of this, the aim of our study was to test whether or not osmotic stress was able to induce mitochondrial damage and to explore the osmotic tolerance of the mitochondria of stallion spermatozoa. Ejaculates from 7 stallions were subjected to osmolalities ranging from 75 to 1500 mOsm/kg, and the effect on sperm membrane integrity and mitochondrial membrane potential was studied. Additionally, the effects of changes in osmolality from hyposmotic to isosmotic and from hyperosmotic to isosmotic solutions were studied (osmotic excursions). The cellular volume of stallion spermatozoa under isosmotic conditions was 20.4 ± 0.33 μm(3). When exposed to low osmolality, the stallion spermatozoa behaved like a linear osmometer, whereas exposure to high osmolalities up to 900 mOsm/kg resulted in decreased sperm volume. Although sperm membranes were relatively resistant to changes in osmolality, mitochondrial membrane potential decreased when osmolalities were low or very high (10.7 ± 1.74 and 16.5 ± 1.70 at 75 and 150 mOsm/kg, respectively, and 13.1 ± 1.83 at 1500 mOsm/kg), whereas in isosmolar controls the percentage of stallion sperm mitochondria with a high membrane potential was 41.1 ± 1.69 (P < .01). Osmotic excursions induced greater damage than exposure of spermatozoa to a given nonphysiologic osmolality, and again the mitochondria were more prone to damage induced by osmotic excursions than was the sperm plasma membrane. In search of intracellular components that could mediate these changes, we have detected for the first time the c-Jun N-terminal kinase 1/2 in stallion spermatozoa, which are apparently involved in the regulation of the viability of these cells.
Publication Date: 2011-03-24 PubMed ID: 21436310DOI: 10.2164/jandrol.110.011957Google 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
- Research Support
- Non-U.S. Gov't
Summary
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The study investigates how extreme changes in temperature and concentrations during cryopreservation of stallion sperm influence the integrity of sperm and specifically the mitochondria. The research finds that mitochondria, a site for production of reactive oxygen species in the sperm, is more susceptible to damage from these changes compared to the outer membrane (plasmalemma). The impact of the c-Jun N-terminal kinase (JNK) pathway, a potential mediator of these changes, is also explored.
The Goal of the Study
- The principal aim of the study was to determine whether changes in osmotic pressure during sperm preservation processes could potentially cause damage to the mitochondria of stallion sperm cells. The tolerance levels of stallion sperm mitochondria to such changes were also investigated.
Methodology
- Investigation was carried out on ejaculates from 7 stallions, and they were subjected to varying osmolality levels (from 75 to 1500 mOsm/kg). This was to simulate and study the effect of such changes on sperm membrane integrity and mitochondrial membrane potential.
- Further, the researchers assessed the effects of transitional osmotic pressure changes from lower to equal (hyposmotic to isosmotic), and higher to equal (hyperosmotic to isosmotic) conditions.
Results
- The study showed that the observed cellular volume of stallion sperm cells was reduced when the osmolality was high (up to 900 mOsm/kg) whereas stallion sperm cells behaved like linear osmometers when exposed to low osmolality.
- The results indicate that while sperm cell membranes were fairly resistant to changes in osmolality, the potential of the mitochondrial membrane decreased when osmolality was very low or very high. This finding suggests that, in the context of cryopreservation, the mitochondria are more vulnerable to osmotic stress than the plasmalemma.
- The study also showed that changes in osmolality damaged stallion sperm cells more when they were transitioned from one osmotic condition to another, rather than maintaining them at a single, non-physiological osmotic pressure. Once again, the mitochondria were more prone to damage induced by these osmotic transitions than the plasmalemma.
Findings in relation to the c-Jun N-terminal kinase (JNK) pathway
- In examining potential cellular components that could mediate these osmotically-induced changes, the researchers detected for the first time the c-Jun N-terminal kinase 1/2 in stallion spermatozoa. This suggests that the JNK pathway might be involved in the regulation of cell viability in the face of osmotic changes.
Cite This Article
APA
García BM, Moran AM, Fernández LG, Ferrusola CO, Rodriguez AM, Bolaños JM, da Silva CM, Martínez HR, Tapia JA, Peña FJ.
(2011).
The mitochondria of stallion spermatozoa are more sensitive than the plasmalemma to osmotic-induced stress: role of c-Jun N-terminal kinase (JNK) pathway.
J Androl, 33(1), 105-113.
https://doi.org/10.2164/jandrol.110.011957 Publication
Researcher Affiliations
- Veterinary Teaching Hospital, Laboratory of Equine Reproduction, Faculty of Veterinary Medicine, University of Extremadura, Avd. de la Universidad s/n, Cáceres, Spain.
MeSH Terms
- Animals
- Flow Cytometry
- Horses
- JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
- JNK Mitogen-Activated Protein Kinases / metabolism
- Male
- Membrane Potentials
- Osmosis
- Spermatozoa / ultrastructure
- Stress, Physiological
Citations
This article has been cited 12 times.- 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).
- Chauvigné F, Ducat C, Ferré A, Hansen T, Carrascal M, Abián J, Finn RN, Cerdà J. A multiplier peroxiporin signal transduction pathway powers piscine spermatozoa. Proc Natl Acad Sci U S A 2021 Mar 9;118(10).
- 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).
- Wei H, Ren Z, Tang L, Yao H, Li X, Wang C, Mu C, Shi C, Wang H. JNK signaling pathway regulates the development of ovaries and synthesis of vitellogenin (Vg) in the swimming crab Portunus trituberculatus. Cell Stress Chaperones 2020 May;25(3):441-453.
- Peña FJ, O'Flaherty C, Ortiz Rodríguez JM, Martín 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).
- Wei X, Li K, Zhang G, Huang Y, Lv J, Li M, Zhao L, Fan C, Pu J, Hou J, Yuan H. B7-H3 promoted proliferation of mouse spermatogonial stem cells via the PI3K signaling pathway. Oncotarget 2018 Jan 5;9(2):1542-1552.
- Anel-Lopez L, Ortega-Ferrusola C, Álvarez M, Borragán S, Chamorro C, Peña FJ, Morrell J, Anel L, de Paz P. Improving sperm banking efficiency in endangered species through the use of a sperm selection method in brown bear (Ursus arctos) thawed sperm. BMC Vet Res 2017 Jun 26;13(1):200.
- Chen J, Zhou A, Xie S, Wang C, Lv Z, Zou J. Comparative Proteomic Identification of Mature and Immature Sperm in the Catfish Cranoglanis bouderius. PLoS One 2016;11(3):e0151254.
- Plaza Davila M, Martin Muñoz P, Tapia JA, Ortega Ferrusola C, Balao da Silva C C, Peña 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.
- da Silva JC, Varela Junior AS, Caldas JS, Freitas Cda S, Botelho JG, Colares EP, Corcini CD. The effects of osmolality on sperm quality in Jenynsia multidentata (Cyprinodontiformes: Anablepidae). Fish Physiol Biochem 2016 Feb;42(1):93-102.
- Chauvigné F, Boj M, Finn RN, Cerdà J. Mitochondrial aquaporin-8-mediated hydrogen peroxide transport is essential for teleost spermatozoon motility. Sci Rep 2015 Jan 14;5:7789.
- Egyptien S, Deleuze S, Ledeck J, Ponthier J. Sperm Quality Assessment in Stallions: How to Choose Relevant Assays to Answer Clinical Questions. Animals (Basel) 2023 Oct 6;13(19).
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