Electrophilic aldehyde products of lipid peroxidation selectively adduct to heat shock protein 90 and arylsulfatase A in stallion spermatozoa.
Abstract: Oxidative stress is a major determinant of mammalian sperm function stimulating lipid peroxidation cascades that culminate in the generation of potentially cytotoxic aldehydes. The aim of this study was to assess the impact of such aldehydes on the functionality of stallion spermatozoa. The impact of exposure to exogenous acrolein (ACR) and 4-hydroxynonenal (4HNE) was manifested in a highly significant dose- and time-dependent increase in mitochondrial reactive oxygen species (ROS), total cellular ROS, a decrease in sperm motility, and a time-dependent increase in lipid peroxidation. Notably, low doses of ACR and 4HNE also caused a significant decrease in zona binding. In contrast, exogenous malondialdehyde, a commonly used marker of oxidative stress, had little impact on the various sperm parameters assessed. In accounting for the negative physiological impact of ACR and 4HNE, it was noted that both aldehydes readily adducted to sperm proteins located predominantly within the head, proximal centriole, and tail. The detoxifying activity of mitochondrial aldehyde dehydrogenase 2 appeared responsible for a lack of adduction in the midpiece; however, this activity was overwhelmed by 24 h of electrophilic aldehyde exposure. Sequencing of the dominant proteins targeted for ACR and 4HNE covalent modification identified heat shock protein 90 alpha (cytosolic) class A member 1 and arylsulfatase A, respectively. These collective findings may prove useful in the identification of diagnostic biomarkers of stallion fertility and resolving the mechanistic basis of sperm dysfunction in this species.
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Publication Date: 2017-04-11 PubMed ID: 28395341DOI: 10.1095/biolreprod.116.145292Google Scholar: Lookup
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Summary
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The study investigates the impact of oxidative stress-generated aldehydes on the functionality of stallion sperm, revealing that these aldehydes cause a significant increase in reactive oxygen species and decrease in sperm motility and zona binding capacity.
Overview of the Research
- The research focuses on the effect of oxidative stress on stallion sperm. Oxidative stress is a key determinant of mammalian sperm function because it stimulates lipid peroxidation cascades that result in the production of potentially cytotoxic aldehydes.
- The primary aim of this study was to evaluate how these aldehydes affect the functionality of stallion spermatozoa.
Experimental Procedure and Results
- Spermatozoa were exposed to acrolein (ACR) and 4-hydroxynonenal (4HNE), two types of aldehydes, under different dosage and time frames.
- There was a significant increase in mitochondrial reactive oxygen species (ROS), total cellular ROS, and a decrease in sperm motility exhibited with the increase in the aldehyde dosage and exposure time.
- Low doses of ACR and 4HNE, interestingly, also resulted in diminished zona binding, which is crucial for fertilization.
- In contrast, exposure to malondialdehyde, another aldehyde often associated with oxidative stress, showed little effect on these parameters.
Spatial Localization and Detoxification
- ACR and 4HNE readily attached (adducted) to sperm proteins primarily in the head, proximal centriole and tail.
- The midpiece showed less adduction due to the detoxifying activity of mitochondrial aldehyde dehydrogenase 2 (ALDH2), but this was overwhelmed by prolonged exposure to the electrophilic aldehydes.
Identifying Aldehyde Targets
- Through protein sequencing, the primary proteins targeted by ACR and 4HNE were identified as heat shock protein 90 alpha (cytosolic) class A member 1 and arylsulfatase A, respectively.
- This can contribute to better understanding of the mechanisms leading to sperm dysfunction in stallions and may prove valuable for identifying diagnostic biomarkers of stallion fertility.
Cite This Article
APA
Hall SE, Aitken RJ, Nixon B, Smith ND, Gibb Z.
(2017).
Electrophilic aldehyde products of lipid peroxidation selectively adduct to heat shock protein 90 and arylsulfatase A in stallion spermatozoa.
Biol Reprod, 96(1), 107-121.
https://doi.org/10.1095/biolreprod.116.145292 Publication
Researcher Affiliations
- Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia.
- Invasive Animals Cooperative Research Centre, University of Canberra, Bruce, Australian Capital Territory, Australia.
- Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia.
- Invasive Animals Cooperative Research Centre, University of Canberra, Bruce, Australian Capital Territory, Australia.
- Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and Information Technology, University of Newcastle, Callaghan, New South Wales, Australia.
- Analytical and Biomedical Research Facility, Research Division, University of Newcastle, Callaghan, New South Wales, Australia.
- 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
- Acrolein
- Aldehyde Dehydrogenase, Mitochondrial / metabolism
- Aldehydes / metabolism
- Animals
- Cerebroside-Sulfatase / metabolism
- HSP90 Heat-Shock Proteins / metabolism
- Horses
- Lipid Peroxidation
- Male
- Malondialdehyde
- Reactive Oxygen Species / metabolism
- Sperm Motility
- Spermatozoa / metabolism
- Zona Pellucida / metabolism
Citations
This article has been cited 9 times.- Umair M, Henning H, Stout TAE, Claes A. A Modified Flotation Density Gradient Centrifugation Technique Improves the Semen Quality of Stallions with a High DNA Fragmentation Index. Animals (Basel) 2021 Jul 1;11(7).
- Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, Gil MC, Ortega-Ferrusola C, Peña FJ. In Stallion Spermatozoa, Superoxide Dismutase (Cu-Zn) (SOD1) and the Aldo-Keto-Reductase Family 1 Member b (AKR1B1) Are the Proteins Most Significantly Reduced by Cryopreservation. J Proteome Res 2021 May 7;20(5):2435-2446.
- Dham D, Roy B, Gowda A, Pan G, Sridhar A, Zeng X, Thandavarayan RA, Palaniyandi SS. 4-Hydroxy-2-nonenal, a lipid peroxidation product, as a biomarker in diabetes and its complications: challenges and opportunities. Free Radic Res 2021 May;55(5):547-561.
- Fatima S, Alwaznah R, Aljuraiban GS, Wasi S, Abudawood M, Abulmeaty M, Berika MY, Aljaser FS. Effect of seminal redox status on lipid peroxidation, apoptosis and DNA fragmentation in spermatozoa of infertile Saudi males. Saudi Med J 2020 Mar;41(3):238-246.
- 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).
- 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).
- Ortiz-Rodriguez JM, Balao da Silva C, Masot J, Redondo E, Gazquez A, Tapia JA, Gil C, Ortega-Ferrusola C, Peña 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.
- Wang Y, Fu X, Li H. Mechanisms of oxidative stress-induced sperm dysfunction. Front Endocrinol (Lausanne) 2025;16:1520835.
- Pilsova Z, Pilsova A, Zelenkova N, Klusackova B, Chmelikova E, Postlerova P, Sedmikova M. Hydrogen sulfide and its potential as a possible therapeutic agent in male reproduction. Front Endocrinol (Lausanne) 2024;15:1427069.
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