Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro.
Abstract: Interaction of equine spermatozoa with oviductal epithelial cells (OEC) prolongs sperm viability and maintains low intracellular calcium concentration ([Ca2+]i) in spermatozoa. Experiments were designed to investigate 1) whether release of spermatozoa from OEC in vitro is associated with elevated [Ca2+]i and 2) whether soluble products from OEC or direct membrane contact between spermatozoa and OEC mediates the effects of OEC on sperm [Ca2+]i. In the first experiment, changes in [Ca2+]i in spermatozoa loaded with indo-1 acetoxymethylester were determined in motile spermatozoa released from OEC monolayers after 4 h of culture compared to [Ca2+]i in spermatozoa still attached to OEC. In addition, [Ca2+]i was determined in spermatozoa incubated with OEC-conditioned medium for 6 h compared to that in spermatozoa incubated in control medium. [Ca2+]i was higher in motile spermatozoa released from OEC than in spermatozoa still attached to OEC after 4 h of incubation. Incubation in OEC-conditioned medium resulted in lower sperm [Ca2+]i only at 4 h of incubation, but not at 0.5, 2, or 6 h of incubation. In the second experiment, a suspension of apical plasma membrane vesicles (AMV) isolated from isthmic oviductal epithelium was used to study the specific effect of sperm contact with OEC membranes on sperm viability, capacitation, and [Ca2+]i. Direct membrane contact between spermatozoa and AMV prolonged sperm viability, delayed capacitation, and maintained low [Ca2+]i in spermatozoa. These results indicated that membrane contact between equine spermatozoa and OEC is required to maintain low [Ca2+]i, delay capacitation, and prolong viability of spermatozoa in vitro. Modulation of capacitation rate for spermatozoa stored in the isthmic sperm reservoir might ensure the availability of a competent sperm population at the time of fertilization.
Publication Date: 1997-04-01 PubMed ID: 9096866DOI: 10.1095/biolreprod56.4.861Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
- Research Support
- U.S. Gov't
- P.H.S.
Summary
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This research investigates how interaction with oviductal epithelial cells (OEC) influences the intracellular calcium concentration of horse sperm cells. The study reveals that physical contact with OECs is essential to maintain low calcium levels, slow down capacitation and prolong sperm cell viability, thus potentially affecting their readiness for fertilization.
Objective and Research Design
- The researchers sought to understand the biological mechanisms by which equine spermatozoa (horse sperm cells) maintain their viability and intracellular calcium concentration when in contact with oviductal epithelial cells (OEC).
- If spermatozoa are separated from OEC, does it lead to an increase in intracellular calcium concentration?
- Is the low calcium concentration maintained by soluble products from OEC or a direct membrane contact between the sperm cells and OEC?
- Two main experiments were conducted: one checking changes in calcium levels in sperm cells released from OEC versus those still attached; another one studying the effects of contact with OEC membranes on sperm cells’ viability, capacitation, and intracellular calcium levels.
Findings of the Research
- The study found that the intracellular calcium concentration was higher in sperm cells released from OEC after 4 hours of incubation than those still attached.
- Sperm cells incubated in OEC-conditioned medium showed lower calcium concentration only after 4 hours, but not at earlier or later time points.
- The second experiment demonstrated that direct membrane contact between sperm cells and OEC prolonged their viability, delayed capacitation (the process that prepares sperm for fertilization), and maintained low intracellular calcium levels.
Implications of the Study
- The results suggest that membrane contact between equine sperm cells and OECs is vital for the former’s survival and readiness for fertilization. It helps maintain low calcium levels, delay capacitation, and keep the sperm cells alive for longer.
- Regulating the rate of capacitation could ensure an available and capable sperm population when fertilization is to occur.
Cite This Article
APA
Dobrinski I, Smith TT, Suarez SS, Ball BA.
(1997).
Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro.
Biol Reprod, 56(4), 861-869.
https://doi.org/10.1095/biolreprod56.4.861 Publication
Researcher Affiliations
- Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA.
MeSH Terms
- Acrosome / ultrastructure
- Animals
- Calcium / metabolism
- Cell Communication
- Cell Membrane / physiology
- Cell Survival
- Cells, Cultured
- Chelating Agents
- Culture Media, Conditioned
- Epithelium / physiology
- Fallopian Tubes / physiology
- Female
- Horses
- Kinetics
- Male
- Sperm Capacitation
- Sperm Head / ultrastructure
- Sperm Motility
- Spermatozoa / cytology
- Spermatozoa / physiology
Grant Funding
- 19854 / PHS HHS
Citations
This article has been cited 19 times.- Sahoo B, Gupta MK. Effect of arginine-induced motility and capacitation on RNA population in goat spermatozoa. Vet Res Commun 2023 Sep;47(3):1427-1444.
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- Raveshi MR, Abdul Halim MS, Agnihotri SN, O'Bryan MK, Neild A, Nosrati R. Curvature in the reproductive tract alters sperm-surface interactions. Nat Commun 2021 Jun 8;12(1):3446.
- Jankovičová J, Sečová P, Michalková K, Antalíková J. Tetraspanins, More than Markers of Extracellular Vesicles in Reproduction. Int J Mol Sci 2020 Oct 14;21(20).
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- Machado SA, Sharif M, Wang H, Bovin N, Miller DJ. Release of Porcine Sperm from Oviduct Cells is Stimulated by Progesterone and Requires CatSper. Sci Rep 2019 Dec 20;9(1):19546.
- Miller DJ. Review: The epic journey of sperm through the female reproductive tract. Animal 2018 Jun;12(s1):s110-s120.
- Silva E, Frost D, Li L, Bovin N, Miller DJ. Lactadherin is a candidate oviduct Lewis X trisaccharide receptor on porcine spermatozoa. Andrology 2017 May;5(3):589-597.
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- Tecle E, Gagneux P. Sugar-coated sperm: Unraveling the functions of the mammalian sperm glycocalyx. Mol Reprod Dev 2015 Sep;82(9):635-50.
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- Kadirvel G, Machado SA, Korneli C, Collins E, Miller P, Bess KN, Aoki K, Tiemeyer M, Bovin N, Miller DJ. Porcine sperm bind to specific 6-sialylated biantennary glycans to form the oviduct reservoir. Biol Reprod 2012 Jun;87(6):147.
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- Zelinger E, Brumfeld V, Rechav K, Waiger D, Kossovsky T, Heifetz Y. Three-dimensional correlative microscopy of the Drosophila female reproductive tract reveals modes of communication in seminal receptacle sperm storage. Commun Biol 2024 Feb 6;7(1):155.
- Sushadi PS, Kuwabara M, Maung EEW, Mohamad Mohtar MS, Sakamoto K, Selvaraj V, Asano A. Arresting calcium-regulated sperm metabolic dynamics enables prolonged fertility in poultry liquid semen storage. Sci Rep 2023 Dec 8;13(1):21775.
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- Hughes JR, McMorrow KJ, Bovin N, Miller DJ. An oviduct glycan increases sperm lifespan by diminishing the production of ubiquinone and reactive oxygen species†. Biol Reprod 2023 Sep 12;109(3):356-366.
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