Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: Functional relationship with zona binding and the zona-induced acrosome reaction

Boerke, Arjan; Tsai, Pu-Sheng; García-Gil, N.; Brewis, Ian Andrew; Gadella, Bart M.

doi:10.1016/j.theriogenology.2008.06.021

Cited by 95 publications

(79 citation statements)

References 52 publications

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“…Since the capacitation-induced aggregation of membrane rafts is thought to be involved in the generation of Capacitation of stallion spermatozoa sperm ZP-binding capability (Boerke et al 2008), it was predicted that the inclusion of mbcd in capacitating media would be advantageous for the promotion of ZP-binding ability in stallion spermatozoa.…”

Section: Discussionmentioning

confidence: 99%

“…The inclusion of albumin is attributed to its unique ability to sequester membrane sterols, such as cholesterol (Boerke et al 2008), and cytotoxic lipid peroxides (Alvarez & Storey 1983). While bicarbonate and calcium fluxes are required for rapid cAMP production and increases in membrane fluidity (Harrison et al 1993), albumin-mediated sterol depletion is critical to achieve increases in protein tyrosine phosphorylation, often considered a hallmark of sperm functional competence in model species such as the mouse (Visconti et al 1995b, Galantino-Homer et al 1997.…”

Section: Introductionmentioning

confidence: 99%

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Capacitation in the presence of methyl-β-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa

et al. 2014

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While IVF has been widely successful in many domesticated species, the development of a robust IVF system for the horse remains an elusive and highly valued goal. A major impediment to the development of equine IVF is the fact that optimised conditions for the capacitation of equine spermatozoa are yet to be developed. Conversely, it is known that stallion spermatozoa are particularly susceptible to damage arising as a consequence of capacitation-like changes induced prematurely in response to semen handling and transport conditions. To address these limitations, this study sought to develop an effective system to both suppress and promote the in vitro capacitation of stallion spermatozoa. Our data indicated that the latter could be achieved in a bicarbonate-rich medium supplemented with a phosphodiesterase inhibitor, a cyclic AMP analogue, and methyl-b-cyclodextrin, an efficient cholesterolwithdrawing agent. The populations of spermatozoa generated under these conditions displayed a number of hallmarks of capacitation, including elevated levels of tyrosine phosphorylation, a reorganisation of the plasma membrane leading to lipid raft coalescence in the peri-acrosomal region of the sperm head, and a dramatic increase in their ability to interact with heterologous bovine zona pellucida (ZP) and undergo agonist-induced acrosomal exocytosis. Furthermore, this functional transformation was effectively suppressed in media devoid of bicarbonate. Collectively, these results highlight the importance of efficient cholesterol removal in priming stallion spermatozoa for ZP binding in vitro.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Capacitation in the presence of methyl-β-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa

et al. 2014

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“…During capacitation, spectrin is severed and in consequence, its network disrupted, just then, the molecules can redistribute. Even though lipid membrane composition has been regarded as the principal mechanism to maintain and stabilize the sperm membrane domains (Boerke et al 2008), we also consider that the spectrin cytoskeleton plays an important role to maintain these membrane domains, specially when taking into account that spectrin contains phospholipid-binding sites, through which it interact with the The staining pattern of spectrin changes in the acrosome during capacitation. The co-localization of spectrin (red) and F-actin (blue) was determined in formaldehyde-fixed non-capacitated sperm (A) and in capacitated sperm in the presence of calpeptin or in the absence of calcium (B).…”

Section: Discussionmentioning

confidence: 99%

Calpain modulates capacitation and acrosome reaction through cleavage of the spectrin cytoskeleton

Bastián¹,

Roa-Espitia²,

Mújica³

et al. 2010

Reproduction

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Research on fertilization in mammalian species has revealed that Ca 2C is an important player in biochemical and physiological events enabling the sperm to penetrate the oocyte. Ca 2C is a signal transducer that particularly mediates capacitation and acrosome reaction (AR). Before becoming fertilization competent, sperm must experience several molecular, biochemical, and physiological changes where Ca 2C plays a pivotal role. Calpain-1 and calpain-2 are Ca 2C-dependent proteases widely studied in mammalian sperm; they have been involved in capacitation and AR but little is known about their mechanism. In this work, we establish the association of calpastatin with calpain-1 and the changes undergone by this complex during capacitation in guinea pig sperm. We found that calpain-1 is relocated and translocated from cytoplasm to plasma membrane (PM) during capacitation, where it could cleave spectrin, one of the proteins of the PM-associated cytoskeleton, and facilitates AR. The aforementioned results were dependent on the calpastatin phosphorylation and the presence of extracellular Ca 2C . Our findings underline the contribution of the sperm cytoskeleton in the regulation of both capacitation and AR. In addition, our findings also reveal one of the mechanisms by which calpain and calcium exert its function in sperm.

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“…In gametes, lipid rafts have been related to sperm maturation, fertilization, and early embryogenesis [27]. Furthermore, certain proteins involved in gamete membrane fusion and zona binding are enhanced in DRMs [28], which suggests that lipid rafts could be involved in sperm-zona pellucida binding and the acrosome reaction [29]. Following in vitro capacitation, membrane rafts become highly enriched in zona binding proteins [28][29][30].…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, certain proteins involved in gamete membrane fusion and zona binding are enhanced in DRMs [28], which suggests that lipid rafts could be involved in sperm-zona pellucida binding and the acrosome reaction [29]. Following in vitro capacitation, membrane rafts become highly enriched in zona binding proteins [28][29][30]. However, contradictory results have been reported, and although some authors have described a redistribution of DRMs after in vitro capacitation [29][30][31], others [32] found no change in the distribution of raft markers after the induction of this process.…”

Section: Introductionmentioning

confidence: 99%

Remodelling of Lipid Rafts during In vitro Capacitation and Acrosome Reaction of Ram Spermatozoa

Colás¹

2013

Biochem Anal Biochem

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Background: Lipid rafts are often known as Detergent-Resistant Microdomains (DRMs). We report for the first time the presence of two lipid raft markers, caveolin-1 and ganglioside GM1, on the ram sperm surface, and the effect of in vitro capacitation and acrosome reaction on these marker distributions, the protein content and lipid composition of DRM and non-DRM fractions. Methods:Caveolin-1 and ganglioside GM1 were evidenced by immunocytochemical and fluorescence analysis, respectively. DRM and non-DRM fractions were separated by an OptiPrep TM density gradient. Cholesterol by fluorometry, GM1 by peroxidase reaction, protein content by spectrophotometry, and fatty acid profiling by gas chromatography were determined.Results: Caveolin-1 was evidenced at the acrosome of 59.2 ± 4.3% fresh spermatozoa, and the proportion of stained cells increased (P<0.05) after capacitation. GM1 was detected at the post-acrosome and tail of all spermatozoa, and no change was found after capacitation. Cholesterol and GM1 were distributed all along the gradient, with a peak in DRM fractions. A higher proportion (P<0.001) of saturated fatty acids was found in DRM fractions, confirmed by the unsaturation index and a higher lipid/protein ratio. In vitro capacitation induced a decrease in the content of saturated fatty acids in both DRM (P<0.001) and non-DRM (P<0.01) fractions. Polyunsaturated fatty acids increased in DRMs after the acrosome reaction. All treatments resulted in lower content of cholesterol and proteins in DRM (P<0.01) and non-DRM fractions (P<0.001), and a higherGM1 content in DRMs (P < 0.05). Conclusions:Lipid raft-like microdomains were isolated in a discrete region of the gradient. Their high content of saturated fatty acids confers a highly ordered environment. Their composition is modified during in vitro capacitation and acrosome reaction. General significance:These results represent the first characterization of ram sperm DRM, and may contribute to a better understanding of the sperm fertilizing potential acquisition mechanism.

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Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: Functional relationship with zona binding and the zona-induced acrosome reaction

Cited by 95 publications

References 52 publications

Capacitation in the presence of methyl-β-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa

Capacitation in the presence of methyl-β-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa

Calpain modulates capacitation and acrosome reaction through cleavage of the spectrin cytoskeleton

Remodelling of Lipid Rafts during In vitro Capacitation and Acrosome Reaction of Ram Spermatozoa

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