Supramolecular organization of the sperm plasma membrane during maturation and capacitation

Jones, Roy; James, P S; Howes, Liz; Bruckbauer, Andreas; Klenerman, David

doi:10.1111/j.1745-7262.2007.00282.x

Cited by 65 publications

(49 citation statements)

References 19 publications

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“…Based on the specificity and action of group X sPLA 2 on different cells (43,65), the phospholipid targets of mGX on sperm are likely phosphatidylcholine, phosphatidylethanolamine, and phosphatidylserine, especially those enriched in polyunsaturated fatty acids at the sn-2 position. Such phospholipids are present in caudae epididymal sperm and reorganized into microdomains in the sperm head plasma membrane during capacitation (10,11,(66)(67)(68)(69). The fact that about 30% of the sperm population is insensitive to mGX sPLA 2 while the other 70% is gradually sensitive (Figure 4) is likely related to the heterogeneous lipid nature of the sperm plasma membrane producing various subpopulations of sperm with different levels of cholesterol, lipid peroxidation, lipid dynamics, and phospholipid asymmetry (70).…”

Section: Figurementioning

confidence: 99%

“…If capacitation clearly depends on cellular redox activity, ion fluxes, and protein phosphorylations, this process is also characterized by a strong dependence on the lipid membrane composition and lipid metabolism. Indeed, major lipid remodeling events of sperm including reorganization of the plasma membrane and formation of membrane subdomains, have been observed during capacitation at both chemical and biophysical levels (10,11). During capacitation, the most well-known modification of the plasma membrane is cholesterol efflux, which plays a major role in sperm maturation both in vivo and in vitro (5).…”

Section: Introductionmentioning

confidence: 99%

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Group X phospholipase A2 is released during sperm acrosome reaction and controls fertility outcome in mice

Escoffier¹,

Jemel²,

Tanemoto³

et al. 2010

J. Clin. Invest.

100

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Ejaculated mammalian sperm must undergo a maturation process called capacitation before they are able to fertilize an egg. Several studies have suggested a role for members of the secreted phospholipase A 2 (sPLA 2 ) family in capacitation, acrosome reaction (AR), and fertilization, but the molecular nature of these enzymes and their specific roles have remained elusive. Here, we have demonstrated that mouse group X sPLA 2 (mGX) is the major enzyme present in the acrosome of spermatozoa and that it is released in an active form during capacitation through spontaneous AR. mGX-deficient male mice produced smaller litters than wild-type male siblings when crossed with mGX-deficient females. Further analysis revealed that spermatozoa from mGX-deficient mice exhibited lower rates of spontaneous AR and that this was associated with decreased in vitro fertilization (IVF) efficiency due to a drop in the fertilization potential of the sperm and an increased rate of aborted embryos. Treatment of sperm with sPLA 2 inhibitors and antibodies specific for mGX blocked spontaneous AR of wild-type sperm and reduced IVF success. Addition of lysophosphatidylcholine, a catalytic product of mGX, overcame these deficiencies. Finally, recombinant mGX triggered AR and improved IVF outcome. Taken together, our results highlight a paracrine role for mGX during capacitation in which the enzyme primes sperm for efficient fertilization and boosts premature AR of a likely phospholipid-damaged sperm subpopulation to eliminate suboptimal sperm from the pool available for fertilization.

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Section: Figurementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Group X phospholipase A2 is released during sperm acrosome reaction and controls fertility outcome in mice

Escoffier¹,

Jemel²,

Tanemoto³

et al. 2010

J. Clin. Invest.

100

View full text Add to dashboard Cite

show abstract

“…The fluid mosaic model also predicted that intrinsic membrane proteins -not associated to the cytoskeleton, the immobile lipid fraction or the extracellular matrix-were also able to diffuse over the surface of a membrane, although their lateral diffusion speed is considerably slower than phospholipids due to the relative larger size of membrane proteins (Cherry, 1979). The fluid mosaic model did predict a random lateral diffusion over a membrane, whilst in sperm membrane biology, it became apparent that both diffusible membrane proteins as well as lipids where not randomly distributed and even showed a marked redistribution when sperm were incubated under in vitro capacitation conditions Gadella and Visconti, 2006;Jones et al, 2007). Within the sperm membrane, the…”

Section: Detection Of Lateral Diffusionmentioning

confidence: 99%

Sperm head membrane reorganisation during capacitation

Gadella¹,

Tsai²,

Boerke³

et al. 2008

Int. J. Dev. Biol.

171

150

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The sperm cell has a characteristic polarized morphology and its surface is also highly differentiated into different membrane domains. Junctional protein ring structures seal the surface of the mid-piece from the head and the tail respectively and probably prevent random diffusion of membrane molecules over the protein rings. Despite the absence of such lateral diffusion-preventing structures, the sperm head surface is also highly heterogeneous. Furthermore, lipid and membrane protein ordering is subjected to changes when sperm become capacitated. The forces that maintain the lateral polarity of membrane molecules over the sperm surface, as well as those that cause their dynamic redistribution, are only poorly understood. Nevertheless, it is known that each of the sperm head surface regions has specific roles to allow sperm to fertilize the oocyte: a specific region is devoted to zona pellucida binding, a larger area of the sperm head surface is involved in the acrosome reaction (intracellular fusion), while yet another region is involved in egg plasma membrane binding and fertilization fusion (intercellular membrane fusion). All three events occur in the area of the sperm head where the plasma membrane covers the acrosome. Recently, lipid ordered microdomains (lipid rafts) were discovered in membranes of many biological specimens including sperm. In this review, we cover the latest insights about sperm lipid raft research and discuss how sperm lipid raft dynamics may relate to sperm-zona binding and the zona-induced acrosome reaction.

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“…The sperm plasma membrane also undergoes changes in surface charge as well as lipid content and distribution. 2,12 In addition, the distribution and post-translational modification of numerous proteins are also altered. [13][14][15] Through the process, the sperm gain the ability to swim forward and the capacity to undergo acrosome reaction and fertilize an ovum.…”

Section: Introductionmentioning

confidence: 99%

Mouse sperm acquire a new structure on the apical hook during epididymal maturation

Lin¹,

Hsu²,

Yen³

2013

Asian J Androl

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Spermatozoa emerging from the testis undergo a maturation process in the epididymis during which they change morphologically, biochemically and physiologically to gain motility and the ability to fertilize ova. We examined mouse epididymal sperm with immunostaining and transmission electron microscopy (EM) and identified a previously unknown structure on the apical hook. The structure has a coiled configuration around 11 nm in thickness and is present at the tip of each corner of the triangular-rod shaped perforatorium. Surveying sperm isolated from various regions of the epididymis indicated that mouse sperm acquire the hook rim (HR) structure during its passage through the proximal two-thirds of the caput epididymidis. The structure withstands vigorous sonication and harsh chemical treatments and remains intact after the acrosome reaction. Its location and sturdiness suggest a function in protecting the apical hook from mechanical wear during fertilization. Our EM images of epididymal sperm also revealed additional novel structures as well as lateral asymmetry of the sperm head, indicating that mouse sperm head has a structure more complex than previously recognized.

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Supramolecular organization of the sperm plasma membrane during maturation and capacitation

Cited by 65 publications

References 19 publications

Group X phospholipase A2 is released during sperm acrosome reaction and controls fertility outcome in mice

Group X phospholipase A2 is released during sperm acrosome reaction and controls fertility outcome in mice

Sperm head membrane reorganisation during capacitation

Mouse sperm acquire a new structure on the apical hook during epididymal maturation

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