Group X phospholipase A2 is released during sperm acrosome reaction and controls fertility outcome in mice
Jessica Escoffier, Ikram Jemel, Akemi Tanemoto, Yoshitaka Taketomi, Christine Payre, Christelle Coatrieux, Hiroyasu Sato, Kei Yamamoto, Seiko Masuda, Karin Pernet-Gallay, Virginie Pierre, Shuntaro Hara, Makoto Murakami, Michel De Waard, Gérard Lambeau, Christophe Arnoult
Jessica Escoffier, Ikram Jemel, Akemi Tanemoto, Yoshitaka Taketomi, Christine Payre, Christelle Coatrieux, Hiroyasu Sato, Kei Yamamoto, Seiko Masuda, Karin Pernet-Gallay, Virginie Pierre, Shuntaro Hara, Makoto Murakami, Michel De Waard, Gérard Lambeau, Christophe Arnoult
View: Text | PDF
Research Article

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

Abstract

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 A2 (sPLA2) 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 sPLA2 (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 sPLA2 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.

Authors

Jessica Escoffier, Ikram Jemel, Akemi Tanemoto, Yoshitaka Taketomi, Christine Payre, Christelle Coatrieux, Hiroyasu Sato, Kei Yamamoto, Seiko Masuda, Karin Pernet-Gallay, Virginie Pierre, Shuntaro Hara, Makoto Murakami, Michel De Waard, Gérard Lambeau, Christophe Arnoult

×

Figure 8

Exogenous mGX sPLA2 reinforces the effect of endogenous mGX on spontaneous AR and improves fertility outcome.

Options: View larger image (or click on image) Download as PowerPoint
Exogenous mGX sPLA2 reinforces the effect of endogenous mGX on spontaneo...
(A) Sperm used for IVF and briefly pretreated with exogenous mGX present a higher rate of spontaneous AR. WT sperm were incubated during the last 10 minutes of capacitation with mGX alone (200 nM), LY329722 alone (1 μM), or mGX preincubated with LY329722. Only mGX treatment triggered significant AR over the untreated condition (n = 6). (B) Recombinant mGX controls the yield of viable embryos, without changing the rate of fertilization. IVF was performed either with OF1 control sperm or with the same sperm briefly treated with 200 nM mGX, and IVF outcome was scored (n = 13). Recombinant mGX increases 2-cell embryos and decreases aborted embryos. (C) Two-cell embryos obtained with mGX-treated sperm developed normally to the blastocyst stage. (D) LY329722 blocks the mGX-dependent increase in fertility. IVF was performed with either control sperm or the same sperm treated briefly with 200 nM mGX or with the same sperm treated with 200 nM mGX but preincubated with 1 μM LY329722 (n = 6). (E) The number of sperm incubated with oocytes does not impact fertility outcome. IVF was performed at 2 different concentrations: 1.5 × 105 and 3 × 105 sperm (sp) (n = 4).