Rapid sperm acrosome reaction in the absence of acrosomal CD46 expression in promiscuous field mice (Apodemus)

Abstract

There is pronounced promiscuity and sperm competition in long-tailed field mice (Apodemus sylvaticus). These mice have evolved unusual sperm behaviour favouring rapid fertilisation, including dynamic formation of sperm trains and their subsequent dissociation. The cell surface complement regulatory (CReg) protein CD46 is broadly expressed in eutherian mammals other than rodents, in which it is expressed solely on the spermatozoal acrosomal membrane. Ablation of the CD46 gene has been associated with a faster acrosome reaction (AR) rate in inbred laboratory mice. Here, we demonstrate that wild-caught field mice of three species, A. sylvaticus, A. flavicollis and A. microps, exhibit a more rapid AR than wild-caught house mice Mus musculus or inbred laboratory BALB/c mice. We also demonstrate that wild-caught field mice of these three species, unlike house mice, produce alternatively spliced transcripts of testicular CD46 mRNA lacking exons 5-7 or 6-7, together with an extended 3 0 -and often truncated 5 0 -utr, leading to failure to express any sperm CD46 protein in both the testis and epididymis. Male field mice may therefore have traded expression of this CReg protein for acrosomal instability, providing a novel genus-specific strategy to favour rapid fertilisation and competitive advantage in the promiscuous reproductive behaviour of wild field mice.

Progress of sperm IZUMO1 relocation during spontaneous acrosome reaction

“…The status of the acrosome was examined immediately under a fluorescent microscope. The obtained results were consistent with data published in Johnson et al (2007).…”

“…In highly promiscuous field mice (Apodemus) with documented multiple paternities (Bryja & Stopka 2005, Bryja et al 2008, Johnson et al 2007, where up to 60% of their sperm undergo synchronised spontaneous AR (Moore et al 2002, Johnson et al 2007, Clift et al 2009), every minute may count in the sperm race to fertilise the egg. Several molecular mechanisms may be involved in speeding up the fertilising process.…”

“…Several molecular mechanisms may be involved in speeding up the fertilising process. One such mechanism is the absent translation of the specific acrosomal transmembrane protein CD46 (Johnson et al 2007), which is thought to be responsible for acrosome integrity in sperm. This is supported by the phenotype of CD46 knockout sperm displaying an increased spontaneous AR rate (Inoue et al 2003).…”

Network Analyses of Sperm–Egg Recognition and Binding: Ready to Rethink Fertility Mechanisms?

“…Indeed, the average number of pups born from CD46 -/ -males was significantly greater than that of wild-type males and the incidence of the spontaneous acrosome reaction doubled in CD46 -/ -sperm, when compared to wild-type sperm (Inoue et al, 2003). These data suggest that CD46 may be involved in regulation of sperm AR (Inoue et al, 2003;Johnson et al, 2007).…”

The slower the better: how sperm capacitation and acrosome reaction is modified in the presence of estrogens

“…In mice, there is a high spontaneous acrosome reaction (Johnson et al 2007), whose rate depends on time of capacitation. The proportion of spontaneous and CaI-induced acrosome reaction gives, therefore, important information to assess the magnitude of the actual effect of estrogens on CaI-induced acrosome reaction.…”