Download The spe-42 gene is required for sperm–egg interactions during C

Developmental Biology 286 (2005) 169 – 181
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The spe-42 gene is required for sperm–egg interactions during C. elegans
fertilization and encodes a sperm-specific transmembrane protein
Tim L. Kroft, Elizabeth J. Gleason, Steven W. L’Hernault*
Department of Biology, Emory University, Atlanta, GA 30322, USA
Received for publication 2 April 2005, revised 15 July 2005, accepted 18 July 2005
Available online 24 August 2005
Abstract
Fertilization, the union of sperm and egg to form a new organism, is a critical process that bridges generations. Although the cytological
and physiological aspects of fertilization are relatively well understood, little is known about the molecular interactions that occur between
gametes. C. elegans has emerged as a powerful system for the identification of genes that are necessary for fertilization. C. elegans spe-42
mutants are sterile, producing cytologically normal spermatozoa that fail to fertilize oocytes. Indeed, male mating behavior, sperm transfer to
hermaphrodites, sperm migration to the spermatheca, which is the site of fertilization and sperm competition are normal in spe-42 mutants.
spe-42 mutant sperm make direct contact with oocytes in the spermatheca, suggesting that SPE-42 plays a role during sperm – egg
interactions just prior to fertilization. No other obvious defects were observed in spe-42 mutant worms. Cloning and sequence analysis
revealed that SPE-42 is a novel predicted 7-pass integral membrane protein with homologs in many metazoan species, suggesting that its
mechanism of action could be conserved.
D 2005 Elsevier Inc. All rights reserved.
Keywords: C. elegans; Spermatozoa; Fertilization; Gamete; Sperm – egg interactions; Spermatogenesis; Oocyte
Introduction
Fertilization requires that gametes meet, recognize each
other, bind and fuse to form a new organism. Our current
understanding of sperm – egg interactions at the plasma
membrane is drawn chiefly from experiments using sea
urchins, mice and, more recently, C. elegans (reviewed in
Geldziler et al., 2004; Neill and Vacquier, 2004; OldsClarke, 2003; Singson, 2001; Singson et al., 2001; Stein et
al., 2004; Vacquier, 1998). While it has long been known
that bindin is the sea urchin sperm plasma membrane ligand
(Vacquier and Moy, 1977), the cognate receptor on the
oocyte vitelline envelope, EBR1, was only recently discovered (Kamei and Glabe, 2003). Many molecules have been
proposed as mouse sperm and egg ligands and receptors (He
et al., 2003; reviewed in Stein et al., 2004), but only the
* Corresponding author.
E-mail address: [email protected] (S.W. L’Hernault).
0012-1606/$ - see front matter D 2005 Elsevier Inc. All rights reserved.
doi:10.1016/j.ydbio.2005.07.020
tetraspanin CD9 on the egg (Kaji et al., 2000; Le Naour et
al., 2000; Miyado et al., 2000) and the Ig superfamily
member Izumo on the sperm (Inoue et al., 2005) have been
shown to disrupt sperm –egg fusion in mice with targeted
deletions in these loci.
The unusual reproductive biology of C. elegans makes it
an excellent model system for the study of sperm – egg
interactions during fertilization. The primary reproductive
mode of C. elegans hermaphrodites is self-fertilization, but
a hermaphrodite’s oocytes can also be fertilized by a male.
A simple yet powerful genetic screen has been used to
identify worms with sperm-specific mutations that affect
fertilization (L’Hernault, 1997). Spermatogenesis-defective
(Spe) hermaphrodites are self-sterile and lay only oocytes,
but their sterility defect can be rescued by a male’s wild type
sperm, which demonstrates that the Spe mutation affects
only sperm. Despite the unusual appearance of amoeboid C.
elegans spermatozoa, they must migrate to the site of
fertilization, recognize the oocyte in a species-specific
manner and fuse with it to form a zygote, which are tasks