Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla CA 92093-0202, USA
Accepted on February 9, 2001;
Abstract
The process of fertilization begins when sperm contact the outermost egg investment and ends with fusion of the two haploid pronuclei in the egg cytoplasm. Many steps in fertilization involve carbohydrate-based molecular recognition between sperm and egg. Although there is conservation of gamete recognition molecules within vertebrates, their homologues have not yet been discovered in echinoderms and ascidians (the invertebrate deuterostomes). In echinoderms, long sulfated polysaccharides act as ligands for sperm receptors. Ascidians employ egg coat glycosides that are recognized by sperm surface glycosidases. Vertebrate egg coats contain zona pellucida (ZP) family glycoproteins, whose carbohydrates bind to sperm receptors. Several candidate sperm receptors for vertebrate ZP proteins have been identified and are discussed here. This brief review focuses on new information concerning fertilization in deuterostomes (the phylogenetic group including echinoderms, ascidians, and vertebrates) and highlights proteincarbohydrate interactions involved in this process.
Key words: acrosome reaction/fertilization/proteincarbohydrate recognition/spermegg interaction/zona pellucida
Introduction
Fertilization is a multistep process and a unique event that involves fusion of two haploid gametes to form a diploid zygote. Sperm must locate, adhere to, and fuse with the egg. The egg must prevent further sperm fusion to avoid pathological polyspermy, a lethal condition. Eggs are surrounded by an extracellular matrix, which varies in composition among animal groups (Figure 1). When sperm contact this matrix, there are primary binding events that, in most deuterostomes, lead to the sperm acrosome reaction (AR). The AR is triggered by increases in intracellular Ca2+ and pH (Darszon et al., 1999) and results in exocytosis of the acrosomal vesicle (an organelle in the sperm head). Following the AR, secondary binding events occur, and the membrane exposed by the AR fuses with the egg plasma membrane. Proteincarbohydrate interactions play a critical role in this complex process. Because there is such a vast literature, this brief review will focus only on deuterostome spermegg recognition events that involve carbohydrateprotein interactions.
|
Echinoderms
Echinoderms are marine invertebrates found at the base of the deuterostome lineage. Because they spawn large quantities of gametes into sea water, they make excellent model organisms for studying molecular events involved in spermegg interaction.
Sea urchins
In sea urchins, proteincarbohydrate interactions take place both at the egg jelly and the vitelline layers. Sperm first contact the egg jelly layer. A 210-kDa multidomain receptor for egg jelly (REJ) on sperm (Moy et al., 1996) binds to the fucose sulfate polymer (FSP) of egg jelly triggering the AR (Vacquier and Moy, 1997
). Females of Strongylocentrotus purpuratus have one of two forms of FSP that are equally potent at AR induction. These FSPs are linear polysaccharides of 1
3-linked
-L-fucopyranosyl units that differ in their sulfation pattern at the C-2 and C-4 positions (Alves et al., 1998
). REJ contains two C-type lectin domains (CRDs, reviewed by Drickamer, 1988
; Moy et al., 1996
), and it may be that each of the two CRDs of REJ binds to each of the forms of FSP. The structures of sulfated polysaccharides from the egg jelly of other sea urchin species have been determined and are species-specific inducers of the AR. Like S. purpuratus, the species Strongylocentrotus franciscanus, Arbacia lixula, and Lytechinus variegatus contain sulfated
-L-fucans, and the sulfated polysaccharide of Echinometra lucunter is a homopolymer of 2-sulfated, 3-linked
-L-galactan (Alves et al., 1997
; Vilela-Silva et al., 1999
). These polysaccharides are AR inducers in the complete absence of a polypeptide.
Following the initial egg jellysperm interaction, the AR expels the protein bindin from the acrosomal vesicle. Bindin coats the sperm acrosomal process, mediates sperm adhesion to eggs, and may mediate spermegg fusion (Vacquier et al., 1995). A 350-kDa glycoprotein receptor for bindin was identified from the vitelline layer of sea urchin eggs (reviewed by Ohlendieck and Lennarz, 1995
). The N-terminus of the protein has a relatively high content of Cys and Pro residues and contains 17 potential O-linked and 5 potential N-linked glycosylation sites (Just and Lennarz, 1997
). The receptor is 70% carbohydrate (Kitazume-Kawaguchi et al., 1997
), and both carbohydrate moieties and the protein backbone are needed for spermegg binding. O-linked, sulfated oligosialylated chains, isolated from the 350-kDa receptor, inhibit fertilization by binding to acrosome-reacted sperm (Dhume and Lennarz, 1995
; Kitazume-Kawaguchi et al., 1997
). Furthermore, bindin binds to sulfated fucose polymers from the egg surface (DeAngelis and Glabe, 1990
). However, the function of the polypeptide chain has been questioned because of its similarity to heat shock protein 110 (Mauk et al., 1997
).
Starfish
There are three major components of starfish (Asteria amurensis) egg jellyglycoproteins, sulfated steroid saponins, and oligopeptides. The AR-inducing substance (ARIS), is an enormous molecule composed of approximately 33% protein, 47% carbohydrate, and 10% sulfate. ARIS has a molecular mass of >104 kDa, but the minimum functional size is 14 kDa (Ushiyama et al., 1995
). Isolated ARIS is capable of inducing the AR in high Ca2+ or high pH sea water. However, in normal sea water, ARIS requires the sulfated steroid saponins (Co-ARIS) to induce the AR (Hoshi et al., 1991
). The structure of the main saccharide chain has been determined to be a repeat of the pentasaccharide,
4-ß-D-Xyl-1
3-
-D-Gal-1
3-
-L-Fuc-4(SO3)-1
3-
-L-Fuc4(SO3)-1
4-
-L-Fuc-1
. Like ARIS alone, isolated polymers composed of 1011 pentasaccharide repeating units induce the acrosome reaction at high Ca2+ concentrations (Koyota et al., 1997
). Thus, spermegg recognition and induction of the AR in both sea urchins and starfish involves large sulfated polysaccharides. It will be interesting to learn if the starfish sperm receptor for the pentasaccharide repeat is similar to the sea urchin sperm receptor REJ.
Ascidians
Glycosidases are enzymes that are typically secreted or stored in lysosomes. In ascidians (sessile marine invertebrates), glycosidases are found on the surface of sperm, and they play a critical role in spermegg recognition. Based on studies of Ciona intestinalis and Phallusia mammillata (Hoshi et al., 1983, 1985), a glycosidase on the surface of sperm was proposed to recognize and bind to glycosides within the vitelline coat (VC) of the egg. In the case of C. intestinalis, the sperm glycosidase,
-L-fucosidase, binds to terminal L-fucose residues of the VC. For P. mammillata, N-acetylglucosaminidase recognizes terminal GlcNAc. The enzymes are thought to act as lectins because their pH optima (
3.9) is well below that of sea water (pH 8) and the rate of hydrolysis is drastically reduced. Examination of glycans present in the vitelline coat of Halocynthia roretzi eggs, where spermegg binding is mediated through
-L-fucosidase on the sperm surface, indicates that the crucial glycans are O-linked and sulfated (Baginski et al., 1999
). Not only do glycosidases occur on the surfaces of sperm, they are also released from the eggs at fertilization as a block to polyspermy (Lambert, 1986
, 1989; Matsuura et al., 1993
, 1995). The evidence suggests that a specific glycosidase on the sperm surface binds to its respective glycoside on the egg VC. This binding triggers eggs to release large quantities of a similar glycosidase, which prevents the binding of supernumerary sperm.
Carbohydrates also play a role in ascidian spermegg interactions at the egg plasma membrane. When vitelline envelopes are removed from the eggs of Ascidia ceratodes, application of wheat germ agglutinin (WGA; >10 µg/ml) will biochemically activate the eggs, as if they had been fertilized. Lower concentrations of WGA do not activate eggs but reduce the ability of sperm to fertilize eggs (Flannery and Epel, 1998).
Vertebrates
The extracellular matrices surrounding eggs of vertebrates vary between phylogenetic groups. However, they all contain members of the ZP glycoprotein family in their egg coats (called the zona pellucida [ZP] in mammals, the vitelline envelope [VE] in amphibians, and the chorion in teleost fish). No such ZP proteins have yet been described in nonvertebrate deuterostome or protostome egg envelopes. Recent reviews have appeared on the molecular basis of spermegg interactions in mammals (Brewis and Moore, 1997; Shalgi and Raz, 1997
; Dell et al., 1999
; Takasaki et al., 1999
; Wassarman, 1999a
,b; Evans, 2000
; Prasad et al., 2000
). Therefore, only the most recent findings regarding the role of carbohydrates in spermegg interaction will be mentioned. Because most of the work on ZP proteins concerns the mouse, this portion of the review will focus on the mouse model and include additional information from other vertebrates.
Glycoproteins of the ZP
ZP3
The mouse ZP is composed of three glycoproteins, mZP1, mZP2, and mZP3 (also called ZPB, ZPA, and ZPC), that are crucial for its structural integrity. mZP2 and mZP3 dimerize to create long filaments that are cross-linked by mZP1. In addition to being structural components, ZP glycoproteins bind to sperm receptors, causing them to cluster and induce signal transduction events leading to the sperm AR. O-linked oligosaccharides of mZP3 are the ligands for sperm that are involved in primary binding and induction of the AR (Florman and Wassarman, 1985 and reviewed by Dell et al., 1999
; Shalgi and Raz, 1997
; Wassarman et al., 1999
; Wassarman, 1999b
). Site-directed mutagenesis shows that mutating Ser-332 or Ser-334 to Ala results in complete inactivation of mZP3 (Chen et al., 1998
), indicating the importance of O-linked oligosaccharides at these sites. The structures of the sperm-binding/AR-inducing components of the O-linked oligosaccharides have yet to be determined. However, several studies have begun to tackle the difficult problem of determining the crucial ZP sugars involved in spermegg interactions in vertebrates.
Examination of spermegg binding by analysis of ZP sugars and the use of neoglycoproteins, monosaccharides, and other polysaccharides have yielded conflicting results. The bioactivity of mZP3 is not dependent on sulfation, N-linked oligosaccharides, or sialic acid residues (Litscher and Wassarman, 1996; Liu et al., 1997
). However, removal of sialic acid from fixed eggs increases sperm binding, suggesting that these residues may conceal sperm binding sites (Mori et al., 1997
). Man-BSA, GlcNAc-BSA, and GalNAc-BSA are capable of inducing the mouse AR, whereas Glc-BSA and Gal-BSA have no effect. The same monosaccharides applied at millimolar concentrations neither induce nor block the AR (Loeser and Tulsiani, 1999
), suggesting that multivalent interactions between carbohydrates of the ZP and their receptors on sperm are necessary for AR induction. Application of L-type Ca2+ channel blockers verapamil or diltiazem to sperm block the mZP3 induced AR. These drugs also block the AR induced by Man-BSA, GlcNAc-BSA, and GalNAc-BSA, lending support to the notion that these neoglycoproteins are affecting the same pathway as mZP3, the natural inducer. However, the G-protein blocker, pertussis toxin, which blocks the mZP3-induced AR, is ineffective at preventing the neoglycoprotein-induced AR (Loeser and Tulsiani , 1999
). Because Man-BSA, GlcNAc-BSA, and GalNAc-BSA have similar affects on sperm as mZP3, this suggests that these sugars may be biologically relevant components of the oligosaccharides of mZP3. Furthermore, structural analysis of mouse ZP-derived glycans indicates the presence of terminal Man, GlcNAc, and GalNAc residues (Easton et al., 2000
).
Removal of Gal from the nonreducing termini of the O-linked oligosaccharides of mZP3 (by treatment with -galactosidase) inhibits sperm binding (Bleil and Wassarman, 1988
), indicating that these terminal Gal residues are essential for spermegg binding. Incubating sperm with the trisaccharide Gal-
-1
3-Gal-ß-1
4-GlcNAc inhibits sperm binding to eggs to a greater extent than incubation with the trisaccharide Gal-ß-1
4-GlcNAc-ß-1
4-GlcNAc, though neither inhibit binding with high affinity (Johnston et al., 1998
). This would indicate that the
-Gal linkage is more important for sperm binding than the ß-Gal linkage. However, the role of terminal Gal residues in sperm binding remains controversial. Another study found that sperm binding was reduced in ß-galactosidase-treated eggs but not
-galactosidase-treated eggs (Mori et al., 1997
). Also,
-galactosyltransferase is necessary for the synthesis of terminal Gal-
-1
3-Gal residues, yet
-galactosyltransferase-null mice are fully fertile (Thall et al., 1995
). Furthermore, Gal residues localize to the inner portion of the ZP, indicating that the initial contact between the ZP and sperm does not involve Gal residues (Aviles et al., 2000
). Studies of other monosaccharides have yielded similarly confusing results. For example, addition of an
-3-fucose residue to the trisaccharide Gal-
-1
3-Gal-ß-1
4-GlcNAc to form Gal-
-1
3-Gal-ß-1
4[Fuc-
1
3]-GlcNAc, yields a tetrasaccharide with high inhibitory activity (Johnston et al., 1998
). However, there is no evidence of fucosylation of O-glycans based on structural analysis of carbohydrates from mouse eggs (Easton et al., 2000
). These examples highlight the difficulties of sorting out biologically relevant carbohydrates involved in spermegg interactions. Understanding this process is further complicated by the fact that spermegg binding involves both low and high-affinity ZP binding sites on sperm (Thaler and Cardullo, 1996
).
ZPs in other vertebrates
In pigs, acrosome-intact sperm bind to ZP proteins over the acrosomal ridge on the anterior portion of the sperm head (Burkin and Miller, 2000). The pig ZP contains ZPA, ZPB, and ZPC (homologues of mZP2, mZP1, and mZP3), and unlike mouse, ZPB (ZP1) is the sperm binding protein (Yonezawa et al., 1997; Kudo et al., 1998
). Analysis of ZPB carbohydrates yields conflicting results. Some studies find that O-linked oligosaccharides and not N-linked oligosaccharides are responsible for spermegg binding (Yurewicz et al., 1991
, 1993), but other studies identify neutral N-linked oligosaccharides of ZPB as the sperm-binding components (Yonezawa et al., 1997
; Kudo et al., 1998
).
Among amphibians, Xenopus laevis has provided the most information about spermegg recognition. Egg VE glycoprotein, gp43 (ZPC or ZP3) contains several O-linked and two N-linked glycosylation sites, one of which is conserved from teleosts to humans (Kubo et al., 1997; Yang and Hedrick, 1997
). Proteolytic cleavage of gp69/64 (ZPA or ZP2) during fertilization results in removal of 27 amino acids from the N-terminus and loss of sperm binding. The N-terminal peptide may contain an O-linked glycan that is involved in the binding process (Tian et al., 1999
). Another analysis of Xenopus ZP proteins identified complex N-linked oligosaccharides of ZPC (mZP3) as the major sperm binding ligands and that sperm binding involves GlcNAc and Fuc residues. Furthermore, mixing isolated ZPA, ZPB and ZPC in a ratio of 1:4:4 (as occurs in the ZP) results in the binding of more sperm than the sum of the separate components (Vo and Hedrick, 2000). This result suggests that instead of having one sperm-binding protein, the molecules may act synergistically to bind sperm.
The chorion surrounding eggs in teleost fish is multilayered and varies in thickness and number of layers. The zebrafish (Danio rerio) has a chorion composed of three morphologically distinct layers and contains four major proteins (116, 97, 50, and 43 kDa; Bonsignorio et al., 1996). The homologue of mZP2 was the first ZP protein identified in teleost fish (Lyons et al., 1993
), and others have been identified since then. Both ZP2 and ZP3 cDNA clones have been identified in zebrafish, but the relationship of the proteins of the zebrafish chorion to the ZP protein family is unknown. In zebrafish ZP3, only one putative N-glycosylation site and no O-glycosylation sites exist (Wang and Gong, 1999
). Interestingly, most teleost sperm lack an acrosome. Instead of penetrating through the chorion, they reach the egg plasma membrane by swimming through a hole in the chorion called the micropyle, implying that AR-inducing oligosaccharides may be unnecessary. In the medaka fish (Oryzias latipes), two groups of glycoproteins exist in the chorion, ZI-1,2 and ZI-3, whose precursors, choriogenin H and choriogenin L, correspond to ZP2 and ZP3 (Murata et al., 1995
, 1997). ZI-1,2 and ZI-3 are sparsely distributed throughout a broad diluted mucous area (DMA) on the surface of the chorion and within the micropyle (Iwamatsu et al., 1997
). It is thought that the sperm bind to ZI-1,2 and ZI-3 to maneuver across the surface of the egg through the DMA until locating the micropyle.
Sperm receptors for egg ZP glycoproteins
The evidence for mZP3 being the ligand for mouse sperm and the inducer of the AR is well supported, but the sperm receptor for mZP3 remains controversial. Candidate ZP receptors will be discussed.
Acrosin is an acrosomal protease, originally thought to be involved in digesting a passage through the ZP. Several lines of evidence suggest that acrosin binds to sulfated polysaccharides of the ZP, as well as Fuc-BSA, Man-BSA, and non-ZP polysulfate saccharides (Jones, 1991; Urch and Patel, 1991
; Jones et al., 1988
). The function of acrosin in mice is questionable, because sperm of acrosin-null mice are still capable of penetrating the ZP and fertilization (Baba et al., 1994
), though not as effectively as normal sperm (Adham et al., 1997
). Also, recombinant boar acrosin binds to the ZP but does not block sperm penetration (Crosby and Barros, 1999
). Recent evidence suggests that acrosins proteolytic activity may function in the dispersal of the acrosomal vesicle contents after the AR (Yamagata et al., 1998
). Thus, the function of acrosin in the mammalian AR will require further work.
ß-14-Galactosyltransferase (GalTase) has been extensively studied as a mammalian sperm receptor involved in sperm binding to mZP3. Agents that inhibit GalTase and addition of purified GalTase inhibit sperm-zona binding in vitro (reviewed by Shur et al., 1998
). GalTase specifically recognizes the oligosaccharides of mZP3 that have sperm-binding activity but does not interact with other mZP glycoproteins (Miller et al., 1992
). mZP3 is thought to elicit the AR by cross-linking or aggregating the sperm receptor on the plasma membrane (Leyton and Saling, 1989
). Anti-GalTase antibodies (but not their Fab fragments) will induce the AR by aggregating GalTase on the sperm plasma membrane (Macek et al., 1991
). Multivalent GlcNAc-BSA is also capable of inducing the mouse sperm AR, whereas millimolar concentrations of the unconjugated sugar have no effect (Loeser and Tulsiani, 1999
). Structural analysis of mouse ZP glycans demonstrates that the ligand for GalTase, GlcNAc, is only present on N-linked and not O-linked oligosaccharides (Easton et al., 2000
). GalTase has been localized to the anterior portion of the sperm head in several mammalian species, including guinea pig, mouse, rat, bull, pig, and rabbit (Larson and Miller, 1997
). GalTase on the surface of porcine sperm binds the ZP. Unlike mouse GalTase, addition of uridine diphosphate galactose has no effect on sperm binding to the oocyte, nor does removal of zona ligands by N-acetylglucosaminidase (Rebeiz and Miller, 1999
). This would argue that GalTase is not necessary for spermzona binding and the AR in pigs. Furthermore, GalTase-null male mice are fertile. However, in vitro studies show that the mutant sperm bind less mZP3 than wild type and do not undergo the AR in response to ZP3 or anti-GalTase antibodies (Lu and Shur, 1997
). This points out the difficulty of correlating effects observed in vitro with the natural process occurring in vivo.
sp56 was identified on the basis of its affinity for mZP3 (Bleil and Wassarman, 1990). Furthermore, it was shown that sp56 localizes to the outer surface of the sperm head and that sperm binding glycopeptides of mZP3 can be crosslinked to sp56 (Cheng et al., 1994
). The cDNA sequence revealed sp56 to be a peripheral membrane protein that contains seven sushi domains and a highly basic COOH-terminal domain (Bookbinder et al., 1995
). AM67 is a guinea pig homologue of sp56 that localizes within the acrosome. Reexamination of the localization of sp56 in mouse sperm revealed that it was also found inside the acrosome (Foster et al., 1997
). Whether sp56 is exclusively internal or external remains unresolved.
Compelling evidence exists that acrosin, GalTase, and sp56 interact with carbohydrates of the ZP and are important components of spermegg interaction. The difficulty lies in teasing out the exact function of each of these receptors in vivo.
Secondary sperm receptors
Several sperm receptors have been identified that are thought to be involved in secondary binding of acrosome-reacted sperm to egg extracellular matrices. ß-N-acetylglucosaminidase is released from mouse sperm during the AR, and the inhibitor, PUGNAC, prevents sperm penetration through the ZP. The glycosidase is thought to remove terminal GlcNAc, releasing the sperm so that it can move through the ZP (Miller et al., 1992). In the toad Bufo arenarum, the enzyme is released from sperm and binds to the VE. Furthermore, inhibition of this enzyme results in inhibition of fertilization in vitro (Martinez et al., 2000
).
Hyaluronan is a glycosaminoglycan composed of the disaccharide repeat (GlcNAcß-14GlcAß-1
3)n, and hyaluronidases selectively degrade the polymer. In mammals, hyaluronan is found in the cumulus matrix surrounding the ZP and the egg perivitelline layer surrounding the plasma membrane (Kan, 1990
; Dandekar et al., 1992
; Camaioni et al., 1996
). PH-20 is a glycosyl phosphatidylinositolanchored membrane protein first identified on the posterior head of guinea pig sperm. It has an N-terminal hyaluronidase domain that is used by acrosome-intact sperm to penetrate the cumulus matrix. Its C-terminal domain is thought to be involved in secondary sperm binding, but the mechanism remains unknown (Hunnicutt et al., 1996
). Homologues of PH-20 have been identified and localized to the same regions in sperm from several other mammalian species, including mouse, rat, human, and macaque (Thaler and Cardullo, 1995
; Sabeur et al., 1997
; Yudin et al., 1999
; Seaton et al., 2000
).
In pigs, a ligand recognized by P-selectin is present in the ZP, and P-selectin exists on the acrosomal membrane of sperm. P-selectin is only detected by antibodies in acrosome reacted sperm, suggesting that it plays a role in sperm-egg recognition following the AR (Geng et al., 1997). Removal of sialic acid (an important glycan of P-selectin ligands) from mZP3 does not affect binding to mouse sperm or the AR (Litscher and Wassarman, 1996
), lending further support to the notion that P-selectin is involved in secondary binding. However, p-selectin deficient mice are fully fertile (Mayadas et al., 1993
).
Summary
The molecules of spermegg recognition in echinoderms appear to be entirely different from those of ascidians and vertebrates. An intriguing possibility is that a sea urchin REJ homologue is a mammalian sperm receptor. A testis-specific mammalian homologue of REJ, PKDREJ, of unknown function, has been cloned from mouse and human (Hughes et al., 1999). The ascidian spermegg recognition system involves glycosidases binding to their appropriate glycosides. In vertebrates, glycosidases have also been implicated in spermegg binding (Martinez et al., 2000
), and in cleaving glycosides so that the sperm can penetrate the ZP (Miller et al., 1992
). Among vertebrates, evidence indicates that the ZP proteins are the crucial molecules responsible for the initial spermegg recognition events. However, the ZP protein family members serve different functions and are differentially glycosylated in the egg coats of different vertebrate groups. Furthermore, there is indirect evidence that carbohydrates play a role in species-specificity of sperm binding in vertebrates (Rankin et al., 1998
; Doren et al., 1999
). Although there is good support that oligosaccharides of the ZP proteins are crucial for primary sperm binding and induction of the AR in vertebrates, the identification of the ZP receptor on sperm remains uncertain. sp56, proacrosin, and GalTase are all candidate ZP receptors. The main focus of research to date has been in identifying primary binding events, but it is apparent from these data that there are many more potential factors in spermegg interactions leading to the fusion of two gametes. Much more work needs to be done to clearly delineate the complicated processes of spermegg interaction during fertilization.
Acknowledgments
Research in our laboratory is funded by NIH HD12986. We thank Eric E. Allen, Lihini I. Aluwihare, and Gary W. Moy for reviewing the manuscript.
Abbreviations
AR, acrosome reaction; ARIS, acrosome reactioninducing substance; CRDs, C-type lectin domains; DMA, diluted mucous area; FSP, fucose sulfate polymer; GalTase, ß-14-galactosyltransferase; REJ, receptor for egg jelly; VC, vitelline coat; VE, vitelline envelope; WGA, wheat germ agglutinin; ZP, zona pellucida.
Footnotes
1 To whom correspondence should be addressed
References
Adham, I.M., Nayernia, K., and Engel, W. (1997) Spermatozoa lacking acrosin protein show delayed fertilization. Mol. Reprod. Dev., 46, 370376.[ISI][Medline]
Alves, A.P., Mulloy, B., Diniz, J.A., and Mourão, P.A. (1997) Sulfated polysaccharides from the egg jelly layer are species-specific inducers of acrosomal reaction in sperms of sea urchins. J. Biol. Chem., 272, 69656971.
Alves, A.P., Mulloy, B., Moy, G.W., Vacquier, V.D., and Mourão, P.A. (1998) Females of the sea urchin Strongylocentrotus purpuratus differ in the structures of their egg jelly sulfated fucans. Glycobiology, 8, 939946.
Aviles, M., Okinaga, T., Shur, B.D., and Ballesta, J. (2000) Differential expression of glycoside residues in the mammalian zona pellucida. Mol. Reprod. Dev., 57, 296308.[ISI][Medline]
Baba, T., Azuma, S., Kashiwabara, S., and Toyoda, Y. (1994) Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J. Biol. Chem., 269, 3184531849.
Baginski, T., Hirohashi, N., and Hoshi, M. (1999) Sulfated O-linked glycans of the vitelline coat as ligands in gamete interaction in the ascidian, Halocynthia roretzi. Dev. Growth Differ., 41, 357364.[ISI][Medline]
Bleil, J.D., and Wassarman, P.M. (1988) Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoproteins sperm receptor activity [published erratum appears in Proc Natl Acad Sci USA 1988 Dec;85(24):9600]. Proc. Natl. Acad. Sci. USA, 85, 67786782.[Abstract]
Bleil, J.D., and Wassarman, P.M. (1990) Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc. Natl Acad. Sci. USA, 87, 55635567.[Abstract]
Bonsignorio, D., Perego, L., Del Giacco, L., and Cotelli, F. (1996) Structure and macromolecular composition of the zebrafish egg chorion. Zygote, 4, 101108.[Medline]
Bookbinder, L.H., Cheng, A., and Bleil, J.D. (1995) Tissue- and species-specific expression of sp56, a mouse sperm fertilization protein [see comments] [published erratum appears in Science 1995 Aug 25;269(5227):1120]. Science, 269, 8689.[ISI][Medline]
Brewis, I.A., and Moore, H.D. (1997) Molecular mechanisms of gamete recognition and fusion at fertilization. Human Reprod., 12, 156165.[Abstract]
Burkin, H.R., and Miller, D.J. (2000) Zona pellucida protein binding ability of porcine sperm during epididymal maturation and the acrosome reaction. Dev. Biol., 222, 99109.[ISI][Medline]
Camaioni, A., Salustri, A., Yanagishita, M., and Hascall, V.C. (1996) Proteoglycans and proteins in the extracellular matrix of mouse cumulus cell-oocyte complexes. Arch. Biochem. Biophys., 325, 190198.[ISI][Medline]
Chen, J., Litscher, E.S., and Wassarman, P.M. (1998) Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. Proc. Natl Acad. Sci. USA, 95, 61936197.
Cheng, A., Le, T., Palacios, M., Bookbinder, L.H., Wassarman, P.M., Suzuki, F., and Bleil, J.D. (1994) Sperm-egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3. J. Cell Biol., 125, 867878.[Abstract]
Crosby, J.A., and Barros, C. (1999) Effect of recombinant boar beta-acrosin on sperm binding to intact zona pellucida during in vitro fertilization. Biol. Reprod., 61, 15351540.
Dandekar, P., Aggeler, J., and Talbot, P. (1992) Structure, distribution and composition of the extracellular matrix of human oocytes and cumulus masses. Human Reprod., 7, 391398.[Abstract]
Darszon, A., Labarca, P., Nishigaki, T., and Espinosa, F. (1999) Ion channels in sperm physiology. Physiol. Rev., 79, 481510.
DeAngelis, P.L., and Glabe, C.G. (1990) Specific recognition of sulfate esters by bindin, a sperm adhesion protein from sea urchins. Biochim. Biophys. Acta, 1037, 100105.[ISI][Medline]
Dell, A., Morris, H.R., Easton, R.L., Patankar, M., and Clark, G.F. (1999) The glycobiology of gametes and fertilization. Biochim. Biophys. Acta, 1473, 196205.[ISI][Medline]
Dhume, S.T., and Lennarz, W.J. (1995) The involvement of O-linked oligosaccharide chains of the sea urchin egg receptor for sperm in fertilization. Glycobiology, 5, 1117.[Abstract]
Doren, S., Landsberger, N., Dwyer, N., Gold, L., Blanchette-Mackie, J., and Dean, J. (1999) Incorporation of mouse zona pellucida proteins into the envelope of Xenopus laevis oocytes. Dev. Genes Evol., 209, 330339.[ISI][Medline]
Drickamer, K. (1988) Two distinct classes of carbohydrate-recognition domains in animal lectins. J. Biol. Chem., 263, 95579560.
Easton, R.L., Patankar, M.S., Lattanzio, F.A., Leaven, T.H., Morris, H.R., Clark, G.F., and Dell, A. (2000) Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen. J. Biol. Chem., 275, 77317742.
Evans, J.P. (2000) Getting sperm and egg together: things conserved and things diverged. Biol. Reprod., 63, 355360.
Flannery, B., and Epel, D. (1998) Effects of wheat germ agglutinin on tunicate egg activation and fertilization: is there a plasma membrane sperm receptor system on Ascidia ceratodes eggs? Dev. Growth Differ., 40, 297306.[ISI][Medline]
Florman, H.M., and Wassarman, P.M. (1985) O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell, 41, 313324.[ISI][Medline]
Foster, J.A., Friday, B.B., Maulit, M.T., Blobel, C., Winfrey, V.P., Olson, G.E., Kim, K.S., and Gerton, G.L. (1997) AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins. J. Biol. Chem., 272, 1271412722.
Geng, J.G., Raub, T.J., Baker, C.A., Sawada, G.A., Ma, L., and Elhammer, A.P. (1997) Expression of a P-selectin ligand in zona pellucida of porcine oocytes and P-selectin on acrosomal membrane of porcine sperm cells. Potential implications for their involvement in sperm-egg interactions. J. Cell Biol., 137, 743754.
Hoshi, M., De Santis, R., Pinto, M.R., Cotelli, F., and Rosati, F. (1983) Is a sperm -L-fucsidase responsible for sperm-egg binding in Ciona intestinalis. In J. Andre, ed., The Sperm Cell, Martinus Nijhoff Publishers, The Hague, pp. 107110.
Hoshi, M., De Santis, R., Pinto, M.R., Cotelli, F., and Rosati, F. (1985) Sperm glycosidases as mediators of sperm-egg binding in ascidians. Zool. Sci., 2, 6569.[ISI]
Hoshi, M., Okinaga, T., Kontani, K., Araki, T., and Chiba, K. (1991) Acrosome reaction-inducing glycoconjugate in the jelly coat of starfish eggs. In B. Baccetti, ed., Comparative Spermatology 20 Years After, Raven Press, New York, pp. 175180.
Hughes, J., Ward, C.J., Aspinwall, R., Butler, R., and Harris, P.C. (1999) Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein. Human Mol. Gen., 8, 543549.
Hunnicutt, G.R., Primakoff, P., and Myles, D.G. (1996) Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol. Reprod., 55, 8086.[Abstract]
Iwamatsu, T., Yoshizaki, N., and Shibata, Y. (1997) Changes in the chorion and sperm entry into the micropyle during fertilization in the teleostean fish, Oryzias latipes. Dev. Growth Differ., 39, 3341.[ISI][Medline]
Johnston, D.S., Wright, W.W., Shaper, J.H., Hokke, C.H., Van den Eijnden, D.H., and Joziasse, D.H. (1998) Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. A second site on sperm binds a nonfucosylated, beta-galactosyl-capped oligosaccharide. J. Biol. Chem., 273, 18881895.
Jones, R. (1991) Interaction of zona pellucida glycoproteins, sulfated carbohydrates and synthetic polymers with proacrosin, the putative egg-binding protein from mammalian spermatozoa. Development (Cambridge), 111, 11551164.[Abstract]
Jones, R., Brown, C.R., and Lancaster, R.T. (1988) Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilization. Development (Cambridge), 102, 781792.[Abstract]
Just, M.L., and Lennarz, W.J. (1997) Reexamination of the sequence of the sea urchin egg receptor for sperm: implications with respect to its properties. Dev. Biol., 184, 2530.[ISI][Medline]
Kan, F.W. (1990) High-resolution localization of hyaluronic acid in the golden hamster oocyte-cumulus complex by use of a hyaluronidase-gold complex. Anat. Rec., 228, 370382.[ISI][Medline]
Kitazume-Kawaguchi, S., Inoue, S., Inoue, Y., and Lennarz, W.J. (1997) Identification of sulfated oligosialic acid units in the O-linked glycan of the sea urchin egg receptor for sperm. Proc. Natl Acad. Sci. USA, 94, 36503655.
Koyota, S., Wimalasir, K.M.S., and Hoshi, M. (1997) Structure of the main saccharide chain in the acrosome reaction-inducing substance of the starfish, Asterias amurensis. J. Biol. Chem., 272, 1037210376.
Kubo, H., Kawano, T., Tsubuki, S., Kawashima, S., Katagiri, C., and Suzuki, A. (1997) A major glycoprotein of Xenopus egg vitelline envelope, gp41, is a frog homolog of mammalian ZP3. Dev. Growth Differ., 39, 405417.[ISI][Medline]
Kudo, K., Yonezawa, N., Katsumata, T., Aoki, H., and Nakano, M. (1998) Localization of carbohydrate chains of pig sperm ligand in the glycoprotein ZPB of egg zona pellucida. Eur. J. Biochem., 252, 492499.[Abstract]
Lambert, C.C. (1986) Fertilization-induced modification of chorion N-acetylglucosamine groups blocks polyspermy in ascidian eggs. Dev. Biol., 116, 168173.[ISI]
Lambert, C.C. (1989) Ascidian eggs release glycosidase activity which aids in the block against polyspermy. Development, 105, 415420.[Abstract]
Larson, J.L., and Miller, D.J. (1997) Sperm from a variety of mammalian species express beta1, 4-galactosyltransferase on their surface. Biol. Reprod., 57, 442453.[Abstract]
Leyton, L., and Saling, P. (1989) Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J. Cell Biol., 108, 21632168.[Abstract]
Litscher, E.S., and Wassarman, P.M. (1996) Characterization of mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro. Biochemistry, 35, 39803985.[ISI][Medline]
Liu, C., Litscher, E.S., and Wassarman, P.M. (1997) Zona pellucida glycoprotein mZP3 bioactivity is not dependent on the extent of glycosylation of its polypeptide or on sulfation and sialylation of its oligosaccharides. J. Cell Sci., 110, 745752.
Loeser, C.R., and Tulsiani, D.R. (1999) The role of carbohydrates in the induction of the acrosome reaction in mouse spermatozoa. Biol. Reprod., 60, 94101.
Loeser, C.R., Lynch, C. II, and Tulsiani, D.R. (1999) Characterization of the pharmacological-sensitivity profile of neoglycoprotein-induced acrosome reaction in mouse spermatozoa. Biol. Reprod., 61, 629634.
Lu, Q., and Shur, B.D. (1997) Sperm from beta 1, 4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development, 124, 41214131.
Lyons, C.E., Payette, K.L., Price, J.L., and Huang, R.C. (1993) Expression and structural analysis of a teleost homolog of a mammalian zona pellucida gene [published erratum appears in J Biol Chem 1998 Mar 27;273(13):7782]. J. Biol. Chem., 268, 2135121358.
Macek, M.B., Lopez, L.C., and Shur, B.D. (1991) Aggregation of beta-1, 4-galactosyltransferase on mouse sperm induces the acrosome reaction. Dev. Biol., 147, 440444.[ISI][Medline]
Martinez, M.L., Martelotto, L., and Cabada, M.O. (2000) Purification and biological characterization of N-acetyl beta-D glucosaminidase from Bufo arenarum spermatozoa. Mol. Reprod. Dev., 57, 194203.[ISI][Medline]
Matsuura, K., Sawada, H., and Yokosawa, H. (1993) Purification and properties of N-acetylglucosaminidase from eggs of the ascidian, Halocynthia roretzi. Eur. J. Biochem., 218, 535541.[Abstract]
Matsuura, K., Sawada, H., and Yokosawa, H. (1995) N-acetylglucosaminidase inhibitor isolated from the vitelline coat of ascidian eggs is a candidate sperm receptor. Biochem. Biophys. Res. Commun., 213, 311316.[ISI][Medline]
Mauk, R., Jaworski, D., Kamei, N., and Glabe, C.G. (1997) Identification of a 97-kDa heat shock protein from S. franciscanus ovaries with 94% amino acid identity to the S. purpuratus egg surface receptor for sperm. Dev. Biol., 184, 3137.[ISI][Medline]
Mayadas, T.N., Johnson, R.C., Rayburn, H., Hynes, R.O., and Wagner, D.D. (1993) Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell, 74, 541554.[ISI][Medline]
Miller, D.J., Macek, M.B., and Shur, B.D. (1992) Complementarity between sperm surface beta-1, 4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature, 357, 589593.[ISI][Medline]
Mori, E., Mori, T., and Takasaki, S. (1997) Binding of mouse sperm to beta-galactose residues on egg zona pellucida and asialofetuin-coupled beads. Biochem. Biophys. Res. Commun., 238, 9599.[ISI][Medline]
Moy, G.W., Mendoza, L.M., Schulz, J.R., Swanson, W.J., Glabe, C.G., and Vacquier, V.D. (1996) The sea urchin sperm receptor for egg jelly is a modular protein with extensive homology to the human polycystic kidney disease protein, PKD1. J. Cell Biol., 133, 809817.[Abstract]
Murata, K., Sasaki, T., Yasumasu, S., Iuchi, I., Enami, J., Yasumasu, I., and Yamagami, K. (1995) Cloning of cDNAs for the precursor protein of a low-molecular-weight subunit of the inner layer of the egg envelope (chorion) of the fish Oryzias latipes. Dev. Biol., 167, 917.[ISI][Medline]
Murata, K., Sugiyama, H., Yasumasu, S., Iuchi, I., Yasumasu, I., and Yamagami, K. (1997) Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc. Natl Acad. Sci. USA, 94, 20502055.
Ohlendieck, K., and Lennarz, W.J. (1995) Role of the sea urchin egg receptor for sperm in gamete interactions. Trends Biochem. Sci., 20, 2933.[ISI][Medline]
Prasad, S.V., Skinner, S.M., Carino, C., Wang, N., Cartwright, J., and Dunbar, B.S. (2000) Structure and function of the proteins of the mammalian zona pellucida. Cells Tiss. Organs, 166, 148164.[ISI][Medline]
Rankin, T.L., Tong, Z.B., Castle, P.E., Lee, E., Gore-Langton, R., Nelson, L.M., and Dean, J. (1998) Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development, 125, 24152424.
Rebeiz, M., and Miller, D.J. (1999) Porcine sperm surface beta1, 4galactosyltransferase binds to the zona pellucida but is not necessary or sufficient to mediate sperm-zona pellucida binding. Mol. Reprod. Dev., 54, 379387.[ISI][Medline]
Sabeur, K., Cherr, G.N., Yudin, A.I., Primakoff, P., Li, M.W., and Overstreet, J.W. (1997) The PH-20 protein in human spermatozoa. J. Androl., 18, 151158.
Seaton, G.J., Hall, L., and Jones, R. (2000) Rat sperm 2B1 glycoprotein (PH20) contains a C-terminal sequence motif for attachment of a glycosyl phosphatidylinositol anchor. Effects of endoproteolytic cleavage on hyaluronidase activity. Biol. Reprod., 62, 16671676.
Shalgi, R., and Raz, T. (1997) The role of carbohydrate residues in mammalian fertilization. Histol. Histopath., 12, 813822.[ISI][Medline]
Shur, B.D., Evans, S., and Lu, Q. (1998) Cell surface galactosyltransferase: current issues. Glycoconj. J., 15, 537548.[ISI][Medline]
Takasaki, S., Mori, E., and Mori, T. (1999) Structures of sugar chains included in mammalian zona pellucida glycoproteins and their potential roles in sperm-egg interaction. Biochim. Biophys. Acta, 1473, 206215.[ISI][Medline]
Thaler, C.D., and Cardullo, R.A. (1995) Biochemical characterization of a glycosylphosphatidylinositol-linked hyaluronidase on mouse sperm. Biochemistry, 34, 77887795.
Thaler, C.D., and Cardullo, R.A. (1996) The initial molecular interaction between mouse sperm and the zona pellucida is a complex binding event. J. Biol. Chem., 271, 2328923297.
Thall, A.D., Maly, P., and Lowe, J.B. (1995) Oocyte Gal-alpha-1, 3gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J. Biol. Chem., 270, 2143721440.
Tian, J., Gong, H., and Lennarz, W.J. (1999) Xenopus laevis sperm receptor gp69/64 glycoprotein is a homolog of the mammalian sperm receptor ZP2. Proc. Natl Acad. Sci. USA, 96, 829834.
Urch, U.A., and Patel, H. (1991) The interaction of boar sperm proacrosin with its natural substrate, the zona pellucida, and with polysulfated polysaccharides. Development (Cambridge), 111, 11651172.[Abstract]
Ushiyama, A., Chiba, K., Shima, A., and Hoshi, M. (1995) Estimation by radiation inactivation of the minimum functional size of acrosome-reaction-inducing substance (ARIS) in the starfish, Asterias amurensis. Zygote, 3, 351355.[Medline]
Vacquier, V.D., and Moy, G.W. (1997) The fucose sulfate polymer of egg jelly binds to sperm REJ and is the inducer of the sea urchin sperm acrosome reaction. Dev. Biol., 192, 125135.[ISI][Medline]
Vacquier, V.D., Swanson, W.J., and Hellberg, M.E. (1995) What have we learned about sea urchin sperm bindin? Devel. Growth Diff., 37, 110.
Vilela-Silva, A.C., Alves, A.P., Valente, A.P., Vacquier, V.D., and Mourão, P.A. (1999) Structure of the sulfated alpha-L-fucan from the egg jelly coat of the sea urchin Strongylocentrotus franciscanus: patterns of preferential 2-O- and 4-O-sulfation determine sperm cell recognition. Glycobiology, 9, 927933.
Vo, L.H., and Hedrick, J.L. (2000) Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC in Xenopus laevis. Biol. Reprod., 62, 766774.
Wang, H., and Gong, Z. (1999) Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. Biochim. Biophys. Acta, 1446, 156160.[ISI][Medline]
Wassarman, P., Chen, J., Cohen, N., Litscher, E., Liu, C., Qi, H., and Williams, Z. (1999) Structure and function of the mammalian egg zona pellucida. J. Exp. Zool., 285, 251258.[ISI][Medline]
Wassarman, P.M. (1999a) Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell, 96, 175183.[ISI][Medline]
Wassarman, P.M. (1999b) The Parkes Lecture. Zona pellucida glycoprotein mZP3: a versatile player during mammalian fertilization. J. Reprod. Fertil., 116, 211216.[Abstract]
Yamagata, K., Murayama, K., Okabe, M., Toshimori, K., Nakanishi, T., Kashiwabara, S., and Baba, T. (1998) Acrosin accelerates the dispersal of sperm acrosomal proteins during acrosome reaction. J. Biol. Chem., 273, 1047010474.
Yang, J.C., and Hedrick, J.L. (1997) cDNA cloning and sequence analysis of the Xenopus laevis egg envelope glycoprotein gp43. Dev. Growth Differ., 39, 457467.[ISI][Medline]
Yonezawa, N., Mitsui, S., Kudo, K., and Nakano, M. (1997) Identification of an N-glycosylated region of pig zona pellucida glycoprotein ZPB that is involved in sperm binding. Eur. J. Biochem., 248, 8692.[Abstract]
Yudin, A.I., Vandevoort, C.A., Li, M.W., and Overstreet, J.W. (1999) PH-20 but not acrosin is involved in sperm penetration of the macaque zona pellucida. Mol. Reprod. Dev., 53, 350362.[ISI][Medline]
Yurewicz, E.C., Pack, B.A., Armant, D.R., and Sacco, A.G. (1993) Porcine zona pellucida ZP3 alpha glycoprotein mediates binding of the biotin-labeled M(r) 55, 000 family (ZP3) to boar sperm membrane vesicles. Mol. Reprod. Dev., 36, 382389.[ISI][Medline]
Yurewicz, E.C., Pack, B.A., and Sacco, A.G. (1991) Isolation, composition, and biological activity of sugar chains of porcine oocyte zona pellucida 55K glycoproteins. Mol. Reprod. Dev., 30, 126134.[ISI][Medline]