A protein from abalone sperm dissolves the egg vitelline layer by a nonenzymatic mechanism

Lewis, Cindy; Talbot, Craig F.; Vacquier, Victor D.

doi:10.1016/0012-1606(82)90167-1

Cited by 129 publications

(129 citation statements)

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“…Samples of Hr VERL, isolated by sucrose density gradient sedimentation, were viewed in the electron microscope after negative staining with uranyl acetate. The micrographs show that VERL is a long, unbranched rod of 13 nm diameter (7,8). The size distribution of lengths was not determined, however, the 20 longest rods imaged were 630 Ϯ 170 nm.…”

Section: Resultsmentioning

confidence: 98%

“…The first type is intimately bonded to the egg plasma membrane and is most extensively characterized in the sea urchin (14,15,26). The second type of egg envelope is elevated from the egg plasma membrane and is found in mollusks (7,8,27), ascidians (28)(29)(30), amphibians (31,32), and mammals (9,33,34). This discussion will pertain only to envelopes that are elevated from the plasma membrane and that the sperm must penetrate to reach the egg plasma membrane.…”

Section: Discussionmentioning

confidence: 99%

“…Lysin creates a 3-m diameter hole in the VE through which the spermatozoan passes to reach the egg cell membrane. Electron micrographs of the lysin-created hole show it is composed of splayed-apart fibers of 13-nm diameter; covalent bonds are not broken when lysin disrupts the VE (7).…”

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confidence: 99%

“…The abalone egg is surrounded by an elevated, glycoproteinaceous vitelline envelope (VE) 0.6 m in diameter (7,8). Spermatozoa bind to the VE, their acrosomal granule exocytoses, and lysin is released.…”

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The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

Swanson

Vacquier

1997

Proc. Natl. Acad. Sci. U.S.A.

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Abalone sperm lysin is a 16-kDa acrosomal protein, which nonenzymatically and species selectively creates a hole in the egg vitelline envelope (VE) through which the sperm passes to reach the egg cell membrane. The crystal structures of both monomeric and dimeric lysins have been solved and the sequences of lysins from 20 abalone species have been determined. As a first step in understanding the molecular mechanism by which lysin creates a hole in the VE, its VE receptor was isolated. The VE receptor for lysin (VERL) is an unbranched, rod-like molecule with an approximate relative molecular mass of 2 million; half the mass being carbohydrate. Fluorescence polarization studies showed positive cooperativity in the binding of lysin to VERL (EC 50 Ϸ9 nM) and were consistent with the species selectivity of lysin in dissolving VEs. Each molecule of VERL bound between 126 and 142 molecules of monomeric lysin (two independent assays), showing that VERL possesses repetitive lysin-binding motifs.Many marine invertebrate species spawn gametes into seawater, where fertilization and embryogenesis occur. In sea urchins (1, 2) and abalone (3, 4), several closely related, congeneric species may have overlapping breeding seasons and habitats. Such species usually exhibit species selectivity (specificity) in experimental cross-fertilizations, meaning that fertilization occurs more readily between homospecific mixtures of sperm and eggs than between heterospecific mixtures. The demonstrated species selectivity in the recognition events between invertebrate sperm and egg is a valuable model bearing on the general problem of the biochemistry of molecular recognition between cells.In marine invertebrates, the study of gamete recognition proteins may also yield information on the mechanism by which species arise in the sea, where barriers to larval transport are not readily apparent (5). Evidence that gamete recognition proteins may be involved in speciation comes from analyses of nucleotide substitutions in sea urchin sperm bindins (1) and abalone sperm acrosomal proteins (4, 6). Such analyses show that the evolution of these proteins has been promoted by positive Darwinian selection, suggesting there is significant adaptive value in altering their primary structure.The availability of large quantities of marine invertebrate gametes permits a detailed characterization of their gamete surface molecules involved in fertilization. The abalone egg is surrounded by an elevated, glycoproteinaceous vitelline envelope (VE) 0.6 m in diameter (7,8). Spermatozoa bind to the VE, their acrosomal granule exocytoses, and lysin is released. Lysin creates a 3-m diameter hole in the VE through which the spermatozoan passes to reach the egg cell membrane. Electron micrographs of the lysin-created hole show it is composed of splayed-apart fibers of 13-nm diameter; covalent bonds are not broken when lysin disrupts the VE (7).Although gamete recognition proteins have been cloned from both mammals (9-13) and invertebrates (1-4, 6, 14-16), the molec...

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Section: Resultsmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

Swanson

Vacquier

1997

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, sites within ZP3 under selection among mammals (13) correspond to the putative sperm binding domain in mouse (14,15). Similarly, the abalone sperm protein lysin binds to the ZP glycoprotein vitelline envelope receptor of lysin (VERL) (9) to facilitate sperm access to the egg membrane surface during fertilization (16), and both proteins show signs of adaptive divergence among abalone taxa (10,17,18). Coevolution between gamete recognition molecules is of significant interest because of their potential contribution to rapid reproductive isolation (19), which theoretical models show can occur even in sympatry if sexual conflict develops between components of male and female fitness (20).…”

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Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs

Aagaard

MacCoss

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

116

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Proteins harboring a zona pellucida (ZP) domain are prominent components of vertebrate egg coats. Although less well characterized, the egg coat of the non-vertebrate marine gastropod abalone (Haliotis spp.) is also known to contain a ZP domain protein, raising the possibility of a common molecular basis of metazoan egg coat structures. Egg coat proteins from vertebrate as well as non-vertebrate taxa have been shown to evolve under positive selection. Studied most extensively in the abalone system, coevolution between adaptively diverging egg coat and sperm proteins may contribute to the rapid development of reproductive isolation. Thus, identifying the pattern of evolution among egg coat proteins is important in understanding the role these genes may play in the speciation process. The purpose of the present study is to characterize the constituent proteins of the egg coat [vitelline envelope (VE)] of abalone eggs and to provide preliminary evidence regarding how selection has acted on VE proteins during abalone evolution. A proteomic approach is used to match tandem mass spectra of peptides from purified VE proteins with abalone ovary EST sequences, identifying 9 of 10 ZP domain proteins as components of the VE. Maximum likelihood models of codon evolution suggest positive selection has acted among a subset of amino acids for 6 of these genes. This work provides further evidence of the prominence of ZP proteins as constituents of the egg coat, as well as the prominent role of positive selection in diversification of these reproductive proteins.adaptive evolution ͉ egg coat proteins ͉ gamete recognition M etazoan eggs are surrounded by a fibrous coat referred to as the zona pellucida, as the vitelline or perivitelline envelope, or as the chorion. The constituent proteins of these structures, which we collectively refer to as egg coats, have been well characterized among vertebrate taxa, including species of mammals (1), teleost fish (2), amphibians (3), and birds (4). These studies show the principle constituents of vertebrate egg coats to be glycosylated proteins sharing a common structural motif of Ϸ260 aa known as the zona pellucida (ZP) domain. ZP domain proteins are found among diverse eukaryotic structures, facilitating protein polymerization through intramolecular disulfide bonds among conserved cysteine resides within the ZP domain (5). For example, the predominant model of mouse egg coat (zona pellucida) formation posits filaments of arrays of two ZP proteins (ZP2 and ZP3) crosslinked via a third (ZP1), resulting in a fibrous matrix completely enclosing the egg (1). Although orthologs of these mammalian proteins are known from egg coat structures across vertebrate lineages (6, 7), non-vertebrate taxa are less well studied and it is not yet clear whether ZP proteins are similarly prominent features of egg coats across metazoans. For example, all known proteins comprising Drosophila egg coat structures lack ZP domains (8). However, a large glycoprotein from the egg coat [vitelline envelope (VE)] of the m...

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Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and electron microscopy for the characterization of the vitelline coat glycoproteins of the polarized egg ofUnio elongatulus

Focarelli

Lupetti

Seraglia³

et al. 1997

Mol. Reprod. Dev.

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A protein from abalone sperm dissolves the egg vitelline layer by a nonenzymatic mechanism

Cited by 129 publications

References 37 publications

The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and electron microscopy for the characterization of the vitelline coat glycoproteins of the polarized egg ofUnio elongatulus

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