Fertilization / Development & Sugar chain
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Role of Glycoconjugates in Species-specific Recognition between Egg and Sperm

 In organisms, recognition between sperms and eggs is required for species maintenance. The eggs are covered with the egg extracellular matrix, which contains a considerable amount of glycoprotein. This matrix usually possesses a site that prevents the recognition of sperms, so a response to protect the egg against an attack from foreign bodies such as bacteria is not elicited.

The sperm is induced by a component of the egg extracellular matrix and is attached to the latter; it increases the [pH]i and [Ca2+]i on receiving a signal from the egg extracellular matrix and evokes exocytosis (acrosome reaction) of the acrosomal vesicle at the tip of the sperm head. It then passes the egg extracellular matrix and the vitelline membrane and arrives at the egg cell membrane. Only the new sperm cell membrane, which is detached by this exocytosis, can fuse with the egg cell membrane1) (Figure). A sugar chain is known to play an important role in the acrosome reaction and in the binding between the egg and sperm.
The ligand from the egg jelly binds to the sperm and induces the acrosome reaction in the eggs of the echinoderm sea urchin. The egg jelly sulfates the polysaccharides on the membrane of the sperm; this polysaccharides has been characterized, and it induces the acrosome reaction in a species-specific manner. In Strongylocentrotus purpuratus, the polysaccharide is a fucose sulfate polymer (FSP). The species specificity of the interaction is determined by the glycoside linkage of the polymer and the pattern of sulfation of the sugar residues.2) S. franciscanus and S. purpuratus belong to the same genus. They differ in the position of the sulfate residue that is linked to their polysaccharides. In the sea urchin S. franciscanus, sulfation of the polysaccharide occurs at the 2-position of fucose, while in S. purpuratus, sulfation occurs at the 4- position.3) Each sperm recognizes this difference and induces a species-specific acrosome reaction. An egg jelly receptor (suREJ1) to which FSP binds on the sperm membrane is present, and an anti-suREJ1 antibody can induce the acrosome reaction. The N-terminal end of SuREJ1 contains two carbohydrate recognition domains (CRDs) superfamily of immunoglobulin type C domains. It is assumed that CRD can contribute to the binding between suREJ1 and FSP, and it is known to be a domain that plays an important role in cell recognition, natural immunity, and cell signaling. Vacquier et al. analyzed the CRD of suREJ1-3 in six species of sea urchins in terms of evolution and found that this domain has an early evolution speed; they also showed that it a the gene which was controlled by positive selection (Darwinian selection).4) The egg jelly of starfish contained three molecules that are involved in the acrosome reaction. In the case of Asterias amurensis, the Co-ARIS of steroidal saponin and peptide asterosap of 34 amino acid residues assist in the reactions of the acrosome reaction-inducing substance (ARIS), which is a large and highly sulfated glycoprotein conjugate. The activity of the sugar chain is maintained by pronase digestion but is lost on hyper-iodine acid oxidation. Ten repeats of five sugar chains 4)-Xylp(13)- -Galp(13)--Fucp(4-SO3-)(13)--Fucp(4-SO3-)(14)--Fucp(1 form the smallest activity unit.5) A. amurensis ARIS induces the acrosome reaction at the same level (intra-species level) for the sperm of a starfish belonging to Asteriidae (same genus as A. amurensis) but not for the sperm of a starfish from a different genus. A similar result was obtained with the egg jelly from four species of starfish belonging to Asteriidae, as well as with the ARIS of A. amurensis. The egg jelly from Asteriidae contains the sugar repeat, including the same sulfate as that in ARIS; however, this repeat is absent in the egg jelly from other starfish. It is believed that the sperm recognizes the structure of the sugar chain of a specific ARIS at the genus level. From these data, we can examine whether the sugar chain and sulfate residues of the sugar repeats contribute to species differentiation by reproductive isolation.

In the case of the egg and sperm binding, sugar chain-modifying enzymes, which usually act as lectins, bind the sperm to the egg. The binding with the fucose ends of the vitelline membrane and the fucosidase of the sperm surface is essential for fertilization in the Protochordata Ciona intestinalis and Halocynthia roretzi. Further, the binding of the GlcNAc end of the vitelline membrane and the hexosaminidase of the sperm surface is necessary for fertilization in Phallusia mammillata.6-8)

As several millions of species inhabit the earth, their gametes should be able to recognize one other. The sugar chain is probably the best tool for ecognition between gametes in organisms.
Midori Matsumoto (Graduate School of Science and Technology, Keio University)
References (1) Darszon A, Beltran C, Felix R, Nishigaki T, Trevino CL: Ion transport in sperm signaling. Dev. Biol., 240, 1-14, 2001
(2) Alves AP, Mulloy B, Moy GW, Vacquier VD, Mourao PA: Females of the sea urchin Strongylocentrotus purpuratus differ in the structures of their egg jelly sulfated fucans. Glycobiology, 8, 939-946, 1998
(3) Hirohashi N, Vilela-Silva AC, Mourao PA, Vacquier, VD: Structural requirements for species-specific induction of the sperm acrosome reaction by sea urchin egg sulfated fucans. Biochem. Biophys. Res. Commun., 298, 403-407, 2002
(4) Mah SA, Swanson WJ, Vacquier VD: Positive selection in the carbohydrate recognition domains of sea urchin sperm receptor for egg jelly(suREJ) proteins. Mol. Biol Evol., 22, 533-541, 2005
(5) Koyota S, Wimalasiri KM, Hoshi M: Structure of the main saccharide chain in the acrosome reaction-inducing substance of the starfish, Asterias amurensis. J. Biol. Chem., 272, 10372-10376, 1997
(6) Hoshi M, Takizawa S, Hirohashi N: Glycosidases,. proteases and ascidian fertilization. Seminar in Dev. Biol., 5, 201-208, 1994
(7) Honegger TG: The involvement of sperm and egg glycosidases in animal fertilization. Trends Glycosci. Glycotech., 4, 437-444, 1992
(8) Baginski T, Hirohashi N, Hoshi M: Sulfated O-linked glycans of the vitelline coat as ligands in gamete interaction in the ascidian, Halocynthia roretzi. Dev. Growth Differ., 41, 357-364, 1999
Links
GP-A05 Mammalian Fertilization and Sugars (Seiichi Takasaki)
Mar. 31, 2006

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