The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization

Abstract

The evolution of barriers to inter-specific hybridization is a crucial step in the fertilization of free spawning marine invertebrates. In sea urchins, molecular recognition between sperm and egg ensures species recognition. Here we review the sulfated polysaccharide-based mechanism of sperm-egg recognition in this model organism. The jelly surrounding sea urchin eggs is not a simple accessory structure; it is molecularly complex and intimately involved in gamete recognition. It contains sulfated polysaccharides, sialoglycans and peptides. The sulfated polysaccharides have unique structures, composed of repetitive units of α-L-fucose or α-Lgalactose, which differ among species in the sulfation pattern and/or the position of the glycosidic linkage. The egg jelly sulfated polysaccharides show species-specificity in inducing the sperm acrosome reaction, which is regulated by the structure of the saccharide chain and its sulfation pattern. Other components of the egg jelly do not possess acrosome reaction inducing activity, but sialoglycans act in synergy with the sulfated polysaccharide, potentiating its activity. The system we describe establishes a new view of cell-cell interaction in the sea urchin model system. Here, structural changes in egg jelly polysaccharides modulate cell-cell recognition and speciesspecificity leading to exocytosis of the acrosome. Therefore, sulfated polysaccharides, in addition to their known functions as growth factors, coagulation factors and selectin binding partners, also function in fertilization. The differentiation of these molecules may play a role in sea urchin speciation.

Sperm and Egg Jelly Coat from Sea Urchin Lytechinus variegatus Collected in Rio de Janeiro Contain Distinct Sialic Acid-Rich Polysaccharides

“…This conclusion was supported by the presence of polysaccharides composed by sulfated fucose units, as reported by previous studies (Vilela-Silva et al 2002;Cinelli et al 2007). Sulfated fucans and sialic acid-rich glycoconjugates are the only carbohydrate-rich molecules found around the egg jelly of sea urchins (Mikami-Takey et al 1991;Vilela-Silva et al 2008). The sea urchin sperm contains a single fraction of acidic polysaccharide sensitive to metachromasy.…”

“…These processes require the presence of species-specific molecules, especially in free spawning marine invertebrates, in order to avoid polyspermy and inter-specific hybridization (Mah et al 2005). Studies on the structural characterization of polysaccharides from sea urchins led to the discovery of unique polymers (Alves et al 1997;Vilela-Silva et al 1999, 2008. These polysaccharides have simple, linear structures, composed of repeating units of oligosaccharides.…”

Structure versus anticoagulant and antithrombotic actions of marine sulfated polysaccharides

“…Recently, however, new and interesting sources of these compounds have been found in the extracellular matrices of certain marine invertebrates Mourão, 2004;2007;Pomin, 2008;2009;Pomin & Mourão, 2008). In contrast with most algal sulfated polysaccharides, the invertebrate polymers exhibit highly regular chemical structures ( Figure 1 and 2A-D), which make it easier to correlate their biological functions with their respective structural features (Pomin, 2008;Pomin & Mourão, 2008;Vilela-Silva et al, 2008). This is of enormous benefi t to the entire fi eld of glycobiology.…”

“…(Holothuroidea) (Mulloy et al 2004) and sea urchins (Echinoidea) (Pomin & Mourão, 2008;Vilela-Silva et al, 2008) or ascidians (Urochordata, Ascidiacea) (Mourão & Perlin, 1987;Santos et al, 1992;Pavão et al, 1995;Pavão et al, 1998;Vicente et al, 2001;Pavão, 2002). The SF ( sea urchin eggs.…”

“…The SF ( sea urchin eggs. As discussed below, these particular MSP are physiologically responsible for controlling the external fertilization in sea urchins in a very restrictive species-specific manner (Mourão, 2007;Vilela-Silva et al, 2008). Among all the MSP with well-defined chemical structures described so far (Figures 1 and 2), there is a single description from the body wall of the sea cucumber ( Figure 1A) (Mulloy et al, 2004), a few examples of SG isolated from the tunic of ascidians ( Figure 2C and 2D) (Mourão & Perlin, 1987;Santos et al, 1992;Pavão et al, 1998), and some reports from specific red algal cell walls ( Figure 2E) (Pereira et al, 2005;Fonseca et al, 2008).…”