Embryos of the sea urchin Strongylocentrotus purpuratus synthesize a dermatan sulfate enriched in 4-O- and 6-O-disulfated galactosamine units

Abstract

Unfertilized eggs of the sea urchin Strongylocentrotus purpuratus are surrounded by a gelatinous layer rich in sulfated fucan. Shortly after fertilization this polysaccharide disappears, but 24 h later the embryos synthesize high amounts of dermatan sulfate concomitantly with the mesenchyme blastula-early gastrula stage when the larval gut is forming. This glycosaminoglycan has the same backbone structure [4-alpha-L-IdoA-1-->3-beta-D-GalNAc-1](n) as the mammalian counterpart but possesses a different sulfation pattern. It has a high content of 4-O- and 6-O-disulfated galactosamine units. In addition, chains of this dermatan sulfate are considerable longer than those of vertebrate tissues. Adult sea urchin tissues contain high concentrations of sulfated polysaccharides, but dermatan sulfate is restricted to the adult body wall where it accounts for approximately 20% of the total sulfated polysaccharides. In addition, sulfation at the 4-O-position decreases markedly in the dermatan sulfate from adult sea urchin when compared with the glycan from larvae. Overall, these results demonstrate the occurrence of dermatan sulfates with unique sulfation patterns in this marine invertebrate. The physiological implication of these oversulfated dermatan sulfates is unclear. One hypothesis is that interactions between components of the extracellular matrix in marine invertebrates occur at higher salt concentrations than in vertebrates and therefore require glycosaminoglycans with increased charge density.

Oversulfated Dermatan Sulfate Exhibits Neurite Outgrowth-promoting Activity toward Embryonic Mouse Hippocampal Neurons

“…Such a modest activity of the adult sea urchin DS also appears to be correlated with its structure. Although the DS preparation contains appreciable proportions of disulfated disaccharide units, iE [Ido-UA-GalNAc(4S,6S)] at 25% and B [IdoUA(2S)-GalNAc(4S)] at 16% (Table I) (33), the former rather than the latter is presumably involved in the activity. This is because porcine skin DS (CS-B), which contains B units at 6%, was not neuritogenic, whereas DSD-1-PG/phosphacan, purified from neonatal mouse brains, which contains a small proportion (5.0%) of D or iD units, exhibits a marked neurite outgrowth promoting activity (15).…”

“…To test this idea, we assessed the neurite outgrowth-promoting activities of previously characterized various oversulfated DS preparations with different structures (31)(32)(33). The oversulfated DS preparations along with oversulfated CS-D and CS-E used in this study are summarized in Table I.…”

“…Two other DS preparations were purified from embryo and adult tissues of sea urchin S. purpuratus. The embryonic preparation was composed primarily of the iE disaccharide unit [IdoUA- GalNAc(4S,6S)] (74%), and the S/Unit was 1.74 (33). Although the adult preparation contained this disulfated disaccharide unit at 25%, it also contained the B disaccharide unit [IdoUA(2S)-GalNAc(4S)] at 16% (33), and the S/Unit value was 1.41, which was significantly lower than that of the embryonic preparation but significantly higher than that (1.06) of porcine skin DS (Table I).…”

“…Oversulfated DS preparations from ascidians A. nigra and S. plicata were isolated as reported previously (31,32). DS preparations from sea urchin S. purpuratus were isolated from the embryos and adult body walls as described previously (33). The purified DSD-1-PG was prepared from postnatal day 1 and postnatal day 15 mouse brains as described previously (12).…”

Role of the Vascular Wall in Sodium Homeostasis and Salt Sensitivity

“…24 Because interactions between components of the extracellular matrix seem to occur at higher salt concentrations in marine invertebrates than vertebrates, GAGs with increased charge density may be needed for keeping the intracellular environment stable, indicating that the more a subject is exposed to sodium, the more sulfated GAGs may be required. 24,25 In humans, highly sulfated heparan sulfates are mainly found in tissues having a barrier function, including skin, lung, intestine, and endothelium. …”