Carbohydrate-carbohydrate interaction as a major force initiating cell-cell recognition

Abstract

Sponges were the earliest multicellular organisms to evolve through the development of cell recognition and adhesion processes mediated by cell surface proteoglycans. Information on sponges has an extra added value because, as a group, they are the oldest Metazoans alive and contribute more to our understanding of life on earth than knowledge of other animal groups. Although the proteoglycans are emerging as key players in various physiological and pathophysiological cellular events, little is known about the carbohydrate moiety of the proteoglycan molecule. Until recently there was no evidence provided for the existence of specific and biologically significant carbohydrate-carbohydrate interaction. We show here that the interaction between single oligosaccharides of surface proteoglycans is relatively strong (in the 200-300 piconewtons range) and in the same range as other relevant biological interactions, like those between antibodies and antigens. This carbohydrate-carbohydrate recognition is highly species-specific and perfectly mimics specific cell-cell recognition. Both the strength and the species-specificity of the carbohydrate-carbohydrate interaction are guaranteed by polyvalency, by compositional and architectural differences between carbohydrates, and by the arrangement of the carbohydrate chain in a three-dimensional context. Ca(2+)-ions are essential and probably provide coordinating forces. Our findings confirm the existence and character of species-specific carbohydrate-carbohydrate recognition fundamental to cell recognition and adhesion events.

Carbohydrate-Carbohydrate Interactions Mediated by Sulfate Esters and Calcium Provide the Cell Adhesion Required for the Emergence of Early Metazoans

“…Ref. 17), the homophilic and calcium-dependent self-interactions between sulfated polysaccharides components of AFs are the primary forces driving cell-cell adhesion in sponges. These interaction forces have been attributed to hydrogen bonds between the hydroxyl groups of sugar moieties of polysaccharides (10).…”

“…Certainly, the multivalent self-interactions of sulfated polysaccharides from AFs mediate cell adhesion in sponges (17). Assays using living sponge cells incubated in the presence of antibodies raised against AF glycans or in high concentrations of their homologous sulfated polysaccharides themselves demonstrated that these molecules must be physiologically available to promote cell adhesion (18,19).…”

The Sweet Love between Marine Sponge Cells

“…arms is 140-180 nm long and has a beaded structure consisting of about 15 globules. MAF promotes adhesion of sponge cells through a two-step process involving: (i) a Ca 2＋ -dependent self-aggregation of the MAF complexes via MAFp3; and (ii) a Ca 2＋ -independent binding to cell surface receptors via MAFp4 (25)(26)(27)(28)(29)(30)44).…”

“…In a more recent study (46), monosaccharide analysis of puried MAF showed the presence of GlcA, Fuc, Man, Gal, GlcNAc, GalNAc, and Gal4,6Pyr in the molar ratio 11:28:9:29:17:1:4, a carbohydrate content of 63z, and a sulfate content of 820 mol/mol. Another recent study focused on the g-200 glycan (29) revealed the occurrence of GlcA, Fuc, Man, Gal, GlcNAc, and GalNAc in the molar ratio 9:29:9:32:18:3.…”

“…The epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor (20)(21)(22). Finally, the g-200 glycan-g-200 glycan self-recognition is responsible for the species-speciˆc marine sponge aggregation (23)(24)(25)(26)(27)(28)(29)(30).…”