Abstract
Early Metazoans had to evolve the first cell adhesion system addressed to maintaining stable interactions between cells constituting different individuals. As the oldest extant multicellular animals, sponges are good candidates to have remnants of the molecules responsible for that crucial innovation. Sponge cells associate in a species-specific process through multivalent calcium-dependent interactions of carbohydrate structures on an extracellular membrane-bound proteoglycan termed aggregation factor. Single-molecule force spectroscopy studies of the mechanics of aggregation factor self-binding indicate the existence of intermolecular carbohydrate adhesion domains. A 200-kDa aggregation factor glycan (g200) involved in cell adhesion exhibits interindividual differences in size and epitope content which suggest the existence of allelic variants. We have purified two of these g200 distinct forms from two individuals of the same sponge species. Comparison of allotypic versus isotypic g200 binding forces reveals significant differences. Surface plasmon resonance measurements show that g200 self-adhesion is much stronger than its binding to other unrelated glycans such as chondroitin sulfate. This adhesive specificity through multiple carbohydrate binding domains is a type of cooperative interaction that can contribute to explain some functions of modular proteoglycans in general. From our results it can be deduced that the binding strength/surface area between two aggregation factor molecules is comparable with that of focal contacts in vertebrate cells, indicating that strong carbohydrate-based cell adhesions evolved at the very start of Metazoan history.
Highlights
By relatively weak forces that, when multimerized, can be potentiated by orders of magnitude, representing a highly versatile form of cell adhesion given the extraordinary plasticity of their structures [6]
Among the few known examples of carbohydrate self-recognition proposed to be specific in biological processes are the multivalent binding of Lewisx epitopes involved in the first steps of embryogenesis [7, 8], glycolipid-glycolipid interactions controlling cell adhesion, spreading, and motility (9 –11), and self-interactions of the glycan portion of sponge proteoglycans leading to species-specific cell adhesion [12, 13]
Sponge cells associate in a species-specific process through multivalent interactions of carbohydrate structures on a type of extracellular proteoglycan termed aggregation factor (14 –16)
Summary
The species-specific carbohydrates could have individual-specific structures and interactions, in view of the fact that allotype rejection could be shown in this lowest extant Metazoan phylum [35, 36]. We have performed force spectroscopy and surface plasmon resonance (SPR) studies of the self-interactions of MAF and MAF subunits purified from different individual sponges. Dissecting MAF into its active adhesive components has allowed us to track the individual self-binding units down to the circular core of the sunburst-like molecule and further down to the g200 glycan itself. The identification of different allelic-like g200 forms suggests a role for carbohydrate-carbohydrate interactions in sponge allogeneic recognition. The results obtained reveal surprisingly high forces and selectivity for this most ancient cell adhesion system and open new perspectives on proteoglycan function-structure relationships
Sign-in/Register to view highlights & summary 
Published Version (
Free)
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call