Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans.
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.
Garcia-Manyes
Sergi
S
Research Center for Bioelectronics and Nanobioscience, Barcelona Science Park, University of Barcelona, Josep Samitier 1-5, Barcelona E-08028, Spain.
Bucior
Iwona
I
Ros
Robert
R
Anselmetti
Dario
D
Sanz
Fausto
F
Burger
Max M
MM
Fernàndez-Busquets
Xavier
X
D000818:Animals; D002448:Cell Adhesion / Q000502:physiology*; D007126:Immunoglobulin Allotypes; D018625:Microscopy, Atomic Force / Q000379:methods*; D008958:Models, Molecular; D008970:Molecular Weight; D011161:Porifera / Q000737:chemistry; D011509:Proteoglycans / Q000737:chemistry* / Q000378:metabolism; D020349:Surface Plasmon Resonance; D013499:Surface Properties
D007126:Immunoglobulin Allotypes; D011509:Proteoglycans