Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans

Sergi Garcia-Manyes, Iwona Bucior, Robert Ros, Dario Anselmetti, Fausto Sanz, Max M. Burger, Xavier Fernàndez-Busquets

Research output: Contribution to journalArticle

30 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)5992-5999
Number of pages8
JournalJournal of Biological Chemistry
Volume281
Issue number9
DOIs
StatePublished - Mar 3 2006
Externally publishedYes

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ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Garcia-Manyes, S., Bucior, I., Ros, R., Anselmetti, D., Sanz, F., Burger, M. M., & Fernàndez-Busquets, X. (2006). Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans. Journal of Biological Chemistry, 281(9), 5992-5999. https://doi.org/10.1074/jbc.M507878200