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

Eduardo Vilanova, Gustavo R. C. Santos, Rafael S. Aquino, Juan J. Valle-Delgado, Dario Anselmetti, Xavier Fernandez-Busquets, Paulo A. S. Mourao

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Abstract

Early metazoans had to evolve the first cell adhesion mechanism addressed to maintain a distinctive multicellular morphology. As the oldest extant animals, sponges are good candidates for possessing remnants of the molecules responsible for this crucial evolutionary innovation. Cell adhesion in sponges is mediated by the calcium-dependent multivalent self-interactions of sulfated polysaccharides components of extracellular membrane-bound proteoglycans, namely aggregation factors. Here, we used atomic force microscopy to demonstrate that the aggregation factor of the sponge Desmapsamma anchorata has a circular supramolecular structure and that it thus belongs to the spongican family. Its sulfated polysaccharide units, which were characterized via nuclear magnetic resonance analysis, consist preponderantly of a central backbone composed of 3-alpha-Glc1 units partially sulfated at 2-and 4-positions and branches of Pyr(4,6)alpha-Gal1 -> 3-alpha-Fuc2(SO3)1 -> 3-alpha-Glc4(SO3) 1 -> 3-alpha-Glc -> 4-linked to the central alpha-Glc units. Single-molecule force measurements of self-binding forces of this sulfated polysaccharide and their chemically desulfated and carboxyl-reduced derivatives revealed that the sulfate epitopes and extracellular calcium are essential for providing the strength and stability necessary to sustain cell adhesion in sponges. We further discuss these findings within the framework of the role of molecular structures in the early evolution of metazoans.

Original languageEnglish
Pages (from-to)9425-9437
JournalJournal of biological chemistry
Volume291
Issue number18
DOIs
Publication statusPublished - 29 Apr 2016
MoE publication typeA1 Journal article-refereed

Keywords

  • Sponges
  • Aggregation factors
  • Polysaccharides
  • Proteoglycans
  • Nuclear magnetic resonance
  • Atomic force microscopy
  • Evolution

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