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J Biol Chem. 2016 Apr 29;291(18):9425-37. doi: 10.1074/jbc.M115.708958. Epub 2016 Feb 25.

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

Author information

1
From the Hospital Universitário Clementino Fraga Filho and Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-913, Brazil.
2
Nanomalaria Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona 08028, Spain, Barcelona Institute for Global Health (ISGlobal), Hospital Clínic-Universitat de Barcelona, Barcelona 08036, Spain, Nanoscience and Nanotechnology Institute (IN2UB), University of Barcelona, Barcelona 08028, Spain, and.
3
Experimental Biophysics and Applied Nanoscience, Faculty of Physics, Bielefeld University, Bielefeld 33615, Germany.
4
Nanomalaria Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona 08028, Spain, Barcelona Institute for Global Health (ISGlobal), Hospital Clínic-Universitat de Barcelona, Barcelona 08036, Spain, Nanoscience and Nanotechnology Institute (IN2UB), University of Barcelona, Barcelona 08028, Spain, and xfernandez_busquets@ub.edu.
5
From the Hospital Universitário Clementino Fraga Filho and Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro 21941-913, Brazil, pmourao@hucff.ufrj.br.

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-α-Glc1 units partially sulfated at 2- and 4-positions and branches of Pyr(4,6)α-Gal1→3-α-Fuc2(SO3)1→3-α-Glc4(SO3)1→3-α-Glc→4-linked to the central α-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.

KEYWORDS:

aggregation factors; atomic force microscopy (AFM); evolution; nuclear magnetic resonance (NMR); polysaccharide; proteoglycan; sponges

PMID:
26917726
PMCID:
PMC4850283
DOI:
10.1074/jbc.M115.708958
[Indexed for MEDLINE]
Free PMC Article

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