Carbohydrate–carbohydrate interactions in cell recognition

Bucior, Iwona; Burger, Max M.

doi:10.1016/j.sbi.2004.08.006

Cited by 132 publications

(105 citation statements)

References 47 publications

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“…The vast structural plasticity of carbohydrates confers many combinatorial possibilities for fine-tuning cell-cell recognition, and their weak and reversible multivalent self-interactions endow strength and flexibility during the formation and maintenance of multicellular tissues (9). Several biological processes such as the early steps of embryo formation, metastasis, and cell-cell adhesion events are mediated by carbohydrate-carbohydrate interactions by means of van der Waals contacts, hydrogen bonds, electrostatic forces, and bridges of divalent ions (9,50).…”

Section: Discussionmentioning

confidence: 99%

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

Vilanova

Santos

Aquino

et al. 2016

Journal of Biological Chemistry

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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-␣-Glc1 units partially sulfated at 2-and 4-positions and branches of Pyr(4,6)␣-Gal133-␣-Fuc2(SO 3 )133-␣-Glc4(SO 3 )133-␣-Glc34-linked to the central ␣-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.Molecular clock estimates, paleobiogeochemical evidence, and the most widely accepted phylogenetic inferences place sponges (phylum Porifera) at the root of the metazoan tree as the oldest extant multicellular animals (1-4). Such ancestry makes modern sponges suitable organisms for studying the cellular and molecular aspects of the evolution of multicellularity (5). A pivotal feature of metazoans is their cell adhesion molecular machinery, which directs the formation and maintenance of a distinctive multicellular morphology (6). In most animals, protein interactions, such as those in the cell junctions of epithelia, mediate cell adhesion (7); however, sponge multicellularity is sustained by a characteristic cell adhesion and recognition mechanism based on specific carbohydrate-carbohydrate interactions (8).Carbohydrates have vast structural plasticity, ubiquitous distribution in vertebrate and invertebrate tissues, and are commonly associated with the cell surface (9). Carbohydrate selfadhesion is maintained by relatively weak forces that can increase in orders of magnitude upon the multimerization of individual epitopes into polysaccharides (10). Some examples of specific carbohydrate self-interactions include the multivalent binding of Lewis x epitopes involved in the first steps of embryogenesis (11), glycolipid-glycolipid interactions controlling cell adhesion, spreading, and motility (12), and self-interactions of sulfated polysaccharides leading to species-specific cell adhesion in sponges (13).Proteoglycan-like molecules termed aggregation factors (AFs) 4 mediate intercellu...

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Section: Discussionmentioning

confidence: 99%

“…Carbohydrates have vast structural plasticity, ubiquitous distribution in vertebrate and invertebrate tissues, and are commonly associated with the cell surface (9). Carbohydrate selfadhesion is maintained by relatively weak forces that can increase in orders of magnitude upon the multimerization of individual epitopes into polysaccharides (10).…”

mentioning

confidence: 99%

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

Vilanova

Santos

Aquino

et al. 2016

Journal of Biological Chemistry

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“…The AFs, identied in several marine sponge species (34,35,(38)(39)(40) are macromolecular complexes with molecular masses in the order of several million Daltons. They are composed mainly of protein and carbohydrate in variable, but substantial amounts, with a high net negative charge (37,41), and are called glyconectin (25) or spongican (27) C. The Red Beard Marine Sponge Microciona prolifera The supramolecular structure of the M. prolifera AF, called MAF, was elucidated by using immunochemical and electrophoretical procedures, combined with AFM imaging (26,27,30,42). The MAF complex has a sunburstlike shape (Fig.…”

Section: B Marine Spongesmentioning

confidence: 99%

“…arms is 140-180 nm long and has a beaded structure consisting of about 15 globules. MAF promotes adhesion of sponge cells through a two-step process involving: (i) a Ca 2＋ -dependent self-aggregation of the MAF complexes via MAFp3; and (ii) a Ca 2＋ -independent binding to cell surface receptors via MAFp4 (25)(26)(27)(28)(29)(30)44).…”

Section: B Marine Spongesmentioning

confidence: 99%

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The Sweet Love between Marine Sponge Cells

Johannis

Adriana

2008

TIGG

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229Trends Glycosci. Glycotechnol. Vol. 20 No. 115 (2008) AbstractTheˆrst step in the marine sponge cell recognition and adhesion operates via a Ca 2＋ -dependent carbohydrate-carbohydrate interaction. For the species Microciona prolifera the 200 kDa N-glycan (g-200) involved in the self-recognition is part of a proteoglycan-like macromolecular complex, the aggregation factor, with a molecular mass of 2×10 4 kDa. The complex has a sunburst-like shape. One of the carbohydrate epitopes involved in the self-interaction is a sulfated disaccharide fragment, b-D-GlcpNAc3S-(1ª3)-a-L-Fucp. In an attempt to mimick the polyvalent g-200 glycan-g-200 glycan self-recognition on the disaccharide level, the disaccharide epitope was synthesized and conjugated with bovine serum albumin, gold nanoparticles, and gold layers. The protein conjugates were used in UV and SPR experiments, the gold glyconanoparticles in TEM experiments, and the gold glycolayers in AFM experiments. It turned out that in the presence of 10 mM CaCl 2 the various disaccharide results match completely those obtained on the polymer level for M. prolifera cells and aggregation-factor-coated beads. A. IntroductionIn biological recognition and adhesion processes, protein-protein, carbohydrate-protein, and carbohydrate-carbohydrate interactions play key roles. The strength of the interactions, whereby carbohydrates are involved is a few orders of magnitude lower than those observed for protein-protein interactions, with carbohydrate-carbohydrate interactions weaker than carbohydrate-protein interactions.For a long time, direct carbohydrate-carbohydrate interactions between glycan chains of glycoproteins, glycolipids, and proteoglycans have been underestimated, if not ignored. However, nowadays the number of reports

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Applications of NMR to Biomolecular Systems of Interactions: An Overview

Hanashima

Yamaguchi

2013

Bio‐Nanotechnology

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Carbohydrate–carbohydrate interactions in cell recognition

Cited by 132 publications

References 47 publications

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

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

The Sweet Love between Marine Sponge Cells

Applications of NMR to Biomolecular Systems of Interactions: An Overview

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