title: Molecular recognition between glyconectins as an adhesion self-assembly pathway to multicellularity.
abstract: The appearance of multicellular forms of life has been tightly coupled to the ability of an organism to retain its own anatomical integrity and to distinguish self from non-self. Large glycoconjugates, which make up the outermost cell surface layer of all Metazoans, are the primary candidates for the primordial adhesion and recognition functions in biological self-assembly systems. Atomic force microscopy experiments demonstrated that the binding strength between a single pair of Porifera cell surface glyconectin 1 glycoconjugates from Microciona prolifera can hold the weight of 1600 cells, proving their adhesion functions. Here, measurement of molecular self-recognition of glyconectins (GNs) purified from three Porifera species was used as an experimental model for primordial xenogeneic self/non-self discrimination. Physicochemical and biochemical characterization of the three glyconectins, their glycans, and peptides using gel electrophoresis, ultracentrifugation, NMR, mass spectrometry, glycosaminoglycan-degrading enzyme treatment, amino acid and carbohydrate analyses, and peptide mapping showed that GNs define a new family of proteoglycan-like molecules exhibiting species-specific structures with complex and repetitive acidic carbohydrate motives different from the classical proteoglycans and mucins. In functional self-assembly color-coded bead, cell, and blotting assays, glyconectins displayed species-specific recognition and adhesion. Affinity-purified monospecific polyclonal antibodies prepared against GN1, -2, and -3 glycans selectively inhibited cell adhesion of the respective sponge species. These results together with species-specific coaggregation of GN carbohydrate-coated beads with cells showed that GN glycans are functional in cell recognition and adhesion. The specificity of carbohydrate-mediated homophilic GN interactions in Porifera approaches the binding selectivity of the evolutionarily advanced immunoglobulin superfamily. Xenoselectivity of primordial glyconectin to glyconectin recognition may be a new paradigm in the self-assembly and non-self discrimination pathway of cellular adhesion leading to multicellularity.
authors.affiliation: Laboratoire des Processus Intégratifs Cellulaires, UMR 6037 CNRS, Faculté des Sciences et Techniques de Rouen, 76821 Mont St Aignan Cedex, France. gradimir@gradimir.com
authors.forename: Gradimir N
authors.initials: GN
authors.lastname: Misevic
authors.forename: Yann
authors.initials: Y
authors.lastname: Guerardel
authors.forename: Lazar T
authors.initials: LT
authors.lastname: Sumanovski
authors.forename: Marie-Christine
authors.initials: MC
authors.lastname: Slomianny
authors.forename: Maurice
authors.initials: M
authors.lastname: Demarty
authors.forename: Camille
authors.initials: C
authors.lastname: Ripoll
authors.forename: Yannis
authors.initials: Y
authors.lastname: Karamanos
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Maes
authors.forename: Octavian
authors.initials: O
authors.lastname: Popescu
authors.forename: Gerard
authors.initials: G
authors.lastname: Strecker
mesh_terms: D000818:Animals; D002118:Calcium / Q000378:metabolism; D002241:Carbohydrates / Q000737:chemistry; D002448:Cell Adhesion; D015815:Cell Adhesion Molecules / Q000737:chemistry*; D002449:Cell Aggregation; D002462:Cell Membrane / Q000378:metabolism; D002849:Chromatography, Gas; D004305:Dose-Response Relationship, Drug; D004587:Electrophoresis, Agar Gel; D004591:Electrophoresis, Polyacrylamide Gel; D006025:Glycosaminoglycans / Q000737:chemistry; D007477:Ions; D009682:Magnetic Resonance Spectroscopy; D013058:Mass Spectrometry; D018625:Microscopy, Atomic Force; D009005:Monosaccharides / Q000737:chemistry; D009844:Oligosaccharides / Q000737:chemistry; D010455:Peptides / Q000737:chemistry; D011134:Polysaccharides / Q000737:chemistry* / Q000276:immunology*; D011161:Porifera; D011485:Protein Binding; D011509:Proteoglycans / Q000737:chemistry; D021241:Spectrometry, Mass, Electrospray Ionization; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
chemical_list: D002241:Carbohydrates; D015815:Cell Adhesion Molecules; D006025:Glycosaminoglycans; D007477:Ions; D009005:Monosaccharides; D009844:Oligosaccharides; D010455:Peptides; D011134:Polysaccharides; D011509:Proteoglycans; D002118:Calcium