Molecular recognition between glyconectins as an adhesion self-assembly pathway to multicellularity.
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.
Misevic
Gradimir N
GN
Laboratoire des Processus Intégratifs Cellulaires, UMR 6037 CNRS, Faculté des Sciences et Techniques de Rouen, 76821 Mont St Aignan Cedex, France. gradimir@gradimir.com
Guerardel
Yann
Y
Sumanovski
Lazar T
LT
Slomianny
Marie-Christine
MC
Demarty
Maurice
M
Ripoll
Camille
C
Karamanos
Yannis
Y
Maes
Emmanuel
E
Popescu
Octavian
O
Strecker
Gerard
G
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
D002241:Carbohydrates; D015815:Cell Adhesion Molecules; D006025:Glycosaminoglycans; D007477:Ions; D009005:Monosaccharides; D009844:Oligosaccharides; D010455:Peptides; D011134:Polysaccharides; D011509:Proteoglycans; D002118:Calcium