Early coevolution of adhesive but not antiadhesive tenascin-R ligand-receptor pairs in vertebrates: A phylogenetic study

• Published in: Molecular and cellular neuroscience 2006-08, Vol.32 (4), p.366-386
• Main Authors: Pesheva, Penka, Probstmeier, Rainer, Lang, Dirk M., McBride, Ruth, Hsu, Nai-Jen, Gennarini, Gianfranco, Spiess, Eberhard, Peshev, Zolo
• Format: Article
• Language: English
• Subjects: Animals; Axon guidance; Axons - drug effects; Cell Adhesion - drug effects; Cell Adhesion - physiology; Cell Adhesion Molecules, Neuronal - pharmacology; Cells, Cultured; Central Nervous System - cytology; Central Nervous System - metabolism; CNS; Contactins; Enzyme-Linked Immunosorbent Assay - methods; Evolution; Evolution, Molecular; Extracellular matrix; Fibronectins - pharmacology; Humans; Immunohistochemistry - methods; In Vitro Techniques; Indoles; Nerve Tissue Proteins - metabolism; Neurons - drug effects; Neurons - metabolism; Oligodendrocyte; Phylogeny; Protein Binding - drug effects; Receptors, Cell Surface - metabolism; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods; Sulfoglycosphingolipids - pharmacology; Tenascin - metabolism; Tenascin-R; Vertebrates - classification; Vertebrates - metabolism
• ISSN: 1044-7431; 1095-9327
• DOI: 10.1016/j.mcn.2006.05.008

Axon growth inhibitory CNS matrix proteins, such as tenascin-R (TN-R), have been supposed to contribute to the poor regenerative capacity of adult mammalian CNS. With regard to TN-R function in low vertebrates capable of CNS regeneration, questions of particular interest concern the (co)evolution of ligand-receptor pairs and cellular response mechanisms associated with axon growth inhibition and oligodendrocyte differentiation. We address here these questions in a series of comparative in vivo and in vitro analyses using TN-R proteins purified from different vertebrates (from fish to human). Our studies provide strong evidence that unlike TN-R of higher vertebrates, fish TN-R proteins are not repellent for fish and less repellent for mammalian neurons and do not interfere with F3/contactin- and fibronectin-mediated mammalian cell adhesion and axon growth. However, axonal repulsion is induced in fish neurons by mammalian TN-R proteins, suggesting that the intracellular inhibitory machinery induced by TN-R-F3 interactions is already present during early vertebrate evolution. In contrast to TN-R-F3, TN-R-sulfatide interactions, mediating oligodendrocyte adhesion and differentiation, are highly conserved during vertebrate evolution. Our findings thus indicate the necessity of being cautious about extrapolations of the function of ligand-receptor pairs beyond a species border and, therefore, about the phylogenetic conservation of a molecular function at the cellular/tissue level.