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J. Biol. Chem., Vol. 279, Issue 46, 47975-47984, November 12, 2004

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Neural Cell Adhesion Molecule-associated Polysialic Acid Potentiates -Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptor Currents^*

Thirumalini Vaithianathan, Katja Matthias, Ben Bahr¶, Melitta Schachner||, Vishnu Suppiramaniam**, Alexander Dityatev||, and Christian Steinhaüser

From the Department of Pharmacal Sciences, Auburn University, Auburn, Alabama 36849, Experimental Neurobiology, Department of Neurosurgery, University of Bonn, Sigmund-Freud-Strasse 25, 53105 Bonn, Germany, ^¶Department of Pharmaceutical Sciences, University of Connecticut, Storrs, Connecticut 06269, and ^||Zentrum für Molekulare Neurobiologie, Universität Hamburg, Martinistrasse 52, 20246 Hamburg, Germany

The highly negatively charged polysialic acid (PSA) is a carbohydrate predominantly carried by the neural cell adhesion molecule (NCAM) in mammals. NCAM and, in particular, PSA play important roles in cellular and synaptic plasticity. Here we investigated whether PSA modulates the activity of the -amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) subtype of glutamate receptors (AMPA-Rs). Single channel recordings of affinity-purified AMPA-Rs reconstituted in lipid bilayers revealed that bacterially derived PSA, called colominic acid, prolonged the open channel time of AMPA-R-mediated currents by severalfold and altered the bursting pattern of the receptor channels but did not modify AMPA-R single channel conductance. This effect was reversible, concentration-dependent, and specific, since monomers of sialic acid and another negatively charged carbohydrate, chondroitin sulfate, did not potentiate single channel AMPA-R currents. Recombinant PSA-NCAM also potentiated currents mediated by reconstituted AMPA-Rs. In pyramidal neurons acutely isolated from the CA1 region of the early postnatal hippocampus, L-glutamate or AMPA (applied in the presence of antagonists blocking voltage-gated Na⁺ and K⁺ currents and N-methyl-D-aspartate and metabotropic glutamate receptors) induced inward currents, which were significantly increased by co-application of colominic acid. Chondroitin sulfate did not affect AMPA-R-mediated currents in CA1 neurons. The effect of colominic acid was age-dependent, since in pyramidal neurons from adult hippocampus, colominic acid failed to potentiate glutamate responses. Thus, our study demonstrates age-dependent potentiation of AMPA receptors by PSA via a mechanism probably involving direct PSA-AMPA-R interactions. This mechanism might amplify AMPA-R-mediated signaling in immature cells, thereby affecting their development.

Received for publication, June 25, 2004 , and in revised form, August 12, 2004.

^* This work was supported by Deutsche Forschungsgemeinschaft Grants DI 702/1–1 (to A. D.) and SFB Tr-3 and JA 942/4 (to C. S.) and by Fonds der Chemischen Industrie (to C. S. and M. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^** To whom correspondence may be addressed. Tel.: 334-844-8296; Fax: 334-844-8331; E-mail: suppivd{at}auburn.edu. To whom correspondence may be addressed. Tel.: 49-40-42803-6250; Fax: 49-89-42803-6302; E-mail: dityatev{at}zmnh.uni-hamburg.de.

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