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J. Biol. Chem., Vol. 277, Issue 49, 47796-47803, December 6, 2002

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Subtype-specific Expression of Group III Metabotropic Glutamate Receptors and Ca²⁺ Channels in Single Nerve Terminals^*

Carmelo Millán, Rafael Luján^§, Ryuichi Shigemoto^¶, and José Sánchez-Prieto

From the  Departamento de Bioquímica, Facultad de Veterinaria, Universidad Complutense, 28040 Madrid, Spain, the ^§ Centro Regional de Investigaciones Biomédicas, Facultad de Medicina, Universidad de Castilla-La Mancha, Campus de Albacete, 02071 Albacete, Spain, and the ^¶ National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan

The release properties of glutamatergic nerve terminals are influenced by a number of factors, including the subtype of voltage-dependent calcium channel and the presence of presynaptic autoreceptors. Group III metabotropic glutamate receptors (mGluRs) mediate feedback inhibition of glutamate release by inhibiting Ca²⁺ channel activity. By imaging Ca²⁺ in preparations of cerebrocortical nerve terminals, we show that voltage-dependent Ca²⁺ channels are distributed in a heterogeneous manner in individual nerve terminals. Presynaptic terminals contained only N-type (47.5%; conotoxin GVIA-sensitive), P/Q-type (3.9%; agatoxin IVA-sensitive), or both N- and P/Q-type (42.6%) Ca²⁺ channels, although the remainder of the terminals (6.1%) were insensitive to these two toxins. In this preparation, two mGluRs with high and low affinity for L(+)-2-amino-4-phosphonobutyrate were identified by immunocytochemistry as mGluR4 and mGluR7, respectively. These receptors were responsible for 22.2 and 24.1% reduction of glutamate release, and they reduced the Ca²⁺ response in 24.4 and 30.3% of the nerve terminals, respectively. Interestingly, mGluR4 was largely (73.7%) located in nerve terminals expressing both N- and P/Q-type Ca²⁺ channels, whereas mGluR7 was predominantly (69.9%) located in N-type Ca²⁺ channel-expressing terminals. This specific coexpression of different group III mGluRs and Ca²⁺ channels may endow synaptic terminals with distinct release properties and reveals the existence of a high degree of presynaptic heterogeneity.

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