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J. Biol. Chem., Vol. 278, Issue 26, 23955-23962, June 27, 2003

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Co-expression of Metabotropic Glutamate Receptor 7 and N-type Ca²⁺ Channels in Single Cerebrocortical Nerve Terminals of Adult Rats^*

Carmelo Millán , Enrique Castro , Magdalena Torres , Ryuichi Shigemoto ¶ and José Sánchez-Prieto  ||

From the Departamento de Bioquímica, Facultad de Veterinaria, Universidad Complutense, 28040 Madrid, Spain, the Departamento de Bioquímica, Biología Molecular y Fisiología, Facultad de Ciencias de la Salud, Universidad de las Palmas de Gran Canaria (ULPG), 35016 Las Palmas, Spain, and the ^¶Division of Cerebral Structure, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan

The modulation of calcium channels by metabotropic glutamate receptors (mGluRs) is a key event in the fine-tuning of neurotransmitter release. Here we report that, in cerebrocortical nerve terminals of adult rats, the inhibition of glutamate release is mediated by mGluR7. In this preparation, the major component of glutamate release is supported by P/Q-type Ca²⁺ channels (72.7%). However, mGluR7 selectively reduced the release component that is associated with N-type Ca²⁺ channels (29.9%). Inhibition of P/Q channels by mGluR7 is not masked by the higher efficiency of these channels in driving glutamate release when compared with N-type channels. Thus, activation of mGluR7 failed to reduce the release associated with P/Q channels when the extracellular calcium concentration, ([Ca²⁺]_o), was reduced from 1.3 to 0.5 mM. Through Ca²⁺ imaging, we show that Ca²⁺ channels are distributed in a heterogeneous manner in individual nerve terminals. Indeed, in this preparation, nerve terminals were observed that contain N-type (31.1%; conotoxin GVIA-sensitive) or P/Q-type (64.3%; agatoxin IVA-sensitive) channels or that were insensitive to these two toxins (4.6%). Interestingly, the great majority of the responses to L-AP4 (95.4%) were observed in nerve terminals containing N-type channels. This specific co-localization of mGluR7 and N-type Ca²⁺-channels could explain the failure of the receptor to inhibit the P/Q channel-associated release component and also reveal the existence of specific targeting mechanisms to localize the two proteins in the same nerve terminal subset.

Received for publication, November 11, 2002 , and in revised form, April 11, 2003.

^* This work was supported by Ministerio de Ciencia y Tecnología (McyT) Grant BFI2001-1436 and Dirección General de Investigación de la Comunidad de Madrid Grant 08.5/0075.1/2000 (both to J. S. -P.). 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 should be addressed. Tel.: 34-91-394-3891; Fax: 34-91-394-3909; E-mail: jsprieto{at}vet.ucm.es.

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