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J. Biol. Chem., Vol. 281, Issue 7, 4274-4284, February 17, 2006

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Purinergic Receptors Mediate Two Distinct Glutamate Release Pathways in Hippocampal Astrocytes^*

From the Consiglio Nazionale delle Ricerche Istituto di Neuroscienze and Dipartimento di Scienze Biomediche Sperimentali, Università di Padova, viale G. Colombo 3, 35121 Padova, Italy

The purinergic P2X₇ receptor (P2X₇R) can mediate glutamate release from cultured astrocytes. Using patch clamp recordings, we investigated whether P2X₇Rs have the same action in hippocampal astrocytes in situ. We found that 2- and 3-O-(4-benzoylbenzoyl)ATP (BzATP), a potent, although unselective P2X₇R agonist, triggers two different glutamate-mediated responses in CA1 pyramidal neurons; they are transient inward currents, which have the kinetic and pharmacological properties of previously described slow inward currents (SICs) due to Ca²⁺-dependent glutamate release from astrocytes, and a sustained tonic current. Although SICs were unaffected by P2X₇Rs antagonists, the tonic current was inhibited, was amplified in low extracellular Ca²⁺, and was insensitive to glutamate transporter and hemichannel inhibitors. BzATP triggered in astrocytes a large depolarization that was inhibited by P2X₇R antagonists and amplified in low Ca²⁺. In low Ca²⁺ BzATP also induced lucifer yellow uptake into a subpopulation of astrocytes and CA3 neurons. Our results demonstrate that purinergic receptors other than the P2X₇R mediate glutamate release that evokes SICs, whereas activation of a receptor that has features similar to the P2X₇R, mediates a sustained glutamate efflux that generates a tonic current in CA1 neurons. This sustained glutamate efflux, which is potentiated under non-physiological conditions, may have important pathological actions in the brain.

Received for publication, September 30, 2005 , and in revised form, November 10, 2005.

^* This work was supported by grants from the Armenise-Harvard University Foundation, Italian University and Health Ministries (FIRB) Grant RBNE01RHZM_003 (to G. C), the Italian Association for Cancer Research (AIRC), and European Community Grant QLG3-CT-2000-00934) (to T. 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.

¹ To whom correspondence should be addressed. Tel.: 39-049-8276075; Fax: 39-049-8276049; E-mail: gcarmi{at}bio.unipd.it.

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