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J. Biol. Chem., Vol. 283, Issue 22, 15122-15126, May 30, 2008

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Permeation Properties of a P2X Receptor in the Green Algae Ostreococcus tauri^*

From the Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, United Kingdom

We have cloned a P2X receptor (OtP2X) from the green algae Ostreococcus tauri. The 42-kDa receptor shares 28% identity with human P2X receptors and 23% with the Dictyostelium P2X receptor. ATP application evoked flickery single channel openings in outside-out membrane patches from human embryonic kidney 293 cells expressing OtP2X. Whole-cell recordings showed concentration-dependent cation currents reversing close to zero mV; ATP gave a half-maximal current at 250 µM. β-Methylene-ATP evoked only small currents in comparison to ATP (EC₅₀ > 5 mM). 2',3'-O-(4-Benzoylbenzoyl)-ATP, β-imido-ATP, ADP, and several other nucleotide triphosphates did not activate any current. The currents evoked by 300 µM ATP were not inhibited by 100 µM suramin, pyridoxal-phosphate-6-azophenyl-2',4'-disulfonic acid, 2',3'-O-(2,4,6-trinitrophenol)-ATP, or copper. Ion substitution experiments indicated permeabilities relative to sodium with the rank order calcium >choline >Tris >tetraethylammonium >N-methyl-D-glucosamine. However, OtP2X had a low relative calcium permeability (P_Ca/P_Na = 0.4) in comparison with other P2X receptors. This was due at least in part to the presence of an asparagine residue (Asn³⁵³) at a position in the second transmembrane domain in place of the aspartate that is completely conserved in all other P2X receptor subunits, because replacement of Asn³⁵³ with aspartate increased calcium permeability by 50%. The results indicate that the ability of ATP to gate cation permeation across membranes exists in cells that diverged in evolutionary terms from animals about 1 billion years ago.

Received for publication, February 25, 2008 , and in revised form, April 1, 2008.

^* This work was supported by the Wellcome Trust. 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.

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¹ To whom correspondence should be addressed: Fax: 44-161-275-1497; E-mail: alan.north{at}manchester.ac.uk.

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