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J. Biol. Chem., Vol. 275, Issue 46, 36049-36055, November 17, 2000

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Interaction of Luminal Calcium and Cytosolic ATP in the Control of Type 1 Inositol (1,4,5)-Trisphosphate Receptor Channels^*

Edwin C. Thrower, Hamid Mobasheri, Sheila Dargan, Phedra Marius, Edward J. A. Lea, and Alan P. Dawson^§

From the School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom

Ca²⁺ within intracellular stores (luminal Ca²⁺) is believed to play a role in regulating Ca²⁺ release into the cytosol via the inositol (1,4,5)-trisphosphate (Ins(1,4,5)P₃)-gated Ca²⁺ channel (or Ins(1,4,5)P₃ receptor). To investigate this, we incorporated purified Type 1 Ins(1,4,5)P₃ receptor from rat cerebellum into planar lipid bilayers and monitored effects at altered luminal [Ca²⁺] using K⁺ as the current carrier. At a high luminal [Ca²⁺] and in the presence of optimal [Ins(1,4,5)P₃] and cytosolic [Ca²⁺], a short burst of Ins(1,4,5)P₃ receptor channel activity was followed by complete inactivation. Lowering the luminal [Ca²⁺] caused the channel to reactivate indefinitely. At luminal [Ca²⁺], reflecting a partially empty store, channel activity did not inactivate. The addition of cytosolic ATP to a channel inactivated by high luminal [Ca²⁺] caused reactivation. We provide evidence that luminal Ca²⁺ is exerting its effects via a direct interaction with the luminal face of the receptor. Activation of the receptor by ATP may act as a device by which cytosolic Ca²⁺ overload is prevented when the energy state of the cell is compromised.

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