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J. Biol. Chem., Vol. 277, Issue 24, 21115-21118, June 14, 2002

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ACCELERATED PUBLICATION
Two-state Conformational Changes in Inositol 1,4,5-Trisphosphate Receptor Regulated by Calcium^*

Kozo Hamada^§, Tomoko Miyata^¶, Kouta Mayanagi^¶, Junji Hirota^**, and Katsuhiko Mikoshiba

From the  Laboratory for Developmental Neurobiology, Brain Science Institute, RIKEN (The Institute of Physical and Chemical Research), 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan, the ^¶ Biomolecular Engineering Research Institute (BERI), 6-2-3 Furuedai, Suita, Osaka, 565-0874, Japan, the  Division of Molecular Neurobiology, Department of Basic Medical Sciences, Institute of Medical Science, University of Tokyo, 4-6-1, Shirokanedai, Minato-ku, Tokyo 108-8639, Japan, and the  Calcium Oscillation Project, International Cooperative Research Project (ICORP), Japan Science and Technology Corporation (JST), 3-14-4, Shirokanedai, Minato-ku, Tokyo 108-0071, Japan

Inositol 1,4,5-trisphosphate receptor (IP₃R) is a highly controlled calcium (Ca²⁺) channel gated by inositol 1,4,5-trisphosphate (IP₃). Multiple regulators modulate IP₃-triggered pore opening by binding to discrete allosteric sites within IP₃R. Accordingly we have postulated that these regulators structurally control ligand gating behavior; however, no structural evidence has been available. Here we show that Ca²⁺, the most pivotal regulator, induced marked structural changes in the tetrameric IP₃R purified from mouse cerebella. Electron microscopy of the IP₃R particles revealed two distinct structures with 4-fold symmetry: a windmill structure and a square structure. Ca²⁺ reversibly promoted a transition from the square to the windmill with relocations of four peripheral IP₃-binding domains, assigned by binding to heparin-gold. Ca²⁺-dependent susceptibilities to limited digestion strongly support the notion that these alterations exist. Thus, Ca²⁺ appeared to regulate IP₃ gating activity through the rearrangement of functional domains.

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