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The Central domain of RyR1 is the transducer for long-range allosteric gating of channel opening.

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Bai XC, Yan Z, Wu J, Li Z, Yan N
OpenAccess logo Cell Res 26 995-1006 (2016)
Related entries: 5gky, 5gkz, 5gl0

Cited: 52 times
EuropePMC logo PMID: 27468892

Abstract

The ryanodine receptors (RyRs) are intracellular calcium channels responsible for rapid release of Ca(2+) from the sarcoplasmic/endoplasmic reticulum (SR/ER) to the cytoplasm, which is essential for the excitation-contraction (E-C) coupling of cardiac and skeletal muscles. The near-atomic resolution structure of closed RyR1 revealed the molecular details of this colossal channel, while the long-range allosteric gating mechanism awaits elucidation. Here, we report the cryo-EM structures of rabbit RyR1 in three closed conformations at about 4 Å resolution and an open state at 5.7 Å. Comparison of the closed RyR1 structures shows a breathing motion of the cytoplasmic platform, while the channel domain and its contiguous Central domain remain nearly unchanged. Comparison of the open and closed structures shows a dilation of the S6 tetrahelical bundle at the cytoplasmic gate that leads to channel opening. During the pore opening, the cytoplasmic "O-ring" motif of the channel domain and the U-motif of the Central domain exhibit coupled motion, while the Central domain undergoes domain-wise displacement. These structural analyses provide important insight into the E-C coupling in skeletal muscles and identify the Central domain as the transducer that couples the conformational changes of the cytoplasmic platform to the gating of the central pore.

Reviews - 5gl1 mentioned but not cited (1)

  1. Regulatory mechanisms of ryanodine receptor/Ca2+ release channel revealed by recent advancements in structural studies. Ogawa H, Kurebayashi N, Yamazawa T, Murayama T. J Muscle Res Cell Motil 42 291-304 (2021)

Articles - 5gl1 mentioned but not cited (2)

  1. The Central domain of RyR1 is the transducer for long-range allosteric gating of channel opening. Bai XC, Yan Z, Wu J, Li Z, Yan N. Cell Res 26 995-1006 (2016)
  2. 'Dusty core disease' (DuCD): expanding morphological spectrum of RYR1 recessive myopathies. Garibaldi M, Rendu J, Brocard J, Lacene E, Fauré J, Brochier G, Beuvin M, Labasse C, Madelaine A, Malfatti E, Bevilacqua JA, Lubieniecki F, Monges S, Taratuto AL, Laporte J, Marty I, Antonini G, Romero NB. Acta Neuropathol Commun 7 3 (2019)


Reviews citing this publication (13)

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Articles citing this publication (36)

  1. Structural mechanism of two gain-of-function cardiac and skeletal RyR mutations at an equivalent site by cryo-EM. Iyer KA, Hu Y, Nayak AR, Kurebayashi N, Murayama T, Samsó M. Sci Adv 6 eabb2964 (2020)
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  22. Insights into channel modulation mechanism of RYR1 mutants using Ca2+ imaging and molecular dynamics. Yamazawa T, Ogawa H, Murayama T, Yamaguchi M, Oyamada H, Suzuki J, Kurebayashi N, Kanemaru K, Oguchi K, Sakurai T, Iino M. J Gen Physiol 152 e201812235 (2020)
  23. The Cytoplasmic Region of Inner Helix S6 Is an Important Determinant of Cardiac Ryanodine Receptor Channel Gating. Sun B, Guo W, Tian X, Yao J, Zhang L, Wang R, Chen SR. J Biol Chem 291 26024-26034 (2016)
  24. Architecture of the human NALCN channelosome. Zhou L, Liu H, Zhao Q, Wu J, Yan Z. Cell Discov 8 33 (2022)
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  26. Molecular mechanism of the severe MH/CCD mutation Y522S in skeletal ryanodine receptor (RyR1) by cryo-EM. Iyer KA, Hu Y, Klose T, Murayama T, Samsó M. Proc Natl Acad Sci U S A 119 e2122140119 (2022)
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  28. Molecular Dynamics Simulations of the Cardiac Ryanodine Receptor Type 2 (RyR2) Gating Mechanism. Greene D, Barton M, Luchko T, Shiferaw Y. J Phys Chem B 126 9790-9809 (2022)
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  31. Identification of Potential Human Ryanodine Receptor 1 Agonists and Molecular Mechanisms of Natural Small-Molecule Phenols as Anxiolytics. Chen Y, Wang X, Zhai H, Zhang Y, Huang J. ACS Omega 6 29940-29954 (2021)
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  33. Eu3+ detects two functionally distinct luminal Ca2+ binding sites in ryanodine receptors. Magyar ZÉ, Bauer J, Bauerová-Hlinková V, Jóna I, Gaburjakova J, Gaburjakova M, Almássy J. Biophys J 122 3516-3531 (2023)
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