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Ca2+ signals initiate at immobile IP3 receptors adjacent to ER-plasma membrane junctions

Author

Listed:
  • Nagendra Babu Thillaiappan

    (University of Cambridge)

  • Alap P. Chavda

    (University of Cambridge
    Cactus Communications Pvt Ltd)

  • Stephen C. Tovey

    (University of Cambridge
    Cairn Research Ltd)

  • David L. Prole

    (University of Cambridge)

  • Colin W. Taylor

    (University of Cambridge)

Abstract

IP3 receptors (IP3Rs) release Ca2+ from the ER when they bind IP3 and Ca2+. The spatial organization of IP3Rs determines both the propagation of Ca2+ signals between IP3Rs and the selective regulation of cellular responses. Here we use gene editing to fluorescently tag endogenous IP3Rs, and super-resolution microscopy to determine the geography of IP3Rs and Ca2+ signals within living cells. We show that native IP3Rs cluster within ER membranes. Most IP3R clusters are mobile, moved by diffusion and microtubule motors. Ca2+ signals are generated by a small population of immobile IP3Rs. These IP3Rs are licensed to respond, but they do not readily mix with mobile IP3Rs. The licensed IP3Rs reside alongside ER-plasma membrane junctions where STIM1, which regulates store-operated Ca2+ entry, accumulates after depletion of Ca2+ stores. IP3Rs tethered close to ER-plasma membrane junctions are licensed to respond and optimally placed to be activated by endogenous IP3 and to regulate Ca2+ entry.

Suggested Citation

  • Nagendra Babu Thillaiappan & Alap P. Chavda & Stephen C. Tovey & David L. Prole & Colin W. Taylor, 2017. "Ca2+ signals initiate at immobile IP3 receptors adjacent to ER-plasma membrane junctions," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01644-8
    DOI: 10.1038/s41467-017-01644-8
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    Cited by:

    1. Máté Katona & Ádám Bartók & Zuzana Nichtova & György Csordás & Elena Berezhnaya & David Weaver & Arijita Ghosh & Péter Várnai & David I. Yule & György Hajnóczky, 2022. "Capture at the ER-mitochondrial contacts licenses IP3 receptors to stimulate local Ca2+ transfer and oxidative metabolism," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Vishal R. Patel & Arturo M. Salinas & Darong Qi & Shipra Gupta & David J. Sidote & Marcel P. Goldschen-Ohm, 2021. "Single-molecule imaging with cell-derived nanovesicles reveals early binding dynamics at a cyclic nucleotide-gated ion channel," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Maria Casas & Karl D. Murray & Keiko Hino & Nicholas C. Vierra & Sergi Simó & James S. Trimmer & Rose E. Dixon & Eamonn J. Dickson, 2023. "NPC1-dependent alterations in KV2.1–CaV1.2 nanodomains drive neuronal death in models of Niemann-Pick Type C disease," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Paloma García Casas & Michela Rossini & Linnea Påvénius & Mezida Saeed & Nikita Arnst & Sonia Sonda & Tânia Fernandes & Irene D’Arsiè & Matteo Bruzzone & Valeria Berno & Andrea Raimondi & Maria Livia , 2024. "Simultaneous detection of membrane contact dynamics and associated Ca2+ signals by reversible chemogenetic reporters," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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