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IP3 receptor isoforms differently regulate ER-mitochondrial contacts and local calcium transfer

Author

Listed:
  • Adam Bartok

    (Thomas Jefferson University
    Semmelweis University)

  • David Weaver

    (Thomas Jefferson University)

  • Tünde Golenár

    (Thomas Jefferson University)

  • Zuzana Nichtova

    (Thomas Jefferson University)

  • Máté Katona

    (Thomas Jefferson University)

  • Száva Bánsághi

    (Thomas Jefferson University)

  • Kamil J. Alzayady

    (University of Rochester)

  • V. Kaye Thomas

    (University of Rochester)

  • Hideaki Ando

    (RIKEN Brain Science Institute
    The University of Tokyo 7-3-1 Hongo)

  • Katsuhiko Mikoshiba

    (RIKEN Brain Science Institute
    ShanghaiTech University)

  • Suresh K. Joseph

    (Thomas Jefferson University)

  • David I. Yule

    (University of Rochester)

  • György Csordás

    (Thomas Jefferson University)

  • György Hajnóczky

    (Thomas Jefferson University)

Abstract

Contact sites of endoplasmic reticulum (ER) and mitochondria locally convey calcium signals between the IP3 receptors (IP3R) and the mitochondrial calcium uniporter, and are central to cell survival. It remains unclear whether IP3Rs also have a structural role in contact formation and whether the different IP3R isoforms have redundant functions. Using an IP3R-deficient cell model rescued with each of the three IP3R isoforms and an array of super-resolution and ultrastructural approaches we demonstrate that IP3Rs are required for maintaining ER-mitochondrial contacts. This role is independent of calcium fluxes. We also show that, while each isoform can support contacts, type 2 IP3R is the most effective in delivering calcium to the mitochondria. Thus, these studies reveal a non-canonical, structural role for the IP3Rs and direct attention towards the type 2 IP3R that was previously neglected in the context of ER-mitochondrial calcium signaling.

Suggested Citation

  • Adam Bartok & David Weaver & Tünde Golenár & Zuzana Nichtova & Máté Katona & Száva Bánsághi & Kamil J. Alzayady & V. Kaye Thomas & Hideaki Ando & Katsuhiko Mikoshiba & Suresh K. Joseph & David I. Yule, 2019. "IP3 receptor isoforms differently regulate ER-mitochondrial contacts and local calcium transfer," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-11646-3
    DOI: 10.1038/s41467-019-11646-3
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    Cited by:

    1. Jia-Rui Zhang & Shi-Yu Shen & Meng-Ying Zhai & Zu-Qi Shen & Wei Li & Ling-Feng Liang & Shu-Yuan Yin & Qiu-Qin Han & Bing Li & Yu-Qiu Zhang & Jin Yu, 2024. "Augmented microglial endoplasmic reticulum-mitochondria contacts mediate depression-like behavior in mice induced by chronic social defeat stress," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. 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.
    3. Iqbal Dulloo & Peace Atakpa-Adaji & Yi-Chun Yeh & Clémence Levet & Sonia Muliyil & Fangfang Lu & Colin W. Taylor & Matthew Freeman, 2022. "iRhom pseudoproteases regulate ER stress-induced cell death through IP3 receptors and BCL-2," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Eunbyul Cho & Youngsik Woo & Yeongjun Suh & Bo Kyoung Suh & Soo Jeong Kim & Truong Thi My Nhung & Jin Yeong Yoo & Tran Diem Nghi & Su Been Lee & Dong Jin Mun & Sang Ki Park, 2023. "Ratiometric measurement of MAM Ca2+ dynamics using a modified CalfluxVTN," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Mailis Liiv & Annika Vaarmann & Dzhamilja Safiulina & Vinay Choubey & Ruby Gupta & Malle Kuum & Lucia Janickova & Zuzana Hodurova & Michal Cagalinec & Akbar Zeb & Miriam A. Hickey & Yi-Long Huang & Na, 2024. "ER calcium depletion as a key driver for impaired ER-to-mitochondria calcium transfer and mitochondrial dysfunction in Wolfram syndrome," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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