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Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery

Author

Listed:
  • Souvik Modi

    (University College London
    Tata Institute of Fundamental Research)

  • Guillermo López-Doménech

    (University College London)

  • Elise F. Halff

    (University College London
    Psychology and Neuroscience, King’s College London)

  • Christian Covill-Cooke

    (University College London)

  • Davor Ivankovic

    (University College London)

  • Daniela Melandri

    (University College London)

  • I. Lorena Arancibia-Cárcamo

    (University College London)

  • Jemima J. Burden

    (University College London)

  • Alan R. Lowe

    (University College London
    Birkbeck College London
    London Centre for Nanotechnology)

  • Josef T. Kittler

    (University College London)

Abstract

Mitochondrial Rho (Miro) GTPases localize to the outer mitochondrial membrane and are essential machinery for the regulated trafficking of mitochondria to defined subcellular locations. However, their sub-mitochondrial localization and relationship with other critical mitochondrial complexes remains poorly understood. Here, using super-resolution fluorescence microscopy, we report that Miro proteins form nanometer-sized clusters along the mitochondrial outer membrane in association with the Mitochondrial Contact Site and Cristae Organizing System (MICOS). Using knockout mouse embryonic fibroblasts we show that Miro1 and Miro2 are required for normal mitochondrial cristae architecture and Endoplasmic Reticulum-Mitochondria Contacts Sites (ERMCS). Further, we show that Miro couples MICOS to TRAK motor protein adaptors to ensure the concerted transport of the two mitochondrial membranes and the correct distribution of cristae on the mitochondrial membrane. The Miro nanoscale organization, association with MICOS complex and regulation of ERMCS reveal new levels of control of the Miro GTPases on mitochondrial functionality.

Suggested Citation

  • Souvik Modi & Guillermo López-Doménech & Elise F. Halff & Christian Covill-Cooke & Davor Ivankovic & Daniela Melandri & I. Lorena Arancibia-Cárcamo & Jemima J. Burden & Alan R. Lowe & Josef T. Kittler, 2019. "Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12382-4
    DOI: 10.1038/s41467-019-12382-4
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    Cited by:

    1. Peng Liao & Long Chen & Hao Zhou & Jiong Mei & Ziming Chen & Bingqi Wang & Jerry Q. Feng & Guangyi Li & Sihan Tong & Jian Zhou & Siyuan Zhu & Yu Qian & Yao Zong & Weiguo Zou & Hao Li & Wenkan Zhang & , 2024. "Osteocyte mitochondria regulate angiogenesis of transcortical vessels," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. 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.
    3. Peng Shi & Xiaoyu Ren & Jie Meng & Chenlu Kang & Yihe Wu & Yingxue Rong & Shujuan Zhao & Zhaodi Jiang & Ling Liang & Wanzhong He & Yuxin Yin & Xiangdong Li & Yong Liu & Xiaoshuai Huang & Yujie Sun & B, 2022. "Mechanical instability generated by Myosin 19 contributes to mitochondria cristae architecture and OXPHOS," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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