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All-optical spatiotemporal mapping of ROS dynamics across mitochondrial microdomains in situ

Author

Listed:
  • Shon A. Koren

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Nada Ahmed Selim

    (University of Rochester Medical Center, Department of Pharmacology and Physiology)

  • Lizbeth Rosa

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Jacob Horn

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • M. Arsalan Farooqi

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Alicia Y. Wei

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Annika Müller-Eigner

    (Research Institute for Farm Animal Biology (FBN))

  • Jacen Emerson

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Gail V. W. Johnson

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

  • Andrew P. Wojtovich

    (University of Rochester Medical Center, Department of Anesthesiology and Perioperative Medicine)

Abstract

Hydrogen peroxide (H2O2) functions as a second messenger to signal metabolic distress through highly compartmentalized production in mitochondria. The dynamics of reactive oxygen species (ROS) generation and diffusion between mitochondrial compartments and into the cytosol govern oxidative stress responses and pathology, though these processes remain poorly understood. Here, we couple the H2O2 biosensor, HyPer7, with optogenetic stimulation of the ROS-generating protein KillerRed targeted into multiple mitochondrial microdomains. Single mitochondrial photogeneration of H2O2 demonstrates the spatiotemporal dynamics of ROS diffusion and transient hyperfusion of mitochondria due to ROS. This transient hyperfusion phenotype required mitochondrial fusion but not fission machinery. Measurement of microdomain-specific H2O2 diffusion kinetics reveals directionally selective diffusion through mitochondrial microdomains. All-optical generation and detection of physiologically-relevant concentrations of H2O2 between mitochondrial compartments provide a map of mitochondrial H2O2 diffusion dynamics in situ as a framework to understand the role of ROS in health and disease.

Suggested Citation

  • Shon A. Koren & Nada Ahmed Selim & Lizbeth Rosa & Jacob Horn & M. Arsalan Farooqi & Alicia Y. Wei & Annika Müller-Eigner & Jacen Emerson & Gail V. W. Johnson & Andrew P. Wojtovich, 2023. "All-optical spatiotemporal mapping of ROS dynamics across mitochondrial microdomains in situ," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41682-z
    DOI: 10.1038/s41467-023-41682-z
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    References listed on IDEAS

    as
    1. John O. Onukwufor & M. Arsalan Farooqi & Anežka Vodičková & Shon A. Koren & Aksana Baldzizhar & Brandon J. Berry & Gisela Beutner & George A. Porter & Vsevolod Belousov & Alan Grossfield & Andrew P. W, 2022. "A reversible mitochondrial complex I thiol switch mediates hypoxic avoidance behavior in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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    Cited by:

    1. Daan M. K. Soest & Paulien E. Polderman & Wytze T. F. Toom & Janneke P. Keijer & Markus J. Roosmalen & Tim M. F. Leyten & Johannes Lehmann & Susan Zwakenberg & Sasha Henau & Ruben Boxtel & Boudewijn M, 2024. "Mitochondrial H2O2 release does not directly cause damage to chromosomal DNA," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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