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

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 and Andrew P. Wojtovich ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41682-z

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