Mitochondrial Populations Exhibit Differential Dynamic Responses to Increased Energy Demand during Exocytosis In Vivo

Author:

Porat-Shliom, Natalie

Harding, Olivia J

Malec, Lenka

Narayan, Kedar

Weigert, Roberto
Author Address

Laboratory of Cellular and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA; National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892, USA; Cell Biology and Imaging Section, Thoracic and Gastrointestinal Oncology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: poratshliomn@mail.nih.gov., National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892, USA., Laboratory of Cellular and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA., Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, 8560 Progress Drive, Frederick, MD 21701, USA; Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD, USA., Laboratory of Cellular and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA; National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: weigertr@mail.nih.gov.,

Abstract:

Mitochondria are dynamic organelles undergoing fission, fusion, and translocation. These processes have been studied in cultured cells; however, little is known about their regulation in cells within tissues in vivo. We applied four-dimensional intravital microscopy to address this in secretory cells of the salivary gland. We found that mitochondria are organized in two populations: one juxtaposed to the basolateral plasma membrane and the other dispersed in the cytosol. Under basal conditions, central mitochondria exhibit microtubule-dependent motility and low fusion rate, whereas basolateral mitochondria are static and display high fusion rate. Increasing cellular energy demand by ß-adrenergic stimulation of regulated exocytosis selectively enhanced motility and fusion of central mitochondria. Inhibition of microtubule polymerization led to inhibition of central mitochondrial motility and fusion and a marked reduction in exocytosis. This study reveals a conserved heterogeneity in mitochondrial positioning and dynamics in exocrine tissues that may have fundamental implications in organ pathophysiology. Published by Elsevier Inc.

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