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Dynamic organization of intracellular organelle networks

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Abstract Intracellular organelles are membrane‐bound and biochemically distinct compartments constructed to serve specialized functions in eukaryotic cells. Through extensive interactions, they form networks to coordinate and integrate their specialized functions for cell physiology. A fundamental property of these organelle networks is that they constantly undergo dynamic organization via membrane fusion and fission to remodel their internal connections and to mediate direct material exchange between compartments. The dynamic organization not only enables them to serve critical physiological functions adaptively but also differentiates them from many other biological networks such as gene regulatory networks and cell signaling networks. This review examines this fundamental property of the organelle networks from a systems point of view. The focus is exclusively on homotypic networks formed by mitochondria, lysosomes, endosomes, and the endoplasmic reticulum, respectively. First, key mechanisms that drive the dynamic organization of these networks are summarized. Then, several distinct organizational properties of these networks are highlighted. Next, spatial properties of the dynamic organization of these networks are emphasized, and their functional implications are examined. Finally, some representative molecular machineries that mediate the dynamic organization of these networks are surveyed. Overall, the dynamic organization of intracellular organelle networks is emerging as a fundamental and unifying paradigm in the internal organization of eukaryotic cells. This article is categorized under: Models of Systems Properties and Processes > Cellular Models Analytical and Computational Methods > Computational Methods Laboratory Methods and Technologies > Macromolecular Interactions, Methods Metabolic Diseases > Molecular and Cellular Physiology
Characterizing spatial distribution of lysosomes. (a) Lysosomes spread throughout the intracellular space of a cultured BS‐C‐1 cell. (b) To check whether lysosomes within the cell in (a) were randomly distributed, complete spatial randomness (CSR) test (Illian, Penttinen, Stoyan, & Stoyan, 2008) was performed. Black solid line: adjusted Ripley's K‐function of the actual distribution of lysosomes at the whole‐cell scale. Red dotted line: adjusted Ripley's K‐function of a random distribution simulated within the same cell geometry. Gray zone: uncertainty envelope of the adjusted Ripley's K‐function of the random distribution. The wide separation between the black solid line and the gray zone confirmed that lysosomes in (a) were not randomly distributed. (c)–(e) Cartoon illustrations of inter‐organelle distances, to‐nucleus distances, and nearest‐neighbor distances, respectively. Labels LYS01 to LYS04 are used to indicate different individual lysosomes. (f)–(h) The three distance distributions, respectively, of lysosomes in a single cell plotted at an interval of 5 seconds for 60 seconds. Color‐coding indicates time. pdf, probability density function (Reprinted with permission from Ba et al. (2018). Copyright 2018 Cell Press)
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Two representative intracellular organelle networks. (a) Left panel: the mitochondrial network of a cultured COS‐7 cell, labeled by mitotracker deep red. Right panel: magnified view of the rectangular region. (b) Left panel: The ER network of another cultured COS‐7 cell, labeled by expressed fusion protein GFP‐sec61γ. Right panel: magnified view of the rectangular region. Both images were collected using a Nikon CSU‐W1 spinning disk confocal microscope under 100× and 1.45 NA. Scale bars: 20 μm
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Three key mechanisms of organelle interactions. (a) Vesicle trafficking. Budding, translocation, and fusion of vesicles mediate indirect material exchange between the donor organelle and the acceptor organelle. (b) Membrane fusion and fission. The fusion and fission of membranes mediate direct material exchange between participating organelles. (c) Membrane contact. Contact between membranes also mediates direct material exchange between participating organelles, but without membrane fusion. Formation of membrane contact is enabled by various tether factors, as illustrated in the magnified view
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Dynamic clustering of lysosomes throughout the intracellular space. (a) Spatial distribution of lysosomes in a COS‐7 cell captured at selected time points of a time‐lapse video. (b) Spatial density maps of lysosomes in corresponding frames, respectively, in (a). Color‐coding indicates the average number of lysosomes per square micrometers. (c) Clusters formed by lysosomes are dynamic and may assemble and disassemble as well as merge and split. Arrowheads point to sites where clusters split. Arrows point to sites where clusters merge. (a–b) Scale bars: 20 μm (Reprinted with permission from Ba et al. (2018). Copyright 2018 Cell Press)
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Laboratory Methods and Technologies > Macromolecular Interactions, Methods
Analytical and Computational Methods > Computational Methods
Models of Systems Properties and Processes > Cellular Models

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