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      A pH-driven transition of the cytoplasm from a fluid- to a solid-like state promotes entry into dormancy

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          Abstract

          Cells can enter into a dormant state when faced with unfavorable conditions. However, how cells enter into and recover from this state is still poorly understood. Here, we study dormancy in different eukaryotic organisms and find it to be associated with a significant decrease in the mobility of organelles and foreign tracer particles. We show that this reduced mobility is caused by an influx of protons and a marked acidification of the cytoplasm, which leads to widespread macromolecular assembly of proteins and triggers a transition of the cytoplasm to a solid-like state with increased mechanical stability. We further demonstrate that this transition is required for cellular survival under conditions of starvation. Our findings have broad implications for understanding alternative physiological states, such as quiescence and dormancy, and create a new view of the cytoplasm as an adaptable fluid that can reversibly transition into a protective solid-like state.

          DOI: http://dx.doi.org/10.7554/eLife.09347.001

          eLife digest

          Most organisms live in unpredictable environments, which can often lead to nutrient shortages and other conditions that limit their ability to grow. To survive in these harsh conditions, many organisms adopt a dormant state in which their metabolism slows down to conserve vital energy. When the environmental conditions improve, the organisms can return to their normal state and continue to grow.

          The interior of cells is known as the cytoplasm. It is very crowded and contains many molecules and compartments called organelles that carry out a variety of vital processes. The cytoplasm has long been considered to be fluid-like in nature, but recent evidence suggests that in bacterial cells it can solidify to resemble a soft glass-type material under certain conditions. When cells become dormant they stop dividing and reorganise their cytoplasm in several ways; for example, the water content drops and many essential proteins form storage compartments. However, it was not clear how cells regulate the structure of the cytoplasm to enter into or exit from dormancy.

          Now, Munder et al. analyse the changes that occur in the cytoplasm when baker’s yeast cells enter a dormant state. The experiments show that when yeast cells are deprived of energy – as happens during dormancy – the cytoplasm becomes more acidic than normal. This limits the ability of molecules and organelles to move around the cytoplasm. Similar results were also seen in other types of fungi and an amoeba. Munder et al. found that this increase in acidity during dormancy causes many proteins to interact with each other and form large clumps or filament structures that result in the cytoplasm becoming stiffer.

          A separate study by Joyner et al. found that when yeast cells are starved of sugar, two large molecules are less able to move around the cell interior. Together, the findings of the studies suggest that the interior of cells can undergo a transition from a fluid-like to a more solid-like state to protect the cells from damage when energy is in short supply. The next challenge is to understand the molecular mechanisms that cause the physical properties of the cytoplasm to change under different conditions.

          DOI: http://dx.doi.org/10.7554/eLife.09347.002

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          Most cited references71

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          Kinesin superfamily motor proteins and intracellular transport.

          Intracellular transport is fundamental for cellular function, survival and morphogenesis. Kinesin superfamily proteins (also known as KIFs) are important molecular motors that directionally transport various cargos, including membranous organelles, protein complexes and mRNAs. The mechanisms by which different kinesins recognize and bind to specific cargos, as well as how kinesins unload cargo and determine the direction of transport, have now been identified. Furthermore, recent molecular genetic experiments have uncovered important and unexpected roles for kinesins in the regulation of such physiological processes as higher brain function, tumour suppression and developmental patterning. These findings open exciting new areas of kinesin research.
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            Feature point tracking and trajectory analysis for video imaging in cell biology.

            This paper presents a computationally efficient, two-dimensional, feature point tracking algorithm for the automated detection and quantitative analysis of particle trajectories as recorded by video imaging in cell biology. The tracking process requires no a priori mathematical modeling of the motion, it is self-initializing, it discriminates spurious detections, and it can handle temporary occlusion as well as particle appearance and disappearance from the image region. The efficiency of the algorithm is validated on synthetic video data where it is compared to existing methods and its accuracy and precision are assessed for a wide range of signal-to-noise ratios. The algorithm is well suited for video imaging in cell biology relying on low-intensity fluorescence microscopy. Its applicability is demonstrated in three case studies involving transport of low-density lipoproteins in endosomes, motion of fluorescently labeled Adenovirus-2 particles along microtubules, and tracking of quantum dots on the plasma membrane of live cells. The present automated tracking process enables the quantification of dispersive processes in cell biology using techniques such as moment scaling spectra.
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              Nonequilibrium mechanics of active cytoskeletal networks.

              Cells both actively generate and sensitively react to forces through their mechanical framework, the cytoskeleton, which is a nonequilibrium composite material including polymers and motor proteins. We measured the dynamics and mechanical properties of a simple three-component model system consisting of myosin II, actin filaments, and cross-linkers. In this system, stresses arising from motor activity controlled the cytoskeletal network mechanics, increasing stiffness by a factor of nearly 100 and qualitatively changing the viscoelastic response of the network in an adenosine triphosphate-dependent manner. We present a quantitative theoretical model connecting the large-scale properties of this active gel to molecular force generation.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                22 March 2016
                2016
                : 5
                : e09347
                Affiliations
                [1 ]Max Planck Institute of Molecular Cell Biology and Genetics , Dresden, Germany
                [2 ]Max Planck Institute for the Physics of Complex Systems , Dresden, Germany
                [3 ]deptBiotechnology Center , Technische Universität Dresden , Dresden, Germany
                [4]Albert Einstein College of Medicine , United States
                [5]Albert Einstein College of Medicine , United States
                Author notes
                Author information
                http://orcid.org/0000-0003-3594-4725
                http://orcid.org/0000-0002-1453-6119
                http://orcid.org/0000-0003-4017-6505
                Article
                09347
                10.7554/eLife.09347
                4850707
                27003292
                b1e9ceeb-8db6-4601-9f88-a438cf08319b
                © 2016, Munder et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 11 June 2015
                : 13 February 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004189, Max-Planck-Gesellschaft;
                Award ID: Core Funding
                Award Recipient :
                Funded by: Dresden International Graduate School for Biomedicine and Bioengineering;
                Award ID: Graduate Student Fellowship
                Award Recipient :
                Funded by: Dresden International Graduate School for Biomedicine and Bioengineering;
                Award ID: Sprinboard-to-Postdoc-Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100005156, Alexander von Humboldt-Stiftung;
                Award ID: Alexander von Humboldt Professorship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100005156, Alexander von Humboldt-Stiftung;
                Award ID: Postdoc Fellowship
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: Reserach Grant, AL 1061/5-1
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Biophysics and Structural Biology
                Cell Biology
                Custom metadata
                2.5
                The cytoplasm behaves as an adaptable fluid that can reversibly transition into a protective solid-like state upon stress.

                Life sciences
                phase transition,macromolecular assembly,cytosolic ph,starvation,dormancy,metabolism,dictyostelium,<i>s. cerevisiae</i>,<i>s. pombe</i>

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