Small-scale displacement fluctuations of vesicles in fibroblasts

Posey, Danielle; Blaisdell-Pijuan, Paris; Knoll, Samantha; Saif, M. Taher A.; Ahmed, Wylie

doi:10.1038/s41598-018-31656-3

Cited by 11 publications

(14 citation statements)

References 55 publications

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“…P (Δ X ) was well described by a Gaussian function as well as those measured for other intracellular cargos (Hasegawa et al, 2019; Hayashi, Hasegawa, et al, 2018; Hayashi, Tsuchizawa, et al, 2018). Note that the abnormal diffusion property (i.e., P (Δ X ) is not a Gaussian function) often reported for intercellular cargo transport(Fakhri et al, 2014; Posey, Blaisdell-Pijuan, Knoll, Saif, & Ahmed, 2018; Shin et al, 2019; Tabei et al, 2013) appeared upon analysis of the whole trajectory without dividing it into CVSs(Hayashi et al, 2013). One reason for the abnormality might be that the trajectory includes multiple velocity values.…”

Section: Resultsmentioning

confidence: 99%

Effects of the dynein inhibitor dynarrestin on the number of motor proteins transporting synaptic cargos

Hayashi

Miyamoto

Niwa

2020

Preprint

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Synaptic cargo transport by the motor proteins kinesin and dynein in the axons of hippocampal neurons was investigated using non-invasive measurement of transport force based on nonequilibrium statistical mechanics and extreme-value statistics on the maximum transport velocity. Although direct physical measurements such as force measurement using optical tweezers are difficult in a non-equilibrium intracellular environment, the proposed noninvasive estimations enabled enumerating force producing units (FPUs) carrying a cargo comprising the motor proteins generating force. The number of FPUs served as a barometer for the stable and long-distance transport by multiple motors, which was then used to quantify the extent of damage to axonal transport resulting from ciliobrevin, a dynein inhibitor. Our results show interrelationships among force, velocity, and the number of FPUs, precisely describing transport dysregulation. Such measures may help quantify the damage to axonal transport resulting from neuronal diseases including Alzheimer's, Parkinson's, and Huntington's diseases in future. KAKENHI (grant No. 17H03659) to K. H., as well as JSPS KAKENHI (grant Nos. 17H05010 and 19H04738) to S. N.

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Section: Resultsmentioning

confidence: 99%

Effects of the dynein inhibitor dynarrestin on the number of motor proteins transporting synaptic cargos

Hayashi

Miyamoto

Niwa

2020

Preprint

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“…However, the typical speed of motor-guided vesicles in these cultures and in other systems is much faster (~0.4-0.5µm/sec) [58][59][60] compared to our measurements (~0.06-0.08µm/sec). Additionally, the motor-guided movement of vesicles along microtubules was shown to be in bursts of directed motion that last ~6-7 seconds followed by a pause for a similar time interval [36,60]. If that was the case for the calcium vesicles, we would have expected to see two peaks of instantaneous speed, a fast-speed peak corresponding to the directed motion and a slow-speed peak corresponding to the pause.…”

Section: Vesicle Speed Is Slower In the Skeletogenic Cells Compared Tmentioning

confidence: 99%

“…In other systems, vesicles were shown to experience a diffusive motion that is not thermal in nature but results from the dynamic remodeling of the cytoskeletal network and the ubiquitous activity of motor proteins that affect every moving object within the cell cytoplasm [36][37][38][39][40]. This mode of diffusion is called "active diffusion" and is characterized by a larger amplitude (step size) compared to the amplitude of thermally-induced diffusion.…”

Section: The Calcium Vesicles Perform a Diffusion Motion In The Skelementioning

confidence: 99%

“…Alternatively, the vesicles can perform a diffusive motion that is constrained by the cellular organelles and affected by the dynamic remodeling of the cytoskeleton network within the cell [35][36][37][38][39][40]. This mode of vesicle diffusion within the cells is called "active diffusion" to distinguish it from thermal diffusion [35][36][37][38][39][40]. Deciphering the mode of motion of the calcium vesicles within the skeletogenic cells and specifically, distinguishing between motor guided motion and diffusion, is essential for understanding the cellular regulation of mineral transport into the biomineralization compartment.…”

Section: Introductionmentioning

confidence: 99%

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Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization

Winter

Morgulis

Gildor

et al. 2020

Preprint

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Biomineralization is the process by which organisms use minerals to harden their tissues and provide them with physical support. Biomineralizing cells concentrate the mineral in vesicles that they secret into a dedicated compartment where crystallization occurs. The dynamics of mineral-vesicle motion and the molecular mechanisms that regulate it, are not well understood. Sea urchin larval skeletogenesis provides an excellent platform for the analyses of vesicle kinetics. Here we used calcein labeling and lattice light-sheet microscopy to investigate the three-dimensional (3D) vesicle dynamics in control sea urchin embryos and in Vascular Endothelial Growth Factor Receptor (VEGFR) inhibited embryos, where skeletogenesis is blocked. We developed computational tools for displaying 3D-volumetric movies and for automatically quantifying vesicle dynamics in the different embryonic tissues. Our findings imply that calcium vesicles perform an active diffusion motion in all the cells of the embryo. This mode of diffusion is defined by the mechanical properties of the cells and the dynamic rearrangements of the cytoskeletal network. The diffusion coefficient is larger in the mesenchymal skeletogenic cells compared to the epithelial ectodermal cells, possibly due to the distinct mechanical properties of the two tissues. Vesicle motion is not directed toward the biomineralization compartment, but the vesicles slow down when they approach it, and probably bind for mineral deposition. Under VEGFR inhibition, vesicle volume increases and vesicle speed is reduced but the vesicles continue in their diffusive motion. Overall, our studies provide an unprecedented view of calcium vesicle 3D-dynamics and illuminate possible molecular mechanisms that control vesicle dynamics and deposition.

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“…Single particle tracking in living cells can be a powerful approach to distinguish different types of particle motion. However, individual particles can undergo multiple types of motion during a single observation lasting 1-10 s. Several methods have been developed to detect different types of motion within particle tracks (e.g., 4,[13][14][15] ).…”

mentioning

confidence: 99%

Vesicular stomatitis virus nucleocapsids diffuse through cytoplasm by hopping from trap to trap in random directions

Holzwarth

Bhandari

Tommervik

et al. 2020

Sci Rep

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Within 2-6 hours after infection by vesicular stomatitis virus (VSV), newly assembled VSV particles are released from the surface of infected cells. In that time, viral ribonucleoprotein (RNP) particles (nucleocapsids) travel from their initial sites of synthesis near the nucleus to the edge of the cell, a distance of 5-10 μm. The hydrodynamic radius of RNP particles (86 nm) precludes simple diffusion through the mesh of cytoskeletal fibers. To reveal the relative importance of different transport mechanisms, movement of GFP-labeled RNP particles in live A549 cells was recorded within 3 to 4 h postinfection at 100 frames/s by fluorescence video microscopy. Analysis of more than 200 RNP particle tracks by Bayesian pattern recognition software found that 3% of particles showed rapid, directional motion at about 1 μm/s, as previously reported. 97% of the RNP particles jiggled within a small, approximately circular area with Gaussian width σ = 0.06 μm. Motion within such "traps" was not directional. Particles stayed in traps for approximately 1 s, then hopped to adjacent traps whose centers were displaced by approximately 0.17 μm. Because hopping occurred much more frequently than directional motion, overall transport of RNP particles was dominated by hopping over the time interval of these experiments. Movement of cellular components is critical for their functions. However, this movement faces a number of barriers, including the dense network of the cytoskeleton 1. For particles too large to diffuse in the cytoplasm (hydrodynamic radius> approximately 50 nm) 2 , movements consist of a mixture of seemingly random motions and directional motion driven by molecular motors on microtubules and actin filaments 3. Viruses face the same hurdles during their intracellular replication cycles and use the same cellular mechanisms to distribute viral components throughout the cell. The purpose of the experiments presented here was to determine the transport modes of the ribonucleoprotein (RNP) core (nucleocapsid) of vesicular stomatitis virus (VSV) across the cytoplasm using a variational Bayesian approach to analyze single particle tracks in living cells 4. Vesiculovirus Indiana, commonly referred to as VSV (Indiana serotype), is one of the prototypes for the large group of viruses with nonsegmented negative strand RNA genomes (order Mononegavirales). These viruses include many human pathogens, such as measles, Ebola, and rabies viruses, as well as many other viruses that infect both animals and plants. These viruses encode an RNA-dependent RNA polymerase that is responsible for transcription of viral mRNAs and replication of genome RNA, and for most of these viruses, the replication cycle occurs entirely in the cytoplasm 5. The VSV RNP core consists of the 11 kb RNA genome encapsidated by approximately 1200 copies of the viral N protein. The RNP also contains approximately 400 copies of the viral P protein and 50 copies of the L protein, which together are responsible for the RNA polymerase activity 6. The resultant mass of t...

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Small-scale displacement fluctuations of vesicles in fibroblasts

Cited by 11 publications

References 55 publications

Effects of the dynein inhibitor dynarrestin on the number of motor proteins transporting synaptic cargos

Effects of the dynein inhibitor dynarrestin on the number of motor proteins transporting synaptic cargos

Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization

Vesicular stomatitis virus nucleocapsids diffuse through cytoplasm by hopping from trap to trap in random directions

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