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Biosci Rep
2018 Jun 29;383:. doi: 10.1042/BSR20180208.
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Retraction of rod-like mitochondria during microtubule-dependent transport.
De Rossi MC
,
Levi V
,
Bruno L
.
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Molecular motors play relevant roles on the regulation of mitochondria size and shape, essential properties for the cell homeostasis. In this work, we tracked single rod-shaped mitochondria with nanometer precision to explore the performance of microtubule motor teams during processive anterograde and retrograde transport. We analyzed simultaneously the organelle size and verified that mitochondria retracted during retrograde transport with their leading tip moving slower in comparison with the rear tip. In contrast, mitochondria preserved their size during anterograde runs indicating a different performance of plus-end directed teams. These results were interpreted considering the different performance of dynein and kinesin teams and provide valuable information on the collective action of motors during mitochondria transport.
Figure 1. Tracking mitochondria in cells(A) Representative confocal image of X. laevis melanocyte expressing EGFP-XTP (green) incubated with MitoTracker Deep Red (red) reveals the variability in mitochondrial morphology (bottom panel). Scale bars: 10 and 3 μm, respectively. (B–E) Representative images obtained during a time-lapse movie of rod-like mitochondria. The frames were analyzed as described in the text to determine the organelle centroid position and main axis length. Inset: binary image of the organelle showing the centroid position (colored circle) and organelle length (yellow line). Scale bar: 3 μm. (E) The mitochondria centroid position (red circles) followed the mean position of the microtubule recovered in the movie (green).
Figure 2. Mitochondial length variation during transport(A) Representative example of a mitochondrion main axis length (L, red) and its trajectory along the microtubule (black). (B) Quantitation of mitochondria length variation during directed motion. L values registered at the beginning (Lo) and at the end (Lf) of retrograde (n=52) and anterograde (n=62) runs were determined whether the mitochondria experienced a retraction, extension, or no variation in their length. The figure includes data of 75 mitochondria (ncells=35).
Figure 3. Properties of mitochondria retraction during retrograde transport(A) Distribution of the relative mitochondria length variation during retrograde runs (nruns=42). The data were fitted with an exponential-decay function (line) obtaining a characteristic retraction length of 13 ± 1%. The figure includes data of 31 mitochondria (ncells=21). (B,C) Representative trajectories of the mitochondria leading and rear edges obtained during retrograde (B) and anterograde (C) runs.
Figure 4. Graphical summary depicting the influence of microtubule motors teams on rod-like mitochondria size during processive transportThe opposed-polarity motors kinesin (blue) and dynein (violet) stochastically attach and detach from the microtubule and pull the cargo against the drag force imposed by the cytoplasm. The schemes shows arbitrary configurations and number of motors attached to mitochondria. To simplify the scheme, we did not include opposed-polarity motors that are also attached to the organelle and/or competing with the motors responsible for the transport during unidirectional runs. (A) During retrograde transport, the leading dyneins work against a higher load and thus move slower than those attached at the rear-end; as a consequence, the mitochondrion retracts. (B) During anterograde transport, kinesins asynchronous step along the track switching from an active state to inactive (and vice versa). Due to the convex-up F-V curve of kinesins, leading and trailing motors present similar speeds and thus the mitochondrion does not change its size.
Figure S1. (A) Representative distribution of L values obtained for retrograde and
anterograde rod-like mitochondrias. (B) The organelles trajectories (N=75) were
analized as described in the text to recover segments of directed motion (runs). The run
length median values and the mean speed experienced by the mitochondria along these
runs were computed. The data is expressed with the standard error.
Anesti,
The relationship between mitochondrial shape and function and the cytoskeleton.
2006, Pubmed
Anesti,
The relationship between mitochondrial shape and function and the cytoskeleton.
2006,
Pubmed
Belyy,
The mammalian dynein-dynactin complex is a strong opponent to kinesin in a tug-of-war competition.
2016,
Pubmed
Benard,
Mitochondrial fusion and division: Regulation and role in cell viability.
2009,
Pubmed
Bieling,
Processive kinesins require loose mechanical coupling for efficient collective motility.
2008,
Pubmed
Blasius,
Two binding partners cooperate to activate the molecular motor Kinesin-1.
2007,
Pubmed
Blehm,
Single-molecule fluorescence and in vivo optical traps: how multiple dyneins and kinesins interact.
2014,
Pubmed
Bruno,
Mechanical properties of organelles driven by microtubule-dependent molecular motors in living cells.
2011,
Pubmed
,
Xenbase
Chan,
Mitochondria: dynamic organelles in disease, aging, and development.
2006,
Pubmed
De Rossi,
When size does matter: organelle size influences the properties of transport mediated by molecular motors.
2013,
Pubmed
,
Xenbase
De Rossi,
Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells.
2017,
Pubmed
Driver,
Productive cooperation among processive motors depends inversely on their mechanochemical efficiency.
2011,
Pubmed
Frederick,
Moving mitochondria: establishing distribution of an essential organelle.
2007,
Pubmed
Fu,
Integrated regulation of motor-driven organelle transport by scaffolding proteins.
2014,
Pubmed
Goychuk,
How molecular motors work in the crowded environment of living cells: coexistence and efficiency of normal and anomalous transport.
2014,
Pubmed
Gross,
Interactions and regulation of molecular motors in Xenopus melanophores.
2002,
Pubmed
,
Xenbase
Hancock,
Bidirectional cargo transport: moving beyond tug of war.
2014,
Pubmed
Hoppins,
The regulation of mitochondrial dynamics.
2014,
Pubmed
Iworima,
Kif5 regulates mitochondrial movement, morphology, function and neuronal survival.
2016,
Pubmed
Jamison,
Two kinesins transport cargo primarily via the action of one motor: implications for intracellular transport.
2010,
Pubmed
Leidel,
Measuring molecular motor forces in vivo: implications for tug-of-war models of bidirectional transport.
2012,
Pubmed
Levi,
Organelle transport along microtubules in Xenopus melanophores: evidence for cooperation between multiple motors.
2006,
Pubmed
,
Xenbase
Liu,
Mitochondrial 'kiss-and-run': interplay between mitochondrial motility and fusion-fission dynamics.
2009,
Pubmed
Mallik,
Cytoplasmic dynein functions as a gear in response to load.
2004,
Pubmed
McCarron,
From structure to function: mitochondrial morphology, motion and shaping in vascular smooth muscle.
2013,
Pubmed
McLaughlin,
Collective dynamics of processive cytoskeletal motors.
2016,
Pubmed
Müller,
Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors.
2008,
Pubmed
Nangaku,
KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria.
1994,
Pubmed
Nelson,
Motor coupling through lipid membranes enhances transport velocities for ensembles of myosin Va.
2014,
Pubmed
Nunnari,
Mitochondria: in sickness and in health.
2012,
Pubmed
Olesen,
Molecular cloning of XTP, a tau-like microtubule-associated protein from Xenopus laevis tadpoles.
2002,
Pubmed
,
Xenbase
Pallavicini,
Lateral motion and bending of microtubules studied with a new single-filament tracking routine in living cells.
2014,
Pubmed
,
Xenbase
Rai,
Dynein Clusters into Lipid Microdomains on Phagosomes to Drive Rapid Transport toward Lysosomes.
2016,
Pubmed
Rai,
Molecular adaptations allow dynein to generate large collective forces inside cells.
2013,
Pubmed
Roger,
The Origin and Diversification of Mitochondria.
2017,
Pubmed
Rogers,
Regulated bidirectional motility of melanophore pigment granules along microtubules in vitro.
1997,
Pubmed
,
Xenbase
Schnitzer,
Force production by single kinesin motors.
2000,
Pubmed
Soppina,
Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes.
2009,
Pubmed
Takshak,
Importance of anisotropy in detachment rates for force production and cargo transport by a team of motor proteins.
2016,
Pubmed
Tanaka,
Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria.
1998,
Pubmed
Varadi,
Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1.
2004,
Pubmed
Welte,
Bidirectional transport along microtubules.
2004,
Pubmed
Woods,
Microtubules Are Essential for Mitochondrial Dynamics-Fission, Fusion, and Motility-in Dictyostelium discoideum.
2016,
Pubmed
Youle,
Mitochondrial fission, fusion, and stress.
2012,
Pubmed
