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Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators

Ashwin I. D’Souza, Rahul Grover, Gina A. Monzon, Ludger Santen, Stefan Diez

Posted on: 25 January 2023

Preprint posted on 28 September 2022

Article now published in Nature Communications at http://dx.doi.org/10.1038/s41467-023-42605-8

To move or not to move: A novel in vitro assay successfully recreates intracellular bidirectional cargo transport, laying the foundations for further understanding

Selected by Divya Pathak

Background:

The cell is a very busy environment, wherein hundreds of molecules and vesicles are being transported at any given moment. Most intracellular cargoes show association with multiple types of motors raising the question– how is the directionality of cargo determined? In this preprint, D’Souza and colleagues try to answer this question.

Regulated intracellular transport is critical for proper cellular functioning, affecting processes like cell division, the positioning of organelles, and organelle transport. Intracellular transport can be long range using microtubules and short range using actin filaments. The microtubule-based motors Kinesin and Dynein carry cargo in opposite directions. What is surprising is that most intracellular cargo shows simultaneous association with multiple Kinesin and Dynein motors. Without a specific regulatory mechanism governing cargo transport, it is likely for the cargo to get stuck in limbo with both the motors engaged and undergoing futile ATPase cycles with no net movement. Alternatively, the cargo might randomly switch direction and end up in a place it’s not destined for. Intracellular cargoes like mitochondria, peroxisomes, endosomes, melanosomes and lipid droplets often move bidirectionally and regularly change direction en route to their final destinations.

Analyzing motor compositions on in vivo cargoes has been experimentally challenging not only due to difficulties in purifying a specific intracellular cargo type, but also the variation in motor-cargo associations over time. For most of the bidirectionally moving cargo, there are three models that can apply1. (1) Tug-of war, in which two oppositely directed motors simultaneously generate force and engage in a physical tug-of-war whose outcome decides the cargo’s direction2,3,4. In this model, changing the number of motors or their organization on cargo dictates the cargo’s net movement. (2) Exclusionary presence through motor association with and dissociation from the cargo. Adapter proteins on the cargo can interact with opposing motors and, depending on their interacting partner, the cargo either moves anterograde or retrograde5. This model prevents the futile use of ATP and ensures coordinated cargo movement without interference from the opposing motor. This model is also supported by the observation that motors exist in inactive states and that this autoinhibition is released upon cargo binding. (3) Activation by opposing motor, in which case the driving motor does not necessarily interfere, but rather activate the opposing motor by sheer stretching/force. It has been shown that inactivating one motor results in reduced motion by the opposing motor as well; disruption of either kinesin or dynein inhibits opposite-polarity vesicle transport6,7.

Until now, most of our insights into bidirectional transport have come from motors recruited to non-vesicular assemblies like DNA scaffolds, quantum dots, coverslips and beads4,8,13,14. These don’t recapitulate native cargo mostly due to the missing complexity of the lipid bilayer of the vesicular cargo9,10,11. Also, most of the reconstituted experiments couldn’t recapitulate the fast transport and directional reversals, and instead showed slowing down of motion and long stationary pauses. This suggested and provided increasing evidence for the exclusionary model in which dynein and kinesin are not active simultaneously on the same cargo. As most cargoes showed association with opposing motors, a model emerged in which external regulators or adaptors coordinate the activity of opposing motors to prevent their simultaneous activation.

Fig 1: Successful reconstitution of bidirectional motility on liposomes a) Schematic diagram of vesicle motility assay reconstituted on Large Unilamellar vesicles (LUVs). KIF16B with its PX domain was targeted to Phosphatidyl Inositol-3-Phosphate on liposomes and Dynein (DDB) complex was His-tagged and targeted to DGS-NTA(Ni) lipid on liposomes. Kymographs characterizing motion of DDB-vesicles (b), KIF16B-vesicles (c), and DDB-KIF16B-vesicles (d). DDB-KIF16B-vesicles show processive unidirectional runs with directional reversals in vitro. (Figure 2 from preprint, provided under CC BY 4.0 International License)

 

 

Fig 2: Increasing KIF16B biases the transport towards plus-end as predicted by the tug-of-war model. Histogram showing minus-end directed (blue), reversals (magenta) and plus-end directed (green) track frequency for DDB-KIF16B-vesicles incubated with 38 nM DDB and increasing concentrations of KIF16B (10, 25, 50, and 75 nM). (Figure 3 from preprint, provided under CC BY 4.0 International License)

 

Key findings:

  1. In this study D’souza et al for the very first time successfully reconstituted bidirectional transport in vitro on liposomes that resemble the majority of the intracellular cargo (Fig. 1). They targeted purified motors – Dynein-Dynactin-BicD2 (DDB) complex and kinesin (KIF 16B) – to 132nm liposomes and could recapitulate the in vivo transport of cargoes including the fast unidirectional runs, intermittent pauses and directional reversals in the absence of any external regulatory protein.
  2. Cargo (liposome) pausing was enhanced when opposing motors were present. Not all pauses were the result of a tug-of-war as vesicles with only one kind of motor – either kinesin or dynein – exhibited processive runs with frequent pauses. The researchers titrated increasing amounts of kinesin (KIF16B) for the same amount of dynein (DDB) and could shift the balance in favor of kinesin-driven runs (Fig. 2). Also, in the pause phase, they observed elongation of cargo along the microtubule as seen for purified endosomes from Dictyostelium. These observations support the tug-of-war model.
  3. The successful reconstitution of bidirectional transport reported in this preprint also suggests that the presence of opposing motors doesn’t hinder the velocity of active driving motors nor slow down transport, reflected by the smooth unidirectional runs seen on DDB-KIF16B liposomes. Instead, presence of opposing motors results in longer pauses marked by the motors engaging in a tug-of war, followed by stochastic fluctuations that can lead to directional reversals without the need of external regulators.
  4. The researchers simulated different motor configurations to explain the bidirectional cargo transport observed experimentally. Their simulation predicts that 3 active motors drive a processive run and that the cargo pauses when 2 of those active motors detach along with the simultaneous attachment of one opposing motor. Pauses were characterized by a force balance between two active motors of opposing polarity and 4 inactive opposing motors (2 of each kind) to stabilize it. Transitioning from a pause to an active run in either direction is initiated by the stochastic detachment of the active motor of the opposing polarity or the attachment of two active motors. For cargo being driven by a low number of engaged motors, their simulation predicts that stochastic attachment or detachment of single motors determines the direction of cargo.

 

Why I chose this preprint?

Richard Feynman once said “What I cannot create, I do not understand”. Developing, or rather creating, this assay to recapitulate bidirectional motility marks the first attempt at improving our understanding of intracellular transport. This assay provides a foundation to build complexity in the form of adapter proteins, bilayer lipid composition etc. to dissect their role in intracellular transport. This is the first time that bidirectional motility has been reconstituted on liposomes which recapitulates the endogenous intracellular cargo. This assay marks the beginning of our ability to understand in vivo transport by trying to create it in vitro.

 

References:

  1. Hancock, W. Bidirectional cargo transport: moving beyond tug of war. Nat Rev Mol Cell Biol (2014); 15, 615–628
  2. Soppina V, Rai AK, Ramaiya AJ, Barak P, Mallik R. Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. PNAS (2009); 106(46):19381-6
  3. Rezaul, K., Gupta, D., Semenova, I., Ikeda, K., Kraikivski, P., Yu, J., Cowan, A., Zaliapin, I. and Rodionov, V. Engineered Tug-of-War Between Kinesin and Dynein Controls Direction of Microtubule Based Transport In Vivo. Traffic (2016); 17: 475-486
  4. Derr ND, Goodman BS, Jungmann R, Leschziner AE, Shih WM, Reck-Peterson SL. Tug-of-war in motor protein ensembles revealed with a programmable DNA origami scaffold. (2012); 338(6107):662-5
  5. Fenton, A.R., Jongens, T.A. & Holzbaur, E.L.F. Mitochondrial adaptor TRAK2 activates and functionally links opposing kinesin and dynein motors. Nat Commun (2021); 12: 4578
  6. Steven P. Gross, Michael A. Welte, Steven M. Block, Eric F. Wieschaus; Coordination of opposite-polarity microtubule motors . J Cell Biol (2002); 156 (4): 715–724
  7. Shabeen Ally, Adam G. Larson, Kari Barlan, Sarah E. Rice, Vladimir I. Gelfand; Opposite-polarity motors activate one another to trigger cargo transport in live cells. J Cell Biol (2009); 187 (7): 1071–1082
  8. Toba S, Watanabe TM, Yamaguchi-Okimoto L, Toyoshima YY, Higuchi H. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. PNAS (2006);103(15):5741-5
  9. Grover R, Fischer J, Schwarz FW, Walter WJ, Schwille P, Diez S. Transport efficiency of membrane-anchored kinesin-1 motors depends on motor density and diffusivity. PNAS (2016);113(46):E7185-E7193
  10. Li Q, Tseng KF, King SJ, Qiu W, Xu J. A fluid membrane enhances the velocity of cargo transport by small teams of kinesin-1. J Chem Phys. (2018);148(12):123318
  11. Nelson SR, Trybus KM, Warshaw DM. Motor coupling through lipid membranes enhances transport velocities for ensembles of myosin Va. PNAS (2014);111, 3986–3995
  12. Gina A. Monzon, Lara Scharrel, Ashwin D’Souza, Verena Henrichs, Ludger Santen, Stefan Diez; Stable tug-of-war between kinesin-1 and cytoplasmic dynein upon different ATP and roadblock concentrations. J Cell Sci (2020); 133 (22): jcs249938
  13. Belyy, V., Schlager, M., Foster, H. et al. The mammalian dynein–dynactin complex is a strong opponent to kinesin in a tug-of-war competition. Nat Cell Biol (2016);18, 1018–1024
  14. Allison M Gicking, Tzu-Chen Ma, Qingzhou Feng, Rui Jiang, Somayesadat Badieyan, Michael A Cianfrocco, William O Hancock Kinesin-1, -2, and -3 motors use family-specific mechanochemical strategies to effectively compete with dynein during bidirectional transport. eLife(2022);  11:e82228

Tags: dynein, intracellular transport, kinesin, microtubule, motility, motors, reconstitution

doi: https://doi.org/10.1242/prelights.33529

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Author's response

The author team shared

1.How could changes in lipid bilayer composition affect motility? In case of the Myosin Va motor, the fluid bilayer of the liposome cargo caused recentering that results in apparent increases in velocity. Increase in velocity has also been seen for teams of Kinesin carrying a liposome cargo. Was there an apparent increase in velocity seen in liposome cargo vs motors attached to similar sized beads? Will introducing gel-like lipids (like DPPC and Cholesterol) modulate/ bias transport parameters?

That’s a great question. We do think that the fluidity of the membrane will affect the re-attachment rates (i.e. attachment right after detachment) of the motors to the microtubule. For a gel-like membrane, motors would rapidly re-attach, as they cannot diffuse away on the cargo membrane. This would lead to a constant tug-of-war between opposite polarity motors and has been observed for non-diffusive cargos such as DNA scaffolds and/or beads. In contrast, on a diffusive membranous cargo the motors can diffuse away from the microtubule upon dissociation, and hence the tug-of-war can be resolved in a finite time period where the winning motors can transport the cargo in their moving direction.

We did not observe an increase in the liposome velocity compared to single motors but rather a reduction in velocity likely due to exclusion effects at high motor densities and to inactive motors acting as anchors for the cargo on the microtubules.

2.How does the vesicle/cargo size affect transport? The experiments and simulations use ~100nm vesicle size and for those cargo sizes, stochastic attachment and detachment determines directionality of cargo. Can you comment on larger cargo (~500nm- 1µm) motion directionality like mitochondria, lipid droplets, and phagosomes with a higher number of engaged motors? Were larger LUVs tried to recapitulate transport?

So far, we have indeed not tested different cargo sizes but this is what we plan to pursue in the future. For larger cargoes, we would expect a higher number of available as well a higher number of MT-bound motors. According to our simulations, we do expect less reversals and more unidirectional or stationary cargoes at a higher number of available motors (as illustrated in Fig. 5e of our manuscript). Having also a higher number of MT-bound motors, we would expect even more stationary cargos and no reversals as we had observed in earlier work (reference 23 in our manuscript) in microtubule gliding assays. However, this would have to be tested with beads or liposomes in experiments or simulations.

3. Beads of 860nm have been found to activate purified dynein in an in vitro motility assay (ref.13); Is it possible to engage dynein in a tug-of-war with kinesin without incorporating the DDB complex when the cargo size is larger?

It might be possible to engage dynein without adaptor molecules in a tug-of-war with kinesins when bound to larger beads. In a way, we previously studied the interplay between adapter-less dynein and kinesin-1 in gliding assays (reference 23 in our manuscript). There, the glass surface served as a large cargo and we readily observed tug-of-war situations. However, in our current study we aimed to mimic the physiological situation as closely as possible which is why we used the full DDB complex as well as full-length Kinesin (KIF16B).

4. Will microtubule roadblocks like Tau and MAP7 increase reversals and pauses to bias transport in the absence of adapter proteins coordinating cargo motility?

Yes, we believe that microtubule-associated proteins such as Tau and MAP7 will affect the attachment and dissociation rates of different motors in distinct ways. For example MAP7 has been shown to recruit kinesin-1.  So, in the presence of MAP7, our expectation is that most of the cargos carried by kinesin-1 (even in presence of dynein) would walk towards the microtubule plus end. However, in case of Tau the effect might be opposite as it has been postulated that Tau inhibits kinesin-1 more than dynein.

5. During short pauses, in unidirectional (DDB-vesicles and KIF16B-vesicles) as well as bidirectional (DDB-KIF16B vesicles) tracks, how often does the cargo dissociate from the microtubule?

At the protein concentrations used in our study, we did not observe any dissociation of cargo from the microtubule.

6. Given that the directional reversals only happen following a pause, does that mean that tenacious or processive motors like kinesin will rarely let non-processive motors like dynein take over as the probability of pausing will be greatly reduced?

We would suggest to skip that question because our dynein along with its adaptor complex dynactin and BICD2 is a highly processive motor.
Otherwise we would answer something like: As it has been seen before, also the competition between non-processive dynein (dynein without adaptor proteins) and processive kinesin, leads to pauses/completely stationary tracks (reference 23 in our manuscript). Thus, pauses do not only occur between tenacious or processive, opposing motors. But dependent on the force-dependent detachment, stepping, and attachment rates, teams might use different mechanisms to counteract opposing forces. Our simulations predict that also processive DDB and KIF16B use distinct mechanisms: While DDB motors share the opposing force more, for KIF16B one motor carries the load and the others are untensioned, ready to take over in case the load-carrying motor detaches.  However, how the pause and/or reversal frequency depends on the number and kind of motors, need to be tested.

 

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