Different microtubules structures assembled by kinesin motors

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Interface-Rich Materials and Assemblies

Different microtubules structures assembled by kinesin motors Weixing Song, Jianxiong Zhu, Weimin Kong, Helmuth Möhwald, and Junbai Li Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b00662 • Publication Date (Web): 18 Jul 2018 Downloaded from http://pubs.acs.org on July 20, 2018

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Langmuir

Different microtubules structures assembled by kinesin motors Delicated to Prof. Helmuth Möhwald

Weixing Song1,*, Jianxiong Zhu2，Weimin Kong1, Helmuth Möhwald3,*，Junbai Li4,*

1 Department of Chemistry, Capital Normal University, Beijing 100048, P.R. China

2 School of Mechanical Engineering, Korea Advanced Institute of Science and Technology (KAIST), 291 Daehak-ro, Yuseong-gu, Daejeon 34141, Republic of Korea

3 Max Planck Institute of Colloids and Interfaces, Am Mühlenberg 1, Golm/Potsdam D-14476, Germany

4 Beijing National Laboratory for Molecular Sciences (BNLMS), International Joint Lab, Institute of Chemistry, Chinese Academy of Science,Beijing 100080, China Email：[email protected], [email protected] , [email protected] Keyword: kinesin; microtubule; streptavidin-biotin; nanostructure; self-assembly

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Abstract: The microtubule-kinesin system is used to form microtubules-based structures via microtubule gliding motility. On the kinesin-coated surface the microtubules can be easily assembled into stable micro- and nanostructures like circles and microtubule bundles using the streptavidin-biotin system. Furthermore, these microtubules structures can still retain performance with kinesin motor movement in spite of different velocities . Collisions bear responsibility for the majority of event leading to circle formation, By taking advantage of biological substances some micro- or nanostructures, difficult to be fabricated by artificial processes, can be easily obtained.

Introduction It is most promising to prepare nanodevices from biological components, because these are smart, biofriendly and biodegradable.1-3 However，there are also major difficulties to be solved. As the individual components are too small and numerous to be manipulated individually, increasingly sophisticated molecular assembly technique had to be developed in recent years.4-10 Basic macromolecular functions have to be coordinated to produce higher-order functions we interpret as life. This means these functions and their interplay have to be understood. Nanobiotechnology may enable one to assemble functional biological macromolecules into constructs performing more sophisticated processes that are unprecedented in the biological world, but this interplay is even more difficult to control for dynamic structures.11-18 2


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Biomolecular motors are promising components for the setup of nanoscale devices and sensors.19-21 As a mechanoenzyme/track system, the kinesin/microtubule system, which normally mediates intracellular molecular trafficking, has been reconfigured as a system for imaging microscale features and processes on synthetic surfaces.22-24 In particular, in vitro transport assays often utilize the geometry of gliding, where motor proteins are bound onto a substrate surface and rapidly propel cytoskeletal filaments in the presence of ATP.22, 24-31 Kinesin is a well-known motor protein that can drive cargos such as vesicles, proteins, and organelles along microtubules in biological cells.

31-32

Kinesin works smartly and efficiently as a nanomachine on the surfaces of

microtubules that are polar cytoskeletal filaments, and they provide tracks to guide the motor from the minus to plus end of microtubules. A critical step in the design and construction of hybrid nanodevices using biomolecular motors is to extract the motors from their natural environment and insert them into an artificial one while retaining their natural function.2, 5, 22, 33-34 Herein, we present an easy approach in which microtubules are assembled into linear microtubule structures using the streptavidin-biotin system and kinesin motors are used to form microtubule circles on a motor-coated surface. Applying microscopy with an energy transfer assay we can reduce photobleaching and observe the motion over extended periods of time. This enables a longermeasurement and development of a more precise model describing the motion. By monitoring the microtubule speed in

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gliding assays, we characterize the slow-down as the microtubule circles glide on the kinesin-coated surface. The pushing force from kinesin motors is much stronger than the resistance caused by the microtubule volume and friction with solution.35-36 We show here, that linear structures and circles on micro- and nanoscales can be easily obtained from biological substances and processes rather than artificial preparation, also be linked still preserving the biological function. Therefore we can study here differences in motion along linear and circular arrays of microtubules as well as the influence of the coupling of tubules. Materials and methods Material: Full length kinesin-1 was kindly donated by Dr. Stefan Diez. The lyophilized tubulin (Cytoskeleton, Denver, CO) was dispersed in BRB80 buffer (80 mM Pipes, pH 6.9/1 mM EGTA/1 mM MgCl2) as a solution of 10 mg/ml. The ratio of 4:2:1 of biotinylated, rhodamine-labeled and unlabeled tubulins was used to copolymerize the rhodamine-labeled biotinylated microtubules with a final concentration of 4 mg/mL in BRB80 buffer with 4 mM MgCl2, 1 mM MgGTP, and 5 % DMSO at 37 °C for 30 min. Microtubules were then diluted in BRB80 buffer supplemented with 10 µM taxol. Streptavidin-Texas red conjugate was purchased from Molecular Probe (USA). Flow chamber fabrication: Glass slides and coverslips (Corning, 50 mm x 24 mm x 0.17 mm) were immersed in KOH saturated solution and subsequently washed with

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ethanol and deionized water. The flow chambers were composed of two coverslips and two strips of a 50 µm double-sided tape with a total volume of 10 µl (50 mm x 4 mm x 0.05 mm). Motility

measurement

of

microtubule

self-assembly

structure:

Rhodamine-labeled biotinylated microtubule (40 µg ml-1) solution was centrifuged at 25000 g for 20 min to remove unpolymerized tubulin and resuspended in fresh BRB80 buffer with 10 µM Taxol. Texas red-labeled streptavidin solution with concentration of 40 µM in BRB80 buffer was added into microtubule solution and incubated for 10 min. A casein solution (0.5 mg mL-1 in BRB80) was introduced into the chamber by filter paper (Ø70, Carl Roth GmbH, Germany) and incubated for 5 min. Subsequently a kinesin solution (20 nM in BRB80) was introduced and also incubated for another 5 min. Then the above microtubule solution supplemented with Texas red-labeled streptavidin was mixed with 3 mM ATP and oxygen scavenger (20 mM Glucose, 0.02 mg mL-1 glucose oxidase, 0.008 mg mL-1 catalase, 0.5% β-mercaptoethanol), and flowed into the kinesin coated chamber. Image acquisition and data analysis: The chamber was sealed and observed under fluorescence using a Leica TCS SP5 laser scanning microscope (63 x water immersion objective). The series of images were processed using Image J (NIH Image, available at http://rsb.info.nih.gov/ij/).

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Transmission Electron Microscopy (TEM): Rhodamine-labeled biotinylated microtubule (40 µg ml-1) solution was washed by centrifugation at 25000 g for 20 min and resuspended in fresh BRB80 buffer with 10 µM Taxol through gently pipetting up and down several times. Texas red-labeled streptavidin solution in BRB80 Buffer was stirred into microtubule solution and incubated. After 10 min, the excess streptavidin was removed through centrifugation at 400,000 × g for 30 min at 25°C in a SW60 rotor (Beckman Coulter, USA). The microtubule samples were prepared by the negative-staining method. Briefly, the microtubule solution (8 µl) was dispersed on a copper grid covered with a Formvar film, and extra solution was removed using a filter paper. Then a drop of 2% uranyl acetate in ethanol solution was spread on the copper grid, incubated for 1 min, and afterwards extra solution was removed. Finally the desiccated sample was observed under a Philips CM 200-FEG high resolution transmission electron microscope (TEM). Velocity measurement of microtubules: The direct time lapse recording of microtubule circular motion enables a determination of the motion velocity of the microtubule. The average velocity per circle v was calculated according to Eq. (1) v = 2πr⋅ n / t

(1)

where r is the average radius for each circle, n is the number of turns of microtubule circular motion and t is the relative time.

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Since the motion is more elliptically, for the calculation one should better use a similar Eq. (2) v = π (r1+r2) ⋅ n / t

(2)

where r1 and r2 are semi-major axis and semi-minor axis, respectively. The velocity of each microtubule structure is measured on 10 samples. Results and discussion The CLSM images (figure 1a, 1b) show, that Texas red-labeled streptavidin has been successfully linked to rhodamine-labeled microtubules. The fluorescence emitted by the Texas-red and rhodamine dye is presented separately as blue and red in the images. In the experiment, the microtubule structures coated by streptavidin were found to fluoresce at about 620 nm, which is emitted by Texas-red labeled streptavidin. It can be obviously concluded that the microtubules are coated by streptavidin. The emission intensity increases with observation time. It is caused by the fact that rhodamine after excitation develops a peak at a wavelength of about 570 nm which can excite Texas-red by energy transfer.37 So the application of two dyes can prolong the investigation of microtubule motion under a fluorescence microscope and provide more data regardless of photobleaching.

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Figure 1. CLSM investigation of microtubules coated with streptavidin. Streptavidin labeled by Texas Red (a). Microtubules labeled by rhodamine (b). TEM images of microtubules linked by streptavidin (c) and the magnified image (d). Schematic of microtubules linked by the biotin-streptavidin bonds (e) The transmission electron microscope images (figure 1c, 1d) show, that the microtubules are strongly linked by the biotin-streptavidin bonds (figure 1e), since negative staining does not break the linkage during the preparation of the TEM samples. Streptavidin has strong non-covalent affinity with D-biotin (Kd～10-15 M),38 and has been applied in many fields.

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Increasing linkages between microtubules were formed during studying the gliding assay. After the microtubule solution was infused into the chamber, the kinesin motors pushed the microtubules forward in the presence of ATP. Through observation and statistics, it has been found that, if the motion direction of the head of a microtubule meets some part of another microtubule at a less than 90-degree angle, both microtubules would be able to link through the streptavidin precoating on a microtubule and be pushed forward together (figure 2, Movie S1 in Supplementary data). In the presence of oxygen scavenger, the microtubule motion can be observed and recorded for the whole experiment including about 3 hours under fluorescence microscopy. However, the existence of two dyes of rhodamine and Texas red can obviously enhance the fluorescence intensity and thus reduce the requirements of the laser intensity, which is very beneficial for clearly observing the microtubule motion and extending the investigation for at least 2 hours on average.

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Figure 2. Time lapse images of forming linear structures. Two microtubules link together during gliding and then move forward together.

With time three or more microtubules would combine and form much bulkier linear self-assembly structures. In fluorescence microscopy the intensity from the microtubules was found to grow significantly. The hollow linear microtubule nanostructures have diameters from dozens of nanometers to hundreds of nanometers, that may be hardly fabricated by artificial methods. The average velocity, an important feature of microtubule motion was obtained by dividing the distance of motion by the corresponding recording time. It seems that the velocities of linear linked microtubules show no significant difference compared to single microtubules. The resistance caused by the microtubule volume during moving is rather small as is the pushing force produced by the kinesin molecules.35-36 The linear structures formed by several microtubules glide on the kinesin-coated surface with the same velocity as the single microtubules. This means that the force exerted by kinesin and the friction increase simultaneously with size.

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Figure 3. Time lapse images of forming circles.

With time the microtubule aggregates tended to form circles. The microtubules glided in all directions due to the random splay of kinesins on the surface. This local microtubules create intersections and cross-link with each other. These intersections create vortices that cause microtubules to form circles or loops.39 Although pinning has been considered to be the primary mechanism underlying ring initiation, the research viewpoint that active self-assembly via collisions is another dominant mechanism of circle formation has been proposed previously.40 When these biotinylated microtubules are partially coated with streptavidin, they become ‘‘sticky’’ because biotin–streptavidin–biotin cross-links can form (figure 3, Movie S2 in Supplementary data).41 The diameters of the circles range from 1.3 to 2 µm according to the investigation of 10 samples. The microscale circles can be more simply fabricated by kinesin motors, an autonomous molecular robot in an artificial process. The micro/nanobiological devices are able to perform many tasks of interest, which will be studied in future. 11


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Compared with the control experiment (without kinesin coating on the surface), both the single microtubule and microtubule aggregates couldn’t form circles. The phenomenon indicates that kinesin plays a key part in the formation of circles. The forces provided by the motors render the microtubule assemblies metastable in the presence of ATP and stable in its absence.42 It has been observed that not only the density of the MTs but also other factors such as driving force, binding force, and steric hindrance were responsible for the polymorphism of MT assembly.43 Kinesins were distributed widely and equally on the glass surfaces and their arrangement was random. One explanation is that a microtubules glides on multiple kinesin heads,44 and the kinesins at the minus-end of the microtubule coming in touch decide the motion direction of the microtubule. The neck domain of the kinesin motor is very flexible and enables microtubules to move forward with coexistence of many kinesins.45-47 Although the motion direction of the minus-end was changed and reversed the original direction, the rest of the microtubules maintained the original direction before coming into contact with the coming kinesins. So the minus end of microtubules had a chance to meet the rest, and they could link each other in the presence of streptavidin.

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Figure 4. Structure of a single microtubule and scheme of the microtubule gliding on a kinesin-coated surface.

Another possibility is presented below: A microtubule is a hollow cylinder in diameter of about 25 nm. Along the microtubule longitudinal axis, α-tubulin and β-tubulin (tubulin heterodimer) are linked alternatingly to form protofilaments (figure 4). 13 protofilaments present a helical arrangement of tubulin heterodimers in the cylinder wall. Each turn of the helix spans 3 tubulin monomers.45,

47

So the

microtubule lateral axis is not perpendicular to the longitudinal axis (protofilament axis). On the other hand, kinesin motors follow the microtubule’s protofilament axis, and they can bind on different protofilaments of a microtubule. The number of kinesin motors binding on those protofilaments is stochastically equal, and this would make a wiggled line. But if, once a deviation from the longitudinal axis is formed, and this would enable a next assembly again preferably with a deviation into the same direction, this would finally yield a circle. So single MTs consist mainly of left-handed protofilament supertwist and are sometimes bent by kinesin-driven sliding into a ring which subsequently rotates counterclockwise.47 The circles rotating in the counterclockwise direction are nearly twice as much as those rotating in the clockwise direction during observing 10 samples. The total microtubule is thus driven to deviate from the track parallel to the longitudinal axis. Eventually the minus end of the microtubule wanders from their path, gets close to the rest part of the microtubule and 13


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forms a circle. So in the same field of view, the microtubules may turn in opposite directions (Movie S3 in Supplementary data). In the presence of ATP, the microtubule circles whirl around the circle centers. The average velocity is constant and does not increase after increasing the ATP concentration through injecting ATP. However, the velocity of microtubule circles is considerably lower than that of the linear microtubule aggregates and single microtubules. The latter reaches around 560 ± 50 nm/s, which is about twice the value of the former, 260 ± 40 nm/s according to 10 samples. Generally, the circle structures have several turns, and under every microtubule turn there are many kinesins working and producing mechanical work to forward the microtubule. Those kinesins under different microtubule turns might provide forces into directions, that deviate from the average one, which reduces the velocity of the total microtubule circle structure. The circle structures therefore possess a higher demand on kinesins under every microtubule turn. Those kinesins working for the same turn must provide cooperative forces to yield a round shape. As previously reported, kinesins work with microtubules in a “hand-over-hand” stepping mechanism. The motor domain of kinesins includes two heads which alternate in taking steps from the minus to plus end of microtubules.27, 46, 50-52 However, the kinesins are randomly fixed on the surface, and the direction of their two heads needs adjustment to realize the total power in round shape. That would

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affect the strength yielded by every kinesin and thus reduce the final velocity of the total circles. In addition, streptavidin labeling may cause steric hindrance and thus lead to the slowdown. But the decline of our microtubule circles is obviously lower compared with the previously report that the microtubules with streptavidin modification move at about 28 nm/s.52 In our observation, enough ATP concentration was provided during observation, and the microtubules can maintain 80% of their velocity after 5h. Moreover, less laser intensity was applied due to the enhanced fluorescence by energy transfer during two fluorescence molecules, reducing the proteins damage caused by laser lighting. In conclusion, microtubules can self-assemble into linear microtubule aggregates without affecting the velocity on the kinesin-coated surface. This indicates, that the force affected by kinesins and friction forces increase the same way by aggregation. It indicates that the surface exposed to the kinesin motors is also causing the friction. The microtubules also can form circular structures in the presence of kinesin and ATP, and the motion velocity decreases to nearly half of that of the linear microtubule structures. This may be ascribed to the fact that a part of the forces exerted by the kinesins is deviating in direction from that of main movement. Those assembled structures have potential application in design and construction of more complicated nanostructures and serve as template for fabricating nanomaterials and sensors.

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Acknowledgement. The authors gratefully acknowledge the financial support of this research by the National Nature Science Foundation of China (Nos. 61404035 and 21773009). References （1） Viswanath, V.; Santhakumar, K., Perspectives on dendritic architectures and their biological applications: From core to cell. Journal of Photochemistry and Photobiology B-Biology 2017, 173, 61-83. （2） Malcos, J. L.; Hancock, W. O., Engineering tubulin: microtubule functionalization approaches for nanoscale device applications. Applied Microbiology and Biotechnology 2011, 90, 1-10. （3） Fakruddin, M.; Hossain, Z.; Afroz, H., Prospects and applications of nanobiotechnology: a medical perspective. Journal of Nanobiotechnology 2012, 10， 31 . （4） Kong, D. S.; Carr, P. A.; Chen, L.; Zhang, S.; Jacobson, J. M., Parallel gene synthesis in a microfluidic device. Nucleic Acids Research 2007, 35, Article No.: e61. （5） Dong, C.; Dinu, C. Z., Molecular trucks and complementary tracks for bionanotechnological applications. Current Opinion in Biotechnology 2013, 24, 612-619. （6） Fujimoto, K.; Nagai, M.; Shintaku, H.; Kotera, H.; Yokokawa, R., Dynamic formation of a microchannel array enabling kinesin-driven microtubule transport between separate compartments on a chip. Lab on a Chip 2015, 15, 2055-2063. （7） Sikora, A.; Ramon-Azcon, J.; Sen, M.; Kim, K.; Nakazawa, H.; Umetsu, M.; Kumagai, I.; Shiku, H.; Matsue, T.; Teizer, W., Microtubule guiding in a multi-walled carbon nanotube circuit. Biomedical Microdevices 2015, 17, 78. （8） Islam, M. N.; Gopalan, V.; Hague, M. H.; Masud, M. K.; Al Hossain, S.; Yamauchi, Y.; Nam-Trung, N.; Lam, A. K.-Y.; Shiddiky, M. J. A., A PCR-free electrochemical method for messenger RNA detection in cancer tissue samples. Biosensors & Bioelectronics 2017, 98, 227-233. 16


Page 16 of 22

Page 17 of 22 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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（9） Susi, T.; Kepaptsoglou, D.; Lin, Y.-C.; Ramasse, Q. M.; Meyer, J. C.; Suenaga, K.; Kotakoski, J., Towards atomically precise manipulation of 2D nanostructures in the electron microscope. 2d Materials 2017, 4, 042004. （10） Lin, Z. H.; Si, T. Y.; Wu, Z. G.; Gao, C. Y.; Lin, X. K.; He, Q., Light-Activated Active Colloid Ribbons. Angew Chem Int Edit 2017, 56, 13517-13520. （11） Bhalerao, K. D.; Eteshola, E.; Keener, M.; Lee, S. C., Nanodevice design through the functional abstraction of biological macromolecules. Appl Phys Lett 2005, 87, 3. （12） Bellan, L. M.; Wu, D.; Langer, R. S., Current trends in nanobiosensor technology. Wiley Interdisciplinary Reviews-Nanomedicine and Nanobiotechnology 2011, 3, 229-246. （13） Tan, S. J.; Campolongo, M. J.; Luo, D.; Cheng, W. L., Building plasmonic nanostructures with DNA. Nature Nanotechnology 2011, 6, 268-276. （14） Wang, J.; Gutierrez, M., Stress-strain behaviour of carbon nanotubes under cyclic loading. Micro & Nano Letters 2007, 2, 111-114. （15） Zhou, X. J.; Zifer, T.; Wong, B. M.; Krafcik, K. L.; Leonard, F.; Vance, A. L., Color Detection Using Chromophore-Nanotube Hybrid Devices. Nano Letters 2009, 9, 1028-1033. （16） Linko, V.; Ora, A.; Kostiainen, M. A., DNA Nanostructures as Smart Drug-Delivery Vehicles and Molecular Devices. Trends in Biotechnology 2015, 33, 586-594. （17） Samanta, A.; Medintz, I. L., Nanoparticles and DNA - a powerful and growing functional combination in bionanotechnology. Nanoscale 2016, 8, 9037-9095. （18） Wu, Z. G.; Wu, Y. J.; He, W. P.; Lin, X. K.; Sun, J. M.; He, Q., Self-Propelled Polymer-Based Multilayer Nanorockets for Transportation and Drug Release. Angew Chem Int Edit 2013, 52, 7000-7003. （19） Baghayeri, M.; Veisi, H.; Ghanei-Motlagh, M., Amperometric glucose biosensor based on immobilization of glucose oxidase on a magnetic glassy carbon 17


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Page 18 of 22

electrode modified with a novel magnetic nanocomposite. Sensors and Actuators B-Chemical 2017, 249, 321-330. （20） Han, K. H.; Kim, J. Y.; Jo, S. G.; Seo, C.; Kim, J.; Joo, J., Sensitive optical bio-sensing of p-type WSe2 hybridized with fluorescent dye attached DNA by doping and de-doping effects. Nanotechnology 2017, 28, 435501. （21） Zhou, C.; Duan, X.; Liu, N., DNA-Nanotechnology-Enabled Chiral Plasmonics: From Static to Dynamic. Accounts of chemical research 2017, 50, 2906-2914. （22） Song, W. X.; Mohwald, H.; Li, J. B., Movement of polymer microcarriers using a biomolecular motor. Biomaterials 2010, 31, 1287-1292. （23） Reuther, C.; Mittasch, M.; Naganathan, S. R.; Grill, S. W.; Diez, S., Highly-Efficient Guiding of Motile Microtubules on Non-Topographical Motor Patterns. Nano Lett 2017, 17, 5699-5705. （24） Hess, H.; Ross, J. L., Non-equilibrium assembly of microtubules: from molecules to autonomous chemical robots. Chemical Society Reviews 2017, 46, 5570-5587. （25） Jeune-Smith, Y.; Agarwal, A.; Hess, H., Cargo loading onto kinesin powered molecular shuttles. J Vis Exp 2010, 3, 2006. （26） Hiyama,

S.;

Moritani,

Y.;

Gojo,

R.;

Takeuchi,

S.;

Sutoh,

K.,

Biomolecular-motor-based autonomous delivery of lipid vesicles as nano- or microscale reactors on a chip. Lab on a Chip 2010, 10, 2741-2748. （27） Nitzsche, B.; Bormuth, V.; Brauer, C.; Howard, J.; Ionov, L.; Kerssemakers, J.; Korten, T.; Leduc, C.; Ruhnow, F.; Diez, S., Studying Kinesin Motors by Optical 3D-Nanometry in Gliding Motility Assays. Methods in Cell Biology, Vol 95 2010, 95, 247-271. （28） Bakewell, D. J. G.; Nicolau, D. V., Protein linear molecular motor-powered nanodevices. Australian Journal of Chemistry 2007, 60, 314-332. （29） Lam, A. T.; VanDelinder, V.; Kabir, A. M. R.; Hess, H.; Bachand, G. D.; Kakugo, A., Cytoskeletal motor-driven active self-assembly in in vitro systems. Soft Matter 2016, 12, 988-997. 18


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Langmuir

（30） Roberts, A. J.; Kon, T.; Knight, P. J.; Sutoh, K.; Burgess, S. A., Functions and mechanics of dynein motor proteins. Nature Reviews Molecular Cell Biology 2013, 14, 713-726. （31） Siddiqui, N.; Straube, A., Intracellular Cargo Transport by Kinesin-3 Motors.

Biochemistry-Moscow 2017, 82, 803-815. （32） Lu, W.; Gelfand, V. I., Moonlighting Motors: Kinesin, Dynein, and Cell Polarity. Trends in Cell Biology 2017, 27, 505-514. （33） Fulga, F.; Nicolau, D. V., Jr.; Nicolau, D. V., Models of protein linear molecular motors for dynamic nanodevices. Integrative Biology 2009, 1, 150-169. （34） Song, W. X.; He, Q.; Cui, Y.; Mohwald, H.; Diez, S.; Li, J. B., Assembled capsules transportation driven by motor proteins. Biochem Bioph Res Co 2009, 379, 175-178. （35） Stracke, R.; Bohm, K. J.; Burgold, J.; Schacht, H. J.; Unger, E., Physical and technical parameters determining the functioning of a kinesin-based cell-free motor system. Nanotechnology 2000, 11, 52-56. （36） Beeg, J.; Klumpp, S.; Dimova, R.; Gracià, R. S.; Unger, E.; Lipowsky, R., Transport of Beads by Several Kinesin Motors. Biophysical Journal 2008, 94, 532-541. （37） Johnson, I.; Spence, M. T. Z.; The Molecular Probes® Handbook, 11th Edition; Life Technologies Corporation, 2010, Chapter 1. （38） Green, N. M., Avidin. In Advances in Protein Chemistry, C.B. Anfinsen, J. J. T. E.; Frederic, M. R., Eds. Academic Press: 1975; Vol. Volume 29, 85-133. （39） Liu, L.; Tuzel, E.; Ross, J. L., Loop formation of microtubules during gliding at high density. J Phys-Condens Mat 2011, 23, 374104. （40） VanDelinder, V.; Brener, S.; Bachand, G. D., Mechanisms Underlying the Active Self-Assembly of Microtubule Rings and Spools. Biomacromolecules 2016, 17, 1048-1056. （41） Luria, I.; Crenshaw, J.; Downs, M.; Agarwal, A.; Seshadri, S. B.; Gonzales, J.; Idan, O.; Kamcev, J.; Katira, P.; Pandey, S.; Nitta, T.; Phillpot, S. R.; Hess, H., 19


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Microtubule nanospool formation by active self-assembly is not initiated by thermal activation. Soft Matter 2011, 7, 3108-3115. （42） Hess, H.; Clemmens, J.; Brunner, C.; Doot, R.; Luna, S.; Ernst, K.-H.; Vogel, V., Molecular Self-Assembly of “Nanowires” and “Nanospools” Using Active Transport. Nano Letters 2005, 5, 629-633. （43） Liu, L.; Tuzel, E.; Ross, J. L., Loop formation of microtubules during gliding at high density. J Phys-Condens Mat 2011, 23, 374104. （44） Leduc, C.; Ruhnow, F.; Howard, J.; Diez, S., Detection of fractional steps in cargo movement by the collective operation of kinesin-1 motors. Proceedings of the National Academy of Sciences of the United States of America 2007, 104, 10847-10852. （45） Kalchishkova, N.; Bohm, K. J., The role of kinesin neck linker and neck in velocity regulation. J Mol Biol 2008, 382, 127-135. （46） Oiwa, K.; Kojima, H., Molecular motors: Keep on moving. Nat Nano 2008,

3, 531-532. （47） Schaap, Iwan A. T.; Carrasco, C.; de Pablo, Pedro J.; Schmidt, Christoph F., Kinesin Walks the Line: Single Motors Observed by Atomic Force Microscopy. Biophysical Journal 2011, 100, 2450-2456. （48） Ray, S.; Meyhofer, E.; Milligan, R. A.; Howard, J., Kinesin follows the microtubule's protofilament axis. Journal of Cell Biology 1993, 121, 1083-93. （49） Kamimura, S.; Mandelkow, E., TUBULIN PROTOFILAMENTS AND KINESIN-DEPENDENT MOTILITY. Journal of Cell Biology 1992, 118, 865-875. （50） Verhey, K. J.; Hammond, J. W., Traffic control: regulation of kinesin motors.

Nature Reviews Molecular Cell Biology 2009, 10, 765-777. （51） Marx, A.; Hoenger, A.; Mandelkow, E., Structures of Kinesin Motor Proteins. Cell Motility and the Cytoskeleton 2009, 66, 958-966. （52） Kawamura, R.; Kakugo, A.; Shikinaka, K.; Osada, Y.; Gong, J. P., Ring-Shaped Assembly of Microtubules Shows Preferential Counterclockwise Motion. Biomacromolecules 2008, 9, 2277-2282. 20


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Different microtubules structures assembled by kinesin motors

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