Study of active self-assembly using biomolecular motors

AbstractSelf-propelled biomolecular motor systems, such as microtubule-kinesin or microtubule-dynein, are intricate natural machines with the ability to convert chemical energy into mechanical work with high efficiency. In recent years, the biomolecular motor systems have emerged as promising candidates for studying active self-assembly based on the in vitro gliding assay of the motor systems. Several strategies have been developed to demonstrate the active self-assembly of biomolecular motors, which provided a wealth of organized and complex structures. Here we review the latest progress in the active self-assembly of microtubule-kinesin and microtubule-dynein with an emphasis on the emergence of various structures and necessary design parameters for controlling their polymorphism.Recent advances in the study of active self-assembly utilizing biomolecular motors are reviewed. Various methodologies developed for demonstrating active self-assembly of biomolecular motors are discussed in detail with an emphasis on the morphological variations of the self-assembled structures.

[1]  Jian Ping Gong,et al.  Growth of ring-shaped microtubule assemblies through stepwise active self-organisation , 2013 .

[2]  M. Cates,et al.  Depletion force in colloidal systems , 1995 .

[3]  Jian Ping Gong,et al.  Prolongation of the active lifetime of a biomolecular motor for in vitro motility assay by using an inert atmosphere. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[4]  H. Hess,et al.  Modeling negative cooperativity in streptavidin adsorption onto biotinylated microtubules. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[5]  J. Gong,et al.  How to integrate biological motors towards bio-actuators fueled by ATP. , 2011, Macromolecular bioscience.

[6]  Yutaka Sumino,et al.  Large-scale vortex lattice emerging from collectively moving microtubules , 2012, Nature.

[7]  J. Fewell,et al.  Models of division of labor in social insects. , 2001, Annual review of entomology.

[8]  J. Gong,et al.  Controlled clockwise-counterclockwise motion of the ring-shaped microtubules assembly. , 2011, Biomacromolecules.

[9]  Jian Ping Gong,et al.  Formation of ring-shaped assembly of microtubules with a narrow size distribution at an air–buffer interface , 2012 .

[10]  R. Wade,et al.  How does taxol stabilize microtubules? , 1995, Current Biology.

[11]  V. Vandelinder,et al.  Cytoskeletal motor-driven active self-assembly in in vitro systems. , 2016, Soft matter.

[12]  Matthew E. Downs,et al.  Microtubule nanospool formation by active self-assembly is not initiated by thermal activation , 2011 .

[13]  K. Kuribayashi-Shigetomi,et al.  Role of confinement in the active self-organization of kinesin-driven microtubules , 2017 .

[14]  Ashutosh Agarwal,et al.  Nanoscale transport enables active self-assembly of millimeter-scale wires. , 2012, Nano letters.

[15]  H. Hess,et al.  Non-equilibrium assembly of microtubules: from molecules to autonomous chemical robots. , 2017, Chemical Society reviews.

[16]  R. Himes,et al.  Alterations in number of protofilaments in microtubules assembled in vitro , 1978, The Journal of cell biology.

[17]  Y. Toyoshima,et al.  Formation of ring-shaped microtubule assemblies through active self-organization on dynein , 2014 .

[18]  Marco Dorigo,et al.  Swarm intelligence: from natural to artificial systems , 1999 .

[19]  Erkan Tüzel,et al.  Loop formation of microtubules during gliding at high density , 2011, Journal of physics. Condensed matter : an Institute of Physics journal.

[20]  J. Spudich,et al.  Fluorescent actin filaments move on myosin fixed to a glass surface. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Henry Hess,et al.  Self-assembly driven by molecular motors. , 2006, Soft matter.

[22]  Jeremy E Niven How Honeybees Break a Decision-Making Deadlock , 2012, Science.

[23]  L. Pelletier,et al.  Mitotic spindle assembly in animal cells: a fine balancing act , 2017, Nature Reviews Molecular Cell Biology.

[24]  Fumio Oosawa,et al.  On Interaction between Two Bodies Immersed in a Solution of Macromolecules , 1954 .

[25]  S. Leibler,et al.  Self-organization of microtubules and motors , 1997, Nature.

[26]  D. J. Kushner,et al.  Self-assembly of biological structures , 1969, Bacteriological reviews.

[27]  A. Konagaya,et al.  Mechanical oscillation of dynamic microtubule rings , 2016 .

[28]  G. Whitesides,et al.  Self-Assembly at All Scales , 2002, Science.

[29]  A. Konagaya,et al.  Depletion force induced collective motion of microtubules driven by kinesin. , 2015, Nanoscale.

[30]  J. Howard,et al.  Mechanics of Motor Proteins and the Cytoskeleton , 2001 .

[31]  R. Kawamura,et al.  Controlling the bias of rotational motion of ring-shaped microtubule assembly. , 2015, Biomacromolecules.

[32]  Bartosz A Grzybowski,et al.  Principles and implementations of dissipative (dynamic) self-assembly. , 2006, The journal of physical chemistry. B.

[33]  Erwin Frey,et al.  Polar patterns of driven filaments , 2010, Nature.

[34]  Viola Vogel,et al.  Molecular self-assembly of "nanowires"and "nanospools" using active transport. , 2005, Nano letters.

[35]  Akira Kakugo,et al.  Effect of length and rigidity of microtubules on the size of ring-shaped assemblies obtained through active self-organization. , 2015, Soft matter.

[36]  P. Satir,et al.  Overview of structure and function of mammalian cilia. , 2007, Annual review of physiology.

[37]  M. Knoblauch,et al.  Biomimetic actuators: where technology and cell biology merge , 2004, Cellular and Molecular Life Sciences CMLS.

[38]  H. Hess,et al.  Controlling self-assembly of microtubule spools via kinesin motor density. , 2014, Soft matter.

[39]  Yoshihito Osada,et al.  Ring-shaped assembly of microtubules shows preferential counterclockwise motion. , 2008, Biomacromolecules.

[40]  J. Spudich,et al.  Assays for actin sliding movement over myosin-coated surfaces. , 1991, Methods in enzymology.

[41]  Henry Hess,et al.  Engineering applications of biomolecular motors. , 2011, Annual review of biomedical engineering.

[42]  P. Rothemund Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[43]  J. Davies,et al.  Molecular Biology of the Cell , 1983, Bristol Medico-Chirurgical Journal.

[44]  Yoshihito Osada,et al.  Microtubule bundle formation driven by ATP: the effect of concentrations of kinesin, streptavidin and microtubules , 2010, Nanotechnology.

[45]  N. Seeman Nucleic acid junctions and lattices. , 1982, Journal of theoretical biology.

[46]  A. Konagaya,et al.  Understanding the emergence of collective motion of microtubules driven by kinesins: role of concentration of microtubules and depletion force , 2017 .

[47]  Henry Hess,et al.  DNA-assisted swarm control in a biomolecular motor system , 2018, Nature Communications.

[48]  J. Gong,et al.  Active self-organization of microtubules in an inert chamber system , 2012 .

[49]  Yoshihito Osada,et al.  Dynamic self-organization and polymorphism of microtubule assembly through active interactions with kinesin , 2011 .