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Biological Nanomotors with a Revolution, Linear, or Rotation Motion Mechanism.

ABSTRACT: The ubiquitous biological nanomotors were classified into two categories in the past: linear and rotation motors. In 2013, a third type of biomotor, revolution without rotation (http://rnanano.osu.edu/movie.html), was discovered and found to be widespread among bacteria, eukaryotic viruses, and double-stranded DNA (dsDNA) bacteriophages. This review focuses on recent findings about various aspects of motors, including chirality, stoichiometry, channel size, entropy, conformational change, and energy usage rate, in a variety of well-studied motors, including FoF1 ATPase, helicases, viral dsDNA-packaging motors, bacterial chromosome translocases, myosin, kinesin, and dynein. In particular, dsDNA translocases are used to illustrate how these features relate to the motion mechanism and how nature elegantly evolved a revolution mechanism to avoid coiling and tangling during lengthy dsDNA genome transportation in cell division. Motor chirality and channel size are two factors that distinguish rotation motors from revolution motors. Rotation motors use right-handed channels to drive the right-handed dsDNA, similar to the way a nut drives the bolt with threads in same orientation; revolution motors use left-handed motor channels to revolve the right-handed dsDNA. Rotation motors use small channels (<2 nm in diameter) for the close contact of the channel wall with single-stranded DNA (ssDNA) or the 2-nm dsDNA bolt; revolution motors use larger channels (>3 nm) with room for the bolt to revolve. Binding and hydrolysis of ATP are linked to different conformational entropy changes in the motor that lead to altered affinity for the substrate and allow work to be done, for example, helicase unwinding of DNA or translocase directional movement of DNA.

SUBMITTER: Guo P

PROVIDER: S-EPMC4771369 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Project description:Biomotors were once described into two categories: linear motor and rotation motor. Recently, a third type of biomotor with revolution mechanism without rotation has been discovered. By analogy, rotation resembles the Earth rotating on its axis in a complete cycle every 24h, while revolution resembles the Earth revolving around the Sun one circle per 365 days (see animations http://nanobio.uky.edu/movie.html). The action of revolution that enables a motor free of coiling and torque has solved many puzzles and debates that have occurred throughout the history of viral DNA packaging motor studies. It also settles the discrepancies concerning the structure, stoichiometry, and functioning of DNA translocation motors. This review uses bacteriophages Phi29, HK97, SPP1, P22, T4, and T7 as well as bacterial DNA translocase FtsK and SpoIIIE or the large eukaryotic dsDNA viruses such as mimivirus and vaccinia virus as examples to elucidate the puzzles. These motors use ATPase, some of which have been confirmed to be a hexamer, to revolve around the dsDNA sequentially. ATP binding induces conformational change and possibly an entropy alteration in ATPase to a high affinity toward dsDNA; but ATP hydrolysis triggers another entropic and conformational change in ATPase to a low affinity for DNA, by which dsDNA is pushed toward an adjacent ATPase subunit. The rotation and revolution mechanisms can be distinguished by the size of channel: the channels of rotation motors are equal to or smaller than 2 nm, that is the size of dsDNA, whereas channels of revolution motors are larger than 3 nm. Rotation motors use parallel threads to operate with a right-handed channel, while revolution motors use a left-handed channel to drive the right-handed DNA in an anti-chiral arrangement. Coordination of several vector factors in the same direction makes viral DNA-packaging motors unusually powerful and effective. Revolution mechanism that avoids DNA coiling in translocating the lengthy genomic dsDNA helix could be advantageous for cell replication such as bacterial binary fission and cell mitosis without the need for topoisomerase or helicase to consume additional energy.

Project description:Precise spatiotemporal regulation is the foundation for the healthy development and maintenance of living organisms. All cells must correctly execute their function in the right place at the right time. Cellular motion is thus an important dynamic readout of signaling in key disease-relevant molecular pathways. However despite the rapid advancement of imaging technology, a comprehensive quantitative description of motion imaged under different imaging modalities at all spatiotemporal scales; molecular, cellular and tissue-level is still lacking. Generally, cells move either 'individually' or 'collectively' as a group with nearby cells. Current computational tools specifically focus on one or the other regime, limiting their general applicability. To address this, we recently developed and reported a new computational framework, Motion Sensing Superpixels (MOSES). Incorporating the individual advantages of single cell trackers for individual cell and particle image velocimetry (PIV) for collective cell motion analyses, MOSES enables 'mesoscale' analysis of both single-cell and collective motion over arbitrarily long times. At the same time, MOSES readily complements existing single-cell tracking workflows with additional characterization of global motion patterns and interaction analysis between cells and also operates directly on PIV extracted motion fields to yield rich motion trajectories analogous for single-cell tracks suitable for high-throughput motion phenotyping. This protocol provides a step-by-step practical guide for those interested in applying MOSES to their own datasets. The protocol highlights the salient features of a MOSES analysis and demonstrates the ease-of-use and wide applicability of MOSES to biological imaging through demo experimental analyses with ready-to-use code snippets of four datasets from different microscope modalities; phase-contrast, fluorescent, lightsheet and intra-vital microscopy. In addition we discuss critical points of consideration in the analysis.

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Biological Nanomotors with a Revolution, Linear, or Rotation Motion Mechanism.

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