Synthetic Systems Powered by Biological Molecular Motors

Saper, Gadiel; Hess, Henry

doi:10.1021/acs.chemrev.9b00249

Cited by 114 publications

(93 citation statements)

References 369 publications

(560 reference statements)

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“…Catalysis-fueled propulsion of biomolecules at the nanoscale is no doubt a fascinating concept and has potential applications in the field of nanoscience and medicine ( 42 – 49 ). However, mounting experimental and theoretical evidence argue against the mechanism, scale, and even the existence of such phenomenon ( 1 , 2 , 14 , 16 , 38 , 50 ).…”

Section: Discussionmentioning

confidence: 99%

Single-molecule diffusometry reveals no catalysis-induced diffusion enhancement of alkaline phosphatase as proposed by FCS experiments

Chen

Shaw

Wilson

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Theoretical and experimental observations that catalysis enhances the diffusion of enzymes have generated exciting implications about nanoscale energy flow, molecular chemotaxis, and self-powered nanomachines. However, contradictory claims on the origin, magnitude, and consequence of this phenomenon continue to arise. To date, experimental observations of catalysis-enhanced enzyme diffusion have relied almost exclusively on fluorescence correlation spectroscopy (FCS), a technique that provides only indirect, ensemble-averaged measurements of diffusion behavior. Here, using an anti-Brownian electrokinetic (ABEL) trap and in-solution single-particle tracking, we show that catalysis does not increase the diffusion of alkaline phosphatase (ALP) at the single-molecule level, in sharp contrast to the ∼20% enhancement seen in parallel FCS experiments using p-nitrophenyl phosphate (pNPP) as substrate. Combining comprehensive FCS controls, ABEL trap, surface-based single-molecule fluorescence, and Monte Carlo simulations, we establish that pNPP-induced dye blinking at the ∼10-ms timescale is responsible for the apparent diffusion enhancement seen in FCS. Our observations urge a crucial revisit of various experimental findings and theoretical models––including those of our own––in the field, and indicate that in-solution single-particle tracking and ABEL trap are more reliable means to investigate diffusion phenomena at the nanoscale.

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Section: Discussionmentioning

confidence: 99%

Single-molecule diffusometry reveals no catalysis-induced diffusion enhancement of alkaline phosphatase as proposed by FCS experiments

Chen

Shaw

Wilson

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…To make the system sustainable, efforts are underway to prevent the degradation or loss of MTs in the system by using reactive oxygen species (ROS)-free environment, and osmolytes (Kabir et al 2011;Islam et al 2016;Bachand et al 2018;Munmun et al 2020). In the future, this knowledge would expand potential applications of biomolecular motors with precisely controlled synchronization, which may ultimately benefit molecular robotics (Hagiya et al 2014;Saper and Hess 2019).…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

Synchronous operation of biomolecular engines

2020

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Biomolecular motor systems are the smallest natural machines with an ability to convert chemical energy into mechanical work with remarkably high efficiency. Such attractive features enabled biomolecular motors to become classic tools in soft matter research over the past decade. For designing suitably engineered biomimetic systems, the biomolecular motors can potentially be used as molecular engines that can transform energy and ensure great advantages for the construction of bio-nanodevices and molecular robots. From the optimization of their prolonged lifetime to coordinate them into highly complex and ordered structures, enormous efforts have been devoted to make them useful in the synthetic environment. Synchronous operation of the biomolecular engines is one of the key criteria to coordinate them into certain different patterns, which depends on the local interaction of biomolecular motors. Utilizing chemical and physical stimuli, synchronization of biomolecular motor systems has become possible, which allows them to coordinate into different higher ordered patterns with different modes of functionality. Recently, programmed synchronous operation of the biomolecular engines has also been demonstrated, using a smart biomaterial to build up swarms reminiscent of nature. Here, we review the recent progress in the synchronized operation of biomolecular motors in engineered systems to explicitly program their interaction and further their applications. Such developments in the coordination of biomolecular motors have opened a broad way to explore the construction of future autonomous molecular machines and robots based on synchronization of biomolecular engines.

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“…In vitro reconstitution of the kinesin-1 (KIF5B) and microtubule system has enabled study of the biophysical properties of motor-protein transport, as well as established a foundation platform for nanotechnology applications including energy-driven assembly, bioanalytical assays, and biocomputation. [16][17][18][19] Microtubules in these systems are typically stabilized against spontaneous depolymerization using the anti-cancer drug paclitaxel (Taxol®), which consequently increases the stiffness of the lament and leads to straighter transport trajectories in gliding motility assays. While enhanced stability is desired for most in vitro experiments and applications, the rapid and efficient removal of stabilizing agents is necessary for experiments requiring native microtubule dynamics.…”

Section: Introductionmentioning

confidence: 99%