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Molecular Machines with Bio-Inspired Mechanisms SPECIAL FEATURE: PERSPECTIVE

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Molecular Machines with Bio-Inspired Mechanisms SPECIAL FEATURE: PERSPECTIVE SPECIAL FEATURE: PERSPECTIVE Molecular machines with bio-inspired mechanisms SPECIAL FEATURE: PERSPECTIVE Liang Zhanga,b, Vanesa Marcosb, and David A. Leigha,b,1 Edited by J. Fraser Stoddart, Northwestern University, Evanston, IL, and approved January 31, 2018 (received for review December 17, 2017) The widespread use of molecular-level motion in key natural processes suggests that great rewards could come from bridging the gap between the present generation of synthetic molecular machines—which by and large function as switches—and the machines of the macroscopic world, which utilize the synchronized behavior of integrated components to perform more sophisticated tasks than is possible with any individual switch. Should we try to make molecular machines of greater complexity by trying to mimic machines from the macroscopic world or instead apply unfamiliar (and no doubt have to discover or invent currently unknown) mechanisms utilized by biological machines? Here we try to answer that question by exploring some of the advances made to date using bio-inspired machine mechanisms. molecular machines | molecular motors | molecular robotics | catenanes | rotaxanes Introduction—Technomimetics vs. Biomimetics in pursuing this second strategy is that the only There are two, fundamentally different, philosophies for “textbook” we have to follow is unclear: Biological designing molecular machinery (1). One is to scale machines are so complex that it is often difficult to down classical mechanical elements from the macro- deconvolute the reasons behind the dynamics of in- scopic world, an approach advocated in many of the dividual machine parts. How and why does each Drexlerian designs for nanomachines (2) and also the peptide residue move in the way it does in order for inspiration behind “nanocars” (3–7), “molecular pis- kinesin to walk along a microtubule; which confor- tons” (8), “molecular elevators” (9), “molecular wheel- mational, hydrogen bonding, and solvation changes barrows” (10), and other technomimetic (11) molecules are necessary to bring about transport; and which only designed to imitate macroscopic objects at the molec- occur as a consequence of other intrinsically required ular level (1). An advantage of this approach is that the intramolecular rearrangements? Applying fundamen- engineering concepts behind such machines and tal principles deduced from small-scale physics and mechanisms are well understood in terms of their biomachines is the approach our group has adopted macroscopic counterparts; a drawback is that many of in building molecular machines over the past two the mechanical principles upon which complex mac- decades (13). Here we outline progress on this path to roscopic machines are based are inappropriate for the synthetic nanomachines, the application of bio-inspired molecular world (1, 12). mechanisms to the design of molecular machines. An alternative philosophy is to try to unravel the workings of an already established nanotechnology, Simple Machines biology, and apply those concepts to the design of Since Stoddart’s invention of the switchable molecular synthetic molecular machines. A potential upside of shuttle (Fig. 1A) (14), chemists have used molecular this, biomimetic, approach is that such designs are switching to perform a variety of “on”/“off” tasks with clearly well-suited to functional machines that operate synthetic mechanically interlocked molecules (15–17). at the nanoscale, even when limited, as nature is, to Catenane and rotaxane switches have been shown to the use of only 20 different building blocks (amino act as bits in molecular electronics (18, 19) and used acids), ambient temperatures and pressures, and wa- for chiroptical switching (20), for fluorescence switch- ter as the operating medium. However, a major issue ing (21), for the writing of information in polymer films aSchool of Chemistry and Molecular Engineering, East China Normal University, 200062 Shanghai, China; and bSchool of Chemistry, University of Manchester, M13 9PL Manchester, United Kingdom Author contributions: L.Z., V.M., and D.A.L. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Published under the PNAS license. 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1712788115 PNAS Latest Articles | 1of8 Downloaded by guest on October 2, 2021 complex tasks. For example, a pair of scissors can be considered a A N compound machine consisting of levers (the handles and blades N Si O O O HN NH O O O O O O O Si pivoting about a fulcrum) connected to wedges (the cutting edges N of the blades). Because matter behaves so differently at different Switches relative affinities length scales, several types of simple machines cannot perform N Macrocycle of thread binding sites the same function they execute at macroscopic scales in the low positional distribution Reynolds number and Brownian motion-dominated environment 84 16 in which molecular-sized machines operate. An inclined plane, for [D5]pyridine CF3CO2D example, has no mechanical advantage nor effect on the motion N of a molecular object; it is the height of an energy barrier, not its N shape, that determines the ease (i.e., rate) at which a barrier to Si O O O H2N NH2 O O O O O O O Si molecular motion is overcome (1). N In a regime where inertia and momentum are irrelevant in N mechanical terms, the basic mechanisms of molecular machines include switching of relative binding affinities at different sites and modifying the kinetics for changes of position of components that <2 >98 occur by random thermal motion (Fig. 1) as well as binding-release Switching the relative macrocycle binding affinity of sites on the track causes the mechanisms, catalytic action, etc. To produce compound mo- distribution of the macrocycle to change through biased Brownian motion. lecular machines capable of more advanced task performance than simple molecular machines, one can follow a similar strategy B Blocks/unblocks — O movement of ring between to that of making compound machines in the macroscopic world O tBu thread binding sites H HNN Me Si Me namely, connect the actions of simple molecular machines in ways O O H H O Ph N N N N Ph H O O Ph N NH HN Blocks/unblocks O O O movement of ring between O tBu thread binding sites H HNN Me Si Me O O H H O Ph N N N N 100 0 a) H+ Ph H O O Ph N b) TBDMSCl H H N N Switches relative affinities of thread binding sites O O 50 50 Unblocking the passage of the macrocycle allows the distribution of the macrocycle to move towards equilibrium through biased Brownian motion. Fig. 1. Simple molecular machine mechanisms. (A) Switching of the thermodynamically favored ring position in a molecular shuttle (25), a process used in numerous (1, 13–26) functional rotaxane switches. 85 15 B ( ) Blocking/unblocking of the ring movement between the 1. E-to-Z compartments of a rotaxane (30). Both actions result in biased t 2. -SiMe2 Bu Brownian motion of the ring along the track. However, note that the 3. +SiMe tBu A 2 consequence of the switching operation in (i.e., the change in the 4. Z-to-E distribution of the macrocycle) is undone by reversing the switch state, whereas the result of the unblocking action in B is not undone O by simply reattaching the blocking group. tBu O Me Si Me NNH H O (22), in controlled release delivery systems (23), for switchable O H H O Ph N N catalysts (24), and as “molecular muscles” (25, 26). However, to N N make molecular machines that can perform more complex tasks, it Ph H O O Ph N is necessary to integrate the dynamics of individual molecular NH HN machine components in a way that achieves more than just the O O sum of the respective parts. Compound Machines—From Switches to Ratchets Before the introduction of kinematic theory (27), scientists and 44 56 engineers considered there to be six different types of simple Fig. 2. A compound molecular machine (30). Note that the thread is mechanical machines (28). These are the three Archimedian structurally identical in both states of the machine shown; only the simple machines (29)—the lever, pulley, and screw—plus the distribution of the macrocycle differs. Combining (and synchronizing wheel-and-axle (including gears), inclined plane, and wedge. the operation of) a switch for the thermodynamically favored position of the macrocycle on the axle with the attachment/release of a Connecting “simple machines” in such a way that the output of blocking group enables the macrocycle distribution to be driven one provides the input for another can integrate their mechanisms away from its equilibrium value, a task that cannot be accomplished and produce “compound machines” capable of performing more by a simple machine process. 2of8 | www.pnas.org/cgi/doi/10.1073/pnas.1712788115 Zhang et al. Downloaded by guest on October 2, 2021 O tBu O HO 5 tBu Me Si Me Me Si Me O O H O O Ph N H N 1. Attach substrate Ph N H N O Ph O H OH Ph O O O-K+ O 6. Detach mechanically 5 interlocking auxiliary 2. Macrocyclization around auxiliary template site tBu O O O O Me Si Me tBu O O NN NN H H H H H Me Si Me Ph N O O N O H H Ph N Ph O O N O O 5 H O O Gate shut Ph O 5 H NH HN NH N O O O O 5. Blocking group 3. Blocking group attachment removal O O O O 4. Switch thermodynamically O OH H HNN H HNN H preferred site of ring on track Ph N O OH N O (here by changing solvent) H H Ph N Ph O O N O O 5 H Gate open O O Ph O 5 NH HN NH HN [D6]DMSO 100% CDCl 100% O O 3 O O O O H HNN O O Rotaxane without intercomponent O recognition elements NH HN O O Fig.
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