Research Article

Reconfiguration of DNA molecular arrays driven by information relay

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Science  28 Jul 2017:
Vol. 357, Issue 6349, eaan3377
DOI: 10.1126/science.aan3377

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Relaying information on DNA tiles

Arrays of modular DNA units can relay information by transforming their internal shape in response to binding of DNA trigger strands. Song et al. synthesized rectangular arrays of double-stranded DNA (see the Perspective by Yang and Lin). Transient square configurations transform into two stable rectangular structures by pinching across a pair of opposing vertices. Binding of DNA trigger strands causes switching into the alternative stable configuration. The tiles thus create a cascade of transformations along a particular pathway, thereby transmitting information about where binding occurred.

Science, this issue p. eaan3377; see also p. 352

Structured Abstract

INTRODUCTION

Information relay at the molecular level is an essential phenomenon in numerous chemical and biological processes. A key challenge in synthetic molecular self-assembly is to construct artificial structures that imitate these complex dynamic behaviors in controllable systems. One promising route is DNA self-assembly, a potent approach for the design and construction of arbitrary-shaped artificial nanostructures with increasing complexity and precision. Nonetheless, despite recent progress in the construction of reconfigurable DNA nanostructures that undergo tailored postassembly transformations in response to different physical or chemical cues, the dynamic behaviors of massive, complex DNA structures remain limited. The existing systems typically exhibit relatively simple dynamic behaviors that involve a single step or a few steps of transformation. Moreover, many of these structures contain mainly static segments joined by a few small reconfigurable domains.

RATIONALE

Here, we demonstrated prescribed, long-range information relay in artificial molecular arrays assembled from modular DNA antijunction units. The small dynamic antijunction unit contains four DNA double-helix domains of equal length and four dynamic nicking points, and can switch between two stable conformations, through an intermediate open conformation. In an array, the driving force of information relay is base stacking: The conformational switch of one antijunction unit will cause the interface between the transformed unit and its neighboring units to become a high-energy conformation with weakened base stacking, leading to transformations in the neighboring units. The array transformation is equivalent to a molecular “domino array”: Once initiated at a few selected units, the transformation then propagates, without the addition of extra “trigger strands,” to neighboring units and eventually the entire array. The specific information pathways by which this transformation occurs can be controlled by adding trigger strands to specific units, or by altering the design of individual units, the connections between units, and the geometry of the array.

RESULTS

The reconfigurable DNA relay arrays were constructed by using both origami and single-strand–brick approaches. In one-pot assembly, we observed that the arrays built from antijunction units exhibited a spectrum of shapes to accommodate different combinations of antijunction conformations. With the incorporation of set strands, we could lock the arrays into prescribed conformations. The more set strands were added, the greater the assembly shifted toward the corresponding array conformation. Other factors, including the size and aspect ratio of an array, the connecting pattern of an array, DNA sequences of an array, cation concentration, and temperature, have been shown to affect the result of one-pot assembly.

The transformation cascade was demonstrated with preassembled arrays. When starting from one conformation, addition of the trigger strand at selected locations of the array initiates structural transformation from the selected sites and propagates to the rest of the array in a stepwise manner without additional trigger strands at other locations. Releasing the old trigger strands and adding new ones can transform the array back to its initial conformation—a reversible process that can be repeated multiple rounds. In addition, we were able to control the propagation pathway to follow prescribed routes, as well as to stop and then resume propagation by mechanically decoupling the antijunctions or introducing “block strands.” The kinetics of array transformation can be enhanced by elevated temperature or formamide. These assembly and transformations were studied mainly by atomic force microscopy and native agarose gel electrophoresis.

CONCLUSION

Our work demonstrates controlled, multistep, long-range transformation in DNA nanoarrays, assembled by interconnected modular dynamic units that can transfer their structural information to neighbors. The array’s dynamic behavior can be regulated by external factors, the shapes and sizes of arrays, the initiation of transformation at selected units, and the engineered information propagation pathways. We expect that the DNA relay arrays will shed new light on how to construct nanostructures with increasing size and complex dynamic behaviors, and may enable a range of applications, such as the construction of molecular devices to detect and translate molecular interactions to conformational changes in DNA structures, to remotely trigger subsequent molecular events.

Information relay in DNA “domino” nanoarrays.

In a manner similar to that of domino arrays (top), the molecular DNA nanoarray transforms in a step-by-step relay process, initiated by the hybridization of a trigger strand to a single unit (middle). Different stages of nanoarray transformation were confirmed by AFM (bottom). Scale bar, 50 nm.

Abstract

Information relay at the molecular level is an essential phenomenon in numerous chemical and biological processes, such as intricate signaling cascades. One key challenge in synthetic molecular self-assembly is to construct artificial structures that imitate these complex behaviors in controllable systems. We demonstrated prescribed, long-range information relay in an artificial molecular array assembled from modular DNA structural units. The dynamic DNA molecular array exhibits transformations with programmable initiation, propagation, and regulation. The transformation of the array can be initiated at selected units and then propagated, without addition of extra triggers, to neighboring units and eventually the entire array. The specific information pathways by which this transformation occurs can be controlled by altering the design of individual units and the arrays.

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