Controllable Covalent-Bound Nanoarchitectures from DNA Frames

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Controllable Covalent-bound Nano-Architectures from DNA Frames Zhiwei Lin, Yan Xiong, Shuting Xiang, and Oleg Gang J. Am. Chem. Soc., Just Accepted Manuscript • Publication Date (Web): 12 Apr 2019 Downloaded from http://pubs.acs.org on April 12, 2019

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Journal of the American Chemical Society

Controllable Covalent-bound Nano-Architectures from DNA Frames Zhiwei Lin1, Yan Xiong1, Shuting Xiang1, and Oleg Gang1,2,3* 1Department

of Chemical Engineering, Fu Foundation School of Engineering and Applied Science, Columbia University, New York, NY, 10027, USA 2Department of Applied Physics and Applied Mathematics, Fu Foundation School of Engineering and Applied Science, Columbia University, New York, NY, 10027, USA 3Center for Functional Nanomaterials, Energy & Photon Sciences Directorate, Brookhaven National Laboratory, Upton, NY, 11973, USA Supporting Information Placeholder ABSTRACT: Could one manipulate nanoscale building blocks using chemical reactions like molecular synthesis to yield new supra-nanoscale objects? The precise control over the final architecture might be challenging due to the size mismatch of molecularly-scaled reactive functional groups and nanoscale building blocks, which limits a control over the valence and specific locations of reaction spots. Taking advantage of programmable octahedral DNA frame, we report a facile approach of engineering chemical reactions between nanoscale building blocks toward formation of controlled nanoarchitectures. Azide and alkyne moieties were specifically anchored onto desired vertices of DNA frames, providing chemically reactive nano-constructs with directionally-defined valence. Akin to the conventional molecular reactions, the formation of a variety of nanoscale architectures was readily achieved upon mixing of the frames with the different reactive valence and at different stoichiometric ratios. This strategy may open a door for a programmable synthesis of suprananoscale structures with complex architectures and diversified functions.

The past decades have witnessed an explosion on the design and synthesis of nanoscale organic and inorganic building blocks,1 with distinctive composition, size, shape and functions.2 Although self-assembly approaches, typically relying on intricate balance of weak interactions or entropic effects,3 have been extensively explored for organizing nanoscale systems,4 it still remains challenging to develop a versatile approach that will be a parallel to supramolecular chemistry at the nanoscale. In recent years, it was a significant interest in establishing self-assembly methods that utilize building blocks with well-defined binding characteristics to control local coordination,5 and that opens possibilities for rational structure formation.5a, 5b However, it is advantageous to adapt approaches from organic synthesis, where both molecular geometry and chemical reactivity play roles in the molecular formation. For example, valence-controlled6 chemical reactions between nanoscale building blocks will allow for generating stable and well-defined architectures. This idea is conceptually simple yet challenging to realize since it is difficult to control simultaneously both valence of nanoscale objects and their chemical reactivity. From experimental point of view, there are two key challenges to operate reactions

between objects in nanometer scale: the precise decoration of nanoobjects with directional and chemically reactive functional groups, and the development of efficient and facile chemistry for establishing inter-object reaction. The recent development of DNA origami technology has enabled one to design arbitrary shape of DNA objects on demand,7 with prescribed surface chemistry8 and rich types of hierarchical organizations.9 The increasing demands of applying DNA objects for desired applications have stimulated researchers to develop methods for DNA origami stabilization,10 including covalent crosslinking10a and positively charged species protection.10c At the same time, for creating larger scale architectures and designed clusters, there is a need to establish methods for permanent covalent binding of DNA constructs. Here we demonstrate such a strategy using a copper-free click chemistry between azide and dibenzocyclooctyl (DBCO).11 The utilization of covalent bonding will expand our toolbox of conjugating DNA object entities beyond DNA hybridization. In contrast with noncovalent bonds, covalent bonds offer permanent ligation between DNA objects. The click reaction occurs upon mixing of compounds without the need for specific conditions (Figure 1a), providing a facile, efficient, and versatile method of conjugating molecules.12 It has been widely utilized in molecular-level ligation of DNA with other materials such as polymers,13 nanoparticles,14 and proteins,15 thus, it is advantageous to utilize this methodology for reactions between nanoscale objects. The combination of DNA origami and click chemistry may offer a versatile platform for engineering nanoscale building blocks through the control of directional chemical reactions. Using octahedral DNA frame as a model building block, we demonstrate the synthesis of various predefined types of nanoscale architectures by manipulating directional chemical reactions among them. This approach works by introducing click functional groups onto the intended vertices of octahedral DNA frame or the surface of gold nanoparticles (AuNPs). These clickable DNA frame or AuNPs can be readily and covalently conjugated together upon mixing by click reaction. Our approach effectively combines the structural programmability of DNA origami with the versatility of click chemistry, providing an alternative access of synthesizing targeted nanoscale architectures.

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To demonstrate the presented idea of building covalentbound architectures, we use an octahedral frame that provides up to 6-fold valence through its vertices. The frame is constructed by twelve six-helix bundles (with a bundle length of 28.6 nm).16 Distinctive single-stranded DNA (ssDNA) are placed at the vertex positions. By installing the clickable functional groups (azide or DBCO) at the end of ssDNA, we anchor up to four clickable functional groups at one desired vertex of octahedra to enhance the efficiency of reactions (Figure 1b); that defines the frame valence. Frames with specifically designed valence number (one, two and four) can be adapted (Figure 1c). By choosing objects with desired valence for click reaction, controlled architectures can be generated, including dimer, trimer, cross-shaped and polymerlike nanostructures. Moreover, extending this approach to AuNPs coating with clickable functional groups, the DNA frame-AuNPs conjugates with specific architectures can be fabricated.

clickable functional groups.16 All of the designed frame exhibit identical mobility to that of A0, indicating that incorporation of click functional groups does not interfere the folding of octahedral frame (Figure 2a). The gel-purified products were then examined by transmission electron microscopy (TEM) imaging, which unambiguously verified the designed architectures (Figure 2b and Figure S2). To illustrate the effectiveness of click reaction between DNA frames, we first studied the formation of the simplest nanostructures, a ligation of two frames (dimer). The click reaction was carried out by mixing upon the gel-purified A1 and B1 frames solution (typically, 100 µL of 4 nmol) in an equimolar ratio, followed by incubating at 45 °C for one week. The successful formation of dimers was verified by TEM (Figure 2c). When we altered the starting materials to A2 and B1 with a molar ratio of 1:3, the formation of intended nanostructures (BAB, trimer) consisting of three frames was observed (Figure 2d). We summarized the formation of resultant structures, as probed by TEM (Figures S3 and S4) in dimers (A1 + B1) and trimers (A2 +B1) reactions in two histograms (Figures 2f and 2g), respectively. The reaction products contain a 0.46 and 0.43 fraction of dimers and trimers, respectively. The construction of dimers and trimers were further verified by agarose gel electrophoresis (Figure S5), where desired bands belonging to dimers and trimers can be clearly identified. As a controlled experiment, neither dimers nor trimers were yielded in the mixed solution of A0 with either B1 or B2 (Figure S6). We also constructed cross-shaped nanostructures with a mass fraction of 0.12 (Figures 2e, 2h and Figure S7), by the association between A4 and B1 frames with an experimental 1:6 molar ratio. These results unambiguously indicate the successful formation of the designed architectures through reaction of clickable DNA frames, where a valence is key factor for architecture control.17

Figure 1. (a) Schematic illustration of copper-free azide-alkyne click reaction between azide (red) and dibenzocyclooctyl (DBCO, blue). (b) The designed octahedral DNA frame with an edge length of 28.6 nm. One vertex is zoomed to show the endon view of structure consisting of four six-helix bundles (6HB). One clickable functional group is placed on each bundle, and up to four functional groups are installed one each vertex. (c) The click reaction between azide- (Am) and DBCO-functionalized (Bn) octahedra with the designated valences for generating controlled architectures, such as dimer, trimer, cross-shape, and 1D polymer DNA frame, depending on the valence of Am and Bn. The design and fabrication of octahedral DNA frame are based on our previously reported procedures.16 Briefly, frames were constructed by folding a 7249-nucleotide-long M13 single-stranded DNA scaffold with 144 short staple oligonucleotides (see Supporting Information). The clickable functional groups were incorporated to the vertices of octahedral DNA frame through a hybridization of azide or DBCO end-capped staple oligonucleotides (see Figure S1 for detailed structure information) during the origami folding. The successful formation of octahedral DNA frame was first confirmed by agarose gel electrophoresis. We denote azidefunctionalized and DBCO-functionalized octahedra as Am and Bn, respectively, where m and n represent the number of vertices bearing reactive functional groups, and valence of the frame. Note that A0 presents an intact octahedral frame without

Figure 2. (a) Agarose gel electrophoresis of octahedral DNA frames (Am and Bn) with various valence, as indicated by m and


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Journal of the American Chemical Society n. (b) Typical TEM image of A1 frame. TEM images of assynthesized (c) dimers, (d) trimers, and (e) cross-shaped pentamer. Scale bar is 50 nm. Statistical histograms of resultant

structures in reaction of (f) A1+B1, (g) A2+B1, and (h) A4+B1, based on analysis of 303, 332, and 334 DNA frames, respectively.

Figure 3. (a) TEM images and their corresponding schematic models of octahedral chains obtained by click reaction between divalent A2 and B2 octahedra. Resulting oligomers contain two to six monomers. Scale bar =50 nm. (b) TEM image of long polymerchain of octahedra. (c) Zoom-in view of polymer-chain in selective area of (b). (d) Experimental (blue) and predicted (red) statistical histogram of resultant structures achieved by the click reaction of A2 + B2, where blue numbers indicate experimental mass fraction. Experimental histogram is built based on statistical analysis of 606 DNA frames. We note that the reaction efficiency of nanoscale DNA frames is lower than that for molecules. Potentially, three reasons can contribute to this difference. First, the concentration of DNA frames for reaction is significantly lower (nanomolar range) than for molecular systems (micromole to millimole).11b Second, the translational and rotational diffusions of DNA frame is much slower than that of molecules.18 Moreover, an appropriate orientation of vertex between two frames is required to allow for a reaction (see Figure S8 and additional discussion). Thus, the combination of dilute concentration, slow diffusion and nanoscale entropic constraints affect the efficiency of DNA frame reactions. In pursuit of step polymerization reaction for generating one-dimensional (1D) chains of octahedra, we selected A2 and B2 as bi-functional monomer units. Identical amount (100 µL of 4 nmol) of A2 and B2 octahedral monomers were mixed for polymerization. After incubating for two weeks, the morphologies of resultant nanostructures were visualized directly by TEM. Representative morphologies, as shown in the Figure 3a, such as dimers, trimers, tetramers, pentamers and hexamers were generally collected. At the same time, the long polymer chain-like structures can also be observed (Figure S9). Remarkably, the longest polymer chain observed contains more than 30 octahedral monomers (Figures 3b and 3c). Based on the statistical analysis of TEM observed 606 octahedral frames (Figures S10 and S11), we built a population histogram summarizing the distribution for all resultant architectures (Figure 3d, blue column). It reveals that the fraction of converted monomers is 0.68, where oligomers with 2 to 6 octahedra and polymer chains longer than 6 octahedra are 0.57 and 0.11, respectively. A remaining fraction of unreacted monomers is 0.32. Next, we evaluated a character of this reaction based on the measured histogram. The theoretical mass fraction in step polymerization of bi-functional system can be expressed as,19

𝑀𝑛 = 𝑛(1 ― 𝑝)2𝑝𝑛 ― 1 where Mn is mass fraction, n is the degree of polymerization, p is the conversion of monomer. Based on this expression, we estimated a predicted histogram using p= 0.68 (Figure 3d, red column). A comparison between the experimental data and the estimation demonstrates an excellent match, which indicates a classic step-polymerization character of the divalent frames reaction .

Figure 4. (a) Schematic illustration of the synthesis of DNA frame and AuNP conjugate. (b) TEM image of dimer conjugates consisting of one DNA frame and one 10nm AuNP. (c) Zoom-in TEM image in the selective area of (b). (d) Statistical histogram for the yield of dimer AuNP-frame conjugate, based on the statistical analysis of 268 DNA frames. Scale bar: 50 nm. Finally, we demonstrate the versatility of developed strategy toward the realization of DNA frame-AuNP conjugates. This was implemented by reacting the azide groups coated AuNP (AuNP-N3) with the DBCO-functionalized frames, as illustrated



in Figure 4a. AuNP-N3 were prepared by hybridizing azide endcapped ssDNA with their complementary strands functionalized AuNPs. Three folds of 10 nm AuNP-N3 and B1 frame (100 µL of 4 nmol for frames) were mixed and incubated at 45 °C for one week. The intended conjugates consisting of one AuNP and one DNA frame were observed (Figures 4b and 4c). On the basis of statistical analysis of 268 DNA frames, the conjugation yield is 0.43, while the rest of frames remain intact (Figure 4d and Figure S12). Using the same strategy, we also constructed the conjugates of 20 nm AuNP with multiple DNA frames by saturating DNA frames in the reaction (molar ratio of DNA frame/AuNP=8/1). Conjugates attaching up to three DNA frames were produced (Figure S13) due to the increase of particle surface. In summary, we have developed a facile approach to manipulate the reaction between nanoscale building blocks with well-defined valence, analogous to reactions between molecular moieties. Diverse nanoscale architectures, including dimer, trimer, cross-shape, 1D polymer-chain of DNA frame as well as DNA frame-AuNPs conjugates have been synthesized. DNA building blocks with well-defined valence and reactivity through incorporation of click chemistry molecular agents offer a new platform for engineering and generating structurally defined and covalently bound nano-architectures.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website, and includes the design, fabrication and purification of DNA frame, experimental details, additional results and discussion.

AUTHOR INFORMATION Corresponding Author Oleg Gang: [email protected] ORCID Zhiwei Lin: 0000-0001-9194-1145 Oleg Gang: 0000-0001-5534-3121 Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT Acknowledgement: Research was supported by the US Department of Energy, Office of Basic Energy Sciences, Division of Materials Sciences and Engineering under grant DESC0008772.

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Controllable Covalent-Bound Nanoarchitectures from DNA Frames

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