Stimulus-Responsive Plasmonic Chiral Signals of Gold Nanorods

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Stimulus-Responsive Plasmonic Chiral Signals of Gold Nanorods Organized on DNA Origami Qiao Jiang, Qing Liu, Yuefeng Shi, Zhen-Gang Wang, Pengfei Zhan, Jianbing Liu, Chao Liu, Hui Wang, Xinghua Shi, Li Zhang, Jiashu Sun, Baoquan Ding, and Minghua Liu Nano Lett., Just Accepted Manuscript • DOI: 10.1021/acs.nanolett.7b03946 • Publication Date (Web): 09 Oct 2017 Downloaded from http://pubs.acs.org on October 9, 2017

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Stimulus-Responsive Plasmonic Chiral Signals of Gold Nanorods Organized on DNA Origami Qiao Jiang, †‡+ Qing Liu, †#+ Yuefeng Shi, §+ Zhen-Gang Wang, † Pengfei Zhan, †# Jianbing Liu, † Chao Liu, † Hui Wang, † Xinghua Shi, † Li Zhang, ‡ Jiashu Sun, †#* Baoquan Ding†#* and Minghua Liu†‡* †

CAS Key Laboratory of Nanosystem and Hierarchical Fabrication, CAS Center for Excellence

in Nanoscience, National Center for Nanoscience and Technology, 11 BeiYiTiao, ZhongGuanCun, Beijing 100190, China ‡

CAS Key Laboratory of Colloid, Interface and Chemical, Thermodynamics, Institute of

Chemistry, Chinese Academy of Sciences, Zhongguancun North First Street 2, Beijing, 100190, China §

Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing

100190, China #

University of Chinese Academy of Sciences, Beijing 100049, China

ACS Paragon Plus Environment

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ABSTRACT: In response to environmental variations, living cells need to arrange the conformational changes of macromolecules to achieve the specific biofunctions. Inspired by natural

molecular

machines,

artificial

macromolecular

assemblies

with

controllable

nanostructures and environmentally responsive functions can be designed. By assembling macromolecular nanostructures with noble metal nanoparticles, environmental information could be significantly amplified and modulated by the assembled plasmonic nanostructures. However, manufacturing dynamic plasmonic nanostructures that are efficiently responsive to different stimuli is still a challenging task. Here we demonstrate a stimulus-responsive plasmonic nanosystem based on DNA origami-organized gold nanorods (GNRs). L-shaped GNR dimers were assembled on rhombus-shaped DNA origami templates. The geometry and chiral signals of the GNR nanoarchitectures respond to multiple stimuli, including glutathione reduction, restriction enzyme action, pH change or photo-irradiation. While the glutathione reduction or restriction enzyme caused irreversible changes in the plasmonic circular dichroism (CD) signals, both pH and light irradiation triggered reversible changes in the plasmonic CD. Our system transduces external stimuli into conformational changes and circular dichroism responses in near-infrared (NIR) wavelengths. By this approach, programmable optical reporters for essential biological signals can be fabricated.

KEYWORDS: stimulus-responsive, plasmonic chiral nanostructure, gold nanorod, DNA origami, self-assembly


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Stimulus-responsive macromolecular systems have evolved to play various essential roles in biological systems.1, 2 Living cells need to spatiotemporally manage the conformational changes of self-assembled biomolecules in response to environmental variations to achieve specific functions. Natural molecules, such as DNA, proteins and polysaccharides, exhibit a responsiveness strongly tied to their chiralities. When this property is detected by differential left- and right-handed circular dichroism (CD), the signals generally appear in the ultraviolet range, which is difficult to elucidate in a complex biological system. In contrast, some noble metal nanoparticles exhibit strong, localized plasmonic resonance absorption in visible and nearinfrared wavelengths.3-10 Interestingly, if biological molecules can be integrated with the plasmonic property of metal nanoparticles, the chiral information can be significantly amplified.10 Thus, the fabrication and modulation of the plasmonic CD of biological molecules become a popular topic. In particular, with intensive plasmonic CD in visible and NIR wavelengths, chiral plasmonic assemblies provide a unique starting point for the development of chirality-based biosensors. Self-assembled chiroplasmonic biosensors with strong optical activity, high sensitivity and low limits of detection have been reported.9, 10 Based on the socalled “DNA origami” technique, gold nanospheres and nanorods have been assembled onto predesigned binding sites, yielding sophisticated geometries with nanoscale precision.4-6, 11-14 By this means, asymmetric plasmonic assemblies, such as gold nanosphere helices,4, 5 nanosphere tetramers,6 crossed gold nanorods11,

12

and nanorod helical superstructures13,

14

have been

produced, all of which exhibit a tunable chiral response. Moreover, the inherent dynamics of DNA enables the regulation of conformational changes of the structured template, which can generate a triggered reconfiguration of the assembled plasmonic nanostructures and an in situ control over the chiral response.15-17 Strand displacement of DNA structures had been used as the


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driving forces.16 But this method will generate the accumulation of nucleic acid wastes and may affect the efficiency of multi-cycle operation.16 Photo-induced isomerization of azobenzeneanchored DNA molecules has been applied to the regulation of nanostructural reconfiguration.17 However, azo-modifications of DNA oligonucleotides involve covalent bonds, the formation of which is costly and requires tedious synthetic work.17 In addition, the operations of plasmonic systems in response to complex environmental stimuli, such as biological signals, have not yet been fully explored. Here, we describe a supramolecular approach to modulate DNA conformation and subsequent chiral plasmonic signals of gold nanorods (GNRs), which efficiently generates a nanostructure responsive to multiple stimuli. We fabricated the novel system by linking the edges of two triangular DNA origami structures to form a rhombus-shaped DNA origami template. The GNRs assembled into an L-shaped configuration on the template to create plasmonic nanoarchitectures that display chiroplasmonic signals. The nucleic acid linkages between the origami blocks were designed to be responsive to different stimuli, such as glutathione reduction, restriction enzyme activity, pH changes or photo irradiation, which can be common indicators of the biochemical environment. A configuration transformation of the L-shaped nanorods is triggered by these biological indicators, and can be in situ transduced into CD changes in the near-IR wavelength range. The construction of the plasmonic assemblies is schematically illustrated in Figure 1a. The design of the triangular DNA origami is based on Rothemund’s method.18 Controller strands (green) were carefully designed to link two triangular origami together to form the rhombusshaped template. Two groups of capture strands (red and blue) are extended from the template to organize the GNRs into plasmonic chiral nanosystem. Two triangular origami nanostructures (I and II) containing different capture strands were respectively assembled by slow annealing the


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M13mp18 genome DNA strand (scaffold), corresponding capture strands, controller and staple strands in a molar ratio of 1:10:10:10 from 95 °C to room temperature (the detailed structure design is presented in Scheme S1). Each side of the triangle-shaped origami was approximately 120 nm long (Figure. S1a). Assembled I and II were purified using filtration devices (100 kDa MWCO, Amicon, Millipore), to remove the excess short DNA strands, and subsequently mixed together. An annealing process (from 45 °C to 25 °C over the course of 2 h for 6 cycles) was performed to assemble the two triangular building blocks into the rhombus origami template (Figure. S1b-c). The controller strands (green) were designed to contain disulfide bonds or other functional DNA sequences, which enabled the conformation of the linking strand and the interorigami separation to respond to environmental stimuli, such as chemical reduction, pH change, enzyme activity or photo irradiation. Two groups of capture strands, marked in red and blue, were applied to opposite surfaces of the template and functioned as binding sites to assemble DNA-modified GNRs. The binding sites were arranged in an “L” configuration so that the assembled GNRs nanostructures display strong CD signals.11,

12, 16, 17

At each binding site,

capture strands with identical sequences were used to assemble each GNR. To avoid nonspecific binding, different sequences were used for the individual GNRs (denoted blue or red in the scheme). The salient addressability of DNA origami allows for the engineering of the structural handedness through precise control over the positions of the two GNRs in the structure. The purified DNA origami and GNRs functionalized with the respective complementary DNA strands were mixed and annealed by decreasing the temperature from 45 °C to 25 °C over the course of 2 h for 30 cycles. After DNA hybridization, the GNRs were organized at the desired binding sites on the DNA template.


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The annealed products were subsequently resolved and analyzed by agarose gel electrophoresis. The gel images of the plasmonic assemblies are shown in Figure S2 (the target bands are highlighted by a green dashed rectangle). The target products were then eluted from the agarose gel using filter columns (GE). Figure 1 displays the atomic force microscopy (AFM) images of the rhombus DNA templates (Figure 1b) and the transmission electron microscopy (TEM) images of the L-shaped nanorod structures (Figures 1c & S3-5), which were consistent with our design. It is noteworthy that in some structures the twisting angle between the two GNRs is not exactly 90°, which may have resulted from a deformation of the DNA origami template during the drying process on the TEM grids. The stimulus-responsive controller strands enable the rhombus structures of the templates and the nanorod assemblies to respond to various environmental changes. Disulfide bonds (-S-S-) were incorporated into DNA controller strands, which enable the controller strands to be cleavable in the presence of the reducing agent glutathione (GSH).19 GSH is a ubiquitous biological tripeptide with multiple biological functions and has even been utilized for therapeutic applications.19,

20

Intracellular GSH concentration is usually in the millimolar range, and the

tripeptide is in a much higher concentration in cancer cells. This unique feature of neoplastic cells can be exploited in the development of GSH-responsive systems for anticancer applications. When exposed to GSH, the disulfide bonds in the controller strands of the origami template are reduced to monothiols, resulting in the dissociation of the rhombus templates (Figure S6) and therefore the two GNRs (Figure 2a & S7). By agarose gel electrophoresis, we estimated the efficiency of the cleavage process (Figure 2b & S8). As shown in Figure 2b, the rhombus origami-GNR architecture, after GSH exposure (25 °C, 12 h) exhibited a more quickly migrating band in the gel, corresponding to triangle origami/GNR structures. At different GSH


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concentrations (0.1, 1, 5 mM), a gradual decrease in the intensity of the bands containing the Lshaped GNRs-origami complex was observed on the gel (Figure 2b), demonstrating a GSHinduced separation of the GNRs-assemblies. L-shaped nanorods dimer displayed a left-handed CD signal (Figure 2c). The characteristic bisignate peak-dip shape of the CD is due to the antisymmetric hybrid models of the near-field coupling between the two GNRs.

11, 12, 16, 17

The

conformational response of the plasmonic architecture to GSH was directly reflected in the chiroptical response. As the GSH concentration increased, the treated chiral assemblies exhibited weaker left-handed CD signals (Figure 2c, S9). A similar strategy was employed to design a plasmonic system sensitive to enzyme activity (Figure S10). The restriction endonuclease EcoRV specifically recognizes DNA substrates containing the nucleotide sequence GATATC and cleaves double-stranded DNA into blunt ended fragments. We incorporated EcoRV restriction sites into the controller strands (Figure S10). After incubation with EcoRV at 37 °C for 1 h, the rhombus origami structures separated due to enzyme-catalyzed cutting of the controller strands (Figure S10). The L-shaped GNR dimers likewise separated (Figure S11), leading to a decrease in the CD intensity (Figure S10).

We next designed a pH-sensitive plasmonic nanostructure by incorporating cytosine-rich imotif 21, 22 sequences into the controller strands (Figure 3a). i-motif DNA molecules are unfolded at neutral pH, while in slightly acidic conditions (pH < 6.5), the C-rich sequences can be stabilized by H+ and form quadruple helix structures. These unique features have been used in DNA-based molecular motor systems.21,

22

A specifically-designed complementary strand

(Figure 3a, pink) was introduced to form a duplex with the i-motif sequence so that the nanorods


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remained apart at neutral pH. Upon acidification of the system, the i-motif sequence-containing controller strands folded due to the presence of protons, and the pink complementary strands were released. Consequently, the two individual nanorods were pulled together, resulting in the formation of L-shaped nanorods dimer with smaller inter-rod distance. The corresponding TEM images are shown in Figure S12. The decreased inter-rod distance of chiral assemblies facilitate an increased left-handed CD signal. Upon decreasing the solution pH (from 8.5 to 4.5), the plasmonic CD signal intensity became enhanced (Figure 3b-c, S13) as the inter-rod distances decreased in the chiral plasmonic nanostructure. Figure 3c shows the cyclical changes in the CD intensity that result from pH-controlled stretching and folding of the plasmonic nanostructure. Reversibility of the chiroptical response is achieved because of the distant and adjacent states of the L-shape GNR dimer governed by DNA origami template configuration. The pH alteration is efficiently converted into conformational changes of the chiral GNR assemblies and can be monitored by CD spectroscopy. Reversible phenotypic adaptations enable living organisms to convert light energy into conformational changes for adjusting to local environmental changes.23 Inspired by photoreactive proteins and natural molecular machines, various artificial nanosensors designed for light-energy conversion and light-signal transduction have been developed.17, 24 Here, we altered the design of the plasmonic nanosystem to exhibit photo-regulation by incorporating telomere DNA sequences into the controller strands in combination with azobenzene moieties (Figure 4a). Telomere DNA sequences consist of simple GT-rich tandem repeats, and telomeric quadruplex repeats are generally conserved in eukaryotes.25 To equip the assembly with unique photochemical characteristics, we included the azobenzene moiety, which has widely been utilized as a photo-regulation molecule. 17, 26, 27 To elaborate, azobenzene derivatives are present


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in the DNA G-quadruplex-stabilizing trans form under visible light (Vis), whereas ultraviolet (UV) irradiation stimulates the formation of the cis form, leading to the disassociation of the DNA-Azo complex. 27 In our study, the azobenzene derivative (Azo) was synthesized27 (Figure S14) to regulate the conformation of the single-strand telomeric DNA (Figure S15) and, consequently, movement of the telomere DNA-controlled chiral GNR assemblies, by light irradiation. Nine single-stranded controller DNA-containing telomeric sequences were used to fabricate the rhombus DNA origami templates for GNR assembly, which were induced to form G-quadruplexes after incubation with the Azo molecules. Upon UV irradiation of the system, the telomere DNA sequence-containing controller strands stretched apart, resulting in the dissociation of Azo. This caused larger gap between the two individual nanorods, though the tiny morphological changes were not observed by TEM (Figure S16).The increased inter-rod distance of the L-shaped nanorod dimer dampened the left-handed CD signal (Figure 4b, S17) compared to that of the structure under visible light, where the chiral plasmonic architectures were stabilized by the trans form of Azo; as the distance of the two individual nanorods decreased upon G-quadruplex formation, the plasmonic CD signal intensity was enhanced (Figure 4b). To provide more insight of photo-regulated GNR nanostructures, numerical calculations were performed using a commercially available finite-difference time domain (FDTD) package Lumerical FDTD Solutions and the results are shown in Figure S18. The theoretical calculation results are in good agreement with the experimental observations. Figure 4c shows the cyclical changes in CD intensity that result from the photo-controlled stretching and folding of the photoregulative system. By alternating between UV and Vis illumination, the reversibility of the chiroptical response between the stretched and folded state of the L-shape GNR dimer controlled


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by telomere DNA became apparent. Thus, an electromagnetic “input” can be efficiently converted into a CD spectroscopy-observable, mechanical output of chiral GNR assemblies. In summary, we have constructed stimulus-responsive chiral plasmonic nanostructures by organizing GNRs into L-shaped configurations using rhombus-shaped DNA origami templates. The rhombus template was prepared by linking two triangular DNA origami nanostructures with rationally designed controller DNA sequences that react to biological signals. We incorporated GSH-sensitive chemical bonds, nuclease-sensitive DNA sequences, pH-sensitive sequences or photo-regulative molecular assemblies into the controller moiety, thereby providing variable elements to control the conformational transitions of the DNA origami nanostructures. Glutathione is crucial to the maintenance of cellular redox homeostasis, while cells must maintain differential pH values within their various compartments. Thus, the ability to monitor cellular GSH concentrations or subcellular pH are valuable in the investigation of cellular physiology and pathophysiology. Self-assembled chiral nanomaterials with intensive plasmonic CD signals exhibit high sensitivity and low limits of detection in bioanalysis.9, 10, 28, 29 Stimulated by the GSH reduction or environmental acidification, the conformations of our plasmonic nanostructures altered, inducing evidential changes in plasmonic CD signals, especially in the near IR range, which is considered a biological transparency window. Chiral plasmonic assemblies are therefore promising in situ probes for the detection of intracellular signals. Induced by the photo-sensitive azobenzene derivative, our G quadruplex-containing plasmonic assemblies demonstrated reversible molecular movement between stretched and folded states, directly converting light signals into a mechanical output. This light-driven DNA nanodevice could be applied to manipulate materials or collect information as a nanoscale unit that generates work through photo-regulation.


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The ability to modulate the plasmonic assemblies as optical probes can be used to enhance signal-to-noise ratios for imaging and sensing within highly complicated biological environments, such as within intact cells, to detect biomarkers or signal molecules.28, 29 Based on DNA nanotechnology, various DNA templates with different sizes, shapes and geometries can be used

to

assemble

three-dimensional

chiroplasmonic

nanostructures.30

Beyond

static

nanostructures, dynamic and stimuli-responsive chiral plasmonic systems are available, in which the chiral optical response can be controlled by external stimuli.30, 31 In response to biological signals, functional DNA motifs or other biological molecules can be integrated into the stimuliresponsive plasmonic nanosystem, advancing the development of intelligent probes for sensing micro-environmental changes or biological processes. Stimulated by biological molecules, e.g., nucleolin overexpression on the surface of tumor vascular endothelia,32 plasmonic nanosensors integrated with protein-recognizing features may generate responsive conformational changes to detectable chiroptical signals. Controlled by cellular pH, chiroplasmonic sensors modulated with pH-responsive and reconfiguring properties could produce active conformational changes and detectable chiroptical signals with spatial and temporal precision. Dynamic and stimuliresponsive chiralplasmonic systems could be further functinalized to recognize tumor-associated antigens, which may be applied in immune response monitoring or circulating tumor cells detection. Our strategy also holds promise for the construction of rationally designed plasmonic nanostructures with precisely controlled chirality, which may be exploited in customized optical signal modulators.


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Figure 1. Scheme for the preparation of stimulus-responsive chiral gold nanorod assemblies on DNA origami and characterization of the plasmonic L-shaped GNR nanostructures. (a) A single-stranded DNA scaffold (M13) hybridizes with staple and capture strands to form two different triangular DNA origami nanostructures (I and II). Controller strands (green), containing responsive sequences, were designed to assemble the two triangles along defined seams to form rhombus-shaped origami nanotemplates. Capture strand groups (red and blue) extending from the binding sites hybridize with the complementary strands on modified GNRs, resulting in organization of GNRs into a left-handed structure. (b) AFM images of the rhombus DNA origami performed in scan-in-fluid mode. Scale bar, 100 nm. (c) TEM image of the L-shaped GNRs nanostructure on the origami template after negative staining. Scale bar, 100 nm.


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Figure 2. GSH responsive GNR nanostructures. (a) Schematic illustration of the structural transformation of GNR-origami architectures. (b) Agarose gel analysis of the GNR-DNA origami complexes before and after GSH treatment (0.1 mM, 1 mM and 5 mM for 12h). (c) GSH concentration-dependent CD spectra of the GNR assemblies.


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Figure 3. pH-responsive GNR plasmonic nanostructures. (a) Schematic illustration of the pHresponse mechanism. The controller strands (green) is designed to contain i-motif sequence and form duplexes with the complementary strands (pink). The pH acidification results in the folding of the linker strand into i-motif, which results in smaller inter-nanorod separation. (b) The pHdependent CD response of the chiral GNR self-assembly. (b) The pH-dependent CD response of the chiral GNR self-assembly. (c) Relative CD intensity during alternative neutral condition and acidification in cycles. Error bars represent the mean ± s.d. of three independent experiments.


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Figure 4. Photo-regulation of GNR plasmonic nanostructures. (a) Schematic illustration of the photo-response mechanism. The controller strands (green) contain telomere DNA sequences and form a G-quadruplex with the photo-regulated azobenzene moiety (blue). Upon irradiation with UV light, the cis form of Azo disassociates from the telomere DNA controller strands and the folded G-quadruplex becomes stretched, resulting in a larger inter-nanorod separation. Upon illumination with visible light, the controller DNA re-folds into the G-quadruplex, aided by the trans form of Azo, leading to smaller inter-nanorod separation. (b) The photo-dependent CD response of the telomere DNA-controlled chiral GNR self-assembly. (c) The photo-dependent CD intensity under alternating UV and visible light. Error bars represent the mean ± s.d. of three independent experiments.


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ASSOCIATED CONTENT Supporting Information. Experimental section, extra figures and results. This material is available free of charge via the Internet at http://pubs.acs.org. AUTHOR INFORMATION Corresponding Author To whom correspondence should be addressed: Baoquan Ding, [email protected]; Jiashu Sun, [email protected]; Minghua Liu, [email protected] Author Contributions +These authors contributed equally. Notes The authors declare no competing financial interests. ACKNOWLEDGMENT This work was supported by the National Natural Science Foundations of China (21573051, 31700871, 21708004, 21273052), Science Fund for Creative Research Groups of the National Natural Science Foundation of China (21721002), National Basic Research Programs of China (2016YFA0201601),

Beijing

Municipal

Science

&

Technology

Commission

(No.

Z161100000116036), Key Research Program of Frontier Sciences, CAS (Grant No. QYZDBSSW-SLH029) and CAS Interdisciplinary Innovation Team.


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Stimulus-Responsive Plasmonic Chiral Signals of Gold Nanorods

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