A pH-operated triplex DNA device on MoS2 nanosheets - Langmuir

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A pH-operated triplex DNA device on MoS2 nanosheets Wei Ji, Dan Li, Wei Lai, Xiaowei Yao, Md. Fazle Alam, Weijia Zhang, Hao Pei, Li Li, and Arun Richard Chandrasekaran Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b04272 • Publication Date (Web): 16 Mar 2019 Downloaded from http://pubs.acs.org on March 18, 2019

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A pH-operated triplex DNA device on MoS2 nanosheets

Wei Ji1, Dan Li1, Wei Lai1, Xiaowei Yao1, Md. Fazle Alam1, Weijia Zhang2, Hao Pei1, Li Li1,* and Arun Richard Chandrasekaran3,*

1Shanghai

Key Laboratory of Green Chemistry and Chemical Processes, School of Chemistry

and Molecular Engineering, East China Normal University, 500 Dongchuan Road, Shanghai, 200241, P. R. China. 2Institutes

of Biomedical Sciences and Zhongshan Hospital, Fudan University, Shanghai 200032,

P. R. China. 3The

RNA Institute, University at Albany, State University of New York, Albany, New York 12222,

USA. *Corresponding authors: [email protected] (L.L.) or [email protected] (A.R.C.)

ACS Paragon Plus Environment

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Abstract

We report a triplex-based DNA device coupled with molybdenum disulfide (MoS2) nanosheets for use as a pH sensing platform. The device transitions from a duplex state at pH 8 to a triplex state at pH 5. The interaction of the device with MoS2 nanosheets in the two states is read out as a fluorescence signal from a pH-insensitive dye attached on the device. We characterized the operation of the DNA device on MoS2 nanosheets, analyzed the pH response and tested reversibility of the system. Our strategy can lead to the creation of a suite of biosensors where the sensing element is a triplex DNA device and the signal response is modulated by inorganic nanomaterials.


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In Tolkien's fantasies The Hobbit and Lord of the Rings, Bilbo Baggins wields a sword that glows blue when orcs or goblins are within proximity, alerting them to imminent danger. Just like the glowing blade, scientists have used fluorescent DNA nanostructures as biosensors to detect small molecules, metal ions, nucleic acids and antigens [1-6]. These structures are dynamic devices and machines that contain reconfigurable parts made of DNA [7-10]. One class of such reconfigurable structures are DNA triplexes, featured prominently in DNA nanotechnology in the past few years [11]. While DNA based motifs and tiles are the essential building blocks of nanoscale construction [12], triplex forming oligonucleotides (TFOs) are often used as appendages that provide additional functionality to these assemblies. TFOs enable postassembly modification [13], reinforce stability of nanostructures [14-15], allow sequence-specific recognition [16], direct site-specific interactions [17-18] and guide chemical reactions [19]. Most importantly, they allow pH-sensitive conformational changes between duplex and triplex states [20]. Here we use a triplex-based DNA device that responds to pH, in combination with molybdenum disulfide (MoS2) nanosheets to demonstrate its potential use as a pH sensing platform.

Two-dimensional transition-metal dichalcogenides such as MoS2 are being tested as alternatives to graphene due to their higher conductivity, increased optical properties, and a higher bandgap [21]. The interaction of graphene with nucleic acids is thoroughly characterized [22-23], and the material is widely in biosensing strategies [24-25]. Scientists now use MoS2 nanosheets in the development of biosensors because, similar to graphene, they adsorb single-stranded DNA molecules via noncovalent forces [26-28]. By attaching a fluorophore on a DNA strand, its interaction with MoS2 nanosheets can be monitored as the fluorescence of the dye is quenched upon adsorption of the single strand on the MoS2 surface (Figure 1a). To be used for biosensing, the single stranded probes are designed to be removed from the surface of the MoS2 nanosheet on recognizing a particular stimuli, resulting in the recovery of quenched fluorescence. To cause


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this event, we use a DNA device that can change conformations in response to changes in the pH of the medium.

Figure 1. Concept and design of a DNA device on two-dimensional MoS2 nanosheets for pH detection. (a) MoS2 nanosheets adsorb single stranded DNA and quench the fluorescence of the attached dye. (b) A DNA device consisting of double stranded and single stranded domains. At pH 5, the single stranded region binds to the duplex region via Hoogsteen base pairing to form an intermolecular triple helix. (c) Our strategy combines the concepts of single strand adsorption by MoS2 and DNA duplex-triplex transition. At pH 8, the DNA device is adsorbed on the MoS2 nanosheets via single stranded tail resulting in quenched fluorescence (left). On changing to pH 5, the device reconfigures to the triplex state, moving the single strand (and the fluorophore) away from the MoS2 surface, resulting in increased fluorescence (right).


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Our DNA device consists of two strands that form a partial duplex (Figure 1b). The remnant single stranded region is designed to contain a TFO sequence that can form a triplex with the duplex region via formation of TAT and C+GC Hoogsteen base pairs. Formation of C+GC triplets requires protonation of the cytosine residues and are only stable at acidic pH [29]. Thus, at pH 8, triplex association is weakened and the TFO dissociates from the duplex region, reversing to the duplex state with a single stranded extension. We combined these two concepts and designed a fluorophore-tagged triplex DNA device that provides a pH-specific readout by its interaction with MoS2 nanosheets (Figure 1c). We used a pH-insensitive dye (rhodamine green) so that fluorescence changes occur only due to transitions of the DNA device at different pH values. At pH 8, the device is in its duplex state and the single-stranded extension is adsorbed on the MoS2 surface, thus quenching the fluorescence of the device. At pH 5, the TFO binds to the duplex domain of the device forming a triplex. This transition moves the dye away from the MoS2 surface, resulting in fluorescence recovery.

First, we tested our device with the MoS2 nanosheets for its quenching efficiency (Figure 2a). Addition of MoS2 nanosheets to the device (at pH 8) quenches its fluorescence to < 5%. We then tested the performance of the device on MoS2 nanosheets at two different pH values. Without MoS2 nanosheets, there is minimal difference in the signal of the device at pH 5 and pH 8 (triplex and duplex, respectively) (Figure 2b). However, in the presence of MoS2, the duplex state of the device (at pH 8) shows a much reduced signal in comparison to the triplex state of the device (at pH 5). In its duplex state, the partial single strand of the device is adsorbed on to the surface of MoS2 nanosheets, thus causing diminished fluorescence. Reconfiguration of the device from the duplex to the triplex state causes the fluorescent signal to increase as the single stranded extension becomes a part of the triplex and is unavailable to MoS2 nanosheets (Figure 2b).


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We then tested the quenching efficiency as a function of MoS2 concentration. We incubated the DNA device with different concentrations of MoS2 nanosheets and analyzed the fluorescence quenching at each concentration (Figure 2c). At pH 8, higher concentrations of MoS2 nanosheets significantly reduced the fluorescence of the device due to adsorption of the fluorophore-tagged single strand to the MoS2 nanosheet. At pH5, quenching was not as pronounced since the device was in the triplex state and released from the MoS2 surface. We used the differential signal of the device on MoS2 nanosheets as an indicator of pH change (Figure 2d).

Figure 2. Characterization of the biosensing platform. (a) Fluorescence quenching efficiency of MoS2 nanosheets on the DNA device. (b) Fluorescence profile of DNA device with and without MoS2 nanosheets at pH 5 and 8. (c) Effect of concentration of MoS2 nanosheets on fluorescence intensity at pH 5 and 8. (d) Differential fluorescence intensity between the device at pH 5 and pH 8, indicating the response of the biosensing platform to changes in the pH.


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We then studied the analysis range of our biosensing platform. The response of the DNA device to pH in turn affects it’s interaction with the MoS2 surface, which is read out as a fluorescence signal (Figure 3a). The signal of the platform at different pH values shows that the resolution of this strategy as a pH sensing tool is high between pH 5 and pH 10 (Figure 3b). Finally, we tested the reversibility of the platform between pH 5 and pH 8 (Figure 3c). We changed the pH of the device/MoS2 platform and found that the transition of the device from its duplex state (pH 8) to triplex state (pH 5) can be repeatedly reversed for multiple cycles.

Figure 3. pH response of the device. (a) Fluorescence spectra and (b) corresponding fluorescence intensities of the device at different pH. (c) Reversibility of the triplex-based pH sensor between pH 5 and pH 8.

Among other applications such as biomolecular analysis [30], photonics [31] and molecular computation [32], dynamic DNA nanostructures are used in point-of-care and in vivo biosensing. In this study, we evaluated the performance of a triplex DNA-based pH sensor that provides a fluorescent readout when coupled with MoS2 nanosheets. While there are previous reports on DNA devices that transition between duplex and triplex states, this is the first study that combines DNA triplexes and MoS2 nanosheets, demonstrating the application of such an interaction in pH sensing. Previous studies have used graphene oxide for this purpose [33], and our study adds to the list of materials that are compatible as pH sensing platforms when combined with DNA


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nanostructures. Given the relative success of using MoS2 nanosheets in drug delivery [34], our platform has the potential to be extended for pH sensing in vivo. The pH range at which our device operates is pH 5 to pH 10. This strategy could be modified to be more responsive to smaller changes in pH by altering the content of C+GC/ TAT triplets in the sequence [35]. In this study, the device undergoes a structural transition in response to pH, causing a signal change on interacting with MoS2 nanosheets. Triplex-based DNA devices are not only limited to pH sensing; their response can be controlled by triplex binders [36], metal ions [37] or small molecules [38]. Further, triplex-based DNA strand displacement [39] can also be incorporated into such devices to provide stimulated responses [40]. Thus, our strategy can lead to the creation of a suite of biosensors where the sensing element is a triplex DNA device and the signal response is modulated by MoS2 nanosheets.

Experimental procedures Materials Tris (hydroxymethyl) aminomethane, magnesium chloride, hydrochloric acid and sodium hydroxide were purchased from Sinopharm Chemical Reagent Co. Ltd. All chemicals were of analytical grade. Monolayer molybdenum disulfide (MoS2) powder was supplied by Nanjing XFNANO Materials Tech Co. Ltd. and suspended in deionized water prior to use. Size distribution of the MoS2 nanosheets as provided by the company indicated a range of 65.5  39.2 nm.

Oligonucleotides were bought from TaKaRa Biotechnology (Dalian) Co. Ltd. and purified with high-performance liquid chromatography. The triplex DNA device is composed of two DNA strands (S1 and S2), in which S1 is labeled with rhodamine green (pH insensitive) at the 3' end. S1: 5'-CTCCTCTTCCTTCTCTGTACATCTCTTCCTTCTCC-Rhodamine Green-3' S2: 5'-AGAGAAGGAAGAGGAG-3'


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Assembly of triplex DNA device Strands S1 and S2 were mixed at equimolar concentrations (5 µM) in Tris buffer (10 mM Tris buffer, 10 mM MgCl2) and annealed in a thermocycler (LongGene A300 fast thermal cycler) from 95 °C to room temperature over a period of 2 h.

Fluorescence measurements of triplex DNA formation Different concentrations of MoS2 nanosheets (0 to 500 µg/mL) was dispersed in 500 µL Tris buffer containing a final concentration of 50 nM triplex DNA device at pH 5 or pH 8. Thereafter, the fluorescence of the samples was monitored by fluorophotometer (Hitachi F-7000). Excitation wavelength was fixed at 503 (±5) nm and emission spectra were collected from 500 to 650 nm with a wavelength step of 2 nm/s. Fluorescence intensity at 530 nm was used for analysis. The adsorption capacity of the nanosheets are given by the slopes of the curves [21]. We calculated the loading capacity of triplex DNA and duplex DNA to be 366.4 and 235.2 (DNA per nanosheet) respectively.

pH range validation MoS2 (400 µg/mL) was dispersed in 500 µL Tris buffer containing a final concentration of 50 nM triplex DNA device at different pH values (pH 4 to pH 12). Following this, the fluorescence of mixed samples was determined using the fluorophotometer. pH-dependent fluorescence curves were obtained from the fluorescence intensities at 530 nm.

Reversibility of the DNA device The cyclic fluorescence experiment was conducted using a fixed concentration of the triplex DNA device (50 nM) in 500 µL Tris buffer with 400 µg/mL of MoS2 at pH 5 in a volume-stirred cuvette, monitoring the fluorescence signal corresponding to the device in the triplex state. Subsequently,


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the pH of the solution was cyclically changed between pH 8 and pH 5 by addition of small aliquots of 3 M NaOH or 3 M HCl.

Acknowledgment This work was supported by Shanghai Science and Technology Committee (STCSM) (Grant No. 18490740500 to L. L.) and the National Science Foundation of China (Grant No. 21722502 to H. P.). L. L. also acknowledges the financial support from the “1000 Youth Talents Plan”. We thank Dr. B. R. Madhanagopal for critical comments on the manuscript.

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Figure 3 203x63mm (300 x 300 DPI)


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A pH-operated triplex DNA device on MoS2 nanosheets - Langmuir

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