Controlled Self-Assembly of λ‑DNA Networks with the SynergisticEffect of a DC Electric FieldMingyan Gao,†,‡ Jing Hu,†,‡ Ying Wang,†,‡ Mengnan Liu,†,‡ Jianfei Wang,†,‡ Zhengxun Song,†,‡

Hongmei Xu,†,‡ Cuihua Hu,*,†,‡ and Zuobin Wang*,†,‡,§

†Ministry of Education Key Laboratory for Cross-Scale Micro and Nano Manufacturing, Changchun University of Science andTechnology, Changchun 130022, China‡International Research Centre for Nano Handling and Manufacturing of China, Changchun University of Science and Technology,Changchun 130022, China§JR3CN & IRAC, University of Bedfordshire, Luton LU1 3JU, U.K.

*S Supporting Information

ABSTRACT: Large-scale and morphologically controlled self-assembled λ-DNAnetworks were successfully constructed by the synergistic effect of a DC electric field.The effect of DNA concentration, direction, and intensity of the electric field, even themodification of the mica surface using Mg2+ on the characteristics of the as-preparedDNA networks, were investigated in detail by atomic force microscopy (AFM). It wasfound that the horizontal electric field was more advantageous to the formation ofDNA networks with more regular structures. At the same concentration, the height ofDNA network was not affected significantly by the intensity change of the horizontalelectric field. The modification of Mg2+ on mica surface increased the aggregation ofDNA molecules, which contributed to the morphological change of the DNAnetworks. Furthermore, DNA molecules were obviously stretched in both horizontaland vertical electric fields at low DNA concentrations.

■ INTRODUCTION

As a promising biomolecule, DNA not only plays anindisputable role in life science and bioengineering, but alsoattracts extensive attention in the field of nanotechnology.1

The intrinsic ability of DNA to arrange itself has promoted thestudies of surface assembly properties of DNA molecules.2

Self-assembly enables DNA molecules to be combined intocomplex structures in a relatively simple step, thus providingremarkably flexible way in the design of various molecularpatterns,3−9 which have potential applications in medicine andengineering as molecular functional devices,10−14 DNA-basedelectrochemical biosensors,15 or act as a scaffold to constructnanostructures,16 such as nanoparticles,17−20 nanorods,21−23

nanowires,24−26 and two-dimensional nanoparticle networks.27

However, it is still a challenge to realize the controllableassembly of DNA molecules into highly oriented interlacedpatterns on a large scale, which thus makes it an obstacle fortheir future application in nanotechnology.Over the past few decades, research into exploring simple

and effective methods for controllable DNA self-assembly hasnever ceased. Among them, the preparation and formationmechanism of DNA self-assembled networks with unique two-dimensional and even three-dimensional structures on a solidsurface have attracted wide attention. DNA networks formedby self-assembly on solid surfaces were generally prepared byfacial deposition method using DNA solution with relativelyhigh concentration. The density, height, and coverage of DNA

networks were usually regulated as reported by adjusting theconcentration of DNA solution, deposition time, and the typeof substrates including mica,28,29 silicon,30 gold,31 or othermaterials.32,33 In addition, whether the surface was modified ornot by salt cations was also a neglectable factor for thefabrication of regular networks.34,35 Nevertheless, althoughlarge-scale two-dimensional DNA networks could be obtainedthrough the methods above, there are still restrictions in thestructural diversity of the prepared DNA networks. Further-more, it has been proved that DNA molecules exhibit atendency of movement36 and stretching37 under electric fields;however, the self-assembly of DNA molecules into specificpatterns under an electric field has rarely been reported.In this work, a series of large-scale and morphologically

controlled self-assembled λ-DNA networks were successfullyfabricated by the synergistic effect of DC electric field. Thedirection of the DC electric field was divided into horizontalelectric field (HEF) and vertical electric field (VEF), and theintensity of the electric field was simply adjusted by changingthe voltage. Different influencing factors including the DNAconcentration, direction, and intensity of the electric field, andeven the modification using Mg2+ for the mica surface wereinvestigated by atomic force microscopy (AFM) in detail on

Received: September 19, 2019Revised: October 12, 2019Published: November 4, 2019

Article

pubs.acs.org/JPCBCite This: J. Phys. Chem. B 2019, 123, 9809−9818

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the morphology of the as-prepared DNA networks. Theobtained information will promote the understanding on thepreparation of controllable self-assembled λ-DNA networksand the application of DNA networks.

■ EXPERIMENTAL SECTIONMaterials. All chemicals were used as received without

purification throughout the study. λ-DNA (48502 bp) waspurchased from Thermo Fisher Scientific Company (China).MgCl2·6H2O was obtained from Beijing Chemical Works(China). Ultrapure water used during the experiments (≥18.2MΩ cm) was purified with a Milli-Q water purification system.The 1.0 × 1.0 cm2

fluorphlogopite (KMg3(AlSi3O10)F2) micasquare pieces were purchased from Taiyuan FluorphlogopiteMica Company (China). The mica used before the subsequentexperiments was freshly cleaved.

DNA Solution Preparation. The 500 ng/μL stocksolution of λ-DNA was diluted to different concentrationswith ultrapure water to concentrations of 1, 5, and 10 ng/μLfor sample preparations.

DNA Sample Preparation under DC Electric Fields. Inorder to investigate the effect of electric field direction on theformation of DNA samples in detail, two forms of electric fieldsincluding the horizontal electric field (HEF) and the verticalelectric field (VEF) were prepared respectively as shown inFigure 1. Herein, the E363A instrument from the KeysightTechnologies Company (USA) was used as the DC electricsource. A pair of indium−tin oxide (ITO) glasses (2.0 × 2.0cm2, 100 Ω/cm2) with the ITO layer thickness of 230 Å ± 50Å were used as the electrodes. The examined distancesbetween the two electrodes of the horizontal and verticalelectric fields were 10 mm and 2 mm, respectively, and the

Figure 1. Schematic drawing for the preparation of DNA samples under horizontal (a) and vertical (b) electric fields.

Figure 2. Typical AFM images (upper part) and height profiles (lower part) of DNA on the bare mica prepared with the different concentrations ofDNA solution: 1 (a), 5 (b), and 10 ng/μL (c).

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mica was placed between the electrodes. After applying the DCvoltage for a few seconds, 3 μL of DNA solution was droppedonto the center of mica surface and the DC voltage was thenkept on for 7 min. Ultimately, the sample was dried in air andprepared for AFM imaging.To figure out the effect of Mg2+ on the deposition of DNA

under the DC electric field, a Mg2+-modified mica surface wasprepared as follows. The 10 mM MgCl2 aqueous solution wasprepared by dissolving 0.2033 g of MgCl2·6H2O into 100 mLof ultrapure water. Then a droplet of the MgCl2 aqueoussolution (2.5 μL) was dropped onto a freshly cleaved micasurface and allowed to spread out. After the sample was leftalone for 3 min, the mica was rinsed with ultrapure water andblown dry with compressed air before dropping the DNAsolution. The Drop Shape Analyzer-DSA100 (Germany) wasutilized to analyze the contact angle of the mica before andafter Mg2+ modifications.In a control experiment, the DNA samples adsorbed on bare

and Mg2+-modified mica surfaces without DC electric fieldswere also prepared according to the same procedures,respectively, as mentioned above.It should be noted that for the vertical electric field, although

not shown in this figure, the downward direction of the electricfield was also examined in this experiment.Atomic Force Microscopy Measurements. The AFM

experiments were carried out using the Agilent 5500 scanningprobe microscope (SPM) from Agilent Technologies Com-pany (USA). The AFM images were acquired in tapping modeusing Tap300Al-G AFM probes (spring constant, 40 N/m)below the resonant frequency (typically, 200−400 kHz) underambient conditions at room temperature.

■ RESULTS AND DISCUSSION

As a control experiment in subsequent studies of DNAdeposition under electric fields, various concentrations of DNAdeposited on bare mica without any electric field wereprepared. It should be noted that all the AFM images usedin this paper were typical of those obtained from at least fiveseparated samples. It was clear to see the changes of DNAmolecular assembly due to the increase of concentration asshown in Figure 2. In the low DNA concentration of 1 ng/μL(Figure 2a), the DNA molecules dispersed irregularly withslight intermolecular entanglement. When the DNA concen-tration increased to 5 ng/μL (Figure 2b), the interconnectiondegree between DNA molecules increased, which led to thetendency of forming a DNA molecular network. Nevertheless,at this moment, the size of meshes was still large andnonuniform with prominent knots, and the end of the freeDNA chain could be seen at the edge of the mesh. When theconcentration of DNA reached 10 ng/μL as shown in Figure2c, an almost complete DNA network with approximatepolygonal meshes appeared in the whole field of vision. TheDNA network meshes became more uniform and smaller insize, clearer in edge without redundant bifurcation. Since thesingle chain height of double stranded DNA (dsDNA)measured by AFM in air was reported to be about 0.5 nm,39

the fibers of the DNA network were measured to bepredominantly 8−16 dsDNA high according to the heightprofile corresponded with the AFM image, which was higherthan the DNA fibers in Figure 2a and Figure 2b. Therefore, thefibers in a DNA network might be DNA bundles formed byoverlapping or interlacing multiple dsDNA chains.40

Figure 3 shows the deposition of 1 ng/μL DNA on the baremica surface under horizontal electric fields. In the experi-ments, the electric fields were parallel to the mica surface at

Figure 3. Typical AFM images (the first column), local amplification images (the second column) and the corresponding 3D topographic maps(the third column) of 1 ng/μL DNA on the bare mica produced under the different HEF DC voltages: 0.5 (a), 1.0 (b), and 2.0 V (c). (Note: Theblue dotted arrow on the 3D topographic maps represents the direction of the horizontal electric field.) The fourth column is the height profiles ofthe transversal section marked with the white dashed line in the local amplification images.

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different voltages. Herein, the positive and negative electrodeswere noted as + and − , respectively. The middle part betweenthe positive and negative electrodes was selected to obtain theAFM images. Compared with the case without applying the

electric field (Figure 2a), at the same concentration of DNAsolution, the number of DNA fibers in the field of visionincreased significantly even at a low voltage of 0.5 V as shownin Figure 3a. In addition, the strands of DNA molecules

Figure 4. Typical AFM images (the first column), local amplification images (the second column), and the corresponding 3D topographic maps(the third column) of 10 ng/μL DNA on the bare mica produced under the different HEF DC voltages: 0.5 (a), 1.0 (b), 1.5 (c), 2.0 (d), and 5.0 V(e). (Note: The blue dotted arrow on the 3D topographic maps represents the direction of the horizontal electric field.) The fourth column is theheight profiles of the transversal section marked with the white dashed line in the local amplification images. (f−j) Corresponding Fouriertransform images of parts a−e, the first column typical AFM images.

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partially contacted and twined around each other to form thenetwork, which was relatively relaxed and roughly extendedalong the direction of the horizontal electric field. This mightbe attributed to the fact that the electric field force increasedthe contact and crossover opportunities of the initially free-distributed DNA molecules in the solution and extended thenetwork in a certain direction. At the voltage of 1.0 V (Figure3b), the density of DNA fibers in the field of vision decreasedand the extension degree of the DNA molecules increased.Moreover, the extension direction of the whole fibers wasdeflected for a certain angle in comparison with that of Figure3a. When the voltage increased to a higher value of 2.0 V(Figure 3c), the DNA molecules were further stretched, wherethe arranged direction of DNA fibers was identical andregularly deviated for a larger angle. Moreover, it wasinteresting that the increase of electric field intensity did notcause significant changes in the height of DNA fibers.Since the concentration of DNA solution was confirmed to

be a crucial factor of forming the DNA network41 and thehorizontal electric field force did affect the deposition of DNAmolecules from the above results, the self-assembly rule ofDNA with higher concentration (10 ng/μL) under thehorizontal electric field at different voltages was furtherinvestigated as shown in Figure 4. The selection of the AFMimaging region was the same as that of Figure 3. When theconcentration of DNA increased, the DNA molecules wereassembled into arrays completely different from those in Figure3a under the same voltage of electric field as shown in Figure4a. The arrays assembled was herringbone-like with forked tailsand oriented toward the same direction, which was almostperpendicular to the direction of electric field. The periodicityof the arrangement was obviously reflected by the bright linespassing through the central point in the Fourier transformimage. In addition to the alteration of arrangement, anotherobvious phenomenon was that the width of the herringbonefibers assembled by DNA molecules increased withoutsignificant change of the height. This might be due to theDNA bundles overlapped or intertwined with multiple dsDNAchains horizontally accumulated into wider rather than thickerfibers under the horizontal electric field, which could also beobserved from the local amplification image and the heightprofiles.Different from the whole stretching of DNA network at a

low concentration after the electric field enhancement, theincrease of the voltage from 0.5 to 1.0 V accompanied by ahigh DNA concentration led to the formation of a large-scalenetwork with unique maze-like structures, uniformly dis-tributed on the surface of mica as shown in Figure 4b. Theuniform distribution of the network can be further confirmedby the nearly circular diffraction ring in the Fourier transformimage (Figure 4g). The meshes in this network were differentin size without the evident directionality, the edges weresmooth without obvious corners. In addition, although thecoverage and density of the DNA network, even the width ofDNA fibers formed in this way were much higher than those ofthe network shown in Figure 2c, the height of the fibers did nothave significant change.When the voltage increased to 1.5 V, the DNA network

arrays with the parallel arrangement appeared on the surface ofthe bare mica, which were extended along the direction of theelectric field as shown in Figure 4c and Figure S1a. Besides, thedirection of periodic arrangement can also be reflected fromthe direction of bright lines passing through the central point

in Figure 4h. The meshes were uniform in size with thepolygonal shape and closely connected with each other. Thewidth and height of the fibers were similar to those in Figure4b. The horizontal accumulation of the DNA bundlesincreased to a higher level as the voltage increased to 2.0 V,where the thin layer with obvious micropores formed by theintermolecular accumulation were clearly visible as shown inthe local amplification image of Figure 4d. The thin layers wereconnected and assembled into a DNA network with seeminglylacerated boundaries, and the herringbone fibers were parallellydistributed to the side of the network possibly formed due tothe transverse pulling effect of electric field force. It was worthnoting that the height of the DNA network formed at thisvoltage still had no significant change with the increase of thevoltage.As the voltage rose to 5 V, the DNA network arrays in the

parallel arrangement with clear and regular boundariesappeared again on the surface of the bare mica, which weredisplayed distinctly in Figure 4e and Figure S1b. Comparedwith the DNA network arrays shown in Figure 4d, the shape ofthe arrays and the distribution of the meshes were moreregular, which could be seen from the highly bright near-circular diffraction ring in Figure 4j. The arrangementperiodicity of the arrays was much clearer since there was anarrower bright line passing through the central point than thatin Figure 4i. Furthermore, similar to Figure 4d, the networkwas fabricated by the connected and assembled thin layers andthere was no significant change in the height of the network.Therefore, by adjusting the intensity of electric field and theconcentration of DNA solution, it is possible to fabricatenetwork arrays with uniform heights and different morphol-ogies.The in situ measurement36 of the DNA networks under the

HEF DC voltages of 0 and 5.0 V was carried out as shown inFigure 5. Unlike the electric field acting on the DNA solution,

the electric field in the test was applied on the dried DNAnetwork deposited on the mica surface. The morphology of theDNA network did not have significant changes as the voltageraised to 5.0 V, indicating that the stretching and movement ofDNA networks were more likely to occur in aqueous media.In order to figure out the influence of surface properties on

DNA self-assembly under the DC electric field, the micamodified by Mg2+ was prepared for the further examination.Figure 6a is the AFM result of a control experiment where thesample was not treated by the electric field. The DNA chainswere loosely and disorderly distributed on the surface of mica

Figure 5. In situ measurement of the DNA network formed with theconcentration of 10 ng/μL DNA solution on the bare mica surfaceunder the HEF DC voltages of 0 (a) and 5.0 V (b).

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without obvious intermolecular contact, crossover, and overlapfor the formation of regular networks. Figure 6b displays thesample treated by the HEF DC voltage of 0.5 V on Mg2+-modified mica. The modification of Mg2+ certainly affected theDNA aggregation behavior that a network with large meshesappeared in the image, which was quite different with thenetwork shown in Figure 4b at the same voltage. In addition to

morphological changes, the height of DNA networks has alsoincreased to a certain degree. As the voltage increased to 1.0 V,the DNA molecules accumulated with each other severely toform parallel long arrays, in which the height of the arrays evenreached nearly 100 nm. Therefore, the surface modification ofmica should be an important factor for the influence of DNAself-assembly in the electric field.

Figure 6. Typical AFM images and the corresponding height profiles of 10 ng/μL DNA on the Mg2+-modified mica produced under the differentHEF DC voltages: 0 (a), 0.5 (b), and 1.0 V (c), respectively. The AFM images and the corresponding 3D topographic maps of bare (d, e) andMg2+-modified (g, h) mica surfaces. Pictures f and i are the water droplet on the bare and Mg2+-modified mica surfaces, respectively.

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For a detailed discussion, the DNA self-assembly was theresult of multiple forces acting together, including theelectrostatic attraction and the hydrophilic force betweenDNA and the mica surface, the attraction force between DNAmolecules,38,41 and the electric field force. The Mg2+ plays arole of bridge between the phosphate groups of DNAmolecules and the surface of mica, which could enhance theelectrostatic attraction and the hydrophilic force between theDNA and the mica surface. The AFM images as well as thecorresponding 3D topographic maps of bare and Mg2+-modified mica surfaces are shown in parts d, e, g, and h ofFigure 6, indicating that the surface roughness has increasedafter the treatment of Mg2+ modification. The increased surfaceroughness on the one hand increased the contact opportunitybetween the DNA molecules and mica surface. On the otherhand, from parts f and i of Figure 6, the increase of surfaceroughness led to the decrease of the surface hydrophilicity,thus the DNA solution was as a result not easy to spread onthe mica surface, which contributed to the accumulation ofDNA to a large extent under the application of electric field.As a comparison, the Mg2+ was mixed with the DNA

solution to obtain the 10 ng/μL DNA/1 mM Mg2+ solution toprepare the samples under the horizontal DC electric field. Asshown in Figure 7a, in the presence of Mg2+, the arrangement

of DNA molecules was different from that of the sample inFigure 2c. Under the action of the electric field, themorphology of the sample did not change significantly, exceptthat the increased deposits of surface buffer salts, as shown inFigure 7b. It can be concluded that the presence of positivelycharged Mg2+ in DNA solution was not conducive to theformation of different DNA networks under the horizontal DCelectric field.In addition to the self-assembly behavior of DNA in the

horizontal electric field, the arrangement of DNA molecules inthe vertical electric field was also investigated. Figure 8 displays

the typical AFM images of 1 ng/μL DNA on the bare micaprepared under different VEF DC voltages. Among them, thedirection of the applied vertical electric field was upward forFigure 8a−c and downward for Figure 8d. It could be seen thatthe distribution of DNA molecules was obviously affected bythe change of voltage. At a low voltage of 0.5 V, the DNAmolecules were interconnected to form a relaxed DNAnetwork showing a similar morphology to that in Figure 3a.When the voltage increased to 0.75 V as shown in Figure 8b,the density of DNA networks decreased and there became atendency for the DNA molecules to be stretched. Moreover,the surface of the area around the DNA molecules seem to berough owning to the deposition of residual buffer salt.42 Figure8c shows that at the voltage of 1.0 V, a higher amount ofresidual buffer salts deposited into a dense thin layer with agreat deal of microporous structures on the mica surface, whichis not found in the sample prepared in the horizontal electricfield. The stretched DNA chains were embedded in the as-formed residual buffer salt layer, and there was no distinctintermolecular contact, crossover, and overlap between them.A possible explanation for the above results could be that the

higher electric density promoted the electrostatic attractionand the hydrophilic force between the DNA and the micasurface rather than the attraction force between the DNAmolecules, which contributed to the enhanced stretching effectof DNA molecules with the increase of the voltage. Althoughthe upward electric field at a relatively high voltage did make adifference on stretching DNA molecules, the formation of thisresidual buffer salt layer was not expected.Correspondingly, for the downward vertical electric field at

1.0 V as shown in Figure 8d, the DNA molecules exhibitstretching result similar to that shown in Figure 8c, but therewas no obvious buffer salt crystallization around the stretchedDNA molecules, which indicated that a surface with richpositive charges is more conducive to the formation of residualbuffer salt layer.Figure 9 shows the distribution of DNA molecules at

different concentrations of DNA solution under the 1.0 Vupward vertical electric field. For a more detailed examinationof DNA with a concentration of 1 ng/μL, the DNA chainembedded in the residual buffer salt layer can be clearly seenfrom the local magnification of Figure 9a. The height of theDNA chain was measured to be approximately 2.5 nm from theheight map, which was about 5 dsDNA high, and the thicknessof the residual buffer layer was nearly 1.0 nm. At theconcentration of 5 ng/μL, the DNA molecules wereaccumulated to form parallel long arrays as shown in Figure9b. From the edge of the arrays, the tentacle-shaped DNAfibers stretched out and contacted with each other to form anetwork structure. There was no residual buffer layer formedon the mica surface. The DNA arrays mainly composed of two

Figure 7. Typical AFM images formed with the 10 ng/μL DNA/1mM Mg2+ solution on the bare mica surface under the HEF DCvoltages of 0 (a) and 5.0 V (b).

Figure 8. Typical AFM images of 1 ng/μL DNA on the bare mica produced under the vertical upward DC voltages of 0.5 (a), 0.75 (b), and 1.0 V(c) and downward VEF DC voltage of 1.0 V (d).

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typical aggregation patterns, as shown in the local magnifica-tion maps. One structure of the patterns was formed by thetightly intertwining and stacking of DNA molecules, whichcontributed to a relatively higher height and narrow width ofthe arrays. At the edge of the arrays where the DNA chainsstretched out, the thin DNA films with the height of about 3−4nm could be found. For another one, a large amount of DNAmolecules curled up under the action of electric field andaccumulated into layered structure with the height of about 2nm. Figure 9c displays that as the concentration increased to10 ng/μL, the regular morphology is not obtained owning tothe serious agglomeration of DNA molecules.

■ CONCLUSIONSIn summary, large-scale morphologically controlled self-assembled DNA networks were fabricated by the synergisticeffect of a DC electric field. By comparison of the AFM imagesof the samples under different electric field directions, it wasshown that the horizontal electric field was more advantageousto the formation of DNA networks with more regularstructures. Moreover, at the same DNA concentration, thechange of horizontal electric field intensity did not affect theheight of DNA network significantly. It was also found that themodification of Mg2+ increased the aggregation of DNA

molecules under the electric field, and thus formed higherDNA networks. In addition to the formation of DNA self-assembly networks, obvious DNA molecular stretching resultsat both horizontal and vertical electric fields were obtained atlow DNA concentrations. The above information may help toprepare controllable self-assembled DNA networks withdiverse patterns and will also promote the application ofDNA in the field of nanotechnology.

■ ASSOCIATED CONTENT*S Supporting InformationThe Supporting Information is available free of charge on theACS Publications website at DOI: 10.1021/acs.jpcb.9b08891.

Typical AFM images (PDF)

■ AUTHOR INFORMATIONCorresponding Authors*E-mail: wangz@cust.edu.cn (Z.W.). Telephone/Fax: +86-431-85582341.*E-mail: huch@cust.edu.cn (C.H.).

ORCIDZuobin Wang: 0000-0002-7168-0918

Figure 9. Typical AFM images (the first column), local amplification images (the second column) and the corresponding 3D topographic maps(the third column) of 1 (a), 5 (b), and 10 ng/μL (c) DNA on the bare mica produced under the 1.0 V VEF DC voltage. (Note: The blue dottedarrow on the 3D topographic maps represents the direction of the vertical electric field.) The fourth column is the height profiles of the transversalsection marked with the white dashed line in the local amplification images.

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NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTS

We are grateful to the National Key R&D Program of China(No.2017YFE0112100), EU H2020 Program (MNR4SCELLNo.734174), Jilin Provincial Science and Technology Program(Nos. 20160623002TC, 20180414002GH, 20180414081GH,20180520203JH and 20190702002GH), and “111” Project ofChina (D17017). This work was also partly supported byChangli Nano Biotechnology (China).

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