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    Controllable self-assembly of parallel gold nanorod clusters by DNA origami

    2019-02-15 02:28:04HngYuTintinMnWeiJiLeileiShiChenweiWuHoPeiChunZhng
    Chinese Chemical Letters 2019年1期

    Hng Yu,Tintin Mn,Wei Ji,Leilei Shi,Chenwei Wu,Ho Pei,*,Chun Zhng,*

    a School of Chemistry and Chemical Engineering,Shanghai Key Laboratory of Electrical Insulation and Thermal Ageing,Shanghai Jiao Tong University,Shanghai 200240,China

    b Shanghai Key Laboratory of Green Chemistry and Chemical Processes,School of Chemistry and Molecular Engineering,East China Normal University,Shanghai 200241,China

    Key words:Gold nanorod DNA origami Cluster Plasmonic Self-assembly

    ABSTRACT Herein we demonstrate the construction of three types of parallel gold nanorod(Au NR)clusters using a DNAorigamirod(DOR)asthe template.Based on the precise control over the position of capture strands on DOR,number and orientation of the Au NRclusters can be well engineered,as evidenced by biological transmission electron microscope(TEM).Importantly,the Au NR clusters exhibit chiroptical responses which are strongly affected by the number of Au NR on rod-like DNA origami.

    Plasmonic metamaterials,which possess numerous unusual optical properties such as circular dichroism(CD)[1],giant nonlinear optical activity[2],and Fano resonance[3],have draw n great attention due to their extensive applications in biosensing,imaging,photonics,and optoelectronics,etc.[4,5].These Artificial plasmonic structures are typically constructed through either topdow n[6–9]or bottom-up[10–14]approaches.However,the former ones are often restricted to resolution,fabrication,and rational three-dimensional(3D)organization of nanoarchitectures[15].Bottom-up methods,on the other hand,provide a new pathw ay to overcome these challenges.Particularly,DNA with unprecedented programmability and addressability,has demonstrated to be one of the most powerful and versatile building blocks for fabrication of sophisticated architectures with well-de fined shapes and functions[16–21].In this fi eld,DNA origami[22,23],undoubtedly a milestone in the progress of DNA nanotechnology,has been utilized not only to construct diverse pure DNA nanostructures[24–28],but also performed as ideal templates to guide the assembly of various nanoscale objects,such asmetallic nanoparticles[29–33],carbon nanotubes[34],quantum dots or organic dyes[35],into highly-ordered structures.

    Among plasmonic metamaterials,the use of anisotropic nanoparticles as building blocks,such as gold nanorods(Au NRs)[36–41],are especially intriguing as they have unique optical and electronic features,including w ide range of optical extinction and strong plasmonic fields,as well as specific absorption ow ing to its anisotropic shape.Furthermore,the accurate assembly of AuNRs may lead to novel optoelectronic features that have never been observed in an individual Au NR as collective properties w ould emerge ow ing to the interparticle coupling upon forming the highly-ordered metamaterials.Importantly,these emerging collective properties can be rationally tuned by multiple geometric parameters,such as size,distance,and orientation[42,43].Along this direction,substantial efforts have been devoted to using DNA origami as template to direct the Au NRassembly and construct a variety of functional architectures,such as rectangular origamitemplated discrete Au NR dimer and helical superstructures with tailored chiroptical responses[44,45].More recently,Liu and coworkers used DNA origami template to create a range of recon fi gurable 3D plasmonic nanosystems,which can respond to matter or external stimuli,including DNAstrands[46],light[47],p H changes[48],and be monitored by CD spectrometry.Nevertheless,high-fi delity and high-yield assembly of Au NRs into elaborate nanoarchitectures still remains challenging,especially w hen the number of involved Au NRs increases.In this work,we designed and engineered three types of anisotropic Au NRclusters with different 3D spatial con fi gurations using a rod-like DNA origami as the template(Fig.1).By tuning the positions of capture strands on the surface of DNAorigaminanorod(DOR),tw o-,three-,and four-Au NRs could be precisely arranged on the longitudinal direction of DOR to form parallel Au NR clusters in a high controllable manner.Then their optical properties were further investigated after the assembly.

    In the material preparation,hexadecyltrimethyl ammonium brom ide(CTAB),sodium borohydride(NaBH4),silver nitrate(AgNO3),tris(2-carboxyethyl)phosphine hydrochloride (TCEP)were supplied by Sigma.Gold (III) chloride trihydrate(HAu Cl4?3H2O)was supplied by J&K.L-Ascorbic acid waspurchased from Macklin.Sodium dodecylsulfate(SDS)was purchased from Beyotime.Non-thiolated DNAsequences were bought from Sangon Biotech,while thiolated DNA sequences were obtained from DNA synthesizer.

    In addition,DNA squences for folding the single-stranded M13mp18 DNA into origami rod were designed by using caDNAno softw are[49].The Au NRs were prepared by follow ing El-Sayed’s method with some modifications[50].Functionalization of the Au NRs with thiolated DNAs was conducted by using a previously reported salt aging method[51].Meanwhile,the annealing processes of constructing DNA origami rod and the Au NRclusters followed Liedl’s method[52]and Yan’s method[43]respectively.After the assembly,DNA origami rods and the Au NRclusters were further puri fied by 1%agarose gel electrophoresis and recoverd by electroelution with dialysis bag.The details of DNA sequences,Au NRsynthesis and functionalization,preparation and puri fi cation of DNA origami rod and AuNR clusters,sample characterizations including UV–vis spectroscropy,CD spectroscropy,agarose gel electrophoresis,AFM,and TEM imaging,etc.are presented in Supporting information.

    Fig.1.Schematic illustration of the rod-like DNA origami-directed assembly of Au NR cluster nanoarchitectures.A long single-stranded M13 DNA is folded by thermal annealing with a set of staple and capture strands to generate a rigid rodlike 54-helix bundle DNA origami template.The capture strands are extended from different sides of the DORsurface to achieve diverse Au NRassembly.On each side,multiple capture strandsarranging evenly along the axisof DORare used to robustly immobilize one Au NR.AuNRs modified with corresponding complementary DNA strands are assembled at the designated positions on the DNA origami via DNA hybridization,forming three types of parallel Au NRclusters:(a)dimers,(b)trimers and(c)tetramers,respectively.

    Fig.1 illustrated the design of DORtemplate and the assembly process of Au NR clusters.First,a rod-like 54-helix bundle DNA origami(45 nm?20 nm)was synthesized follow ing a typical method initiated by Rothemund[22],which can nicely match the length of gold nanorod used in this study.To further employ it as the template,tw o to four groups of the capture strands were introduced and extended from outside surface of the DNA origami rod.In detail,to achieve robust immobilization of Au NRs on DOR,multiple(fi ve to ten,see Supporting information for the details)single-stranded overhangs for each group of capture strands were arranged along the longitudinal axis to form a binding site for immobilizing an Au NR(for details,see Supporting information).To construct Au NR clusters with different numbers,these capture strand groupswere evenly arranged around the longitudinal axisof DORs with C2,C3,and C4 rotational symmetries.Then AuNRs(?45 nm?12 nm on average)modified by thiolated DNAswith the sequences complementary to the single-stranded overhangs were synthesized follow ing previously reported method[50,51,53].Hence,DNA-modified Au NRs could be attached to the designated positions on the DNA origami rod through DNA hybridization.In this w ay,different types of anisotropic Au NR clusters can be successfully assembled,including AuNR dimers,trimers,and tetramers,in which all Au NRs are parallel to the axis of the DOR.From the top view of these parallel Au NRclusters,the Au NRs endpoints are located as a line segment,regular triangle,and rhombus,respectively.

    With all designed DNA strands together,the rod-like DNA origami template was fi rst assembled by folding the long M 13mp18 scaffold strand with staple and capture strands at a ratio of 1:10:10 via a thermal annealing process from 80?Cto 25?C.Then the assembled product was characterized by agarose gel electrophoresis.Asshow n in Fig.2a,a slightly faster mobility of the target DNA origami was observed in comparison with that of the pristine M 13mp18 scaffold,which could be attributed to its tightly packed structure[54].After removing the excessstaple strandsand unintended aggregates,the puri fied DNA origami was further visualized by transmission electron microscopy(TEM)and atomic force microscopy(AFM).As show n in Fig.2,monodispersed rodlike nanostructures could be clearly observed(Figs.2c and d,Figs.S2 and S3 in Supporting information),dimensions of which were highly in agreement with our design.

    Fig.2.Characterizations of the DNA origami rods and the formation of AuNR clusters.(a)Agarose gel analysis of the self-assembled DOR stained by ethidium bromide and imaged under UV light.Lane 1:M 13mp18 scaffold strand.Lane 2:The annealed products.The lowest bright band represents the excessive staple strands,followed by the DOR band above and some of unintended aggregates.(b)The formation of AuNR clusters by annealing the puri fied DOR template and the DNA-modified Au NRs together,which were determined by agarose gel electrophoresis.Lane 1:free DNA-modified AuNRs.Lane 2:the annealed Au NRcluster samples.The lowest band represents the excessive Au NRs,followed by the Au NR cluster band(dimer in this gel)above and some unintended aggregates.(c,d)AFM image(c)and TEM image(d)of the DNA origami rods after puri fi cation.

    With the puri fied DOR in hand,DNA-modified Au NRs were further added in the solution and immobilized on the DOR template.To achieve high yield of the assembly,excess singlestranded DNA-functionalized Au NRs(ssDNA-Au NRs,with complem entary sequences to the capture overhangs)were used and mixed with the DORs,followed by a multi-cycle annealing process over 25 h.After that,the assembled product of anisotropic Au NR clusters were analyzed by agarose gel electrophoresis(Fig.2b and Fig.S4 in Supporting information).In all cases,sharp bands with lower gel mobility could be observed,which was located above the ssDNA-Au NR sample,indicating the good monodispersity of the assembled clusters.After puri fi cation of the target products from the gel by electroelution in a dialysis bag,the structures of anisotrop ic Au NR clusters were characterized by biological transmission electron microscopy(TEM)(Fig.3 and Figs.S5–S10 in Supporting information).Even though the drying process on TEM grids caused deformation of the assem bled plasm onic nanostructures in some degree,their native con fi gurations were basically preserved and could be discriminated clearly,which mainly owes to the good rigidity of the DNAorigamitemplate.It is w orth noting that,in the zoom-in TEM images,all those three types of Au NR architectures display corresponding side-by-side spatial con fi gurations,which match very well with our design of parallel Au NRclusters.All these results demonstrate the excellent template role of rod-like DNA origami in precise control of the Au NRs’arrangement.Furthermore,the UV–vis spectral analysisof the Au NRclusters described above was carried out.Compared to the spectrum of ssDNA-AuNRs,absorptions of the organized plasmonic clusters was slightly blue-shifted,which may be aroused by interparticle coupling (Fig.S11 in Supporting information).

    Finally,we implemented CD measurements using a circular dichroism spectrometer.Interestingly,chiral optical response of the assembled Au NR clusters was observed by the analysis of circular dichroism spectroscopy although they were designed to be highly symmetric architectures.Fig.4 show s the CD spectra of these three types of parallel AuNRclusters.It is apparent that the anisotropic plasmonic clusters exhibit dramatical chiral optical responses with characteristic bisignate signatures,which can be attributed to the dipole-plasmon Coulomb interactions between Au NRs and chiral helices of double-stranded DNAs(dsDNA)[55,56].The left-handedness is induced by the parallel orientation of Au NRs relative to dsDNA in the template.While keeping the same concentration of Au NRclusters,it is found that the tetramers displayed the strongest CDsignal,followed by the AuNRtrimers.In contrast,Au NR dimers exhibit much weaker CD signal,which re fl ects the less extent of cooperative dipole-plasmon interactions between Au NR clusters and dsDNA helices[56].

    Fig.4.CD spectra of the parallel AuNRclusters:dimers,trimers,and tetramers.The increasing trend of the CD intensity demonstrates its dependence on rod number.The concentrations of Au NR clusters are the same for these three samples during the measurements.

    In summary,we have employed a DNA origami rod as the template to guide the construction of diverse anisotropic Au NR clusters with side-by-side 3D con fi gurations.The remarkable programmability and addressability of origami structure ensures the precise spatial control of the plasmonic components,resulting in the well-de fined Au NRdimer,trimer,and tetramer.With these new ly engineered nanostructures,predictable and dramatical CD response at their optical frequencies was observed due to the dipole-plasmon interactions between Au NRs and dsDNA helices and the intensity of CDsignal was found to be highly related to the number of AuNRin the clusters.Our work may broaden horizon in bottom-up fabrication of plasmonic nanoarchitectures with more complex 3D con fi gurations and exploration of their emerging properties.Furthermore,it is also possible to realize precise 3D assemblies using other building blocks(e.g.,quantum dots and magnetic nanoparticles)to construct more functional metamaterials and devices,which may perform as good platforms for biosensing,surface enhanced Raman scattering,drug delivery,and so on.

    Acknow ledgm ents

    This work was supp orted by the National Natural Science Foundation of China(Nos.21504053,21661162001,21673139,91527304,21722502),Shanghai Pujiang Talent Project(No.16PJ1402700),the Innovation Fund from Joint Research Center for Precision Medicine set up by Shanghai Jiao Tong University&Af fi liated Sixth People's Hospital South Campus(No.IFPM 2016B001), and the special program for collaborative innovation in Shanghai University of Medicine&Health Sciences(SPCI-17-15-001).

    Appendix A.Supplem entary data

    Supplementary data associated with thisarticle can be found,in the online version,at https://doi.org/10.1016/j.cclet.2018.04.020.

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