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aWroclaw University of Technology, Institut

Wybrzeze Wyspianskiego 27, 50-370 Wrocla

wroc.plbLaboratoire de Photonique Quantique et M

Cachan, 61, avenue du President Wilson, 94cLBPA, UMR 8113 CNRS, ENS de Cachan,

Cachan, France

† Electronic supplementary information (Epolarization analysis model, estimation ofand scans and polar graphs of nano10.1039/c3nr03319h

Cite this: Nanoscale, 2013, 5, 10975

Received 27th June 2013Accepted 29th August 2013

DOI: 10.1039/c3nr03319h

www.rsc.org/nanoscale

This journal is ª The Royal Society of

Gold nanorods as multifunctional probes in a liquidcrystalline DNA matrix†

Joanna Olesiak-Banska,*a Marta Gordel,ac Katarzyna Matczyszyn,a Vasyl Shynkar,b

Joseph Zyssb and Marek Samoca

We show how a single gold nanorod can serve as a multifunctional probe in an organized DNA matrix.

Polarization analysis of two-photon luminescence excited with a femtosecond laser enables imaging of

the orientation of a single nanorod, which reports the orientation of DNA strands. Carefully controlled

photoinduced heating by the same laser is able to degrade the DNA matrix in a highly localized volume.

1 Introduction

Theranostic agents, which combine both diagnostic and thera-peutic activity, are of major interest for nanomedicine. In order toimprove selectivity and sensitivity of the treatment of variousdiseases, efficiently detected and more personalized probes areneeded. Several nanostructures have been proposed tomeet theserequirements: magnetic nanoparticles, carbon nanotubes, poly-meric nanoparticles, and gold nanoparticles.1 Among them, goldnanorods received much attention as luminescent markers forbiological systems.2,3 In addition to their small size, nanorodsallow for easy tuning of the surface-plasmon resonance (SPR) inthe near infrared spectral range,4,5 which is particularly advanta-geous in bioimaging. Extinction spectra of NRs show two surface-plasmon resonances corresponding to the longitudinal (l-SPR)and the transverse (t-SPR) mode. Of special signicance is the factthat the NRs have a much higher luminescence quantum yieldthan gold nanospheres.6 Their absorption, scattering and one-(1PL) and two-photon excited luminescence (2PL) are stronglypolarization dependent, which enables their precise localizationand probing at the single particle level.2,7,8 Moreover, the photo-thermal properties of Au NRs can be successfully used in photo-activated detection and treatment of biological samples.9–11 Strongabsorption of NIR light by NRs selectively attached to malignantcells, and fast release of the heat to the surroundings allows forthe treatment of infected tissue, while keeping intact the

e of Physical and Theoretical Chemistry,

w, Poland. E-mail: joanna.olesiak@pwr.

oleculaire, Institut d'Alembert, ENS de

235 Cachan, France

61 Avenue du President Wilson, 94235

SI) available: The NR UV-Vis spectrum,the temperature increase in a nanorodrods under illumination. See DOI:

Chemistry 2013

contiguous healthy tissues. However, only limited quantitativeinformation about imaging and photoinduced heating of a singlenanoparticle embedded in biological systems is currently avail-able. The focus in the literature has been on the description of agel-uid phase transition of phospholipid membranes.12,13

However, an efficient internalization of gold nanoparticles by cellsand cell nucleus targeting was conrmed by numerous publica-tions,14–16 thus the understanding of interactions of gold NRs witha condensed DNA phase is of great importance.

In this study, we exploit gold nanorods as orientation markersand, simultaneously,photothermalagentsactingon thenanometerscale in theDNAmatrix.Weimageandmanipulate theorganizationof DNA strands self-assembled into lyotropic liquid crystal (LC)phases. DNA LC is considered as a model of DNA organization invivo, as DNA liquid crystal phases were found in a number of livingorganisms.17–19 DNA strand organization, characteristic for specicLCphases, canbevisualizedwithseveral techniques,butamongthevarious types of microscopy that can be employed here we havesingled-out polarization-sensitive two-photon uorescencemicroscopy (ps-2PFM). This choice hasmultiple advantages.Whenusing conventional intercalatingor groovebindingdyemarkers, ps-2PFM can, in particular, provide full information about DNAordering in three dimensions.20,21 In this contributionwe show thata single gold NR can serve as an efficient luminescent probe for ps-2PFM in DNA, based on its strong two-photon absorption andsubsequent luminescence. We investigate the orientation of NRswith respect to DNA and image NR distribution in DNA LC phases.As the DNA LC phase behaviour depends strongly on temperature,wealsoanalyse thephotothermaleffects in theDNA–NRsystemthatcan be applied for the control of highly localized organization anddisorganization of DNA.

2 Experimental section2.1 Gold nanorod synthesis and characterization

Gold NRs with the maximum of l-SPR band at 845 nm weresynthesized using a seed growth method (see Fig. S1†).22 All the

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Fig. 1 (a) TEM image of the investigated gold NRs and (b) undulating columnarhexagonal phase of DNA intercalated with EB and doped with gold NRs. Thephoto is taken under PLM with crossed polarizers.

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chemicals were purchased from Sigma Aldrich. The adoptedprocedure is based on preparation of primary nuclei, 3.5 nmgold seeds. We use 250 ml of 0.01 M gold chloride solution, with600 ml 0.01 M solution of ice-cooled borohydride as a reducingagent of gold salts (gold(III) chloride trihydrate) (reduction ofAu3+ to Au0) and 7.5 ml of 0.1 M hexadecyltrimethylammoniumbromide as a capping agent. Aer a few minutes the seedsolution becomes brown. The subsequent step is the rapidgrowth of nanoparticles. Ascorbic acid (320 ml of 0.1 M) is used,which reduces the Au3+ gold salt to Au1+ in the presence of CTABmicelles. 300 ml of 0.01 M solution of silver nitrate is added,inuencing formation of rod shape nanoparticles. The seedsolution (0.26 ml) is injected and the growth solution is leundisturbed in the water bath at 27 �C. The longitudinal SPRpeak has a tendency to blue shi with time. To prevent thecontraction nanorods are additionally stabilized by treatment oftheir surface with Na2S.23 Na2S, 1 mM solution, is added into thegrowth solution aer one hour. The solution is le for 15minutes. Aer the synthesis, NRs are separated from sphericalnanoparticles by centrifugation (twice at 14 000 rpm).

The average size of NRs was evaluated on the basis of imagesobtained with a FEI Tecnai G2 20 X-TWIN Transmission Elec-tron Microscope. The obtained NRs had an average aspect ratioof 3.4.

2.2 DNA liquid crystal preparation and characterization

The preparation of DNA liquid crystal phases doped with goldnanorods followed the procedure of DNA–dye sample prepara-tion described in ref. 20,21,24. We used DNA isolated fromsalmon roe, purchased from Sigma-Aldrich, sonicated with aUP200S ultrasonic homogenizer (Hielscher GmbH) in order toget homogeneous-length chains (app. 500–1500 bp). The aqueoussolutions of DNA were doped with a uorescent dye in order tovisualize the orientation of DNA strands in comparison with thegold NR orientation. We chose an intercalator ethidium bromide(EB, purchased from Sigma Aldrich), as its orientation isperpendicular to the orientation of DNA and supposedly to theorientation of NRs, which should facilitate the discriminationbetween their uorescence. Series of DNA–EB–NR samples wereprepared with the nal concentrations: cDNA ¼ 10 mg ml�1 andcEB ¼ 1.93 mM, which corresponds to [EB]/[DNA] ¼ 1/50 and cNR¼ 1 � 10�8 M. The droplets (15 ml) were deposited on a cleanglass plate. The formation of liquid crystal phases was observedunder an Olympus 60BX polarized light microscope (PLM).

2.3 Two-photon microscopy and polarization analysis

The optical setup of a two-photon microscope combined withpolarimetric analysis used a Ti:sapphire laser (Spectra PhysicsMai Tai HP, 100 fs, repetition rate 80 MHz) with the incidentwavelength range tunable within l ¼ 690–1020 nm. The laserbeam passed through an achromatic half-wave plate mountedon a motorized rotation stage, in order to continuously vary thepolarization direction of the incident light. Light was focusedtightly, using a high numerical aperture oil-immersion micro-scope objective (100�, NA ¼ 1.4). The sample was mounted onan XYZ piezoelectric scanning stage, and the two-photon excited

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emission was collected in epi-uorescence mode through thesame microscope objective. The emitted signal was separatedfrom the incident light on a dichroic mirror and split by apolarizing beam-splitter into two orthogonally polarized ps-2PFM components IX and IY, recorded by two avalanchephotodiodes working in a photon counting regime.

3 Results3.1 Liquid crystalline DNA doped with gold nanorods

We synthesized gold NRs according to the procedure describedin ref. 5 and 22. The mean width and length of a NR were 10.6nm and 36.0 nm, respectively, as determined from TEM images(Fig. 1a), and the maximum of the l-SPR was located at 845 nm.Then, DNA liquid crystal phases were prepared with DNAstained with the intercalating agent ethidium bromide anddoped with gold NRs. Fig. 1b shows a polarized light microscopy(PLM) image of a dried droplet of DNA–EB–NR solution. Acharacteristic zigzag pattern is observed near the rim of thedroplet, which corresponds to the columnar hexagonal phasewith undulations induced by linear defects.20,24,25 In the processof drying, DNA chains are deposited along the contact line of adroplet. Simultaneously, they undulate due to the radial stressof receding meniscus and are similar to the structure obtainedin samples without NRs. A detailed investigation of the orien-tation of DNA in these structures, with application of ps-2PFM,was performed previously.20 DNA strands were found to beparallel to each other within one domain. At the border betweentwo domains they tilt and form a certain angle with respect tothe chains in the adjacent domain.

3.2 Two-photon microscopy of NRs in DNA liquid crystal

In order to resolve the three-dimensional organization of NRs inthe DNA LC phase, we took advantage of the intrinsic 3Dsectioning of two-photon microscopy. Gold nanorods exhibitvery high two-photon absorption cross-section26 and emit brightluminescence under two-photon excitation. We scanned a drieddroplet of the liquid crystalline DNA–EB–NR sample at several Zpositions up to a position outside the droplet (Fig. 2). Thepositions of bright spots of 2PL of gold NRs indicated a uniformdispersion of nanoparticles in the sample volume, starting from�1 mm below the droplet surface. Two-photon excited

This journal is ª The Royal Society of Chemistry 2013

Fig. 2 XY 2PL intensity scans performed at various depths within the drieddroplet of DNA solution doped with gold NRs. lexc ¼ 840 nm.

Fig. 3 (a) 2PL intensity raster scans of a border area of two LC domains formed iperformed with horizontal and vertical polarization of the incident light, respectivelyin (a) or (b) are marked with black or white circles, respectively. Red circles mark spotsspots numbered as 1 and 2 (distinct from the bright spots). The direction of DNA stra(c) The statistics of NR orientation with respect to DNA orientation calculated from sand v-, respectively.

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uorescence of EB provided the information about the locationof LC domains (alternation of low and high intensity regions).Contrary to numerous publications,27–29 we did not observe anyaccumulation of NRs at the LC domain borders or in defects of acolumnar phase. It proves that Au NRs form a homogeneousphase when dispersed in water solutions of dye-doped DNA.

The relative orientation of NRs with respect to DNA chainswas determined in detail through the ps-2PFM analysis. At rst,we investigated 2PL intensity scans of the border regionbetween two LC domains. Scans were performed with twoorthogonal polarizations of the incident light (Fig. 3a and b,polarization denoted with white arrows). We applied low-powerillumination (P ¼ 0.1 mW) with lexc ¼ 910 nm, which is asuitable wavelength for the excitation of EB molecules, asdetermined in our previous studies.30 As a result, images of twoadjacent low- and high-intensity domains were obtained withdistribution of bright spots, which we recognized as single goldNRs. In order to conrm the orientation of the dye and DNA, wecollected the angular dependence of 2PF outside the brightspots (Fig. 3, polar graphs 1 and 2). We followed the modeldeveloped in ref. 20 (see ESI for details†) and tted the twopolarization components with the relative angle J between theEB dye and DNA, set to 80� and the thickening of the conedistribution of the dye, DJ at 15� (see Fig. 3). The averagedirection of DNA was found to be 4 ¼ 163� and 90� in the rstand the second point of the scan, respectively. Hence, as DNAchains are almost perpendicular to the dye, DNA takes theorientation parallel and perpendicular to the polarization of theexcitation in the low- and high-intensity domains, respectively.

A 2PL signal of a single gold nanorod is highly dependent onthe polarization of the incident light and NRs are excited withthe highest efficiency, when the polarization of the illumination

n a dried droplet of DNA–EB–NR solution, lexc ¼ 910 nm. Scans (a) and (b) were(denoted by white arrows). Bright spots corresponding to gold NRs, observed onlyvisible in both images. Polar graphs of 2PF of EB bound to DNA were measured atnds and of the dye as determined from polar graphs is depicted outside the scans.everal different samples. Horizontal and vertical orientations are abbreviated as h-

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coincides with their long axis.2,31 We assigned horizontal (h-)and vertical (v-) orientations to NRs visible in Fig. 3a and b,respectively. It is clearly visible that most NRs are present in thedomain, where DNA is parallel to the direction of the incidentlight polarization, thus they follow the direction of DNA chains.To conrm this observation, we counted the NRs in horizontal,vertical and intermediate positions (black, white and red circles,respectively) in several scans collected in two different droplets.As a result, 68 � 5% of NRs in each domain exhibited anorientation parallel to DNA, 20 � 1% were perpendicular and12 � 1% of the total number of NRs were visible under bothhorizontally and vertically polarized light (Fig. 3c). If we takeinto account that the NR solution aer the synthesis containsup to 15% nanospheres (based on TEM images), which exhibitan isotropic emission32 and may contribute to the nanoparticlesvisible in both Fig. 3a and b, the presented percentages are thelower limit of the number of ordered nanorods. Thus, themajority of NRs follow the orientation of DNA strands andpolarization analysis of 2PL from gold NRs provides informa-tion about ordering features of DNA.

3.2 Two-photon microscopy of a single gold NR

In the following analysis, we focused on a single NR. As irradia-tion with an fs laser beam was shown to induce shape trans-formation in nanorods,32 we determined optimum conditions for

Fig. 4 Scans of the 2PL intensity of gold NRs in a DNA LC matrix, and the directionpolarization analysis of individual NRs and the inset shows the polarization analysis oand the inset shows the polar graph of NR no. 2, P¼ 0.05 mW; (c) scan after the poladroplet of DNA–EB water solution doped with gold NRs. White dashed lines mark tinset in scan (d) shows a polar graph of 2PL of one of the nanorods. The position o

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imaging below the energy threshold of NR melting (see ESI†).Then, we scanned a restricted area of a sample. High-resolution2PL intensity scans in Fig. 4, taken with the horizontal polari-zation of the incident light, show several gold NRs embedded inDNA. Aer the polarization analysis presented in the inset ofFig. 4a, a subsequent scan reveals the disappearance of theinvestigated NR (Fig. 4b). The same procedure repeated for thesecond NR results in a similar loss of the nanorod (Fig. 4c). Bothpolar graphs display a high 2PL intensity at a few initial incidentpolarization angles, and then a rapid decrease of the intensity atthe remaining angles, the nal 2PL intensity being much lowerthan its initial values. We performed similar experiments withlower power of the laser and in samples with and without EBstaining (see ESI†). For power up to 50 mW a gradual decrease of2PL intensity was observed and up to a few degrees shi of themaximum 2PL intensity angles, corresponding to a change of theinitial position of a nanorod (Fig. S4†). A change in the Z direc-tion restores the 2PL intensity (Fig. S5†). Thus, the possibleexplanation of the observation is an escape of the investigated NRout of the focal plane. If power of the order of 5 mW is applied, theNR does not change its position (Fig. S6†). On the other hand, forpower higher than 50 mW a signicant deformation of 2PL polargraphs is observed, presumably due to a considerable heating ofthe nanorod and the surroundings (Fig. S4†). The remaininguorescence visible in polar graphs in Fig. 4 comes from the EBmolecules in the DNA matrix, as the 2PL intensity of nanorods

of the incident light polarization is denoted with white arrows. (a) Scan before thef the NR no. 1, P ¼ 0.05 mW; (b) scan after the polarization analysis of the NR no. 1rization analysis of NR no. 2. (d)–(f) 2PL intensity scans of the area at the rim of thehe border between the droplet (to the right) and the glass plate (to the left). Thef the investigated nanorod is indicated with a white circle in all three images.

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embedded in DNA without EB drops to zero during theillumination.

A different effect was observed in the vicinity of the rim of adried droplet. Fig. 4d–f present three scans of the same areanear the droplet boundary. A columnar phase is usually formedseveral tens of micrometres apart from the contact line of adroplet, and between the droplet border and the columnarphase domains a region of very thin DNA lm is found. Weperformed the 2PL polarization analysis of one of the nanorodsin this region, and observed a rapid decrease of 2PL intensitywithin the rst several seconds of the measurement, andsubsequent increase of the intensity with the maximum at�120�. The initial horizontal position of the NR under investi-gation seemed to change to almost a vertical one. 2PL scantaken immediately aer the polar graph revealed the absence ofthe investigated NR (Fig. 4e), but the NR is visible in a scan withvertical incident illumination, which is a proof of the NR reor-ientation (Fig. 4f). Considering that in several hundred nmthick DNA lm NRs cannot escape out of the focus, we are in agood position to observe their rotation and reorientation in thedirection perpendicular to the polarization of the incident light.As 2PL remains polarized, nanoparticles did not reshape or meltin our experiment (as was shown in ref. 32 and 33).

Fig. 5 Temperature profile evolution in time around a NR in the DNA matrixilluminated with a laser beam of the incident average power P ¼ 0.05 mW(calculated from eqn (1)).

4 Discussion

Aer the NR excitation with fs laser pulse, the absorbed energyis used to create a distribution of hot electrons due to electron–electron interactions.34 This energy is subsequently dissipatedto the lattice via electron–phonon interactions.34 The next stepis the heat transfer to the surroundings. Various time scales arereported for this heat diffusion, from several tens of ps up toseveral ns, depending on the nanoparticle size and on thenature of the surrounding medium.34–37 In our experiments thetime interval between subsequent laser pulses is 12.5 ns, thuswe expect that nanoparticles thermalize before the illuminationby subsequent laser pulses.

The dissipated heat increases the matrix temperature. In ourcase heating of the DNA LC leads to a phase transition from aliquid crystalline to an isotropic liquid phase, which increases LCuidity and releases the constraints imposed by DNA strands onthe NR direction. A similar order–disorder phase transitioninduced in a phospholipidmembrane by gold nanoparticles (NPs)was reported by Urban et al.13 They calculated that an Au NP(diameter¼ 80 nm) illuminated with a continuous wave (cw) laserheats an area of radius �350 nm. However, Baffou et al. demon-strated a much more conned temperature prole characterizingpulsed illumination, in comparison with cw illumination (1/r3

versus 1/r temperature spatial decrease, respectively).38

We estimated the temperature prole around a gold NR, withthe assumption of a point-like heat source, based on a distri-bution of the heat power density, to be

DTðr; tÞ ¼ Q

csrsð4pastÞ3=2exp

�� r2

4ast

�(1)

where Q is the thermal energy released by the source Q ¼ Fs1PA,F is a laser uence at the focus (in our case, when lexc ¼ 910 nm,

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P ¼ 50 mW, F ¼ 0.127 mJ cm�2), and s1PA is the one-photonabsorption cross-section (see ESI†). cs is the specic heatcapacity of the matrix and rs is the matrix density. as is thediffusivity equal to k/rscs, where k is the thermal conductivity ofa matrix. According to our knowledge, the information aboutspecic heat capacity and the thermal conductivity of DNA isnot available in the literature, thus, for the calculations weassumed for these parameters the values of water and PVApolymer, specically, cs ¼ 4187 J kg�1 K�1 and 1650 J kg�1 K�1,and k ¼ 0.6 Wm�1 K�1 and 0.21 Wm�1 K�1, respectively.38,39

Fig. 5 presents the evolution of the heated area aer one and80 000 laser pulses (12.5 ns and 1 s of illumination, respec-tively). The initial temperature rise of a nanoparticle calculatedfrom eqn (S1)† is 45 K. The temperature increment drops downrapidly to a fraction of a degree in a few nanoseconds time. Thetemperature increase by DT¼ 40 K above the room temperatureresults in DNA LC phase transition.24 The uidity of the DNAmatrix increases, which enables the escape of a NR out of thefocus. However, note that in Fig. 4a–c nanorods situated asclose as half a micron apart from the irradiated nanorod are notaffected by its movement. The absorption of an fs pulseproduces a temperature increase restricted to less than 1 mm3,which is much more localized than in the case of cw illumina-tion. The change of the average power of the laser to 100 mWand5 mW introduces the increase of the temperature equal to 90 Kand 4 K, respectively. Thus, in the former case boiling of watersurrounding the nanorod is possible, which explains thedeformations of the 2PL polar graph (Fig. S4†).

The escape of nanorods from the focus is facilitated bylocalized heating, but the origin of NR movement is funda-mental optical forces, which originate from scattering andabsorption of light. Optical gradient forces of a focused laserbeam, acting in axial and radial directions, allow for trapping ofgold nanoparticles down to 18 nm in diameter.40 They dependstrongly on the refractive index nm of the nanoparticlesurroundings. Axial force increases with increasing refractiveindex, whereas for radial forces it is not only the magnitude, butalso the direction which changes with nm.41 When nm < 1.1,nanoparticles are dragged towards the beam axis, whereas forlarger nm they are pushed out of the focus of the beam.

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Refractive index of the DNAmatrix in our experiments is�1.5,42

which implies a radial force pointing outward from the beamaxis. This light force combined with a uid matrix results in theescape of a gold nanorod out of the focus of the laser beam or atleast reorientation of the NR if the motion is restricted.

The effect of nanoparticle escape, although unfavourablefrom the imaging point of view, can be exploited in well-local-ized photothermal therapy. DNA ordering has a signicantimpact on the cell viability. We suggest that the local modi-cation of the organization of DNA helices may disrupt the DNAfunctioning, and, as a consequence, the functioning of thewhole cell. Liquid crystalline properties and precise orderingare exhibited not only by DNA, but also by other biomoleculesconstituting cells, e.g. lipids in biomembranes, collagen in thecytoplasm, etc. The introduction of gold NRs into cells aertarget-specic functionalization of their surface would allowone to visualize their position and orientation under ps-2PFM.Then, photoinduced heating of precisely selected NRs may beused to destabilize specic cell components and allow for themanipulation of cell structure and integrity.

5 Conclusions

In conclusion, we performed a detailed investigation of theapplications of gold nanorods as orientation markers andphotothermal agents in DNA liquid crystalline systems. Whenembedded in DNA LC phases, gold NRs exhibit goodmiscibility,as conrmed by three-dimensional images performed under atwo-photon microscope. Approximately 68% of NRs orientthemselves parallel to the long axis of DNA strands, thus thelocal organization of DNA strands can be resolved. During theillumination with a tightly focused, low intensity fs laser beam,controlled heating of a single NR introduces a temperatureincrease of the matrix up to 343 K. The application of nanorodsand two-photon microscopy enables precise localization andrestriction of the heated region to less than 1 mm3. In summary,a single gold nanorod combines bright two-photon lumines-cence with photothermal properties, and may be applied as amultifunctional, theranostic probe in condensed biologicalenvironments.

Acknowledgements

The authors gratefully acknowledge Katarzyna Brach and Mag-dalena Klekotko for help with DNA LC preparation. This workwas supported by the National Science Centre grant no. 2011/01/N/ST5/02404 and 2012/04/M/ST5/00340, the Foundation forPolish Science, under “Welcome” program, and by a statutoryactivity subsidy from the Polish Ministry of Science and HigherEducation for the Faculty of Chemistry of WUT.

Notes and references

1 K. Y. Choi, G. Liu, S. Lee and X. Chen, Nanoscale, 2012, 4,330–342.

10980 | Nanoscale, 2013, 5, 10975–10981

2 H. F. Wang, T. B. Huff, D. A. Zweifel, W. He, P. S. Low, A. Weiand J. X. Cheng, Proc. Natl. Acad. Sci. U. S. A., 2005, 102,15752–15756.

3 S. C. Tang, Y. Y. Fu, W. F. Lo, T. E. Hua and H. Y. Tuan, ACSNano, 2010, 4, 6278–6284.

4 J. Zhu, K. T. Yong, I. Roy, R. Hu, H. Ding, L. L. Zhao,M. T. Swihart, G. S. He, Y. P. Cui and P. N. Prasad,Nanotechnology, 2010, 21, 285106.

5 M. Gordel, J. Olesiak-Banska, K. Matczyszyn, C. Nogues,K. Pawlik, M. Buckle and M. Samoc, Proc. SPIE, 2012, 8424,84242F.

6 M. Yorulmaz, S. Khatua, P. Zijlstra, A. Gaiduk and M. Orrit,Nano Lett., 2012, 12, 4385–4391.

7 W. S. Chang, J. W. Ha, L. S. Slaughter and S. Link, Proc. Natl.Acad. Sci. U. S. A., 2010, 107, 2781–2786.

8 C. Sonnichsen and A. P. Alivisatos, Nano Lett., 2005, 5, 301–304.

9 X. H. Huang, I. H. El-Sayed, W. Qian and M. A. El-Sayed, J.Am. Chem. Soc., 2006, 128, 2115–2120.

10 L. Tong, Y. Zhao, T. B. Huff, M. N. Hansen, A. Wei andJ. X. Cheng, Adv. Mater., 2007, 19, 3136–3141.

11 D. Bartczak, O. L. Muskens, T. M. Millar, T. Sanchez-Elsnerand A. G. Kanaras, Nano Lett., 2011, 11, 1358–1363.

12 H. Y. Ma, P. M. Bendix and L. B. Oddershede, Nano Lett.,2012, 12, 3954–3960.

13 A. S. Urban, M. Fedoruk, M. R. Horton, J. Radler, F. D. Stefaniand J. Feldmann, Nano Lett., 2009, 9, 2903–2908.

14 T. B. Huff, M. N. Hansen, Y. Zhao, J. X. Cheng and A. Wei,Langmuir, 2007, 23, 1596–1599.

15 D. H. Dam, J. H. Lee, P. N. Sisco, D. T. Co, M. Zhang,M. R. Wasielewski and T. W. Odom, ACS Nano, 2012, 6,3318–3326.

16 A. G. Tkachenko, H. Xie, D. Coleman, W. Glomm, J. Ryan,M. F. Anderson, S. Franzen and D. L. Feldheim, J. Am.Chem. Soc., 2003, 125, 4700–4701.

17 M. Nakata, G. Zanchetta, B. D. Chapman, C. D. Jones,J. O. Cross, R. Pindak, T. Bellini and N. A. Clark, Science,2007, 318, 1276–1279.

18 A. Leforestier and F. Livolant, Proc. Natl. Acad. Sci. U. S. A.,2009, 106, 9157–9162.

19 Y. Bouligand and V. Norris, Biochimie, 2001, 83, 187–192.20 H. Mojzisova, J. Olesiak, M. Zielinski, K. Matczyszyn,

D. Chauvat and J. Zyss, Biophys. J., 2009, 97, 2348–2357.21 J. Olesiak-Banska, H. Mojzisova, D. Chauvat, M. Zielinski,

K. Matczyszyn, P. Tauc and J. Zyss, Biopolymers, 2011, 95,365–375.

22 T. K. Sau and C. J. Murphy, Langmuir, 2004, 20, 6414–6420.23 D. A. Zweifel and A. Wei, Chem. Mater., 2005, 17, 4256–4261.24 J. Olesiak, K. Matczyszyn, H. Mojzisova, M. Zielinski,

D. Chauvat and J. Zyss,Mater. Sci.-Poland, 2009, 27, 813–823.25 I. I. Smalyukh, O. V. Zribi, J. C. Butler, O. D. Lavrentovich and

G. C. L. Wong, Phys. Rev. Lett., 2006, 96, 177801.26 J. Olesiak-Banska, M. Gordel, R. Kolkowski, K. Matczyszyn

and M. Samoc, J. Phys. Chem. C, 2012, 116, 13731–13737.27 H. Yoshida, Y. Tanaka, K. Kawamoto, H. Kubo, T. Tsuda,

A. Fujii, S. Kuwabata, H. Kikuchi and M. Ozaki, Appl. Phys.Express, 2009, 2, 12501.

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:19:

34.

View Article Online

28 R. Bitar, G. Agez and M. Mitov, So Matter, 2011, 7, 8198–8206.

29 D. Coursault, J. Grand, B. Zappone, H. Ayeb, G. Levi, N. Felidjand E. Lacaze, Adv. Mater., 2012, 24, 1461–1465.

30 J. Olesiak-Banska, P. Hanczyc, K. Matczyszyn, B. Norden andM. Samoc, Chem. Phys., 2012, 404, 33–35.

31 K. Imura and H. Okamoto, J. Phys. Chem. C, 2009, 113,11756–11759.

32 P. Zijlstra, J. W. M. Chon and M. Gu, Phys. Chem. Chem.Phys., 2009, 11, 5915–5921.

33 A. Bouhelier, R. Bachelot, G. Lerondel, S. Kostcheev, P. Royerand G. P. Wiederrecht, Phys. Rev. Lett., 2005, 95, 267405.

34 G. V. Hartland, Chem. Rev., 2011, 111, 3858–3887.35 M. B. Mohamed, T. S. Ahmadi, S. Link, M. Braun and

M. A. El-Sayed, Chem. Phys. Lett., 2001, 343, 55–63.

This journal is ª The Royal Society of Chemistry 2013

36 M. Hu and G. V. Hartland, J. Phys. Chem. B, 2002, 106, 7029–7033.

37 S. Link, A. Furube, M. B. Mohamed, T. Asahi, H. Masuharaand M. A. El-Sayed, J. Phys. Chem. B, 2002, 106, 945–955.

38 G. Baffou and H. Rigneault, Phys. Rev. B: Condens. MatterMater. Phys., 2011, 84, 035415.

39 W. J. Roff, J. R. Scott and J. Pacitti, Fibres, lms, plastics andrubbers: a handbook of common polymers, Butterworths,London, 1971.

40 P. M. Hansen, V. K. Bhatia, N. Harrit and L. Oddershede,Nano Lett., 2005, 5, 1937–1942.

41 M. Fedoruk, A. A. Lutich and J. Feldmann, ACS Nano, 2011, 5,7377–7382.

42 S. Elhadj, G. Singh and R. F. Saraf, Langmuir, 2004, 20, 5539–5543.

Nanoscale, 2013, 5, 10975–10981 | 10981