Hybrid Silver Nanocubes for Improved Plasmon ... - ACS Publications

Subscriber access provided by University of Winnipeg Library

Article

Hybrid Silver Nanocubes for Improved Plasmon-Enhanced Singlet Oxygen Production and Inactivation of Bacteria Nicolas Macia, Roger Bresoli-Obach, Santi Nonell, and Belinda J. M. Heyne J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b12206 • Publication Date (Web): 09 Dec 2018 Downloaded from http://pubs.acs.org on December 9, 2018

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Journal of the American Chemical Society

Hybrid Silver Nanocubes for Improved Plasmon-Enhanced Singlet Oxygen Production and Inactivation of Bacteria Nicolas Maciaa, Roger Bresoli-Obachb, Santi Nonellb, Belinda Heynea* aDepartment bInstitut

of Chemistry, University of Calgary, Alberta, Canada.

Quimic de Sarria, Universitat Ramon Llull, Barcelona, Spain.

ABSTRACT: Plasmonic nanoparticles can strongly interact with adjacent photosensitizer molecules, resulting in significant alteration of their singlet oxygen (1O2) production. In this work, we report the next generation of metal-enhanced 1O2 nanoplatforms exploiting the lightning rod effect, or plasmon hot spots, in anisotropic (non-spherical) metal nanoparticles. We describe the synthesis of Rose Bengal decorated silica-coated silver nanocubes (Ag@SiO2-RB NCs) with silica shell thicknesses ranging from 5 to 50 nm based on an optimized protocol yielding highly homogeneous Ag NCs. Steady-state and time-resolve 1O2 measurements demonstrate not only the silica shell thickness dependence on the metal-enhanced 1O2 production phenomenon, but also the superiority of this next generation of nanoplatforms. A maximum enhancement of 1O2 of approximately 12-fold is observed with a 10 nm silica-shell, which is amongst the largest 1O production metal enhancement factor ever reported for a colloidal suspension of nanoparticles. Finally, the Ag@SiO 2 2 RB NCs were benchmarked against Ag@SiO2-RB nanospheres previously reported by our group, and the superior 1O2 production of Ag@SiO2-RB NCs resulted in improved antimicrobial activities in photodynamic inactivation experiments using both gram-positive and -negative bacteria model strains.

INTRODUCTION Noble metal nanomaterials possess rich and intriguing optical properties which have triggered their use in a wide range of fields, from optoelectronics1,2 and spectroscopy3–5 to imaging6–8 and sensing.9–11 This interest for metal nanostructures originates from their ability to support a localized surface plasmon resonance, i.e. they can confine and enhance incident light within their volume due to the collective oscillations of the conduction band electrons upon interaction with an external electromagnetic field.12,13 The enhanced electromagnetic field near these nanoparticles’ surface has been shown to promote a plethora of photophysical processes, including Raman scattering,14,15 fluorescence,16–18 Föster resonance energy transfer,19 phosphorescence20 and singlet oxygen (1O2) 21–24 production. Singlet oxygen is the lowest and most stable excited state of molecular oxygen and is a highly reactive species.22,25 Despite its minute size, 1O2 is a broadly used chemical reagent and a well-known cytotoxic agent.25–27 Singlet oxygen is most commonly produced by photosensitization, a process involving a photosensitizer molecule which produces 1O2 upon light exposure via

energy transfer.26,27 The possibility of enhancing 1O2 production using metal nanostructures has been a driving force to improve applications for which 1O2 is key, such as for the development of more effective methods in photodynamic therapy of cancer10,28 and in antimicrobial photodynamic inactivation of microorganisms (PDI).27 Indeed, when 1O2 is generated nearby or within tumor cells and micro-organisms, it can readily react with diverse cellular targets, causing deleterious damages to their structural integrity, which will ultimately lead to their inactivation and death.29,30 However, many photodynamic agents suffer from several drawbacks, such as their tendency to aggregate in biological media, their poor cellular uptake and lowto-moderate 1O2 yield.31,32 Plasmon enhanced 1O2 production, which results from the plasmonic coupling between photosensitizers and noble metal nanoparticles, is a promising method to increase the effectiveness of PDI. The factors affecting the extent of such plasmonic coupling are numerous and include, but are not limited to, the degree of spectral overlap between the surface plasmon band and the absorption profile of the molecule of interest,33 its triplet and 1O2 production

1 ACS Paragon Plus Environment

Journal of the American Chemical Society 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

quantum yield21 and the metal nanostructure size, shape and composition.34–37 Another critical parameter to control is the separation distance between the molecule and the metal surface, which needs to be within a suitable range to ensure a maximal enhancement, typically between 10-20 nm.24,38,39 To date most plasmon enhanced 1O2 production systems reported consist of nanoparticles immobilized on solid substrates, strongly limiting their application.40–42 More recently, few hybrid plasmonic nanostructures modified with photosensitizers in colloidal suspensions, including our own, have been reported for inactivating bacteria.24,33,43– 46 Amongst those, silver and gold nanospheres are the most widely used nanostructures for plasmon enhanced 1O production applications. Although these systems 2 have been shown to lead to reasonable enhancement of 1O production, in the current study, we hypothesized 2 that the use of anisotropic, i.e. non-spherical, nanostructures could represent a new avenue to design more efficient nanoplatforms for metal enhanced 1O2 production. Indeed, engineering anisotropy in metal nanoparticles has been shown to be a powerful approach to boost the efficiency of several plasmonenhanced phenomena, such as SERS47–49 and plasmonenhanced fluorescence.37,50–52 In particular, anisotropic nanoparticles that bear corners and edges can localize stronger near-field enhancement at their vertices due to the so called lightning rod effect, which results from the accumulation of electronic charges at the nanoparticle tips.49 Photophysical processes in molecules located in proximity to these regions of high intensity plasmonic fields, also known as “hot-spots”, can experience enormous enhancement, e.g. in the range of 101-102 for fluorescence10 and up to 105-108 for Raman scattering.14 Here, we report a hybrid nanoparticle system decorated with a photosensitizer that exploits the lightning rod effect as the next generation of metal enhanced 1O2 nanoplatforms. First, we describe the synthesis of Rose Bengal (RB) decorated silica-coated silver nanocubes (Ag@SiO2-RB NCs). Silver nanocubes (Ag NCs) were selected as an anisotropic core morphology, while silica was chosen as a rigid spacer as its thickness can be easily tuned, here from approximately 5 to 50 nm, to achieve the optimal separation distance and maximize 1O2 production. Silica can also be easily modified with amino functional groups onto which RB can be conjugated via carbodiimide crosslinking chemistry. The 1O2 production was monitored using two different detection techniques, namely direct and indirect. The former relies on the intrinsic phosphorescence emission of 1O2 at 1270 nm whereas the latter follows the photobleaching reaction of a 1O2 sensitive probe. Previously, we have used a similar methodology to successfully optimize RB

Page 2 of 12

decorated silica-coated silver nanospheres (Ag@SiO2RB NSs) for metal-enhanced 1O2 production.24 Here, we show that the maximum 1O2 production enhancement reached with the Ag@SiO2-RB NCs exceeds the one reported for the NSs. We explain this improvement in terms of the lighting rod effect considering that Ag NCs support a higher enhanced local electric field magnitude at its corners compared to the Ag NSs, as shown by finite-difference time-domain simulations. Building on these results, we benchmarked the antimicrobial efficiency of the Ag@SiO2-RB NCs reported here against Ag@SiO2-RB NSs in photodynamic inactivation experiments on both Staphylococcus aureus (grampositive) and Escherichia coli (gram-negative) bacteria strains. Overall, our results demonstrate that the Ag@SiO2-RB NCs show superior performance than the Ag@SiO2-RB NSs in terms of metal enhanced 1O2 production and inactivation of both gram-types of bacteria.

RESULTS AND DISCUSSION Nanoparticle design. Hybrid nanocubes were synthesized according to the protocol illustrated in scheme 1. First, silver nanocubes (Ag NCs) were prepared by an optimized variation of the sulfidemediated polyol method using CF3COOAg as silver precursor (Figures S1-S4).53,54 Using our optimized protocol, the prepared Ag NCs have an edge length of 44 4 nm with ca. 14 nm radius of curvature at the edges (Figure 1c), which is in the typical range of sizes used in metal-enhanced studies. The normalized extinction spectrum of Ag NCs in Figure 1a displays a strong and narrow plasmon dipole resonance at 442 nm, indicative of a small nanoparticle size distribution, as well as two other surface plasmon mode resonances at 380 and 347 nm, consistent with the extinction spectra of Ag NCs of similar sizes previously reported.54 The synthesis of homogeneous and monodispersed anisotropic metal nanoparticles is notoriously challenging.55–57 However, we were able to obtain monodispersed and homogeneous Ag NCs in high yields by controlling the concentration of iron (Fe) in the ethylene glycol used as a solvent, which is known to act as an oxidative etchant during the polyol synthesis of Ag NCs (see section 1 in the Supporting Information).58 Rose Bengal, which is a FDA approved photodynamic therapy drug, was chosen as a singlet oxygen (1O2) photosensitizer for this study due to its high 1O2 quantum yield ( = 0.75 in H2O) and for its absorbance profile with a λ max located at 549 nm.59 According to previous publications, it is crucial to select a dye that has some degree of spectral overlap with the nanoparticle surface plasmon band for optimal metal enhanced phenomena.33


Page 3 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Journal of the American Chemical Society Figure 1. a) Normalized extinction spectrum of the Ag NCs. b) Zeta-potentials of Ag NCs, silica-coated Ag NCs, aminated silica-coated Ag NCs and RB decorated silicacoated Ag NCs. c) TEM image of Ag NCs. d-h) TEM images of silica-coated Ag NCs with increasing silica-shell thicknesses. Scale bars = 50 nm.

TEOS NH4OH

APTES

IPA/H2O

EtOH

O O Si O

NH2

EDC.HCl RB pH = 6

O

O O Si O

I

Cl

Cl Cl

N H

Cl I

O I

O I

OH

Scheme 1. Attachment of Rose Bengal (RB) to silver nanocubes. The silver nanocubes were first coated with silica via the base -catalyzed Stöber process and aminated with APTES. Rose Bengal was conjugated to the aminated nanoparticles using carbodiimide crosslinking with EDC in buffered conditions. The Ag NCs were then coated with a silica layer via a base-catalyzed Stöber process (Scheme 1). Silica was chosen as a coating agent, as it presents low cytotoxicity, and it can be modified with a variety of functional groups.60 More importantly for plasmonic-enhanced phenomena where distance is key, silica can act as a solid spacer with tunable thickness between the metal core and the dye.

Figure 2. a) UV-visible absorbance spectra of the Ag@SiO2RB NCs (red) and their etched counterparts (blue). b) TEM image of the etched nanoparticles. Scale bar = 50 nm.

The hydrolysis and condensation chemistry of silica polymerization around nanoparticles can be easily controlled by finely tuning the concentration of the silicate (tetraethyl orthosilicate, TEOS) added during the coating process. The silica-coated Ag NCs (Ag@SiO2 NCs) were characterized by TEM and UV-visible spectroscopy. Size analysis of the TEM images of the Ag@SiO2 NCs (Figure 1d-h) revealed that by varying the TEOS concentration between 26 and 760 µM, we obtained average silica shell thicknesses of 5.1 0.7 nm (sample A), 9.8 0.8 nm (sample B), 15.0 1.5 nm (sample C), 28.8 1.8 nm and 49.0 2.0 nm (sample E; see Figure S5 and Table S1 in the Supporting Information for details). Importantly, the Ag NC cores preserved their cubic morphology once coated with silica (Figure 1d-h). Then, the Ag@SiO2 NCs were aminated with (3aminopropyl)triethoxysilane (APTES, scheme 1), as confirmed by Zeta ()-potential measurements. Indeed, Ag@SiO2-NH2 NCs present a shift from a negative potential value to a positive one upon amination due to the presence of protonated amino groups on the



nanoparticles’ surface in water at pH = 6 (Figure 1b). The final stage of the nanoparticles’ functionalization consists of the dye conjugation on the Ag@SiO2-NH2 NCs via carbodiimide crosslinking reaction (scheme 1). The carboxylate moiety of RB was conjugated to the amino functional group on the nanoparticles’ surface with N-(3-dimethylaminopropyl)-N’-ethylcarbodiimide hydrochloride (EDC HCl) as a crosslinking agent in MES buffered solution at pH = 6. The resulting Ag@SiO2-RB NCs present a negative -potential value due to masking of the amino groups when the dye is tethered on the nanoparticle’s surface (Figure 1b). The RB absorbance profile can also be seen on the surface plasmon band in the extinction spectra of the synthesized Ag@SiO2-RB NCs (Figures 2a, S6). The dye loading on the nanoparticles’ surface was quantitatively calculated from the number of unreacted RB molecules left in the supernatants during the purification step of the Ag@SiO2-RB NCs by centrifugation following the crosslinking reaction. The RB surface coverage was kept low, ranging from 23% to 5% of the maximum expected values for 5 to 50 nm shell thickness, respectively (see the Supporting Information for more details, Figure S7). The decrease in surface coverage is not surprising considering that the concentrations in APTES and RB were kept constant for each silica shell size, while the overall nanoparticle’s surface area is increased for bigger silica shells. This difference in surface coverage will be taken into consideration in the remainder of the study (vide infra). Metal-enhanced 1O2 production. In order to quantify the influence of the metal-core on the 1O2 production from the dye bound on the nanoparticle’s surface, one has to compare its 1O2 production to a control sample. This control sample has to reflect the 1O2 production in comparable conditions to that in the system of study but in the absence of any metal-dye interactions. Finding such a control sample to study plasmon-enhanced phenomena is challenging, and many approaches have been suggested in the literature. For instance, Jang et al. and Ke et al. have compared their nanoparticles with an equivalent concentration of free dyes in solution.61,62 However, a bound photosensitizer does not necessarily have the same 1O2 production ability than a free one, and therefore can lead to either an over or under-estimation of the metal enhancement effect.63 Other methods include synthesizing control silica nanoparticles decorated with the dye.39 However, using this approach, one has to finely control the size of the silica nanoparticles as well as the dye loading on its surface. A more convenient approach consists of dissolving the metal core using a strong etching agent, such as cyanide ions or nitric acid, producing coreless nanoshells, or “etched” nanoparticles.64,65 Although

Page 4 of 12

providing a more representative control sample (same nanoparticle and photosensitizer concentrations, same photosensitizer surface coverage), these strong etching agents might also release the photosensitizers from the nanoparticles surface by cleaving the dye-nanoparticle bond. Fortunately, in the case of silver-silica core-shell nanoparticles, it has been shown that a “softer” etching reagent, chloride ions can be used.19,23,24,66 Therefore, to confirm the influence of the Ag NC on RB 1O2 photosensitization, the control sample used in this study were prepared from the Ag@SiO2-RB NCs by dissolving the Ag cores with addition of chloride ions from sodium chloride. The etching resulted in the disappearance of the plasmon band (Figures 2a, S6, Table S2). TEM imaging of the etched nanoparticles also offers strong evidence that the etching procedure was successful as the Ag NC cores have been dissolved to produce hollow etched nanoparticles (Figure 2b). Furthermore, the difference in surface coverage between each sample mentioned earlier is accounted for when comparing the hybrid Ag NCs samples to their etched counterparts.

Figure 3. a) Representative singlet oxygen time-resolved phosphorescence signal monitored at 1270 nm of RBAg@SiO2 NC (B, red) and of its etched counterpart (blue) in air-equilibrated aqueous solution and their corresponding bi-exponential fittings. b) Representative photobleaching of ABDA followed at 380 nm as a function of the irradiation time of sample RB-Ag@SiO2 NC (B, red) and its etched


Page 5 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


counterpart (blue) in air equilibrated aqueous solution and their corresponding linear fittings.

The 1270 nm time-resolved 1O2 luminescence signals were obtained for all the Ag@SiO2-RB NCs samples (A to E) and their etched counterparts (Figure 3a, S8-S9 and Supporting Information for details). These signals illustrate the effect of the Ag NC core on the RB 1O2 production. Quantitative information was extracted from the signals, and we obtained three key parameters, namely the singlet oxygen lifetime (), the RB triplet state lifetime (T) and the signal intensity (S0) (See section 2 in Supporting Information for more details). Both the Ag@SiO2-RB NCs and their etched counterparts remained stable after irradiation with a 532 nm laser for 10 minutes during the course of the measurement (Figure S10). Values of  and T are in good agreement with the typically reported values in air-equilibrated water (Table S3). Also, the lifetimes were independent to the presence or absence of a metal core and to the silica shell thickness (Figure S11). This result is reminiscent of the one obtained in our previous study and is not surprising.24 Since 1O2 lifetime is largely dominated by the non-radiative decay of 1O2, even a significant increase in the radiative component would leave 1O2 lifetime unchanged. The capability of the Ag@SiO2-RB NCs and their etched counterparts to produce 1O2 was also evaluated indirectly by using 9,10-anthracenediylbi(methylene)dimalonic acid (ABDA) as a chemical trap. The Ag@SiO2-RB NCs produce more 1O2 than the etched nanoparticles for all samples, as shown by a faster photobleaching rate of the probe when exposed to the same irradiation conditions (Figure 3b, S12-S13). Controls have been performed to ensure that the photobleaching of ABDA resulted only from its reaction with 1O2 (Figure S14). Also, metal nanostructures have been shown to photosensitize 1O2 on their own.67 However, we have carried out control experiments on both Ag@SiO2 NCs and Ag NCs using both detections approaches and neither show any 1O2 production (Figure S15). Therefore, the 1O2 detected here via direct and indirect means can be attributed to its production by photosensitization of the RB attached onto the surface of the nanoparticles.

Figure 4. Singlet oxygen enhancement factors as a function of the separation distance (silica shell thickness) between the Ag NC core and RB obtained by direct (green diamonds) and indirect (orange hexagons) detection methods.

The effect of the metal core on the 1O2 production by RB was evaluated by determining an enhancement factor, EF. For the direct detection of 1O2 luminescence, EFdirect is defined as the ratio of the signal intensity, S0 for the Ag@SiO2-RB NCs to the S0 for their corresponding etched equivalents. On the other hand, EFindirect is obtained by fitting the pseudo-first order kinetics of ABDA photobleaching with a linear regression and is defined as the ratio of the slope of ABDA photobleaching with Ag@SiO2-RB NCs to the slope obtained with their corresponding etched equivalents (see the Supporting Information for details).

Figure 5. Comparison of the peak EF values for the Ag@SiO2-RB NCs (B) and the Ag@SiO2-RB NSs obtained by direct and indirect detection. EF values of Ag@SiO2-RB NSs is from Ref. 24. The other values are from this work.

The EF calculated for all the samples using either of the techniques reveal a dependence of metal enhanced 1O production on the separation distance between the 2 metal core and the photosensitizer (Figure 4), similar to



the one observed for other reported systems. For short separation distances between the Ag NC core and RB, the EF is close to unity. Then, EF reaches a maximum at a silica shell size of 10 nm. At larger separation distances, EF quickly decreases: EFindirect reaches 1 at 50 nm while EFdirect remains slightly above 1; an effect which is attributed to enhanced scattering from larger nanoparticles. Although they follow the same trend, the EF values obtained by the two different detection techniques differ in magnitude, as observed in our previous study.24 This is not surprising as the indirect detection methodology using a chemical trap provides only the total amount of 1O2 available for reaction in solution, while the direct methods reports on the amount of singlet oxygen and the radiative decay probability. It is worth highlighting that the EFdirect of 12.2 achieved with the Ag@SiO2-RB NCs at 10 nm shell thickness obtained here is amongst the largest 1O2 metal enhancement factor ever reported for a colloidal suspension of nanoparticles. To confirm the advantages of using a cube-based nanoparticle instead of a sphere-based system for metal enhanced 1O2 production, we have benchmarked the Ag@SiO2-RB NCs (B) to the Ag@SiO2-RB NSs coated with a 10 nm silica shell reported in an earlier publication by our group. For both the EFindirect and the EFdirect, the values reported24 for the Ag@SiO2-RB NSs, 1.6  0.4 and 10.3 0.3, respectively are smaller than the ones obtained for the Ag@SiO2-RB NCs of 4.0  0.1 and 12.2  0.5, respectively (Figure 5). The shape of the nanoparticle is responsible for the improved plasmonic enhancement effect. Indeed, the inhomogeneous distribution of localized surface plasmon fields in anisotropic nanoparticles which possesses morphological features such as sharp apexes and tips can lead to the formation of plasmonic hot spots which originate from the so-called lightning rod effect (vide supra). These hot spots typically lead to a stronger enhancement in the local electric field of plasmonic nanomaterials.14,49 3-Dimensional simulations of the enhanced electric field by finite-difference time-domain (FDTD) theoretically predicts a 1.5-time stronger enhancement from our modeled Ag nanocube compared to the Ag nanosphere under the same excitation conditions (Figures S16-17). Care was taken to model the Ag nanocube with rounded corners to be more representative to the actual nanoparticles synthesized, as sharper corners would lead to an over estimation of the enhanced field values. The computed enhanced field value is consistent with the stronger EF value of about 1.2-fold measured for the1O2 luminescence signals of Ag@SiO2-RB NCs (B) compared to the Ag@SiO2-RB NSs, showing that nanostructures

Page 6 of 12

with plasmonic hot spots make better metal enhanced 1O producers. 2 Metal enhanced 1O2 production for improved photodynamic inactivation of bacteria. The enhanced 1O production of the hybrid plasmonic nanoparticles 2 makes them great candidates for improved photodynamic inactivation of bacteria (PDI). We sought to compare the antimicrobial efficiency of the Ag@SiO2RB NCs (B) to the one of Ag@SiO2-RB NSs against two strains of model bacteria, gram-positive S. aureus and gram-negative E. coli. Ag@SiO2-RB NSs were synthesized according to the literature, yielding a Ag NSs core with a diameter of 67 10 nm and a silica shell thickness of 11 1 nm, as determined by TEM (Figure S18a). The spectral overlap between RB and the surface plasmon band of the Ag NSs is equivalent to the one with the surface plasmon band of the Ag NCs (Figure S18b). Similar RB surface coverages were obtained for Ag@SiO2-RB NCs (B, 17%) and Ag@SiO2-RB NSs (13%), and sample concentrations were adjusted to achieve equivalent photosensitizer concentration when performing the experiments (see the Supplementary Information for more detail). The bacteria were incubated with a final RB concentration equivalent to 1.1 µM for 30 minutes prior irradiation with green LEDs (520 nm) at room temperature. Interestingly, the nanoparticles display almost no dark cytotoxicity against the bacteria (Figure 6). This was confirmed by incubating the nanoparticles with the bacteria in the dark for the same time intervals and no decrease in cell colonies was observed (Figure S19). Also, the etched counterparts of Ag@SiO2-RB NCs (B) and NSs have also been tested against both S. aureus and E. coli (Figure S19). They display low antimicrobial efficiencies against both strain of bacteria with reduction of 2-log10 and 1-log10 after the longest irradiation period when tested against S. aureus and E. coli, respectively. The antimicrobial efficiencies of the etched nanoparticles are comparable to the ones obtained for free RB under the same irradiation conditions and at the same working concentration of 1.1 µM than in the nanoparticle samples (Figure 6). These results reflect that the nanoparticles themselves do not act as an antimicrobial agent but rather just as a platform to carry RB and to boost its 1O2 production.


Page 7 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Journal of the American Chemical Society observed (Figure S20). Finally, silver nanoparticles by themselves have been shown to kill bacteria by two possible means: i) the release of toxic Ag ions70 and ii) the heat generation via the photothermal effect when irradiated.71 Thus, controls with the Ag@SiO2 NCs (B) and NSs have been performed on both E. coli and S. aureus and we found that cell viability was not affected even at the longest irradiation times, once again confirming that the photodynamic action of both nanoparticles studied is due only to the 1O2 production by RB, at the nanoparticle’s concentrations used (Figure S20).

CONCLUSION

Figure 6. Survival curves of S. aureus (a) and E. coli (b) with Ag@SiO2-RB NCs (B, red squares), Ag@SiO2-RB NSs (brown circles) and 1.1 µM RB as a control (black triangles) under green LED irradiation.

The Ag@SiO2-RB NCs (B) demonstrate a remarkable full inactivation (7-log10 reduction in colony forming units) of S. aureus after 2 hours of green light irradiation, compared to a 3-log10 decrease in the cellular survival for the RB-Ag@SiO2 NSs under the same conditions (Figure 6a). A similar trend is observed against E. coli, for which the Ag@SiO2-RB NCs (B) achieve a viability decrease of 6-log10 after 220 minutes of irradiation, compared to a milder 4-log10 inactivation when the cells were incubated with the RB-Ag@SiO2 NSs (Figure 6b). The latter results are not surprising considering that gram-negative bacteria, such as E. coli, are well known to be less susceptible to PDI than gram-positive bacteria due to their more complex outer membrane structure. Other important parameters to consider when comparing different nanoparticles in PDI experiments are their hydrodynamic (Z) diameters and potentials.68,69 Here, the Z-diameters, determined by DLS, and -potentials for both nanoparticles tested are within the same range which minimizes potential differences in cellular uptakes and therefore, cannot account for the differences in antimicrobial efficiency

In conclusion, we have developed a new generation of hybrid nanoparticles modified with a photosensitizer to boost its 1O2 production based on anisotropic metal nanostructures. We prepared Rose Bengal decorated silica-coated silver nanocubes (Ag@SiO2-RB NCs) with tunable separation distance between the metal core and the photosensitizer. The effect of the Ag NC core on Rose Bengal’s 1O2 production was investigated using both direct and indirect detection methods, which resulted in remarkable 12.2-fold and 4.0-fold enhancement factors maxima, respectively at an optimal silica shell thickness of 10 nm. These enhancement factor values are higher than the ones previously reported for Ag nanosphere (NS)-based plasmonic platform for metal enhanced 1O2 production. The benefits of the anisotropic Ag NC core were correlated with FDTD simulation results, indicating that the local enhanced electric field of Ag NCs is 1.5 times stronger than the one for Ag NSs, which contributes to a stronger metal enhanced 1O2 production. In addition, we also benchmarked the Ag@SiO2-RB NSs to the new Ag@SiO2-RB NCs for photodynamic inactivation of gram-positive S. aureus and gram-negative E. coli bacteria. The Ag@SiO2-RB NCs exhibited better antimicrobial efficiencies against both bacteria strains tested. The Ag@SiO2-RB NCs reported herein represents a first proof-of-concept where we can exploit the intrinsic electromagnetic hotspots produced by the lightning rod effect in anisotropic metal nanoparticles to design a new and promising generation of plasmonic hybrid nanoparticles that boost 1O2 production. Altogether, our results pave the way to using more complex anisotropic nanoparticles that have been shown to produce even larger enhanced electric fields, such as higher polyhedral nanocrystals and branched nanostructures, to design better plasmonic-based antimicrobial agents.

EXPERIMENTAL SECTION



Synthesis of Ag NCs. Silver nanocubes (Ag NCs) were prepared using Xia’s sulfide-mediated polyol synthesis procedure with slight modifications. In a typical synthesis, 10 mL ethylene glycol was placed in a 100 mL aqua regia cleaned round bottom flask, capped and heated with stirring in an oil bath at 150 C for 30 minutes. Then, 100 µL 3.0 mM NaSH.xH2O, 1.0 mL 3.0 mM HCl and 2.5 mL 25 mg/mL PVP-55,000 (all solutions were freshly made in ethylene glycol) were sequentially injected in the flask. Two minutes later, 800 µL 282 mM CF3COOAg in ethylene glycol was quickly added to the solution. The flask was then recapped and heated for an additional hour. Progression in colors was observed from colorless to bright yellow after 2 minutes to orange after 20 minutes to dark brown when the reaction was completed (Figure S4). The reaction was quenched by placing the flask in an ice bath for 20 minutes. The Ag NCs were isolated and purified by adding 20 mL anhydrous ethanol to the flask and centrifuging at 5,000g during 75 minutes. The resulting pellets were re-suspended in ethanol and further centrifuged twice. The resulting Ag NCs were finally re-suspended in 12 mL anhydrous ethanol and kept in a plastic test tube at 4 C. The Ag NCs were stable under such storage conditions for at least one month. Synthesis of Ag@SiO2 NCs. 2 mL of the as prepared Ag NCs were centrifuged at 11,000g for 10 minutes and resuspended in 2 mL of ultrapure water. The resuspended Ag NCs were quickly added to a 50 mL polyproylene tube containing 20 mL of isopropanol, 2 mL of ultrapure water and 400 µL of NH4OH 30%, followed by the controlled addition of freshly made TEOS solution by using a pressure-controlled syringe pump (Fusion 100, Chemyx Inc., Stafford). The concentrations and volumes of TEOS as well as the addition rates used to obtain each silica shell thickness are listed in Table S1 in the Supplementary Information. Following the addition of TEOS, the solution was stirred at room temperature for an addition 2 hours prior collecting them by three cycles of centrifugation (1 hour, 5,000g) and resuspension in 10 mL anhydrous ethanol. Synthesis of Ag@SiO2-RB NCs. First, the Ag@SiO2 NCs were modified with amino functional groups. Ten µL APTES were added at 2 µL/minute in 5 mL of the previously synthesized Ag@SiO2 NCs. The mixture was stirred at room temperature for 1-hour prior being stirred at 65 C for 1 hour. Then, the solution was further stirred at room temperature for 12 hours. The Ag@SiO2-NH2 NCs were then centrifuged (30 minutes, 5,000g) and washed with anhydrous ethanol 3 times and kept at 4 C. Second, RB was conjugated to the Ag@SiO2NH2 NCs by a carbodiimide crosslinking. Thirteen mg of EDC were dissolved in 6 mL of 5.3 µM RB in MES buffer (pH 6.00). The solution was stirred at room temperature for 20 minutes before adding the Ag@SiO2-NH2 NCs resuspended in 5 mL MES buffer. The mixture was stirred for an additional 3 hours at room temperature. The Ag@SiO2-RB NCs were collected by centrifugation (30 minutes, 4,500g) and were washed with ultrapure water 3 times. The Ag@SiO2-RB NCs were finally resuspended in 6 mL of ultrapure water and stored in a 15 mL polypropylene tube in the dark at 4 C until further use. Etching of the nanoparticle cores. Volumes of Ag@SiO2RB NCs were diluted with ultrapure water to the desired concentrations for analysis and mixed with various NaCl concentrations depending on the sample silica-shell thickness (see Table S2 in the Supplementary Information for volumes of

Page 8 of 12

nanoparticles and concentrations of NaCl used for each samples). The samples were mixed on an orbital shaker for 12 hours at room temperature and in the dark. Nanoparticles characterization. The nanoparticle samples were well sonicated before each characterization. The UVvisible extinction spectra were recorded with a spectrophotometer (Cary 50, Varian, Palo Alto, CA). The size and the morphology of all the nanoparticles were investigated with a transmission electron microscope (H-7650, Hitachi High Technologies, Pleasanton, CA) operating at 80 kV. 10 µL of the samples were drop-casted on glow-discharged carbon coated 300 square mesh grids (Electron Microscopy Sciences, Hatfield, PA). Particle size distribution was evaluated by analyzing the images with ImageJ. The zeta-potential and dynamic light scattering measurements were performed on a Nano-ZS Zetasizer (Malvern Instruments, U.K.). Indirect detection of 1O2. The production of 1O2 was followed by monitoring the photobleaching reaction as a function of the irradiation time of the water-soluble 1O2 specific probe ABDA mixed with the nanoparticle samples in airequilibrated ultrapure water by UV-visible absorption spectroscopy. A final concentration of 0.1 mM ABDA was added to the sample. The samples were irradiated with a slide projector (Kodak, Rochester, NY) equipped with an Osram EXR halogen light bulb (300 W, 82 V) and a longpass colored glass filter (435 nm cut-on wavelength). All measurements were performed in triplicates. Direct detection of 1O2. Singlet oxygen 1270 nm phosphorescence kinetic traces were acquired with a timeresolved near-infrared (TRNIR) detection system. A diodepumped Nd:YAG laser (FTSS355-Q3, CryLas, Germany) working at 1 kHz repetition rate and tuned at 532 nm was used as the excitation source for RB. A 1150 nm cut-on longpass filter (FEL1150, ThorLabs, Newton, NJ) and a 1064 nm notch filter (NF1064-44, ThorLabs) were mounted side by side at the entry port of a monochromator (Digikröm CM110 1/8 m, Spectral Products, Putnam, CT). A TE-cooled PMT (model H10330A-45, Hamamatsu, Japan) working at -908 V was used as the detector at the exit port of the monochromator. The PMT output was amplified to a voltage pulse using a 1.1 GHz preamplifier module (PAM-102-T, PicoQuant GmbH, Germany) connected to a multichannel scaler (TimeHarp 260-Nano, PicoQuant). The signal monitored at 1270 nm was collected for 600 s with 256 ns resolution for each time-resolved 1O2 emission curves recorded. The time resolved curves were chi-squared fitted to equation (1) using Prism 7.0 (GraphPad Software Inc., La Jolla, CA) with , T and S0 as free parameters. The goodness of the fittings was assessed by the residual plots. 

( ( ) ― exp ( ))

S(t) = 𝑆0( ― ) exp  T

―t

―t



T

(eq. 1)

FDTD simulations. FDTD is considered as a suitable technique in plasmonics to simulate the enhanced electromagnetic field of metal nanostructures when interacting with light. The simulations were performed with Lumerical FDTD Solutions (Lumerical, Vancouver, Canada). The computational domain was set to 120x120x120 nm3 with a grid spacing of 0.5 nm and was terminated with perfectly matched layers (PML). Mesh size was fixed at 0.5 nm with a conformal variant 1 refinement option which ensure a more accurate simulation at the metal/dispersive media interface. The complex dielectric function of silver was modeled according to


Page 9 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Palik’s database while the dispersion medium was set to the refractive index of water (1.33). Excitation was carried out by a total-field scattered-field source. The overall simulation was calculated over a frequency range of 300-700 nm. Photodynamic inactivation of bacteria. The bacteria strains selected were S. aureus ATCC6538 and E. coli ATCC25922. They were grown overnight in lysogeny broth (LB) medium at 37 C in an orbital shaking incubator stirring at 220 rpm. An aliquot from the stationary phase was grown in fresh LB to an optical density value of approximately 0.5-0.6 at 600 nm, which corresponds to ca. 107 colony forming units (CFU)/mL. Then, the bacteria suspensions were centrifuged (10 minutes, 3,000g) and resuspended in the same volume of sterile 0.01 M phosphate saline buffered (PBS, pH 7.4) 3 times. To test the nanoparticles antimicrobial activities, 3 mL of the bacterial suspensions were incubated with aliquots of Ag@SiO2-RB NCs and NSs coated with 10 nm silica shell thickness and their etched counterparts resuspended in sterile PBS. Care was taken to adjust the concentrations of nanoparticles to the same values. After incubating the bacteria with the nanoparticles in the dark for 30 minutes, 1.5 mL aliquots were placed in 24-well plates and irradiated from the top by a green (520 nm) LED exposure panel (EXPO-LED equipped with five 4 W LED lamp tubes, Luzchem, Ottawa, Canada). To determine the CFU, aliquots were taken from the well containing the bacteria/nanoparticles suspensions and serially diluted 101-106 in sterile PBS and then streaked on LB agar plates according to a method reported elsewhere.72 All the experiments and controls were performed in triplicates.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. List of the reagents used. Optimization of the synthesis of Ag NCs and their characterization: extinction spectrum and TEM image of Ag NCs obtained with higher iron content ethylene glycol (Figure S1), TEM of the Ag NCs (Figure S2), reproducibility tests (Figure S3), progression of the Ag NCs reaction colors (Figure S4), silica-shell thickness (Figure S5), experimental conditions to obtain different silica-shell thickness (Table S1), experimental details on the silver core etching procedure (Table S2), extinction spectra of the nanoparticles and their etched counterparts (Figure S6), Rose Bengal surface coverage (Figure S7). Singlet oxygen direct detection: time-resolved near-infrared signals at 1270 nm (Figure S8), the fitted parameters S0,  and T (Table S3), the fitting residuals (Figure S9), the nanoparticles’ extinction spectra before and after the laser irradiation (Figure S10) and the lifetimes as a function of the distance from the nanoparticle metallic core (Figure S11). Singlet oxygen indirect detection: reaction scheme of ABDA with 1O2 (scheme S1), absorption spectrum of ABDA photobleaching (Figure S12), ABDA photobleaching kinetics (Figure S13). Singlet oxygen detection control experiments (Figures S14-S15). FDTD simulations (Figure S16-S17). Extinction spectrum and TEM image of Ag@SiO2-

RB NSs (Figure S18). Photodynamic inactivation of S. aureus and E. coli control experiments (Figure S19-20).

AUTHOR INFORMATION Corresponding Author * [email protected]

ACKNOWLEDGMENT This work was supported by the Natural Sciences and Engineering Council of Canada (NSERC), the Canada Foundation for Innovation (CFI), the University of Calgary and the Spanish Ministerio de Economía y Competitividad, grant number CTQ2016-78454-C2-1-R. N.M. gratefully acknowledges NSERC for an Alexander Graham Bell Canada Graduate Scholarship-Doctoral and Alberta Innovates for a Nanotechnology Doctoral Scholarship.

REFERENCES (1)

(2)

(3)

(4)

(5)

(6)

(7)

(8)

(9)

(10)

(11)

(12)

Li, Z.; Clark, A. W.; Cooper, J. M. Dual Color Plasmonic Pixels Create a Polarization Controlled Nano Color Palette. ACS Nano 2016, 10 (1), 492–498. Han, J. H.; Kim, D.; Lee, T.-W.; Jeon, Y.; Lee, H. S.; Choi, K. C. Color Purifying Optical Nanothin Film for Three Primary Colors in Optoelectronics. ACS Photonics 2018, 5 (8), 3322–3330. Li, J.-F.; Li, C.-Y.; Aroca, R. F. Plasmon-Enhanced Fluorescence Spectroscopy. Chem. Soc. Rev. 2017, 46 (13), 3962–3979. Laing, S.; Jamieson, L. E.; Faulds, K.; Graham, D. SurfaceEnhanced Raman Spectroscopy for in Vivo Biosensing. Nat. Rev. Chem. 2017, 1, 60. Wonner, K.; Evers, M. V; Tschulik, K. Simultaneous Optoand Spectro-Electrochemistry: Reactions of Individual Nanoparticles Uncovered by Dark-Field Microscopy. J. Am. Chem. Soc. 2018, 140 (40), 12658–12661. Wang, K.; Shangguan, L.; Liu, Y.; Jiang, L.; Zhang, F.; Wei, Y.; Zhang, Y.; Qi, Z.; Wang, K.; Liu, S. In Situ Detection and Imaging of Telomerase Activity in Cancer Cell Lines via Disassembly of Plasmonic Core–Satellites Nanostructured Probe. Anal. Chem. 2017, 89 (13), 7262–7268. Liu, Y.; Yang, Z.; Huang, X.; Yu, G.; Wang, S.; Zhou, Z.; Shen, Z.; Fan, W.; Liu, Y.; Davisson, M.; et al. GlutathioneResponsive Self-Assembled Magnetic Gold Nanowreath for Enhanced Tumor Imaging and Imaging-Guided Photothermal Therapy. ACS Nano 2018, 12 (8), 8129– 8137. Reguera, J.; Jiménez de Aberasturi, D.; Henriksen-Lacey, M.; Langer, J.; Espinosa, A.; Szczupak, B.; Wilhelm, C.; LizMarzán, L. M. Janus Plasmonic–Magnetic Gold–Iron Oxide Nanoparticles as Contrast Agents for Multimodal Imaging. Nanoscale 2017, 9 (27), 9467–9480. Le, N. H.; Nguyen, B. K.; Ye, G.; Peng, C.; Chen, J. I. L. Tuning the Sensing Performance of Multilayer Plasmonic Core– Satellite Assemblies for Rapid Detection of Targets from Lysed Cells. ACS Sensors 2017, 2 (11), 1578–1583. Kumar, A.; Kim, S.; Nam, J. M. Plasmonically Engineered Nanoprobes for Biomedical Applications. J. Am. Chem. Soc. 2016, 138 (44), 14509–14525. Anker, J. N.; Hall, W. P.; Lyandres, O.; Shah, N. C.; Zhao, J.; Van Duyne, R. P. Biosensing with Plasmonic Nanosensors. Nat. Mater. 2008, 7 (6), 442–453. Scaiano, J. C.; Stamplecoskie, K. Can Surface Plasmon



(13) (14)

(15)

(16)

(17)

(18)

(19)

(20)

(21)

(22)

(23)

(24)

(25)

(26)

(27)

(28)

(29)

(30)

Fields Provide a New Way to Photosensitize Organic Photoreactions? From Designer Nanoparticles to Custom Applications. J. Phys. Chem. Lett. 2013, 4 (7), 1177–1187. Gray, S. K. Theory and Modeling of Plasmonic Structures. J. Phys. Chem. C 2013, 117, 1983–1994. Cardinal, M. F.; Vander Ende, E.; Hackler, R. A.; McAnally, M. O.; Stair, P. C.; Schatz, G. C.; Van Duyne, R. P. Expanding Applications of SERS through Versatile Nanomaterials Engineering. Chem. Soc. Rev. 2017, 46 (13), 3886–3903. Li, J.-F.; Zhang, Y.-J.; Ding, S.-Y.; Panneerselvam, R.; Tian, Z.-Q. Core–Shell Nanoparticle-Enhanced Raman Spectroscopy. Chem. Rev. 2017, 117 (7), 5002–5069. Anger, P.; Bharadwaj, P.; Novotny, L. Enhancement and Quenching of Single-Molecule Fluorescence. Phys. Rev. Lett. 2006, 96 (11), 113002. Ming, T.; Chen, H.; Jiang, R.; Li, Q.; Wang, J. PlasmonControlled Fluorescence: Beyond the Intensity Enhancement. J. Phys. Chem. Lett. 2012, 3 (2), 191–202. Aslan, K.; Gryczynski, I.; Malicka, J.; Matveeva, E.; Lakowicz, J. R.; Geddes, C. D. Metal-Enhanced Fluorescence: An Emerging Tool in Biotechnology. Curr. Opin. Biotechnol. 2005, 16 (1), 55–62. Lessard-Viger, M.; Rioux, M.; Rainville, L.; Boudreau, D. FRET Enhancement in Multilayer Core-Shell Nanoparticles. Nano Lett. 2009, 9 (8), 3066–3071. Zhang, Y.; Aslan, K.; Previte, M. J. R.; Malyn, S. N.; Geddes, C. D. Metal-Enhanced Phosphorescence: Interpretation in Terms of Triplet-Coupled Radiating Plasmons. J. Phys. Chem. B 2006, 110 (49), 25108–25114. Zhang, Y.; Aslan, K.; Previte, M. J. R.; Geddes, C. D. Plasmonic Engineering of Singlet Oxygen Generation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105 (6), 1798–1802. Macia, N.; Heyne, B. Using Photochemistry to Understand and Control the Production of Reactive Oxygen Species in Biological Environments. J. Photochem. Photobiol. A Chem. 2015, 306, 1–12. Mooi, S. M.; Heyne, B. Amplified Production of Singlet Oxygen in Aqueous Solution Using Metal Enhancement Effects. Photochem. Photobiol. 2014, 90 (1), 85–91. Planas, O.; Macia, N.; Agut, M.; Nonell, S.; Heyne, B. Distance-Dependent Plasmon-Enhanced Singlet Oxygen Production and Emission for Bacterial Inactivation. J. Am. Chem. Soc. 2016, 138 (8), 2762–2768. Ogilby, P. R. Singlet Oxygen: There Is Indeed Something New under the Sun. Chem. Soc. Rev. 2010, 39 (8), 3181– 3209. DeRosa, M. C.; Crutchley, R. J. Photosensitized Singlet Oxygen and Its Applications. Coord. Chem. Rev. 2002, 233–234, 351–371. Singlet Oxygen: Applications in Biosciences and Nanosciences; Nonell, S., Flors, C., Eds.; Comprehensive Series in Photochemical & Photobiological Sciences; Royal Society of Chemistry: Cambridge, 2016; Vol. 1. García Calavia, P.; Bruce, G.; Pérez-García, L.; Russell, D. A. Photosensitiser-Gold Nanoparticle Conjugates for Photodynamic Therapy of Cancer. Photochem. Photobiol. Sci. 2018. Brynildsen, M. P.; Winkler, J. A.; Spina, C. S.; MacDonald, I. C.; Collins, J. J. Potentiating Antibacterial Activity by Predictably Enhancing Endogenous Microbial ROS Production. Nat. Biotechnol. 2013, 31, 160. Wainwright, M.; Maisch, T.; Nonell, S.; Plaetzer, K.; Almeida, A.; Tegos, G. P.; Hamblin, M. R. Photoantimicrobials—Are We Afraid of the Light? Lancet Infect. Dis. 2017, 17 (2), e49–e55.

(31)

(32)

(33)

(34)

(35)

(36)

(37)

(38)

(39)

(40)

(41)

(42)

(43)

(44)

(45)

Page 10 of 12

Hamblin, M. R.; Hasan, T. Photodynamic Therapy: A New Antimicrobial Approach to Infectious Disease? Photochem. Photobiol. Sci. 2004, 3 (5), 436–450. Lovell, J. F.; Liu, T. W. B.; Chen, J.; Zheng, G. Activatable Photosensitizers for Imaging and Therapy. Chem. Rev. 2010, 110 (5), 2839–2857. Hu, B.; Cao, X.; Nahan, K.; Caruso, J.; Tang, H.; Zhang, P. Surface Plasmon-Photosensitizer Resonance Coupling: An Enhanced Singlet Oxygen Production Platform for BroadSpectrum Photodynamic Inactivation of Bacteria. J. Mater. Chem. B 2014, 2 (40), 7073–7081. Asselin, J.; Legros, P.; Grégoire, A.; Boudreau, D. Correlating Metal-Enhanced Fluorescence and Structural Properties in Ag@SiO2 Core-Shell Nanoparticles. Plasmonics 2016, 11 (5), 1369–1376. Khaing Oo, M. K.; Yang, Y.; Hu, Y.; Gomez, M.; Du, H.; Wang, H. Gold Nanoparticle-Enhanced and SizeDependent Generation of Reactive Oxygen Species from Protoporphyrin IX. ACS Nano 2012, 6 (3), 1939–1947. Camacho, S. A.; Aoki, P. H. B.; Albella, P.; Oliveira, O. N.; Constantino, C. J. L.; Aroca, R. F. Increasing the Enhancement Factor in Plasmon-Enhanced Fluorescence with Shell-Isolated Nanoparticles. J. Phys. Chem. C 2016, 120 (37), 20530–20535. Niu, C.; Song, Q.; He, G.; Na, N.; Ouyang, J. Near-InfraredFluorescent Probes for Bioapplications Based on SilicaCoated Gold Nanobipyramids with Distance-Dependent Plasmon-Enhanced Fluorescence. Anal. Chem. 2016, 88 (22), 11062–11069. Yan, Y.; Meng, L.; Zhang, W.; Zheng, Y.; Wang, S.; Ren, B.; Yang, Z.; Yan, X. High-Throughput Single-Particle Analysis of Metal-Enhanced Fluorescence in Free Solution Using Ag@SiO2 Core–Shell Nanoparticles. ACS Sensors 2017, 2 (9), 1369–1376. Abadeer, N. S.; Brennan, M. R.; Wilson, W. L.; Murphy, C. J. Distance and Plasmon Wavelength Dependent Fluorescence of Molecules Bound to Silica-Coated Gold Nanorods. ACS Nano 2014, 8 (8), 8392–8406. Zhang, Y.; Aslan, K.; Previte, M. J. R.; Geddes, C. D. MetalEnhanced Singlet Oxygen Generation: A Consequence of Plasmon Enhanced Triplet Yields. J. Fluoresc. 2007, 17 (4), 345–349. Toftegaard, R.; Arnbjerg, J.; Daasbjerg, K.; Ogilby, P. R.; Dmitriev, A.; Sutherland, D. S.; Poulsen, L. Metal-Enhanced 1270 Nm Singlet Oxygen Phosphorescence. Angew. Chem., Int. Ed. 2008, 47 (32), 6025–6027, S6025/1– S6025/4. Ragas, X.; Gallardo, A.; Zhang, Y.; Massad, W.; Geddes, C. D.; Nonell, S. Singlet Oxygen Phosphorescence Enhancement by Silver Islands Films. J. Phys. Chem. C 2011, 115 (33), 16275–16281. Wijesiri, N.; Ozkaya-Ahmadov, T.; Wang, P.; Zhang, J.; Tang, H.; Yu, X.; Ayres, N.; Zhang, P. Photodynamic Inactivation of Multidrug-Resistant Staphylococcus Aureus Using Hybrid Photosensitizers Based on Amphiphilic Block Copolymer-Functionalized Gold Nanoparticles. ACS Omega 2017, 2 (9), 5364–5369. Wijesiri, N.; Yu, Z.; Tang, H.; Zhang, P. Antifungal Photodynamic Inactivation against Dermatophyte Trichophyton Rubrum Using Nanoparticle-Based Hybrid Photosensitizers. Photodiagnosis Photodyn. Ther. 2018, 23, 202–208. Ding, R.; Yu, X.; Wang, P.; Zhang, J.; Zhou, Y.; Cao, X.; Tang, H.; Ayres, N.; Zhang, P. Hybrid Photosensitizer Based on Amphiphilic Block Copolymer Stabilized Silver


Page 11 of 12 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

(46)

(47)

(48)

(49)

(50)

(51)

(52)

(53) (54)

(55)

(56)

(57)

(58)

Journal of the American Chemical Society Nanoparticles for Highly Efficient Photodynamic Inactivation of Bacteria. RSC Adv. 2016, 6 (24), 20392– 20398. Silvero C., M. J.; Rocca, D. M.; de la Villarmois, E. A.; Fournier, K.; Lanterna, A. E.; Pérez, M. F.; Becerra, M. C.; Scaiano, J. C. Selective Photoinduced Antibacterial Activity of Amoxicillin-Coated Gold Nanoparticles: From OneStep Synthesis to in Vivo Cytocompatibility. ACS Omega 2018, 3 (1), 1220–1230. Fales, A. M.; Crawford, B. M.; Vo-Dinh, T. Folate ReceptorTargeted Theranostic Nanoconstruct for SurfaceEnhanced Raman Scattering Imaging and Photodynamic Therapy. ACS Omega 2016, 1 (4), 730–735. Atta, S.; Tsoulos, T. V; Fabris, L. Shaping Gold Nanostar Electric Fields for Surface-Enhanced Raman Spectroscopy Enhancement via Silica Coating and Selective Etching. J. Phys. Chem. C 2016, 120 (37), 20749–20758. Reguera, J.; Langer, J.; Jiménez de Aberasturi, D.; LizMarzán, L. M. Anisotropic Metal Nanoparticles for Surface Enhanced Raman Scattering. Chem. Soc. Rev. 2017, 46 (13), 3866–3885. Theodorou, I. G.; Jawad, Z. A. R.; Jiang, Q.; Aboagye, E. O.; Porter, A. E.; Ryan, M. P.; Xie, F. Gold Nanostar Substrates for Metal-Enhanced Fluorescence through the First and Second Near-Infrared Windows. Chem. Mater. 2017, 29 (16), 6916–6926. Xu, S.; Jiang, L.; Nie, Y.; Wang, J.; Li, H.; Liu, Y.; Wang, W.; Xu, G.; Luo, X. Gold Nanobipyramids as Dual-Functional Substrates for in Situ “Turn On” Analyzing Intracellular Telomerase Activity Based on Target-Triggered PlasmonEnhanced Fluorescence. ACS Appl. Mater. Interfaces 2018, 10 (32), 26851–26858. Cui, Y.; Niu, C.; Na, N.; Ouyang, J. Core–Shell Gold Nanocubes for Point Mutation Detection Based on Plasmon-Enhanced Fluorescence. J. Mater. Chem. B 2017, 5 (27), 5329–5335. Skrabalak, S. E.; Au, L.; Li, X.; Xia, Y. Facile Synthesis of Ag Nanocubes and Au Nanocages. Nat. Protoc. 2007, 2, 2182. Zhang, Q.; Li, W.; Moran, C.; Zeng, J.; Chen, J.; Wen, L.-P.; Xia, Y. Seed-Mediated Synthesis of Ag Nanocubes with Controllable Edge Lengths in the Range of 30-200 Nm and Comparison of Their Optical Properties. J. Am. Chem. Soc. 2010, 132 (32), 11372–11378. Wuithschick, M.; Paul, B.; Bienert, R.; Sarfraz, A.; Vainio, U.; Sztucki, M.; Kraehnert, R.; Strasser, P.; Rademann, K.; Emmerling, F.; et al. Size-Controlled Synthesis of Colloidal Silver Nanoparticles Based on Mechanistic Understanding. Chem. Mater. 2013, 25 (23), 4679–4689. Abadeer, N. S.; Murphy, C. J. Recent Progress in Cancer Thermal Therapy Using Gold Nanoparticles. J. Phys. Chem. C 2016, 120 (9), 4691–4716. Burrows, N. D.; Harvey, S.; Idesis, F. A.; Murphy, C. J. Understanding the Seed-Mediated Growth of Gold Nanorods through a Fractional Factorial Design of Experiments. Langmuir 2017, 33 (8), 1891–1907. Ma, Y.; Li, W.; Zeng, J.; McKiernan, M.; Xie, Z.; Xia, Y. Synthesis of Small Silver Nanocubes in a Hydrophobic Solvent by Introducing Oxidative Etching with Fe(Iii) Species. J. Mater. Chem. 2010, 20 (18), 3586–3589.

(59)

(60)

(61)

(62)

(63)

(64)

(65)

(66)

(67)

(68)

(69)

(70)

(71)

(72)

Ludvíková, L.; Friš, P.; Heger, D.; Šebej, P.; Wirz, J.; Klán, P. Photochemistry of Rose Bengal in Water and Acetonitrile: A Comprehensive Kinetic Analysis. Phys. Chem. Chem. Phys. 2016, 18 (24), 16266–16273. Hanske, C.; Sanz-Ortiz, M. N.; Liz-Marzán, L. M. SilicaCoated Plasmonic Metal Nanoparticles in Action. Adv. Mater. 2018, 30 (27), 1707003. Jang, B.; Park, J.-Y.; Tung, C.-H.; Kim, I.-H.; Choi, Y. Gold Nanorod−Photosensitizer Complex for Near-Infrared Fluorescence Imaging and Photodynamic/Photothermal Therapy In Vivo. ACS Nano 2011, 5 (2), 1086–1094. Ke, X.; Wang, D.; Chen, C.; Yang, A.; Han, Y.; Ren, L.; Li, D.; Wang, H. Co-Enhancement of Fluorescence and Singlet Oxygen Generation by Silica-Coated Gold Nanorods Core-Shell Nanoparticle. Nanoscale Res. Lett. 2014, 9, 666. Yanyan, G.; Snezna, R.; Peng, Z. Rose Bengal-Decorated Silica Nanoparticles as Photosensitizers for Inactivation of Gram-Positive Bacteria. Nanotechnology 2010, 21 (6), 65102. Magnan, F.; Gagnon, J.; Fontaine, F.-G.; Boudreau, D. Indium@silica Core–Shell Nanoparticles as Plasmonic Enhancers of Molecular Luminescence in the UV Region. Chem. Commun. 2013, 49 (81), 9299–9301. Aslan, K.; Wu, M.; Lakowicz, J. R.; Geddes, C. D. Fluorescent Core-Shell Ag@SiO2 Nanocomposites for MetalEnhanced Fluorescence and Single Nanoparticle Sensing Platforms. J. Am. Chem. Soc. 2007, 129 (6), 1524–1525. Tu, S.; Rioux, D.; Perreault, J.; Brouard, D.; Meunier, M. Fluorescence and Scattering Dual-Mode Multiplexed Imaging with Gold–Silver Alloy Core Silica Shell Nanoparticles. J. Phys. Chem. C 2017, 121 (16), 8944– 8951. Vankayala, R.; Sagadevan, A.; Vijayaraghavan, P.; Kuo, C.L.; Hwang, K. C. Metal Nanoparticles Sensitize the Formation of Singlet Oxygen. Angew. Chemie Int. Ed. 2011, 50 (45), 10640–10644. Stauber, R. H.; Siemer, S.; Becker, S.; Ding, G.-B.; Strieth, S.; Knauer, S. K. Small Meets Smaller: Effects of Nanomaterials on Microbial Biology, Pathology, and Ecology. ACS Nano 2018, 12 (7), 6351–6359. Xu, M.; Soliman, M. G.; Sun, X.; Pelaz, B.; Feliu, N.; Parak, W. J.; Liu, S. How Entanglement of Different Physicochemical Properties Complicates the Prediction of in Vitro and in Vivo Interactions of Gold Nanoparticles. ACS Nano 2018. Xiu, Z.; Zhang, Q.; Puppala, H. L.; Colvin, V. L.; Alvarez, P. J. J. Negligible Particle-Specific Antibacterial Activity of Silver Nanoparticles. Nano Lett. 2012, 12 (8), 4271–4275. Han, S.; Han, K.; Hong, J.; Yoon, D.-Y.; Park, C.; Kim, Y. Photothermal Cellulose-Patch with Gold-Spiked Silica Microrods Based on Escherichia Coli. ACS Omega 2018, 3 (5), 5244–5251. Jett, B. D.; Hatter, K. L.; Huycke, M. M.; Gilmore, M. S. Simplified Agar Plate Method for Quantifying Viable Bacteria. Biotechniques 1997, 23 (4), 648–650.



Page 12 of 12

Insert Table of Contents artwork here

ACS Paragon Plus Environment

12

Hybrid Silver Nanocubes for Improved Plasmon ... - ACS Publications

Recommend Documents