Nanoantennas as Biomarkers for Bacterial Detection - Analytical

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Nanoantennas as Biomarkers for Bacterial Detection Hiroshi Shiigi, Takamasa Kinoshita, Maho Fukuda, Dung Quynh Le, Tomoaki Nishino, and Tsutomu Nagaoka Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.5b00415 • Publication Date (Web): 17 Mar 2015 Downloaded from http://pubs.acs.org on March 24, 2015

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Analytical Chemistry

Nanoantennas as Biomarkers for Bacterial Detection Hiroshi Shiigi,*,† Takamasa Kinoshita,† Maho Fukuda,† Dung Quynh Le,† Tomoaki Nishino,† and Tsutomu Nagaoka†

†

Department of Applied Chemistry, Osaka Prefecture University

1-2 Gakuen, Naka, Sakai, Osaka 599-8570, Japan.

Tel.: +81-72-254-9875 Fax: +81-72-254-9875 *

[email protected]

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ABSTRACT Understanding the biology of bacteria is critical for exploiting their beneficial properties and for preventing and treating bacterial diseases. Nanobioscience is an area that has recently seen major scientific progress. Here, we demonstrate a raspberry-shaped nanostructure with a high density of gold nanoparticles acts like excellent antennas owning to their optical properties, which permit sensitive detection and analysis of bacterial cells. By using antibodies, these nanoantennas can be engineered to recognize only specific bacterial species. This system provides a new technique that will allow for more sensitive detection of specific bacteria.


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Pathogenic bacteria are a major public health concern worldwide, as they cause such widespread problems as hospital-acquired infections and food poisoning. Methods for the rapid detection and identification of pathogenic bacteria in food, clinical, and environmental samples are required to prevent and diagnose infectious diseases.1–3 The high signal enhancement capability of biological sensors has spurred considerable efforts in developing antenna systems based on metal nanoparticles (NPs) that can detect single molecules.4–6 Metal NPs, which have electrical and optical properties differing from those of bulk metals, have been the focus of much interest in recent years. In particular, gold NPs (Au NPs), which have highly dense electron structures and chemical stability, are considered to have the most potential for use in a broad area of electronic, optic, and biomedical applications.7–12 Because the specific properties of Au NPs depend strongly on their dispersibility, it is necessary to control their placement. Au NPs are capable of producing an enhanced optical field near their surface that can be tuned throughout the visible spectrum by changing their size, shape, dispersion, and local environmental conditions. In addition, molecules adsorbed on an Au NP surface undergo surfaceenhanced Raman scattering (SERS) effects based on coupling of the plasmon band, in which collective oscillation of the conduction band electrons occurs upon visible light absorption.13–15 Free electrons on an Au NP surface express localized surface plasmon resonance (LSPR) involving collective vibrations induced by interaction with visible light. The LSPR may depend on a combination of factors, namely, the size, shape, and distance between adjacent Au NPs, as well as the value of the surrounding dielectric constant.15–17 Correspondingly, controlling the LSPR of a nanoantenna structure should be possible through careful assembly of Au NPs. By assembling Au NPs, a nanoantenna achieves control of LSPR based on the concept of “effective use of light.” 18,19 Au NPs exhibit excellent elastic light-scattering properties and are used as nanoantennas for sensing and detecting single molecules.20–23 We have reported previously a simple formation of an antenna through the electrostatic interaction of Au NPs on the surface of bacteria and the optical characteristics depends strongly on their aggregation and dispersion states on the bacteria, and moreover, a raspberry-shaped nanostructure that has a high density of Au NPs serves as a high sensitive antenna.24 The raspberry-structure adsorbed on a bacterium indicated a strong light-scattering intensity, comparing to those of Au NPs. Our previous studies illuminate a new detection procedure for microorganisms based on the concept of “effective use of light.” We show here a raspberry-shaped nanostructure acts like a high sensitive antenna on the surface of specific bacteria for a rapid detection and analysis of bacterial cells. 3 ACS Paragon Plus Environment


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EXPERIMENTAL SECTION Chemicals. All chemicals were reagent grade. Ultrapure water (>18 MΩ cm) sterilized by UV light was used for all experiments. Bacterial strains of Escherichia coli (NBRC 3972) and Pseudomonas aeruginosa (NBRC 13738) were obtained from the National Institute of Technology and Evaluation Biological Resource Center (NBRC). Heat-killed E. coli O157:H7, O26:H11, and O111 were obtained from Kirkegaard & Perry Laboratories, Inc. (KPL), and were used for safety in this study. The anti-E. coli O157:H7 antibody was also obtained from KPL. Bacterial culture and sample preparation. A strain of bacteria was cultured in agar growth medium (E-MC35, Eiken Chemical Co., Japan) at 30°C for 48 h. Colonies were suspended in liquid growth medium (30 mL) and cultured at 30°C for 24 h. After centrifugation at 6,500 rpm for 15 min, the supernatant was removed. The precipitate was suspended in fresh phosphate buffer by shaking for 1 min. The suspension was centrifuged using the same conditions described above. These procedures were repeated three times. The resulting suspension (9.2 × 109 cells/mL) was used for the following experiments. Preparation of antibody-immobilized nanoraspberries. The nanoraspberries used here were prepared by chemical reduction in aqueous media. An aqueous aniline solution (0.1 M) was added to an aqueous solution of chloroauric acid (0.01%), stirred at 80°C for 20 min, and centrifuged at 8,500 rpm (5°C). The resulting precipitate, which did not include unreacted species, was dispersed in 30 mL ultrapure water.24–27 We introduced an anti-E. coli O157:H7 antibody to the nanoraspberry using 1ethyl-3-(3-dimethylaminopropyl) carbodiimide hydrochloride (EDC) and N-hydroxysuccinimide (NHS) as coupling agents.28 Dark-field observations. Dark-field microscopy detects only the light scattered by a structure, while directly transmitted light is blocked using a dark-field condenser. Dark-field light-scattering images were acquired using an optical microscope (Eclipse 80i, Nikon, Japan) with a dark-field condenser, a 100-W halogen lamp, and a charge-coupled device (CCD) camera. Scattering spectra were obtained using a miniature grating spectrometer (USB4000, Ocean Optics), which was connected to the microscope using an optical fiber. Typical acquisition times were 100 ms. The light-scattering spectra were corrected for spectral variations in the system response, and the white-light intensity distribution (main intensity, 600 nm) through division by bright-field spectra was recorded through the sample. The collection volume based on the cross-sectional area (approximately 10 µm2) for the combination of 100× objective (NA 0.9) and optical fiber (core diameter, 400 µm) used here. Drops of nanoparticle 4 ACS Paragon Plus Environment

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dispersion (10 µL), bacterial suspensions, and mixtures thereof were each pipetted onto a glass slide and dried in air to measure dark-field light scattering. This technique allowed for the study of single particles, aggregates, or both dispersed thinly on a substrate, because only diffracted and scattered light generate the dark-field image. Spectroscopic measurements. We applied the antibody-introduced raspberry for identification of E. coli. The raspberry dispersion (0.0087 wt%, 0.5 mL) was added to E. coli suspension (0.5 mL). The mixture solution of 10 µL was dropped on a slide glass and stood at room temperature for 1 h. The lightscattering spectra and dark-field images were obtained using the dark-field microscope system mentioned above. We also performed a spectroscopic measurement to determine the bacterial concentration in the sample solution using the antibody-introduced raspberry. The antibody-introduced raspberry dispersion (0.0087 wt%, 0.5 mL) was added to different amounts of E. coli O157 suspension (101−106 cells/mL, 0.5 mL). The total 1-mL solution was mixed and stood at room temperature for 1 h. We applied this solution to the determination of E. coli O157 using a UV-VIS spectrometer. There was no peak-shift in the UV-VIS spectrum based on the raspberry labels. Therefore, we focused on the absorbance at 600 nm. The absorbance at 600 nm depends on the number of E. coli O157:H7 in the solution (n = 10). RESULTS AND DISCUSSION The membranes of gram-negative bacteria, such as E. coli, P. aeruginosa, Salmonella enterica, and Serratia marcescens, contain lipopolysaccharides (LPS) that consist of repeating hydrophilic Oantigenic oligosaccharide side chains, a hydrophilic core polysaccharide chain, and a hydrophobic lipid moiety (lipid A), as shown in Scheme 1. Intact bacterial LPS molecules (10–20 kDa) comprise three structural components that are localized to the outer layer of the cell membrane and are exposed on the cell surface of non-capsulated strains.29–31 LPS is an integral component of the cell wall and includes functional groups, such as hydroxyls, phosphates, carboxylates, and amines, that extend outward from the cell body along with polysaccharides, and is released when the cell walls of dead bacteria are degraded. The identities of gram-negative bacteria can be determined by their surface structure, because different species possess different repetitive sequences of saccharide subunits. Observations acquired using a zeta-potential analyzer indicate that gram-negative bacteria possess a negatively charged surface when dispersed in ultrapure water and exhibit a negative zeta potential (−10 to −30 mV) at pH > 2.8. This suggests that the surface of a bacterium is negatively charged due to phosphate and carboxylate groups, which outweigh the positive charge of amino groups.32 Bacteria have no characteristic absorption (see Figure S1), except 5 ACS Paragon Plus Environment


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for the absorption peak at 260 nm based on their nucleic acids, but exhibit weak light-scattering based on their cytoplasm, which consists of 70% water, 17% proteins, 7% nucleic acids, and other components (lipids and polysaccharides), as shown in Figure 1A. Therefore, it is difficult to detect a bacterium directly without labeling. Scheme 1. Schematic of the outer membrane of a typical gram-negative bacterium.

pH-dependence of the zeta potential of (a) E. coli and (b) P. aeruginosa in buffer solution (ionic strength, 2.6 mM). Metal NPs scatter light intensely and the spot size of the scattered light observed in the dark-fields is often far larger than their true size of individual NPs (Figure 1B).33–37 It is expected that metal NPs serve as a nanometer-sized index for biological imaging.38–40 However, metal ions eluted from NPs are cytotoxic to bacteria and cause degradation of the outer membrane of dead bacteria.41,42 The excellent light-scattering properties and chemical stability of Au NPs make it possible to use them for building antennas on the bacterial surface.24 However, the adsorption of Au NPs on a bacterium generates a significant change in their light-scattering properties, such as color (wavelength) and strength (intensity), and the change in these properties is sensitive to the dispersibility of the adsorbed Au NPs.24,33–37 In order to form antennas to receive and transmit a constant signal on the bacterial surface, we focused on a nanometer-sized raspberry structure comprised of numerous Au NPs. We previously reported a simple processing technique for developing a uniformly structured raspberry-shaped hybrid consisting of aniline oligomers and Au NPs.24–27 The hybrid structure 6 ACS Paragon Plus Environment

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comprises assemblies of Au NPs coated and encapsulated with organic aniline oligomers as a linker and/or matrix, as shown in Figure 2. Because the aniline oligomers of the backbone are closely overlapped through π-stacking of aromatic rings, they behave like a polyaniline (PANI) in this hybrid. The raspberry-shaped hybrid has a high density of dispersible Au NPs separated by aniline oligomers. Thus, the raspberry structure emits strongly enhanced light through LSPR coupling, which is caused by incident visible light absorption due to the many non-contacting Au NPs in the raspberry structure. The nanoraspberry is a specific structure comprised of repeated sequences of Au NP-aniline oligomer-Au NP. The mean diameter of the raspberries is approximately 100 nm, and the aniline oligomer is strongly linked to adjacent Au NPs with a mean diameter of 5 nm. The raspberry is positively charged between pH 1.6–6.2, without contamination by smaller Au NPs. In contrast, the zeta potential of gram-negative bacteria is negative over a wide pH range. Therefore, we expected that electrostatic interactions between the raspberries and the bacteria would not disrupt the outer membrane, and that strong light scattering would be achieved by the raspberries.

Figure 1. (A) Light-scattering spectra and dark-field images of (a) E. coli and (b) P. aeruginosa on a glass slide. (B) Light-scattering spectra and dark-field images of (a) nanoraspberry and (b) 5-nm Au NP. Acquisition time was 100 ms. The scale bars in dark-field images are 1 µm. Scanning electron microscopy (SEM) observations showed that almost all of the nanoraspberries adsorbed to the bacterial surface and not to the substrate, indicating that electrostatic interactions dominate between the raspberry structures and the bacterium, as shown in Figure 3A. Different amounts of bacteria were added to the raspberry dispersion (0.0087 wt%, 0.5 mL), and the amount of nanoraspberries bound to the bacteria depended strongly on the amount of bacteria added. When the raspberries are completely adsorbed to the bacteria, we can estimate the number of raspberries per bacterium. The average number of raspberries adsorbed on a bacterium was estimated from SEM images, and was calculated as 1.0 × 10−14 g of the weight of one raspberry from the specific gravity of 7 ACS Paragon Plus Environment


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gold (19 g/cm3). The raspberry-labeled bacterium scattered white light very strongly, and revealed greater scattering intensity than that of a non-labeled bacterium. Dark-field images show significant dependency on the number of adsorbed raspberries on the light scattering of a bacterium (Figure 3A). An increase in the strength of light scattering indicates an increase in the amount of raspberries adsorbed on a bacterium. Thus, the raspberry emits highly intense light through the coupling of LSPR generated by absorption of the incident light.43,44 The formation of highly sensitive nanoantennas on bacteria was readily accomplished using raspberries.

Figure 2. Characteristics of the form and surface of a nanoraspberry. (a) TEM image and model illustration. (b) Distribution of nanoraspberry diameters. (c) pH-dependence of the zeta potential.

Figure 3. (A) SEM and dark-field images of a bacterium labeled with nanoraspberries. Acquisition time was 100 ms. Average number of raspberries on a bacterium, indicated in the images, was estimated from the SEM images. (B) Dependence of the light-scattering intensity at 600 nm on the number of 8 ACS Paragon Plus Environment

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raspberries on a bacterium. (C) Dark-field images of bacteria labeled with an average of (a) 60 and (b) 120 raspberries per bacterium. As just discussed, the nanoraspberry structure possesses excellent light-scattering properties. Lightscattering intensity was shown to depend strongly on the number of raspberries adsorbed per bacterium (Figure 3B). Although the intensity increased gradually from 0 (non-labeled bacterium, red symbol) to 30 raspberries per bacterium, it increased drastically at >30 raspberries, and plateaued at approximately 60 raspberries per bacterium, suggesting that aggregation of adsorbed raspberries progresses gradually and ultimately saturates the bacterial surface. We can consider that light scattering also depends strongly on the state of aggregation of raspberries adsorbed to a bacterium. Free raspberries were observed on the substrate, and the number of free raspberries increased as more raspberries were added to the solution (Figure 3C). Although excess raspberries bound to the substrate were observed when there were over 60 raspberries per bacterium, their weak light scattering was distinctly different from the strong light scattering by raspberries adsorbed to the bacteria. In order to impart selectivity into the nanoraspberry, we have attempted to introduce an antibody to the raspberry structure, as shown in Scheme 2. Scheme 2. Schematic of nanoantenna formation using an antibody-introduced raspberry on a bacterium.

(a) The introduction of anti-E. coli O157:H7 antibody to the raspberry structure. (b) Selective formation of nanoantenna through antigen-antibody reaction on a bacterial surface. We applied this anti-E. coli O157:H7 antibody-introduced raspberry to E. coli O157, as shown in Figure 4A. It was confirmed that the antibody-introduced raspberry structure was bound selectively through the specific antigen-antibody reaction to a bacterium in the dark-field microscopic observation. A weak light-scattering characteristic of E. coli O26 and O111 was also observed, as well as that of nonlabeled E. coli O157. The light-scattering intensity of the raspberry-labeled E. coli was more than three 9 ACS Paragon Plus Environment


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times greater than those of non-labeled bacteria, including E. coli O26 and O111. The raspberry was added to the bacterial suspension containing the cells at various concentrations, as shown in Figure 4B. We conducted the UV-VIS spectroscopic measurements with an amount of bacteria (less than 106 cells/mL) in which the effect of light scattering by the bacteria is negligible in the visible region (Figure S1). There was no peak-shift in the UV-VIS spectra based on the raspberry labels. Therefore, we focused on absorbance at 600 nm. The absorbance at 600 nm, based on the raspberry labels, increased linearly with an increasing amount of bacteria, and became equal to the intensity of the raspberry (0.45) at around 106 cells/mL. These results are suggestive of the dispersion state of the bound raspberries onto a bacterium and/or the dispersibility of the raspberry-bound bacteria in solution.24–27 In the case of a larger amount of bacteria, the raspberry labels bind to each bacterium in a dispersed manner (Figure 4Bb). With lesser bacteria, the raspberries are concentrated on a small amount of bacteria, and aggregates precipitate in the solution (Figure 4Ba). In this case, we have measured free raspberries dispersed in solution without binding to bacteria. These results reveal that the absorbance depends strongly on both the amount of free raspberries and the dispersion state of raspberry-labeled bacteria in the solution.

Figure 4. (A) Light-scattering spectra and dark-field images of E. coli O157, O111, and O26 after labeling with the antibody-introduced raspberry. Acquisition time was 100 ms. (B) Dependence of absorbance at 600 nm on the number of E. coli O157:H7 in the solution (n = 10). The antibodyintroduced raspberry dispersion (0.0087 wt%, 0.5 mL) was added to the bacterial suspension (101−106 cells/mL, 0.5 mL). Illustrations (a and b) correspond to a and b in the graph, respectively. CONCLUSION We demonstrate here a method for the simple and rapid detection of pathogenic bacteria utilizing Au NPs that are aggregated as a nanoantenna. We successfully and efficiently formed nanoantennas through the antigen-antibody specific reaction between the raspberries and E. coli O157. This simple and rapid 10 ACS Paragon Plus Environment

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detection system promises to provide a new technique that will benefit efforts to improve safety by better detection of pathogenic bacteria. The characteristic optical properties of the raspberries are due to their aggregation and dispersion states, which provide useful information regarding the bacteria. Moreover, our studies illuminate the concept of the "effective use of light" based on the effective absorption and emission of light by nanoantennas comprised of numerous Au NPs. ASSOCIATED CONTENT Supporting Information Additional experimental details and supporting data describing antibody introduction into the raspberry are available free of charge via the Internet at http://pubs.acs.org/. AUTHOR INFORMATION Corresponding Author [email protected]

Author Contributions All authors contributed equally.

Notes The authors declare no competing financial interests. ACKNOWLEDGMENT We gratefully acknowledge the financial support provided by the Ministry of Agriculture, Forestry, and Fisheries through a science and technology research promotion program for agriculture, forestry, fisheries, and food industry. We also acknowledge financial support from the Japan Society for the Promotion of Science (JSPS) through a Grant-in-Aid for Scientific Research (B) (KAKENHI 25288039) and Grant-in-Aid for Challenging Exploratory Research (KAKENHI 26620072).



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REFERENCES (1) Daly, P.; Collier, T.; Doyle, S. Lett. Appl. Microbiol. 2002, 34, 222–226. (2) Wang, J.; Gao, J. Q.; Liu, D. J.; Han, D. X.; Wang, Z. X. Nanoscale 2012, 4, 451–454. (3) Tokonami, S.; Nakadoi, Y.; Takahashi, M.; Ikemizu, M.; Kodama T.; Saimatsu, K.; Dung, L. Q.; Shiigi, H.; Nagaoka, T. Anal. Chem. 2013, 85, 4925–4929. (4) Nie, S. M.; Emory, S. R. Science 1997, 275, 1102–1106. (5) Kneipp, K.; Wang, Y.; Kneipp, H.; Perelman, L. T.; Itzkan, I.; Dasari, R.; Feld, M. S. Phys. Rev. Lett. 1997, 78, 1667–1670. (6) Camden, J. P.; Dieringer, J. A.; Zhao, J.; Van Duyne, R. P. Acc. Chem. Res. 2008, 41, 1653–1661. (7) El-Sayed, M. A. Acc. Chem. Res. 2001, 34, 257–264. (8) Park, S. J.; Taton, T. A.; Mirkin, C. A. Science 2002, 295, 1503–1506. (9) Nakao, H.; Shiigi, H.; Yamamoto, Y.; Tokonami, S.; Nagaoka, T.; Sugiyama, S.; Ohtani, T. Nano Lett. 2003, 3, 1391–1394. (10) Daniel, M.-C.; Astruc, D. Chem. Rev. 2004, 104, 293–346. (11) Burda, C.; Chen, X.; Narayanan, R.; El-Sayed, M. A. Chem. Rev. 2005, 105, 1025–1102. (12) Shiigi, H.; Tokonami, S.; Yakabe, H.; Nagaoka, T. J. Am. Chem. Soc. 2005, 127, 3280–3281. (13) Garrell, R. L. Anal. Chem. 1989, 61, 401A–411A. (14) Campion, A.; Kambhampati, P. Chem. Soc. Rev. 1998, 27. 241–250. (15) Kneipp, K.; Kneipp, H.; Itzkan, I.; Dasari, R. R.; Feld, M. S. Chem. Rev. 1999, 99, 2957–2976. (16) Mie, G. Ann. Phys. 1908, 25, 377–445. (17) Hu, H.; Duan, H.; Yang, J. K. W.; Shen, Z. X. ACS Nano 2012, 6, 10147–10155. (18) Moreau, A.; Ciracì, C.; Mock, J. J.; Hill, R. T.; Wang, Q.; Wiley, B. J.; Chilkoti, A.; Smith, D. R. Nature 2012, 492, 86–89. (19) Acuna, G. P.; Möller, F. M.; Holzmeister, P.; Beater, S.; Lalkens, B.; Tinnefeld, P. Science 2012, 338, 506–510. (20) Schultz, D. A. Curr. Opin. Biotechnol. 2003, 14, 13–22. (21) Schultz, S.; Smith, D. R.; Mock, J. J.; Schultz, D. A. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 996– 1001. (22) Cao, Y.; Jin, R.; Mirkin, C. A. Science 2002, 297, 1536–1540. (23) Cognet, L.; Tardin, C.; Boyer, D.; Choquet, D.; Tamarat, P.; Lounis, B. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 11350–11355.


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(24) Shiigi, H.: Fukuda, M.; Tono, T.; Takada, K.; Okada, T.; Dung, L. Q.; Hatsuoka, Y.; Kinoshita, T.; Takai, M.; Tokonami, S.; Nakao, H.; Nishino, T.; Yamamoto Y.; Nagaoka, T. Chem. Commun. 2014, 50, 6252–6255. (25) Shiigi, H.; Yamamoto, Y.; Yoshi, N.; Nakao, H.; Nagaoka, T. Chem. Commun. 2006, 4288–4290. (26) Shiigi, H.; Muranaka, Y.; Yamamoto, Y.; Nagaoka, T. Anal. Sci. 2013, 29, 937–939. (27) Shiigi, H.; Muranaka, Y.; Hatsuoka, Y.; Yamamoto, Y.; Nagaoka, T. J. Electrochem. Soc. 2013, 160, H813–H817. (28) Arya S. K.; Dey, A.; Bhansali, S. Biosens. Bioelectron. 2011, 28, 166–173. (29) Rietschel, E. T.; Kirikae, T.; Schade F. U.; Mamat, U.; Schmidt, G.; Loppnow, H.; Ulmer, A. J.; Zähringer, U.; Seydel, U.; Di Padova, F. FASEB J. 1994, 8, 217–225. (30) Shephard, J.; McQuillan, A. J.; Bremer, P. J. Appl. Environ. Microbiol. 2008, 74, 6980–6986. (31) Soares, T. A.; Straatsma, T. P.; Lins, R. D. J. Braz. Chem. Soc. 2008, 19, 312–320. (32) Fein, J. B.; Daughney, C. J.; Yee, N.; Davis, T. A. Geochim. Cosmochim. Acta 1997, 61, 3319– 3328. (33) Talley, C. E.; Jackson, J. B.; Oubre, C.; Grady, N. K.; Hollars, C. W.; Lane, S. M.; Huser, T. R.; Nordlander, P.; Halas, N. J. Nano Lett. 2005, 5, 1569–1574. (34) Murphy, C. J.; Sau, T. K.; Gole, A. M.; Orendorff, C. J.; Gao, J.; Gou, L.; Hunyadi, S. E.; Li, T. J. Phys. Chem. B 2005, 109, 13857–13870. (35) Ni, W.; Kou, X.; Yang, Z.; Wang, J. ACS Nano 2008, 2, 677–686. (36) Sönnichsen, C.; Franzl, T.; Wilk, T.; von Plessen, G.; Feldmann, J.; Wilson, O.; Mulvaney, P. Phys. Rev. Lett. 2002, 88, 77402. (37) Kuwata, H.; Tamaru, H.; Esumi, K.; Miyano, K. Appl. Phys. Lett. 2003, 83, 4625–4627. (38) Xu, X.-H. N.; Chen, J.; Jeffers, R.; Kyriacou, S. Nano Lett. 2002, 2, 175–182. (39) Kyriacou, S.; Brownlow, W.; Xu, X.-H. N. Biochemistry 2004, 43, 140–147. (40) Hu, R.; Yong, K.-T.; Roy, I.; Ding, H.; He, S.; Prasad, P. N. J. Phys. Chem. C 2009, 113, 2676– 2684. (41) Hayden, S. C.; Zhao, G.; Saha, K.; Phillips, R. L.; Li, X.; Miranda, O. R.; Rotello, V. M.; EI-Sayed, M. A. J. Am. Chem. Soc. 2012, 134, 6920–6923. (42) Xiu, Z.-m.; Zhang, Q.-b; Puppala, H. L.; Colvin, V. L.; Alvarez, P. J. J. Nano Lett. 2012, 12, 4271– 4275. (43) Schlather, A. E.; Large, N.; Urban, A. S.; Nordlander, P.; Halas, N. J. Nano Lett. 2013, 13, 3281– 3286.



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(44) Urban, A. S.; Shen, X.; Wang, Y.; Large, N.; Wang, H.; Knight, M. W.; Nordlander, P.; Chen, H.; Halas, N. J. Nano Lett. 2013, 13, 4399–4403.


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Nanoantennas as Biomarkers for Bacterial Detection - Analytical

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