Bioinspired Synergy Sensor Chip of Photonic Crystals-Graphene

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Bioinspired synergy sensor chip of photonic crystalsgraphene oxide for multi-amines recognition Wanjie Ren, Meng Qin, Xiaotian Hu, Fengyu Li, Yuanfeng Wang, Yu Huang, Meng Su, Wenbo Li, Xin Qian, Kang-lai Tang, and Yanlin Song Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.8b01549 • Publication Date (Web): 18 May 2018 Downloaded from http://pubs.acs.org on May 18, 2018

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Analytical Chemistry

Bioinspired synergy sensor chip of photonic crystalscrystals-graphene oxide for multimulti-amines recognition Wanjie Ren1, 2, Meng Qin1, Xiaotian Hu1, 2, Fengyu Li1,*, Yuanfeng Wang3, Yu Huang1, Meng Su1, 2, Wenbo Li1, Xin Qian1, 2, Kang-lai Tang4 and Yanlin Song1 1

Key Laboratory of Green Printing, Institute of Chemistry, Chinese Academy of Sciences (ICCAS), Beijing Engineering Research Center of Nanomaterials for Green Printing Technology, Beijing National Laboratory for Molecular Sciences (BNLMS), Beijing 100190, China 2 University of Chinese Academy of Sciences, Beijing 100049, China 3 Key Laboratory of Evidence Science, China University of Political Science and Law, Beijing, 100088, China 4 Sports Medicine Center, Southwest Hospital, Third Military Medical University, Chongqing 400038, China ABSTRACT: Benefiting from the integrated functions of cilia and glomeruli in the olfactory system, animals can discriminate various odours even in hostile environments. Inspired by this synergetic system of response and signal processing units, a sensor chip of graphene oxide (GO) and photonic crystals (PCs) is fabricated. The GO aerogel functions like the olfactory cilia, which effectively captures the analytes and generates abundant sensing signals for recognition; and the PCs act as the olfactory glomeruli, whose periodic structure enables selective enhancement of the fluorescent signals to realize further signal processing. Ten biogenic amines and seven drug amines are effectively discriminated. The integrated sensor strategy of response and signal manipulation units will promote enormous pursuits of rapid clinical diagnosis or intractable pathology analysis.

Amines like biogenic amines and drug amines are very important to human life. For example, biogenic amines (e.g. dopamine, serotonin, noradrenaline) may act as neurotransmitter or hormone in the nervous system and other basic physiological systems.1 Many studies have found that biogenic amines can affect the affective state and sleep of human.2-4 Also, diseases like attention deficit hyperactivity disorder and Parkinson’s disease are caused by dopamine dysfunction in human body.5-7 Significantly, drug amines (e.g. methamphetamine, cocaine, ethylmorphine) abuse is seriously endangering human health and jeopardizing society civilization.8 Over commitment of methamphetamine can cause a stimulant psychosis which may present symptoms like paranoia, hallucinations, delirium, delusions.9 It is highly desired to sense various amines, particularly in physiological environment. However, the detection and accurate recognition of multiple analytes in complex environment are tough due to the signal interference and screening.10-12 In nature, animals can recognize various odors even in hostile environments with their olfactory system. As scheme 1a showing, numerous cilia protrude from the olfactory neurons into the mucus for the sensitive capture of odor molecules. The olfactory neurons which share same olfactory receptors converge their axon into the olfactory bulb to form glomeruli where the odorous information is sorted out and coded for brain discrimination.13-15 This bilayer structure combines the response toward external stimuli and the signal manipulation process together to achieve the successful discrimination of the olfactory system. In fact, the main points to achieve successful analysis of complex sample are accurate

monitoring and data manipulation.16 Inspired by the bilayer structure of the olfactory system, we designed a sensingprocessing bilayer detection device via the integration of graphene oxide (GO) aerogel and photonic crystals (PCs) (scheme 1b). The GO aerogel can work like cilia to effectively capture the analytes, due to the micron porous structure;17 the fluorescent molecules/GO complexes can act like the “the taste receptors” to produce sensing information; the PCs can function as glomeruli to process sensing information, mainly relying on the capability of fluorescence selective enhancement.18 Combining the universal recognition process of GO and the optically selective amplification of PCs, we use the bilayer integrated sensor achieved the discrimination of different amines, which are very important to the social civilization and human health. GO is a fascinating 2D material (Fig. S1a), which has large π-π conjunction structure and numbers of oxygen containing groups (e.g. hydroxyls, epoxies groups, carboxyl groups, and so on).19 Due to its unique structure features, GO can interact with polymeric, organic and biological molecules via electrostatic forces, van der Waals forces, hydrogen bonding, π-π stacking, and hydrophobic interactions, acting as a quencher for fluorophores.20-22 These characteristics make GO an ideal sensing platform. Chen et al. used photoinduced charge transfer (PCT) process between GO and dopamine achieved the sensitive detection of dopamine;23 Ren et al. studied the competitive adsorption-desorption behavior of Rhodamine 6G (R6G) and dopamine on the surface of GO;21

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Scheme 1 Design of the bilayer integrated sensor inspired by the olfactory system. (a) The cilia on the surface layer capture odor molecules and trigger olfactory response; the glomeruli in the inner layer sort out and code the odorous information for brain discrimination. (b) The designed GO-PCs bilayer integrated sensor. GO aerogel layer effectively captures the analytes; PCs selectively enhance fluorescence signals.

other groups also used GO as a fluorescence resonance energy transfer (FRET) acceptor to quench the emission of different fluorophores and achieved successful discrimination of ATP, proteins, degraded antibodies, cells, bacteria, and so on.24-30 PCs are a class of dielectric materials, which have photonic band-gap properties and periodic modulation of the refractive index.31,32 Because of its effective manipulation of light propagation, PCs are widely applied in the sensing area such as the detection of ions, volatile organic compounds, biomolecules, and so on.33-37 In this work, based on the competitive interactions of fluorophores and amines to GO, we use GO aerogel as a universal recognition element to quench the fluorescence of fluorophores (Fig. S1b-d) and also capture amines; and PCs to selectively enhance the fluorescence of desorbed fluorophores. This bilayer structure not only retains the non-specific interac-

Figure 1 Scanning Electron Microscope (SEM) characterization of the designed GO-PCs bilayer integrated sensor. (a) Top view of the bilayer integrated sensor. PC1-PC3 are composed of poly(StMMA-AA) latex particles in different diameters (The bottom PCs layer is covered by GO layer). (b)-(d) The enlarged (crosssectional) view of the integrated sensor with different amplification views (scale bar: a. 1 cm b. 100 µm; c. 10 µm; d. 1 µm).

tures, and even amines at different concentrations and in mixtures are successful discriminated. RESULTS AND DISCUSSION Sensing Principle. The detailed sensing principle is illustrated in Fig. S2. The FRET process will occur between fluorophore molecules and GO under the interaction of electrostatic forces, π-π stacking, and so on, with the fluorescence of fluorescent molecules quenched. When the solutions of amines contact with GO, fluorescent molecules can be desorbed because of the competitive adsorption of amine molecules. The desorbed fluorescent molecules firstly released into water, and then got into the PCs matrix, which leading to selectively amplified fluorescence. To achieve the bilayer integrated sensor, we, firstly, fabricated PCs pixels in the microplate (Fig. 1a: bottom) with three different sizes of poly(styrene/methyl methacrylate/acrylic acid) [poly(St-MMA-AA)] latex particles (Fig. S3). Next GO solutions (5 mg/mL) were dropped into the holes and freeze-dried (Fig. 1a: top). Then the solution of fluorescent molecules was spotted onto the GO aerogel layer respectively (for example, R6G was spotted when the PCs is PC2) and freeze-dried again to keep the structure of the GO aerogel. The concentration of fluorescent molecules used in the sensing platform were determined by quenching experiments (Fig. S4). From the UV-vis absorption and Raman spectra results (Fig. S5), it is evidenced that fluorescent molecules have been retained in the GO layer.25 Scanning Electron Microscope (SEM) images in Fig. 1b-Fig. 1d clearly show the micron porous structure of GO aerogel and the periodic structure of PCs in the bilayer integrated sensor. The successful discrimination by sensor-arrays requires sufficient information about the analytes.38 To fulfill this demand, we used acridine orange (AO), rhodamine (R6G) and rhodamine B (RB) (emissions at 530, 550 and 575 nm respectively) as the fluorophores to provide multiple fluorescent sensing information. Hence, each amine analyte possesses its signal pattern, resulting from their various structures which lead to differential competitive adsorption-desorption process against the fluorophores. As shown in Fig. 2a-c and Fig. S6a, three kind amines: β-phenylethylamine

tions of GO to different analytes, but also retain the specific fluorescence amplification of PCs to various fluorophores. Ten biogenic amines and seven drug amines with similar struc-


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Figure 2 Fluorescent responses and the PCs effect on different fluorophores. (a)-(c) Fluorescence change of the integrated sensor without PCs after addition of dopamine, β-phenethylamine and spermine, respectively (the concentration of the solution is 2 mM, and the excitation wavelengths used for AO, R6G and RB are 460, 500 and 520 nm respectively). (d) Fluorescence spectra of fluorophores and stop bands of the PCs. (e) The fluorescence change of the integrated sensor (the fluorophore is R6G, the PCs is PC2) with the concentration increase of dopamine (0, 0.05, 0.1, 0.2, 0.5, 1, 2, 5 and 10 mM). (f) The effect of PC2 on fluorescence change (R6G) caused by dopamine (∆I=I-I0, where I is the fluorescence intensity in the presence of dopamine solution, and I0 is the fluorescence intensity when the concentration of dopamine is 0 mM).

(PEA), dopamine (DA) and spermine (SI), cause distinctive fluorescent signal output on the GO layer without PCs present. For the fluorophores of AO and R6G, DA causes the most significant and SI causes the smallest fluorescence change, with different levels of relative intensity for these three different amines. For the fluorophore of RB, SI causes the most significant, and DA causes the least fluorescence change. These appearances fulfill the request of the array sensing that each sensing element interacts differentially with the analytes.39 The Function of Photonic Crystals. In order to achieve effective signal processing, PCs are employed to further differentiate the sensing information to the analytes, relying on the selective amplification of fluorescence. We selected poly(StMMA-AA) particles with three different diameters to form PCs, whose stopbands (located at 537, 560 and 600 nm) respectively matched the emissions of AO, R6G and RB (centered at 530, 550 and 575 nm, Fig. 2d). Since the properties of fluorescence enhancement of the PCs are ascribed to the emission reflection from the surface and the slow photos effect on the band edges, when the blue-edge of the stopband considerably overlaps the emission of the fluorophore, the fluorescent intensity shows the most significant enhancement.32,38 We observed the fluorescence enhancing and detection sensitivity improvement by PCs through a dopamine concentrationdependence investigation (Fig. 2e, Fig. S6b and Fig. 2f). The fluorescence intensity increases along with the concentration of dopamine, and the absolute fluorescence intensity change of the integrated sensor (the fluorophore is R6G and the PCs is PC2) shows around 10-fold higher fluorescence to dopamine, compared with the counterpart sensing platform without PCs. We also compared the fluorescence enhancement effect of different PCs toward the same fluorophore. As shown in Fig. S6c, the stopband

Figure 3 Discrimination results of biogenic amines. (a) LDA score plot of 10 biogenic amines (1 mM) by bare GO sensor without PCs. (b) LDA score plot of 10 biogenic amines (1 mM) by integrated sensor. (c) HCA results of 10 biogenic amines (1 mM) by integrated sensor.

blue-edge of PC1 matches the emission peak of AO, resulting in the strongest fluorescence enhancement. The PC2 and PC3 also show the fluorescence enhancement effect but lower than PC1 (about 1.5-fold to PC3). Similarly, for R6G and RB, PC2 and PC3 can mostly amplify their fluorescence, respectively.



As a result, featured fluorescent signals to each amine analyte are further enhanced, leading to more distinguished signal patterns, which benefits the discrimination of the analytes. Detection of Biogenic Amines. To investigate the sensing capability of the bilayer integrated sensor chip, multi-analysis of 10 different biogenic amines (structures shown in Fig. S7) was carried out. The fluorescence responses were recorded in 3 channels (CH 1: 535 nm, CH 2: 570 nm, CH 3: 605 nm, with UV 365 nm excitation). Linear discriminant analysis (LDA) and hierarchical clustering analysis (HCA) were used to evaluate the similarities between data clusters.40 In the score plot of LDA, the gathering of the clusters into groups means the good reproducibility of the sensing platform, and the distance of the cluster in spatial distribution reveals the differential of fluorescent signal of the amines. HCA, as an unsupervised multivariate analysis, was used to investigate the similarity clustering of the analytes through dimensionality reduction analysis.32 We compared the discrimination results of the biogenic amines (1 mM) by using integrated sensor and the bare GO sensor. As shown in Fig. 3a, the bare GO sensor, without PCs layer as the signal processing unit, cannot separate the data clusters of biogenic amines, demonstrating only 84% correct classification in the jackknifed classification matrix (Fig. S8a-b). By contrast, the integrated sensor shows a clear spatial isolation of the 10 biogenic amines (Fig.3b), and the HCA results (Fig.3c) give the similarity clustering of the amines. The jackknifed classification matrix (Fig. S8c-d) also shows 100% correct classification of these amines. Besides, amines in gradient concentrations were also correctly classified (Fig. S9). Thus, signal processing by PCs layer is indispensable to realize successful discrimination. To further explore the capability of the integrated sensor, we investigated the recognition of amines at different concentrations and in mixtures. Different amines at various concentrations (Fig. S10) and in mixtures (Fig. S11) are also successfully discriminated.

cient narcotics control. Fig. 4a lists seven drug amines, i.e. noscapine, ethylmorphine, cocaine, caffeine, ketamine, methamphetamine, 3,4-methylened-oxymethamphetamine, which are the most addictive narcotics and the main objectives to control. Urine is a complex sample, which may contain many interferents. In the experiment we use the control sample as the basic point, all the interferences in the urine was included in the control sample. The interferences of urine could be eliminated via background deducting operation. As shown in Fig. 4b, using the same integrated sensor, we achieved the discrimination of drug amines in artificial urine. The jackknifed classification matrix also shows a complete and clear 100% correct classification (Fig. S12). Since more obvious difference on molecular structures, the drug amines discrimination analysis shows higher-resolution with lower concentration. All the results demonstrate the sensing capabilities of the integrated sensor chip in complex environments and practical applications. CONCLUSION In conclusion, inspired by the bilayer structure of the olfactory system, an integrated sensor chip combining the response unit of GO and the signal manipulation unit of PCs is fabricated, achieving the facile recognition of different amines. The GO aerogel functions like the olfactory cilia, which effectively captures the analytes and generates abundant sensing signals for recognition, due to the micron porous structure; and the PCs act as the olfactory glomeruli, whose periodic structure enables selective enhancement of the fluorescent signals to realize improved discrimination of sensing information. The bilayer structure not only retains the non-specific interactions of GO with different analytes to reach universal recognition, but also retains the specific fluorescence amplification of PCs to achieve effective signal processing. The integrated sensor can facilely discriminate biogenic amines and drug amines with similar structures. Furthermore, it can also be used to distinguish amines at different concentrations and in mixtures. The integrated sensor strategy of response and signal manipulation units contributes to effective multi-analytes detection and complex system analysis and, will promote enormous pursuit of rapid clinical diagnosis or intractable pathology analysis.

ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Experimental details and additional data (PDF)

AUTHOR INFORMATION Corresponding Author *[email protected] Figure 4 Discriminative analyses of 7 drug amines. (a) Structures of 7 drug amines. (b) LDA score plot of 7 drug amines (6 µg/mL) in artificial urine. LDA shows 100% correct classification for all complex drug samples in simulated clinical environment.

Detection of Drug Amines. We also promoted our endeavor to the rapid detection of drug amines for the pursuit of effi-

ORCID Fengyu Li: 0000-0003-2481-6111

Author Contributions W. R. and M. Q. contributed equally to this work.


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Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT F. Y. Li and Y. L. Song thank the financial support of the National Nature Science Foundation of China (Grant Nos. 51773206, 51473172, 51473173), the National Key R&D Program of China (Grant Nos. 2016YFB0401603, 2016YFC1100502 and 2016YFB0401100), and the “Strategic Priority Research Program” of Chinese Academy of Sciences (Grant No. XDA09020000).

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Inspired by the bilayer integrated structure of the olfactory system, a sensor chip using the GO aerogel to capture analytes (as olfactory cilia function) and the PCs to selectively amplify fluorescence for signal processing (as olfactory glomeruli function) was fabricated and achieved multi-analysis of different amines. This integrated sensor strategy will promote applications in rapid clinical diagnosis or intractable pathology analysis.


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Bioinspired Synergy Sensor Chip of Photonic Crystals-Graphene

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