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A Ratiometric Two-photon Fluorescent Probe for Detecting and Imaging Hypochlorite Yenleng Pak, Sang Jun Park, Qingling Xu, Hwan Myung Kim, and Juyoung Yoon Anal. Chem., Just Accepted Manuscript • DOI: 10.1021/acs.analchem.8b02195 • Publication Date (Web): 13 Jul 2018 Downloaded from http://pubs.acs.org on July 14, 2018
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Analytical Chemistry
A Ratiometric Two-photon Fluorescent Probe for Detecting and Imaging Hypochlorite Yen Leng Pak‡a, Sang Jun Park‡b, Qingling Xuc, Hwan Myung Kim*b, Juyoung Yoon*a. a
Department of Chemistry and Nano Science, Ewha Womans University, Seoul 120-750, Korea. Department of Energy Systems Research, Ajou University, Suwon, Gyeonggi-do 443-749, Korea. c School of Chemical Sciences, University of Chinese Academy of Sciences, Beijing 100049, P. R. China. b
ABSTRACT: The ratiometric fluorescent probe B6S, which contains pyrene as a fluorophore and imidazoline-2-thione as a reactive site, was developed for detection of hypochlorite (OCl-). B6S displays a high specificity toward OCl- in contrast to other ROS and RNS. The probe has a low detection limit and operates under biological conditions. Moreover, the low cytotoxicity of B6S enables it to be utilized effectively for OCl- imaging in living cells and tissues by using two-photon microscopy. The findings indicate that B6S has the capability of serving as a probe to explore the biological functions of OCl- in living system.
INTRODUCTION Free radicals and related species that derive from molecular oxygen, termed reactive oxygen species (ROS), have drawn great attention in recent years. ROS are generated through different endogenous pathways in the human body and participate in many physiological and pathological processes. In addition, ROS serve as significant signaling species that mediate a broad range of biological acitivies.1-3 The ROS, hypochlorite (OCl-), is known to display antibacterial activity that is associated with its strong oxidizing properties.4-6 In the human immune system, endogenous OCl- is produced by myeloperoxidase (MPO) mediated peroxidation of chloride ions in phagocytic leukocytes7-9 in response to invading bacteria and pathogens.10,11 Excessive or abnormal generation of OCl- causes tissue damage related to the development of several diseases including arthritis, atherosclerosis and cancer.12,13 As a result, a great effort has been given to the development of methods for detecting and imaging OCl- in living systems as part of studies aimed at clarifying its physiological and pathological consequences as well as elucidating its specific functions.14-21 Owing to advantages associated with its high sensitivity and selectivity, ease of operation and capability for real-time sensing, fluorescent imaging employing fluorescent probes has become an attractive method in the biological sciences.22-31 Moreover, in the past several decades two-photon imaging (TPM), employing ratiometric fluorescent probes, has emerged as an important technique.32-36 In contrast to one-photon microscopy, TPM has numerous beneficial features, including the competency of tissue imaging at increased depths (down to 1 mm), higher spatial resolution, and lower levels of photo-damage and photo-bleaching.37,38 One of challenges confronting the development of a probe to detect OCl- is the design of a novel chemo-recognition process that responds to this ROS in a rapid, selective and sensitive manner and that is compatible with environments present in living systems. Recently, we developed novel, imidazoline-2-thione based fluorescent probes for highly selective and sensitive detection of OCl-.17,39 However, these sensors operate using only one wavelength. Ratiometric fluorescent probes for this ROS would be more advantageous because they would simplify data acquisi-
tion, minimize background noise and reduce autofluorescence interference from cellular organelles.40-42 In the investigation described below, we designed and synthesized the new ratiometric two-photon fluorescent probe, 1-methyl3-(pyren-4-ylmethyl)-1,3-dihydro-2H-imidazole-2-thione (B6S), which contains an imidazoline-2-thione group for OCl- detection and a pyrene moiety that serves as the emitting fluorophore. Highly specific reaction of OCl- with the imidazoline-2-thione group in B6S, which emits excimer emission, produces the corresponding imidazolium derivative B6 accompanied by a change from excimer to monomer emission.43-45 The high utility of B6S was demonstrated by its application in living cells and tissues to monitor production of endogenous OCl- using two-photon microscopy. EXPERIMENTAL SECTION Materials and Chemicals. Chemicals and solvents were from commercial sources and were used as received. 1H NMR and 13C NMR spectra were recorded using a Bruker Avance 300 M and 500 M NMR spectrometers. Mass spectra were obtained using a 6200 series TOF/6500 series Q-TOF. UV absorption spectra were obtained using a UVIKON 933 double-beam UV-vis spectrometer. Fluorescence emission spectra were obtained by using a RF5301/PC spectrofluorophotometer (Shimadzu). Scheme 1. Chemical structure and synthesis of B6S.
Synthesis of 1-methyl-3-(pyren-4-ylmethyl)-1,3-dihydro-2Himidazole-2-thione (B6S): A solution of B6 (0.5 g, 1.7 mmol)46, sulfur (0.27 g, 8.4 mmol) and sodium methoxide (0.45 g, 8.33 mmol) in anhydrous methanol (20 mL) was stirred at 65 ˚C for 15 h. Following solvent removal, dichloromethane was added and the resulting solution was washed with water. The organic phase was collected, dried over MgSO4 and concentrated in vacuum, giving a residue which was subjected to silica gel column chromatography using dichloromethane/methanol (30/1, v/v) as eluent. This gave B6S as pale yellow solid (0.42 g, 1.28 mmol, 76.4%). 1H NMR (300 MHz, DMSO-d6) δ (ppm): 8.51 (d, J = 9.3 Hz, 1H),
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Analytical Chemistry 8.35-8.26 (m, 4H), 8.23-8.15 (m, 2H), 8.13-8.08 (m, 2H), 7.89 (d, J = 7.8 Hz, 1H), 7.17 (d, J = 2.4 Hz, 1H), 6.97 (d, J = 2.4 Hz, 1H), 5.94 (s, 2H), 3.57 (s, 3H). 13C NMR (125.7 MHz, DMSO-d6) δ (ppm): 131.5, 131.3, 131.0, 130.9, 128.9, 128.9, 128.8, 128.2, 128.0, 127.6, 127.1, 126.3, 126.2, 125.6, 124.8, 124.5, 123.8, 119.7, 117.7, 49.0, 35.4. HR-MS (ESI): m/z calcd for C21H17N2S [M+H]+ 329.1112, found 329.1119. Fluorescence Assays in Solution. A stock solution of B6S (1 mM) in N,N-dimethylformamide (DMF) was diluted with PBS (10 mM, pH = 7.4, 5% DMF) to a final B6S concentration of 10 µM, and then treated with an appropriate aliquot of an ROS or RNS before fluorescence measurements with excitation at 355 nm and spectral slit widths of 3.0 and 5.0 nm. ROS and RNS Stocks Preparation.39 H2O2 was prepared with distilled water by using a 28% of H2O2 solution. NaClO was obtained by dilution of a 5% aqueous solution in water. With deionized water, a 70% solution was diluted to prepare tert-Butyl hydroperoxide (tBuOOH). 2,2'-azobis(2-amidinopropane) dihydrochloride was used to generate hydroxyperoxyl radical (ROO•).47-49 NO• was prepared by using sodium nitroferricyanide(III) dihydrate. The hydroxyl radical (•OH) was produced through the reaction between 200 µM of ferrous chloride and 400 µM of H2O2. Based on the published procedures,49,50 ONOO- was generated and the absorbance at 302 nm was used to calculate its concentration. Cytotoxicity tests. Cells in culture media were seeded in a 96well plate. After standing overnight, the cells were incubated with different concentrations of B6S for 24 h. To identify cell viability, reagents were removed and 0.5 mg/ml of MTT media was added to the cells, which were then incubated for 4 h at 37 ˚C in a CO2 incubator. The produced formazan was dissolved in 0.1 mL of dimethylsulfoxide (DMSO) and the solution was subjected to analysis using a Spectramax Microwell plate reader (OD at 650 nm). The mean cell viability was calculated as a percentage of the mean vehicle control and from three independent experiments. Cell Culture. Raw 264.7 cells were cultured on glass-bottomed dishes (NEST), sustained for 2 d in a 5% of CO2-humidified atmosphere at 37 °C. The serum-free medium was used as growth medium before labeling, and then 10 µM of B6S was added into the cells and incubated for 30 min. The culture medium for Raw 264.7 cells is supplementation of DMEM with 10 % fetal bovine serum, 100 µg mL-1 of streptomycin and 100 unit mL-1 of penicillin. Two-Photon Fluorescence Imaging. Two-photon fluorescence microscope images were obtained using multiphoton microscopes (Leica TCS SP8 MP) with ×40 oil objectives, numerical aperture (NA) = 1.30 and DMI6000B Microscope (Leica). To excite the probe, a mode-locked titanium-sapphire laser source (Mai Tai HP; Spectra Physics, 100 fs, 80 MHz) was used at 730 nm and 2.30 W as an output power, which corresponds to 1.11 x 106 W cm-2 focal plane’s average power. To maintain an appropriate cell atmosphere, live cell incubator system (Chamlide IC; Live Cell Instrument) was used to conduct the live cell imaging. Measurement of Two-Photon Cross Section. Femtosecond (fs) fluorescence analysis system was used to measure the twophoton cross-section (δ) as previously described elsewhere.51-53 Briefly, B6S (1.0 x 10-6 M) was dissolved in PBS buffer (10 mM, pH 7.4). Rhodamine 6G was used as reference to measure the intensities of two-photon excited fluorescence (TPEF) at 720-880 nm.53 The two-photon absorption (TPA) cross section was estimated with δ = δr(SsФrφrcr)/(SrФsφscs): where the s subscript refers to sample and r subscript stands for reference molecules.53 The intensities of the TPEF collected by charge-coupled device camera are represented as S, while Φ and φ are the one-photon fluorescence quantum yield and overall fluorescence collection efficiency. The δr is refer to two-photon absorption cross section of
the reference, and then c is the number density of the molecules in solution. Photostability. Photostability of B6S in Raw 264.7 cells was determined by measuring the intensities of TPEF as a function of time at the multiple selected sites of B6S treated cells. The digitized intensity was recorded with 2.00 sec intervals for the duration of 1 h using xyt mode. The TPEF intensities were collected at 380-600 nm when excited at 730 nm with femto-second pulses. RESULTS AND DISCUSSION The synthesis of B6S from B646 is explained in Scheme 1. Specifically, reaction of the imidazolium derivative B6 with sulfur in the presence of sodium methoxide produces B6S in a 76% yield. In the initial phase of this study, the spectroscopic responses of B6S to various ROS and RNS were assessed. As inspection of the spectrum in Figure S1 shows, the UV/Vis absorption spectrum of B6S contains absorption bands centered at 330 and 342 nm, and a shoulder at 360 nm. Upon addition of OCl- (100 µM) to a solution of B6S, the intensity of the shoulder decreases and a spectrum generated that corresponds to that of B6 is generated. In addition, under excitation of 355 nm, B6S in PBS exhibits a strong, broad and featureless fluorescence band centered at 482 nm, which matches that of the pyrene excimer (Figure 1). This observation indicates that the pyrene moieties in the excited state of B6S form a co-facial excimer.54,55 Addition of 0 to 100 µM OCl- to a B6S solution results in rapid appearance of intense (11-fold increase) peaks at 378 and 394 nm accompanied by a decrease in the intensity of the excimer emission at 482 nm. The new peaks match those of the typical fine structured emission bands of the pyrene monomer. The ratio of the fluorescence intensities at 482 and 378 nm (F482/F378) decreases 124-fold upon addition of 0 to 40 µM OCl- (Figure S2). The detection limit of B6S to OCl- was found as 0.2 µM, a value that is much lower than those reported concentration (20-400 µM) generated by neutrophils (Figure S4).56,57 Furthermore, the fluorescence response of B6S to OCl- varies only slightly over the broad pH range of 2 to 10 (Figure 2). High selectivity is an essential property of all ratiometric fluorescent probes. Importantly, results arising from the current effort show that B6S possess an excellent selectivity toward OCl- over the other ROS and RNS shown in Figure 3. Specifically, adding of OCl- (100 µM) to a solution of B6S induces a significant decrease 500 378 nm 400
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Figure 1. Changes of B6S (10 µM) fluorescence spectra as the addition of OCl- (0-100 µM). λex = 355 nm, slit 3/5 nm. Inset: photographs of B6S in the absence (left) and presence (right) of 100 µM of OCl- under UV irradiation (365 nm) and its excimer and monomer structures.
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NaOCl. The two-photon microscopic images of Raw 264.7 cells labeled with B6S were simultaneously obtained from the 380-430 nm (Fblue) and 480-600 nm (Fgreen) channels and their ratios were analyzed. We chose the ratio Fgreen/Fblue because clearer images were generated with this ratio than with its inverse form (Fblue/Fgreen). The results show that the average emission intensity ratios (Fgreen/Fblue) Raw 264.7 containing B6S gradually decrease from 4.4 to 2.8 upon NaOCl treatment (Figure S9).
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Figure 3. Relative fluorescence responses of B6S (10 µM) to various ROS (100 µM): 1. Blank, 2. H2O2, 3. NaOCl, 4. tBuOOH, 5. ROO•, 6. ONOO-, 7. HO•, 8. •NO in PBS (10 mM, pH 7.4) at room temperature. in the ratio F482/F378 while various other ROS and RNS, including H2O2, hydroxyl radical (•OH), tBuOOH, •NO, peroxynitrite (ONOO-) and ROO•, do not. The fluorescence changes described above are thought to be caused by OCl- promoted oxidative transformation of B6S, which displays pyrene excimer emission, to BS, which displays monomeric pyrene emission. To gain information to support this proposal, a 10 mM of phosphate-buffered saline solution (pH 7.4, 5% dimethylformamide) of B6S (10 µM) and OCl- (100 µM) was incubated for 1 min and then subjected to ESI-MS analysis. A peak at m/z 297 was observed in the mass spectrum, which is same as that of the molecular ion of B6 (Figure S5). In addition, the UV-vis and fluorescence spectra of this solution (Figure S6) were found to be identical to those of B6. Importantly, the results of a standard MTT assay indicates that B6S at low micromolar concentrations displays no marked cytotoxicity to cells (Figure S7). Thus, a cell imaging study was carried out using two-photon microscopy (TPM) to determine if B6S is applicable to ratiometric fluorescence imaging of OCl- in live biological samples. Before the initiation of cell imaging experiments, we measured the two-photon action cross-section of B6S. The results show that B6S has its highest TPA at 730 nm (Figure S8). Additionally, B6S has high photostability in live cells, as indicated by the observation that the two-photon excited fluorescence (TPEF) intensity of B6S remains almost constant after continuous irradiation with 2 s intervals for 1 h (Figure 4). With this information in hand, we carried out TPM imaging of Raw 264.7 macrophages containing various concentrations of
Figure 4. (a) Raw 264.7 cells incubated with B6S and its twophoton microscopic image. (b) The relative TPEF intensity from A-C in Figure (a) as a function of time. The digitized intensity was recorded with 2.00 sec intervals for the duration of 1 h using xyt mode. The TPEF intensities were collected at 380-600 nm when excited at 730 nm with femto-second pulses. Scale bar = 50 µm. Next, we assessed the endogenous OCl- response of B6S in live cells. Lipopolysaccharides (LPS), interferon gamma (IFN-γ) and phorbol myristate acetate (PMA) are known to promote production of H2O2 in macrophages, which is then converted to OCl– by the action of myeloperoxidase (MPO). Incubation of cells containing B6S with ROS inducers (100 ng mL-1 LPS, 50 ng mL-1 IFN-γ and 10 nM PMA) was found to cause a reduction in the average emission intensity ratio (Fgreen/Fblue) to 2.7 (Figure 5c) which is similar to that brought about by treatment of the cells with 500 µM NaOCl in the absence of the MPO inducers (Figure 3b). Furthermore, the reduction of Fgreen/Fblue remains at 3.9 when the MPO inhibitors 4-aminobenzoic acid hydrazide (4-ABAH)58 and flufenamic acid (FFA)59 are present in the cells (Figure 5d and e). These results show that TPM images of B6S directly reflect the presence of OCl- in the live cells.
Figure 5. Pseudocolored ratiometric two-photon microscopic images of Raw 264.7 cells incubated with 5 µM of B6S for 30 min. Cells were pretreated with (a) 0, (b) 500 µM of NaOCl for 30 min, (c) 100 ng mL-1 of LPS (16 h), 50 ng mL-1 of IFN-γ (4 h), 10 nM of PMA (30 min), (d) LPS, IFN-γ, PMA and 50 µM of 4ABAH (4 h) and (e) LPS, IFN-γ, PMA and 50 µM of FFA (4h) before treated with B6S. (f) Average Fgreen/Fblue ratios of the corresponding TPM images. Images were obtained using 730 nm
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excitation and 380-430 nm (blue) and 480-600 nm (green) emission windows. Scale bars = 25 µm. CONCLUSIONS In summary, this investigation has led to the successful development of B6S as a new ratiometric and two-photon emission probe to detect OCl-. Fluorescence emission from a solution of B6S undergoes a 104 nm blue-shift upon addition of OCl-. Moreover, we demonstrated that, owing to its beneficial properties including a short response time, high specificity and low cytotoxicity, B6S can be employed in living cell and tissues to detect and image exogenous and endogenous OCl-. The results suggest that B6S as a versatile probe will be an important addition to the imaging tool box used in research focusing on OCl- in living systems.
ASSOCIATED CONTENT Supporting Information The Supporting Information is available free of charge on the ACS Publications website. Synthetic schemes and methodology, inclusion of additional data such as 1H NMR, 13C NMR, ESI-MS, UV−vis, and fluorescence spectra (Figures S1-S15) (PDF)
AUTHOR INFORMATION Corresponding Author * E-mail:
[email protected]. Phone: +82 (031) 219-2609 * E-mail:
[email protected]. Phone: +82 (02) 3277-2400
ORCID Hwan Myung Kim: 0000-0002-4112-9009 Juyoung Yoon: 0000-0002-1728-3970
Author Contributions ‡
Equal contribution by these two authors to this work.
Notes No declaration for any conflict of interest.
ACKNOWLEDGMENT This study was supported financially by National Research Foundation of Korea (2012R1A3A2048814 to J. Y.; 2016R1E1A1A02920873 to H. M. K.) and National Natural Science Foundation of China (No. 21708041 for Q. X.). The Korea Basic Science Institute (Western Seoul) is acknowledged for the LC/MS data. FAB mass spectrometric data were performed by using a Jeol JMS 700 high resolution mass spectrometer at Korea Basic Science Institute (Daegu).
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