“Turn-on” fluorescent probe for detection of H2S and its applications in bioimaging

Article abstract of DOI:10.1016/j.saa.2017.08.002

A novel fluorescent probe (named YQ-1) containing disulfide-bond coumarin derivative was developed for H₂S. In response to H₂S, YQ-1 showed remarkable fluorescent emission enhancement at 462?nm. Besides, YQ-1 exhibited higher selectivity, faster response rate, low cytotoxicity and low detection limit (0.052?μM). Further, YQ-1 was used to detect the presence of H₂S level in living A549 cells, indicating YQ-1 has good membrane permeability and fluorescence properties.

Full text of DOI:10.1016/j.saa.2017.08.002

Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 189 (2018) 8–12
Contents lists available at ScienceDirect
Spectrochimica Acta Part A: Molecular and Biomolecular
Spectroscopy
journal homepage: www.elsevier.com/locate/saa
“Turn-on” fluorescent probe for detection of H2S and its applications
in bioimaging
Qi Zhao a,1, Jin Kang a,1, Ying Wen a, Fangjun Huo b, Yongbin Zhang b, Caixia Yin a,
⁎
a
Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Key Laboratory of Materials for Energy Conversion and Storage of Shanxi Province, Institute of Molecular
Science, Shanxi University, Taiyuan 030006, China
b
Research Institute of Applied Chemistry, Shanxi University, Taiyuan 030006, China
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 3 June 2017
Received in revised form 19 July 2017
Accepted 1 August 2017
Available online 03 August 2017
A novel fluorescent probe (named YQ-1) containing disulfide-bond coumarin derivative was developed for H2S.
In response to H2S, YQ-1 showed remarkable fluorescent emission enhancement at 462 nm. Besides, YQ-1
exhibited higher selectivity, faster response rate, low cytotoxicity and low detection limit (0.052 μM). Further,
YQ-1 was used to detect the presence of H2S level in living A549 cells, indicating YQ-1 has good membrane
permeability and fluorescence properties.
© 2017 Elsevier B.V. All rights reserved.
Keywords:
H2S
Fluorescent probe
Coumarin
Bioimaging
1. Introduction
inhalation exposures to H2S have also resulted in respiratory, olfactory,
cardiovascular, neurological, hepatic, and developmental neurochemical
Hydrogen sulfide (H2S), an important endogenously produced
gaseous signaling compound, plays an essential role in cellular physiology
and pathology. It is also considered the third most important
gasotransmitter for regulating cardiovascular, neuronal, immune, endo-
crine, and gastrointestinal systems, along with nitric oxide and carbon
monoxide [1–3]. Endogenous H2S is synthesized by mammalian tissues
via two pyridoxal-5′-phosphate-dependent enzymes responsible for me-
tabolism of L-Cysteine, cystathionine β-synthase (CBS) and cystathionine
γ-lyase (CSE), and by a third pathway that involves the combined action
of 3-mercaptopyruvate sulfurtransferase (3-MST) and cysteine amino-
transferase (CAT) [4–8]. Some studies show that production of endoge-
nous H2S and the exogenous administration of H2S can exert effects in
various pathologies [9]. In addition, endogenous H2S as a signal molecule,
it modulates blood pressure and neuronal activity, relaxes vascular
smooth muscle, inhibits insulin signaling, and possess antiinflammatory
and anti-apoptotic properties [10–13]. A variety of disease phenotypes
have been linked to endogenous levels of H2S, including Alzheimer's dis-
ease, Down's syndrome, diabetes, and liver cirrhosis [14–17]. On the
other hand, the excess H2S in the environment will stimulate respiratory
system and excessive inhalation will make people mental confusion, car-
diac arrest and even death [18]. Single, short-term and medium-term
effects and abnormal growth in developing cells [19]. Therefore, efficient
and reliable measurements of H2S concentrations in living systems would
be helpful to understand human health and disease.
The fluorescence based assays with advantages of high selectivity
and sensitivity, real-time imaging, non-invasive detection and high spa-
tiotemporal resolution [20–25], in contrast with the traditional detec-
tion method of H2S such as colorimetric assays, gas chromatography,
and sulfide precipitation [26–28]. Over the past few years, the synthesis
and design strategies for the development of fluorescent probes was
mainly based on unique reaction mechanisms, including H2S-mediated
reductions of azides or nitro groups, nucleophilic addition of H2S, cop-
per sulfide precipitation reaction, thiolysis of leaving groups [29–32].
Since M. Xian's group laboratory and several other groups reported
the first reaction-based fluorescent probes for H2S detection [33–37].
The strategy was based on a distinct H2S-mediated nucleophilic
addition followed by an intramolecular cyclization to turn on the fluo-
rescence signals [38]. This approach is particularly specific for H2S,
thus all of these works have us to design new H2S fluorescent probe.
In this work, we report a reactive disulfide-containing probe for the
detection of H2S based on the potential double nucleophilic attack of
H2S. This coumarin derivative was prepared from 2,2′-Dithiosalicylic
acid in one step using the procedure shown in Scheme 1. Theoretically,
the release of fluorophore involves two stages, that is, twice nucleophilic
reaction of H2S with disulfide-bond and ester group of YQ-1, whereas
other thiols such as cysteine can only undergo nucleophilic reaction
once. Therefore, the fluorescent signal should be selective only for H2S.
⁎
Corresponding author.
E-mail address: yincx@sxu.edu.cn (C. Yin).
Qi Zhao and Jin Kang contributed equally.
1
http://dx.doi.org/10.1016/j.saa.2017.08.002
1386-1425/© 2017 Elsevier B.V. All rights reserved.

Q. Zhao et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 189 (2018) 8–12
9
Scheme 1. The synthesis of YQ-1.
YQ-1 displayed a remarkable fluorescence “turn on” response to H2S
with low detection limit and high selectivity. Furthermore, YQ-1 was
successfully applied in fluorescent imaging in living cells.
(d, J = 7.7 Hz, 2H), 7.56 (s, 2H), 7.51 (s, 2H), 7.41 (d, J = 8.3 Hz,
2H), 6.53 (d, J = 9.6 Hz, 2H). 13C NMR (DMSO d6, 150 MHz): δ
(ppm): 163.2, 159.1, 153.5, 152.0, 143.2, 139.1, 134.0, 131.9, 128.9,
126.0, 125.2, 124.9, 118.2, 116.4, 115.2, 109.8 (Fig. S1). ESI-MS m/z:
[probe +H]+ Calcd. For 595.0443, Found 595.0542 (Fig. S2).
2. Materials and Methods
2.1. Materials and Instruments
2.3. Solutions Preparation and Optical Measurements
All solvents and reagents for synthesis and analyses were of analyti-
cal grade and bought from Sigma-Aldrich (St. Louis, MO) without further
purification. The solutions of cation were prepared from their chloride
salts. A pH meter (Mettler Toledo, Switzerland) was used to determine
the pH. TLC analysis was performed using precoated silica plates.
HITACHI F-7000 fluorescence spectrophotometer was employed to
measure fluorescence spectra. Shanghai Huamei Experiment Instru-
ment Plants, China, provided a PO-120 quartz cuvette (10 mm). 1H
NMR and 13C NMR experiments were performed with a Bruker
AVANCE-600 MHz NMR spectrometer, respectively (Bruker, Billerica,
MA). Coupling constants (J values) are reported in hertz. ESI determina-
tions were carried out on AB Triple TOF 5600plus System (AB SCIEX,
Framingham, USA). The ability of YQ-1 reacting to H2S in the living
cells was also evaluated using Leica Dmi8 Microsystems.
The stock solutions of H2S (2 mM) was prepared in deionized water,
sodium hydrosulfide solid was added to aqueous solution to prepare a
H2S solution. Reagents with analytical grades and demineralized water
were used for preparing the solutions. Stock solutions (2 mM) of F−
,
,
Cl−, Br−, I−, NO−3 , NO2−, AcO−, HCO−3 , CO32−, SCN−, SO32−, SO42−
S2O23−, ClO4−, PO34−, Cys, Hcy, GSH, were prepared by direct dissolution
of proper amounts of sodium salts. All other chemicals used were of an-
alytical grade.
The optical properties of YQ-1 were measured by UV–visible absorp-
tion spectra and fluorescence emission spectra in an aqueous solution
(PBS:MeCN = 7:3, pH = 7.4) using the following various analytes: F−
,
Cl−, Br−, I−, NO3−, NO2−, AcO−, HCO−3 ,CO32−, SCN−, SO23−, SO42−, S2O23−
,
ClO−4 , PO34−, Cys, Hcy, GSH. And any changes of fluorescence intensity
were detected using fluorescence instrument (λex = 410 nm, slit:
5 nm/5 nm).
2.2. Preparation and Characterization of the YQ-1
Synthesis of probe (YQ-1) is summarized in Scheme 1. 2,2′-
2.4. Cell Viability Assay
Dithiosalicylic acid (210 mg, 1.0 mmol), 4-dimethylaminopyridine
(40
mg,
0.3
mmol),
1-(3-dimethylaminopropyl)-3-
A549 cells were also used to study the cytotoxicity of YQ-1. The cell
viability assay was assessed by Cell Counting Kit-8 (CCK-8), and the ab-
sorbance at 450 nm was measured to explicate the cells viability [39].
A549 cells were seeded on a 96-well microtiter to a total volume of
100 μL/well, then the cells were incubated at 37 °C in a 5% CO2 incubator
for 24 h. Different concentrations of YQ-1 (0, 1, 2.5, 5, 10, 20, 30 and 50
μM) were then added to the wells. After incubation for 5 or 10 h, CCK-8
(10% in serum free culture medium) was added to each well, and the
plate was incubated for another 1 h. The absorbance of each well was
measured at 450 nm on a microplate reader.
ethylcarbodiimidehydrochloride (EDC, 400 mg, 2.1 mmol) and 7-
hydroxycoumarin (370 mg, 2.1 mmol) were mixed in 30 mL anhydrous
dichloromethane. The mixture was stirred at room temperature over-
night. The solvent was removed under reduced pressure. The resulting
residue was further purified by column chromatography on silica gel
using petroleum: dichloromethane: ethyl acetate (5:1:1, v/v/v) as
eluent to give the target as off-white solids (445 mg, 75%). 1H NMR
(DMSO d6, 600 MHz): δ (ppm): 8.36 (d, J = 7.7 Hz, 2H), 8.13 (d, J =
9.4 Hz, 2H), 7.87 (d, J = 8.0 Hz, 2H), 7.77 (t, J = 8.9 Hz, 2H), 7.74
Fig. 1. UV–vis spectral change (a) and fluorescence spectral change (b) of YQ-1 (10 μM) on the addition of H2S (0–100 μM) to the PBS: MeCN = 7:3 (v/v, pH = 7.4) solution. λex = 410 nm,
slit: 5 nm/5 nm. Inset: the color change of YQ-1 without and with addition of H2S under UV irradiation.

10
Q. Zhao et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 189 (2018) 8–12
exhibited a major absorption band centered at 320 nm and the intensity
decreased with the increasing concentration of H2S (0–100 μM).
Fig. 1(b) displayed the corresponding fluorescence spectra of YQ-1 (10
μM) upon the titration with different equivalents of H2S in MeCN-PBS
buffer (10 mM, pH = 7.4, 3:7, v/v), the fluorescence emission intensity
at 462 nm gradually increased with the increase of H2S concentration.
Meanwhile, the fluorescence of the solution changed from colorless to
blue under illumination with a 365 nm UV lamp.
3.2. The Selective Response of YQ-1 to H2S
In order to evaluate the selectivity of probe to H2S, YQ-1 (10 μM) was
treated with various relevant analytes, including F−, Cl−, Br−, I−, NO3−,
NO−2 , AcO−, HCO3−, CO32−, SCN−, SO32−, SO42−, S2O23−, ClO4−, PO43−, Cys,
Hcy, GSH, then their fluorescence emission was determinated by fluo-
rescence spectrophotometer. As shown in Fig. 2, comparing with other
analytes, fluorescence dramatic enhancement was observed upon the
addition of H2S (0.1 mM), even at high concentrations (1 mM), the re-
sponse of YQ-1 to any of the tested thiols was very low, exhibiting at
least 140- to 700-fold selectivity towards sulfide, which indicated that
YQ-1 was an excellent turn-on sensor for H2S. Furthermore, a visual
fluorescence color change photograph for H2S and other analytes
under illumination with a 365 nm UV lamp was recorded in Fig. S4.
These results distinctly demonstrated the outstanding selectivity of
YQ-1.
Fig. 2. The Fluorescence responses of YQ-1 (10 μM) solution in PBS: MeCN = 7:3 (10 mM,
pH = 7.4, 3:7, v/v) solution with H2S (0.1 mM) and other various relevant analytes
(1 mM): F−, Cl−, Br−, I−, NO3−, NO−2 , AcO−, HCO−3 , CO32−, SCN−, SO23−, SO42−, S2O32−
,
ClO−4 , PO34−, Cys, Hcy, GSH (λex = 410 nm).
2.5. Cell Imaging Experiments
The A549 cells were grown in Dulbecco's Modified Eagle's medium
supplemented with 12% Fetal Bovine Serum and 1% antibiotics at 37
°C in humidified environment of 5% CO2. The cells were plated on 6-
well plates and were incubated overnight. Before the experiments,
cells were washed with PBS 3 times. YQ-1 dissolved in MeCN (10 μL,
10 μM) was added to the cell medium (2 mL) at 10 μM final concentra-
tion. After incubating for 30 min, excess YQ-1 was lightly washed with
phosphate buffered saline (10 mM, pH = 7.4, 3:7, v/v) three times.
Meanwhile, another portion of A549 cells pre-treated with YQ-1 was
treated with H2S (50 μM) and incubated for further 30 min at 37 °C.
Cell imaging was then carried out after washing cells with PBS buffer
three times. Besides, YQ-1 could achieve blue channel recognition and
fluorescence images were recorded.
3.3. pH Dependence of YQ-1
As the pH value of biological environment is often considered as an
extremely influencing factor on interactions. To evaluate the effect of
different pH values on the fluorescence response of probe towards
H2S, the fluorescence intensity changes of probe induced by H2S were
investigated at pH 2–9. As shown in Fig. 3, YQ-1 gave obvious fluores-
cence enhancement responses at pH 7–9 with the addition of H2S,
which indicated that the fluorescence probe to H2S works fine in this
pH range. In contrast, YQ-1 is no fluorescent and the fluorescence inten-
sity is nearly unchanged in the pH range 2–6. YQ-1 did not show signif-
icant signals change at acidic pH (2–6) probably as a result of the weak
nucleophilicity of H2S under such a pH range. Accordingly, physiological
pH 7.4 is selected for further research.
3. Results and Discussion
3.1. Optical Properties of YQ-1
3.4. The Time-dependence in the Detection Process of H2S
The UV–vis absorbance and fluorescence emission spectra were in-
vestigated to evaluate the optical properties of YQ-1 in MeCN-PBS buffer
(10 mM, pH = 7.4, 3:7, v/v). As the Fig. 1(a) shows, YQ-1 (10 μM)
To further understand the reaction of YQ-1 with H2S, time-depen-
dence modulations in the fluorescence spectra of probe were monitored
in the presence of 10 equiv. of H2S (Fig. 4). From the fluorescence curve
Fig. 3. Fluorescence intensity at 462 nm of probe (10 μM) at different pH values in the
presence of H2S (100 μM) and in the absence of H2S.
Fig. 4. Reaction time profiles of YQ-1 in the presence of H2S in PBS: MeCN = 7:3 (10 mM,
v/v, pH = 7.4) solution.

Q. Zhao et al. / Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 189 (2018) 8–12
11
fluorophore, which was confirmed by MS (Fig. S3), 1H NMR (Fig. S1,
S2). As shown in Scheme 2, the cyclization product 7-Hydroxycoumarin
is the raw material for the synthetic probe and confirmed by MS (Fig.
S3). The ESI-MS of the probe + NaHS, m/z: 163.09. Furthermore, 1H
NMR titrations experiment was performed with the aim of supporting
our points. As shown in Fig. S5, with addition of NaHS (resolved in
D2O) to probe in DMSO d6, the resonance of the original proton at
8.43(Ha), 8.15(Hd), 7.57(Hb), 6.55(Hc) ppm disappeared and new
peaks at 8.03(Ha), 7.85(Hd), 6.56(Hb), 6.05(Hc) ppm appeared. These
signal changes demonstrated how the nucleophilic addition-cyclization
process occurred during the detection process of YQ-1 towards H2S.
3.7. Cell Viability Assay
In terms of practical applications, biocompatibility is essential for
bio-probes. The effect of bio-probes on the physiological behaviors of
cells should be emphasized in the matter of live cell imaging applica-
tions [45]. Accordingly, cytotoxicity of YQ-1 for human A549 cells was
studied by CKK-8 method (Fig. S6). Cytotoxicity experiments displayed
minimal cytotoxicity of YQ-1 towards A549 cells at a concentration of
50 μM (92.3% viability). In general, at the staining concentration of
YQ-1, no evident cytotoxic responses were observed for all of the tested
cells after incubation for 10 h. These results showed that YQ-1 exhibited
good biocompatibility and low cytotoxicity for luminescence cell imag-
ing under the applied conditions.
Fig. 5. The linearity of the relative fluorescence intensity versus H2S concentration.
we can figure out that the maximal fluorescence signal was reached
within 10 min, indicating the sensor can achieve real-time detection
of H2S. Therefore, 10 min reaction time was chosen for the following
experiments.
3.5. The Detection Limit of YQ-1 for H2S
3.8. Imaging of Living Cell
The detection limit of YQ-1 for H2S was investigated in the Fig. 5 and
was found to be 0.052 μM based on the definition by IUPAC (CDL =
3Sb/m) [40–43]. The detection limit for H2S was calculated by the equa-
tion: detection limit = 3σ/m, where σ = standard deviation of 10 blank
measurements and m = slope obtained from the graph of fluorescence
intensity versus concentration of H2S. YQ-1 is able to detect low micro-
molar concentrations of H2S.
To evaluate the capability of YQ-1 to detect H2S in cells, A549 cells
stain with YQ-1 (10 μM) were treated with 50 μM NaHS for 30 min. As
show in Fig. 6b, A549 cells only incubated with YQ-1 (10 μM) for
30 min, fluorescence could not observed in the blue channel. In a further
experiment it was found that the fluorescence intensities from the blue
channel clearly increased after the cells were incubated with NaHS
(Fig. 6d). These cell experiments showed the good cell-membrane
permeability of YQ-1, thus it could be used to detect the presence of
H2S in living cells.
3.6. Proposed Mechanism
The reaction mechanism of the present system was investigated and
showed in Scheme 2. As expected, YQ-1 would specifically react with
H2S to release the fluorophore. H2S (pKa 6.9) as a nucleophile could
react with\\S\\S\\group of YQ-1 and generate an unstable intermedi-
ate A. If the electrophile presented at suitable position, such as the ester
group shown in A, the\\SH group should undergo a spontaneous cycli-
zation to release the fluorophore 7-Hydroxycoumarin A2 and form
product A1 [44]. When YQ-1 was treated with biological thiols, product
B should not undergo the cyclization to release the fluorophore, thus
fluorescence enhancement was not observed from the solution contain-
ing GSH, Cys, Hcy. These results clearly demonstrated the excellent se-
lectivity of YQ-1 even when H2S coexisted with biological thiols. We
presumed that the color change and fluorescence enhancement could
be attributed to the intramolecular cyclization that releases the
4. Conclusions
In summary, a novel probe YQ-1 for highly selective and sensitive
detection of H2S based on coumarin derivatives was synthesized and
characterized, which can be used as a fluorescent response probe for
H2S in PBS: MeCN (10 mM, 7:3, v/v) solution. This reaction proved to
be selective for H2S and it did not proceed with other biological thiols
such as cysteine and glutathione. Furthermore, YQ-1 displayed a conve-
nient detection process (within 10 min), a good linearity range, low cy-
totoxicity and a low detection limit of H2S (0.052 μM). The fluorescence
scanning microscopic experiments demonstrated that YQ-1 can be used
to detect intracellular H2S in living A549 cells.
Scheme 2. Proposed sensing process of YQ-1for H2S.

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