A BODIPY-based fluorescent sensor for the detection of Pt2+ and Pt drugs

Article abstract of DOI:10.1039/d0cc00027b

A BODIPY-based fluorescent sensor PS with an NO₄S₂ podand ligand was studied for the selective detection of Pt²⁺ over 21 cations as well as selected platinum drugs in aqueous medium. The platinum sensor PS shows 28-fold, 22-fold and 14-fold fluorescence turn-on enhancements to Pt²⁺, cisplatin and nedaplatin, and was thereby employed to detect platinum drugs in A-549 human lung cancer cells.

Full text of DOI:10.1039/d0cc00027b

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A BODIPY-based fluorescent sensor for the detection of Pt2+ and
Pt drugs
Received 00th January 20xx,
Accepted 00th January 20xx
DOI: 10.1039/x0xx00000x
Fung-Kit Tang,a† Jiaqian Zhu,b† Fred Ka-Wai Kong,c Maggie Ng,c Qingyuan Bian,a Vivian
Wing-Wah Yam,*c Anfernee Kai-Wing Tse,*d Yu-Chung Tse*e and Ken Cham-Fai Leung*a
A BODIPY-based fluorescent sensor PS with NO4S2 podand ligand development of next generation of platinum drugs. The current
was studied for selective detection of Pt2+ over 22 cations as well as analysis of platinum usually involves destructive methods,
selected platinum drugs in aqueous medium. The platinum sensor which requires sophisticated sample pre-treatment and costly
PS shows a 28-fold, 22-fold and 14-fold fluorescent turn-on instruments.20-24 Meanwhile, some studies have incorporated
enhancements to Pt2+, cisplatin and nedaplatin, thereby employed the platinum drug with a luminescent labelling agent to allow
to detect platinum drugs in A-549 human lung cancer cells.
biological imaging of the drug in cellulo to provide real time
visualization of cisplatin or other platinum drugs.25-29 However,
the extensive modifications of the platinum drug structures may
limit their drug actions, thereby the results may not truly reveal
the localization of drugs.
As a result, a direct detection protocol for the original drugs
or drug metabolites would be more favorable to study the
actual drug dynamics in real time. The progress is limited due to
the difficulty in molecular recognition, and the detection of
organoplatinum drugs is challenging because of its slow ligand
exchange rate.30-32 To date, a few literatures have reported the
use of small molecular sensors for specific detection of
organoplatinum drugs.33-40 Koide and coworkers have reported
the detection of platinum species based on Pt-catalyzed Tsuji–
Platinum has been known and widely used in our daily life,
including jewelry, automotive catalytic converters, chemistry
research, industrial processing and medicines. Since the
discovery of cisplatin complex in 19651 as a cell growth inhibitor
(DNA alkylating agents), platinum complexes have evolved to
become common chemotherapeutic agents for carcinomas,
such as testicular, ovarian and lung cancers.2-6 To date, many
platinum derivatives have been developed to enhance the
7
solubility, drug circulation and efficacy.5, For example, the
modification of the stationary ligands8 and the oxidation of Pt(II)
to form Pt(IV) prodrugs.9 Based on these strategies, a number
of platinum drug delivering systems have been developed in the
research.10-15 However, the utilization of platinum drugs is often
controversial. It has been reported that platinum drugs or salts
are associated with allergy, ototoxicity, neurotoxicity and
nephrotoxicity.16-19
Therefore, studying the drug actions and side effects of
current platinum drugs has become a crucial factor in the
a. Department of Chemistry, State Key Laboratory of Environmental and Biological
Analysis, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR, P. R. China
b. Centre for Cancer and Inflammation Research, School of Chinese Medicine, Hong
Kong Baptist University, Hong Kong SAR, P. R. China.
c.
Department of Chemistry, The University of Hong Kong, Pokfulam Road, Hong
Kong SAR, P. R. China
d. Programme of Food Science and Technology, Division of Science and Technology,
Beijing Normal University-Hong Kong Baptist University United International
College, Zhuhai 519087, P. R. China
Fig. 1 (a) Chemical structure of PS. (b) Fluorescence spectra of PS (5
μM) upon addition of various cations and metal ions (20 mol equiv.).
(c) Photographs of PS (5 µM) with 20 mol equiv. of different cations
and metal ions in quartz cuvettes under 360 nm UV light. Conditions:
DMF–HEPES (v/v = 3:7, 10 mM, pH = 7.2, 25 C), λex = 500 nm.
e. Guangdong Provincial Key Laboratory of Cell Microenvironment and Disease
Research, Department of Biology, Southern University of Science and Technology
(SUSTech), Shenzhen, 518055, P. R. China
† Equal contribution
Electronic supplementary information (ESI) available: experimental details,
synthesis, NMR, MS, UV–Vis, fluorescence spectra and in vitro cell experiments.
*
Email:
cfleung@hkbu.edu.hk,
wwyam@hku.hk,
kaiwingtse@uic.edu.hk,
tseyc@sustech.edu.cn
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Trost reaction, but the reaction may require the addition of emission intensity at 520 nm was insignificant comVpieawreArdtictleoOtnhlianet
2+
2+
PPh3 as a reducing agent.33, 34 Tae and coworkers reported a of Pt . In the interference test with other cations, only Pd
rhodamine triazole conjugate for Pt(II) species with a ring- slightly altered the fluorescence signal, but PS can still give
opening strategy.35 Recently, New and coworkers have reported comparable emission intensities in the presence of other
a fluorescein sensor for monofunctional platinum drugs.37 Ang existing ions (Fig. S4, ESI†). Overall, the selectivity performance
and co-workers have also reported several chemosensors for showed that PS was applicable to distinguish Pt2+ from other
the detection of cisplatin from Pt(IV) prodrugs.38-40 A brief relevant soft metal ions. Moreover, the selectivity for different
summary of these Pt chemosensors is highlighted in Table S1 of Pt(II) complexes and organoplatinum drugs was also tested. PS
ESI†. Herein, we report the design of a novel boron- could recognize K2PtCl4 and PtCl2 in aqueous medium, but the
dipyrromethene (BODIPY)-based fluorescent sensor PS for increase in emission intensity with PtCl2 was to a lesser extent
DOI: 10.1039/D0CC00027B
molecular recognition of Pt2+ and organoplatinum drugs.
due to its poor solubility in aqueous medium (Fig. S5, ESI†).
PS was synthesized via a six-step protocol (Scheme S1, ESI†). Surprisingly, PS could also recognize cisplatin and nedaplatin,
In brief, thiosalicylic acid was employed to form a O‒S‒N‒S‒O which both gave significant fluorescence turn-on response with
podand-like ligand which mimics methionine as a strong 22-fold and 14-fold, respectively. Other drug derivatives like
nucleophile for Pt(II) species.41-44 The ligand scaffold with oxaliplatin, carboplatin and Pt(IV) complex 6 gave no emission
carboxylate groups could enhance the water solubility, and the enhancement (Fig. 2).
thioethers could form a recognition site for the molecular Pt(II)
Fluorescence titration of PS against Pt2+ was studied,
species. The proposed detection scheme is depicted in Scheme revealing that the fluorescence intensity was linearly
S3 in ESI; its fluorescence off-on phenomenon is based on a proportional to the concentration of Pt2+ in the range of 0–200
photoinduced electron transfer (PeT) mechanism, which is a µM (Fig. S6, ESI†). The effect of pH on the performance was also
common strategy employed in the design of fluorescence investigated, in which PS did not give any fluorescence change
sensors.45-49 The intermediate compounds were characterized with variation of pH of the solution mixture. PS was able to
by 1H and 13C NMR spectroscopy and high-resolution mass show significant fluorescence turn-on with Pt2+ between pH 5
spectrometry (HRMS) (Fig. S20–S39, ESI†).
and pH 10, suggesting a reliable detection method for Pt2+ in
The photophysical properties of PS were studied. PS showed biologically relevant pH range (Fig. S7, ESI†). The Job’s plot
no obvious change in the UV–visible absorption spectrum but a suggested a 1:1 binding stoichiometry between PS and Pt2+ (Fig.
strong green fluorescence signal was observed upon the S8, ESI†). The absolute photoluminescence quantum yields of
addition of Pt2+ (Fig. S1–S2, ESI†). The time course of PS in the presence of analytes were measured, and the
fluorescence enhancement of PS towards Pt2+ was measured, measured values were consistent with the result from the
and an incubation time of 6 h was chosen as a reference point selectivity studies (Fig. S9–S10, ESI†).
(Fig. S3, ESI†). The fluorescence performance of PS in aqueous
To further understand the binding of PS, a model ligand
solution for different cations or metal ions was further studied compound L was synthesized (Scheme S2, ESI†). The reaction
to prove its effectiveness. PS exhibited a high selectivity for Pt2+ mixtures of K2PtCl4 and cisplatin with compound L were
+
over the other 22 types of cations or metal ions including NH4 , analyzed by mass spectrometry. The high resolution mass
Li+, Na+, K+, Mg2+, Ca2+, Al3+, Cr3+, Mn2+, Fe2+, Fe3+, Co2+, Ni2+, Cu2+, spectra also indicated a 1:1 binding between Pt2+ and the ligand
Zn2+, Pd2+, Ag+, Cd2+, Au3+, Hg2+ and Pb2+, and the selectivity motif, and the isotopic pattern analysis of the m/z peaks
performance was retained in the interference test (Fig. 1 and suggested the complexation of [L–H+Pt]+ and [L–2H+Pt+Na]+
Fig. S4, ESI†). Only Ag+ gave a slight turn-on response, but the species (Fig. S11–S12, ESI†). Unfortunately, single crystals of the
complex could not be isolated for further analysis, but the 195Pt
NMR of the complex ensemble showed a chemical shift from
‒1617 ppm to ‒1582 ppm, suggesting a change of the
coordination environment (Fig. S13, ESI†). To investigate the
detection mechanism of PS towards Pt2+, geometry
optimizations have been carried out on PS and PS+Pt2+ by
density functional theory (DFT). The result of DFT calculation
suggested that PS+Pt2+ in the O^S^S^O conformation is more
stable than those in the O^S^N^O and O^S^N^S binding modes
by 7.88 kcal mol–1 and 12.33 kcal mol–1, respectively (Fig. S14,
ESI†). The optimized geometries of PS and PS+Pt2+ in the
O^S^S^O binding mode, with selected structural parameters,
and their molecular orbital diagrams are shown in Fig. 3a–3b
Fig. 2 Fluorescence response of PS (5 µM) upon addition of different
and Fig. S15‒S16, ESI†. Upon the excitation of the BODIPY
moiety, in the absence of Pt2+, there are two occupied orbitals
localized on the O^S^S^O moiety of PS between the HOMO and
the LUMO of the BODIPY moiety. This can facilitate the
reductive PeT to the BODIPY moiety and hence the fluorescence
is quenched. On the other hand, when Pt2+ is bound by the
Pt complexes (20 mol equiv.) with time. Inset (top): photograph of PS
(5 µM) with different Pt complexes (20 mol equiv.) in quartz cuvettes
under 360 nm UV light after incubation of 12 h. Conditions: DMF–
water solution (v/v = 1:9, pH = 7, 25 C), λex = 500 nm. The
corresponding complex structures and names are shown in index for
reference.
2 | J. Name., 2012, 00, 1-3
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Fig. 3 The ground-state geometries of (a) PS and (b) PS+Pt2+ in the
O^S^S^O binding mode optimized at the PBE0 level, and (c) their
molecular orbital diagrams. Hydrogen atoms are omitted for clarity.
The bond lengths and angles shown in (a) and (b) are in Å and
degrees whereas the energies shown in (c) are in Hartree. The label
of BODIPY and O^S^S^O in (c) represents the orbitals localized on the
BODIPY moiety and the O^S^S^O ligand respectively.
Fig. 4 Confocal laser scanning microscopic images (CLSM) of A549
cells. (Left) Cells were exposed with different platinum species (10
µM) for 4 h and then incubated with PS (10 µM) for 30 min at 37 C.
(a) K2PtCl4; (b) cisplatin; (c) oxaliplatin; (d) nedaplatin and (e)
carboplatin. (Right) Cells were exposed with different concentration
of cisplatin (0.1–10 µM) for 4 h and then incubated with PS (10 µM)
for 30 min at 37 C. (f) 0.1 µM; (g) 1 µM; (h) 5 µM and (i) 10 µM of
cisplatin. Scale bar represents 10 μm.
O^S^S^O ligand of PS, there are no occupied orbitals between
the HOMO and LUMO of the BODIPY moiety. As a result, it is
unfavorable for the reductive PeT to occur and these calculation
results are consistent with the proposed detection scheme
(Fig.3c and Scheme S3, ESI†). All the data suggested that PS and
its model compound L could recognize Pt2+ in the coordination
site.
5‒10. Our studies showed that PS binds to Pt2+ in a 1:1 ratio in
O^S^S^O binding conformation, and chelation induced
fluorescent off-on is based on the PeT mechanism. The cell
imaging experiments have successfully demonstrated the
localization of cisplatin and other drug derivatives in A-549
cancer cells. Since the application and research of
organoplatinum drugs are inevitable in clinics nowadays, PS can
serve as a reliable imaging tool for the study of post-Pt-drug
treatment, drug resistance and development of new
generations of drugs. Based on this sensor scaffold, further
optimization and design will be required in the future to furnish
an enhanced chemotherapy.
The authors acknowledge the mass spectrometry assistance
by Dr. Judy T.S. Lum in Department of Chemistry, Dr. Tao Wang
and Mr. David T.W. Chik from the State Key Laboratory of
Environmental and Biological Analysis, HKBU. F.-K.T.
acknowledges Ms. Regina Huang in Department of Chemistry,
HKBU for the discussion and design of experiments. K.C.-F.L.
acknowledges the financial support from the State Key
Laboratory of Environmental and Biological Analysis and the
President’s Award for Outstanding Performance in Research
Supervision of HKBU. The computations were performed using
the research computing facilities offered by the HKU
Information Technology Services (ITS).
With favorable in vitro testing results in aqueous medium,
PS was then applied to monitor the platinum dynamics in A-549
human lung carcinomas, which is a common study target for Pt
51
complexes.50,
We first demonstrated that PS exerted no
apparent cytotoxic effects against A-549 cells using MTT (3-(4,5-
dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay
(Fig. S17, ESI†). The probe concentration of PS can be up to 20
µM without significant alteration to the cell viability. For
confocal imaging, cells were treated with different Pt(II)
derivatives (10 µM) for 4 h, followed by treatment of PS (10 µM)
for 30 min. Then the cells were washed twice with PBS and fixed
with ice-cold methanol. By using a confocal laser scanning
microscope with excitation at 488 nm, the fluorescence images
revealed that Pt(II) derivatives (including K2PtCl4, cisplatin and
nedaplatin) showed strong green fluorescence in the cytoplasm
and medium fluorescence in the nuclei of A-549 cells (Fig. 4a,
4b, 4d and Fig. S18, ESI†). Moreover, oxaliplatin and carboplatin
displayed very weak fluorescence signals upon PS treatment
(Fig. 4c and 4e), which is consistent with our finding (Fig. 2 and
Fig. S9, ESI†). In addition, we observed that the fluorescence
intensities increased with the concentration of cisplatin from
0.1 µM to 10 µM (Fig. 4f–4i and Fig. S19, ESI†). Overall, these
results showed that PS is capable of detecting cisplatin and
other Pt(II) derivatives in human cells.
Conflicts of interest
There are no conflicts to declare.
In conclusion, a fluorescent chemosensor PS with high
selectivity for Pt2+, cisplatin and nedaplatin was discovered. PS
could detect Pt2+ in aqueous medium with working pH range of
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A novel BODIPY-based fluorescent sensor PS was designed for
imaging Pt2+, cisplatin and nedaplatin in aqueous medium and
biological environments, providing great potential for studying the Pt-
drug metabolism and the development of new organoplatinum drugs.
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