Tetraphenylethylene conjugated: P -hydroxyphenacyl: Fluorescent organic nanoparticles for the release of hydrogen sulfide under visible light with real-time cellular imaging

Article abstract of DOI:10.1039/c8ob01629a

Hydrogen sulfide (H₂S) behaves like a two-edged sword, at low concentrations it has beneficial and cytoprotective effects, while at higher concentrations it exhibits toxicity. Hence there is a keen interest in developing light responsive H₂S donors with a spatio-temporal controlled release. Herein, we report visible light activatable tetraphenylethylene conjugated p-hydroxyphenacyl (TPE-pHP-H₂S) nanoparticles for the release of hydrogen sulfide (H₂S) with a real time monitoring ability. Our newly designed photoresponsive single component organic nanoparticle based H₂S donor is built by integrating the tetraphenylethylene (TPE) moiety and p-hydroxyphenacyl (pHP) group so that it can display both aggregation-induced emission (AIE) and excited state intramolecular proton transfer (ESIPT) properties. Aggregation-induced emission enhancement was exhibited by our TPE-pHP-H₂S NP donor, which was then explored for the cellular imaging application. The ESIPT by the pHP moiety provided unique advantages to our TPE-pHP-H₂S NP donor which include (i) the excitation wavelength extended to >410 nm (ii) a large Stokes shift (iii) a low inner filter effect and (iv) real-time monitoring of H₂S release by a simple fluorescent colour change. In vitro studies showed that the TPE-pHP-H₂S NP donor presents excellent properties like real-time monitoring, photoregulated H₂S release and biocompatibility.

Full text of DOI:10.1039/c8ob01629a

Organic &
Biomolecular Chemistry
View Article Online
View Journal | View Issue
PAPER
Tetraphenylethylene conjugated
p-hydroxyphenacyl: fluorescent organic
nanoparticles for the release of hydrogen sulfide
under visible light with real-time cellular imaging†
Cite this: Org. Biomol. Chem., 2018,
6, 7903
1
a
a
b
b
C. Parthiban, Pavithra M., L. Vinod Kumar Reddy, Dwaipayan Sen,
a
a
Melvin Samuel S. and N. D. Pradeep Singh
*
Hydrogen sulfide (H
protective effects, while at higher concentrations it exhibits toxicity. Hence there is a keen interest in
developing light responsive H S donors with a spatio-temporal controlled release. Herein, we report
visible light activatable tetraphenylethylene conjugated p-hydroxyphenacyl (TPE-pHP-H S) nanoparticles
for the release of hydrogen sulfide (H S) with a real time monitoring ability. Our newly designed photo-
responsive single component organic nanoparticle based H S donor is built by integrating the
2
S) behaves like a two-edged sword, at low concentrations it has beneficial and cyto-
2
2
2
2
tetraphenylethylene (TPE) moiety and p-hydroxyphenacyl (pHP) group so that it can display both aggre-
gation-induced emission (AIE) and excited state intramolecular proton transfer (ESIPT) properties.
2
Aggregation-induced emission enhancement was exhibited by our TPE-pHP-H S NP donor, which was
then explored for the cellular imaging application. The ESIPT by the pHP moiety provided unique advan-
Received 27th July 2018,
Accepted 3rd October 2018
tages to our TPE-pHP-H S NP donor which include (i) the excitation wavelength extended to >410 nm (ii)
2
a large Stokes shift (iii) a low inner filter effect and (iv) real-time monitoring of H
fluorescent colour change. In vitro studies showed that the TPE-pHP-H S NP donor presents excellent
properties like real-time monitoring, photoregulated H S release and biocompatibility.
2
S release by a simple
DOI: 10.1039/c8ob01629a
2
rsc.li/obc
2
1
4
(
NO). Interestingly, studies have shown that the biological
Introduction
effects of H S are dependent on its concentration, at low con-
2
In recent times, substantial research work has been carried centrations it has beneficial and cytoprotective effects, while at
1
5
2
out for the development of external stimuli responsive higher concentrations it exhibits toxicity. Hence, several H S
1
–5
16
gasotransmitters.
Among the existing gasotransmitters, donors triggered by different stimuli (pH, reaction with glu-
1
7
18
hydrogen sulfide (H S) is more significant due to its influence tathione (GSH), esterase-activated release, redox-controlled
2
6
19
20
over a wide range of physiological and pathological processes.
S acts as a signaling molecule and mediator of important them light induced H
cellular processes causing several beneficiary effects like anti- attention because of their ability to provide spatio-temporal
release, and temperature ) have been developed. Among
H
2
2
S donors have gained considerable
2
1–23
inflammatory, antioxidative, vasorelaxant and cytoprotective control over the release.
7
,8
effects.
H
2
S is made endogenously in a smaller amount by
To date, different types of UV light responsive
different mammalian tissues as a protecting factor against Gasotransmitter Donors (GDs) for the release of H S have been
2
2
4–26
many diseases like cardiovascular disease, metabolic syn- developed.
But the major limitation of using UV light
9
–13
drome, obesity and neurodegenerative diseases.
Recent responsive GDs for the release of H S is the phototoxicity
2
studies have acknowledged that H S is a third gaseous trans- associated with the UV light. Of late, Chakrapani and co-
2
mitter, in addition to carbon monoxide (CO) and nitric oxide workers described BODIPY-caged thiocarbamate based visible
2
7
light activated carbonyl sulfide (COS) release. The released
COS consequently gets hydrolysed into H S in the presence of
carbonic anhydrase (Fig. 1a). The limitation of the abovemen-
2
a
Department of Chemistry, Indian Institute of Technology Kharagpur,
Kharagpur-721302, West Bengal, India. E-mail: ndpradeep@chem.iitkgp.ernet.in
2
tioned visible light activated H S donor is its inability to
b
Centre for Biomaterials, Cellular and Molecular Theranostics, VIT University,
monitor the release of H S in real time. Furthermore, the
2
Vellore-632014, Tamil Nadu, India
above visible light activated H
(carbonic anhydrase) for the release of H S. Later, our group
2
S donor needs an external agent
†
Electronic supplementary information (ESI) available. See DOI: 10.1039/
2
7
c8ob01629a
2
This journal is © The Royal Society of Chemistry 2018
Org. Biomol. Chem., 2018, 16, 7903–7909 | 7903

View Article Online
Paper
Organic & Biomolecular Chemistry
Keeping the importance of AIE and ESIPT in mind, we
intend to design for the first time a photoresponsive single
component organic nanoparticle based H S donor which can
2
exhibit the combined benefits of AIE and ESIPT phenomena.
The H S donor was developed by integrating the tetraphenyl-
2
ethylene (TPE) moiety and p-hydroxyphenacyl (pHP) group
(
2
Fig. 1c). Our designed H S donor provided advantages like (i)
aggregation-induced emission enhancement (ii) a large Stokes
shift (iii) the excitation wavelength extended to >410 nm, (iv)
unlocking of photorelease of H S in the aggregated state, (v)
2
real-time monitoring of H S release by a simple fluorescent
2
colour change and (vi) no requirement of additional reagent
for the release of H S.
2
Results and discussion
The TPE-pHP-H
2
S donor was synthesized according to the fol-
lowing procedure (Scheme 1). The synthesis of compounds 2
2
8
and 3 was carried out according to the reported procedure.
On the other hand, compound 4 was treated with 4-nitrobenzo-
phenone (5) in the presence of TiCl in dry THF at reflux for
4
5
h to afford 6. Next, compound 6 was treated with 10% Pd/C
in dry ethanol at reflux for 4 h to furnish 7. Finally, the reac-
tion between 3 and 7 for 3 h in methanol at reflux yields our
desired product 8. The products were characterized by NMR
1
13
(
(
H and
Fig. S6†).
The TPE-pHP-H
C) spectroscopy (Fig. S1 to S5†) and HR-MS
2
S NP (nanoparticle) donor was prepared by
the reprecipitation technique (Scheme S1†). The surface mor-
2 2
Fig. 1 Visible light-triggered H S donors, (a) COS/H S donor, (b) ESIPT
phology of the TPE-pHP-H S NP donor was monitored by high-
2
2
based H S donor, and (c) design of AIE + ESIPT based photoresponsive
resolution transmission electron microscopy (HR-TEM). It
showed that the prepared nanoparticles were spherical in
shape with a size ∼35 nm (Fig. 2a). A DLS (dynamic light scat-
single component organic nanoparticles for H
monitoring ability.
2
S release with a real time
developed a visible light activated ESIPT based H
2
S donor
using p-hydroxy phenacyl as a phototrigger with a real time
2
8
monitoring ability (Fig. 1b).
Recently, AIE, a novel photophysical phenomenon, has
been utilized in a wide range of applications, such as cell
imaging, biosensing and therapeutics, fluorescent sensors,
2
9–31
optoelectronic and energy devices etc.
This AIE process
has attracted great attention from the scientific community
because of its unique properties like high signal to noise ratio,
tremendous photostability in the solution phase and remark-
able emission properties of a molecule in the aggregated state.
AIE chromophores are extremely emissive in their aggregated
3
0
state however they exhibit weak fluorescence in solution. The
regulated intramolecular motion in the aggregated state plays
a substantial role. Among the different AIE chromophores,
tetraphenylethylene (TPE) has excellent fluorescence in the
aggregated state, because of the restriction of molecular
Scheme 1 Synthesis of the TPE-pHP-H
a) Bromoacetyl bromide, AlCl , CH Cl
acetone, H O, 2 h; (c) Zn, TiCl , THF, reflux, 5 h; (d) (NH
Pd/C, EtOH, reflux; (e) MeOH, reflux, 3 h.
2
S donor. Reaction conditions:
, 35 °C, 15 h; (b) Na S·9H O,
·H O, 10%
3
2
motion. TPE has been used in various applications such as
chemo/biosensors, solar cells, optoelectronic devices, field
(
3
2
2
2
2
2
4
2
)
2
2
3
3–36
effect transistors and light emitting diodes.
7904 | Org. Biomol. Chem., 2018, 16, 7903–7909
This journal is © The Royal Society of Chemistry 2018

View Article Online
Organic & Biomolecular Chemistry
Paper
trations in aqueous acetonitrile were recorded and we observed
an increase in the emission intensity of TPE-pHP-H S NPs
2
(
Fig. S7†).
To examine the photochemical properties of the
TPE-pHP-H S NP donor, a solution of TPE-pHP-H S NP donor
2
2
4
(
1 × 10− M, 5 mL) in CH
3
CN/PBS buffer (0.1 : 9.9 v/v) was irra-
diated with a medium-pressure mercury lamp (125 W, incident
1
6
intensity (I ) = 2.886 × 10 quanta per s) as the source of
0
visible light (λ ≥ 410 nm) using a suitable UV cut-off filter
(
2
1 M NaNO solution) with constant stirring for 20 min. The
photodecomposition of the TPE-pHP-H S NP donor was ana-
2
lyzed by reversed-phase HPLC. As shown in Fig. 4a, the steady
t
disappearance of a peak at R = 7.42 min corresponding to the
TPE-pHP-H S NP donor indicates gradual photodecomposition
Fig. 2 TPE-pHP-H
b) DLS.
2
S NP donor (a) HR-TEM in aqueous acetonitrile and
2
(
of the
H
2
S
donor with respect to irradiation time.
Furthermore, the appearance and continuous increase in the
intensity of the new peak at R = 4.67 min indicate the for-
t
tering) study in Fig. 2b shows that the synthesized nano- mation of the photoproduct (13). The newly formed peak at
particles have ∼35 nm of diameter on average, which is almost
similar to the size obtained in the HR-TEM image.
t
R = 4.67 was validated as the photoproduct by co-injection
and further established by isolation and characterization by H
1
The photophysical properties of our newly synthesized H
2
S
NMR spectroscopy (Fig. S8†). In addition, the time-dependent
donor were investigated. The UV spectrum indicated that the decomposition of the TPE-pHP-H
2
S NP donor was found with
4
−1
TPE-pHP-H S donor has an absorption band at 372 nm a first-order rate constant of 2.76 × 10 s (Fig. 4b).
2
(
Fig. 3b). Emission studies were also carried out to understand
the ESIPT behavior of the TPE-pHP-H
S donor. In non-hydro- TPE-pHP-H
gen bonding solvents (chloroform, benzene), only one emis- potassium ferrioxalate as an actinometer. The stability of the
sion band at λmax = 549 nm (keto form) of the TPE-pHP-H
TPE-pHP-H S NP donor was also confirmed under dark con-
donor was noted (Fig. 3a). In non-hydrogen bonding solvents, ditions in CH CN/PBS containing 10% fetal bovine serum
there is an ultrafast proton transfer occurring from the (pH = 7.4) and different pH solutions (pH = 6 and 8) for one
hydroxyl group of the pHP group to the nitrogen atom of the week ∼32 °C. It is clearly shown that the TPE-pHP-H S NP
TPE moiety (ESIPT). In addition, in polar aprotic solvents donor is relatively stable in biological media and in various pH
THF, ACN) and polar protic solvents (MeOH, EtOH), we found solutions in the dark.
two emission bands at λmax = 460 nm (enol form) and λmax
To analyze H S release from the TPE-pHP-H
49 nm (keto form) (Fig. 3c). The new emission at 460 nm we utilized the standard methylene blue assay. In this
enol form) is due to the existence of a hydrogen bond study, a 100 μM solution of TPE-pHP-H S NP donor in pH
between the solvent and the hydroxyl group of the TPE- 7.4 ACN/PBS buffer (0.1 : 9.9) was prepared. Upon
pHP-H
S donor which restricts the ESIPT process. In addition, irradiation of the TPE-pHP-H S NP donor, we noted an
emission spectra of TPE-pHP-H S NPs at different concen- increase in absorption maximum at 663 nm with increasing
Furthermore, the photochemical quantum yield (Φp) of the
S NP donor was determined as 0.18 ± 0.05 with
2
2
2
S
2
3
2
(
=
2
2
S NP donor,
5
(
2
2
2
2
irradiation time, validating the ability of the TPE-pHP-H
NP donor to release H S (Fig. 5a). In addition, we carried
out a time-dependent H S generation study; it was observed
2
S
2
2
that the H
tion with a rate constant of 1.22 × 10
trations of H S extended a maximum of ∼40 μM in about
2
S generation followed a pseudo-first-order reac-
7
−1
s
. The concen-
2
2
0 min and dropped afterward, probably due to volatiliz-
ation of H S gas (Fig. 5b).
In addition, to demonstrate the H S release only in the
2
2
2
presence of light, we observed the release of H S by intermit-
tently switching the visible light source on and off. Fig. 6
shows that on every occasion the light source was switched off,
H
2
S release stopped; this evidently specifies that only external
stimulus light induces H S release.
With reference to the literature
2
3
7,38
and our previous
we proposed a mechanism for the photochemical
release of H S from the TPE-pHP-H S NP donor in aqueous
acetonitrile solution as shown in Scheme 2.
2
8,39
work,
Fig. 3 (a) Keto and enol form of the TPE-pHP-H
2
S NP donor, (b) UV-Vis
S NP
absorption spectra and (c) emission spectra of the TPE-pHP-H
2
2
2
−4
donor (1 × 10 M) in various solvents (Ex = 350 nm).
This journal is © The Royal Society of Chemistry 2018
Org. Biomol. Chem., 2018, 16, 7903–7909 | 7905

View Article Online
Paper
Organic & Biomolecular Chemistry
Fig. 4 (a) HPLC profiles of the TPE-pHP-H
2
S NP donor at fixed time intervals (0–20 min) of irradiation using visible light (≥410 nm) and (b) time
2
course of disappearance of the TPE-pHP-H S NP donor was resolved by HPLC analysis.
Fig. 5 (a) Spectra of methylene blue assay. Red line: Na
various times and (b) time-dependent H S release of the TPE-pHP-H
be pseudo-first-order (rate constant of 1.22 × 10 s ).
2 2 2
S (50 μM). Other lines: H S release from the TPE-pHP-H S NP donor upon irradiation at
2
2
S NP donor was resolved by methylene blue assay and curve fitting found to
7
−1
from the pHP group to the tetraphenyl moiety (9), which
results in the deprotonation of the pHP group to yield inter-
mediate 10. The zwitterionic intermediate 10 then undergoes
intersystem crossing (ISC) to its triplet excited state, from the
triplet state it undergoes photo-Favorskii rearrangement to
give an assumed spirodiketone 11 with the simultaneous
release of the H S. The spirodiketone is then subject to hydro-
2
lytic ring opening to yield the photoproduct (13). Moreover, at
various pH values the release rate (Table S1†) supported the
ESIPT assistance in the photorelease.
To support the unlocking of photorelease of H S by our
2
donor in the aggregated state, the photolysis of the TPE-
pHP-H S NP donor was carried out under visible light
2
Fig. 6 Progress of the release of H
in bright and dark environments (ON indicates the start of visible light
irradiation and OFF indicates the end of visible light irradiation).
2
S from the TPE-pHP-H
2
S NP donor
(
≥410 nm) in various ACN–H
S release was calculated against different water fractions of
ACN (Fig. S10†). The photochemical quantum yield progress-
ively increased with increasing f and it was obtained to be the
highest at f = 99 vol% (Table S2†). No considerable H
At first the aggregation between the molecules (TPE- release was recorded below f = 80 vol% and in pure ACN. This
2
O solvent systems. The ratio of
H
2
w
w
2
S
w
pHP-H
Upon irradiation, the TPE-pHP-H
its singlet state (S1), then it undergoes a rapid ESIPT process rescence colour change from yellow to green on photoirradia-
2
S) leads to an inhibition of the intramolecular rotation. proposes that aggregation initiates the H
2
S release process.
2
S NP donor gets excited to Our newly designed H S donor displays a noticeable fluo-
2
7906 | Org. Biomol. Chem., 2018, 16, 7903–7909
This journal is © The Royal Society of Chemistry 2018

View Article Online
Organic & Biomolecular Chemistry
Paper
2
Scheme 2 Proposed AIE + ESIPT induced H S-releasing mechanism.
tion. At 0 min, the excitation of the TPE-pHP-H S NP donor demonstrate the real time monitoring capability of the TPE-
2
1 × 10− M, 0.1 : 9.9 ACN/PBS buffer at pH 7.4) at λmax = 372 nm pHP-H
4
S NP donor, confocal microscopy images were obtained
(
2
produced only a yellow-emission band at λmax = 549 nm. The at 0, 10 and 20 min of irradiation by visible light respectively.
steady increase in the irradiation time (0–20 min) results in a Initially, the cell shows a yellow fluorescence due to aggrega-
continuing decrease in the emission intensity at λmax
49 nm, with a simultaneous increase in the new emission irradiation for 10 min, we observed a light green fluorescence
band at λmax = 486 nm (Fig. 7). The blue shift of the emission (Fig. 8c); it shows decomposition of the TPE-pHP-H S NPs
=
tion and cellular uptake of 8 (Fig. 8b) and after visible light
5
2
2
suggests the formation of the photoproduct (the blue shift is donor and H S release. After irradiation for 20 min, we
attributed to the disruption of conjugation from the phenolic observed a complete fluorescence colour change from yellow
hydroxyl group to the carbonyl group). The release of H S from to green (Fig. 8d), it clearly shows complete photolysis of the
2
2 2 2
the TPE-pHP-H S NP donor was confirmed by fluorescence TPE-pHP-H S NP donor to release H S. Moreover, for the detec-
quenching of coumarin–hemicyanine dye (Scheme S2 and tion of the intracellular H S level we have used coumarin–
2
Fig. S11†).
To investigate the cellular uptake and real-time monitoring
hemicyanine fluorescence dye (Fig. S14†).
2
We carried out the cytotoxicity test of the TPE-pHP-H S NP
of H S release from the TPE-pHP-H S NP donor within cells, donor by using MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl-
2
2
cervical cancer cells HeLa were incubated with the TPE- tetrazolium bromide) assay on HeLa cells before and after
pHP-H S NP donor for 8 h. After incubation, a bright yellow photolysis (Fig. 9a and b). HeLa cells were incubated with
2
fluorescence (Fig. 8) was produced inside the cells showing various concentrations of TPE-pHP-H S NP donor (1, 5, 10, 15,
2
good cellular internalization. The co-localization experiments 20 µm) for 6 h, and then exposed to photolysis with visible
−
1
2
(Fig. S12 and S13†) suggest that the TPE-pHP-H S NP donor light for 20 min. MTT was added to the cells at 0.4 mg ml
went selectively into the lysosomes of the HeLa cells. To after 72 h of incubation. From the results, we observed that
Fig. 7 (a) Fluorescence response of the TPE-pHP-H
2
S NP donor with incremental addition of water (0–99%) and (b) fluorescent spectral change of
the TPE-pHP-H S NP donor during photolysis at regular intervals of time (0–20 min).
2
This journal is © The Royal Society of Chemistry 2018
Org. Biomol. Chem., 2018, 16, 7903–7909 | 7907

View Article Online
Paper
Organic & Biomolecular Chemistry
ability was found to be unlocked only in its aggregated state.
Upon visible light irradiation, the TPE-pHP-H S NP donor gets
2
excited to its singlet state and then undergoes the ESIPT
process to release H S. We also demonstrated that our H S
2 2
donor released H S in a spatio-temporal controlled manner.
2
Furthermore, we demonstrated the real-time monitoring capa-
bility of our H
of a change in fluorescence from yellow to green. Thus, our
synthesized TPE-pHP-H S NP donor accomplished the con-
trolled release of H S under the visible light without the help
2
S donor at the cellular level with the assistance
2
2
of any external agent. In the future, we will focus on develop-
ing a near infra-red (NIR) activatable gasotransmitter donor
for the release of two different gasotransmitters with a real
time monitoring ability.
Conflicts of interest
There are no conflicts to declare.
Fig. 8 Confocal microscopy images of internalization of the TPE-
Acknowledgements
2
pHP-H S NP donor in HeLa cells: (a) bright-field image, (b) 0 min,
(
c) 10 min and (d) 20 min. Scale bar = 50 µm.
We thank DST-SERB (Grant No. EMR/2016/005885) for
financial support. DST-FIST for 600 and 400 MHz NMR.
C. Parthiban thanks the Science & Engineering Research Board
(
SERB), New Delhi for N-PDF.
References
1
Z. Xiao, T. Bonnard, A. Shakouri-Motlagh, R. A. L. Wylie,
J. Collins, J. White, D. E. Heath, C. E. Hagemeyer and
L. A. Connal, Chem. – Eur. J., 2017, 23, 11294.
2
3
4
Y. Zhao, H. Wang and M. Xian, J. Am. Chem. Soc., 2011,
1
33, 15.
T. Liu, Z. Xu, D. R. Spring and J. Cui, Org. Lett., 2013, 15,
310.
2
Y. Wang, G. Zhang, M. Gao, Y. Cai, C. Zhan, Z. Zhao,
D. Zhang and B. Z. Tang, Faraday Discuss., 2017, 196,
9.
Fig. 9 Cell viability assay of the TPE-pHP-H
cell line: (a) before and (b) after photolysis for 20 min. Values are
2
S NP donor in the HeLa
depicted as mean
experiments.
± standard deviation from three independent
5
6
J. Liang, B. Z. Tang and B. Liu, Chem. Soc. Rev., 2015, 44,
2798.
C. Zhan, X. You, G. Zhang and D. Zhang, Chem. Rec., 2016,
16, 2142.
there is no confirmation of the inhibition of proliferation of
HeLa cells by the TPE-pHP-H S NP donor before and after
2
photolysis, this clearly shows that the H S donor TPE-pHP-H S
2
7 J. L. Wallace and R. Wang, Nat. Rev. Drug Discovery, 2015,
14, 329.
2
NPs are not cytotoxic at the studied concentration.
8 D. J. Polhemus and D. J. Lefer, Circ. Res., 2014, 114,
7
30.
B. L. Predmore and D. J. Lefer, Expert Rev. Clin. Pharmacol.,
011, 4, 83.
9
2
Conclusion
1
0 D. J. Polhemus, Z. Li, C. B. Pattillo, G. Gojon, T. Giordano
In conclusion, we have demonstrated photoresponsive single
and H. Krum, Cardiovasc. Ther., 2015, 33, 216.
component fluorescent organic nanoparticles for H S release, 11 S. Mani, A. Untereiner, L. Wu and R. Wang, Antioxid. Redox
2
utilizing the combined benefits of AIE and ESIPT phenomena
with a real time monitoring ability. Our TPE-pHP-H S NP 12 J. Beltowski, G. Wojcika and A. J. Wisniewska, Biochem.
donor exhibited yellow fluorescence and the photorelease Pharmacol., 2018, 149, 60.
Signaling, 2014, 20, 805.
2
7908 | Org. Biomol. Chem., 2018, 16, 7903–7909
This journal is © The Royal Society of Chemistry 2018

View Article Online
Organic & Biomolecular Chemistry
Paper
1
1
1
1
3 B. D. paul and S. H. Snyder, Biochem. Pharmacol., 2018, 27 A. K. Sharma, M. Nair, P. Chauhan, K. Gupta, D. K. Saini
49, 101. and H. Chakrapani, Org. Lett., 2017, 19, 4822.
4 W. Zhang, N. Wang, Y. Yu, Y. M. Shan, B. Wang, X. M. Pu 28 Y. Venkatesh, J. Das, A. Chaudhuri, A. Karmakar,
1
and X. Q. Yu, Chem. – Eur. J., 2018, 24, 4871.
T. K. Maiti and N. D. Pradeep Singh, Chem. Commun., 2018,
54, 3106.
5 R. O. Beauchamp, J. S. Bus, J. A. Popp, C. J. Boreiko and
D. A. Andjelkovich, Crit. Rev. Toxicol., 1984, 13, 25.
6 J. Kang, Z. Li, C. L. Organ, C. M. Park, C. T. Yang,
29 Y. Wang, G. Zhang, M. Gao, Y. Cai, C. Zhan, Z. Zhao,
D. Zhang and B. Z. Tang, Faraday Discuss., 2017, 196, 9.
A. Pacheco, D. Wang, D. J. Lefer and M. Xian, J. Am. Chem. 30 J. Liang, B. Z. Tang and B. Liu, Chem. Soc. Rev., 2015, 44,
Soc., 2016, 138, 6336. 2798.
7 D. Liang, H. Wu, M. W. Wong and D. Huang, Org. Lett., 31 C. Zhan, X. You, G. Zhang and D. Zhang, Chem. Rec., 2016,
015, 17, 4196. 16, 2142.
8 Y. Zheng, B. Yu, K. Ji, Z. Pan, V. Chittavong and B. Wang, 32 W. Zhang, N. Wang, Y. Yu, Y. M. Shan, B. Wang, X. M. Pu
1
1
2
Angew. Chem., Int. Ed., 2016, 55, 4514.
9 A. Stein and S. M. Bailey, Redox Biol., 2013, 1, 32.
0 Y. Zhao, T. D. Biggs and M. Xian, Chem. Commun., 2014,
and X. Q. Yu, Chem. – Eur. J., 2018, 24, 4871.
33 H. Zhang, H. Li, J. Wang, J. Sun, A. Qin and B. Z. Tang,
J. Mater. Chem. C, 2015, 3, 5162.
1
2
5
0, 11788.
1 P. Stacko, L. Muchova, L. Vitek and P. Klan, Org. Lett., 2018,
0, 4907.
34 H. T. Feng, S. Song, Y. C. Chen, C. H. Shen and Y. S. Zheng,
J. Mater. Chem. C, 2014, 2, 2353.
35 Z. Zhao, J. W. Y. Lam and B. Z. Tang, J. Mater. Chem., 2012,
22, 23726.
36 X. Liu, J. Jiao, X. Jiang, J. Li, Y. Cheng and C. Zhu, J. Mater.
Chem. C, 2013, 1, 4713.
2
2
2
2
2
2
2
2 M. Popova, T. Soboleva, S. Ayad, A. D. Benning and
L. M. Berreau, J. Am. Chem. Soc., 2018, 140, 9721.
3 R. Sakla and A. Jose, ACS Appl. Mater. Interfaces, 2018, 10,
1
4214.
37 X. Luo, J. Wu, T. Lv, Y. Lai, H. Zhang, J. Jian Lu, Y. Zhang
and Z. Huang, Org. Chem. Front., 2017, 4, 2445.
38 P. Klan, T. Solomek, C. G. Bochet, A. Blanc, R. Givens,
M. Rubina, V. Popik, A. Kostikov and J. Wirz, Chem. Rev.,
2013, 113, 119.
4 N. O. Devarie-Baez, P. E. Bagdon, B. Peng, Y. Zhao,
C. M. Park and M. Xian, Org. Lett., 2013, 15, 2786.
5 Y. Zhao, S. G. Bolton and M. D. Pluth, Org. Lett., 2017, 19,
2
278.
6 Z. Xiao, T. Bonnard, A. Shakouri-Motlagh, R. A. L. Wylie, 39 S. Barman, S. K. Mukhopadhyay, S. Biswas, S. Nandi,
J. Collins, J. White, D. E. Heath, C. E. Hagemeyer and
M. Gangopadhyay, S. Dey, A. Anoop and N. D. P. Singh,
L. A. Connal, Chem. – Eur. J., 2017, 23, 11294.
Angew. Chem., Int. Ed., 2016, 128, 4266.
This journal is © The Royal Society of Chemistry 2018
Org. Biomol. Chem., 2018, 16, 7903–7909 | 7909