H2S-Activable MOF Nanoparticle Photosensitizer for Effective Photodynamic Therapy against Cancer with Controllable Singlet-Oxygen Release

Article abstract of DOI:10.1002/anie.201708005

Photodynamic therapy (PDT) has emerged as an important minimally invasive tumor treatment technology. The search for an effective photosensitizer to realize selective cancer treatment has become one of the major foci in recent developments of PDT technolo

Full text of DOI:10.1002/anie.201708005

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Accepted Article
Title: H₂S-activable MOF Nanoparticle Photosensitizer for Effective
Photodynamic Therapy against Cancer with Controllable Singlet-
oxygen Release
Authors: Yu Ma, Xiangyuan Li, Aijie Li, Peng Yang, Caiyun Zhang, and
Bo Tang
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.201708005
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H2S-activable MOF Nanoparticle Photosensitizer for Effective
Photodynamic Therapy against Cancer with Controllable Singlet-
oxygen Release
Yu Ma, Xiangyuan Li, Aijie Li, Peng Yang, Caiyun Zhang, and Bo Tang *
Abstract: Photodynamic therapy (PDT) has emerged as an
important minimally invasive tumor treatment technology. The
search for an effective photosensitizer to realize selective cancer
treatment has become one of the major focus in recent
developments of PDT technology. Controllable singlet-oxygen
release based on specific cancer-associated events, as another
major layer of selectivity mode, has attracted great attention in
recent years. Here, for the first time, we demonstrated that a novel
mixed-metal functionalized metal-organic framework nanoparticle
(MOF NP) photosensitizer can be activated by a hydrogen sulfide
(H2S) signaling molecule in a specific tumor microenvironment for
PDT against cancer with controllable singlet-oxygen release in living
cells. The effective removal of tumors in vivo further confirmed the
satisfactory treatment effect of the MOF NP photosensitizer.
constructed from metal ions/clusters and organic linkers (or
bridging ligands), have been extensively studied. Combining the
benefits of nanostructures and the intrinsic properties of bulk
crystalline MOFs，such as the controllable composition, high
porosity, large surface area, abundant in metal active sites,
potential
for
post-synthetic
modification
and
good
biocompatibility, these materials, acted as effective nanoparticle-
based delivery platforms, have shown great potential in
biomedical applications.6 Thus far, only a few examples of MOF
NP PSs with molecular PSs as bridging ligands or embedded in
the framework for PDT have been reported.7 Among these
systems, only one MOF NP platform investigated targeting by
folate post modification.7a However, spatiotemporal controllable
ROS release based on specific cancer-associated events, as
another major layer of selectivity mode, has not been achieved
in these novel MOF NP delivery systems.
Photodynamic therapy (PDT), as a new minimally invasive tumor
treatment technology, has attracted great attention for its
satisfactory clinical effects.1 Compared with conventional
therapeutics, such as surgery, chemotherapy and radiation
therapy, PDT treatment possesses several unique advantages
including noninvasiveness, negligible drug resistance, quick
curative effect, repeatable administration without cumulative
toxicity, no inhibition to the host immune system and low side
effects.1a,2 Specifically, PDT treatment involves three key
components: a photosensitizer (PS), a light source and reactive
oxygen species (ROS). Upon irradiation, the excited PS
transfers energy to the surrounding oxygen in the tissue to
generate ROS, which can be exploited to induce cell apoptosis
and necrosis.3 From the view point of the entire treatment
process, the PS is the key factor in determining the antitumor
efficacy. Porphyrin derivatives and its analogues are the main
clinically used PSs currently.4 However, due to their hydrophobic
nature, insufficient tumor localization, easy accumulation, limited
permeation and retention (EPR) effect and/or complex synthetic
modification, etc,5 the design and synthesis of simple and
effective delivery systems with precisely controlled composition
for porphyrinic molecules to the tumor sites has become an
important research subject.
Figure 1. Simple structural fragment of MOF NP-1 and the proposed strategy
for 1O2 generation in cancer therapy.
In the present work, for the first time, we demonstrated that a
novel mixed-metal functionalized MOF NP PS can be activated
by hydrogen sulfide (H2S) in a specific tumor microenvironment
for effective treatment of colon adenocarcinoma cancer,
according to the fact that the content of H2S is significantly high
in human colon adenocarcinoma cells8. As far as we known, this
controllable singlet-oxygen (1O2) release based on H2S-
activation has not been reported thus far. On account of another
fact that metalated derivatives of PSs can effectively modulate
photodynamic activity,9 we first employed zinc metalated
5,10,15,20-tetrakis(4-methoxycarbonylphenyl)porphyrin
(ZnTcpp) as a photosensitive bridging ligand to construct a novel
single-component MOF NP PS. Then, Cu2+ ions, an important
H2S-responding site in H2S fluorescence probes,10 were selected
as metal nodes of the network. As expected, the paramagnetic
Cu2+ ions not only completely quenched the ligand-based
fluorescence of the MOF NPs but also significantly minimized
the ROS production efficiency of the photosensitive ligand.
When H2S appeared, the Cu2+ ions were taken out from the
Metal-organic framework nanoparticles (MOF NPs), as a
new type of miniature crystalline porous MOF materials
[*]
Dr. Y. Ma,[+] X. Li,[+] A. Li, Dr. P. Yang, C. Zhang, Prof. B. Tang
College of Chemistry, Chemical Engineering and Materials Science
Collaborative Innovation Center of Functionalized Probes for
Chemical Imaging in Universities of Shandong, Key Laboratory of
Molecular and Nano Probes, Ministry of Education, Institute of
Molecular and Nano Science, Shandong Normal University
Jinan 250014, P. R. China
E-mail: tangb@sdnu.edu.cn
[+] These authors contributed equally.
Supporting information for this article is given via a link at the end of
the document.
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MOF nodes, and thus, the luminophor photosensitive ligand was
simultaneously obtained. In other words, this turn-on type single-
component fluorescence MOF NP PS should be able to achieve
effective cancer therapy with controllable photosensitive ligand
release. The details of this strategy have been illustrated in
Figure 1.
The new nanoscale copper-zinc mixed-metal organic-
framework {Cu2(ZnTcpp)H2O}n (NP-1) was prepared via a
hydrothermal microemulsion method. Based on the
consideration that Cu2+ ions are preferable to coordinate with
nitrogen atoms,11 Zn2+ metalation of the porphyrin ligand within
the N-containing heterocycle with ZnCl2 was first carried out.
Then, NP-1 was obtained by the reaction of the ligand ZnTcpp
and Cu(NO3)23H2O in reverse microemulsion system under
hydrothermal conditions (for details, see Supporting Information).
Our efforts to grow bulk single crystals suitable for X-ray
crystallographic measurement did not succeed. Fortunately, the
powder X-ray diffraction (PXRD) pattern for NP-1 is in good
agreement with that of a {Cu2(CuTcpp)·H2O}n MOF thin films12
(Figure S1). In addition, the Cu/Zn ratio from energy-dispersive
spectrum (EDS) illustrated that the porphyrin centers were
completely occupied by Zn2+ ions (Figure S2). These
measurements all reveal that NP-1 also exhibits two-
dimensional (2D) layer networks. In this structure, each
porphyrin linker, with the center site occupied by a Zn2+ ion is
coordinated to four different Cu2(COO)4 paddlewheel units
through the carboxylate groups and interconnects these
binuclear paddlewheel units into 2D infinite layers. All the
parallel layers are slipped with each other and further stacked
into a 3D supramolecular architecture through weak interactions
(e.g. hydrogen bonds and/or van der Waals interactions). This
stacking mode provides the maximum PS loading compared
with other MOF NPs photosensitizer so far (calcd 85.7%), which
is necessary to achieve highly effective PDT of cancers once the
Cu2+ switch is triggered.
Figure 2. (a) Adsorption spectra of NP-1 (black) and ZnTcpp (red); (b)
fluorescence spectra of NP-1 obtained upon titration with HS- from 0 to 70 μM,

ex = 420 nm; (c) fluorescence spectra of NP-1 in the low-concentration region;
(d) linear correlation between the fluorescence intensity and the corresponding
concentration of NaHS.
upon treatment of 10 μM NP-1 with 70 μM NaHS in aqueous
solution buffered at physiological pH,
a
considerable
fluorescence enhancement was observed. To evaluate the
response of the PS to the H2S level, varying concentrations of
NaHS were added to the solutions of NP-1 (10 μM) (Figure 2b
and 2c). An excellent linear correlation between the
fluorescence intensities and the added NaHS concentrations
was observed (Figure 2d). To further establish the possibility of
the efficient activation, we examined the response time of NP-1
to NaHS through reaction kinetics. As shown in Figure S6a, the
fluorescence intensity reached a maximum within 1 min. All
these experiments proved that NP-1 can be effectively activated
by H2S in vitro.
The typical uniform plate morphology of the as-synthesized
NP-1 was confirmed by transmission electron microscopy (TEM)
images. As shown in Figure S3, the MOF NP plates possess an
average diameter of 120 nm. Dynamic light scattering (DLS)
measurements provided an average size of 105 nm for the NPs
(Figure S4). This PS with suitable size showed fine aqueous
dispersibility and no need for toxic organic cosolvent (Figure S3).
After being immersed in the phosphate-buffered saline (PBS)
and in serum proteins for 14 d at room temperature and at 50 C,
respectively, the PXRD patterns were still in good agreement
with that of as-synthesized NP-1, indicating that NP-1 has
sufficient stability in aqueous medium under physiological
conditions (Figure S1).
The experiments on selectivity were then carried out. As
shown in Figure S6b, compared with the large and immediate
increment of the fluorescence intensity upon the addition of 100
μM NaHS, almost no fluorescence increment was observed
upon addition of abundant biologically relevant glutathione. We
also examined serum protein and other reactive individual
species shown in Figure S6b and S7. Similarly, these species
induced no or very limited fluorescence response. All these
results portended that NP-1 should be able to be selectively
activated by H2S in living cells.
The 1O2 generation ability of NP-1 under irradiation in the
absence and presence of H2S was then evaluated by a 1O2
probe disodium of 9,10-anthracenediyl-bis(methylene)dimalonic
acid (ABMD). The ABMD molecule can react with 1O2 to produce
endoperoxide, which would cause a decrease in the absorption
intensity of ABMD.13 And the decreased intensity of ABMD
Subsequently, we investigated the spectroscopic properties
of NP-1. The adsorption spectrum of NP-1 displayed a Soret
band at 442 nm and two Q bands at 560 nm and 600 nm (Figure
2a). The number of Q bands decreased compared to the
spectrum of H2Tcpp, which illustrates that the porphyrin centers
in NP-1 have been filled with Zn2+ ions (Figure 2a and Figure
S5). To clarify the role of H2S in activating this nanoPS, the
emission spectra were then recorded. As shown in Figure 2b,
1
absorption has a positive correlation with the quantity of O2. As
shown in Figure 3, the absorption intensity of ABMD quickly
decreased with an extended irradiation time from 0 to 6 min in
the presence of NaHS, while the variation of the absorption
intensity in the absence of NaHS was very limited, almost
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PS in practical applications, a colon tumor model that could be
treated with PDT in the clinic through an endoscope was
Figure 3. ABMD absorption spectra as a function of irradiation time of NP-1
before (a) and after (b) titrating with NaHS.
negligible. Therefore, we reasonably concluded that NP-1
allowed for H2S-controllable 1O2 generation.
To prove that the novel NP-1 could really be specifically
activated by H2S in living cells for cancer therapy, confocal
fluorescence microscopy studies were performed on Calcein-AM
and propidium (PI) stained HepG2 cells (Human hepatocellular
liver carcinoma cells). As shown in Figure 4a and 4c, before
being treated with NaHS, no ZnTcpp fluorescence was observed
but only the fluorescence from the Calcein-AM stained cells
were detected whether it is irradiated or not. These results
suggested that NP-1 in living cells cannot be activated in the
absence of H2S and no cells apoptosis occurred. As a control,
after being treated with NaHS but without irradiation, not only
strong green fluorescence for Calcein-AM but also strong red
fluorescence for ZnTcpp was observed (Figure 4b), indicating
that NP-1 was activated successfully by H2S but no apoptosis
occurred. The imaging results from Figure 4b, combined with an
approach based on inductively coupled plasma atomic emission
spectroscopy (ICP-AES)14 confirmed that NP-1 was indeed
taken in by the HepG2 cells (for details, see the Supporting
Information). However, after being treated with NaHS and
irradiation simultaneously, strong red fluorescence for ZnTcpp
was also observed. Compared with the control group, strong
yellow fluorescence for PI was observed for the first time, but the
green fluorescence for Calcein-AM disappeared, as shown in
Figure 4d. This costaining imaging not only well confirmed this
PS could really be specifically activated by H2S in living cells but
also confirmed the ability of H2S-activable NP-1 for effective
cancer therapy in living cells.
Figure 4. Confocal images of Calcein-AM and PI stained HepG2 cells with
different treatments: a) 10 μM NP-1 without irradiation; b) 10 μM NP-1 and 50
μM NaHS without irradiation; c) 10 μM NP-1 with irradiation; d) 10 μM NP-1
and 50 μM NaHS with irradiation. The irradiation power was 100 mW/cm2.
employed to estimate in vivo anticancer efficacy of NP-1.
According to the fact that the content of H2S is significantly high
in human colon adenocarcinoma cells (HCT116 cells),8 HCT116
subcutaneous xenograft nude mice were firstly prepared. After
the tumor volume reached 80-100 mm3, the mice were randomly
divided into five treatment groups (n ≥ 4, Figure 5). In the
experimental group, NP-1 dispersed in PBS buffer (1.0 mg/ml)
was directly injected into the tumor site of each mouse. Ten
hours after the injection, the tumor region was irradiated with a
600-nm Xenon lamp at 100 mW/cm2 for 30 min. As shown in
Figure 5b, the growth of the tumor was quickly suppressed over
the first two days. In contrast, the tumor growth of the control
groups was not effectively suppressed (Figure 5b and S11). To
further speed up the removal of the tumor and evaluate the
toxicity of higher treatment doses of NP-1, the mice were treated
again on the fourth day. As expected, the tumor almost
disappeared within two days upon this treatment. As shown in
Figure 5d, among the four tumors in the experimental group, one
tumor was completely eradicated, while the sizes of the other
originally larger tumors significantly decreased. Meanwhile, the
body weights of all mice were continuously monitored
throughout the entire treatment. As shown in Figure 5c, no
obvious changes of body weight were observed. This conclusion
is also in good agreement with the MTT assay on HTC116 cells
in the presence of NP-1 activated by intrinsic H2S without any
stimulant (Figure 5e). Imaging fluorescence activation in
HCT116 cells then further confirmed the PS could really be
activated specifically by H2S in this HCT116 subcutaneous
xenograft tumor (Figure S12). In addition, the treatment efficacy
To further examine the PDT efficacy of NP-1 and ZnTcpp
ligand, MTT assays were performed on the HepG2 cells. As
shown in Figure S8a, optimal PDT efficacy was observed in the
experimental groups treated with H2S activated NP-1, while
almost no cytotoxicity was observed in the dark control or blank
control groups. In comparison, the ZnTcpp-treated groups with
various concentrations of the ZnTcpp ligand (0-100 μM),
exhibited only moderate PDT efficacy (Figure S8b). In addition,
from these control groups (Figure S8-S10), we also concluded
that both NP-1 and ZnTcpp themselves have good
biocompatibility.
Motivated by the above results, in vivo antitumor efficacy of
NP-1 was then investigated. Considering the importance of the
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of NP-1 in terms of tumor cell death was also evaluated by H&E
staining on tissue sections from the different treatment groups.
The tumors treated with activated NP-1 upon irradiation
above. The damaged degree of tumor tissue, evaluated by H&E
staining (Figure S13 and S16), was also consistent with the
above results. All these results demonstrated that under the
same treatment conditions, the higher the H2S level in tumor
cells, the better the treatment effect of PDT will be obtained.
In summary, we have presented a novel MOF NP PS to
achieve selective PDT for cancers. Based on the
paramagnetism of the metal nodes, the MOF NPs can
successfully act as a H2S-activatable PS for controllable 1O2
release. To the best of our knowledge, spatiotemporal
controllable 1O2 release based on specific cancer-associated
events, as another major layer of selectivity mode, has not been
achieved in these novel MOF NP PSs. In addition, it has been
proved to be an extremely effective delivery platform with the
maximum loading capability compared with the other MOF NP
PS so far. Moreover, the effective removal of tumors in vivo
further confirmed the satisfactory treatment effect of NP-1. With
the facile modification and functionalization properties of MOFs,
we anticipate these MOF NPs allow a rational design for further
clinical translation. For example, this NP-1 synthesized in
reverse microemulsion system combined with a PEG-modified
long-circulating liposome platform, whose clinical application has
been well known, will achieve longer circulation in vivo, multi-
targeting and triggered release properties to cancer cells.
Overall, this work not only presented a novel PS for PDT but
also demonstrated the great potential of developing
multifunctional MOF NP PSs for selective therapy of cancers
with controllable ROS release based on other specific cancer-
associated events.
Figure 5. In vivo antitumor efficacy of NP-1 on HCT116 subcutaneous
xenograft nude mice. (a) Photographs of the mice with different treatments. (b)
Tumor growth inhibition curve after different treatments. (c) Mice body weight
curves with relevant treatments. (d) Photo of the tumors of four parallel
experimental groups after the PDT. (e) MTT assay of the HCT116 cells in the
presence of different concentrations of NP-1 activated by intrinsic H2S.
Acknowledgements
This work was supported by 973 Program (2013CB933800) and
National Natural Science Foundation of China (21390411,
21535004, 21675103, 21602126).
exhibited a wider range of tissue damage in tumor sections than
that for only monomeric ZnTcpp, while no histopathological
abnormalities were found in the tumor sections and normal
tissues for other control groups (Figure S12-S16). All these
results indicated that NP-1 could be effectively activated in
HCT116 tumor-bearing mice by the intrinsic H2S and provided a
significant therapeutic effect safely.
Keywords: metal organic frameworks • photodynamic therapy •
controllable release • singlet-oxygen • selectivity
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Entry for the Table of Contents (Please choose one layout)
COMMUNICATION
We demonstrated for the first time that
a novel mixed-metal functionalized
MOF NPs photosensitizer can be
activated by hydrogen sulfide (H2S)
signaling molecule in specific tumor
microenvironment for photodynamic
therapy against cancer with
Yu Ma, Xiangyuan Li, Aijie Li, Peng
Yang, Caiyun Zhang, and Bo Tang *
Page No. – Page No.
H2S-activable MOF Nanoparticle
Photosensitizer for Effective
Photodynamic Therapy against
Cancer with Controllable Singlet-
oxygen Release
controllable singlet-oxygen release.
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