Upconversion-like Photolysis of BODIPY-Based Prodrugs via a One-Photon Process

Article abstract of DOI:10.1021/jacs.9b09034

Photochemical reactions at lower energy than the absorption window are currently achieved by multi-photon processes, including two-photon absorption and photon upconversion, which have limited energy utilization efficiency. Here, we report a one-photon strategy based on triplet-triplet energy transfer (TTET) between a photosensitizer and a photocleavable molecule to achieve photolysis at low energy. To verify this concept, we chose platinum(II) tetraphenyltetrabenzoporphyrin (PtTPBP) as the photosensitizer and synthesized a boron-dipyrromethene (BODIPY)-based prodrug as the photocleavable molecule. Photolysis of the prodrug is achieved by TTET upon excitation of PtTPBP at 625 nm with a photolysis quantum yield of 2.8%. Another demonstration shows an unexpected higher photolysis quantum yield than the direct excitation at 530 nm. This strategy opens a new path for achieving photolysis at long wavelengths, benefiting the applications in biological studies, photopharmacology, and photoresponsive drug delivery.

Full text of DOI:10.1021/jacs.9b09034

Communication
Cite This: J. Am. Chem. Soc. XXXX, XXX, XXX−XXX
pubs.acs.org/JACS
Upconversion-like Photolysis of BODIPY-Based Prodrugs via a One-
Photon Process
†
†,‡
§
∥
†,‡
∥
§
Wen Lv, Yafei Li, Feiyang Li, Xin Lan, Yaming Zhang, Lili Du, Qiang Zhao,
∥
,†,‡
David L. Phillips, and Weiping Wang*
†Laboratory of Molecular Engineering and Nanomedicine, Dr. Li Dak-Sum Research Centre, The University of Hong
Kong-Karolinska Institutet Collaboration in Regenerative Medicine, The University of Hong Kong, Hong Kong, China
‡
Department of Pharmacology and Pharmacy, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong, China
§
Key Laboratory for Organic Electronics and Information Displays & Jiangsu Key Laboratory for Biosensors, Institute of Advanced
Materials, Nanjing University of Posts and Telecommunications, Nanjing 210023, China
∥
Department of Chemistry, The University of Hong Kong, Hong Kong, China
*
S Supporting Information
1
0,11
photocleavable groups.
photon excitation.
The second strategy is to use two-
Due to the small two-photon absorption
cross sections of current photocages, high-power femtosecond
1
3,14
ABSTRACT: Photochemical reactions at lower energy
than the absorption window are currently achieved by
multi-photon processes, including two-photon absorption
and photon upconversion, which have limited energy
utilization efficiency. Here, we report a one-photon
strategy based on triplet−triplet energy transfer (TTET)
between a photosensitizer and a photocleavable molecule
to achieve photolysis at low energy. To verify this concept,
we chose platinum(II) tetraphenyltetrabenzoporphyrin
15
pump lasers are required for two-photon excitation. The
third strategy is to excite photocages utilizing upconversion
luminescence systems, including lanthanide-doped upconver-
sion nanoparticles (UCNPs) and triplet−triplet annihilation-
based upconversion (TTA-UC).
16
17,18
However, the theoretical
upconversion quantum yield of these upconversion systems is
less than 0.5, since at minimum two photons are required to
1
5,19,20
(
PtTPBP) as the photosensitizer and synthesized a
produce one upconverted photon.
Internal energy
boron-dipyrromethene (BODIPY)-based prodrug as the
photocleavable molecule. Photolysis of the prodrug is
achieved by TTET upon excitation of PtTPBP at 625 nm
with a photolysis quantum yield of 2.8%. Another
demonstration shows an unexpected higher photolysis
quantum yield than the direct excitation at 530 nm. This
strategy opens a new path for achieving photolysis at long
wavelengths, benefiting the applications in biological
studies, photopharmacology, and photoresponsive drug
delivery.
consumption during multi-step energy-transfer processes
further decreases upconversion quantum yields, resulting in
low photolysis efficiencies. Therefore, a simple energy-transfer
strategy is highly desired for photolysis with long-wavelength
light excitation. Here, we present a one-photon upconversion-
like strategy, where light at lower energy than the onset of
absorption of the photocleavable group can achieve the high-
energy-demanding cleavage reaction based on a triplet−triplet
energy transfer (TTET) process.
Studies have found that photolysis can occur from the first
excited triplet state (T ) in addition to the first excited singlet
1
21,22
state (S1).
We hypothesize that a photocleavable molecule
hotochemistry plays an important role in designing
could be sensitized to the T state by a photosensitizer with a
1
P
controllable molecules, which offers promising optical
higher T energy level and a lower S energy level through
1
1
1
−4
tools for chemical, biological, and medical applications.
TTET process to achieve the photolysis reaction of interest.
The lower S energy level of the photosensitizer results in
longer absorption wavelengths than that of the photocleavable
molecule, allowing lower energy photons to be used for
excitation. The effect of which is like upconversion-based
photolysis, in that a low-energy photon is used to achieve a
higher-energy photolysis reaction. In the strategy, the T state
of the photocleavable molecule is populated by the photo-
sensitizer through TTET. Since photolysis can occur from the
Photolysis or photocleavage reactions can be used to release
desired functional molecules at appropriate times and locations
1
5
,6
with light excitation. The reactions normally occur following
excitation with light at the absorption wavelengths of the
photocleavable molecule. In biological and medical applica-
tions, substantial efforts have been focused on increasing the
excitation wavelength because long-wavelength light exhibits
deeper tissue penetration depths and lower photocytotox-
1
7
,8
T state of the photocleavable molecule, TTA is not necessary.
icity.
1
Therefore, a second photon is not required for the cleavage
One strategy is to develop long-wavelength light-excitable
(
Figure 1). This one-photon upconversion-like photolysis
photocleavable groups or photocages, including derivatives of
6
,9
10,11
offers a simpler energy-transfer process compared with the
coumarin, boron-dipyrromethene (BODIPY),
and Ru-
1
2
(
II) complexes. These compounds, however, usually require
multi-step organic syntheses and have relatively low photolysis
quantum yields compared to short-wavelength light-excitable
Received: August 21, 2019
©
XXXX American Chemical Society
A
DOI: 10.1021/jacs.9b09034
J. Am. Chem. Soc. XXXX, XXX, XXX−XXX

Journal of the American Chemical Society
Communication
designed and synthesized a photocleavable prodrug, BODI-
PY1-Cb, by modifying BODIPY1 with an anticancer drug
molecule, chlorambucil (Cb) (Supporting Information).
BODIPY1-Cb exhibited absorption and emission spectra
with peaks at 543 and 570 nm, respectively (Figure 2B and
Figure S2A). From its emission peak, the S energy level of
1
23
BODIPY1-Cb was calculated to be 2.18 eV. PtTPBP is a
24
common photosensitizer with S energy level of 1.8 eV.
1
Compared with BODIPY1-Cb, PtTPBP has a lower S energy
1
level and longer maximum absorption wavelength (613 nm,
Figure 2B), necessary in order to function as a low-energy
photosensitizer.
From the phosphorescence spectrum of PtTPBP (Figure
S2B), the T energy level of PtTPBP was calculated to be 1.61
1
23
eV. Since BODIPY1-Cb did not exhibit a clear phosphor-
escence peak, time-dependent density functional theory (TD-
Figure 1. Jablonski diagram of the one-photon upconversion-like
photolysis via a TTET process (red lines) and the photolysis by direct
excitation at the absorption wavelengths of photocleavable molecules
DFT) was used to calculate its T energy level, which was
1
determined to be 1.52 eV (Figure S3). The results show that
PtTPBP has a higher T energy level but a lower S energy
(
blue lines). Other possible relaxation pathways from excited states
1
1
are not shown in the diagram. S , ground singlet state; S , first excited
0
1
level than BODIPY1-Cb (Figure 2A), satisfying the energy
requirement for the one-photon upconversion-like photolysis.
The nanosecond transient absorption spectra of BODIPY1-Cb
exhibited a bleaching of the absorbance band at 546 nm
singlet state; T , first excited triplet state; ISC, intersystem crossing;
1
TTET, triplet−triplet energy transfer. The S energy levels of the
0
photosensitizer and photocleavable molecule are set at the same level.
(
Figure 2C) with a lifetime of 21.82 ± 10.11 μs (Table S1).
traditional TTA-UC-based photolysis (Figure S1), which
means less internal energy consumption and more efficient
energy utilization.
The T lifetime of PtTPBP (42.92 ± 0.80 μs) was determined
from the phosphorescence lifetime at 770 nm. The long T1
lifetime of both BODIPY1-Cb and PtTPBP supports an
1
Based on the energetic requirements described above, a
3
3
efficient TTET process from PtTPBP* to BODIPY1-Cb*.
photosensitizer should have a higher T energy level but a
1
The TTET rate constant (kTTET) was calculated to be (6.17 ±
lower S energy level than the photocleavable molecule to
1
9
−1 −1
1
.84) × 10 M
s
(Figure 2D), which is comparable to
25,26
achieve the photolysis. Therefore, we chose meso-methyl
position-substituted BODIPY (BODIPY1) and platinum(II)
tetraphenyltetrabenzoporphyrin (PtTPBP) as the photocage
and photosensitizer, respectively (Figure 2A). We further
9
−1 −1
literature kTTET values (approximately 10 M s ).
To demonstrate whether cleavage relaxation occurs from the
1
30 nm LED (Figure 3A). The irradiation within the
T state of BODIPY1-Cb, we irradiated BODIPY1-Cb with a
5
absorption window of BODIPY1-Cb can directly promote
the molecule to the S state. The heavy atoms in BODIPY1-Cb
1
can enhance intersystem crossing (ISC) and facilitate
conversion from the S state to the T state. In air-saturated
1
1
solutions, the decomposition of BODIPY1-Cb and generation
of free Cb were mainly due to the cleavage relaxation from the
S state, since the T state of BODIPY1-Cb could be quenched
1
1
by oxygen molecules. In N -saturated solutions, a much higher
2
cleavage efficiency was observed (Figure 3B and Table S2),
which indicates that BODIPY1-Cb can be cleaved from its T1
state. Almost all BODIPY1-Cb was decomposed after 10 s of
2
the irradiation at 44 mW/cm , which released 48.31 ± 1.05%
of free Cb with generation of byproducts as photolysis of other
11
BODIPY-modified molecules did.
Photolysis of BODIPY1-Cb by photosensitization with
PtTPBP was assessed by irradiating a N -saturated solution
2
containing the two molecules with a 625 nm LED and
analyzing the reaction mixture with high-performance liquid
chromatography (HPLC) (Figure S4). A new peak located at
∼11.2 min was observed along with the disappearance of the
BODIPY1-Cb signal at ∼29.0 min. The new peak showed the
same elution time as that of free Cb and as the peak from the
BODIPY1-Cb solution treated with 530 nm light. The
generation of Cb was further confirmed by the mass
spectrometric analysis of the reaction mixture (Figures S5−
S7). In contrast, irradiation of BODIPY1-Cb alone with 625
nm light did not cleave BODIPY1-Cb to release Cb. These
results demonstrate that the photolysis of BODIPY1-Cb can be
achieved by irradiation of PtTPBP with 625 nm red light,
Figure 2. (A) S and T energy levels and chemical structures of the
1
1
photosensitizer (PtTPBP) and the photocleavable molecule (BOD-
IPY1-Cb). (B) Absorption spectra of BODIPY1-Cb and PtTPBP in
−
5
dichloromethane (c = 10 M). (C) Nanosecond transient absorption
spectra of BODIPY1-Cb (10− M) in N -saturated toluene. λ = 355
5
2
ex
nm. (D) Stern−Volmer plot of phosphorescence intensity quenching
−
5
of PtTPBP (10 M) by BODIPY1-Cb through a TTET process in a
N -saturated methanol solution containing 5% toluene and 10%
2
dichloromethane (n = 3). kq is the phosphorescence intensity
quenching constant of PtTPBP during the TTET process, kTTET is
the rate constant of the TTET process.
B
DOI: 10.1021/jacs.9b09034
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Journal of the American Chemical Society
Communication
under both N - and air-saturated conditions. This conclusion is
2
supported by the negligible difference in photolysis efficiencies
under the both conditions (Figure 3E and Table S2). The T1
energy level of BODIPY2-Cb was calculated to be 1.42 eV
(
Figure S11), which is lower than that of PtTPBP (1.61 eV),
3
enabling energy transfer to occur from PtTPBP* to
3
BODIP2-Cb*. As shown in Figure 3F, irradiation at 625 nm
also cleaved BODIPY2-Cb in the presence of PtTPBP. The
photolysis efficiency of BODIPY2-Cb was lower under the air-
saturated conditions than under the N -saturated conditions,
2
which is due to the decreased T lifetime of both PtTPBP and
1
BODIPY2-Cb by oxygen molecules. The results demonstrate
that the one-photon upconversion-like photolysis strategy can
be applied to photocleavable molecules with a short T lifetime
1
and low photoreaction efficiency.
An unexpected result was obtained when we analyzed the
photolysis quantum yield of BODIPY2-Cb. The photolysis
quantum yield upon sensitization by PtTPBP at 625 nm was 5-
fold greater than that upon direct 530 nm light irradiation
without photosensitization (Table S2). This means that our
one-photon upconversion-like strategy can achieve photolysis
of BODIPY2-Cb with a longer excitation wavelength as well as
higher photolysis quantum yield than direct photolysis from
excitation at its absorption wavelength. The result is
unexpected, because one-photon upconversion-like excitation
has more energy transfer processes than direct excitation and is
supposed to have a lower photolysis quantum yield. This
experimental observation has not been previously reported in
upconversion-based photolysis, which usually has a much
lower photolysis quantum yield than direct photolysis due to
the extra photon upconversion process and energy transfer
from upconversion systems to photocleavable molecules
(Figure S1). The result is presumably attributable to the
Figure 3. (A) Photolysis reaction of BODIPY1-Cb. Photolysis rate of
BODIPY1-Cb (B−D) and BODIPY2-Cb (E, F) after irradiation with
5
30 nm light (B, E) or 625 nm light (C, D, and F) for different time
2
periods. All irradiations were done with an LED at 44 mW/cm . n = 3.
which has deeper tissue penetration depths than the green light
7
,8
at 530 nm.
To evaluate the influence of photosensitizer concentration
on the TTET-based photolysis, different molar equivalents of
PtTPBP were used in the photolysis assay of BODIPY1-Cb
facts that the cleavage relaxation from the T
efficient than that from the S state for BODIPY2-Cb and the
state is more
1
upon 625 nm light irradiation in N -saturated solutions. As
1
2
expected, the release of Cb by the cleavage of BODIPY1-Cb
was accelerated with increasing molar equivalents of PtTPBP
TTET process is more efficient than ISC in terms of
3
populating BODIPY2-Cb*. This study provides new insight
(
Figure 3C,D), which is attributed to the accelerated TTET
into decreasing excitation energy while increasing photolysis
efficiency for some photocleavable molecules.
In summary, we have demonstrated that photocleavable
process with increased molar ratios of PtTPBP to BODIPY1-
Cb. In the presence of 0.1 equiv of PtTPBP, 30 s of the
irradiation at 44 mW/cm2 decomposed almost all the
BODIPY1-Cb and released 41.74 ± 4.46% of free Cb, which
is close to the percentage of released Cb by direct irradiation of
BODIPY1-Cb with 530 nm light. The corresponding
molecules can undergo photolysis by populating the T
with longer-wavelength-absorbing photosensitizers. The proc-
ess requires that the photosensitizers have higher T energy
levels but lower S energy levels than the photocleavable
state
1
1
1
photolysis quantum yield Φ was calculated to be ∼2.8%
molecules. The one-photon upconversion-like photolysis
strategy could be applied to other pairs of photosensitizers
and photocleavable molecules that fulfill the energy matching.
Finding suitable pairs, especially for photosensitizers with
absorption in the near-infrared range, is a challenging but
worthwhile exploration. Compared to TTA-UC-based photol-
ysis, the one-photon upconversion-like photolysis requires a
simpler energy-transfer process, which is attractive for practical
applications. Furthermore, our method can increase both the
excitation wavelength and the photolysis efficiency of photo-
cleavable molecules. Like the application of TTA-UC-based
photolysis, the photosensitizers and BODIPY-based prodrugs
could be encapsulated within the hydrophobic core of
polymeric nanoparticles in aqueous solutions, which achieves
photorelease of drugs in biological systems. Therefore, this
TTET-based one-photon upconversion-like photolysis offers a
new platform for improving the performance of photo-
activation systems for applications in biological studies,
photoactivated chemotherapy, and targeted drug delivery.
BC
27,28
using Reinecke’s salt actinometry (Table S2).
The TTET-
based photolysis was also investigated in air-saturated
solutions, which showed approximately 68 times decrease in
photolysis quantum yield (Figure 3C,D and Table S2) due to
3
3
the quenching of both PtTPBP* and BODIPY1-Cb* by
29
oxygen molecules.
We further tested our hypothesis using another photo-
cleavable molecule with a shorter T1 lifetime and lower
photoreaction efficiency. We designed the molecule BODI-
PY2-Cb, whose chemical structure is similar to that of
BODIPY1-Cb but without iodine modification and with
fluorine substitution of methyl groups (Scheme S1).
BODIPY2-Cb exhibited similar absorption and emission
spectra with BODIPY1-Cb (Figures S8 and S9), but with a
shorter T lifetime (1.91 ± 0.01 μs) (Table S1 and Figure
1
S10). The lack of iodine atoms in BODIPY2-Cb led to
3
0
inefficient ISC. Therefore, photolysis of BODIPY2-Cb upon
direct irradiation at 530 nm mainly occurs from the S state
1
C
DOI: 10.1021/jacs.9b09034
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Journal of the American Chemical Society
Communication
photons of visible/near-infrared light. J. Am. Chem. Soc. 2018, 140,
ASSOCIATED CONTENT
Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/jacs.9b09034.
■
7
(
343−7346.
11) Slanina, T.; Shrestha, P.; Palao, E.; Kand, D.; Peterson, J. A.;
Dutton, A. S.; Rubinstein, N.; Weinstain, R.; Winter, A. H.; Klan, P. In
*
S
́
search of the perfect photocage: structure−reactivity relationships in
meso-methyl BODIPY photoremovable protecting groups. J. Am.
Chem. Soc. 2017, 139, 15168−15175.
General experimental considerations, detailed proce-
dures, and additional supporting data, including Figures
S1−S22, Tables S1 and S2, and Scheme S1 (PDF)
(12) Arora, K.; Herroon, M.; Al-Afyouni, M. H.; Toupin, N. P.;
Rohrabaugh, T. N., Jr; Loftus, L. M.; Podgorski, I.; Turro, C.;
Kodanko, J. J. Catch and release photosensitizers: combining dual-
action ruthenium complexes with protease inactivation for targeting
invasive cancers. J. Am. Chem. Soc. 2018, 140, 14367−14380.
AUTHOR INFORMATION
Corresponding Author
wangwp@hku.hk
ORCID
Qiang Zhao: 0000-0002-3788-4757
Weiping Wang: 0000-0001-7511-3497
Notes
The authors declare the following competing financial
interest(s): A PCT application was filed with No. PCT/
CN2019/101689.
■
*
(13) Matsuzaki, M.; Hayama, T.; Kasai, H.; Ellis-Davies, R. G. C.
Two-photon uncaging of γ-aminobutyric acid in intact brain tissue.
Nat. Chem. Biol. 2010, 6, 255−257.
(14) Li, M.; Wong, N.; Xiao, J.; Zhu, R.; Wu, L.; Dai, S.; Chen, F.;
Huang, G.; Xu, L.; Bai, X.; Geraskina, M. R.; Winter, A. H.; Chen, X.;
Liu, Y.; Fang, W.; Yang, D.; Phillips, D. L. Dynamics of oxygen-
independent photocleavage of blebbistatin as a one-photon blue or
two-photon near-infrared light-gated hydroxyl radical photocage. J.
Am. Chem. Soc. 2018, 140, 15957−15968.
(15) Zhou, J.; Liu, Q.; Feng, W.; Sun, Y.; Li, F. Upconversion
luminescent materials: advances and applications. Chem. Rev. 2015,
115, 395−465.
ACKNOWLEDGMENTS
This work was supported by Dr. Li Dak-Sum Research Fund
Start-up Fund) of The University of Hong Kong, Seed Fund
for Basic Research of The University of Hong Kong (No.
01711159053), Guangdong-Hong Kong Technology Coop-
eration Funding Scheme (No. 2017A050506016), and Young
Scientists Fund of the National Natural Science Foundation of
China (No. 81803469). The computations were performed
using research computing facilities provided by Information
Technology Services, The University of Hong Kong.
■
(16) Zhao, L.; Peng, J.; Huang, Q.; Li, C.; Chen, M.; Sun, Y.; Lin,
Q.; Zhu, L.; Li, F. Near-infrared photoregulated drug release in living
tumor tissue via yolk-shell upconversion nanocages. Adv. Funct. Mater.
(
2
(
014, 24, 363−371.
2
17) Wang, W.; Liu, Q.; Zhan, C.; Barhoumi, A.; Yang, T.; Wylie, R.
G.; Armstrong, P. A.; Kohane, D. S. Efficient triplet−triplet
annihilation-based upconversion for nanoparticle phototargeting.
Nano Lett. 2015, 15, 6332−6338.
(18) Huang, L.; Zhao, Y.; Zhang, H.; Huang, K.; Yang, J.; Han, G.
Expanding anti-stokes shifting in triplet−triplet annihilation upcon-
version for in vivo anticancer prodrug activation. Angew. Chem., Int.
Ed. 2017, 56, 14400−14404.
REFERENCES
■
(19) Wu, M.; Congreve, D. N.; Wilson, M. W. B.; Jean, J.; Geva, N.;
(
1) Xie, C.; Sun, W.; Lu, H.; Kretzschmann, A.; Liu, J.; Wagner, M.;
Butt, H.; Deng, X.; Wu, S. Reconfiguring surface functions using
visible-light controlled metal-ligand coordination. Nat. Commun.
018, 9, 3842.
2) Lemke, E. A.; Summerer, D.; Geierstanger, B. H.; Brittain, S. M.;
Schultz, P. G. Control of protein phosphorylation with a genetically
encoded photocaged amino acid. Nat. Chem. Biol. 2007, 3, 769−772.
3) Hansen, M. J.; Hille, J. I. C.; Szymanski, W.; Driessen, A. J. M.;
Welborn, M.; Van Voorhis, T.; Bulovic, V.; Bawendi, M. G.; Baldo, M.
A. Solid-state infrared-to-visible upconversion sensitized by colloidal
nanocrystals. Nat. Photonics 2016, 10, 31−34.
2
(
(
20) Liu, Q.; Zhang, Y.; Peng, C.; Yang, T.; Joubert, L. M.; Chu, S.
−
2
Single upconversion nanoparticle imaging at sub-10 W cm
irradiance. Nat. Photonics 2018, 12, 548−553.
̌
21) Solomek, T.; Wirz, J.; Klan, P. Searching for improved
́
(
(
photoreleasing abilities of organic molecules. Acc. Chem. Res. 2015,
8, 3064−3072.
22) Klessinger, M.; Michl, J. Excited States and Photochemistry of
Feringa, B. L. Easily accessible, highly potent, photocontrolled
modulators of bacterial communication. Chem. 2019, 5, 1293−1301.
4) Li, Y.; Zhang, Y.; Wang, W. Phototriggered targeting of
4
(
(
Organic Molecules; Wiley-VCH Press: United States of America, 1995;
Chapter 7.
nanocarriers for drug delivery. Nano Res. 2018, 11, 5424−5438.
̌
5) Klan, P.; Solomek, T.; Bochet, C. G.; Blanc, A.; Givens, R.;
́
(
(23) Zhang, Z.; Chen, C.; Chen, Y.; Wei, Y.; Su, J.; Tian, H.; Chou,
Rubina, M.; Popik, V.; Kostikov, A.; Wirz, J. Photoremovable
protecting groups in chemistry and biology: reaction mechanisms
and efficacy. Chem. Rev. 2013, 113, 119−191.
P. Tuning the conformation and color of conjugated polyheterocyclic
skeletons by installing ortho-methyl groups. Angew. Chem., Int. Ed.
2018, 57, 9880−9884.
(
6) Hansen, M. J.; Velema, W. A.; Lerch, M. M.; Szymanski, W.;
Feringa, B. L. Wavelength-selective cleavage of photoprotecting
groups: strategies and applications in dynamic systems. Chem. Soc.
Rev. 2015, 44, 3358−3377.
(24) Lin, Y.; Koch, M.; Brigeman, A. N.; Freeman, D. M. E.; Zhao,
L.; Bronstein, H.; Giebink, N. C.; Scholes, G. D.; Rand, B. P.
Enhanced sub-bandgap efficiency of a solid-state organic intermediate
band solar cell using triplet−triplet annihilation. Energy Environ. Sci.
2017, 10, 1465−1475.
(25) Cui, X.; Zhao, J.; Zhou, Y.; Ma, J.; Zhao, Y. Reversible
photoswitching of triplet−triplet annihilation upconversion using
dithienylethene photochromic switches. J. Am. Chem. Soc. 2014, 136,
9256−9259.
(
7) Olejniczak, J.; Carling, C. J.; Almutairi, A. Photocontrolled
release using one-photon absorption of visible or NIR light. J.
Controlled Release 2015, 219, 18−30.
(8) Rwei, A. Y.; Wang, W.; Kohane, D. S. Photoresponsive
nanoparticles for drug delivery. Nano Today 2015, 10, 451−467.
(9) Lin, Q.; Yang, L.; Wang, Z.; Hua, Y.; Zhang, D.; Bao, B.; Bao, C.;
Gong, X.; Zhu, L. Coumarin photocaging groups modified with an
electron-rich styryl moiety at the 3-position: long-wavelength
excitation, rapid photolysis, and photobleaching. Angew. Chem., Int.
Ed. 2018, 57, 3722−3726.
(26) Deng, F.; Blumhoff, J.; Castellano, F. N. Annihilation limit of a
visible-to-UV photon upconversion composition ascertained from
transient absorption kinetics. J. Phys. Chem. A 2013, 117, 4412−4419.
(27) Montalti, M.; Credi, A.; Prodi, L.; Gandolfi, M. T. Handbook of
Photochemistry; CRC Press: Boca Raton, 2006; Chapter 12.
(28) Wegner, E. E.; Adamson, A. W. Photochemistry of complex
ions. III. absolute quantum yields for the photolysis of some aqueous
(
10) Peterson, J. A.; Wijesooriya, C.; Gehrmann, E. J.; Mahoney, K.
M.; Goswami, P. P.; Albright, T. R.; Syed, A.; Dutton, A. S.; Smith, E.
A.; Winter, A. H. Family of BODIPY photocages cleaved by single
D
DOI: 10.1021/jacs.9b09034
J. Am. Chem. Soc. XXXX, XXX, XXX−XXX

Journal of the American Chemical Society
Communication
chromium(III) complexes. chemical actinometry in the long wave-
length visible region. J. Am. Chem. Soc. 1966, 88, 394−404.
(29) Zhang, K. Y.; Yu, Q.; Wei, H.; Liu, S.; Zhao, Q.; Huang, W.
Long-lived emissive probes for time-resolved photoluminescence
bioimaging and biosensing. Chem. Rev. 2018, 118, 1770−1839.
(30) Zhao, J.; Xu, K.; Yang, W.; Wang, Z.; Zhong, F. The triplet
excited state of BODIPY: formation, modulation and application.
Chem. Soc. Rev. 2015, 44, 8904−8939.
E
DOI: 10.1021/jacs.9b09034
J. Am. Chem. Soc. XXXX, XXX, XXX−XXX