Photophysical properties and photodynamic therapy activity of a meso-tetra(4-carboxyphenyl)porphyrin tetramethyl ester-graphene quantum dot conjugate

Article abstract of DOI:10.1039/C8NJ06175K

Novel meso-tetra(4-carboxyphenyl)porphyrin tetramethyl ester metal derivatives were synthesised and characterized. These derivatives were interacted with graphene quantum dots (GDQs). Spectroscopic evidence that was obtained showed that the resultant conjugates were stable due to the strong π-π stacking interaction between the GQDs and the porphyrins. The fluorescence and singlet oxygen generating behaviour of the porphyrins and the nanoconjugates were investigated following incorporation. The dark toxicity and photodynamic therapy activities of the porphyrins and the nanoconjugates were successfully studied using MCF-7 breast cancer cells. Cell viability for the dark toxicity was more than 90% for all complexes. The PDT activities at the highest concentration of 120 μg ml^?1 showed a decrease in cell viability down to 15.2% for the GaClTMPP-GQDs.

Full text of DOI:10.1039/C8NJ06175K

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Photophysical properties and photodynamic therapy
activity of a meso-tetra(4-carboxyphenyl)porphyrin
tetramethyl ester–graphene quantum dot conjugate†
Cite this:DOI: 10.1039/c8nj06175k
Muthumuni Managa, * Bokolombe Pitchou Ngoy and Tebello Nyokong
*
Novel meso-tetra(4-carboxyphenyl)porphyrin tetramethyl ester metal derivatives were synthesised and charac-
terized. These derivatives were interacted with graphene quantum dots (GDQs). Spectroscopic evidence that
was obtained showed that the resultant conjugates were stable due to the strong p–p stacking interaction
between the GQDs and the porphyrins. The fluorescence and singlet oxygen generating behaviour of the por-
phyrins and the nanoconjugates were investigated following incorporation. The dark toxicity and photodynamic
therapy activities of the porphyrins and the nanoconjugates were successfully studied using MCF-7 breast cancer
cells. Cell viability for the dark toxicity was more than 90% for all complexes. The PDT activities at the highest
Received 6th December 2018,
Accepted 16th February 2019
DOI: 10.1039/c8nj06175k
ꢀ1
rsc.li/njc
concentration of 120 mg ml showed a decrease in cell viability down to 15.2% for the GaClTMPP–GQDs.
low cell-uptake efficiency limit their widespread application in
biomedicine. Various nanocarriers have been actively devel-
Introduction
There has been great interest in improving cancer treatments oped for porphyrins in order to enhance their physicochemical
1
3–15
due to high morbidity and mortality that is often associated applications
where cellular uptake has limited their broad
with this disease. Among the emerging cancer therapies, photo- application; an example of one of these nanocarriers is graphene
dynamic therapy (PDT) surpasses the traditional methods, which quantum dots (GQDs).
1,2
include surgery, chemotherapy and radiotherapy. The advan-
GQDs are known to have excellent optical and electronic
tages of PDT over traditional methods are that it is non-invasive in properties coupled with high photostability, aqueous solubility
1
6,17
nature, has fewer side effects, causes negligible drug resistance and bio-compatibility.
and has low systemic toxicity.
These properties have made GQDs
1–4
very attractive as alternatives to semiconductor QDs for appli-
PDT is a process that requires a combination of laser light cations in fluorescence bio-imaging, sensing (biosensors and
with an appropriate wavelength, a photosensitizer (PS), and chemosensors), photocatalysis, drug delivery and as photosen-
5
,6
18–21
molecular oxygen to elicit a therapeutic response. The pro- sitizers in photodynamic therapy (PDT).
duction of singlet oxygen has been reported to depend on the GQDs are well known PDT agents with high singlet oxygen
2
1
triplet state population and the effectiveness of the energy quantum yields. Hence, combining the two PDT agents
transfer process between the excited triplet state of the photo- (porphyrins and GQDs) is expected to improve the PDT through
sensitizer and ground state molecular oxygen. The electro- a synergistic effect. meso-Tetra(4-carboxyphenyl)porphyrin tetra-
nically excited photosensitizer transfers its energy to the ground methyl ester has been reported before but we report for the first
state molecular oxygen to produce an excited singlet oxygen, time the GaCl and Zn derivatives as well as the photophysical
which acts as the chief cytotoxic species in PDT.
7
2
2
6
,8
behaviour of meso-tetra(4-carboxyphenyl)porphyrin tetramethyl
Porphyrins have received great attention as the first and ester and metal derivatives non-covalently linked to GQDs.
9
8
second generation of PS because of their effective singlet oxygen Ester-containing porphyrins are known PDT agents, hence an
1
10–12
(
O ) generation ability, low toxicity and aromaticity.
However, ester containing porphyrin is employed in this work. The pre-
2
their poor physicochemical stability, hydrophobic property and sence of delocalized p electrons facilitates the interaction of
porphyrins with GQDs through non-covalent p–p stacking.
Centre for Nanotechnology Innovation, Department of Chemistry,
Rhodes University, Grahamstown 6140, South Africa. E-mail: m.managa@ru.ac.za,
Experimental
Materials and methods
t.nyokong@ru.ac.za; Fax: +27 46 6225109; Tel: +27 46 6038260/8801
†
Electronic supplementary information (ESI) available: Equipment used, proce-
dure for in vitro dark toxicity and PDT, photochemical and photophysical para-
meters, NMR spectra of TMPP and mass spectra of TMPP, GaClTMPP and ZnTMPP.
See DOI: 10.1039/c8nj06175k
Zn tetraphenyl porphyrin (ZnTPP), gallium chloride and zinc
chloride were purchased from Sigma-Aldrich. Dichloromethane
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(
(
DCM), dimethyl sulfoxide (DMSO) and dimethylformamide N = 6.13, found: C 68.20, H = 3.96, N = 6.11 MALDI-TOF-MS
DMF) were purchased from Merck. All other reagents and m/z calc.: 950.05. Found (M–Cl) 914.55.
+
solvents were obtained from commercial suppliers and used
Self-assembly, Scheme 2. The non-covalent coordination
as received. Graphene quantum dots (GQDs) were synthesized (p–p stacking) of GQDs with the metal-free meso-tetra(4-carboxy-
23
following the procedures reported elsewhere and the conjuga- phenyl)porphyrin tetramethyl ester and the metal derivatives
19
19
tion of the porphyrins to the GDQs was as previously described.
The metal-free meso-tetra(4-carboxyphenyl)porphyrin tetramethyl sence of delocalized p electrons facilitates the interaction of
ester (TMPP) was synthesized as reported before.
was achieved following a method employed before. The pre-
2
2
GQDs with porphyrins through non-covalent p–p stacking. The
The MCF-7 breast cancer cells were obtained from Cellonex. nanocomposites are represented as TMPP–GQDS, ZnTMPP–GQDs
Dulbecco’s phosphate-buffered saline (DPBS) and Dulbecco’s and GaClTMPP–GQDs.
modified Eagle’s medium (DMEM) were obtained from Lonza,
1
1
0% (v/v) heat-inactivated fetal calf serum (FCS), and the
ꢀ
1
Results and discussion
00 mg ml -penicillin–100 unit per ml-streptomycin–ampho-
s
tericin B mixture were obtained from Biowest , and octanol Characterization of the porphyrin–GQD conjugates
was obtained from SAARCHEM.
The syntheses of GaClTMPP and ZnTMPP are shown in Scheme 1.
Equipment employed in this work as well as the pro-
The complexes were characterized by elemental analyses, NMR,
cedure for the in vitro dark toxicity and PDT can be found in
the ESI.†
IR, and MALDI-TOF mass spectroscopy. The obtained data were
consistent with the predicted structure. The representation of the
nanocomposites of GQDs and the porphyrins via p–p stacking are
shown in Scheme 2.
Synthesis
Metallo porphyrins, Scheme 1. In a two-necked flask, DMF
was brought to reflux temperature while stirring and then, UV-Vis spectra
TMPP (0.1 g, 1.18 mmol) was added and the temperature was
brought to 100 1C. Then, zinc chloride (0.05 g, 0.36 mmol) or
gallium chloride (0.05 g, 0.28 mmol) was added and the mixture
was heated continously for 15 min. The completion of the
reaction was checked using a UV/Vis spectrophotometer. The
reaction vessel was then allowed to cool to room temperature.
DMF/water mixture (30 ml) was added to the resulting product
to precipitate the metallated porphyrin, and then the product
was filtered off and washed and then air dried.
The ground state electronic absorption spectra of porphyrins are
characterized by an intense band called the Soret or B band at about
400 nm and the Q bands are observed between 500 and 600 nm.
These porphyrin phenomena are explained by the Gouterman’s four-
24
orbital model. In this model, the two highest occupied molecular
orbitals (HOMOs), the a1u and a2u and lowest unoccupied mole-
25
g
cular orbitals (LUMO), the degenerate e are taken into account.
The Soret bands of TMPP and TMPP–GQDs are observed at
19 nm, and an additional peak is observed for the TMPP–GQDs
4
ZnTMPP. Yield: (21%) UV/Vis (DMF) l
4.51), 559 (3.94), 598 (3.65). H NMR (600 MHz, CDCl ) d 8.84
nm (log e): 422
max
1
(
3
(s, 8H), 8.46 (d, J = 7.5 Hz, 8H), 8.31 (d, J = 7.5 Hz, 8H), 4.13 (s,
36 4 8
12H) ppm. Calc. for C52H N O Zn: C = 68.61, H = 3.99, N = 6.16,
found: C 68.59, H = 3.97, N = 6.15 MALDI-TOF-MS m/z calc.:
+
9
10.24. Found (M + H) 911.07.
GaClTMPP. Yield: (19%) UV/Vis (DMF) lmax nm (log e): 422
1
(
(
(
4.51), 559 (3.94), 598 (3.65). H NMR (600 MHz, CDCl
3
) d 8.82
s, 8H), 8.47 (d, J = 7.5 Hz, 8H), 8.33 (d, J = 7.5 Hz, 8H), 4.15
s, 12H) ppm. Calc. for C H N O Ga: C = 68.29, H = 3.97,
5
2
36 4 8
Scheme 1 Metal insertion into metal free meso-tetra(4-carboxyphenyl)-
Scheme 2 Representation of the interaction between porphyrins and
porphyrin tetramethyl ester.
GQDs.
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Fig. 2 Electronic absorption spectra and fluorescence emission spectra
of GQDs. Excitation wavelength at 340 nm in DMF.
TMPP–GQDs as well as between ZnTMPP and ZnTMPP–GQDs.
Red shifts have been observed in the porphyrin–graphene oxide
2
8
nanoconjugates. GQDs show typical broad absorption and
1
9
narrow emission with a fluorescence emission spectrum at
45 nm upon excitation at 340 nm. The GQDs were shown to be
4
stable even when left in solution as no spectral changes were
observed.
Fig. 3 shows the emission spectra of H
2
and Zn porphyrin
and the porphyrin–GQD conjugates (as examples). The spectra of
2
9
TMPP and ZnTMPP are typical of porphyrins with two bands
differing in intensity. The additional emission peak observed in
the spectra is due to the GQDs. The decreases in the intensity
of the low energy band of the porphyrins could be due to the
presence of the GQDs.
Raman spectra
The quality of the as-synthesized GQDs and their nanoconjugates
were confirmed by laser Raman spectral analysis, Fig. 4.
GQDs are known to exhibit the diagnostic Raman bands
termed as the G and D bands resulting from the E tangential
Fig. 1 Normalised electronic absorption spectra of (A) TMPP, (B) ZnTMPP
and (C) GaClTMPP and porphyrin–GQD conjugates in DMF.
2
g
2
vibrational mode of the sp bonded carbons and the disordered
2
between 330 nm and 392 nm (Fig. 1); this peak has been
A1g breathing vibrational mode of the aromatic sp carbon rings,
2
associated with the p–p* transition of the sp carbon electrons respectively. The intensity ratio of the D band to the G band for
of the graphene core of GQDs as shown in the spectrum the conjugates was calculated to be above 1 as shown in Fig. 4,
1
9,26
for GQDs, Fig. 2.
The four Q-bands of the metal-free pre- which is an indication that porphyrin molecules successfully
cursor collapsed into two Q-bands following metalation, con- interacted with the GQDs by p–p stacking. The D : G ratio is
firming the successful insertion of GaCl and Zn as a central generally considered as a good parameter for measuring the
metal.
The Soret bands of ZnTMPP, GaClTMPP, ZnTMPP–GQDs and
GaClTMPP–GQDs were observed at 421 nm, 422 nm, 428 nm and
extent of functionalization of GQDs.
Dynamic light scattering
430 nm, respectively, Table 1. Red shifts were observed in the The sizes of the nanoconjugates were analysed using dynamic
Soret bands following the insertion of the central metals. Red light scattering (DLS) measurements, Fig. 5.
2
7
shifts have been reported to be the result of the insertion of
The conjugates of GQDs with metal-free porphyrins have
the central metal. Introduction of a heavy metal such as gallium a smaller size as compared to the corresponding metallated
and zinc could result in a degree of perturbation and electron derivatives, Fig. 5. It has been reported that central metals
27
delocalisation within the porphyrin macrocycle. The GaClTMPP within the cavity of the porphyrins have the ability to change
3
0
is red shifted as compared to ZnTMPP and this is due to the large the hydrophobicity of the molecule. The DLS sizes of TMPP–
size of gallium. GQDs, ZnTMPP–GQDs and GaClTMPP–GQDs were determined
There were also red shifts observed in the Soret band to be 19.9 nm, 24.9 nm and 28.6 nm respectively, compared
between GaClTMPP and GaClTMPP–GQDs, and TMPP and to GQDs alone at 10 nm, Table 1. DLS results show that there
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Table 1 The photophysical parameters for the porphyrins and their conjugates with GQDs in DMF
a
Complexes
lAbs (nm)
(FF(GQDs)
)
t
F(GQDs) (ns)
(FF(Porp)
)
t
F(Porp) (ns)
Eff
(F
D
) (ꢁ 0.01)
GQDs (10 nm)
TMPP
TMPP–GQDs (19.9 nm)
ZnTMPP
ZnTMPP–GQDs (24.9 nm)
GaClTMPP
343
418
423
421
428
422
430
0.35
—
0.14
—
0.09
—
0.07
6.1
—
2.48
—
1.96
—
1.73
—
—
—
—
55
—
71
—
77
—
0.15
0.29
0.19
0.26
0.05
0.10
4.8
15.5
3.7
8.9
3.1
8.2
0.38
0.42
0.43
0.49
0.44
0.51
GaClTMPP–GQDs (28.6 nm)
a
Values in brackets are the DLS sizes in nm.
Fig. 4 Raman spectra of (A) GDQ, (B) TMPP–GQDs, (C) ZnTMPP–GQDs
and (D) GaClTMPP–GQDs.
Fig. 3 Normalised fluorescence emission spectra of (A) TMPP and
B) ZnTMPP and porphyrin–GQD conjugates. Excitation l = 490 nm
(
in DMF.
was an increase in the sizes of the GQD nanoconjugates
compared to the GQDs alone, which is also an indication of Fig. 5 Dynamic light scattering of GDQs, TMPP–GQDs, ZnTMPP–GQDs
and GaClTMPP–GQDs 1% DMF.
the formation of supramolecular assemblies of the GQDs and
the porphyrins.
Photophysical and photochemical parameters
Transmission electron microscopy (TEM) was used to determine Equations for the determination of fluorescence (F
the morphology and size distribution of the as-synthesized singlet oxygen (F
Transmission electron microscopy (TEM) images
F
) and
D
) quantum yields may be found in the ESI.†
GQDs, Fig. 6.
Fluorescence lifetimes (s ) and quantum yields (U )
f
F
The TEM images of the GQDs on their own show that the
GQDs are monodispersed and the size ranges from 9–11 nm. The fluorescence lifetime (t
f
) of a complex defines the time
The GQDs in the presence of porphyrins show aggregation. a molecule spends in the excited state before returning to
Porphyrins are known to show aggregation upon covalent and the ground state through fluorescence and it is directly related
non-covalent interactions with the nanoparticles, due to the to the fluorescence quantum yield. The t of all the com-
f
interaction between the porphyrins adsorbed onto adjacent plexes was determined using a time-correlated single photon
nanoparticles. Aggregation by p–p stacking is common in count (TCSPC) method, following excitation at the emission
3
1
porphyrins.
maxima.
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Fig. 8 Emission spectra of GQDs and absorption spectra of GaClTMPP.
GQDs excitation at 340 nm in DMF.
Fig. 6 Transmission electron micrographs of GQDs, TMPP–GQDs,
ZnTMPP–GQDs and GaClTMPP–GQDs.
FRET is a non-radiative energy transfer process which occurs
between a photoexcited donor fluorophore upon the absorption
The fluorescence quantum yields (F
F
) were determined by the of higher energy photons and an acceptor molecule in close
3
2
comparative method, by comparing the fluorescence intensity of proximity to the donor fluorophore. FRET efficiency (Eff) was
the complexes to that of ZnTPP standard where the porphyrin determined experimentally from the fluorescence quantum
was excited and H SO standard where the GQDs were excited. In yields of the donor in the absence (FF(GQDs)) and presence
2
4
conjugate
33
Table 1, the F
F
and t
f
are represented as FF(Porp) and tf(Porp) when (FF(GQDs) ) of the acceptor using eqn (1):
exciting where porphyrins absorb (490 nm), and FF(GQDs) and
conjugate
FðGQDsÞ
F
F
tf(GQDs) when exciting where GQDs absorb (340 nm).
Eff ¼ 1 ꢀ
(1)
The quenching of the GQD emission by Zn 5,10,15,20-
FðGQDsÞ
3
2
tetra(1-pyrenyl)porphyrin (ZnTPrP) has been reported, and
similar quenching was obtained in this work. The FF(GQDs)
went from 0.35 for GQDs alone to 0.14, 0.09 and 0.07 for the
TMPP–GQDs, ZnTMPP–GQDs and GaClTMPP–GQDs, respectively,
Table 1. The tf(GQDs) values also shortened for the GQDs in the
presence of porphyrins. A typical fluorescence decay profile for
the ZnTMPP–GQDs as an example is shown in Fig. 7. Mono-
exponential decay profiles were obtained.
FRET efficiencies were high for the GaClTMPP–GQD conju-
gates as compared to the other conjugates. This may be due to a
more red-shifted Soret band compared to the other porphyrins,
resulting in more overlap with GQD emission, Fig. 8.
FRET results from dipole–dipole interactions and is extre-
mely dependent on the center-to-center separation distance
between the donor and the acceptor (r), the degree of spectral
overlap of the donor’s fluorescence emission spectrum and the
The quenching of the GQD emission may be due to F o¨ rster
resonance energy transfer (FRET) and other processes that deactivate
3
4,35
acceptor’s absorption spectrum
as shown in Fig. 8.
32
the excited state. The decrease in FF(GQDs) and tGQDs (when exciting
Singlet oxygen quantum yield (U
Singlet oxygen is the major cytotoxic species responsible for the
cancer cell death in PDT. The F were determined to be 0.38,
.42, 0.43, 0.49, 0.44 and 0.51 for the TMPP, TMPP–GQDs,
D
)
where GQDs absorb) observed in Table 1 may be due to FRET.
D
0
ZnTMPP, ZnTMPP–GQDs, GaClTMPP and GaClTMPP–GQDs
respectively. Diamagnetic metals such as zinc and gallium have
been shown to have high triplet and singlet oxygen quantum
yields, and long triplet lifetimes which are essential for the
3
6
photosensitization process. The electron-donating groups are
3
7
known to increase intersystem crossing (ISC) in porphyrins,
hence the presence of GQDs in the conjugates increases ISC,
D
resulting in improved F values of the porphyrins in the pre-
sence of GQDs.
MCF-7 breast cancer cell studies
In vitro dark toxicity. The dark toxicity studies of the
ꢀ1
molecules were performed at 5, 10, 20, 40, 80 and 120 mg ml
,
Fig. 7 Fluorescence decay profile of ZnTMPP–GQDS as an example in DMF. Fig. 9. At all concentrations, the cell viability percentages
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Fig. 10 PDT for porphyrins and their conjugates at 5, 10, 20, 40, 80 and
ꢀ
1
ꢀ2
1
20 mg ml and 40 J cm
.
Fig. 9 Dark toxicity plots for porphyrins and their conjugates at 5, 10, 20,
ꢀ
1
4
0, 80 and 120 mg ml .
were all above 90%. In vitro dark toxicity is undesirable for
photosensitizers aimed for use in PDT. The dark toxicity of
the photosensitizers was determined in 1% DMSO which was
used as the stock diluent. DMSO (1%) used had a negligible
effect on the cells seen in this work and this has also been
3
8–40
reported.
Fig. 11 PDT micrographs of MCF7 breast cancer cells of (A) GaClTMPP
and (B) GaClTMPP–GQDs.
Upon analysis of the triplicate replicate data of each concen-
tration, we observed no statistically significant difference as the
p-value was found to be greater than 0.05.
Photodynamic therapy. The photo-irradiations were per-
formed using a 420 nm LED and the irradiation time was
Fig. 11 shows the PDT micrographs of the MCF7 breast
cancer cells of (A) GaClTMPP and (B) GaClTMPP–GQDs when
irradiated at 40 J cm . The difference in the presence of the
GQDs can be seen in Fig. 11(B) where more cell death occurred.
ꢀ
2
300 s. The absorbance of the 96-well plates was measured at
an excitation wavelength of 450 nm using a Synergy 2 multi-
mode microplate reader (BioTek1). There were no changes
in the spectra of the porphyrins following irradiation for the
PDT studies, hence confirming the stability. The phototoxicity
of TMPP, TMPP–GQDs, ZnTMPP, ZnTMPP–GQDs, GaClTMPP
and GaClTMPP–GQDs against MCF-7 breast cancer increased
upon irradiation and increased with increase in concentration.
*
P o 0.05, is considered to be a statistically significant
difference. We observed a statistically significant difference as
the concentration increased. There was a significant difference
between the dark toxicity and the PDT data for all complexes.
As the concentration increased, the cell viability decreased, Conclusions
Fig. 10.
Porphyrins and GQDs have been interacted through p–p interaction
The GaClTMPP–GQDs showed higher phototoxicity at 15%
cell viability as compared to the TMPP, TMPP–GQDs, ZnTMPP,
ZnTMPP–GQDs and GaClTMPP at 120 mg ml . An increase in
PDT activities were observed for the porphyrins in the presence
of GQDs.
In PDT, an excited triplet state of the photosensitizer trans-
fers its energy to the ground state molecular oxygen resulting in
the production of singlet oxygen which is the main cytotoxic
species in PDT. Thus, the PDT activity is expected to follow the
same trend as the singlet oxygen quantum yields which was
evident in this work, Fig. 10.
to enhance the photophysical properties. Different spectroscopic
techniques were used to characterize the nanocomposites and the
interaction mechanism. Fluorescence and singlet oxygen quantum
yields improved for porphyrins in the presence of GQDs, which also
improved the PDT activities. Low dark toxicity of the nanocomposites
was observed which indicated high promising application in PDT.
ꢀ
1
Conflicts of interest
There are no conflicts to declare.
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Acknowledgements
20 D. Qu, M. Zheng, P. Du, Y. Zhou, L. Zhang, D. Li, H. Tan,
Z. Zhao and Z. Xied, Nanoscale, 2013, 5, 12272–12277.
This work was supported by the Department of Science and
Technology (DST)/Nanotechnology (NIC) and National Research
Foundation (NRF) of South Africa through DST/NRF South African
Research Chairs Initiative for Professor of Medicinal Chemistry
and Nanotechnology (UID 62620) and Rhodes University.
2
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