Efficient energy transfer between coronene-modified permethyl-β-cyclodextrins and porphyrin for light induced DNA cleavage

Article abstract of DOI:10.1039/c7cc00736a

A novel supramolecular assembly was constructed by the noncovalent complexation of hexa-cata-hexabenzocoronene modified permethyl-β-cyclodextrins with tetrasodium tetraphenylporphyrintetrasulfonate in water, exhibiting highly efficient excited energy tran

Full text of DOI:10.1039/c7cc00736a

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Efficient Energy Transfer between Coronene-Modified Permethyl-
β-cyclodextrins and Porphyrin for Light Induced DNA Cleavage
Jie Yu,a Ying-Ming Zhang,a Pei-Yu Lia and Yu Liu*ab
Received 00th January 20xx,
Accepted 00th January 20xx
DOI: 10.1039/x0xx00000x
www.rsc.org/
A
novel supramolecular assembly was constructed by the there is a relative paucity of studies on the structure–activity
noncovalent complexation of hexa-cata-hexabenzocoronene relationship of CHBC–porphyrin system, especially in
modified permethyl-β-cyclodextrins with tetrasodium noncovalent binding manner. In the previous work, we have
a
tetraphenylporphyrintetrasulfonate in water, exhibiting highly presented a series of biocompatible nanocarriers and photo-
efficient excited energy transfer behaviors and promising DNA modulated nanoassemblies based on CD–porphyrin
photocleavage ability.
conjugation.10,11 In the wake of these fascinating results by us
and other researchers, we herein reported a CHBC derivative
(CHBC-1) bearing three permethyl-β-cyclodextrins (PMCDs),
which endowed CHBC core with good water solubility.12
Moreover, taking advantage of the strong binding ability of
PMCD with sulfonated porphyrin,13 a supramolecular network
was constructed in aqueous solution. Moreover, an efficient
energy transfer process from CHBC-1 to porphyrin occurred in
this artificial nanoassembly and more significantly, the
The fabrication of nanometer-scaled architectures with unique
structures and function is a crucial aspect in supramolecular
chemistry and nanoscience. In this regard, the synthesized
nanographenes via “bottom-up” method have been attracted
considerable attraction because of their special structural and
physical properties.1 It is generally recognized that hexa-peri-
hexabenzocoronene
(PHBC)
and
hexa-cata-
hexabenzocoronene (CHBC) occupy the key position in the
study of nanographenes.2 Taking advantage of intrinsic
properties of PHBC and CHBC, including intermolecular π-π
stacking behaviors and superior electronic performance, many
supramolecular architectures have been elaborately
constructed and showed inventive applications in the area of
electronic devices,3 bioimaging,4 and chemical sensing.5
obtained nanoassembly
photocleavage ability.
exhibited
excellent
DNA
As an important class of organic dyes, porphyrins have been
explored as functional building blocks arising from their
excellent electroactive and photochemical properties.6 Many
endeavors have been devoted to the covalent combination of
hexabenzocoronenes with porphyrins. For instance, the first
PHBC–porphyrin triad was synthesized by Wong et al. and
applied as a photovoltaic device.7 Hirsch and Jux et al.
reported a covalently linked PHBC–porphyrin conjugate and
Drewello and Jux et al. reported a porphyrin derivative with
two PHBC units and explored its absorption and emission
features of such superbenzene–porphyrin conjugate.8,9
However, in contrast to these known PHBC–porphyrin systems,
Scheme 1 Syntheses of CHBC-1 and the structure of TPPSS.
Alkynyl-substituted CHBC derivative
4 was synthesized
according to the reported literature with slight modification.14
Then, permethyl-β-CDs (PMCD) were grafted onto CHBC core
via the Cu(I)-catalyzed Huisgen 1,3-dipolar cycloaddition
(Scheme 1). The obtained host compound CHBC-1 was
comprehensively characterized by 1H, 13C NMR, and HR-
MALDI-TOF spectroscopy (Figures S1–S3 in the ESI). Owing to
a.Department of Chemistry, State Key Laboratory of Elemento-Organic Chemistry,
Nankai University, Tianjin 300071, P. R. China.
b.Collaborative Innovation Center of Chemical Science and Engineering (Tianjin),
Nankai University, Tianjin 300071, P. R. China. E-mail: yuliu@nankai.edu.cn
†
Electronic Supplementary Information (ESI) available: synthesis and
characterization of multifunctional supramolecular conjugate and the experimental
details. See DOI: 10.1039/x0xx00000x
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the strong binding affinity of TPPSS with PMCD cavity, the Figure S6, the 1H NMR spectrum of CHBC-1 in CDCl3 was
binary CHBC-1/TPPSS supramolecular assembly could be easily distinctly different from the one in D2O. As judged from the 2D
fabricated by mixing CHBC-1 with TPPSS in aqueous solution, NOESY spectrum in CDCl3, the peaks at 8.78–8.93 and 7.90
which was sufficiently characterized by spectroscopic and ppm could be assigned to the protons of the coronene and
microscopic investigation, as described below.
triazole rings, respectively (Figure S7 in the ESI). According to
As shown in Figure 1a, the absorption peaks centered at 278, the NOESY spectra of CHBC-1 in D2O, the cross-peaks between
390, and 424 nm were assigned to the absorption spectral the protons of coronene and PMCD were observed, indicating
features of CHBC-1. This information, along with the comp- that the benzene ring of coronene was self-included into the
ound characterization data, jointly confirmed that CHBC-1 was cavity of PMCD (Figure S8 in the ESI).6a,10 The optimized
successfully synthesized.11–15 Meawhile, by comparing with the molecular modulation of CHBC-1 also corroborated that CHBC-
spectral superposition of CHBC-1 and TPPSS, the absorption 1 existed in the self-included conformation in aqueous solution
peak of CHBC-1/TPPSS complex gave bathochromic shift from (Figure S9 in the ESI). In the CHBC-1/TPPSS complex, the
412 to 416 nm. The circular dichroism experiments provided phenyl protons of TPPSS at 7.6–8.5 ppm exhibited multiple
additional evidence on the noncovalent association between cross-peaks with the PMCD, whereas the previously observed
CHBC-1 and TPPSS. That is, both CHBC-1 and CHBC-1/TPPSS cross-peaks between the protons of CHBC-1 and PMCD
complex gave negative circular dichroism signals, whereas the disappeared (Figure S10 in the ESI).6a,10 These NMR results
assembly’s circular dichroism signals were more intensive than demonstrated that CHBC-1 moiety was compelled from the
CHBC-1 and TPPSS around 386 and 412 nm (Figure S4 in the cavity due to the strong binding ability of PMCD with
ESI). Since coronene was not a chiral molecule, the well- porphyrin derivatives. There was no obvious Tyndall effect in
defined circular dichroism signals of CHBC-1 was obviously CHBC-1 or TPPSS solution, suggesting that the neither CHBC-1
contributed to the PMCD-induced circular dichroism. These nor TPPSS could be self-assembled to form large-sized
spectroscopic phenomena jointly suggest that TPPSS was aggregates. Comparatively, CHBC-1/TPPSS assembly exhibited
included into the hydrophobic cavity of PMCD. As shown in a clear Tyndall effect in solution (Figure S11 in the ESI).
Figure S19, the inflection point occurred at the molar fraction Meanwhile, the zeta potential value of the assembly was
of 0.33, corresponding to the 2:1 complexation stoichiometry negative, implying that negative charges were located on the
between PMCD and TPPSS.13 Subsequently, the complexation surface of CHBC-1/TPPSS aggregates (Figure S12 in the ESI).
stoichiometry of CHBC-1 with TPPSS was also identified by Job Furthermore, the morphology of supramolecular assembly was
plot, where the inflection point occurred at the molar fraction also characterized by microscopic investigation. As shown in
of 0.4, indicating a 2:3 complexation stoichiometry (Figure 1b). the TEM image, there were two-dimensional netlike
Meanwhile, the curve of the absorbance intensity versus the nanostructures and meanwhile,
a number of flake-like
[CHBC-1]/[TPPSS] molar ratio showed an inflection point at the nanostructures were found in the SEM image (Figure S13 in
molar ratio of 0.67, further suggesting the formation of host– the ESI).
guest complex in 2:3 molar ratio (Figure S5 in the ESI).
Although it was not easy to directly obtain the binding
constant between CHBC-1 and TPPSS in 2:3 complexation
stoichiometry, it is known that the TPPSS/PMCD complex was
stable enough to fabricate various functional supramolecular
assemblies in water.6,10,11,13b,16a Thus, we can also reasonably
speculate that the CHBC-1/TPPSS complex in our case would
stably exist in aqueous solution.
Fig. 2 a) Normalized spectra of Q-band of TPPSS and emission spectrum of CHBC-1 in
phosphate buffer (pH 7.2, λex = 380 nm) at 25 °C; b) Excitation spectra of TPPSS,
TPPSS/PMCD and CHBC-1/TPPSS complexes by monitoring the emission wavelength at
655 nm ([CHBC-1] = 1 × 10−6 M, [TPPSS] = 1.5 × 10−6 M, [PMCD] = 3 × 10−6 M).
The photophysical behaviors were further investigated in
the CHBC-1/TPPSS assembly. The Q-band of TPPSS and
emission spectrum of CHBC-1 was normalized in Figure 2a. In
the range of 450–700 nm, the absorption spectrum of TPPSS
Fig. 1 a) UV/Vis absorption spectra of CHBC-1, TPPSS, CHBC-1/TPPSS ([CHBC-1] = 4×10−6
largely overlapped with the fluorescence emission spectrum of
CHBC-1, which indicated that an efficient excited-energy
transfer (EET) process might take place in the CHBC-1/TPPSS
assembly.8–9 Subsequently, the EET process in CHBC-1/TPPSS
M, [TPPSS] = 6×10−6 M), b) Job plot for CHBC-1 upon complexation with TPPSS in pH=
7.2 phosphate buffer (absorption changes recorded at 412 nm for TPPSS; [CHBC-1] +
[TPPSS] = 5×10−6 M).
The noncovalent complexation of CHBC-1 with TPPSS was was investigated by fluorescence spectroscopy. When
also investigated by means of NMR spectroscopy. As shown in different amount of TPPSS was added to the CHBC-1 solution,
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the fluorescence intensity of CHBC-1 was nearly 100% was measured to be 19.9 Å with the optimized molecular
quenched, while the porphyrin emission was observed at the modulation from the minimized energy method (Figure S16 in
same time (Figure 3). In the control experiments, although the ESI). The followings are some reasons for the efficient EET
both TPPSS and PMCD/TPPSS systems gave the fluorescence process between CHBC-1 and TPPSS. First, the absorption
emission, the emission intensity of CHBC-1/TPPSS complex was spectrum of TPPSS largely overlaps with the fluorescence
1.9 times higher than the reference groups under the same spectrum of CHBC-1. Second, the strong noncovalent
experimental condition, implying the EET-assisted fluorescence interaction between PMCD and TPPSS draws the donor and
enhancement (Figure S14 in ESI). In our case, the host–guest acceptor together, and the closer center-to-center distance is
complexation with the hydrophobic cavity of PMCD could beneficial to the efficient EET process. Third, the TPPSS
greatly deter the negatively charged porphyrins from self- moieties were included and protected by the cavity of PMCD,
quenching or solvent attacking, thus leading to the different by which the self-quenching or solvent attacking can be
photophysical behaviors as compared to the non-bound avoided to a great extent in water.
porphyrins in water. We further investigated the effect of
Considering that the reactive oxygen species (ROS) can be
diffusional collision and no spectral change was observed in 4 generated by nanographene and porphyrin, agarose gel
or TPPSS when TPPSS was added to the solution of precursor 4 electrophoresis assay was performed to investigate the photo-
in DMSO (Figure S15 in the ESI). These results clearly indicated induced DNA cleavage ability of CHBC-1/TPPSS supramolecular
that the florescence energy could be transferred from excited assembly.17 As shown in Figure 4, no DNA cleavage activity was
CHBC-1 to TPPSS moieties in aqueous solution.
found for CHBC-1/TPPSS, CHBC-1 and PMCD/TPPSS in the dark.
In addition, it was found that the excited spectra of CHBC- In contrast, among all the examined samples, the CHBC-
1/TPPSS, PMCD/TPPSS and TPPSS were similar to their 1/TPPSS supramolecular assembly displayed much higher
corresponding absorption spectra (Figure 2b). Although the β cleavage activity than CHBC-1 and PMCD/TPPSS under visible
band of CHBC overlapped with the Soret band of TPPSS, the light irradiation (Lane 2 in Figure 4). That is, the closed
excitation and absorption signals of CHBC-1/TPPSS assembly supercoiled DNA (from I) was completely decomposed to
were more intensive than the ones of PMCD/TPPSS and TPPSS nicked circular DNA (form II, 87%) and liner DNA (form III, 13%).
in the range of 360–385 nm. Thus, it is believed that the Furthermore, the control experiment was performed to
fluorescence emission of CHBC-1/TPPSS was mainly investigate the mechanism of DNA photocleavage. That is, KI,
contributed to the energy transfer from excited CHBC-1 to NaN3 and DMSO were selected as the scavengers of hydrogen
TPPSS moieties.
peroxide, singlet oxygen and hydroxyl radical, respectively.18 It
was found that the photo-induced DNA cleavage activity of
CHBC-1 and CHBC-1/TPPSS complex was inhibited by NaN3 and
KI, but DMSO was ineffective, suggesting that the hydrogen
peroxide and singlet oxygen were the correlative ROS
generated by CHBC-1/TPPSS and responsible for the DNA
cleavage (Figures S17–S18 in the ESI).
Fig. 3 Fluorescence spectral changes of CHBC-1 upon addition of TPPSS (0–1.5 equiv) in
pH 7.2 phosphate buffer solution at 25 °C ([CHBC-1] = 1 × 10−6 M, λex = 380 nm).
According to Forster’s rules,16 the EET efficiency (E) was
achieved 99% in the CHBC-1/TPPSS assembly. Furthermore, in
the presence of 1.5 equiv TPPSS, the absolute fluorescence
quantum yield (Φ) of CHBC-1 decreased from 9.1% to 0.3%.
Using the measured Φ, the E was calculated to be 97%, which
was similar to the value obtained above. As shown in Figure
S20, the fluorescence lifetime of CHBC-1 decreased from 23.3
ns to 3.7 ns. Along with the steady fluorescence spectroscopic
results, it jointly indicated that the energy transfer from
coronene to the porphyrin likely goes through a Förster
mechanism. The center distance between the donor (CHBC-1)
and acceptor (TPPSSS) also played an important role in the EET
efficiency.16a The distance from the center of CHBC-1 to TPPSS
Fig. 4 Photocleavage of pBR322 DNA (5 ng/μL). Lane1: the blank control; Lane 2: CHBC-
1/TPPSS (0.01 mM/0.015 mM); Lane3: CHBC-1 (0.01 mM); Lane4: TPPSS/PMCD systems
(0.015 mM/0.02 mM); (+) in the presence and absence (–) of visible light.
In conclusion, benefiting from the highly affinitive
noncovalent binding,
a netlike nanographene/porphyrin
supramolecular assembly was successfully fabricated from
CHBC-modified PMCDs and TPPSS in aqueous solution.
Noticeably, an efficient energy transfer was achieved from
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13 (a) K. Kano, R. Nishiyabu, T. Asada and Y. Kuroda, J. Am.
Chem. Soc., 2002, 124, 9937-9944. (b) G. Liu, X. Xu, Y. Chen,
X. Wu, H. Wu and Y. Liu, Chem. Commun., 2016, 52, 7966-
7969.
14 (a) Q. Zhang, H. Peng, G. Zhang, Q. Lu, J. Chang, Y. Dong, X.
Shi and J. Wei, J. Am. Chem. Soc., 2014, 136, 5057-5064; (b) J.
nanographene to porphyrin in this artificial nanoassembly with
a high efficiency up to 97%. Moreover, the supramolecular
assembly exhibited excellent photo-induced DNA cleavage
ability. Consequently, the present work not only reveals an
excited-energy transfer process in nanographene/porphyrin
supramolecular assembly, but also exhibits the possible
application of nanographene/porphyrin conjugation in the
field of photodynamic therapy.
Yu, Y. Chen, Y.-H. Zhang, X. Xu and Y. Liu, Org. Lett., 2016, 18
4542-4545.
,
15 (a) Y. S. Cohen, S. Xiao, M. L. Steigerwald, C. Nuckolls and C.
R. Kagan, Nano Lett., 2006, 2838-2841; (b) A. A.
6,
We thank the National Natural Science Foundation of China
(Grant Nos. 21432004, 21472100, and 91527301) for financial
support.
Gorodetsky, C.-Y. Chiu, T. Schiros, M. Palma, M. Cox, Z. Jia,
W. Sattler, I. Kymissis, M. Steigerwald and C. Nuckolls,
Angew. Chem. Int. Ed., 2010, 49, 7909-7912.
16 (a) Z.-Y. Gu, D.-S. Guo, M. Sun and Y. Liu, J. Org. Chem., 2010,
75, 3600-3607; (b) K. Kilsa, J. Kajanus, J. Martensson and B.
Albinsson, J. Phys. Chem. B, 1999, 103, 7329-7339.
Notes and references
17 (a) Y. Chen, D. Zhao and Y. Liu, Chem. Commun., 2015, 51
12266-12269; (b) X. Xiong, L. Gan, Y. Liu, C. Zhang, T. Yong, Z.
Wang, H. Xu and X. Yang, Nanoscale, 2015, , 5217-5229.
,
1
(a) M. Ball, Y. Zhong, Y. Wu, C. Schenck, F. Ng, M. Steigerwald,
S. Xiao and C. Nuckolls, Acc. Chem. Res., 2015, 48, 267-276;
(b) M. Kastler, J. Schmidt, W. Pisula, D. Sebastiani and K.
Müllen, J. Am. Chem. Soc., 2006, 128, 9526-9534; (c) K.
Müllen and J. P. Rabe, Acc. Chem. Res., 2008, 41, 511-520; (d)
C.-Y. Chiu, B. Kim, A. A. Gorodetsky, W. Sattler, S. Wei, A.
7
18 (a) X.-W. Liu, Y.-M. Shen, J.-S. Shu, Y. Xiao, S.-B. Zhang and J.-
L. Lu, J. Fluoresc., 2015, 25, 1527-1535; (b) H. Kumar, V.
Devaraji, R. Prasath, M. Jadhao, R. Joshi, P. Bhavana and S. K.
Ghosh, Spectrochim. Acta, Part A, 2015, 151, 605-615.
Sattler, M. Steigerwald and C. Nuckolls, Chem. Sci., 2011, 2,
1480-1486.
2
3
(a) L. Chen, Y. Hernandez, X. Feng and K. Müllen, Angew.
Chem. Int. Ed., 2012, 51, 7640-7654; (b) J. Wu, W. Pisula and
K. Müllen, Chem. Rev., 2007, 107, 718-747; (c) A. Narita, X.-Y.
Wang, X. Feng and K. Müllen, Chem. Soc. Rev., 2015, 44
6616-6643.
,
(a) L. Chen, K. S. Mali, S. R. Puniredd, M. Baumgarten, K.
Parvez, W. Pisula, S. De Feyter and K. Müllen, J. Am. Chem.
Soc., 2013, 135, 13531-13537; (b) S. Xiao, S. J. Kang, Y. Zhong,
S. Zhang, A. M. Scott, A. Moscatelli, N. J. Turro, M. L.
Steigerwald, H. Li and C. Nuckolls, Angew. Chem. Int. Ed.,
2013, 52, 4558-4562; (c) Y. Yamamoto, T. Fukushima, Y. Suna,
N. Ishii, A. Saeki, S. Seki, S. Tagawa, M. Taniguchi, T. Kawai
and T. Aida, Science, 2006, 314, 1761-1764; (d) J. Cao, Y.-M.
Liu, X. Jing, J. Yin, J. Li, B. Xu, Y.-Z. Tan and N. Zheng, J. Am.
Chem. Soc., 2015, 137, 10914-10917.
4
5
C. Zhang, Y. Liu, X.-Q. Xiong, L.-H. Peng, L. Gan, C.-F. Chen
and H.-B. Xu, Org. Lett., 2012, 14, 5912-5915.
(a) V. Vij, V. Bhalla and M. Kumar, ACS Appl. Mater.
Interfaces, 2013, 5, 5373-5380; (b) P.-C. Zhu, L.-N. Luo, P.-Q.
Cen, J.-T. Li and C. Zhang, Tetrahedron Lett., 2014, 55, 6277-
6280.
6
(a) Y. Liu, C.-F. Ke, H.-Y. Zhang, J. Cui and F. Ding, J. Am. Chem.
Soc., 2008, 130, 600-605; (b) F. J. M. Hoeben, M. Wolffs, J.
Zhang, S. De Feyter, P. Leclere, A. P. H. J. Schenning and E. W.
Meijer, J. Am. Chem. Soc., 2007, 129, 9819-9828; (c) Z.-Q. Li,
Y.-M. Zhang, D.-S. Guo, H.-Z. Chen and Y. Liu, Chem. - Eur. J.,
2013, 19, 96-100.
7
W. W. H. Wong, T. Khoury, D. Vak, C. Yan, D. J. Jones, M. J.
Crossley and A. B. Holmes, J. Mater. Chem., 2010, 20, 7005-
7014.
8
9
J. M. Englert, J. Malig, V. A. Zamolo, A. Hirsch and N. Jux,
Chem. Commun., 2013, 49, 4827-4829.
D. Lungerich, J. F. Hitzenberger, M. Marcia, F. Hampel, T.
Drewello and N. Jux, Angew. Chem. Int. Ed., 2014, 53, 12231-
12235.
10 J. Zhao, H.-Y. Zhang, H.-L. Sun and Y. Liu, Chem. - Eur. J., 2015,
21, 4457-4464.
11 H.-L. Sun, Y. Chen, J. Zhao and Y. Liu, Angew. Chem. Int. Ed.,
2015, 54, 9376-9380.
12 (a) R. Kabe, X. Feng, C. Adachi and K. Müllen, Chem. - Eur. J.,
2014, 9, 3125-3129; (b) J. M. Englert, F. Hauke, X. Feng, K.
Müllen and A. Hirsch, Chem. Commun., 2010, 46, 9194-9196.
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