Regulating morphologies and near-infrared photothermal conversion of perylene bisimide: Via sequence-dependent peptide self-assembly

Article abstract of DOI:10.1039/c8cc00177d

The assembly behavior of perylene bisimide (PBI) can be precisely organised by the conjugation of sequence-dependent di-peptides in aqueous media. The assembled nanostructures and consequent properties of PBI aggregates can be tuned by the use of differen

Full text of DOI:10.1039/c8cc00177d

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DOI: 10.1039/C8CC00177D
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Regulating Morphologies and Near-infrared Photothermal
Conversion of Perylene Bisimide by Sequence-Dependent Peptide
Self-Assembly
Received 00th January 20xx,
Accepted 00th January 20xx
Lingyun Cui,a, † Yang Jiao,b, †Anhe Wang,a, † Luyang Zhao,a Qianqian Dong,a Xuehai Yan,a Shuo Baia, *
DOI: 10.1039/x0xx00000x
www.rsc.org/
The assembly behavior of perylene bisimide (PBI) can be precisely behaviour of PBI in aqueous media along with their formed
organised by conjugation of sequence-dependent di-peptides in supramolecular structure with enhanced photothermal
aqueous media. The assembled nanostructures and consequent conversion efficiency in a facile way is still challenging.
properties of PBI aggregates can be tuned by the use of
Supramolecular self-assembly of sequence-dependent peptide
differential peptide sequences with improved yield of radical building blocks has become an increasingly attractive strategy to
anions and enhanced photothermal conversion efficiency.
create functional nano-architectures for applications in drug
delivery, optoelectronic devices, cell scaffolds, nanofabrication and
tumour therapy.6 For instance, the self-assembly of aromatic short
peptides which are composed of aromatic group at the N-terminus
and short peptide sequence with only two amino acids, is governed
by aromatic π-stacking, hydrogen bonding and electrostatic
interactions enhancing the recognition between molecules and the
sequence of peptide chains.3, 7 PBI could be used as aromatic ligand
in peptide building blocks forming nanostructures with
photothermal property. The use of differential peptide sequences
could easily organize PBI precisely and tune the self-assembled
morphologies and consequent physiochemical properties of PBI
aggregates, which may enhance the yield of radical anions and
photothermal conversion efficiency.8
Perylene bisimide (PBI), one of the most valuable
functional dyes with stable chemical and optical properties,
has been applied widely in electronic, photonic devices and
solar cells et al..1 In particularly, PBI radical anions have a
strong absorption in near-infrared (NIR) region, which is called
“biological window” as most biological tissues are highly
transparent in this region from 780 to 1300 nm with low
degree of absorption.2 Therefore, such NIR system has
promising bio-applications especially in photothermal therapy
and light-triggered drug release.3 However, hydrophobic PBI
aromatic cores as well as derived radical anions are inclined to
aggregate in aqueous media causing luminescent quenching
and
a loss of free radical yield, which leads to low
photothermal conversion relative to the total input of light
energy. Several works have been performed to overcome the
issue via tuning the assembly behaviour of PBI in aqueous
media by various ingenious strategy.5 For instance, Würthner
and co-workers covalently introduced bulky substituent onto
the bay regions of PBI cores leading to an improvement in PBI
radical anions yield in non-aqueous solvents.5b Zhang and co-
workers used host-guest supramolecular strategy to prevent
aggregation of PBI aromatic cores and promote the formation
of aromatic radical anions in aqueous solution, which
improved
the
photothermal
conversion
efficiency
significantly.5c Nevertheless, how to tune the self-assembly
Scheme 1 Chemical structures and self-assembly process of
PBI-[GY]2 and PBI-[GD]2 and cartoon of radical anions
generated by chemical reduction leading to different NIR
photothermal conversion efficiency.
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In this work, we demonstrated that the self-assembly for details). Each system contained 24 PBI-peptide solutes,
behaviour of PBI in aqueous solution can be regulated by using 20000 water molecules and sodium ions equal to the amount
different di-peptide sequences (glycine-tyrosine, GY and of carboxylic groups in the system. All the carboxylic groups
glycine-aspartic acid, GD) conjugated to PBI cores, which leads are deprotonated due to the aqueous media at pH 8. The
to different nanostructures like nanofibers and nanospheres simulation results clearly showed that both of these two
via tunable molecular interactions (as shown in Scheme 1). monomers assembled to nanostructures, in which 18 of PBI-
The obtained nanostructures are highly dependent on the [GY]2 molecules assembled to a nanofiber consistent with
peptide sequences and showed clearly different radical yields experiment (Fig. 1c), while PBI-[GD]2 molecules arranged to
and photothermal conversion efficiency after irradiation by disordered oligomeric aggregates, as shown in Fig. 1d.
NIR laser.
PBI conjugated with bola- di-peptides were synthesized by
introducing GY or GD at both ends of the perylene moiety
(denoted as PBI−[GY]2, PBI−[GD]2, respectively; ESI† for details).
To determine the critical aggregation concentration (CAC) of
PBI-[GY]2 and PBI-[GD]2 in PBS buffer solution, UV-Vis spectra
of PBI derivatives at different concentrations were recorded.
As shown in Fig. S1a and b, the maximum absorptions of PBI-
[GY]2 and PBI-[GD]2 were located at 505 and 502 nm,
respectively. The absorption continuously increased from
2×10−6 to 1×10−4 M with the same spectral shape, indicating no
change of aggregate type. By plotting and fitting the maximum
absorbance to the concentration (Fig S1a, b insert), the CAC of
PBI-[GY]2 and PBI-[GD]2 in PBS buffer was calculated to 0.016
and 0.019 mM, respectively. By changing one amino acid of di-
peptide sequences from tyrosine to aspartic acid which
afforded extra COOH groups and much stronger electrostatic
repulsion, the CAC of PBI-[GD]2 compared with PBI-[GY]2
increased. It was also expected that enhanced hydrophilicity of
side chains of PBI-[GD]2 could influence the consequent
fluorescent performance. The fluorescent spectra of PBI-[GY]2
(Figure S1c) showed that a hypsochromic shift occurred from
Fig. 1 a) and b) TEM images of PBI-[GY]2 and PBI-[GD]2
612 to 594 nm when the concentration of PBI-[GY]2 decreased,
assembled in PBS buffer solution, respectively; c) and d) the
suggesting J-aggregation type of molecules.9 In addition, with
corresponding molecular dynamics simulation.
the decrease of concentrations, the fluorescent intensity was
strengthened firstly and then weakened due to the dis-
assembly of aggregates and dilution of single molecules. In
In the two systems, stacking distance between two
contrast, the emission peak of PBI-[GD]2 was split into 549 and
aggregated molecules is both 0.323 nm with deviance smaller
592 nm with a similar hypsochromic shift and increasing
than 0.010 nm statistically (Fig. S2a), indicating that the
intensity ratio between the two peaks due to the overlap of
distance is mostly determined by the interactions between PBI
emission and absorption spectra when the concentration
moieties rather than that of terminal amino acids. Besides, the
decreased (Fig. S1d). We reasonably believe that the extra
slipped-parallel stacking pattern of PBI moieties results from
electrostatic repulsion from deprotonated COOH groups
the larger electron density of π-surface than the edges of the
caused the reduction of interactions among hydrophobic PBI
molecules, as revealed by the electrostatic potential map
moieties, resulting in different fluorescent emission
(Fig.S2b). Moreover, the angle between two PBI moieties are
performance.
distributed over 0~40° for PBI-[GY]2, while exhibite a maximum
Transmission electron microscope (TEM) was used to
distribution at 23° on average of PBI-[GD]2 (Fig. S2c, d). It’s
determine the self-assembled morphologies of both molecules.
because that the charged aspartic acid based peptide
Fig. 1(a, b) indicated the formation of nanofibers of PBI-[GY]2
sequences form more intermolecular electrostatic interactions
with a diameter around 20 nm and length up to micrometers
resulting in oligomers. However, using protonated tyrosine
in PBS buffer solution, while the nanostructures of PBI-[GD]2
instead of aspartic acid forms long-range of hydrogen bonds.
tuned to spherical aggregates with an average diameter
The terminal amino acids also provide decisive effects on
around 50 nm. The difference of molecular interactions
assembled structures according to energy differences from
between PBI cores and peptide side chains may cause distinct
start to end state. At the start state, the solutes randomly
supramolecular
arrangements
and
self-assembled
disperse in a water box which can be regarded as an aqueous
solution. At the end of simulation, the solutes assemble to
nanostructures. The energy difference between start and end
nanostructures.10 To understand the influence of terminal
amino acids on the assembly behaviour, self-assembly
processes of both PBI-[GY]2 and PBI-[GD]2 were simulated (ESI†
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(∆E) was summarized in Table S1. The energy contributions of bands between 700-900 nm. As shown in Fig.
2a, the
PBI (including the interactions of PBI-PBI, PBI-water and PBI- absorption band of PBI-[GY]2 radical anions appeared at 729
ions) are 10.4 and −2.2 kJ·mol−1 for the two molecules, and 813 nm, while that of PBI-[GD]2 radical anions located at
respectively. Compared with a typical hydrogen bond energy 726 and 810 nm. The titration experiments with different ratio
ranged 8~40 kJ·mol−1, the contributions of PBI are quite small. between PBI derivatives and Na2S2O4 were performed to
In contrast, the contributions of terminal amino acids are optimize the yield of radical anions. Fig.2b showed the
significant. The energy contribution of tyrosine is 19.4 kJ·mol−1, characteristic absorption bands of PBI radical anions after
indicating an energy-disfavoring process, whereas the energy reduction, which revealed the nanostructures of PBI-[GY]2 and
contribution of aspartic acid is −83.8 kJ·mol−1 (Table S1), PBI-[GD]2 reached the maximum yield of PBI radical anions at
indicating a strong energy-favoring process. As shown in Fig. the ratio (PBI derivatives: Na2S2O4) of 1:0.35 and 1:0.6,
1
d, aggregated oligomers form dynamic COO—-water-Na+ respectively. Excess reducing agents are disadvantageous for
clusters and COO−–Na+ ion pairs which counterbalance the the production of radical anions with an absorption in NIR
strong Coulomb repulsive interactions between carboxylic region as depictured in Fig. 2c. The stronger electrostatic
groups and shorten the distance to neighbor oligomer repulsion of charged PBI-[GD]2 causing dissociation of
aggregates as the role of charge screening. This seems to aggregates provided more radical anions, in contrast, the
indicate an assembling tendency towards an eventual stronger
π-stacking interactions of PBI-[GY]2 were
nanosphere.
predominant and led the molecules remained in ground states.
Electron paramagnetic resonance (EPR) spectroscopy was
performed to provide the direct evidence of the formation of
PBI radical anions.5b Both of PBI-[GY]2 and PBI-[GD]2 solutions
gave the typical EPR signals, certifying the existence of free
radicals. As displayed in Fig. 2d, intense resonance with a g-
factor of 2.0038 can be detected with no hyperfine coupling to
the carbon or nitrogen nuclei of the aromatic core, which was
consistent with previous observation.5b It also indicated that
nanostructures derived from PBI-[GD]2 have more high yield
efficiency of PBI radical anions than that of PBI-[GY]2 at the
same conditions. Meanwhile UV data also indicated that the
formed PBI radical anions from PBI-[GY]2 and PBI-[GD]2 could
stood for at least 20 min at our experimental conditions (Fig.
S3), which is stable enough for the following photothermal
conversion performance.
Fig. 2 a) UV-Vis Spectra of PBI-[GY]2 and PBI-[GD]2 radical anion
in PBS solution; b) The titration experiments with different
ratio between PBI derivatives and Na2S2O4; c) The chemical
equation between PBI derivatives and Na2S2O4, d) EPR spectra
of the radical anions generated from PBI-[GY]2 (2 mM) and PBI-
[GD]2 (2 mM).
Then sodium dithionite (Na2S2O4) was selected as a
reducing agent to produce PBI radical anions. The PBI-[GY]2
and PBI-[GD]2 solution were constantly bubbled for 30 min
with nitrogen gas to remove oxygen in PBS buffer and
subsequently injected with freshly prepared Na2S2O4 solution.
The colour of the solution changed from red to purplish red
immediately, suggesting the forming of PBI radical anions. The
UV-Vis data proved the formation of radical anions in PBS
buffer as indicated by the decrease of PBI absorption between
400-600 nm and the concomitant increase of new absorption
Fig. 3 a) Temperature evolution of PBI-[GY]2 (left) and PBI-[GY]2
(right) radical anions with different concentration under NIR
irradiation; b) The corresponding reusability and stability.
Table 1 Temperature elevation and photothermal conversion
efficiency with different concentration of PBI-[GY]2 and PBI-
[GD]2:
PBI-[GY]2
PBI-[GD]2
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that more radical anions of PBI-[GD]2 are generated by the
irradiation of NIR with much higher efficiency compared of
PBI-[GY]2. The tunable self-assembly behaviour and enhanced
photothermal conversion efficiency may potentially provide
tools to facilitate the design and applications of controllable
drug delivery and release and photothermal therapy.
C(mM)
0.02
0.15
1.0
∆ T (oC)
3.3(±0.2)
3.7(±0.2)
η (%)
∆ T (oC)
η (%)
3.4(±0.3)
4.3(±0.5)
6.4(±0.2)
8.4(±0.5)
11.5(±0.2) 16.4(±1.2)
13.3(±1.4) 25.6(±3.4) 21.1(±0.4) 36.8(±2.4)
27.7(±0.1) 49.1(±3.0) 34.1(±1.7) 59.5(±2.8)
10
PBI radical anions have an excellent photothermal
conversion under the irradiation of near-infrared (NIR) laser.
Herein, PBI-[GY]2 and PBI-[GD]2 aggregates were exposed to a
808 nm NIR laser with a power of 1.0 W.cm−2 at room
temperature. As shown in Fig. 3a, both PBI radical anions from
PBI-[GY]2 (left) and PBI-[GD]2 (right) could convert NIR light to
heat effectively. The temperature elevation was enhanced
when the concentration increased for both PBI derivatives,
however, the photothermal conversion efficiency of PBI-[GD]2
radical anions was much higher than that of PBI-[GY]2 radical
anions as shown in Table 1 (the method to calculate η for
details in ESI†, Fig. S4). For instance, the temperature of PBI-
[GY]2 and PBI-[GD]2 solution with a concentration of 10 mM
was improved by 27.7 and 34.1oC in 15 min, respectively. In
contrast, PBS buffer solution as a control only increased less
than 2 oC under the same condition. The photothermal
conversion efficiency of PBI-[GY]2 radical anions was 49.1% and
for PBI-[GD]2 reached 59.5%, which can be explained by the
higher yield of radical anions after the reduction of PBI-[GD]2
compared with that of PBI-[GY]2. The inserted photos showed
the gel formation of PBI-[GY]2 only when the concentration
was above 10 mM due to the contribution of tyrosine forming
long arrangement of hydrogen bonding.
Acknowledgement
The authors acknowledge financial support from the National
Natural Science Foundation of China (Project No. 21774132,
21703253, 21644007) and the Talent Fund of the Recruitment
Program of Global Youth Experts.
Notes and references
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The reusability and stability of PBI-[GY]2 and PBI-[GD]2
solution were crucial for the application in photothermal
conversion. Fig. 3b displayed 6 cycles of temperature evolution
of PBI-[GY]2 and PBI-[GD]2 solution after reduction under NIR
laser irradiation. It was observed that the temperature
evolution of PBI-[GY]2 and PBI-[GD]2 solution have no obvious
change which demonstrated the good reusability and stability.
Meanwhile, the size of the nanostructures of PBI-[GY]2
decreased from micro- to nano- scale due to the electrostatic
repulsion after the reduction which broken the long fiber into
short one, whereas that of PBI-[GD]2 retained their original
structure and size as shown in Fig. S5.
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Conclusions
In conclusion, we demonstrate the use of different peptide
sequences to conjugate and organise PBI moieties precisely,
which assemble to tunable nanostructures with enhanced
yield of radical anions and photothermal conversion efficiency.
By changing of end amino acid from tyrosine to aspartic acid,
the assembled morphologies show distinct formation of
nanofiber and nanosphere respectively. The stronger
electrostatic repulsion of charged PBI-[GD]2 causing
dissociation of aggregates provides more radical anions, in
contrast, the stronger π-stacking interactions of PBI-[GY]2 are
predominant and lead the PBI molecules to remain in ground
states. Photothermal conversion experiment demonstrates
8
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4 | J. Name., 2012, 00, 1-3
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DOI: 10.1039/C8CC00177D
Regulating Morphologies and Near-infrared Photothermal Conversion of
Perylene Bisimide by Sequence-Dependent Peptide Self-Assembly
†
†
†
Lingyun Cui,a, Yang Jiao,b, Anhe Wang,a, Luyang Zhao,a Qianqian Dong,a Xuehai Yan,a Shuo
Baia, *
The Table of Contents:
The assembly behavior of perylene bisimide (PBI) can be precisely organised by conjugation of
sequence-dependent di-peptides in aqueous media. The assembled nanostructures and
consequent properties of PBI aggregates can be tuned by the use of differential peptide
sequences with improved yield of radical anions and enhanced photothermal conversion
efficiency.
1