Muscle-Mimetic Synergistic Covalent and Supramolecular Polymers: Phototriggered Formation Leads to Mechanical Performance Boost

Article abstract of DOI:10.1021/jacs.0c10918

A thin filament stimulated by Ca2+ to combine with myosin is the structural basis to achieve filament sliding and muscle contraction. Though a large variety of artificial materials has been developed by mimicking muscle, the on-demand combination of the actin filament and myosin has never been precisely reproduced in polymeric systems. Herein, we show that both the combination process and the combined structure of actin filament and myosin have been mimicked to construct synergistic covalent and supramolecular polymers (CSPs). Specifically, photoirradiation as a stimulus induces the independently formed covalent polymers (CPs) and supramolecular polymers (SPs) to interact with each other through activated quadruple H-bonding. The resultant CSPs possess a unique network structure which not only facilitates the synergistic effect of CPs and SPs to afford stiff, strong, yet tough materials but also provides efficient pathways to dissipate energy with the damping capacity of the representative material being higher than 95%. Furthermore, muscle functions, for example, by becoming stiff during contraction and self-growth by training, are imitated well in our system via in situ phototriggered formation of CSP in the solid state. We hope that the fundamental understanding gained from this work will promote the development of synergistic CSP systems with emergent functions and applications by mimicking the principle of muscle movements.

Full text of DOI:10.1021/jacs.0c10918

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Muscle-Mimetic Synergistic Covalent and Supramolecular Polymers:
Phototriggered Formation Leads to Mechanical Performance Boost
Zhaoming Zhang,† Lin Cheng,† Jun Zhao, Hao Zhang, Xinyang Zhao, Yuhang Liu, Ruixue Bai, Hui Pan,
Wei Yu, and Xuzhou Yan*
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ABSTRACT: A thin filament stimulated by Ca2+ to combine with
myosin is the structural basis to achieve filament sliding and
muscle contraction. Though a large variety of artificial materials
has been developed by mimicking muscle, the on-demand
combination of the actin filament and myosin has never been
precisely reproduced in polymeric systems. Herein, we show that
both the combination process and the combined structure of actin
filament and myosin have been mimicked to construct synergistic
covalent and supramolecular polymers (CSPs). Specifically,
photoirradiation as a stimulus induces the independently formed
covalent polymers (CPs) and supramolecular polymers (SPs) to
interact with each other through activated quadruple H-bonding.
The resultant CSPs possess a unique network structure which not
only facilitates the synergistic effect of CPs and SPs to afford stiff, strong, yet tough materials but also provides efficient pathways to
dissipate energy with the damping capacity of the representative material being higher than 95%. Furthermore, muscle functions, for
example, by becoming stiff during contraction and self-growth by training, are imitated well in our system via in situ phototriggered
formation of CSP in the solid state. We hope that the fundamental understanding gained from this work will promote the
development of synergistic CSP systems with emergent functions and applications by mimicking the principle of muscle movements.
tions.10−19 The powerful functions of myofibril indicate that
the elegant combination of CPs and SPs through proper
INTRODUCTION
■
Supramolecular polymers (SPs) have been recognized as
interactions is a promising strategy to produce advanced
crucial components for living systems due to their roles in
materials. Nevertheless, the complicated structures of CPs and
biological functions, such as cell division, mediator for
SPs as well as their on-demand combination in myofibril show
actuation, and regulation of physiological process.1,2 In fact,
for many of these biological functions, their implementations
not only rely on individual supramolecular polymers but also
that developing artificial synergistic CSPs by mimicking
myofibril for specific properties or functions is a significant
challenge.
need the cooperation of specific covalent polymers (CPs). The
The construction of artificial synergistic CSPs needs to
working mode of myofibril in muscle contraction is a typical
rationally integrate SPs and CPs in one system. In 2016, Stupp
representative according to the sliding filament theory.3−6
et al. designed an ingenious system in which covalent and
Actin filament, a kind of SP in thin filament formed by
noncovalent polymerizations took place simultaneously to
supramolecular assembly of actin, possesses a large number of
form hybrid polymers as cylindrical fibers, and noncovalent
binding sites in its structure. When it receives the stimulus of
polymerization was shown to promote the covalent polymer-
Ca2+, the blocked binding sites are exposed and then bind to
ization.20 Whereafter, the same group further created hybrid
the head of myosin (CP in thick myofilament) through
systems with fascinating actuation properties by adopting
supramolecular interactions (Figure 1a). The stimulus-
sequential supramolecular and covalent polymerizations.21,22
triggered noncovalent combination of actin filament and
myosin is the structural basis to achieve the filament sliding.
Such a polymeric system with CPs and SPs working
Received: October 15, 2020
synergistically can be called synergistic covalent and supra-
molecular polymers (CSPs).7 Inspiration is often drawn from
nature to solve problems existing in artificial materials.8,9
Generally, individual CPs or SPs have their own advantages
but also possess inherent limitations for practical applica-
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Figure 1. Design of muscle-mimetic synergistic CSPs. (a) Actin filament, myosin, and their combination triggered by Ca2+ in myofibril, which act as
the inspiration source. (b) Schematic representation and chemical structures of the CPs, SPs, and the photoinduced formation of synergistic CSPs
to mimic myofibril.
Almost simultaneously, our group utilized the successive
covalent and supramolecular polymerizations to obtain
synergistic CSPs, which exhibited peculiar robust yet dynamic
properties.7 These simultaneous and sequential strategies stand
for a significant advancement toward constructing synergistic
CSPs. However, synergistic CSPs similar to myofibril, in which
CPs and SPs are independently formed and then connected on
demand to function by stimulus-triggered supramolecular
interactions, have yet to be achieved.
Herein, we report a de novo chemical design of the
synergistic CSP system in which both the responsive
combination and corresponding covalent and supramolecular
structures of the myosin and actin filament during muscle
contraction are reproduced. Specifically, similar to the Ca2+-
induced combination of actin filament and myosin, photo-
irradiation as a stimulus was employed to induce the
independent CPs and SPs to interact with each other through
activated quadruple H-bonding, thereby leading to the
formation of synergistic CSPs in a new way. The representative
synergistic CSP exhibits good mechanical properties, including
the aspects of stiffness (Young’s modulus = 145 MPa), strength
(maximum stress = 12.0 MPa), ductility (1506%), and
toughness (136 MJ/m3). Particularly, it also has unusual
performance in energy dissipation with a damping capacity
higher than 95%, which implies its enormous potential as
mechanically adaptive materials. These superior performances
benefit from the delicate muscle-mimetic structure, that is, a
tough but dynamic network formed by supramolecular
interactions connected CPs and SPs. Furthermore, the
photoinduced in situ combination of CPs and SPs in the
solid state endows the material with muscle-like functions.
Upon irradiation, the material becomes stiff like muscle
behaving during a contraction. Besides, the photostimulus
also gives rise to simultaneous enhancement of self-healing
efficiency and mechanical strength of the CSP, which is
reminiscent of muscle growth based on the reconstruction of
fibril after physical exercise.
RESULTS AND DISCUSSION
■
Design, Synthesis, and Structural Characterization.
To achieve the goal of mimicking myofibrils, the two
components of CPs and SPs first need to be rationally
designed. As shown in Figure 1b, the CPs adopted here are
polynorbornene derivatives prepared by ring-opening meta-
thesis polymerization (ROMP). The side chain of the CPs
decorates with a large number of 2,7-diamido-1,8-naphthyr-
idine (DAN) units, which is designed to imitate the structure
of thick myofilaments possessing many myosin heads arranged
on their surface (Figure 1a). The SPs mimicking the thin
filaments rely on a special monomer with three functional
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Figure 2. Partial 1H NMR spectra (400 MHz, CDCl3, 298 K) of pure SP (a) and SP mixed with CP-2 followed by UV irradiation (b). AFM phase
images of CSP-2 (c) and control-2 (d).
groups (Figure 1b). The group of benzo-21-crown-7 (B21C7)
and its complementary secondary ammonium salt are able to
bind with each other through host−guest recognition to form
the SPs (Figure 1b). The remaining functional group, namely,
the 2-ureido-4[1H]-pyrimidinone (UPy) moiety, serves as the
binding site like that on the thin filament which is initially
protected by nitrobenzyl group. In myofibril, the Ca2+
stimulates the thin filament to uncover the binding sites for
myosin, hence realizing the combination of actin filament and
myosin. Such a biological process is readily reproduced in this
work. When the UPy binding sites are protected by nitrobenzyl
groups, the combination between the CPs and SPs is
prohibited. However, once stimulated by UV irradiation, the
UPy sites can be deprotected and exposed. It has been found
that the UPy unit is able to selectively form strong
heterocomplementary quadruple H-bonds with the DAN
group.23−25 Therefore, the photoirradiation leads to the
integration of independent CPs and SPs to form synergistic
CSPs connected by activated quadruple H-bonding. Different
from the simultaneous or sequential covalent and supra-
molecular polymerizations, by mimicking myofibril, we employ
a fully new method of stimulus-induced combination (SIC) to
afford synergistic CSPs.
norbornenyl exo-di-n-butyl ester. In this way, three CPs with
different DAN contents were prepared. By mixing these three
CPs with SPs in a 1:1 molar ratio of DAN and UPy moieties
followed by photoirradiation, we constructed synergistic CSP-
1, -2, and -3 (Figure 1b). To deeply understand the properties
of the CSPs, two control samples corresponding to CSP-2
were also designed (Scheme S2). In the structure of control-1,
the amino group is not in the form of secondary ammonium
salt, but protected by the Boc group, which hampers the host−
guest recognition to form SPs. The control-2 is a sample whose
DAN units are acidized by HPF6 to destroy the possible weak
H-bonding. As such, the CPs and SPs in control-2 are simply
mixed.
The syntheses of the key monomers, CPs, and SP are
summarized in the Supporting Information. The CSP-2 was
prepared by photoirradiation of the mixed CP-2 and SP in
1
solution (λ = 365 nm). As exhibited in the H NMR spectra
(Figure 2b), the characteristic NH protons of the UPy moiety
were obviously different from those on the UPy-UPy dimer
formed by irradiation of pure SPs (Figure 2a), but highly
consistent with the formation of UPy-DAN heterodimer.23−26
Therefore, the mixed CP-2 and SP in solution interacted with
each other through heterocomplementary quadruple H-
bonding to form CSP-2 upon photoirradiation. Particularly,
the integrated structure of the CSP-2 was well preserved in the
The density of the DAN units on the CPs can be tuned by
controlling the ratio of the dilute monomer, that is,
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Figure 3. (a) DSC curves of CSP-1, -2, and -3 and control-1 and -2 recorded by the second heating scan from −40 to 90 °C with a heating rate of
20 °C/min. (b) Stress−strain curves of CSP-1, -2, and -3 recorded with a deformation rate of 100 mm/min. (c) Young’s moduli and toughness of
CSP-1, -2, and -3 calculated based on their stress−strain curves. (d) Stress−strain curves of CSP-2 and control-1 and -2 recorded with a
deformation rate of 100 mm/min. (e) Young’s moduli and toughness of CSP-2 and control-1 and -2 calculated based on their stress−strain curves.
(f) Ashby plot of “toughness” and “strain at break” of CSP-2 and other reported polymer systems classified into CSPs in literatures.
bulk state, which was proved by the solid-state 13C NMR
(Figure S36). Besides, the morphology study by atomic force
microscopy (AFM) also supported the combination of CPs
and SPs. For example, compared with the phase image of CSP-
2 (Figure 2c), more distinct phase separation was observed in
the image of control-2 whose CPs and SPs cannot interact with
each other (Figure 2d). It is reasonable that the formation of
heterocomplementary quadruple H-bonding are beneficial to
the blend of CPs and SPs to inhibit their self-aggregation. In
addition, the lower phase shift of CSP-2 than that of control-2
indicates higher elasticity of CSP-2, which also supports the
strong interaction of the CPs and SPs in CSP-2.
Thermal Properties of the CSPs and Controls. Thermal
gravimetric analysis (TGA) study showed that all samples
including CSP-1, -2, and -3 and control-1 and -2 had good
thermal stability with the decomposition temperatures higher
than 200 °C (Figure S38). The differential scanning
calorimetry (DSC) of the samples were also studied (Figure
3a). The glass transition temperature (Tg) values of CSP-1, -2,
and -3 were measured as 64, 33, and 8.0 °C, respectively,
showing a decreasing tendency. It can be explained that the
quadrupole H-bonding-modulated CPs and SPs are able to
form a network structure, and the networks with more UPy−
DAN connection points generally restrict the motion of the
chain segments more powerfully, thus exhibiting higher Tg. In
addition, due to the lack of interchain interactions, the Tg
values of control-1 (1.0 °C) and -2 (29 °C) were lower than
that of CSP-2.
the values are 156, 145, and 39.7 MPa for CSP-1, -2, and -3,
respectively (Figure 3c). The strain at break had the opposite
trend with the values of 15% for CSP-1, 1506% for CSP-2, and
2465% for CSP-3 (Figure 3b). Except for CSP-1 with a brittle-
hard property, both CSP-2 and -3 had outstanding perform-
ance in toughness with the values of 136 and 122 MJ/m3,
respectively (Figure 3c). Among these three samples, the CSP-
2 has more balanced properties, which might be due to its
appropriate density of connection points, and thus would be
focused on in the following sections.
Subsequently, the mechanical properties of CSP-2 were
compared with those of the two control samples. There was no
obvious advantage of CSP-2 in terms of ductility due to the
character of linear polymer for control-1 and -2 (Figure 3d).
However, it was much more superior for CSP-2 in other
mechanical properties. The Young’s moduli were 145 MPa for
CSP-2, 0.6 MPa for control-1, and 34.5 MPa for control-2, and
the maximum stresses for the three samples were 12.0, 0.2, and
3.1 MPa, respectively (Figure 3e). Such an obvious advantage
was also observed in the aspect of toughness which showed the
values of 136 MJ/m3 for CSP-2, 10.8 MJ/m3 for control-1, and
28.2 MJ/m3 for control-2 (Figure 3e). As for the two controls,
control-1 can be regarded as a linear CP, and control-2
possesses coexisting CPs and SPs. However, there is no
significant interaction between them. Therefore, the prominent
properties of CSP-2 originate from the synergistic effect of CPs
and SPs, which is closely related to the photoactivated
quadruple H-bonding connection points. Notably, the
mechanical properties of the CSP-2 are also compared with
the reported cases which are classified as synergistic CSPs
according to the principle of which supramolecular interactions
in polymer structures could connect with each other to form
distinct SP chains.27−35 As shown in Figure 3f, in terms of
strain at break and toughness, our CSP-2 is superior to the
others, which might be due to the unique muscle-mimetic
structural design of our system.
Fundamental Mechanical Properties of the CSPs and
Controls. In myofibril, the combination of actin filament and
myosin offers a strong structure to support the filament’s
sliding. To explore whether their typical mechanical properties
are able to emerge in our artificial system, a series of tensile
tests were performed. The stress−strain curves of CSP-1, -2,
and -3 were shown in Figure 3b. Young’s moduli of the
samples increased with the density of connection points and
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Figure 4. (a) Cyclic tensile test curves of CSP-2 and control-1 and -2 at a strain of 500% under the deformation rate of 100 mm/min. (b) Energy
dissipation and damping capacity of CSP-2 and control-1 and -2 calculated based on the loading/unloading curves. (c) Cyclic tensile test curves of
CSP-2 recorded with increased maximum strains. (d) Energy dissipation and damping capacity for each circle of the cyclic tensile test curves.
Figure 5. (a) Cyclic temperature ramp curves of CSP-2 in the range of 40−80 °C with a heating/cooling rate of 5.0 °C/min. (b) Stress relaxation
experiments of CSP-2 at different temperatures. (c) Strain sweep rheological analysis of CSP-2 at a constant angular frequency of 1.0 rad/s. (d)
Master curves of CSP-2 at a reference temperature of 40 °C. (e) Tensile stress−strain curves of CSP-2 at different stretching rates. (f) Fitting curve
of yielding stress as a function of logarithm of strain rate.
Energy Dissipation of the CSPs and Control Samples.
In addition to the highlighted fundamental mechanical
properties, the synergistic CSPs also have unusual performance
in energy dissipation. Energy dissipation reflects the ability of
the materials to convert the mechanical energy into heat, which
can be calculated by integrating the area of the cyclic tensile
curves. As shown in Figure 4a, with the same strain of 500%,
the area of CSP-2 was much larger than those of the two
control samples, and the values of the energy dissipation were
calculated as 34.9 MJ/m3 for CSP-2, 0.80 MJ/m3 for control-1,
and 9.30 MJ/m3 for control-2. Damping capacity, which is
defined as the ratio of energy dissipation to the incoming
energy,36,37 was calculated as 95.1, 65.8, and 89.6% for CSP-2
and control-1 and -2, respectively (Figure 4b). One of the
most prominent features of these results was that the damping
capacity of control-1 is much weaker than those of the other
samples. On the basis of their structural differences, it is
reasonable to speculate that the SPs play a vital role in energy
dissipation. In addition, the damping ability of CSP-2 was
superior to that of control-2 where CPs and SPs do not have
significant interactions and higher than the reported CSP with
the CPs and SPs connected by a covalent bond in our previous
work (86.5%).7 These observations suggest that the good
damping capacity of CSP-2 originates from its unique
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structure, where the CPs and SPs are connected by quadruple
H-bonding. This speculation is further supported by the high
damping capacity of CSP-3 (91.2%).
viscoelastic region (about 2%) was observed because the
network was intact at this temperature, and the increase of
strain was accompanied by the damage of the network
structure through the dissociation of supramolecular inter-
actions. In contrast, the network decomposed at 70 °C; thus,
corresponding curves exhibited broad linear viscoelastic region
(∼100%). It could be speculated that the stress relaxation may
mainly result from the decomposition of network arising from
the dissociation of host−guest recognition, but weakening
and/or even dissociation of the quadruple H-bonding at high
temperature should also contribute to it.
The progressive loading−unloading experiments of CSP-2
were conducted to trace the changes of energy dissipation and
damping capacity on different strains (Figure 4c,d). The
energy dissipation increased almost linearly with the applied
strains of the sample, and the value of energy dissipation at an
applied strain of 1400% reached 125 MJ/m3, indicative of good
energy dissipation ability. Different from energy dissipation,
the damping capacity of CSP-2 always maintained at a high
level in the strain range of 100−1400%, and the mean value
under all strains was 95.6%. Therefore, the damping capacity of
CSP-2 was relatively stable and independent of varied
deformations. The comparison of damping capacity between
CSP-2 and different kinds of the reported energy dissipating
materials were summarized in Figure S42. It was found that the
damping capacity of CSP-2 is higher than most of the energy-
dissipation materials including bulky polymers,38,39 hydro-
gels,40,41 and natural materials42,43 and is comparable to the
hydrogel fibers which set the record in damping capacity.37
These results mean that the muscle-mimetic design would
make our CSP-2 a good candidate for energy absorption
applications.
Insights into the Structure−Property Relationship of
CSP-2. The above studies have disclosed that the CSP-2
possesses good mechanical properties and damping ability,
which results from its peculiar biomemetic structure. Then, to
figure out the relationships between the properties of the CSP-
2 and its structure, a series of rheology measurements were
carried out. The results of cyclic temperature ramp of CSP-2
were shown in Figure 5a. When the temperature was ramped
up from 40 to 80 °C, both the G′ and G″ substantially
decreased, and a peak emerged around 59 °C in the tan δ curve
at the same time, indicating the existence of a transition. An
opposite viscoelastic transition was observed in the ramp-down
process. Intriguingly, the two tan δ curves overlapped well with
each other above 57 °C but showed an evident hysteresis
below that temperature. The reason for this phenomenon
might be that 57 °C can be seen as a critical temperature, that
is, above it the supramolecular interactions start to dissociate,
but their reassociation at lower temperature has a time delay,
thus leading to the hysteresis.
The stress relaxation experiment is an effective tool to reveal
the structure information on polymers from their mechanical
behaviors. Obvious relaxation could be observed in all stress
relaxation curves recorded at different temperatures, but the
relaxation rate increased at elevated temperatures (Figure 5b).
The extent of the stress relaxation was also highly dependent
on the temperature: Similar to the polymers with permanent
cross-links, the applied force was kept at lower temperatures
(30−50 °C) even extending the relaxation time to 1 h, but it
could be quickly and fully released at temperatures higher than
60 °C, like the behavior of linear polymers. These results
support that synergistic CSP-2 has a network structure. At
temperatures lower than 50 °C, the topological structure is
frozen by the network, leading to the slow and incomplete
stress relaxation. In contrast, stress relaxation is accelerated
when the network structure is fractured by temperatures higher
than 60 °C. Besides, the network started to break at 60 °C is
consistent with the result of the temperature ramp test. These
analyses were further supported by the strain sweep tests
(Figure 5c). At a lower temperature (35 °C), a narrow linear
To comprehensively demonstrate the dynamic behaviors of
the CSP at different time scales, the master curves were
obtained at the reference temperature of 40 °C for CSP-2 by
using the time−temperature superposition (TTS) principle
(Figure 5d). The high-frequency region (>10−2 rad/s) with G′
> G″ was the glassy regime where the network was frozen.
Below the crossover point of 10−2 rad/s, the region was
assigned as the dissipative regime (G′ < G″). The super-
imposed curves in this regime were recorded at temperatures
higher than 60 °C which could weaken or dissociate the
supramolecular interactions of host−guest recognition and
quadruple H-bonding as analyzed above, thus resulting in
dissipative behaviors. Notably, partial restriction of dynamics
was observed in the range of 10−8−10−5 rad/s. Since the
supramolecular interactions should be basically in an
uncomplexed state at such lower frequencies (corresponding
to high temperatures), the observation might be related to
Rouse dynamics of the CP chains. The terminal regime of the
curves, lower than 10−8 rad/s, was the viscous flow regime.
The slope values lower than the true terminal relaxation, that
is, G′ and G″, are 2 and 1, respectively, were an indication of
secondary interactions affecting the chain dynamics.44,45 In
addition, the superposition of the data failed starting from 60
°C to higher temperatures, which was consistent with the
structure changes of the CSP-2. It is noteworthy that the
regime of the elastic plateau was absent in the curves, but it
was commonly observed in the system with strong network
structures including covalent bond connected CSPs in our
previous work.7 The phenomenon implies that the CSP-2 has a
highly dynamic network structure.
Moreover, to evaluate the energy required for initially
fracturing the network, tensile tests with different stretching
rates were performed and showed that the mechanical
properties of CSP-2 were highly stretching-rate-dependent
(Figure 5e). The plot of yielding stress against the logarithm of
deformation rate in Figure 5f had a linear relationship in
accord with the Eyring model of the mechanically induced
dissociation of noncovalent bonds:46,47
ε
̇
≈ e−(E −0.5σ V )/(k T)
y
y
a
b
̇
ε, σy, Ey, and Va are the strain rate, yielding stress, activation
energy, and effective activation volume, respectively. The
activation volume extracted by data fitting was 5.8 nm3, which
can be regarded as the size of polymer segments involved in
the motion associated with yielding. The apparent activation
energy used to evaluate the energy barrier to overcome the
mobile segments was calculated to be 23.0 kJ/mol. For CSP-2,
the initial fracture of the network structure might be
responsible for the yielding; hence, the energy to destroy the
intact network through the dissociation of supramolecular
interactions is about 23.0 kJ/mol.
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Figure 6. (a) Photographs of the film before and after irradiation. (b) Force separation curves of the film before and after irradiation from the
retraction of the cantilever. (c) Young’s moduli extracted from the force separation curves of the film before and after irradiation. (d) Storage
modulus as a function of irradiation time for CSP-2. (e) Stress−strain curves of CSP-2 recorded with a deformation rate of 100 mm/min. (f)
Stress−strain curves of the virgin and healed CSP-2 specimens with and without irradiation recorded with a deformation rate of 100 mm/min. (g)
Young’s moduli and maximum stress calculated based on the stress−strain curves of the healed CSP-2 specimens with and without irradiation.
Assisted by the working mechanism of the myofibril, the
structure−property relationships of our CSPs can be
established. In myofibril, the combination mode of actin
filament and myosin plays a crucial role in filament sliding. On
the one hand, the binding force, namely, supramolecular
interaction, is strong enough to support the sliding of actin
filament driven by the myosin; On the other hand, the
combination is also dynamic, such that the combined actin
filament and myosin are easily to be separated after
accomplishing one cycle of filament sliding. Such a critical
role of supramolecular connections is also reflected in our CSP
systems. The activated quadruple H-bonding, as cross-links of
the CPs and SPs, could facilitate the two components to work
synergistically, thus leading to the stiff yet tough material.
Moreover, apart from the quadruple H-bonding connections,
the SPs are formed by host−guest recognition, both of which
make our CSPs a highly dynamic network. When external
stress is applied to the CSPs, the network is readily to dissipate
energy through various pathways, eventually showing unusual
behavior in energy dissipation. Therefore, the unique muscle-
mimetic structure in which the CPs and SPs are cross-linked by
supramolecular interaction endows the materials with prom-
inent mechanically adaptive properties.
Muscle-Mimetic Functions of CSP-2. As mentioned
above, on the basis of the combination of CPs and SPs, the
filament sliding gives rise to the muscle contraction, and
becoming stiff is one of the most obvious characteristics during
the process. In addition, the strength of muscles could be
enhanced by training in which the destruction and
reconstruction of the fibril lead to the growth of muscles.48−50
Both functions of muscles involve complicated dynamic
processes and thus are difficult to mimic in the fabrication of
artificial materials. Given the good mechanical performance
and unique dynamics of our CSPs, we speculate that if the
photoinduced integration of CPs and SPs is possible in the
solid state, then these two muscle functions would be achieved
in a sense in our artificial system.
In order to verify the possibility, films containing
independent CPs and SPs with protected UPy were first
made. After 2 h of irradiation, an obvious color change was
observed from an initial dark yellow to a final brown (Figure
6a), which was attributed to the deprotection. Modulus
measurements of the films before and after irradiation were
performed using AFM, and the corresponding force−
separation curves were shown in Figure 6b. It is well-known
that the slope of the retract curves is linearly related to the
stiffness of the materials. Hence, the higher slope of the curve
after irradiation demonstrated that the film became much
stiffer. The Young’s moduli extracted from the retract curves
were 3.40 and 104.3 MPa for the samples before and after
irradiation, respectively (Figure 6c). On the basis of these
results, it is reasonable to conclude that the photoinduced
combination of CPs and SPs could stiffen our CSP material in
the solid state, reminiscent of the Ca2+-triggered muscle
contraction.
The changes of mechanical properties during the photo-
induced integration could be traced in situ by the rheometer
equipped with a light-emitting diode (LED) fixture. The
resulted plot of the storage modulus against irradiation time
were shown in Figure 6d. Before irradiation, the storage
modulus was constant. When the irradiation started at the time
of 2 h, the modulus increased gradually with the irradiation
time, and it tended to level off after being irradiated for 3 h.
This result implied that the materials with various stiffness can
be obtained by controlling the irradiation time, which is
meaningful for various applications. Subsequently, the
mechanical property changes of the irradiated film were
further characterized by macroscopic tensile tests, which
showed a distinct enhancement compared with sample before
irradiation (Figures 6e and S48). Before irradiation, the values
of Young’s modulus, maximum stress, and toughness for the
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J. Am. Chem. Soc. XXXX, XXX, XXX−XXX

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Article
system were 26.0 MPa, 3.20 MPa, and 20.6 MJ/m3,
respectively. In contrast, these parameters were enhanced to
84.6 MPa, 10.6 MPa, and 66.2 MJ/m3 after irradiation.
Therefore, these results indicate that the photoinduced
combination of CPs and SPs could enhance the mechanical
properties of the materials, and such a phenomenon is
somewhat similar to the function of stiffness change shown
by muscle contraction.
Structural reconstruction after damage along with enhanced
mechanical properties are the main features of self-growing
materials. Here, photoinduced self-healing of our material was
investigated. As shown by the stress−strain curves (Figure 6f),
the sample without irradiation was only restored a little, as
shown by the limited breaking strain of 14.3% after 2 h of
healing. In contrast, the sample with 2 h of irradiation could be
stretched up to 121% of its original length. Furthermore, the
overall mechanical properties of the material were also
improved upon irradiation. As shown in Figure 6g, the
Young’s modulus was enhanced from 26.0 to 78.8 MPa, and
the maximum stress was improved from 3.60 to 10.3 MPa. As
such, the self-healing process is accompanied by marked
mechanical property enhancement, resembling the self-growing
behavior of muscles after physical exercise.
AUTHOR INFORMATION
■
Corresponding Author
Xuzhou Yan − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR
China; orcid.org/0000-0002-6114-5743;
Email: xzyan@sjtu.edu.cn
Authors
Zhaoming Zhang − School of Chemistry and Chemical
Engineering, Frontiers Science Center for Transformative
Molecules, Shanghai Jiao Tong University, Shanghai 200240,
PR China
Lin Cheng − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR
China; orcid.org/0000-0002-5615-9198
Jun Zhao − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Hao Zhang − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Xinyang Zhao − School of Chemistry and Chemical
Engineering, Frontiers Science Center for Transformative
Molecules, Shanghai Jiao Tong University, Shanghai
200240, PR China
CONCLUSIONS
■
In summary, inspired by the working mechanism of myofibril
during muscle contraction, we have designed a polymeric
system in which the combination of CPs and SPs was triggered
by photoirradiation to generate synergistic CSPs cross-linked
by activated quadruple H-bonding. Both the combination
process and the resultant covalent and supramolecular
structures in CSPs are similar to those of actin filament and
myosin in myofibril. The results of tensile tests exhibited that
the synergistic CSPs had remarkable mechanical properties in
terms of stiffness (Young’s modulus = 145 MPa), strength
(maximum stress = 12.0 MPa), ductility (1506%), and
toughness (136 MJ/m3). Furthermore, they also possessed
unusual ability in energy dissipation with the damping capacity
above 95% in a large strain range of 100−1400%. Rheology
measurements revealed that the tough but dynamic network
structure, constructed by mimicking myofibril, is responsible
for the good mechanical performance. Particularly, the material
with photoinduced combination of CPs and SPs in the solid
state exhibited muscle-like functions. The stiffness change
observed in muscle contraction was reproduced in our artificial
materials whose strength was obviously enhanced upon
irradiation. The training-induced growth of muscle was also
mimicked by our material in which photoinduced self-healing
and enhancement of mechanical properties took place
simultaneously. The muscle-mimetic design with a photo-
triggered structure and property modulation of our CSPs could
find broad potential applications as smart supramolecular
materials.
Yuhang Liu − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Ruixue Bai − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Hui Pan − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Wei Yu − School of Chemistry and Chemical Engineering,
Frontiers Science Center for Transformative Molecules,
Shanghai Jiao Tong University, Shanghai 200240, PR China
Complete contact information is available at:
https://pubs.acs.org/10.1021/jacs.0c10918
Author Contributions
†Z.Z. and L.C. contributed equally to this work.
Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
X.Y. acknowledges the financial support of the NSFC/China
(21901161 and 22071152) and Natural Science Foundation of
Shanghai (20ZR1429200). W.Y. acknowledges the support
from NSFC/China (51625303 and 21790344).
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ASSOCIATED CONTENT
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* Supporting Information
The Supporting Information is available free of charge at
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