Light-Driven Expansion of Spiropyran Hydrogels

Article abstract of DOI:10.1021/jacs.0c02201

The incorporation of molecular switches in organic structures is of great interest in the chemical design of stimuli-responsive materials that mimic the complex functions of living systems. Merocyanine dyes that convert to spiropyran moieties upon exposure to visible light have been extensively studied as they can be incorporated in hydrated covalent networks that will expel water when this conversion occurs and induce a volumetric shrinkage. We report here on a sulfonate-based water-soluble photoswitch that, in contrast to the well-known systems, triggers a volumetric expansion in hydrogels upon exposure to photons. Contraction is in turn observed under dark conditions in a highly reversible manner. The novel behavior of the photoswitch incorporated in the covalent network was predicted by coarse-grained simulations of the system's chemical structure. Using pH control and polymeric structures that differ in lower critical solution temperature, we were able to develop hydrogels with highly tunable volumetric expansion. The novel molecular function of the systems developed here led to materials with the negative phototaxis observed in plants and could expand the potential use of hydrogels as sensors, soft robots, and actuators.

Full text of DOI:10.1021/jacs.0c02201

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Light-Driven Expansion of Spiropyran Hydrogels
Chuang Li, Aysenur Iscen, Liam C. Palmer, George C. Schatz, and Samuel I. Stupp*
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ABSTRACT: The incorporation of molecular switches in organic
structures is of great interest in the chemical design of stimuli-
responsive materials that mimic the complex functions of living
systems. Merocyanine dyes that convert to spiropyran moieties
upon exposure to visible light have been extensively studied as they
can be incorporated in hydrated covalent networks that will expel
water when this conversion occurs and induce a volumetric
shrinkage. We report here on a sulfonate-based water-soluble
photoswitch that, in contrast to the well-known systems, triggers a
volumetric expansion in hydrogels upon exposure to photons.
Contraction is in turn observed under dark conditions in a highly
reversible manner. The novel behavior of the photoswitch
incorporated in the covalent network was predicted by coarse-
grained simulations of the system’s chemical structure. Using pH control and polymeric structures that differ in lower critical
solution temperature, we were able to develop hydrogels with highly tunable volumetric expansion. The novel molecular function of
the systems developed here led to materials with the negative phototaxis observed in plants and could expand the potential use of
hydrogels as sensors, soft robots, and actuators.
reversibly control the association between a photoswitchable
azobenzene guest and an α-cyclodextrin host.29 This interaction
acts as a supramolecular cross-link causing reversible expansion
and contraction of the hydrogel with irradiation. More recently,
Feringa et al. reported a string-shaped hydrogel made of
macroscopically aligned supramolecular assemblies of photo-
responsive molecular motors that can bend in response to
light.30 These examples demonstrate that conformational
changes in photoswitchable molecules can induce macroscopic
actuation in hydrogels.
Spiropyrans are interesting photoswitches that interconvert
between two isomers, a ring-closed spiropyran form (SP) and
ring-opened merocyanine form (MC), which differ in dipole
moment, molecular volume, polarity, and net charge.31 Recent
work has shown that the incorporation of spiropyrans in
materials can cause significant changes in their physical and
chemical properties upon irradiation, leading for example to
phase transitions of thermoresponsive polymers,32−34 removal
of cross-links in polymer networks,35 reconfiguration of a
supramolecular nanotube,36 self-assembly of nanoparticles,37
movement of droplets,38 as well as macroscopic actuation such
INTRODUCTION
■
Natural systems transduce light energy to drive a variety of useful
processes, such as photosynthesis in leaves,1 photoactivation of
pigments that enables human vision,2 and phototropic motion
induced by photoisomerization of phytochromes.3 These
natural light-driven systems have inspired the synthetic
development of artificial light responsive materials4,5 that can
perform complex functions with applications in catalysis,6,7
sensing,8 adhesion,9 bioengineering,10,11 drug delivery,12 as well
as soft robotics.13−15 Light offers inherent advantages over other
stimuli, including the possibility to instantly turn on or off the
signal and to vary the wavelength, not requiring contact with the
photoresponsive substance, and the ability to introduce spatial
and directional specificity. All of these advantages have
motivated the development of photoactive materials based on
polymers,16 liquid crystal elastomers,17,18 and gels.19 Photo-
responsive hydrogels are particularly interesting as biomaterials
due to their structural similarity to the extracellular matrix and
the possibility of changing mechanical properties through light
exposure.20 Researchers have incorporated various photoactive
components such as photocleavable groups,21,22 photothermal
agents,23 and molecular photoswitches24 into hydrogel matrices
to tune their physical, chemical, and biological properties.
Molecular photoswitches, such as azobenzenes,25 diary-
lethenes,26 stilbenes,27 spiropyrans,28 and their derivatives, are
useful because they can selectively and reversibly reconfigure
conformations upon irradiation. For example, Harada et al.
reported on a supramolecular hydrogel in which light is used to
Received: February 27, 2020
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Figure 1. (A) Design of novel polymerizable, water-soluble spiropyrans (molecules 1b−1d) for photoexpansion rather than the well-known
photocontraction behavior in water-insoluble spiropyrans (molecule 1a). (B) Plot of the expected amount of net charge and corresponding measured
volume changes before and after light irradiation for different moieties 1a−1d. (C) Plot of the probability of different molecules having nearest MCH
or SP neighbors within 7 Å for both the ring-opened form (top) and ring-closed form (bottom) using a radial distribution (see Figure S10) function
calculated from coarse-grained simulations. (D) Plot of the probability of finding the indicated average number of water beads (four waters per
MARTINI bead) with the ring-opened (MCH) and ring-closed (SP) form in monomers 1a, 1b, and 1d calculated from the coarse-grained simulations
used for the data shown in C.
as bending39 and walking.40 However, the spiropyrans used in
these systems were water-insoluble and required organic
solvents for the preparation of materials which limits their
functionality. Although water-soluble spiropyrans have been
reported41 and used as small molecules for electrostatic
assembly,42 there are no examples known of water-soluble
spiropyrans containing polymerizable sites that can be chemi-
cally incorporated into hydrogel networks to tune their physical
properties using light. We report here on the molecular design
and chemical synthesis of sulfonate-based polymerizable water-
soluble spiropyran molecules that can be covalently attached to a
hydrogel network and demonstrate their novel photoactuation
behavior.
hydrophobic SP form, in agreement with previously reported
results.39,40 In contrast, hydrogels containing sulfonated
spiropyrans (1b−1d) were found to expand in volume under
the same irradiation conditions (Figure 1A). We hypothesized
that this photoexpansion behavior is related to a change in
charge after light irradiation. Figure 1B shows that the net charge
of 1a decreases from +1 to 0, resulting in a light-driven
contraction to 89% of its original volume (Figure S15). In
contrast, the net charge in 1b and 1c increases from 0 to −1
upon light irradiation, which may explain the observed
photoexpansion to 102% and 103% of their original volume,
respectively. Furthermore, the amount of net charge in 1d
increases from −1 to −2 resulting in a greater light-driven
volume expansion (105% of the original volume). In addition,
we observed that this light-induced expansion only occurs in
acidic environments where the phenol group of merocyanine is
protonated (Figure S16).
To gain atomistic insight into this photoexpansion behavior,
we carried out molecular dynamics (MD) simulations using a
coarse-grained (CG) model (see the SI, Figures S17−S21 for
details). The presence of SO3− groups can affect the interactions
between spiropyran molecules, which we quantified by
calculating the number of neighboring spiropyran molecules
found in the first solvation shell of a given spiropyran (Figure
1C). All three spiropyrans (1a, 1b, and 1d) appear to have
predominantly zero or one other spiropyran neighbor in their
first solvation shells in the MCH form (we did not model here 1c
since its charges are so similar to 1b). The simulations show that
RESULTS AND DISCUSSION
■
We first synthesized spiropyran molecules containing both a
polymerizable methacrylate group and sulfonate groups to
achieve water solubility (1a-1d, see the SI, Figures S1−S13 for
details). These molecules were covalently incorporated into
cross-linked polymer networks using aqueous free-radical
polymerization in the presence of N-isopropylacrylamide
monomers, N,N′-methylenebis(acrylamide) cross-linkers and
ammonium persulfate/tetramethylethylenediamine initiators
(see the SI, Figure S14 for details). After incubation in acidic
water (5 mM HCl) in the dark, the hydrogel containing
molecule 1a without any sulfonate groups was found to contract
upon irradiation due to isomerization of the positively charged
hydrophilic merocyanine form (MCH+) to the uncharged
B
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Figure 2. (A) Expansion kinetics of hydrogel samples containing photoswitch 1d upon light irradiation at different values of pH. (B) UV−vis spectra of
water-soluble spiropyran (1d) at different pH values after equilibration in the dark. (C) Plot of UV−vis absorbance of MCH− and SP2− as a function of
time for solutions containing photoswitch 1d under dark conditions followed by irradiation after pH was elevated from 2.37 to 6.01. (D) Expansion
kinetics of hydrogel samples containing 1d exposed to sequential stimuli of elevated pH followed by light or vice versa (red and blue curves) or
simultaneous exposure to both stimuli (black curve).
in systems containing the nonsulfonated spiropyran 1a the
isomerization from MC to SP under light leads to the formation
of clusters among the hydrophobic moieties. In contrast,
systems containing sulfonated spiropyrans (1b and 1d) which
experience an increase in charge upon irradiation do not form
clusters presumably as a result of repulsive electrostatic
interactions. We also found that the interaction between
spiropyran and water decreased for 1a and increased for 1b
and 1d upon irradiation, indicating that the photoinduced
decrease (or increase) in charge density facilitates water
diffusion out of and into the gel (Figures 1D and S9). These
simulations provide insight on the role of water diffusion in the
observed photoexpansion of hydrogels containing 1b−1d.
We found that degree of photoexpansion can be tuned by
varying the solution pH during light irradiation and we chose to
test samples in a range of pH 2.5 to 6.0 based on the previously
reported pKa value of the phenolate moiety of the sulfonated
merocyanine.42 For example, hydrogels containing the 1d
moiety expanded to 105% of its original volume upon irradiation
with light at a solution pH of 2.37. This ratio was found to
increase gradually with increasing pH (Figure 2A). A similar
trend was observed for hydrogels containing 1b and 1c moieties
(Figure S22). To better understand why this happens, we
collected UV−vis spectra using aqueous solutions containing
the same concentration of disulfonated 1d at different pH values
without irradiation. After equilibration overnight in the dark, we
found that the absorbance intensity of MCH− at 425 nm
decreased with increasing pH (Figure 2B). This indicated that
the reaction equilibrium between SP2− and MCH− shifted
toward SP2− with higher pH in the dark. We tracked this
equilibration at pH 6.01 by following the intensity changes at
425 nm (MCH−) and 225 nm (SP2−). Figure 2C shows that in
the dark the absorbance intensity of MCH− spontaneously
decreased while that of SP2− increased and eventually became
constant after 84 min. The absorbance intensity of MCH−
decreased gradually to zero in 30 min under light irradiation,
indicating the complete isomerization to the SP2− form. This
process was applied to hydrogel samples containing the 1d
moiety, where we first observed spontaneous expansion in the
dark with higher solution pH due to the re-equilibration of the
reaction SP2−↔MCH− to favor the SP2− form, followed by a
secondary photoinduced expansion behavior when light is
turned on (Figure 2D, red circles). We explored a different
pathway, namely applying the two stimuli separately to the same
gel in reverse order and achieved the same final expansion ratio
(Figure 2D, blue triangles). Importantly, simultaneous activa-
tion with pH and light leads to faster expansion kinetics relative
to either sequential pathways (Figures 2D, black squares, and
S23). One could imagine that the amount of photoisomerization
(MCH → SP) is a critical parameter that determines the extent
of expansion, and indeed we found that the photoexpansion is
dependent on the total amount of the photoswitches grafted on
PNIPAM polymers (Figure S24). The expansion ability
increases with a higher ratio of photoswitches, reaching a
plateau at a 1:50 molar ratio. In experiments described below, we
therefore chose to keep a 1:50 (SP/monomer) ratio and a water
bath at pH of 2.37 to protonate the gel in the dark, and materials
were then transferred to a water bath at pH 6.01 for
photoactuation.
In addition to the effect of pH, the extent of photoexpansion is
also tunable by choosing different polymer backbones with
variable lower critical solution temperature (LCST; Figure
S25A). This can be achieved by replacing the PNIPAM with
different molar ratios of di(ethylene glycol) methyl ether
methacrylate (DEGMA) and oligo(ethylene glycol) methyl
ether methacrylate (OEGMA, Mn = 500) during copolymeriza-
tion (Figure 3A). Keeping the concentration of spiropyrans and
environmental pH constant and the temperature fixed at room
temperature, we found that the photoexpansion of hydrogels
containing 1d was inversely correlated with the LCST of the
polymers used (Figure 3B). The same trend was observed for
hydrogels containing 1b (Figure S25B). Since the LCST of all
C
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Figure 3. (A) Synthesis of photoactive polymers with different LCSTs by varying the molar ratio of DEGMA and OEGMA. (B) Plots of photoinduced
expansion ratio (black) of hydrogel samples containing 1d and of LCST (red) as a function of molar percentage OEGMA monomer in the network.
(C) Schematic representation of light-induced expansion effect on hydrogel samples with different LCST.
polymers used is above room temperature, we expect the
polymer chains with a lower LCST to collapse and coil more
than those with a higher LCST due to their hydrophobicity
(Figure S21). Upon irradiation, the increase in charge density
causes water to enter into the polymeric network and the
collapsed polymer chains should become extended, thus leading
to a large expansion ratio (Figure 3C). Conversely, polymer
chains with higher LCST values should be less coiled at room
temperature and only exhibit minimal expansion when extended
as a result of photoisomerization.
Inspired by phototaxis in plants, we sought to develop a series
of phototactic artificial muscle networks (Figure 4A). As shown
in Figure 4B, the rod-like gel containing 1a monomer bends
toward the light source due to inhomogeneous contraction in
the hydrogel (Figure S26), and we refer to this system as a
positive phototactic (PP) artificial muscle. However, rod
hydrogels synthesized with monomers 1b−1d bend away from
the light source because the surface exposed to the light source
expands first, creating an expansion gradient. This opposite
bending behavior is defined here as a negative phototactic (NP)
artificial muscle. Both PP and NP artificial muscles recover to
their original unbent shape with longer irradiation time since the
deformational gradient disappears in these systems as photons
diffuse through the hydrogel. Most importantly, the bending
angle of the NP artificial muscles is highly tunable using different
spiropyran moieties (Figure 4C) or by varying the LCST of the
network’s polymeric backbone (Figure 4D). Keeping the same
backbone, rod hydrogels containing 1d exhibit the largest
bending angle and fastest bending speed relative to that of 1b
and 1c since 1d has a higher charge density (SP2−) after
irradiation (Figure 4E and Movie S1). For a given spiropyran
molecule (1b), rod gels containing a polymeric backbone with a
lower LCST exhibit larger bending angles and faster bending
speeds because of the larger expansion of these gels (Figure 4F
and Movie S2). As we have multiple spiropyran molecules and
polymer backbones to choose from, it is possible with these
systems to program a range of bending angles and actuation
kinetics using different combinations of spiropyrans and
polymeric networks. Furthermore, reversible bending of these
NP artificial muscles is highly reproducible through control of
irradiation and pH conditions. Figure 4G shows that the
maximum bending angle is recovered after four bending−
D
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Figure 4. (A) Schematic representation of light-activated artificial muscles mimicking positive (1a) or negative (1b−1d) phototaxis. (B) Photographs
of bending hydrogels containing 1a and a PNIPAM network as a result of the well-known photocontraction in these systems (bending toward the
light). The dashed lines represent the positions before (long) and after irradiation (short) and the numbers indicate the change of height after
irradiation. (C) Photographs of bending hydrogels containing the sulfonated spiropyrans (1b−1d) and a PNIPAM backbone induced by
photoexpansion (bending away from the light). (D) Photographs of bending hydrogels containing 1b and different poly(DEGMAx-co-OEGMAy)
networks. The numbers on the left represent the relative molar ratio of DEGMA and OEGMA. (E) Plot of bending angles as a function of irradiation
time in photoexpanding hydrogels containing different spiropyrans and PNIPAM backbones. (F) Plot of bending angles as a function of irradiation
time for photoexpanding hydrogels containing 1b and poly(DEGMAx-co-OEGMAy) networks with different relative molar ratios of DEGMA and
OEGMA. (G) Plot of changes in maximum bending angles over four light−dark cycles for three different artificial muscles containing 1b and
poly(DEGMAx-co-OEGMAy) networks. The numbers represent the relative molar ratio of DEGMA and OEGMA. The light and dark periods take 40
and 100 min, respectively.
unbending cycles for three different types of NP artificial
muscles.
on photoexpansion, thus allowing its enhancement and fine-
tuning by changing the sulfonate substitution of spiropyran
moieties and the LCST of the expanding network by varying
chemical composition. The novel light-triggered photoexpan-
sion of organic materials reported here will contribute to the
molecular design of synthetic systems able to mimic functions of
living matter such as plant phototaxis and the energy
transduction of mammalian muscles.
CONCLUSION
■
In summary, we have synthesized a series of polymerizable
sulfonated spiropyran molecules and covalently incorporated
them into 3D cross-linked networks. This enabled the novel
observation of negative phototactic behavior as a result of
photoexpansion triggered by visible light. Coarse-grained
simulations suggest that small changes in the chemical structure
of spiropyran moieties in the polymeric network can be used to
tune their interactions with water, which in turn impact directly
on the observed photoexpansion. We also found that exposure of
the systems to photons and pH changes has a synergistic effect
ASSOCIATED CONTENT
■
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* Supporting Information
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/jacs.0c02201.
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AUTHOR INFORMATION
■
Corresponding Author
Samuel I. Stupp − Center for Bio-inspired Energy Science,
Simpson Querrey Institute, Department of Materials Science and
Engineering, Department of Chemistry, Department of
Biomedical Engineering, and Department of Medicine,
Northwestern University, Chicago, Illinois 60611, United States;
orcid.org/0000-0002-5491-7442; Email: s-stupp@
northwestern.edu
Authors
Chuang Li − Center for Bio-inspired Energy Science, Simpson
Querrey Institute, Northwestern University, Chicago, Illinois
60611, United States; orcid.org/0000-0002-1573-5208
Aysenur Iscen − Department of Chemical and Biological
Engineering, Northwestern University, Evanston, Illinois 60208,
United States; orcid.org/0000-0002-9609-4552
Liam C. Palmer − Center for Bio-inspired Energy Science, Simpson
Querrey Institute and Department of Chemistry, Northwestern
University, Chicago, Illinois 60611, United States; orcid.org/
0000-0003-0804-1168
George C. Schatz − Department of Chemical and Biological
Engineering and Department of Chemistry, Northwestern
University, Evanston, Illinois 60208, United States; orcid.org/
0000-0001-5837-4740
Complete contact information is available at:
https://pubs.acs.org/10.1021/jacs.0c02201
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Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
This work was supported by the Center for Bio-Inspired Energy
Science (CBES), an Energy Frontier Research Center funded by
the U.S. Department of Energy (DOE) Office of Basic Energy
Sciences (DE-SC0000989). This work made use of the
IMSERC at Northwestern University, which has received
support from the NIH (1S10OD012016-01/1S10RR019071-
01A1), Soft and Hybrid Nanotechnology Experimental
(SHyNE) Resource (NSF ECCS-1542205), the State of Illinois,
and the International Institute for Nanotechnology (IIN). This
work made use of the MatCI Facility which receives support
from the MRSEC Program (NSF DMR- 1720139) of the
Materials Research Center at Northwestern University. We
acknowledge Mark Seniw for creating schematic illustrations.
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