Robust magnetic double-network hydrogels with self-healing, MR imaging, cytocompatibility and 3D printability

Article abstract of DOI:10.1039/c9cc04241e

Herein, we have fabricated a novel robust self-healing magnetic double-network hydrogel by multiple interactions between bondable magnetic Fe₃O₄ and chitosan-polyolefin matrix, and the hydrogel also exhibits an excellent magnetogenic effect and MR imageability. The practical potential of the magnetic double-network hydrogel is further revealed by its 3D-printing performance.

Full text of DOI:10.1039/c9cc04241e

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Conformational control of nonplanar free base porphyrins:
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Robust magnetic double-network hydrogels with self-healing, MR
imaging, cytocompatibility and 3D printability
Fangli Gang,a,b Hao Yan,d Chunyang Ma,b Le Jiang,b Yingying Gu,e Ziyu Liu,e Lingyun Zhao,b,c Xiumei
Received 00th January 20xx,
Accepted 00th January 20xx
Wang,b,c Jiwen Zhang,*a and Xiaodan Sun*b,c
DOI: 10.1039/x0xx00000x
Herein, we have fabricated a novel robust self-healing magnetic the extracellular matrix, which can effectively dissipate
double-network hydrogel by multiple interactions between energy.18-21 The general method of preparing robust magnetic
bondable magnetic Fe3O4 and chitosan-polyolefin matrix, and the DN hydrogels is to physically disperse magnetic particles (Fe2O3,
hydrogel also exhibits excellent magnetogenic effect and MR Fe3O4) in the hydrogel matrix, resulting in uneven network
imageability. The practical potential of the magnetic double- structure and poor mechanical properties, due to the easy
network hydrogel is further revealed by their 3D-printing agglomeration of the nano-filler particles.22-24 Furthermore,
performance.
magnetic hydrogels with high strength usually do not have good
26
self-healing25,
and compatibility. Therefore, designing a
Functional composite material made of nanoparticles with
unique optical, electrical and magnetic properties and
hydrogels can realize the functions of image monitoring,
controlled drug release and multi-modal combination therapy,
after implantation in vivo.1-8 Therefore, they have attracted
wide attention in the field of biomedicine. In recent years,
magnetic hydrogels, which are composed of magnetic particles
and hydrogel matrix, have developed rapidly because of their
magnetic hydrogel with multiple functions remains a big
challenge.
Herein, we report a novel robust magnetic nano-Fe3O4
composite polyolefin-chitosan (AAD-CS-Fe) double network
hydrogel with multiple functions (Scheme 1). Fe3O4
nanoparticles about 40~50 nm synthesized following an
improved solvothermal method27 (Fig. S1) have relatively few
surface groups and have been proven very suitable for in situ
surface coating and in situ reaction.28, 29 Then, magnetic nano-
Fe3O4 was treated with HCl solution (pH≈1) to expose more Fe
ions as bonding sites (Scheme 1a), and coordinated with
different carboxyl group/hydroxy group in AAD terpolymer,
thus improving the dispersion of magnetic particles in hydrogels
(Fig. S2). Subsequently, one-step amidation reaction of acryloyl
chloride with dopamine hydrochloride gives a dopamine
acrylamide (DAm) for the synthesis of a polyolefin polymer
chain (Scheme 1b), with the aim of increasing the cell affinity of
the hard hydrogel. Finally, AA, AM and DAm monomers were
chemically polymerized by APS in the presence of chitosan and
nano-Fe3O4, to form a physically and chemically crosslinked
polyolefin-chitosan double network hydrogel (Scheme 1c). The
synthesized hydrogels were immersed in saturated NaCl
solution to increase the physical entanglement between
chitosan molecular chains by forming intermolecular
aggregation, which further enhances the mechanical properties
of the hydrogels.30
13
promising applications in drug release,9-11 actuators,12,
photonic crystals14, 15 and biomedical engineering.16, 17 Despite
extensive research into the development of magnetic
hydrogels, only a few studies have attempted to capture other
functional properties, such as high mechanical strength and
self-healing. The development of magnetic hydrogels with self-
healing and high mechanical strength is of great significance for
the development of biomedical fields such as tissue
engineering, cancer treatment and medical device.
Double network (DN) hydrogels are emerging to enhance
the mechanical performance of conventional hydrogels due to
its rigid-flexible structure resembling collagen-proteoglycans in
a. College of Chemistry & Pharmacy, Shaanxi Key Laboratory of Natural Products &
Chemical Biology, Northwest A&F University, Yangling, Shaanxi, 712100, China
b. State Key Laboratory of New Ceramics and Fine Processing, School of Materials
Science and Engineering, Tsinghua University, Beijing,100084, China.
c. Key Laboratory of Advanced Materials of Ministry of Education of China, School of
Materials Science and Engineering, Tsinghua University, Beijing 100084, China.
d. Harvard Medical School and Wellman Center for Photomedicine, Massachusetts
General Hospital, 50 Blossom Street, Boston, MA 02114, USA.
Taking advantages of rigid-flexible coordinated DN
architecture and synergistic effect including the coordination of
Fe ion on the surface of the nanoparticle with the carboxyl
group/hydroxyl group, hydrogen bonds and π-π stacking, the
AAD-CS-Fe DN hydrogel exhibited uniform porous network
e. Division of Surgery and Interventional Science, University College London, Gower
Street, London, UK.
†Electronic Supplementary Information (ESI) available: Experimental procedures
and supporting figures. See DOI: 10.1039/x0xx00000x
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healed gel had no obvious cuts and can bear stretching without
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DOI: 10.1039/C9CC04241E
Scheme 1 Schematic strategy of the design of nano-Fe3O4
composite double-network hydrogels. Chemical synthesis of a)
hydrochloric acid etched nano-Fe3O4; b) DAm; c) AAD
terpolymer. d) Illustration of nanocomposite DN hydrogel.
Hydrogen bonds were displayed in rectangular dashed boxes,
while ions coordination in circular dotted box and π-π stacking
in hexagonal dotted box.
Fig. 1 Characterization of the hydrogels. a) SEM images of the
internal microstructures of the hydrogels at different
concentrations of Fe3O4 nanoparticles in water. I) 0 mg·mL-1; II)
16 mg·mL-1. b) Compressive strength and compressive moduli
of different hydrogels. c) The storage modulus (G′) of different
hydrogels in the frequency range of 0.01 to 10 Hz at 1.0% strain
amplitude. d) Tensile strength and tensile elongation of
different hydrogels. e) Swelling ratio (g/g) of various hydrogels
at different time points in PBS. f) Self-healing properties of AAD-
CS-Fe DN hydrogel.
structure (Fig. 1a), excellent mechanical properties (Fig. 1b-1e)
and self-healing properties (Fig. 1f). To investigate the
mechanical properties of the AAD-CS-Fe DN hydrogel, a series
of control hydrogels were prepared (Table S1). As shown in Fig.
1b and 1d, the first six DN hydrogel exhibited a compressive
strength of 0.38 to 2.23 MPa, a tensile strength of 54.02 to
421.77 KPa, and a compressive modulus of 0.24 to 2.51 MPa,
which is much higher than that of a SN hydrogel (0.24 MPa,
39.27 KPa, 0.11 MPa). Similarly, the comparison of the storage
modulus (G′) in Figure 1c showed that the SN hydrogel was less
rigid than all DN hydrogels. However, due to the absence of a
rigid network, a SN hydrogel containing only a flexible network
exhibited a greater tensile elongation (234.23%) and a higher
swelling ratio (5.89 g/g). Subsequently, considering the addition
of different iron contents will also affect the mechanical
properties of the hydrogel, we set up several control groups to
verify the effect of iron on the performance of hydrogel,
including AAD-CS without any Fe, AAD-CS-Fe3+ containing Fe3+,
AAD-CS-nano containing nano-iron oxide particles and AAD-CS-
Fe containing HCl-treated nano-Fe3O4. As can be seen from Fig.
1b and 1c, the compressive strength, compressive modulus and
G′ are both AAD-CS-Fe > AAD-CS-Fe3+> AAD-CS-nano > AAD-CS,
indicating that the increase of DN hydrogel strength is due to
the synergistic effect of coordination of Fe ions exposed on the
surface of nanoparticles and nanoparticles themselves. In
addition, the strength of AAD-CS-Fe hydrogel can be adjusted to
a large extent (0.25 MPa to 2.29 MPa) by changing the filling
amount of nano-Fe3O4 particles and the ratio of other
components (Fig. S3). Furthermore, in this work, the self-
healing of the robust magnetic hydrogels is attributed to
multiple dynamic ions coordination bonds between carboxyl or
hydroxyl groups and Fe ions on the surface of nanoparticles, and
hydrogen bonds between various groups (Scheme 1d). As
illustrated in Fig. 1f, the hydrogel was cut into four pieces and
Fig.2 Magnetothermal properties and imageability of AAD-CS-
Fe DN hydrogel containing 16 mg/mL nano-Fe3O4. a)
Macroscopic picture of the magnetic hydrogel under the
attraction of a magnet. b) Heat-induction properties of 0.25 g
Fe3O4-based magnetic hydrogels (8 mg/mL Fe3O4) in 0.5 mL H2O
under AMF with different intensities after 600 s. c) Heat-
induction properties of DN hydrogels with different Fe
concentration under AMF. d) T2-weighted MR images of
hydrogels with different concentrations of nano-Fe3O4.
This ionic coordination on the surface of magnetic nano-
Fe3O4 synergized with hydrogen bonds and π-π stacking
significantly improved the mechanical properties, self-healing
and anti-swelling ability of the composite hydrogel, while
o
immediately re-contacted at 70 C. After contact for 12 h, the
2 | J. Name., 2012, 00, 1-3
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keeping the excellent magnetocaloric effect and MR imaging of
hydrogels entrusted by nano-Fe3O4 (Fig. 2). The magnetic
properties of DN hydrogels are also attributed to the addition
of 50 nm diameter paramagnetic nano-Fe3O4 (Fig. 2a), and its
inductive thermal properties depend on the nano-Fe3O4
dopants at a certain AMF (282 kHz, 180 Oe), generally showing
a dose dependency (Figure 2b). Moreover, the hydrogel
exhibited enhanced heating ability at higher intensity AMF
(Figure 2c). The hydrogel with heat-induction property may be
used in the treatment of tumors and drug-controlled release.27,
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DOI: 10.1039/C9CC04241E
28
Furthermore, the imageable function of the hydrogel also
provides the possibility of "theranostics" after implanting in the
body. As can be seen from the Fig. 2d, the signal enhancement
of the T2-weighted MR image of the hydrogel increases with
increasing Fe3O4 content.
In general, most of reported hard hydrogels have poor cell
affinity and are not conducive to cell adhesion and growth.
Therefore, the addition of propylene dopamine (DAm)
monomer (Scheme 1b) to a robust magnetic DN hydrogel can
effectively improve its cell affinity (Fig. 3). The ability of the
hydrogels to interact with cells was assessed by culturing L929
fibroblasts on the surface of prepared hydrogels.
Representative confocal laser scanning microscopy (CLSM) of
LIVE/DEAD assay and SEM images showed more living cells on
the AAD-Fe and AAD-CS-Fe hydrogels than AA-CS-Fe hydrogel,
indicating that the addition of adhesion-promoting DAm in the
hydrogels facilitated cells-gels favorable interaction. In
addition, the fibroblasts adhered and spread more after CS and
nano-Fe3O4 incorporation, which indicated that formation of
DN hydrogels enhanced the cell affinity of hydrogels. Further
quantitative evaluation of cell proliferation on hydrogels after 3
and 5 days of culture using CCK-8 assay was shown in Fig. 3g.
After 3 days of culture, the DAm-containing hydrogels had
higher cell viability as compared to the DAm-free ones,
evidenced by a greater number of living cells in Fig. 3g,
indicating that DAm promoted cell proliferation during the
initial stage. After 5 d of incubation, L929 cells proliferated on
all hydrogels, and DAm-containing nanocomposite DN
hydrogels have higher cell viability than other component
hydrogels. These results indicated that DAm, nano-Fe3O4 and
double network structures played a key role in promoting cell
adhesion and proliferation on the hydrogels.
The personalized customization of hydrogels or the
construction of complex anatomical structures through 3D
printing can further reveal the practical application potential of
robust magnetic hydrogels in biomedical fields.33-37 However,
the printing of hydrogels is often limited by the inability to form
quickly after extrusion, so the approach we take was to print the
gel in a pre-solution of a saturated sodium chloride solution
containing APS. A video (Movie S1) of DN hydrogel printing was
provided in the Supporting Information. The 3D printing process
was as follows: in the first step, the AAD-CS-Fe DN hydrogel
containing 8 mg/mL nano-Fe3O4 precursor without APS was
prepared in the needle tube. Afterwards, a saturated sodium
Fig.3 Cytocompatibility of the various hydrogels. Representative
CLSM images of LIVE/DEAD assay and SEM images of L929 on a,
d) AA-CS-Fe hydrogel; b, e) AAD-Fe hydrogel; and c, f) AAD-CS-
Fe hydrogel. g) Cell proliferation on hydrogels after 1, 3 and 5
days of culture. * represents statistical significance (p < 0.05).
Fig. 4 3D Printing preparation and characterization of AAD-CS-
Fe DN hydrogel containing 8 mg/mL nano-Fe3O4. a) 3D model of
the DN hydrogel in the pre-solution just after printing. b) 3D
printed various shapes. Quadrangular pyramid, left ear,
hexagonal prism, cuboid, nose, letters, octopus (from left to
right, from top to bottom). The height of the corresponding
models is shown in the red box.
chloride solution containing APS was prepared as a pre-solution
to receive the gel. After printing, the models were stabilized in
the pre-solution for several hours and rinsed with deionized
water. Fig. 4 demonstrates the various custom shapes of the 3D
printed DN hydrogel. Quadrangular pyramid and hexagonal
prism presented printing of objects or scaffolds with uniform
holes. Cuboid and letters showed printing of objects with high
vertical aspect ratios. Left ear, nose and octopus demonstrated
the ability to print complex structures with overhangs and high
vertical aspect ratios. 3D printing is often used in biomedical
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8. M. L. Xu, L. Y. Guan, S. K. Li, L. Chen and Z. Chen, Chem. Commun.,
applications to print anatomical complex structures that are not
cut by scalpels. In order to be used in vivo, the printed hydrogel
scaffold should not lose its shape and strength after being
soaked in water for a long time. In Fig. 4b, there was no obvious
change in the morphology of DN hydrogels in the deionized
water for 24 h.
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2019, 55, 5359-5362.
DOI: 10.1039/C9CC04241E
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In summary, a combination of chitosan-polyolefin double
network hydrogel and bondable magnetic nano-Fe3O4 were
employed to meet the excellent mechanical properties, self-
healing and cytocompatibility of magnetic hydrogel. Fe ions are
exposed as bonding sites on the surface of magnetic Fe3O4
etched by HCl to ionic coordinate with different carboxyl
groups/hydroxy groups, which increased the dispersion of
Fe3O4 in hydrogels. This ionic coordination synergized with
hydrogen bonds and π-π stacking to improve the mechanical
properties, self-healing and anti-swelling ability of magnetic DN
hydrogels, while keeping the excellent magnetocaloric effect
and MR imaging of hydrogels entrusted by nano-Fe3O4.
Moreover, the dopamine acrylamide (DAm) monomer in the
AAD triblock copolymer gives the hydrogel better cell affinity
and self-healing. Changes in the Fe3O4 content and composition
ratio leads to the controllability of the hydrogel strength with
good cytocompatibility. Notably, to demonstrate the potential
of the robust magnetic hydrogel implantation in vivo, several 3D
printing anatomical structures was constructed. Considering
the magnetism performance pairing with high-strength (>2
MPa), self-healing, cytocompatibility, MR imaging and 3D
printability, the developed hydrogel offers superior
functionalities than previously reported.
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This work was supported by Intergovernmental
cooperation in science and technology [2016YFE0125300]; the
National Key Research and Development Program of China
[2016YFB0700802]; Major projects of the National Social
Science Funding (17ZDA019); the National Natural Science
Foundation of China (81671829); Tsinghua University Initiative
Scientific Research Program (2017THZWYX07).
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There are no conflicts to declare.
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