A Printable Magnetic-Responsive Iron Oxide Nanoparticle (ION)-Gelatin Methacryloyl (GelMA) Ink for Soft Bioactuator/Robot Applications

Abstract

The features or actuation behaviors of nature's creatures provide concepts for the development of biomimetic soft bioactuators/robots with stimuli-responsive capabilities, design convenience, and environmental adaptivity in various fields. Mimosa pudica is a mechanically responsive plant that can convert pressure to the motion of leaves. When the leaves receive pressure, the occurrence of asymmetric turgor in the extensor and flexor sides of the pulvinus from redistributing the water in the pulvinus causes the bending of the pulvinus. Inspired by the actuation of Mimosa pudica, designing soft bioactuators can convert external stimulations to driving forces for the actuation of constructs which has been receiving increased attention and has potential applications in many fields. 4D printing technology has emerged as a new strategy for creating versatile soft bioactuators/robots by integrating printing technologies with stimuli-responsive materials. In this study, we developed a hybrid ink by combining gelatin methacryloyl (GelMA) polymers with iron oxide nanoparticles (IONs). This hybrid ION-GelMA ink exhibits tunable rheology, controllable mechanical properties, magnetic-responsive behaviors, and printability by integrating the internal metal ion-polymeric chain interactions and photo-crosslinking chemistries. This design offers the inks a dual crosslink mechanism combining the advantages of photocrosslinking and ionic crosslinking to rapidly form the construct within 60 s of UV exposure time. In addition, the magnetic-responsive actuation of ION-GelMA constructs can be regulated by different ION concentrations (0-10%). Furthermore, we used the ION-GelMA inks to fabricate a Mimosa pudica-like soft bioactuator through a mold casting method and a direct-ink-writing (DIW) printing technology. Obviously, the pinnule leaf structure of printed constructs presents a continuous reversible shape transformation in an air phase without any liquid as a medium, which can mimic the motion characteristics of natural creatures. At the same time, compared to the model casting process, the DIW printed bioactuators show a more refined and biomimetic transformation shape that closely resembles the movement of the pinnule leaf of Mimosa pudica in response to stimulation. Overall, this study indicates the proof of concept and the potential prospect of magnetic-responsive ION-GelMA inks for the rapid prototyping of biomimetic soft bioactuators/robots with untethered non-contact magneto-actuations.

Keywords: DIW printing; gelatin methacryloyl (GelMA); iron oxide nanoparticles (IONs); magnetic-responsive materials; soft bioactuators/robots.

Figure 1

Schematic illustration of ION-GelMA inks for applications in biomimetic soft bioactuators/robots. Representation of the synthesis of (a) GelMA and (b) IONs, and (c) the fabrication of printed biomimetic mimosa pudica-like magnetic-responsive bioacutaors.

Figure 2

Characterization of IONs and ION−GelMA hydrogels. (a) The TEM image shows the IONs with a nanoscale size. (b) The XRD spectrum confirmed the synthesis of IONs with a typical ION X-ray diffraction pattern. (c) The FTIR spectrum shows the characteristic peaks of the functional groups of GelMA polymers, ION−GelMA inks, and IONs. (d) The compressive modulus of GelMA hydrogels in the absence or presence of alginic acid after UV crosslink. * denotes a significant difference (p < 0.05) between the two groups. (e) The optical images show the ION−GelMA hydrogels with different ION concentrations after UV crosslink and the treatment of calcium chloride solution. (f) The SEM images indicate the ION morphology in the cross-section of ION−GelMA hydrogels.

Figure 3

(a) Optical images of the magnetic field-induced movement process of ION-GelMA hydrogels with different ION concentrations. (b–d) The compressive modulus, mass loss percentage, and swelling ability of ION-GelMA hydrogels with different ION concentrations after 60 s of UV treatment. (*: comparison with 0% group, p < 0.05; **: comparison with 0% group, p < 0.01; #: comparison with 3% group, p < 0.05; &: comparison with 5% group, p < 0.05; @: comparison with 7.5% group, p < 0.05).

Figure 4

Evaluation of injectability and printability of ION-GelMA inks. (a) The effect of ION concentrations on the shear-thinning behavior of ION-GelMA inks. (b) The injectability testing of ION-GelMA inks with different ION concentrations shows the inks with a rapid gel-fluid transition behavior. (c) The optical images and (d) the semi-quantified printability of a printed grid pattern made from ION-GelMA inks. (e) The printed patterns (i.e., spiral, square-spiral, and dragonfly) of 5% ION-GelMA ink through an extrusion 3D printer.

Figure 5

Evaluation of the magnetic-responsive actuation behavior of printed ION-GelMA constructs. (a) The optical images of printed 2D ION-GelMA lattice and cross-in-square shapes under a magnetic actuation process show the shapes with a transformation ability. (b) The bioactuation mechanism of Mimosa pudica. The schematic figures of the fabrication of ION-GelMA Mimosa pudica-like constructs through the (c) mold-casting method and (d) DIW printing technology. The optical images of (e) mold-cast and (f) printed ION-GelMA biomimetic Mimosa pudica-like constructs under a magnetic actuation process indicated the Mimosa pudica-like constructs with a magnetic-responsive actuation behavior. All scale bar = 1 cm.