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Progress in Bioinspired Dry and Wet Gradient Materials from Design Principles to Engineering Applications - PubMed

  • ️Wed Jan 01 2020

Review

Progress in Bioinspired Dry and Wet Gradient Materials from Design Principles to Engineering Applications

Xiaoxiao Dong et al. iScience. 2020.

Abstract

Nature does nothing in vain. Through millions of years of revolution, living organisms have evolved hierarchical and anisotropic structures to maximize their survival in complex and dynamic environments. Many of these structures are intrinsically heterogeneous and often with functional gradient distributions. Understanding the convergent and divergent gradient designs in the natural material systems may lead to a new paradigm shift in the development of next-generation high-performance bio-/nano-materials and devices that are critically needed in energy, environmental remediation, and biomedical fields. Herein, we review the basic design principles and highlight some of the prominent examples of gradient biological materials/structures discovered over the past few decades. Interestingly, despite the anisotropic features in one direction (i.e., in terms of gradient compositions and properties), these natural structures retain certain levels of symmetry, including point symmetry, axial symmetry, mirror symmetry, and 3D symmetry. We further demonstrate the state-of-the-art fabrication techniques and procedures in making the biomimetic counterparts. Some prototypes showcase optimized properties surpassing those seen in the biological model systems. Finally, we summarize the latest applications of these synthetic functional gradient materials and structures in robotics, biomedical, energy, and environmental fields, along with their future perspectives. This review may stimulate scientists, engineers, and inventors to explore this emerging and disruptive research methodology and endeavors.

Keywords: Biomaterials; Materials Design; Materials Structure.

© 2020 The Author(s).

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Graphical abstract
Figure 1
Figure 1

Several Representative Organisms of D-gradient (A) An SEM images and the CLSM maximum intensity projection of a gecko seta. The CLSM image of a single gecko seta shows an overlay image of three different autofluorescences of blue, green, and red, which give off an excitation wavelength of 458, 561, and 633 nm, respectively. The results show that the protein in the seta presents a gradient distribution. The model was established by theoretically analyzing the geckos' friction and adhesion behavior and the schematic of an XY-plane bionic material preparation process (Tian et al., 2006; Zhou et al., 2015; Dong et al., 2020). (B) An SEM image and the CLSM maximum intensity projection of a spatula-like adhesive tarsal setae of the second adhesive pad of a foreleg of a female Coccinella septempunctata. The CLSM images show the tips of beetle's material composition is mainly determined by resilin. The protein resilin decreases toward to the bottom of the beetle (Peisker et al., 2013). (C) Bamboo stems and its SEM images. The cellulose fibers' gradient distribution decreases from the outside to the inside of the bamboo stems. At the bottom of the figure a cross-sectional mathematical model of bamboo culm before and after growth-induced deformation can be seen (Habibi et al., 2015; Silva et al., 2006; Wang et al., 2017b). (D) SEM images of a shell and a sketch of the indentation part of the nacre structure, which present the “brick and mortar” state. The variation of the stiffness of shell-related biocomposites with the aspect ratio of ceramic bricks and volume fraction of ceramic as laid down (Gao et al., 2003; Jiao et al., 2016; Song et al., 2015). (E) SEM images of butterfly wings in the shape of a “Christmas tree” and a 3D symmetrical model (Mejdoubi et al., 2013).

Figure 2
Figure 2

Several Representative Organisms of W-gradient (A) The SEM images of squid beaks and the schematic of the content of histidine-rich proteins decreases from the tip to the base (Fox et al., 2013; Miserez et al., 2008; Tan et al., 2015). (B) The mussel's picture and the SEM image of mussel's byssal plaques and the diameter of pores present a gradient state of plaques. The schematic diagram of Fe3+ ions regulating interactions between positively charged proteins as well as reveals the important role of Fe3+ in mussel thread (Waite, 2017; Lee et al., 2011). (C) The SEM images and the schematic diagram of the Laplace pressure gradient during the water collection process of spider silk (Wang et al., 2016b; Zheng et al., 2010). (D) Cactus and the SEM image of a single spine. Driving force diagram of cactus generated by Laplace pressure gradient and the surface-free energy gradient. Due to the Laplace pressure is relatively small, the water drop on the cone spine should toward the base side with a larger radius (R2) (Ju et al., 2012).

Figure 3
Figure 3

Several Representative Organisms of W-gradient (A) A picture of a water strider resting on water and the SEM image of a small region of its leg. The microstructure of the water strider's legs produces a Laplace pressure difference and can stay on the water for a long time. A schematic model of the water strider floating on water and the cross-section model of the air water interface of a Partially Submerged leg (Zhang et al., 2011; Watson et al., 2010). (B) A pitcher plant and the SEM images of the surface. The Laplace pressure formed by the surface structure is the main reason for the water collection. The modeling for biomimetic slippery surface of Nepenthes alata's slippery zone and the schematic diagram liquid diffusion in the negative direction (−s) and positive direction (+s) (Chen et al., 2016; Yong et al., 2017; Zhang et al., 2015, 2017). (C) A hygroscopically responsive bilayer structures and the SEM images of wheat awns. A picture of wheat awn under wet and dry conditions and an SEM image in the back scattering mode of a section through wheat awn (Shin et al., 2018). (D) The geometry model of pine cone and the deformation diagram. The state of pine cone under wet and dry conditions and their SEM images (Reyssat and Mahadevan, 2009; Lin et al., 2016).

Figure 4
Figure 4

The Models of Gradient Phenomenon Inspired from Organisms (A) Composite in organisms in a gradient state. The addition of composites in a gradient state to material can improve its durability. The main representatives are the gecko and ladybird. (B) Gradient state of brick and mortar structure. This structure can improve the mechanical properties of the design materials and enhance the toughness and strength. The typical organism is a shell. (C) The pore structure inside the organisms' present gradient. The gradient distribution of pore structure provides the impetus for the growth of organisms, such as bamboo and mussels. (D) The gradient microstructure with a Christmas tree shape. This is a structural model for butterflies' wings, which are reflective and hydrophobic. (E) Hierarchical gradient structure. The different density of each layer can make the structure have deformation characteristics under certain circumstances, such as wheat awns. (F) Two or more ions in organism present a gradient. Through the REDOX reaction between different ions, the designed material has specific functions like self-healing ability.

Figure 5
Figure 5

The Hierarchical Structure of Nature Animals (A) Hierarchical structures of a Tokay gecko, including optical images of a Tokay gecko, its foot, and its toe; SEM images of a setal array, spatula pads, and a magnified view of a spatula pad (Yu et al., 2011). (B) Rational, design, and fabrication of a wet/dry hybrid nano adhesive (Lee et al., 2007). (C) Schematic diagram of carbon nanotube modifications with polydopamine (Li et al., 2019). (D) Schematics of vertical aligned CNT arrays with laterally distributed CNT segments adhering on a target surface; FEA model for simulating the macroscopic adhesive behaviors of vertical aligned CNT arrays and a snapshot of a lateral CNT being peeled from substrate in molecular dynamics (Hu et al., 2012). (E) Schematic diagram of the self-healing principle of a mussel thread (Xu et al., 2019). (F) Schematic diagram of a polymer system of a mussel adhesive protein simulation (Lee et al., 2002; Brubaker et al., 2010).

Figure 6
Figure 6

Examples of Fabrication Artificial Gradient Structure Materials (A) Schematic representation of individual polyelectrolytes in solution, poly-His−polyAsp and poly-His−polyGlu complexes in solution, polyHis−polyAsp LbL and polyHis−polyGlu Layer-by-Layer (Tan et al., 2013). (B and C) (B) The picture of a Humboldt squid Dosidicus gigas and the optical image of the fabricated ChitoDX film (the left). The brief reaction scheme where L-dopa is oxidized and covalently cross-links with chitosan (the right) (Zhang et al., 2016). (C) The schematic of water-enhanced mechanical gradient nanocomposite and the film casting and photo-cross-linking process (Fox et al., 2013). (D) Synthetic strategy of chitosan derived bioinspired organic/inorganic composites (Zvarec et al., 2013). (E) Schematic diagram of fabrication process of bionic butterfly wings. (F) The SEM image of SiO2 inverse replica to bionic butterfly wings (Han et al., 2013).

Figure 7
Figure 7

Examples of Artificial Structures with Gradient Properties can Exhibit Motion Characteristics when Performing Their Function (A) Schematic illustration of capillary microfluidic system for generating the microfibers containing droplets (Wu et al., 2018b). (B) Anatomy of the silk-spinning system of spiders (Kang et al., 2011). (C) Photograph of the supercontractile fiber and schematic illustration of SCF undergoing supercontraction at high humidity (Wu et al., 2018a). (D) Synthesized branched wire structures (Heng et al., 2014). (E) Schematic diagram of an electrothermal and shape-memory graphene sponge with specific wettability (Wang et al., 2017a). (F) Schematic showing reversible unidirectional water spreading on the smart artificial peristome (Zhang et al., 2017). (G) Design and fabrication of the biomimetic film (Tang et al., 2018). (H) The present strategy of utilizing the geometry-gradient's slippery surface to directionally transport gas bubbles in an aqueous environment (Zhang et al., 2018).

Figure 8
Figure 8

Examples of Bionic Smart Surface Inspired from Pitcher Plant (A) A flower made of paper-plastic double petals by mimicking the pine cones. It closes in the dry air and opens in the water (Reyssat and Mahadevan, 2009). (B) Diagrams about principle of the blocking force measurement on a pine cone and a bicomposite analogue. The force produced due to the difference in the coefficient of active and passive layers (Le Duigou and Castro, 2016). (C) The variation of contact angles and sliding angles of the surface of bionic pine cone for different anodization times (Li et al., 2016). (D) Spatial distribution robots of a bionic pine cone in relative humidity and velocity images of humidity robots of different lengths (Shin et al., 2018).

Figure 9
Figure 9

Tissue Engineering and Regenerative Medicine (A) Preparation of gradient hydrogel constructs for microscopic observation (Wei et al., 2017). (B) Confocal images of the entire view of encapsulated KIA-GFP cells (Wei et al., 2017). (C) The fabrication of gradient structure for shape and water and heat transportation (Song et al., 2020). (D) The multigradient targeting microbubble system for tumor diagnostics and therapy (Duan et al., 2016).

Figure 10
Figure 10

Examples of Devices with Gradient Structure and Multifunctions in Energy Field (A) The schematic illustration of the preparation, optical image, cross-section SEM image, and magnified SEM image of the gradient-layered BaTiO3NWs/p(VDF-HFP) nanocomposities. (B) The relationship between the discharge energy density, charge-discharge efficiency of the gradient layer BaTiO3NWs/p(VDFHFP) nanocomposite, and the BaTiO3 content in the intermediate layer. (C) Schematic diagram of the gradient crosslinked structure of a squid beak and the biomimetic free-standing and highly CCNA with gradually crosslinking structure. (D) The specific capacitances under increasing compressive strains of CCNA. (E) The application of CCS prepared based on CCNA as a sensor. Apply a small pressure of 30 KPa on the flexible integrated watchband to light up the green LED, apply a medium pressure of 55 KPa to light up the blue LED, and apply a high pressure of 80 KPa to light up the red LED. And the relative capacitance response obtained from CSS during compression.

Figure 11
Figure 11

Examples of Devices with Gradient Structure in Environmental Applications (A) Schematic diagram of enzyme immobilization and catalytic process and dead-end filtration equipment. (B) Schematic diagram of lecithin modification and enzyme immobilization on the membrane. (C) The overall schematic diagram of the bottom-up fabrication strategy of nacreous nanocomposite and the schematic diagram of each part of the finished interface. (D) The enhanced ratio of specific strength of the prepared nacreous bulk nanocomposite. (E) A process diagram of bioinspired hierarchical helical nanocomposite macrofibers are made by combining a facile wet-spinning process with a subsequent multiple wet-twisting procedure.

Figure 12
Figure 12

Examples of Gradient Structure in Robot Fields (A) Schematic diagram of a wheat-awns-inspired robot. The principle in the picture shows the ratcheting of two legs attached to a bilayer actuator. (B) Schematic diagram of the designed robot driven by environmental humidity. (C) The schematic of the reversible moisture-responsive movements and the cross-section region of the pine cone. (D) The schematic diagram of the actuator with the oriented microchannels by laser etching and the schematic diagram of the actuator under the oil response. (E) Schematic diagram of the prepared artificial quadrilateral windmill driven in response to oil.

Figure 13
Figure 13

Examples of a Fully Soft with Gradient Structure which can be Trigger by Environmental Humidity or Electroheating (A) Schematic diagram of the changes of the actuator under a different relative environmental humidity of 23°C. (B) The schematic diagram of surface gradient energy in biological recovery and the movement of a soft robot on the surface inspired by the beetles. (C) The gradient structure of bamboo and the distribution of internal fibers, as well as the SEM image of MXenes of the bionic bamboo structure. (D) Moisture-absorbing actuator model diagram of the G-MXCP actuator and MXene/CNF/PDA/BOPP double-layer actuators with different mechanical adaptability.

Figure 14
Figure 14

Applications Prospect of Bionic Gradient in the Future, such as Artificially Intelligent, Environmental Friendly, Sustainable Materials

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