Biomimetic Nanomaterials: Comparison
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Please note this is a comparison between Version 2 by Jason Zhu and Version 1 by Tatiana Zimina.

Biomimetic nanomaterials (BNMs) are functional materials containing nanoscale components and having structural and technological similarities to natural (biogenic) prototypes. Despite the fact that biomimetic approaches in materials technology have been used since the second half of the 20th century, BNMs are still at the forefront of materials science. “Biomimetics” is a concept introduced in 1957 by Otto Schmitt that, generally, means the imitation of structures, characteristics, models, and compositions of natural objects to solve various problems. The word “biomimetic” comes from the Greek word “bios” (life) and the suffix “mimetic” (mimicry). This concept also includes approaches and processes mimicking biological or natural ones such as, for example, the synthesis of nanomaterials or nanostructures that reproduce the physicochemical, mechanical, and biological properties of natural (biogenic) materials at the nano- or macroscale. Similar to the formation of biogenic materials, the technology of biomimetic materials includes the processes of self-assembly and interfacial molecular recognition. Other important directions of development for such materials are biopolymers and biocomposites, which are receiving immense consideration in biomedical and other fields.

  • biomimetics
  • nanomaterials
  • nanoparticles

1. Magnetic Biomimetic Nanomaterials

The biomimetic synthesis approach has been successfully used in the synthesis of magnetic materials ranging from ferrimagnetic Fe3O4 (found in magnetotactic bacteria (MTB)) to hard magnetic alloys (such as FePt and CoPt). The use of protein cages for the synthesis of magnetic BNMs provides a number of unique advantages since such structures are of biological origin and, at the same time, are suitable for scalable production and can also be modified using chemical or genetic engineering approaches to give them a specific chemical or structural functionality [82,83][1][2]. Ten years ago [64][3], the overwhelming majority of publications on the synthesis of magnetic NPs were devoted to physical and chemical methods, while only a small part of the works was related to biological methods (using protein constructs, bacteria, or fungi). In recent years, the development of the technology of magnetic BNMs has made it possible to reproduce chains of magnetic NPs similar to those formed in MTBs in a laboratory. Various biomimetic approaches to the synthesis of such chains with optimal properties for biomedical use have been demonstrated [84][4].
One of the studied types of magnetic BNMs is polymer-coated and nonpolymer-coated magnetite NPs obtained using magnetosome-associated MTB proteins [32][5]. When implementing this method, the biomineralization of Fe3O4 is carried out in an oxygen-free aqueous solution containing the recombinant magnetosome protein, usually for 30 days. Such magnetic NPs can be used for photothermia or magnetic hyperthermia, chemotherapy, and enzyme immobilization [32,48,85,86,87][5][6][7][8][9]. It was experimentally established in [32][5] that, when two magnetosome proteins (MamC and Mms6) were used for biosynthesis at once, it was possible to obtain magnetic NPs that were close in shape and size to magnetosome crystals [88][10].
Another option for magnetic BNMs is the use of engineered structures based on bacterial magnetosomes. In this case, magnetosomes are isolated from MTB cells and subjected to purification, followed by biotinylation or encapsulation in an inorganic shell. Such magnetic NPs can be used for contrast enhancement in magnetic resonance imaging, magnetic particle imaging, and magnetic hyperthermia [44,89][11][12].
The construction of magnetic BNMs based on magnetite NPs coated with hydroxyapatite (HAP) is described. The preparation of such constructs is usually carried out by introducing a liquid HAP precursor into a solution containing preliminarily formed magnetite cores.
Integration in a single biomimetic matrix (for example, SiO2) of magnetic NPs and the active substance is possible. Such BNMs can be obtained by the hydrolysis of tetramethyl orthosilicate in the presence of preliminarily obtained magnetite NPs and an enzyme solution. A possible area of application is the development of biocatalysts for targeted enzyme prodrug therapy [37][13].
An analysis of the methods for the synthesis of magnetic BNMs allowed uresearchers to draw the following conclusions. The first group of methods included the introduction of precursors of the HAP biomimetic component into a colloidal solution of magnetic NPs [35[14][15],51], acrylamide and ethylene glycol dimethacrylate copolymerization in the presence of S-naproxen on silica-coated Fe3O4 NPs [90][16], preliminarily prepared Fe3O4 NP incubation in an alkaline dopamine solution [93][17], and the self-assembly of Fe3O4 NPs coated with a hydrophilic polymer into 1D nanochains in water [95][18].
Methods of the second group, from ourthe point of view, were more promising due to the ability to create a material structure similar to natural analogues at the level of individual atoms. They included the biosynthesis of magnetic NPs from oxygen-free solutions containing recombinant MamC in anaerobic conditions [32,48,85[5][6][7][8][9],86,87], magnetite biomineralization using PEGylated human ferritin NPs [52][19], and the silica encapsulation or biotinylation of isolated bacterial magnetosomes [44,89][11][12]. Thus, the methods of the second group made it possible to achieve a combination of the advantages of biogenic magnetic NPs (magnetosomes) and their synthetic counterparts, minimizing the disadvantages of both.

2. Metal and Metal Oxide Biomimetic Nanomaterials

The physical and chemical properties of metal and metal oxide NPs can be controlled by choosing their micro- or nanoenvironments during synthesis. Some of the best-known platforms currently in use, in particular for the biomimetic synthesis of metal oxides, include ferritin, viral capsids, or bacterial cells. These biotemplates provide strictly defined conditions for the formation of NPs and, thus, their narrow distribution in shape and size [96][20]. In addition, such synthetic approaches are of interest due to the development of environmentally friendly NP technology. One of the most discussed approaches is the synthesis of metal NPs using organisms, of which plants are considered the best candidates and are suitable for the scalable production. The growing advantages of using plants and herbs for the biomimetic synthesis of metal NPs has prompted scientists to search for the mechanisms of metal ion biological reduction and to study in more depth the mechanisms of metal NP synthesis in plants [97][21]. Obtaining Ag NPs for the purpose of therapy for multiresistant pathogenic microorganisms can be carried out using plant components. Thus, the preparation of such NPs by the reduction of silver nitrate in an aqueous solution with the addition of extract of Musa balbisiana or Phlomis bracteosa seedlings, as well as Saraca indica leaves, as a reducing agent, has been described [55,98,99][22][23][24].
The development of biomimetic methods for the synthesis of metallic nanomaterials plays an important role in dentistry. In recent years, various approaches have been used to modify the topographical or chemical properties of traditional implant surfaces in order to improve the adhesion of the implant material to bone cells. Changing the surface of a titanium implant makes it possible to stimulate the bone tissue, minimizing the period of osseointegration and ensuring the good transfer of occlusal mechanical loads from the implant to the bone [38][25].
A titanium base with a nanostructured calcium phosphate coating obtained by introducing HAP ceramic particles into a plasma jet directed at the treated Ti surface can be used in dentures [100][26].
One of the areas of application of metallic BNMs is the detection and elimination of natural and synthetic pollutants. Gold, silver, and bimetallic Ag-Au NPs for the purpose of creating sensors for biological substances and research in the field of nanotoxicology were obtained using a biomimetic method in an aqueous solution of gelatin with the successive addition of silver nitrate or hydrogen tetrachloroaurate [39][27].
The new, proposed biomimetic methods for obtaining Au NPs and Ag NPs include the use of “cubosomes”, model cubic nanostructures based on lipid membranes. Such BNMs are obtained through incubating preformed Au or Ag NPs with cubosomes in an aqueous solution [34][28]. The purpose of BNMs based on cubosomes is the targeted delivery of drugs.
Another important direction in the development of BNM technology for use in sensors of biological substances and oncology is the production of metal–organic frameworks (MOFs) [58,101][29][30]. Pt NPs could be synthesized using MOFs prepared using Fe(III)tetra(4-carboxyphenyl)porphine chloride as a template [101][30]. More complex structures, porphyrin Zr-MOFs coated with a cell membrane for the purposes of antiangiogenesis and photodynamic therapy in oncology, were obtained using solution chemistry followed by the deposition of manganese oxide from KMnO4 and camouflaging with a cell membrane [58][29]. Composite sponges of stearic acid do not exhibit good adsorption capacity as compared to MOFs and carbonaceous-material-based sponges. Moreover, they have complex synthesis procedures and difficult oil recovery methods. Azam et al. [102][31] fabricated a composite sponge with hydrophobicity as high as that of stearic acid sponges, as high an oil absorption capacity as that of MOF-based sponges, and excellent reusability of up to 10 cycles utilizing the inherited properties of MOFs (i.e., high surface area, controllable pore size, and chemical functionality at the molecular level), the nonwetting and superhydrophobic property of stearic acid, and the regular 3D skeleton of a highly porous polyurethane sponge.
The reseauthorchers of [103][32] explored the use of MOFs formed using the self-assembly of metal ions and organic building blocks to safeguard collagen integrity in the functional dentin matrix. They demonstrated that collagen fibrils (from demineralized human dentin) could induce the biomimetic growth of MOF crystals as protective coatings to strengthen and stabilize the fibrils. Chen et al. [104][33] focused on the recent progress in biomimetic MOF catalysts. The reseauthorchers summarized principles and strategies for the design and synthesis of biomimetic MOF catalysts, discussed structure-related catalytic properties, and particularly addressed important factors, including (1) active sites, (2) microenvironment, (3) transmission channels, and (4) co-catalytic sites, on the distinct catalytic properties of biomimetic MOFs. In addition, some examples have been given to illustrate the synergistic catalysis between multiple factors that are closely related to enzymatic catalysis. It is highly desirable, yet remains challenging, to achieve the synergy of specific functions between MOF host and guest species. Cheng et al. [105][34] obtained a novel MOF composite biomimetic structure inspired by a natural multienzyme system and based on the co-encapsulation of glucose oxidase and L-arginine into Cu-MOFs with Fenton-like catalytic activity to achieve a synergistic antibacterial effect. A facile strategy to prepare a biomimetic cascade reaction system by combining the advantages of enzyme immobilization and biomimetic catalysis in a one-pot reaction system based on a hierarchically porous metal–organic framework was reported [106][35].
MOFs are ideal candidates for building biomimetic systems because their uniform cavities can generate a high density of biomimetic active centers. In addition, thermally and chemically stable MOFs can be built with a variety of metal clusters. Furthermore, the channels of MOFs provide confined pockets, which protect the catalytic centers and enhance substrate specificity [107][36]. Liang et al. [108][37] reported that a wide range of biomacromolecules, including proteins, DNA and enzymes, could efficiently induce MOF formation and control the morphology of the resultant porous crystal via a biomimetic mineralization process under physiological conditions. The reseauthorchers demonstrated that the biomimetic mineralization of MOFs formed a nanoporous shell, which encapsulated the biomacromolecules and afforded unprecedented protection from biological, thermal, and chemical degradation with the maintenance of bioactivity.
Singh et al. [109][38] proposed a protective framework offering thermal stability especially for vaccines wherein additives and stabilizers alone may not be sufficient. The reseauthorchers applied an MOF biomimetic mineralization technique for live viral vaccine encapsulation. This is a ubiquitous stabilization technology that is a simple, rapid, and one-step scalable approach using cost-effective ingredients and ambient aqueous conditions. Water-stable Fe(III)-based MOFs, which exhibit intrinsic peroxidase-like activities, catalyzing the oxidation of 3,3′,5,5′-tetramethylbenzidine and o-phenylenediamin when H2O2 served as the oxidant, were constructed and characterized [110][39]. Their catalytic performances strongly relied on pH value, temperature, catalyst dosage, and H2O2 concentration. Compared to natural enzymes, peroxidase mimetics had the advantages of low cost, ease of preparation and storage, greater resistance to biodegradation, and less vulnerability to denaturation. The presented results could provide a possibility of building MOF-based platforms as enzymatic mimic catalysts and could facilitate their utilization in immunoassays and biotechnology. With a reactivity that mimicked the activity of an enzyme, the MOF-based material also catalyzed the isotopic exchange of oxygen between water and carbon dioxide. Wright et al. [111][40] provided convincing evidence that the metal nodes in MOFs had high structural fidelity with respect to the active sites of enzymes.
Ma et al. [112][41] designed a renewable, inexpensive, and easy-to-assemble filter prepared by growing an MOF on wood, followed by high-temperature carbonization. The proposed filter demonstrated a superior dye removal performance and was expected to replace commercial activated carbon and to be successfully applied in practical wastewater treatment fields. The effect of a peptide or protein sequence on the biomimetic mineralization of zeolite imidazolate frameworks (ZIFs), as well as a general approach to make peptide@ZIFs via a biomimetic mineralization process, was investigated [113][42]. The reaction rate of peptide@ZIF formation was compared for different types of peptides with different isoelectric points. Wang et al. [114][43] developed a new MOF–poly(amidoxime) composite membrane with a permeable macroporous structure, good mechanical properties, and high efficiency for uranium extraction from seawater. Cancer-cell-membrane-coated, triphenylphosphonium-decorated nano-MOF constructs were synthesized to achieve homologous mitochondria-targeted sonodynamic therapy efficacy in combination with simultaneous delivery of the Toll-like receptor agonist R837 as an immune adjuvant [115][44].
For classical, well-developed BNMs based on metal particles and metal oxides, reduction from precursor solutions is most often used as a method. Nevertheless, in recent years, a newer class of BNMs including metal components has been developed rapidly in the form of MOFs. The wide perspectives of this class of materials are mainly due to its multifunctionality, including antiangiogenesis and photodynamic therapy [58][29]; biosensing [101][30]; sonodynamic therapy and immune checkpoint blockade immunotherapy [115][44]; protection from biological, thermal, and chemical degradation with the maintenance of bioactivity [108][37]; antibacterial therapy; and biomimetic catalysis [106][35]. Nevertheless, the technology of MOFs and, especially, composite BNMs containing MOFs is still challenging [104][33].
This may be due, from ourthe point of view, not only to the chemical natures of the oxide and metal components of BNMs, but to the differences in the main claimed applications of these materials, as shown later in Section 5.

3. Organic, Ceramic, and Hybrid Biomimetic Nanomaterials

BNMs based on organic and ceramic components are by far the most widely represented compared to the two groups of BNMs described above. When obtaining BNMs based on organic components, molecular mechanisms for constructing proteins and peptides can be used, which control the synthesis of nanosized objects and the self-assembly of systems of multifunctional materials of a higher order. For this, solid-binding peptides are used, and the formation, assembly, and organization of functional nanoobjects are controlled [119][45]. Protein- and peptide-based biomimetic mineralization has been shown to be an efficient and promising strategy for the synthesis of magnetic and ceramic NPs. Proteins or peptides can bind metal ions through various metal-binding sites, such as N-terminal amines or multi-metal binding sites, and thus, their unique structures allow them to be used as NP growth templates [120][46]. A new class of biomimetic polymers is peptoids (or poly-N-substituted glycines), which are perceived due to highly efficient synthesis, high chemical stability, resistance to enzymatic hydrolysis, and biocompatibility. Due to their properties, amphiphilic peptoids are considered as customizable building blocks for obtaining BNMs with hierarchical structures and specified functionalities [121][47].
The development of ceramic BNM technology is largely aimed at creating scaffolds that mimic natural tissue and reproduce its properties, such as composition and microstructure. In particular, for bone tissue engineering, this is most often achieved by fabricating highly porous ceramic structures that resemble cancellous bone. These scaffolds possess many important properties, including biological activity, space for cells, and ingrowth of new tissues, as well as acceptable mechanical strength. However, when using such scaffolds, the new tissue is often disorganized and has poor mechanical properties [122][48]. The formation of three-dimensional tissue in the laboratory is highly dependent on the biomimetic environment, engineered extracellular matrix, and cell type, as well as biologically active components. Scaffolds should resemble the structural and biochemical features of the natural extracellular environment in order to support and control cell migration and growth [123][49]. In addition to being used in solving tissue-engineering problems, biomimetic ceramic scaffolds are often loaded with various therapeutic molecules to increase their biological effectiveness [124][50]. The peptide-mediated remineralization of artificially induced tooth lesions and the characteristics of orientation, formation, and composition of a newly formed enamel-like apatite layer were experimentally evaluated. Amelogenin was used as a model peptide [41,125][51][52].
A biomimetic design of light, high-temperature ceramics based on functionally differentiated structures was proposed. Such structures can be found in nature, in particular, on cross-sections of the bones, teeth, and stems of many plants, such as bamboo. Originally conceived for spacecraft heat shields, functionally differentiated structures are finding more and more applications in other areas, including biomedicine [126][53]. Researchers are attracted by the hierarchical structure of nacre, which contains at least six levels of hierarchy in the size range from a few millimeters to ~100 nm. In addition, the biomineralization of nacre is carried out by the self-assembly of elementary units under mild conditions at ambient temperature and either neutral or physiological pH, always in an aquatic environment [127][54]. For the production of bioactive orthopedic biomaterials using biomimetic nanocrystalline apatites, several approaches have been used, among which are in situ formation, which allows obtaining a highly reactive structure, and low-temperature molding [128][55]. Biomimetic ceramics of complex shapes can be obtained on the basis of self-forming, two-layer microstructures based on aluminum oxide. Such a material is produced by the repeated coagulation of a suspension of Al2O3 NPs with a ferrofluid under the action of a magnetic field, followed by high-temperature annealing [36][56].
A promising object of research is biomimetic catalysts based on chiral nanomaterials, which can cause the same biological effects as natural catalysts and has demonstrated high efficiency in biological applications [129][57]. The biomimetic synthesis of materials and the template growth of inorganic or hybrid networks using self-assembling, hybrid, organic–inorganic interfaces are also of considerable interest to researchers since artificially obtained hybrid materials lie at the junction of the organic, inorganic, and biological worlds [130][58].
Fatima et al. [9][59] obtained a composite based on bacterial cellulose waste modified with bioactive plant extract. The material showed high bactericidal activity against S. aureus and produced a clear inhibition zone, whereas negligible activity was observed against E. coli, indicating its bactericidal activity mainly against Gram-positive bacteria. Overall, their study illustrated that there is a huge potential for developing valuable biomaterials from food wastes and utilizing their liquid-holding capabilities for value-added applications in the medical and pharmaceutical fields. Chen et al. [131][60] reported a bamboo–nigrosine–poly(N-isopropylacrylamide) composite hydrogel actuator capable of complex deformations and near-infrared light response based on bamboo sheets. The simple and rapid ultraviolet in situ polymerization method closely connected bamboo and hydrogel so that the composite hydrogel actuator was difficult to peel off during the actuation process. In addition, the composite hydrogel actuator exhibited diverse shape deformations because of the natural anisotropy of the bamboo sheets. A composite thermoresponsive actuator with multifunctional actuation upon an alternative magnetic field was fabricated [132][61]. Fe3O4-NP-embedded thermoplastic polyurethane film and a photo-crosslinkable electrospun fibrous poly(N-isopropylacrylamide) mat formed the bilayer actuator.
The removal of systemically administered bacterial toxins could be accomplished using anisotropic polymeric NPs camouflaged with an erythrocyte membrane. Spherical particles of poly(lactic acid-glycolic acid) (PLGA) were immobilized on a film of polyvinyl alcohol and glycerol mechanically stretched to change the shape of the NPs from isotropic to anisotropic, and then erythrocyte membranes were deposited with an ultrasonic treatment [33][62].
Important areas of application for polymeric NPs camouflaged by cell membranes are bioimaging, phototheranostics, and the development of nanovaccines. NPs of PLGA with tumor cell membrane envelopes could be obtained by depositing the drug in PLGA using precipitation from a solution, followed by coating with a cell membrane [45][63].
As well as metal NPs (see Section 4), more complex NPs can be obtained biomimically using plant extracts as sources of natural reducing agents and stabilizers. Thus, Ag–TiO2 NPs were obtained through sonochemical synthesis using Origanum majorana leaf extract as a restoring and stabilizing agent, which could be used for antibacterial and antioxidant therapy [40][64].
Much attention from BNM researchers has been paid to works in the field of dentistry, primarily to the restoration of demineralized tooth enamel. One of proposed approaches is amelogenin-containing chitosan hydrogel [133,134][65][66]. The preparation of this material is carried out by the mixing of a solution of chitosan, calcium chloride, and recombinant porcine amelogenin, followed by mechanical agitation. Li et al. used HAP crystallized with a polyamidoamine (PAMAM) dendrimer template [135,136,137][67][68][69]. The treated tooth enamel was placed in a solution containing CaCl2, KH2PO4, and PAMAM dendrimers modified with carboxyl groups.
An important task in the preparation of BNMs based on NPs of different natures (oxide, metal, polymer, and semiconductor) is the possibility of experimental evaluation of the efficiency of coating particles with a cell membrane obtained from tumor cells or normal human cells (macrophages, platelets, or erythrocytes).
The use of a fluorescence-quenching assay to assess the integrity of cell membranes covering BNMs has been proposed. Using this approach, the reseauthorchers of [138][70] measured and compared the degree of membrane coverage of BNMs and found that the approach used today did not provide adequate integrity of the cell membrane. It was demonstrated that such partially coated NPs were able to enter tumor cells through a cooperative mechanism based on NP aggregation.
Another large group of problems solved through the use of BMNs and, in particular, materials based on a natural or artificial phospholipid membrane encapsulating a drug agent is the therapy of inflammatory diseases, including atherosclerosis. The potential use for anti-inflammatory therapy of leukocyte-based biomimetic NPs obtained by combining phospholipids and leukocyte membrane proteins followed by incubation with binding antibodies has been described. Moreover, the process can be carried out both in a batch [109][38] and in a continuous flow (microfluidic) [67][71] reactor. Such biomimetic nanovesicles are called leukosomes [67,139][71][72].
In addition to leukocytes, macrophages can serve as a basis for constructing BNMs intended for the treatment of atherosclerosis. The reseauthorchers of [46][73] proposed a construct based on a macrophage membrane in which polymeric NPs capable of responding to reactive oxygen species (ROS) were camouflaged. The synthesis was carried out by applying a shell of cell membranes to preliminarily obtained polymeric NPs by extrusion through a polycarbonate membrane with a pore size of 400 nm. The resulting ROS-responsive biomimetic NPs had a small hydrodynamic size with a negative surface charge, retained functional proteins from macrophage membranes, and demonstrated ROS-responsive drug release. Due to cell membrane camouflage, the NPs were able to effectively avoid capture by macrophages and target inflammatory endothelial cells. In addition, such BNMs have demonstrated the ability to inhibit the proliferation of macrophages and smooth muscle cells in vitro without significant cytotoxicity.
As one of the most intensively developing classes of nanomaterials, hybrid BNMs have attracted considerable attention, especially toward the development of technologies for their formation. It was concluded that there were two main groups of hybrid BNMs: the first one included BNMs based on biomimetic nanoceramics, and the second one was based on the use of biogenic or artificial cell membranes with organic (polymeric) or inorganic functional cores. WResearchers believe that both groups of BNMs can be considered as equally prospective for biomedical use.
Biomimetic nanoceramics have been obtained using various methods, including Al2O3 NP repeated coagulation with ferrofluid under a magnetic field following sintering [36][56], nonstoichiometric silicon nitride (SixNy) deposition on both sides of a silicon wafer using low-pressure chemical vapor deposition [142][74], self-assembly of a layered chitosan–maleic acid matrix followed by monetite mineralization and transformation to HAP [147][75], and alumina powder addition to a chitosan solution followed by alginate dissolution and genipin (cross-linking agent) addition. The main proposed application of these biomimetic nanoceramics has been tissue engineering for orthopedic and dentistry purposes.
Membrane-camouflaged NPs have usually been synthesized, for example, via drug-encapsulating PLGA prepared via nanoprecipitation with a consequent coating with cancer cell membranes [45][63], RBC hypotonic treatment and extrusion followed by mixing with PLGA NPs via extrusion through a porous membrane [66][76], stretching of spherical PLGA NPs immobilized on a PVA-glycerol film followed by sonication-assisted coating with ultrasound-derived RBC membranes [33][62], and biodegradable NPs conjugated with (3-aminopropyl)triethoxysilane followed by incubation with proteolipid solution [144][77]. Such BNMs have been mainly proposed for the development of drug delivery carriers.
 

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