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Distribution and Forms of Siliceous Structures Among. Morphology of Structures. Formation and Arrangement of Structures. Cytoplasmic Organization. Skeletal Association with Cytoplasmic Membranes. Surface modification of MSNs, e. Specific targeting of drugs to their target location and a controlled release of the drug will certainly entail a reduction of the applied drug doses and reduce unwanted side effects of drugs. Avoiding pre-mature release of loaded cargo from MSNs is possible by sealing the pores, e.

To liberate cargos from MSNs only in response to a specific trigger effect, sophisticated stimulus-responsive systems have been developed. One prominent approach is the use of redox responsive gatekeepers, since release of cargos after endocytosis of the nanoparticles in the intracellular, reductive environment is achieved. Different gatekeepers, such as cadmium sulfide CdS nanoparticles [ ] Figure 7 A , collagen [ ] or a cross-linked polymeric network [ ] were linked to a functionalized silica surface.

Intracellular thiols readily cleave the disulfide bonds and detach the gatekeepers from the entrance of the pores, resulting in the release of the encapsulated cargo molecules. Stimulus-responsive systems for controlled release of cargo molecules from mesoporous silica nanoparticles. A redox-responsive release adapted from [ ] ; B light irradiation adapted from [ ] ; C enzymatic removal of gatekeeper adapted from [ ] ; D pH-sensitive release adapted from [ ]. Another strategy for stimulus responsive release is based on enzymatic removal of a gatekeeping agent, e.

The latter two are also examples for dual stimuli-responsive systems since they allow cap removal not only enzymatically, but also via temperature shifts. Application of light-sensitive molecules as gatekeepers empowers spatiotemporal control over drug release. Examples include azobenzene derivatives as gatekeepers [ , ] Figure 7 B , photosensitizers that mediate opening of a nanoparticle supported membrane [ ], or a red-light based photoactivation approach [ ].

Different approaches use competitive displacement [ ] or changes in pH [ , ] Figure 7 D as trigger for stimulus responsive release of cargo molecules from mesoporous silica materials. Altogether, multifunctional MSNs combining efficient cargo loading, a strategy for containment and stimulus-responsive release of cargo, and a moiety for targeting to a desired location are major constituents for establishing an advanced drug delivery system.

The high porosity, the large surface area and pore sizes of mesoporous silica allows detection of even very large bio-analytes and the incorporation of a high amount of sensor molecules into the porous matrix. These advantages lead to an improved detection limit and a faster diffusion of the analytes through the mesopores to the sensor molecule providing a shorter response time.

Effective sensors for glucose, H 2 O 2 , NO 2 , ATP or neurotransmitters were generated by immobilization of sensor molecules on mesoporous silica materials [ , , , , , ]. The various possibilities for functionalization of mesoporous silica materials also enable development of further diagnostic or imaging applications [ , ]. However, despite the tremendous progress in generating tailored mesoporous silicas and the many examples for their application, the major disadvantages are complicated syntheses and harsh reaction conditions.

Furthermore, the elaborate, hierarchically structured silica architectures observed in nature are currently still out of reach for chemical silica syntheses. The ability to form even complex nanostructured silica under ambient, very benign conditions draws the attention to biogenic or biomimetically formed silica. Geological deposits of fossilized skeletons of diatoms are referred to as diatomaceous earth, diatomite or kieselguhr. The main component is silicon dioxide besides minor quantities of aluminum and iron oxide, whereas the exact composition depends on the place of origin [ ].

Because of the high content of diatom silica frustules, diatomaceous earth has specific properties such as low density and conductivity but a large surface area and adsorption capacity due to porosity. Owing to these characteristics, diatomaceous earth has for a long time been extensively used as adsorbent [ ], natural insecticide [ ], insulating material [ ], filter aid in wastewater treatment [ , ], or as catalyst carrier for photocatalytic reactions [ , ]. Due to the highly porous, hierarchically nanopatterned architecture, diatom silica also has a remarkable mechanical stability and displays photoluminescence and properties of a photonic crystal [ , , ].

This unique combination of properties, produced under physiological conditions, has led to even more advanced applications as discussed above for synthetic silica materials. Frustules of diatoms can be used as templates for the production of metal surfaces with elaborate patterned features that are valuable for Surface Enhanced Raman Spectroscopy SERS. Coating of purified diatom frustules with metal layers followed by dissolution of silica leaves metallic materials that reflect the exact nanopattern of the silica template [ ].

Furthermore, silica frustules of diatoms are useful templates for conversion of silica in other materials, such as nanocrystalline silicon or amorphous graphite [ , ]. In both examples, the nanoscale structures of the diatom silica are preserved [ , ]. The transformation of diatom silica templates significantly increases the specific surface area of the formed highly porous silicon or carbon materials, thus providing materials with possible applications in sensing, catalysis, bio- chemical separation or energy storage and harvesting.

Alternatively, the mineral composition of diatom frustules can be changed. GeO 2 or TiO 2 can be incorporated into the nanostructure of the silica cell wall by addition of Ge OH 4 or TiCl 4 to the culture medium and exploitation of diatoms as in vivo catalysts. Such Si-Ge composite materials could be applicable in the fabrication of electroluminescent display devices, battery electrodes or dye-sensitized solar cells [ ]. Diatom shells display an efficient visible photoluminescence emission strongly dependent on the environmental conditions. This luminescence can be quenched or enhanced by several gaseous substances, thus diatom biosilica can be used as material in optical gas sensing applications [ , ].

In addition, functionalization of intact diatom frustules with an antibody was shown to enable biosensing of complimentary antigens via photoluminescence [ ]. Tethering of biomolecules to biosilica is achieved by silanization of the surface silanol groups and coupling of a heterobifunctional crosslinker followed by the attachment of the biomolecule, e. Other potential applications of biosilica as carrier for covalent bound antibodies include immunoprecipiation and immunoisolation [ ], or the development of a diagnostic device for electrochemical detection of biomolecules [ ].

The possibility to selectively modify purified diatom biosilica with biological molecules also enables the development of silica microcapsules for targeted drug delivery. The silica shells of diatoms are highly convenient as an inert biomaterial carrier for drug delivery applications.

Their hollow body structures and the micro- and nanoscale porosity allow straightforward loading and sustained release of hydrophobic and hydrophilic cargo molecules [ , ]. Functionalization of diatom silica surfaces with different organosilanes allows tuning of the drug loading and release properties [ , ]. In a different approach, living diatoms are exploited to achieve immobilization of an active enzyme in the biologically produced nanoporous silica material [ ].

Silaffin proteins are involved in the silica formation process in diatoms and become tightly associated with the newly deposited frustules. Genetic fusion of a target enzyme with a silaffin gene and expression of such a fusion protein results in immobilization of the enzyme in the silica matrix. The enzyme containing biosilica can be gently purified and since the enzymes are not completely enclosed within the silica, their activity is largely retained whereas protein stability is significantly increased.

This method has also proven applicable to oligomeric enzymes or enzymes that require posttranslational modifications or cofactors for activity [ ]. Apparent advantages of this method include that the physiological conditions are beneficial for protein integrity and that the protein encapsulation in the nanostructured biosilica provides an ideally suited, mechanical stable and resistant matrix that ensures simultaneously substrate accessibility. Besides synthetic silica and biogenic silica, biomimetic silica formation has gained more attention due to the possibility to combine mild reaction conditions with control over silica structure and relatively simple cargo loading.

Approaches toward bioinspired and biomimetic silica formation were stimulated by the progress in unraveling the molecules involved in silica biomineralization processes in nature. A number of biomolecules could be identified including silaffins and LCPAs from diatoms that proved to be directly involved in the molecular processes leading to silica formation [ 49 , 57 ].

Investigations of their structures and their functional role in silica precipitation revealed chemical and physical prerequisites of biomolecules for activity in silica precipitation. An overall cationic character, more precisely lysine residues in case of peptides and proteins, and the ability to self-assemble in solution have been validated as required features of biomolecules that can induce silica formation. Transferring these insights of biological silica formation to in vitro processes enabled the development of novel silica materials with defined structures and properties under mild, physiological reaction conditions.

Bio- Molecules that have been successfully used in biomimetic silica formation include peptides and proteins such as poly- l -lysine PLL , poly- l -arginine PLA , the R5 peptide, lanreotide, block-copolypeptides and lysozyme, diverse polyamines such as polyallylamine PAA , polyethyleneimine PEI or amine-terminated dendritic structures Table 2. Overview of silica structures obtained with different silica precipitating biomolecules. The use of silica-precipitating molecules at room temperature results in formation of amorphous silica that can adopt a large variety of morphologies, depending on the exact conditions and additives Table 2.

Spherical silica is the thermodynamically preferred structure and is readily obtained using native silaffins [ 57 , 59 ], the R5 peptide [ 60 , 81 , 82 ] and linear or cyclic amines [ , , , ]. Nevertheless, the morphology of precipitated silica can be influenced by variation of the reaction conditions or by the chemical and structural nature of the mediating additive. Using the R5 peptide as a silica precipitating agent, different morphologies deviating from the common silica spheres that are obtained under static reaction conditions, e.

An externally applied electrostatic or hydrodynamic force field was shown to induce fiber-like structures [ ]. The presence of polyhydroxyl compounds, e. Purified predominantly cationic silaffin-1A results in the formation of spherical silica particles with diameters from to nm but in mixture with mainly anionic, glycosylated silaffin-2 the silica material changes to a composite of small silica nuclei [ 57 ].

Polycationic peptides such as poly- l -lysine PLL and poly- l -arginine PLA are well-known to precipitate silica from a solution of silicic acid [ 72 , ]. Under static conditions PLL has been shown to trigger the formation of silica spheres and hexagons, whereas perturbation of the reaction mixture or application of an electrostatic field change silica morphologies to fiber-like, dendrite-like or ladder shapes with periodic voids [ , , ]. The hexagonal silica plates observed by PLL-mediated silica formation are closely linked to PLL chain length and self-assembly of PLL into a helical conformation in the presence of phosphate anions [ , ].

A different study showed that PLL assembles into microspheres in the presence of citrate as counterion and the surface of these microspheres can be coated with silica [ ]. Using large molecular weight PLL, it was recently shown that mesoporous silica materials with pore size distributions comparable to synthetic MCM can be obtained without harsh reaction conditions [ ].

Notably, application of bio-inspired, arginine-based surfactants in silica formation followed by calcination gives porous silica materials [ ]. Since self-assembly emerged to be a prerequisite for silica formation activity, different molecules were considered as structure directing silica formation agents. Block copolypeptides such as poly l -cysteine 30 -b- l -lysine self-assembled into structured aggregates in solution mediate the formation of ordered silica morphologies. The oxidation state of the cysteines in these polypeptides affects the self-assembly and the morphology of the resulting silica material can encompass hard silica spheres under reducing conditions as well as silica in packed columns with oxidized copolypeptide [ ].

The synthetic octapeptide lanreotide is known to self-assemble into nanotubes [ ] and when used as template double-walled silica nanotubes can be produced [ ]. Also amphiphilic peptides such as A 6 K or V 6 K, which self-assemble into nanotubes or lamellar stacks can be used as organic templates in biomimetic silica formation. The presence of anions is necessary in these systems and depending on the peptide and anion composition or on external forces different silica morphologies could be obtained Table 2 [ ].

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Recently, hybrid silica nanoparticles were generated with elastin-like polypeptide ELP micelles. These polypeptides self-assemble into micelles and serve as effective templates for biomimetic silica formation mediated by the R5-peptide. This method allows for facile loading of target molecules to silica particles for the development of drug delivery systems [ ]. In addition to the peptide-based silica precipitating agent discussed above, amines and polyamines are generally able to precipitate silica due to their polycationic character [ 71 ].

The morphology of the silica material obtained e.

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The size of the silica particles obtained from PAA directly correlates with concentrations of phosphate or sulfate anions and depends on the pH of the reaction solution [ 77 , 78 ]. Similar influences were also observed in the case of long chain polyamines LCPAs isolated from diatoms [ 54 ]. LCPAs isolated from diatoms are unique biomolecules and studying the structure-function relationship of synthetic mimics revealed an influence of alkyl chain length, number of amino groups and degree of methylation on silica precipitation activity and the morphology of silica material [ 79 , ].

This understanding allowed the formation of hollow silica spheres and nonporous silica material [ ]. Linear or branched polyethyleneimines PEI are simple polyamines but commonly used in biomimetic silica formation since they lead to almost exclusively spherical silica particles in phosphate containing buffer system [ ]. Different architectures of the PEI polymers or variation of the reaction conditions gave various silica materials, e.

Amine-terminated dendrimers were also used as variable templates for silica formation, in which the polypropylenimine-dendrimers PPI share the same momomeric units as the native LCPAs from diatoms [ ]. Silica precipitating activity of amine-terminated dendrimers turned out to be dependent on the presence of phosphate anions and the size of the silica spheres can be controlled by phosphate concentration [ , ].

The large variety of molecules with silica precipitating activity, the many options to influence the resulting silica structures and the mild reaction conditions led to development of diverse biotechnological applications based on biomimetic silica formation. A prominent application is immobilization of sensitive biomolecules such as enzymes Figure 8. Generally, immobilization of biomolecules in mechanically stable and chemically inert silica matrices has the advantage of stabilizing the biomolecule, thereby often allowing transfer of these biomolecules to non-physiological environments and extend its lifetime, e.

Physical immobilization of biomolecules, i. Schematic overview of enzyme immobilization via biomimetic silica formation and the application fields of silica immobilized enzymes. Enzyme immobilization in biomimetic silica has been achieved with different silica-precipitating agents, e. Silica immobilization of the multimeric enzyme phenylalanine ammonia lyase was achieved with PEI, where coating of the enzyme with PEI prevented enzyme subunit dissociation and PEI served as silica precipitating agent [ ].

The enzymes typically become entrapped in the silica material with moderate to high efficiency while preserving enzymatic activity. However, not only the enzymatic activity of silica-entrapped enzymes can be rapidly assessed but also the structure using solid state NMR [ ]. Confining enzymes in regular silica matrices could also be highly useful for structure elucidation using X-ray crystallography. Silica immobilized enzymes can serve as biocatalysts [ , ] and the simultaneous immobilization of multiple enzymes enabled the construction of a continuous silica biocatalyst device in which one enzyme recycles the cofactor for the other enzyme [ ].

Another approach is based on immobilizing two coupled enzymes producing hydrogen peroxide. This silica-enzyme composite material was used to develop an enzyme based, environmental friendly anti-fouling paint for ship hulls [ ]. For a similar application lysozyme, a cationic protein that was shown to be able to initiate silica formation [ , ], was incorporated into silica-lysozyme biocomposites that retain the antimicrobial properties of lysozyme and can be used as antifouling material as well [ ].

These limitations can be overcome using covalent fusions of the R5 peptide to the target enzyme. This fusion can be achieved genetically and such protein-silaffin chimeras can initiate silica formation and result in controlled and efficient self-entrapment in the silica matrix [ , , ]. The ability of self-entrapment of fusion proteins containing the R5 peptide has been exploited in the generation of biosensors [ , ].

Immobilization of carbonic anhydrase into bioinspired silica led to stabilization of this sensitive enzyme and opens the route for the development of an ecofriendly and efficient method to capture the greenhouse gas CO 2 [ , ]. However, genetically fused and recombinantly expressed silaffin peptides lack the typical posttranslational modifications seen in diatoms and therefore major factors that control silica morphology and properties such as pore sizes are not accessible by this strategy. Recently, we could demonstrate how posttranslational modifications of synthetic R5 variants influence the formation of silica material with different morphologies [ 83 ].

Based on these findings a novel strategy for silica encapsulation of target proteins was established, in which chemically modified R5 peptides were covalently linked to target proteins through expressed protein ligation [ , ]. The resulting covalent conjugates of target proteins and modified R5 peptides precipitated silica efficiently and led to homogenous and functional encapsulation of the proteins in the resulting silica particles, highly superior to the random entrapment observed after simple co-precipitation [ ].

In addition, covalent conjugation of other cargo such as small molecules and peptides to the synthetic R5 peptide allows efficient encapsulation of the cargo into biomimetic silica particles [ 83 , ]. In combination with controlled release, e. R5-cargo conjugates can be obtained via selective conjugation of thiol-functionalized cargo molecules, such as drug molecules, bioactive peptides or proteins, to a thiol-containing R5 peptide and result in high efficiencies of cargo encapsulation under mild conditions in a one-step procedure [ ].

The advantageous mechanical properties of silica nanospheres also facilitate the application of entrapped enzymes in continuous flow-through reactors. Silica immobilized nitrobenzene nitroreductase was used to construct a microfluidic reactor for screening of cancer prodrug activation [ ]. Another example showcases the immobilization of butyrylcholinesterase to screen the potency of cholinesterase inhibitors. Here a histidine-tagged R5 peptide variant was used to mediate selective binding to cobalt coated agarose beads.

The R5-coated agarose mediated silica formation and enzyme encapsulation after addition of a silica precursor [ ]. Such silica materials with different core structures should hold high potential for future use in biotechnology, bioimaging and medical applications [ ]. The feasibility of silica deposition on planar surfaces has many potential practical uses.

The R5 peptide has been used to deposit ordered arrays of silica nanospheres into a polymer hologram for construction of photonic devices [ ]. Poly- l -lysine was also used for controlled patterned silica coating of surfaces under mild reaction conditions [ ]. The integration of silica-encapsulated enzymes on planar surfaces empowers the generation of stabilized biosensors or enzyme microarrays and could be achieved with the R5 peptide or lysozyme [ , ]. The deposition of silica or a silica-enzyme layer on a gold surface mediated by lysoszyme increases the surface area and is therefore valuable for enhancing sensitivity in surface plasmon resonance spectroscopy applications [ ].

Entrapment of enzymes in carbon-nanofiber silica composites provides a conductive matrix for the enzyme and gives rise to novel electrochemical biosensor systems [ , , ]. Overall, there is a multitude of very appealing applications of functionalized silica materials in biotechnology, medicine and in the controlled assembly of microscopic structure. Many recent examples are described above and especially the mild biomimetic silica variants will play a more important role in the near future.

Applications of biomimetic silica that can be envisioned span the biotechnological use of tailor-made particles loaded with a specific bio- catalyst or combinations thereof that allow reusing of such valuable enzymes and installation of reaction chains for more complex transformations. A renewed interest in core-shell particles that contain a core of gold e. Medical application of biomimetic silica particles could also be further tweaked by using biocompatible but still fully controllable approaches to generate silica materials with controlled pore size and particle diameter.

Such materials could be used as improved delivery tools for sensitive peptide and protein cargos in living systems. Critical aspects that need to be considered are the overall size, homogeneity and stability of functionalized biomimetic silica materials that can vary depending on several parameters such as pH, ion strength, temperature, etc. Recent reports on potential toxic effects of silica nanoparticles [ , ] also need to be taken into account when developing new biomimetic silica materials for in vivo use.

To this end, a recent debate about the contribution of peptide- and protein coronas assembling around nanoparticles, almost independent of the material used to create them, should be kept in mind since detrimental effects on particle function as well as an in vivo safety can be expected. Several publications have been addressing this point over the past few years [ , , ].

National Center for Biotechnology Information , U. Journal List Mar Drugs v. Mar Drugs. Published online Aug Carolin C. Lechner 1 and Christian F. Christian F.

Silicon and Siliceous Structures in Biological Systems

Author information Article notes Copyright and License information Disclaimer. Received Jun 30; Accepted Jul This article has been cited by other articles in PMC. Abstract Biomineralization processes leading to complex solid structures of inorganic material in biological systems are constantly gaining attention in biotechnology and biomedical research. Keywords: biomineralization, silaffins, diatoms, posttranslational modifications. Silica Biomineralization in Diatoms 2. Diatom Biology and Cell Cycle Diatoms are eukaryotic, unicellular organisms which are ubiquitously found in both marine and fresh water environments in all parts of the world as long as sufficient amounts of nutrients are present.

Open in a separate window. Figure 1. Figure 2. Silaffin Proteins and Peptides Silaffins were initially identified from the diatom C. Figure 3. Figure 4. Table 1 Overview of silaffin variants identified from different diatom species. Chemical and Mechanistic Aspects of Silica Formation Amorphous silica is formed by a complex inorganic polymerization process with orthosilicic acid as the monomeric building block. Figure 5. Silaffin-Induced Silica Precipitation In case of the silaffins a model for their silica formation activity that is in agreement with the model for silica formation by LCPAs was proposed [ 76 ].

Figure 6. Biotechnological Applications of Silica The scope of applications of silica is tremendous due to its unique chemical and mechanical properties and its easy availability. Synthetic Silica Materials Porous silica is a suitable material for biotechnological and medical applications because of its chemical inertness and biocompatibility.

Figure 7. Diatomaceous Earth and Biogenic Diatom Silica Geological deposits of fossilized skeletons of diatoms are referred to as diatomaceous earth, diatomite or kieselguhr. Biomimetic Silica Besides synthetic silica and biogenic silica, biomimetic silica formation has gained more attention due to the possibility to combine mild reaction conditions with control over silica structure and relatively simple cargo loading.

Formation of Biomimetic Silica with Different Silica-Precipitating Agents Bio- Molecules that have been successfully used in biomimetic silica formation include peptides and proteins such as poly- l -lysine PLL , poly- l -arginine PLA , the R5 peptide, lanreotide, block-copolypeptides and lysozyme, diverse polyamines such as polyallylamine PAA , polyethyleneimine PEI or amine-terminated dendritic structures Table 2.

Table 2 Overview of silica structures obtained with different silica precipitating biomolecules. Biotechnological Applications Based on Biomimetic Silica The large variety of molecules with silica precipitating activity, the many options to influence the resulting silica structures and the mild reaction conditions led to development of diverse biotechnological applications based on biomimetic silica formation. Figure 8. Outlook Overall, there is a multitude of very appealing applications of functionalized silica materials in biotechnology, medicine and in the controlled assembly of microscopic structure.

Conflicts of Interest The authors declare no conflict of interest. References 1. Wedepohl K. The composition of the continental crust. Exley C. Silicon in life: A bioinorganic solution to bioorganic essentiality. Birchall J. The essentiality of silicon in biology. Nielsen F. Ultratrace Elements in Nutrition. Schwarz K. Growth-promoting effects of silicon in rats. Carlisle E.

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