Biomedical Applications: 55 (Modern Aspects of Electrochemistry)

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[Full text] Slp-coated liposomes for drug delivery and biomedical applications: po | IJN

Slp can self-assemble on the surface of liposomes in a proper environment via electrostatic interactions, which could be employed to functionalize liposomes by forming Slp-coated liposomes for various applications. Among the molecular characteristics, the stability, adhesion, and immobilization of biomacromolecules are regarded as the most meaningful. Compared to plain liposomes, Slp-coated liposomes show excellent physicochemical and biological stabilities.

In view of these favorable features, Slp-coated liposomes are highly likely to be an ideal platform for drug delivery and biomedical uses. This review aims to provide a general framework for the structure and characteristics of Slp and the interactions between Slp and liposomes, to highlight the unique properties and drug delivery as well as the biomedical applications of the Slp-coated liposomes, and to discuss the ongoing challenges and perspectives.

Keywords: S-layer protein, liposomes, self-assembly, interactions, drug delivery, biomedical applications. Slp forms a crystalline array of proteins called S-layer on the outermost envelope of bacteria and archaea with a molecular weight of 40— kDa. As a result, Slp-coated liposomes have received increasing attention in the past decade. Liposomes are nanovesicles composed of phospholipid bilayers that have various beneficial characteristics, such as good cell affinity, 7 , 8 targeting properties, 9 — 11 and sustained drug-release behavior.

Therefore, increasing attention has been paid to the surface engineering of liposomes using various biological or chemical materials to improve their features. Hence, Slp-coated liposomes may be used as a powerful vehicle for drug delivery to resolve problems such as instability, drug leakage, and poor targeting.

Therefore, understanding these interactions is necessary and urgent for the development of Slp-coated liposomes. In the current review, after the introduction of the structure and characteristics of Slp, the interactions between Slp and liposomes are summarized. Various advantages of Slp-coated liposomes, including their excellent stabilities, adhesion and immobilization of biomacromolecules, and applications in drug delivery and biomedicine, are reviewed in detail Table 1. The challenges and perspectives of Slp-coated liposomes are also discussed.

Figure 1 Schematic drawing of self-reassembly of Slp on solid supports, in suspension, at an air—water interface, and on liposomes as well as in solution nanotubes, ribbons, mono- and double-layer sheets. Reassembly of S-layer proteins. Reproduced with permission. All rights reserved. In , Houwink and Le Poole first observed crystalline arrays of biomacromolecules on the outermost cell surface of Spirillum serpenes by electron microscopy. Since then, many studies have revealed that this biomacromolecule, now named Slp, is also present on the cell surface of other bacteria and archaea.

The disordered regions occupy almost half of the full length of Slp, and simultaneously, the high content of disordered regions results in the flexibility of Slp to alter its conformation for adapting to the phase interface, which has a crucial role in self-assembly on the surface of liposomes. Figure 2 Schematic drawing of various Slp lattice morphologies containing oblique p1, p2 , square p4 , or hexagonal p3, p6 symmetries.

S-layers: principles and applications. Slp lattices construct the outermost cell surface framework of archaea and bacteria, maintaining the stability of the cell morphology. Simultaneously, Slp lattices can provide cells with protection against changes in extrinsic stress factors eg, various mechanical forces, osmotic pressure, radiation, and rapid variation in pH values and the influence of antimicrobial peptides such as human defensin LL 48 as well as lysozyme.

The substance-selective crystalline arrays consisting of Slp are able to control the exchange of substances between bacterial cells and the environment. All of these diverse functions reflect the acclimatization of prokaryotes. Remarkably, the self-assembly property of Slp broadens its application potential in the molecular engineering and nanobiomaterial fields. Following are some of the applications of Slp:. Liposomes are biomimetic vesicle-like drug delivery systems composed of phospholipid molecules and cholesterol.

Due to their good biocompatibility and biodegradability, passive targeting, and slow-release potential, as well as their strong tissue affinity, liposomes have been investigated as carriers of various drugs, such as antitumor drugs, antimicrobial drugs, RNAs, and proteins. Liposomes were first discovered by Bangham in , and in , Rahman proposed that liposomes can be an ideal drug carrier. Later, many related studies were performed.

To date, liposomal doxorubicin, liposomal amphotericin B, and liposomal paclitaxel have been applied in the clinic. However, poor stability, drug leakage, short retention time, and undesirable tissue distribution of conventional liposomes limit further clinical applications. Figure 3 Brief summary of surface engineering of liposomes. PEGylation is the most common strategy which has the ability to reduce clearance by the RES, thus enhancing the in vivo circulating time of liposomes.

1. Introduction

In addition, PEGylation can delay drug leakage, improving the stability of liposomes. However, PEGylation will affect the normal release of drugs and uptake of cells, thereby decreasing the effect of the drug. Its exceptional bioadhesive ability can prolong the retention time of liposomes in specific tissues, leading to improved bioavailability. Hence, a chitosan-modified strategy has been widely used in liposomal delivery of genes. Collagen protein can enhance the in vitro and in vivo stability of liposomes.

Furthermore, membrane-active peptide 63 , 64 and cell-penetrating peptide 65 , 66 facilitate the intracellular delivery of liposomes. Surface-modified liposomes with Slp also have various advantages eg, enhancing stabilities and promoting gastrointestinal adhesion and have received increasing attention in recent decades.

Due to its capability to self-assemble on the surface of lipid layers, Slp has been employed to functionalize liposomes. In particular, the formation of Slp crystalline arrays on the surface of positively charged liposomes by interaction of exposed carboxyl groups of Slp with positively charged groups on the surface of liposomes can significantly enhance the stability of liposomal membranes, 67 — 70 protecting liposomes from strong mechanical forces and high-temperature environments.

In recent years, a series of electron microscopy technologies, such as the thin-sectioned, freeze-dried, and freeze-etched methods, 30 , 71 — 78 have been adopted to elucidate the location and ultrastructure of Slp lattices. In addition, information on lattice constants, such as average size, was provided by atomic force microscopy 31 , 79 — 83 and small-angle X-ray scattering. In essence, a liposome is a closed lipid membrane with a morphology that is similar to the cell.

Hence, some clues on the interactions of Slp with liposomes could be obtained from the interactions between Slp and microbial cells. It was reported 1 , 88 that there are five modes of interaction between Slp and different species of bacteria and archaea: 1 in most archaea, hydrophobic transmembrane domains of Slp can transfix the cell envelope and then combine with hydrophobic groups of phospholipid molecules via hydrophobic forces Figure 4A , thereby directly attaching to the cytoplasmic membrane; 2 Slp of some archaea possesses lipid-modified glycoprotein subunits, allowing Slp to directly anchor on the surface of the cell envelope Figure 4B ; 3 only a few archaea have a rigid wall layer as an intermediate layer between the Slp and the cell envelope Figure 4C ; 4 in Gram-positive bacteria, Slp links with the rigid peptidoglycan-containing layer by secondary cell wall polymers Figure 4D ; and 5 in Gram-negative bacteria, the interaction mode is more complex: Slp is attached to the lipopolysaccharide LPS of the outermost layer Figure 4E.

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Notes: A In most archaea, hydrophobic transmembrane domains transfixing the cell envelope make Slp anchor at the cell envelope, and B in some other archaea, the lipid-modified domains in Slp drive this process. C Only a few archaea possess a rigid wall layer mediating the process of Slp binding to the cell envelope.

D In Gram-positive bacteria, Slp interacts with the peptidoglycan layer indirectly via secondary cell wall polymers, E while Gram-negative bacterial cell envelopes express more complex components, and Slp needs to attach to the lipopolysaccharide of the outermost layer. However, for liposomes, there are no complex components eg, peptidoglycan and LPS that can support the interaction between liposomes and Slp.

There is mounting evidence that electrostatic forces drive the self-assembly process of Slp. The fact that Slp lattices tend to form on zwitterionic phospholipids and positively charged phospholipids, but not on negatively charged phospholipids, suggests electrostatic interactions between exposed carboxyl groups on Slp lattices and positively charged or zwitterionic lipid head groups. At least two to three structural domains in Slp named contact points have been shown to exist between Slp and lipid film. Hence, Slp-coated lipid films are also referred to as semifluid membranes.

This issue was examined by a study on the interaction regions between Slp and liposomes via the monitoring of adiabatic compressibility. Adiabatic compressibility can indicate the contribution of the conformational mobility of polar head groups as well as hydrophobic regions. Analysis of adiabatic compressibility confirmed that such a contribution preferentially came from the conformational variation of polar head groups, suggesting that contact points of Slp interact with polar head groups rather than hydrophobic tail groups.

For example, Hollmann et al 92 extracted glycosylated Slp from Lactobacillus kefir and non-glycosylated Slp from Lactobacillus brevis , and then, glycosylated Slp-coated liposomes GSLs and non-glycosylated Slp-coated liposomes nGSLs were obtained. The results demonstrated that the GP value of GSLs was higher than that of nGSLs, which indicated that the affinity of glycosylated Slp to liposomes was stronger than that of non-glycosylated Slp due to more water molecules penetrating the membrane of nGSLs.

Meanwhile, these findings also illustrated that uncharged glycosylated moieties could affect the interactions between Slp and liposomes, and this effect may be mediated by glycosylated moieties changing the charge distribution. Figure 5 Schematic drawing of Slp interacting with liposomes. Notes: The self-assembly of Slp on the surface of liposomes is mainly attributed to electrostatic forces. Intriguingly, the orientation of polar head groups of surfactant molecules tilts toward the surface normal to increase the positive charge density within linking regions to enhance the electrostatic force.

In fact, the formation of Slp lattices on the surface of liposomes depends not only on the interactions between Slp and phospholipid molecules but also on the interactions between Slp subunits.

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As Figure 6 suggests, there are self-assembly sites in the structure of Slp that support the formation of Slp lattices. However, these lattices are not very stable because this is a dynamic equilibrium process. Hence, we hypothesize that the components in the medium, especially the composition of ions, should also be investigated in depth when preparing Slp-coated liposomes.

Figure 6 Schematic illustration showing the influence of cations on the formation of Slp lattices. Without any addition of cations, D the dynamic equilibrium of the three conformations provides an opportunity to expose self-assembly sites, E allowing lattice formation. F Electron microscopy observation of p4 arrays of SlpB Copyright In summary, successful S-layer formation on the surface of liposomes mostly relies on two self-assembly modes: 1 the electrostatic assembly between Slp and liposomes; and 2 the intermolecule assembly between Slp monomers.

The former helps Slp to anchor onto the lipid membranes, and the latter drives the formation of S-layer. It is known that Slp-coated liposomes possess high stability and it is not easy for Slp to loss from liposomal membranes due to the relatively strong intermolecular assembly between Slp subunits. Of course, the stability depends on the surface charges of liposomes and the species of Slp.

Self-assembly properties and interactions between Slp and liposomes are the basis for the development of Slp-coated liposomes. Once Slp is coated on the surface of liposomes, liposomes are endowed with unique features, such as excellent physicochemical and biological stabilities, gastrointestinal adhesion, and immobilization of biomacromolecules. These unique features suggest a series of clinical potential, which lay the foundation for Slp-coated liposomes as an ideal platform for drug delivery and biomedical uses.

In general, particle size and zeta potential are used to characterize the physicochemical stability of liposomes because these two properties not only reveal stability but also affect the in vivo pharmacokinetic process of liposomes. Compared with plain liposomes, Slp-coated liposomes display an interesting variation in zeta potential.

With the increasing ratio of Slp to lipid, the zeta potential decreases significantly 29 , 97 , 98 until the inversion of the potential. Hence, the Slp-coating efficiency of positively charged liposomes is much better than that of negatively charged or neutral liposomes. However, the reduction of the potential becomes less, and the value of the potential tends toward invariance with the continuous enhancement of the ratio of Slp to lipid, which is the result of the limited area of liposomes for reassembly of Slp.

For example, Hollmann et al 98 prepared a positively charged liposome composed of soybean lecithin, cholesterol, and stearylamine with a molar ratio of After incubation for minutes with Slp extracted from L. In summary, the variation of the zeta potential can be employed to characterize the amount of Slp reassembled on the surface of liposomes. Contrary to the zeta potential, the coating of Slp does not significantly influence the particle size of the liposomes.

Research by Hollmann et al 98 found that the particle size of liposomes increased by 21 nm from to nm after coating with Slp. The slight increase in particle size exactly conforms to the 5—25 nm thickness of the S-layer on bacteria. Poor stability is known to restrict the development and application of liposomes due to the fusion and membrane disruption propensity of liposomes. Hence, developing a technology to improve the stability of liposomal membranes is critical to expand the application potential of liposomes.

Liposomes are assembled by phospholipid molecules via hydrophobic forces. However, this is a weak interaction; hence, the membrane of the plain liposome is weak and can easily be disrupted by environmental stress factors eg, low pH value, mechanical force, and rapid variation in temperature , leading to disordered phospholipid molecule arrays Figure 7A , which cause membrane deformation and drug leakage.

When Slp self-assembles on the surface of the liposome by electrostatic forces, the arrays of phospholipid molecules would be restored to the ordered state Figure 7B , and then, the shape of the liposome would tend to be spherical to maintain the lowest energy state, which is the result of the protective function of Slp crystalline arrays for reducing the influence of environmental stress factors.

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Hollmann et al 97 extracted Slp from L. To evaluate the stabilities in the conditions simulating the gastrointestinal environment, researchers studied the effects of pancreatic extract and bile salts. The results indicated that after incubation of pancreatic extract for 60 and minutes with bile salts, Slp-coated liposomes retained more carboxyfluorescein than control liposomes Figure 7A and B. Therefore, Slp-coated liposomes possessed higher physicochemical stability than plain liposomes. Other stress factor evaluation assays, such as changes in pH value Figure 7C , 97 rapid variation in temperature Figure 7D , and strong mechanical forces Figure 7E and F , all proved the higher stability of Slp-coated liposomes relative to plain liposomes.

It was also observed that the coating of Slp would lead to a delayed release. Figure 7 Evidence of the enhanced stabilities of Slp-coated liposomes. Notes: A The arrays of plain liposome membrane molecules and B the arrays of Slp-coated liposome membrane molecules. C Percentage of CF enclosed by plain liposomes and Slp-coated liposomes in an environment with pH values of 2.

Biological stability in the circulatory system is a core subject in liposomal delivery to the targeted sites. This biological stability mainly reflects the ability of the liposome to avoid the capture of RES. The RES, with key roles in the recognition and clearance of foreign particles, is a major constraint to nanoparticle-based drug delivery systems, such as liposome-based drug delivery system. On the other hand, Slp coating decreases membrane fluidity, which hinders lipid extraction by high-density lipoproteins, reducing the risks of liposome breakdown.

Collectively, Slp-coated liposomes display significantly higher physicochemical and in vivo biological stabilities than plain liposomes through extended circulation, which broaden their applications in tumor-targeting technology. Specific tissue affinity has traditionally been a continuously explored topic for liposomes.

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Chemical and thermal denaturation of crystalline bacterial S-layer proteins: an atomic force microscopy study. Nanometric transducers have been used to obtain new classes of biosensor devices. Remarkably, the self-assembly property of Slp broadens its application potential in the molecular engineering and nanobiomaterial fields. Bioconjug Chem. Gene probe assays on a fibre-optic evanescent wave biosensor. The course covers all these topics and implies active interaction between the tutor and students during the classes. Pundir CS, Chauhan N.

With this property, site-specific drug delivery and targeted drug delivery can be achieved. In particular, if liposomes show specific adhesion to the gastrointestinal epithelial cell line, the drug bioavailability mediated by liposomal oral drug delivery systems will increase.

In recent years, increasing research has been conducted to prove that Slp mediates bacterial adhesion to host cells, especially the gastrointestinal epithelial cell line. Another study reported that adhesion of Lactobacillus acidophilus ATCC to the human colorectal adenocarcinoma cell line HT was reduced dramatically when Slp was removed. All of these studies support the view that Slp induces adhesion. However, most studies were carried out in vitro with different cell strains, and adhesion to the gastrointestinal mucosa in vivo, especially that by Slp-coated liposomes, has rarely been investigated in depth.

Our previous study investigated the effects of Slp coating on the gastric and intestinal mucoadhesion of liposomes, in which the Slp-coated liposomes and control liposomes were all labeled by fluorescein isothiocyanate FITC. After 7 and 12 hours of oral administration, the stomach and intestine were excised, and the mucosa was scraped off gently with a glass slide.

Then, the mucosal scrapings were observed under a fluorescence microscope. The results Figure 8A and B showed that the fluorescence in gastric and intestinal mucosa at 7 and 12 hours after Slp-coated liposome oral administration was stronger than that of the control liposomes, which confirmed that Slp could also enhance the adhesion of liposomes to gastrointestinal mucosa. Figure 8 Mechanism of Slp promoting drug internalization of liposomes and fluorescence microscopy of gastric and intestinal mucosal scrapings after A 7 and B 12 hours of intragastric administration of Slp-coated liposomes and plain liposomes, respectively.

Notes: a Gastric mucosa of Slp-coated liposomes. Hollmann et al 98 found that Slp from L. Simultaneously, an enhanced ability to transfer cargo molecules into Caco-2 cells from Slp-coated liposomes compared to control liposomes demonstrated that adhesion mediated by Slp was crucial for facilitating drug internalization, as shown by flow cytometry. The mechanism of drug internalization by Slp-coated liposomes is illustrated in Figure 8.

Currently, there is mounting evidence that the epithelial cell surface and extracellular matrix ECM express Slp receptors that can bind to Slp, inducing adhesion. From Table 2 , we can see that fibronectin, collagen, and laminin are the most common receptors of Slp. They are primarily found in the ECM and on the surface of intestinal cells.

Hence, Slp-coated liposomes can potentially be used in a variety of oral drug delivery systems, particularly for biomacromolecular drugs, such as vaccines. However, interactions of Slp with TLR2 and TLR4 will trigger the expression of proinflammatory factors, thereby stimulating the innate immune system and T helper cell responses rather than inducing adhesion.

Meanwhile, Slp-coated liposomes can significantly facilitate drug internalization. Therefore, Slp-coated liposomes could be a promising tool for the oral delivery of biomacromolecular drugs. Table 2 Summary of Slps with their receptors and their targeted cells or locations Notes: The interaction modes or regions between Slp and their receptors are also listed in this table. Abbreviation: ECM, extracellular matrix. Currently, liposomes are typically used in targeted drug delivery systems. Surface modification of liposomes can promote their locations in targeting tissues.

In particular, modification by biomacromolecules such as antibodies is very important for targeted drug delivery systems. Slp constructs a crystalline array of self-assembling proteins on the bacterial cell surface layer, and Slp was shown to immobilize biomacromolecules. To functionalize liposomes, researchers have used various approaches to immobilizing biomacromolecules by Slp. Three methods for immobilizing biomacromolecules by Slp have been reported. The first method is genetic recombination technology protein fusion technology ; the genes encoding Slp and functional domains of biomacromolecules are all ligated into plasmids and heterologously expressed in Escherichia coli.

Through this method, Slfp will be obtained. Slfp retains the capability of the Slp moiety to self-assemble on the interface and possesses functional domains of biomacromolecules that exert key effects. The fusion protein could self-assemble on glass slides, silicon wafers, and various types of membranes, allowing the orientated and dense surface display of LamA.

Catalytic function assays demonstrated that LamA immobilized by SbpA in a periodic and oriented fashion could catalyze twice the glucose release from the laminarin polysaccharide substrate compared to randomly immobilized LamA.

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The second method involves biomacromolecule immobilization by Slfp, which contains specific linking domains. First, Slp fuses with the specific linking domains via gene recombination technology. Then, the biomacromolecules interact with the specific linking domains by covalent bonds or non-covalent bonds for the purpose of immobilization. Additionally, some biomacromolecules are immobilized by Slp via direct interactions or crosslinkers the third method. An interesting study reported that Slp as an immobilization matrix for aptamers could be applied in biosensors.

Thrombin aptamers ThromApt-SH and ofloxacin aptamers OflApt-NH 2 were immobilized on the surface of Slp lattices via crosslinkers such as p-maleimidophenyl isocyanate, 1-ethyl 3-dimethylamino-propyl carbodiimide, and sulfosuccinimidyl N-maleimidomethyl cyclohexanecarboxylate. Laser-induced fluorescence spectroscopy, IAsys resonant mirror sensor , and quartz crystal microbalance with dissipation monitoring QCM-D analyses proved that aptamers immobilized on solid supports by Slp showed good recognition for thrombin and ofloxacin and could thus have broad applications in biosensor fields.

Table 3 lists some biomacromolecules immobilized by Slp and Slfp. Furthermore, the immobilization function of Slp can also be utilized in liposome-based drug delivery systems. As mentioned above, Slp can self-assemble on the surface of liposomes and immobilize biomacromolecules; that is, Slp promotes the surface engineering of liposomes. Hence, the rSbpA-EGFP-coated liposomes can be used to monitor the distribution of liposomal drug delivery systems in vivo. Meanwhile, a recrystallization experiment demonstrated that rSbpA-GG could form a square lattice symmetry on the outermost region of the emulsomes, which indicated that rSbpA-GG still possessed the capability to self-assemble on the phase interface.

Ultimately, immune colloidal gold technique was employed to confirm the IgG-binding feature of rSbpA-GG-coated emulsomes. Furthermore, Figure 9B2 shows that p4 symmetry was established. Portland Press, Ltd. A functional chimaeric S-layer-enhanced green fluorescent protein to follow the uptake of S-layer-coated liposomes into eukaryotic cells. Biochem J. S-layer fusion protein as a tool functionalizing emulsomes and CurcuEmulsomes for antibody binding and targeting. Colloids Surf B Biointerfaces.

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S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays. Proc Natl Acad Sci. Copyright National Academy of Sciences, U. Copyright , with permission from Elsevier. Abbreviation: TEM, transmission electron microscopy. Another typical method for Slp-coated liposome immobilization of biomacromolecules is the use of streptavidin-biotin system. There are two mechanisms involved in the streptavidin-biotin system.

Figure 9C and C1 illustrates one mechanism with ferritin as an example. Firstly, Slp fuses with streptavidin to form an rSlp-streptavidin fusion protein, which reassembles on the surface of the liposome. Then, biotinylated ferritin can bind to the streptavidin domain. Afterward ferritin can bind to the streptavidin-terminal region, achieving the aim of immobilization of the ferritin on the liposomal surface Figure 9D and D1. However, research on Slp-coated liposome immobilization of biomacromolecules remains limited. Hence, this research still has profound academic significance and broad prospects.

The most promising application of Slp-coated liposomes is drug delivery. Slp-coated liposomes possess strong physicochemical stability that protects their cargo molecules against the mimetic gastrointestinal environment rapid variations in pH and temperature, mechanical force, pancreatic extract and bile salts.

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To confirm this point, Hollmann et al 98 constructed an Slp-coated liposome carrying calcein and then evaluated whether the Slp-coated liposomes promoted drug internalization in human colon adenocarcinoma Caco-2 cells by flow cytometry. Thus, the researchers theorized that the drug internalization mechanism of Slp-coated liposomes is endocytosis by Caco-2 cells. Furthermore, the results of MTT assays showed that Slp-coated liposomes did not reduce the viability of Caco-2 cells at any of the concentrations tested Figure 10F. Figure 10 Evidence of Slp-coated liposomes promoting drug internalization and surface engineering of liposomes and as carriers of vaccines for oral administration.

Interaction of S-layer proteins of Lactobacillus kefir with model membranes and cells. J Liposome Res. Hollmann et al showed that that Slp-coated liposomes indeed display promising potential as drug carriers for oral administration, especially oral delivery of biomacromolecular drugs.

Hence, a newly developed oral delivery system could eliminate the critical delivery bottleneck of biomacromolecular drugs.

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Therefore, appropriate gastrointestinal environment and drug internalization are the key factors that should be considered for oral delivery systems of biomacromolecular drugs. The key results are presented in Figure 10G. The IgG level of the ig-HepB group at the eighth week was 4. Slp-coated liposomes exhibited a better biological efficiency than unmodified liposomes, but much lower than that of the Sc-HepB group IgG level However, unlike the Sc-HepB group, the IgG levels of the other three oral administration groups all increased at the 10th and 12th week.

However, it is interesting to note that the IgG levels of the three oral administration groups all showed an upward trend over time, while the IgG levels of the Sc-HepB group showed a downward trend.

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We inferred that the differences in pharmacokinetic processes between subcutaneous injection and oral administration led to this phenomenon. These findings also suggested that the interval dose and time should be fully considered when developing an oral delivery system for a vaccine. These results showed that the Slp-coated liposomes were able to improve the oral delivery efficiency of vaccines significantly. However, the efficiency was still not strong enough for the clinical application in oral administration, which may be the main cause that limits the publication of the related literature.

As noted in the previous section, immobilization of biomacromolecules is another unique property of Slp-coated liposomes. This feature will drive the functionalization of liposomes to achieve targeted drug delivery. Emulsomes are a vesicle-based delivery system for the delivery of hydrophobic drugs. As shown in Figure 10H , the emulsome comprises a solid emulsion core surrounded by phospholipid layers.

Hence, the structure of the emulsome is like a liposome-entrapped solid emulsion. Thus, the surface characteristics of emulsomes are the same as those of liposomes. The research above also revealed the functionalization potential of Slp-coated liposomes. As we continue to explore design strategies, our progress in oral delivery of biomacromolecular drugs and targeted drug delivery by Slp-coated liposomes will continue. We also believe that the biomedical engineering uses of Slp combined with the favorable characteristics of liposomes will drive a series of biomedical applications.

As an important biomaterial, Slp has already been researched in the biomedical field. A regular crystalline array of Slp provides a firm platform for biomacromolecules, enabling it to be a novel biocatalyst, , a potential agent for biomimetic therapy, and a biosensor. Increasing evidence has confirmed that Slp-coated liposomes display great potential in the biomedical engineering field in addition to drug delivery. In , Ilk et al first reported that uptake of an S-layer-enhanced green fluorescent fusion protein-coated liposome into eukaryotic cells could be visualized by confocal laser scanning microscopy.

Traditional labeling modes of fluorescent molecules for nanomedicine involve physical adsorption and chemical conjugation. The potentially toxic agents used in the process of chemical conjugation probably diffuse through the lipid bilayer into the interior of the liposome. This functional liposome has good application potential in the continuous development of liposomes and in vivo imaging technology of specific cells. Figure 11 Biomedical applications of Slp-coated liposomes in imaging technology, as biocatalysts, and in preparation of biomimetic membranes.

RmlA nanolattice. Blue circles:biocatalytic RmlA epitopes arbitrary positions ; yellow symbols: rSgsE. L Fluorescence microscopy confirming the formation of planar biomimetic membranes. John Wiley and Sons. First published on May 24, Due to its abundant carboxylic and amino groups and its ability to form regular crystalline arrays, Slp has usually been employed to construct a biocatalytic surface for the immobilization of enzymes. The immobilization of enzymes can facilitate the separation and reuse of enzymes, thus reducing the cost of industrial production.

This discrepancy was due to the formation of double-layered Slp on the surface of the nanotube. These double-layer structures with a face-to-face inward orientation of the catalytic epitopes bury the catalytic domains in the intralayer of the nanotube, which dramatically inhibits the efficiency of the reaction Figure 11H. This enhancement was mainly attributed to the full surface display of catalytic epitopes Figure 11I. For recycling and reuse, the liposomal biocatalyst could be separated by centrifugation, and From this example, we can see the promising application potential and economic value of Slp-coated liposomes in the immobilization of enzymes for constructing novel biocatalysts.

In addition to these biomedical applications, the interactions between Slp and liposomes are typically employed to prepare biomimetic-supported lipid membranes for studying the characteristics and functions of transmembranes and membrane-bound proteins. Furthermore, biomimetic-supported lipid membranes can be used to investigate biomembrane-mediated interactions and cell signal transduction.

Schrems et al adopted the interactions between liposomes and Slp to prepare biomimetic-supported lipid membranes. Subsequently, the researchers observed that the phospholipid molecules fully covered the surface of solid supports Figure 11L , which confirmed the successful formation of planar biomimetic membranes. Thus, Slp-coated liposomes have shown promising potential in some biomedical engineering fields, including imaging technology, catalytic chemistry, and biomedical investigation. Although some encouraging progress has been made, developing appropriate biomedical applications of Slp-coated liposomes still requires further research.

The present review provides an overview of the development of Slp and Slp-coated liposomes. The latter has emerged as an interesting candidate for drug delivery and biomedical uses because of the distinguishing features of Slp-coated liposomes, including favorable physicochemical and biological stabilities, adhesion to specific cells or tissues, and immobilization of biomacromolecules for multifunctionalization of liposomes. However, there are some difficulties in the development of Slp-coated liposomes.

Critical challenges that still remain and need to be explored are listed below, which will serve as a roadmap to further elucidate the future beneficial effects of Slp-coated liposomes. Although Slp-coated liposomes are expected to be suitable candidates for the oral delivery of vaccines, the enhancement of oral delivery of vaccines is not satisfactory. To our knowledge, the oral delivery efficiency of biomacromolecular drugs mostly relies on the gastrointestinal retention time, the uptake by gastrointestinal epithelial cells, and the ability to defend against the extreme gastrointestinal environment.

Slp-coated liposomes have shown improvements in the stability and retention time in the gastrointestinal tract. However, absorption by the gastrointestinal tract is not sufficient. Therefore, strategies to improve the penetration of Slp-coated liposomes into epithelial cells should be developed in the future.

As Slp is a virulence factor, the toxicity and side effects of Slp in the circulation system and organs have to be identified. Further elucidation of the toxicity and side effects of different Slp molecules will lead to an enhanced design of Slp-coated liposome-based drug delivery systems for specific disease therapy. Thus, the usage of positively charged surfactants is crucial for the effective coating of Slp. However, positively charged surfactants display cytotoxicity in our bodies.

Positively charged surfactants can disrupt the cell membrane, thereby causing cell death. Hence, the usage of positively charged surfactants in various Slp-coated liposomes should be investigated in depth, and not only should the reasonable coating efficiency be considered, but the side effects or toxicity of the indispensable components in Slp-coated liposomes should also be taken into account. Compared with those of other supports such as metal nanoparticles and silicon supports , the rigidity and physicochemical stabilities of liposomes are slightly weak.

This disadvantage sometimes limits the use of liposomes as the support for Slp in various biomedical applications. Nevertheless, liposomes composed of phospholipid molecules have a typical biomimetic cell structure with good biocompatibility and biodegradability in vivo, which is not available in the case of other supports or nanoscale materials. Hence, we believe the Slp-coated liposomes have major advantages as in vivo biosensors or biocatalysts as well as diagnostic reagents. For industrial applications, a conventional liposome is usually produced by an aseptic technique due to its poor resistance to high temperature and pressure.

The more complicated structure of the Slp-coated liposome will cause major difficulties in industrial production, such as high technical barriers and high industrial cost. This issue is also an obstacle to the widespread application of Slp-coated liposomes. Although there are several challenges, given the considerable potential applications, it is worthwhile to devote more efforts to this promising multifunctional platform for drug delivery and biomedical applications.

In recent years, Slp has been gradually employed to construct novel biosensors for cancer diagnosis, detection of chemical ions, and nanoelectronic applications. With the extensive research on Slp, particularly the in-depth depiction of the mechanism of bacterial invasion of host epithelial cells, Slp has already been investigated as an antimicrobial agent for bacteria-induced gastrointestinal disease therapy.