Barnacle Cement Research Articles

Bioassays and virtual screening to identify potent natural antifouling compounds from the brown macroalga Dictyota dichotoma

Macroalgae are one of the potential natural sources for the isolation of novel eco-friendly antifouling compounds. In this study, the antifouling activity of an extract of the brown macroalga Dictyota dichotoma collected from the Red Sea was tested against bacteria isolated from the marine biofilm and larval forms of the barnacle. A maximum inhibition of barnacle larval settlement of 89.36% was observed in 25 µg ml-1 extract concentration at 24 h treatment. The secondary metabolite composition of the extract was analyzed by GC-MS and compounds were used as ligands for molecular docking with barnacle cement protein. The toxicity profile of secondary metabolites present in the extract was predicted through in silico analysis. The results indicate that the crude extract of the alga inhibited the biofilm formation by the bacteria and significantly reduced the settlement of the barnacle larvae. GC-MS analysis of the extract revealed the presence of five metabolites, including two fatty acids. All metabolites showed higher binding affinity with barnacle cement than the reference compound, copper. Among the secondary metabolites detected in the algal extract, the cholestane derivative exhibited maximum binding affinity (–14.2 kcal mol-1) with barnacle cement. The metabolites also showed positive for crustacean and fish toxicity in toxicity prediction using an in silico method.

An Overview on the Adhesion Mechanisms of Typical Aquatic Organisms and the Applications of Biomimetic Adhesives in Aquatic Environments.

Water molecules pose a significant obstacle to conventional adhesive materials. Nevertheless, some marine organisms can secrete bioadhesives with remarkable adhesion properties. For instance, mussels resist sea waves using byssal threads, sandcastle worms secrete sandcastle glue to construct shelters, and barnacles adhere to various surfaces using their barnacle cement. This work initially elucidates the process of underwater adhesion and the microstructure of bioadhesives in these three exemplary marine organisms. The formation of bioadhesive microstructures is intimately related to the aquatic environment. Subsequently, the adhesion mechanisms employed by mussel byssal threads, sandcastle glue, and barnacle cement are demonstrated at the molecular level. The comprehension of adhesion mechanisms has promoted various biomimetic adhesive systems: DOPA-based biomimetic adhesives inspired by the chemical composition of mussel byssal proteins; polyelectrolyte hydrogels enlightened by sandcastle glue and phase transitions; and novel biomimetic adhesives derived from the multiple interactions and nanofiber-like structures within barnacle cement. Underwater biomimetic adhesion continues to encounter multifaceted challenges despite notable advancements. Hence, this work examines the current challenges confronting underwater biomimetic adhesion in the last part, which provides novel perspectives and directions for future research.

Bio-inspired barnacle cement coating of biodegradable magnesium alloy for cerebrovascular application

Bio-inspired barnacle cement coating of biodegradable magnesium alloy for cerebrovascular application

Antifouling activities of proteinase K and α-amylase enzymes: Laboratory bioassays and in silico analysis

The application of enzymes as antifoulants is one of the environment-friendly strategies in biofouling management. In this study, antifouling activities of commercially available proteinase K and α-amylase enzymes were evaluated using barnacle larva and biofilm-forming bacteria as test organisms. The enzymes were also tested against barnacle cement protein through in silico analysis. The results showed that both enzymes inhibited the attachment of bacteria and settlement of barnacle larvae on the test surface. The lowest minimum inhibitory concentration of 0.312 mg ml−1 was exhibited by proteinase K against biofilm-forming bacteria. The calculated LC50 values for proteinase K and α-amylase against the barnacle nauplii were 91.8 and 230.96 mg ml−1 respectively. While α-amylase showed higher antibiofilm activity, proteinase K exhibited higher anti-larval settlement activity. Similarly, in silico analysis of the enzymes revealed promising anti-settlement activity, as the enzymes showed good binding scores with barnacle cement protein. Overall, the results suggested that the enzymes proteinase K and α-amylase could be used in antifouling coatings to reduce the settlement of biofouling on artificial materials in the marine environment.

Barnacle cement protein as an efficient bioinspired corrosion inhibitor

To prevent corrosion damage in aggressive environments such as seawater, metallic surfaces are coated with corrosion inhibitors usually made of organic molecules. Unfortunately, these inhibitors often exhibit environmental toxicity and are hazardous to natural habitats. Thus, developing greener and effective corrosion inhibitors is desirable. Here, we present an alternative green inhibitor, the recombinant protein rMrCP20 derived from the adhesive cement of the barnacle Megabalanus rosa and show that it efficiently protects mild steel against corrosion under high salt conditions mimicking the marine environment. We reveal that these anti-corrosion properties are linked to the protein’s biophysical properties, namely its strong adsorption to surfaces combined with its interaction with Fe ions released by steel substrates, which forms a stable layer that increases the coating’s impedance and delays corrosion. Our findings highlight the synergistic action of rMrCP20 in preventing corrosion and provide molecular-level guidelines to develop alternative green corrosion inhibitor additives.

Non-fibril amyloid aggregation at the air/water interface: self-adaptive pathway resulting in a 2D Janus nanofilm.

The amyloid states of proteins are implicated in several neurodegenerative diseases and bioadhesion processes. However, the classical amyloid fibrillization mechanism fails to adequately explain the formation of polymorphic aggregates and their adhesion to various surfaces. Herein, we report a non-fibril amyloid aggregation pathway, with disulfide-bond-reduced lysozyme (R-Lyz) as a model protein under quasi-physiological conditions. Very different from classical fibrillization, this pathway begins with the air-water interface (AWI) accelerated oligomerization of unfolded full-length protein, resulting in unique plate-like oligomers with self-adaptive ability, which can adjust their conformations to match various interfaces such as the asymmetric AWI and amyloid-protein film surface. The pathway enables a stepwise packing of the plate-like oligomers into a 2D Janus nanofilm, exhibiting a divergent distribution of hydrophilic/hydrophobic residues on opposite sides of the nanofilm. The resulting Janus nanofilm possesses a top-level Young's modulus (8.3 ± 0.6 GPa) among amyloid-based materials and exhibits adhesive strength two times higher (145 ± 81 kPa) than that of barnacle cement. Furthermore, we found that such an interface-directed pathway exists in several amyloidogenic proteins with a similar self-adaptive 2D-aggregation process, including bovine serum albumin, insulin, fibrinogen, hemoglobin, lactoferrin, and ovalbumin. Thus, our findings on the non-fibril self-adaptive mechanism for amyloid aggregation may shed light on polymorphic amyloid assembly and their adhesions through an alternative pathway.

A bioinspired synthetic fused protein adhesive from barnacle cement and spider dragline for potential biomedical materials

Biomaterials with excellent biocompatibility, mechanical performance, and self-recovery properties are urgently needed for tissue regeneration. Inspired by barnacle cement and spider silk, we genetically designed and overexpressed a fused protein (cp19k-MaSp1) composed of Megabalanus rosa (cp19k) and Nephila clavata dragline silk protein (MaSp1) in Pichia pastoris. The recombinant cp19k-MaSp1 exhibited enhanced adhesion capability beyond those of the individual proteins in both aqueous and non-aqueous conditions. cp19k-MaSp1 protein fiber scaffolds prepared through electrospinning have adequate hydrophilicity compared to cp19k and MaSp1 protein fiber scaffolds, and offer improved overall porosity compared to MaSp1 protein fiber scaffolds. The cp19k-MaSp1 protein fiber scaffolds showed excellent proteolytically stable properties because of only 9.6 % depletion after incubation in a biodegradation solution for 56 d. The cp19k-MaSp1 protein fiber scaffolds present remarkably high extreme tensile strength (112.7 ± 11.6 MPa) and superior ductility (438.4 ± 43.9 %) compared with cp19k (34.4 ± 8.1 MPa, 115.4 ± 32.7 %) and MaSp1 protein fiber scaffolds (65.8 ± 9.3 MPa, 409.6 ± 23.1 %), also 68.4 % of tensile strength was recovered by incubation in K+ buffer after multiple stretches, which create a favorable cell adhesion, growth, and proliferation environment for human umbilical vein endothelial cells (HUVECs). The improved biocompatibility, extensive adhesion, mechanical strength, and self-recovery properties make the bioinspired synthetic cp19k-MaSp1 a potential candidate for biomedical tissue reconstruction.

Adaptive Adhesions of Barnacle-Inspired Adhesive Peptides.

The strategy of robust adhesion employed by barnacles renders them fascinating biomimetic candidates for developing novel wet adhesives. Particularly, barnacle cement protein 19k (cp19k) has been speculated to be the key adhesive protein establishing the priming layer in the initial barnacle cement construction. In this work, we systematically studied the sequence design rationale of cp19k by designing adhesive peptides inspired by the low-complexity STGA-rich and the charged segments of cp19k. Combining structure analysis and the adhesion performance test, we found that cp19k-inspired adhesive peptides possess excellent disparate adhesion strategies for both hydrophilic mica and hydrophobic self-assembled monolayer surfaces. Specifically, the low-complexity STGA-rich segment offers great structure flexibility for surface adhesion, while the hydrophobic and charged residues can contribute to the adhesion of the peptides on hydrophobic and charged surfaces. The adaptive adhesion strategy identified in this work broadens our understanding of barnacle adhesion mechanisms and offers valuable insights for designing advanced wet adhesives with exceptional performance on various types of surfaces.

Synthesis of robust underwater glues from common proteins via unfolding-aggregating strategy

Underwater adhesive proteins secreted by organisms greatly inspires the development of underwater glue. However, except for specific proteins such as mussel adhesive protein, barnacle cement proteins, curli protein and their related recombinant proteins, it is believed that abundant common proteins cannot be converted into underwater glue. Here, we demonstrate that unfolded common proteins exhibit high affinity to surfaces and strong internal cohesion via amyloid-like aggregation in water. Using bovine serum albumin (BSA) as a model protein, we obtain a stable unfolded protein by cleaving the disulfide bonds and maintaining the unfolded state by means of stabilizing agents such as trifluoroethanol (TFE) and urea. The diffusion of stabilizing agents into water exposes the hydrophobic residues of an unfolded protein and initiates aggregation of the unfolded protein into a solid block. A robust and stable underwater glue can thus be prepared from tens of common proteins. This strategy deciphers a general code in common proteins to construct robust underwater glue from abundant biomass.

Self-assembly of a barnacle cement protein into intertwined amyloid fibres and determination of their adhesive and viscoelastic properties.

The stalked barnacle Pollicipes pollicipes uses a multi-protein cement to adhere to highly varied substrates in marine environments. We investigated the morphology and adhesiveness of a component 19 kDa protein in barnacle cement gland- and seawater-like conditions, using transmission electron microscopy and state-of-the art scanning probe techniques. The protein formed amyloid fibres after 5 days in gland-like but not seawater conditions. After 7-11 days, the fibres self-assembled under gland-like conditions into large intertwined fibrils of up to 10 µm in length and 200 nm in height, with a distinctive twisting of fibrils evident after 11 days. Atomic force microscopy (AFM)-nanodynamic mechanical analysis of the protein in wet conditions determined E' (elasticity), E'' (viscosity) and tan δ values of 2.8 MPa, 1.2 MPa and 0.37, respectively, indicating that the protein is a soft and viscoelastic material, while the adhesiveness of the unassembled protein and assembled fibres, measured using peak force quantitative nanomechanical mapping, was comparable to that of the commercial adhesive Cell-Tak™. The study provides a comprehensive insight into the nanomechanical and viscoelastic properties of the barnacle cement protein and its self-assembled fibres under native-like conditions and may have application in the design of amyloid fibril-based biomaterials or bioadhesives.

Barnacle-Inspired Wet Tissue Adhesive Hydrogels with Inherent Antibacterial Properties for Infected Wound Treatment.

Currently, antibiotics are the most common treatment for bacterial infections in clinical practice. However, with the abuse of antibiotics and the emergence of drug-resistant bacteria, the use of antibiotics has faced an unprecedented challenge. It is imminent to develop nonantibiotic antimicrobial agents. Based on the cation-π structure of barnacle cement protein, a polyphosphazene-based polymer poly[(N,N-dimethylethylenediamine)-g-(N,N,N,N-dimethylaminoethyl p-ammonium bromide (ammonium bromide)-g-(N,N,N,N-dimethylaminoethyl acetate ethylammonium bromide)] (PZBA) with potential adhesion and inherent antibacterial properties was synthesized, and a series of injectable antibacterial adhesive hydrogels (PZBA-PVA) were prepared by cross-linking with poly(vinyl alcohol) (PVA). PZBA-PVA hydrogels showed good biocompatibility, and the antibacterial rate of the best-performed hydrogel reached 99.81 ± 0.04% and 98.80 ± 2.16% against Staphylococcus aureus and Escherichia coli within 0.5 h in vitro, respectively. In the infected wound model, the healing rate of the PZBA-PVA-treated group was significantly higher than that of the Tegaderm film group due to the fact that the hydrogel suppressed inflammatory responses and modulated the infiltration of immune cells. Moreover, the wound healing mechanism of the PZBA-PVA hydrogel was further evaluated by real-time polymerase chain reaction and total RNA sequencing. The results indicated that the process of hemostasis and tissue development was prompted and the inflammatory and immune responses were suppressed to accelerate wound healing. Overall, the PZBA-PVA hydrogel is shown to have the potential for infected wound healing application.

A high-performance bio-based adhesive comprising soybean meal, silk fibroin, and tannic acid inspired by marine organisms

The sustainable development of high-performance bio-based adhesives is both important and challenging for the wood industry. Herein, inspired by the hydrophobic property of barnacle cement protein and the adhesive property of mussel adhesion protein, a water-resistant bio-based adhesive was developed from silk fibroin (SF) rich in hydrophobic β-sheet structures and tannic acid (TA) rich in catechol groups as reinforcing components and soybean meal molecules rich in reactive groups as substrates. SF and soybean meal molecules formed a water-resistant tough structure through a multiple cross-linking network including covalent bonds, hydrogen bonds, and dynamic borate ester bonds constructed by TA and borax. The wet bond strength for the developed adhesive achieved 1.20 MPa, exhibiting its excellent application capabilities in humid environments. The storage period of the developed adhesive (72 h) was 3 times that of pure soybean meal adhesive owing to the enhanced mold resistance of the adhesive by TA. Furthermore, the developed adhesive demonstrated excellent biodegradability (45.45 % weight loss in 30 days) and flame retardancy (limiting oxygen index of 30.1 %). Overall, this environmental and efficient biomimetic strategy provides a promising and feasible route to develop high-performance bio-based adhesives.

Self-assembling Bioadhesive Inspired by the Fourth Repetitive Sequence of Balanus albicostatus Cement Protein 20kDa (Balcp-20k).

Barnacle cement proteins are multi-protein complexes composed of a series of functionally related synergistic proteins that enable barnacles to adhere strongly and consistently to various underwater substrates. There is no post-translational modification of barnacle cement proteins, which provides a possibility for the synthesis of similar adhesive materials. Balcp-20k has four repetitive sequences with multiple conserved cysteine groups. Whether these repeats are separate functional units and the role of cysteine in adhesion is not clear. In order to investigate the adhesion properties of Balcp-20k, we amplified and expressed R4 (DHLACNAKHPCWHKHCDCFC)4, which is a quadruple repeat of Balcp-20k's fourth repetitive sequence, and S0R4 (DHLASNAKHPSWHKHSDSFS)4, all cysteine of R4 replaced by serine. Analysis showed that R4 had a similar structure to Balcp-20k, and the amyloid fibrils structure formed by self-assembly of R4 played an important role in improving the adhesion strength. The absence of disulfide bonds in S0R4 prevents self-assembly, and the failure of self-assembly after the reduction of disulfide bonds of R4 by DTT indicates that disulfide bonds play an important role in self-assembly. With adhesion and coating analysis, it was found that R4 has good adhesion on different materials surfaces, which is better than Balcp-20k, while S0R4 has weak adhesion, which is only better than BSA.

Hydration and antibiofouling of TMAO-derived zwitterionic polymers surfaces studied with atomistic molecular dynamics simulations

Zwitterionic polymers have emerged as a class of highly effective ultralow fouling materials for critical marine coating and biomedical applications. The recently developed trimethylamine N-oxide (TMAO)-derived zwitterionic polymers have demonstrated excellent antibiofouling capability in various chemical environments; however, it remains unclear how they interact with proteins at the microscopic level. To further investigate the antifouling mechanisms, we performed atomistic molecular dynamics (MD) simulations in combination with free-energy computations to provide an in-depth molecular understanding of the interactions of TMAO polymer brush (pTMAO) surfaces with proteins of opposite charges (positively charged lysozyme and negatively charged barnacle cement protein) in aqueous environments (pure water and saline solution). Our simulations revealed ordered structures of a condensed hydration water layer on the pTMAO surfaces in pure and saline water. The quantitative free energy analyses showed that the pTMAO surface has small protein desorption energy, but with a strong hydration energy barrier near the polymer surfaces to resist protein adsorption compared to other biofouling surfaces. The addition of salts only has a slight effect on the pTMAO surface’s exclusion of proteins due to the small interference of the structure of interfacial water. This study provides detailed knowledge of the strong surface hydration of zwitterionic polymers and its relation to salt impact, protein adsorption, and antibiofouling behavior of these important materials.

Advance in barnacle cement with high underwater adhesion

AbstractAdhesives play an important role in the areas of biomedicine and engineering manufacture. Barnacle cement is a polyprotein complex secreted by barnacle, which can bind with various kinds of underwater substances; therefore, becoming a hotspot of new bionic adhesive materials because of its superior adhesion. The low solubility and complicated secretion process of barnacle cement hinder current understanding of its components, physicochemical properties, synthetic process, and so forth. This review mainly summarizes the latest research advances and applicable potentials of barnacle cement characterized by rapid adhesion, uneasy degradation, polymerized curing in an underwater environment, and so forth, and provides reference for both research and development of bioinspired synthetic wet adhesives.

Short Peptides Derived from a Block Copolymer-like Barnacle Cement Protein Self-Assembled into Diverse Supramolecular Structures

Peptides capable of self-assembling into different supramolecular structures have potential applications in a variety of areas. The biomimetic molecular design offers an important avenue to discover novel self-assembling peptides. Despite this, a lot of biomimetic self-assembling peptides have been reported so far; to continually expand the scope of peptide self-assembly, it is necessary to find out more novel self-assembling peptides. Barnacle cp19k, a key underwater adhesive protein, shows special block copolymer-like characteristics and diversified self-assembly properties, providing an ideal template for biomimetic peptide design. In this study, inspired by Balanus albicostatus cp19k (Balcp19k), we rationally designed nine biomimetic peptides (P1-P9) and systematically studied their self-assembly behaviors for the first time. Combining microscale morphology observations and secondary structure analyses, we found that multiple biomimetic peptides derived from the central region and the C-terminus of Balcp19k form distinct supramolecular structures via different self-assembly mechanisms under acidic conditions. Specifically, P9 self-assembles into typical amyloid fibers. P7, which resembles ionic self-complementary peptides by containing nonstrictly alternating hydrophobic and charged amino acids, self-assembles into uniform, discrete nanofibers. P6 with amphipathic features forms twisted nanoribbons. Most interestingly, P4 self-assembles to form helical nanofibers and novel ring-shaped microstructures, showing unique self-assembly behaviors. Apart from their self-assembly properties, these peptides showed good cytocompatibility and demonstrated promising applications in biomedical areas. Our results expanded the repertoire of self-assembling peptides and provided new insights into the structure-function relationship of barnacle cp19k.

Adhesive Materials Inspired by Barnacle Underwater Adhesion: Biological Principles and Biomimetic Designs.

Wet adhesion technology has potential applications in various fields, especially in the biomedical field, yet it has not been completely mastered by humans. Many aquatic organisms (e.g., mussels, sandcastle worms, and barnacles) have evolved into wet adhesion specialists with excellent underwater adhesion abilities, and mimicking their adhesion principles to engineer artificial adhesive materials offers an important avenue to address the wet adhesion issue. The crustacean barnacle secretes a proteinaceous adhesive called barnacle cement, with which they firmly attach their bodies to almost any substrate underwater. Owing to the unique chemical composition, structural property, and adhesion mechanism, barnacle cement has attracted widespread research interest as a novel model for designing biomimetic adhesive materials, with significant progress being made. To further boost the development of barnacle cement–inspired adhesive materials (BCIAMs), it is necessary to systematically summarize their design strategies and research advances. However, no relevant reviews have been published yet. In this context, we presented a systematic review for the first time. First, we introduced the underwater adhesion principles of natural barnacle cement, which lay the basis for the design of BCIAMs. Subsequently, we classified the BCIAMs into three major categories according to the different design strategies and summarized their research advances in great detail. Finally, we discussed the research challenge and future trends of this field. We believe that this review can not only improve our understanding of the molecular mechanism of barnacle underwater adhesion but also accelerate the development of barnacle-inspired wet adhesion technology.

Mussel‐ and Barnacle Cement Proteins‐Inspired Dual‐Bionic Bioadhesive with Repeatable Wet‐Tissue Adhesion, Multimodal Self‐Healing, and Antibacterial Capability for Nonpressing Hemostasis and Promoted Wound Healing

AbstractMassive bleeding and wound infection are the major problems often observed during severe trauma, and achieving rapid hemostasis in cases of high‐dose bleeding in arteries and viscera remains an acute clinical demand. Herein, a mussel‐ and barnacle cement proteins‐inspired dual‐bionic hydrogel is first proposed. Benefiting from abundant phenolic hydroxyl groups, a tough dissipative matrix, removal of interfacial water, as well as dynamic redox balance of phenol‐quinone, the multinetwork hydrogel achieves repeatable robust wet‐tissue adhesiveness (151.40 ± 1.50 kPa), a fast multimodal self‐healing ability, and excellent antibacterial property against both Gram‐positive/negative bacteria. For rabbit/pig models of cardiac penetration holes and femoral artery injuries, the dual‐bionic bioadhesive shows better hemostatic efficiency than commercial gauze due to the synergistic effect of strong wound sealing capability, excellent red blood cell capturing property, and activation of hemostatic barrier membrane. More interestingly, the hydrogel combined with commercial hemostatic sponge presents accelerated wound healing as well as great potential for treating deep‐wound hemorrhage in a battlefield environment. Overall, owing to these unique advantages, the novel tissue‐adhesive hemostat opens up a new avenue to rapid sealing hemostasis and wound healing applications.

Enhanced bone regeneration by Aloe vera gel conjugated barnacle cement protein composite hyaluronic acid hydrogel based hydroxyapatite derived from cuttlefish bone

Injectable Aloe vera gel W (AGW®)-conjugated Barnacle Cement Protein (BCP) composite Hyaluronic Acid (HA) hydrogels provide local periodontal tissue for bone filling in periodontal surgery. We developed a novel type of injectable self-supported hydrogel (2 mg/ml of AGW®-BCP/HA) based cuttlefish bone derived hydroxyapatite (CBH) for dental graft, which could good handling property, biodegradation or biocompatibility with the hydrogel disassembly and provided efficient cell adhesion activity and no inflammatory responses. Herein, the aim of this work was to evaluate bone formation following implantation of CBH and collagen membrane in rabbit calvarias defects. Eight male New Zealand rabbits were used and four circular calvarias defects were created on each animal. Defects were filled with different graft materials: 1) collagen membrane, 2) collagen membrane with CBH, 3) collagen membrane with bovine bone hydroxyapatite (BBH), and 4) control. The animals were sacrificed after 2 and 8 weeks of healing periods for histologic analysis. Both sites receiving CBH and BBH showed statistically increased augmented volume and new bone formation (p<0.05). However, there was no statistical difference in new bone formation between the CBH, BBH and collagen membrane group at all healing periods. Within the limits of this study, collagen membrane with CBH was an effective material for bone formation and space maintaining in rabbit calvarias defects.

Design of a genetically programmed barnacle-curli inspired living-cell bioadhesive.

In nature, barnacles and bacterial biofilms utilize self-assembly amyloid to achieve strong and robust interface adhesion. However, there is still a lack of sufficient research on the construction of macroscopic adhesives based on amyloid-like nanostructures through reasonable molecular design. Here, we report a genetically programmed self-assembly living-cell bioadhesive inspired by barnacle and curli system. Firstly, the encoding genes of two natural adhesion proteins (CsgA and cp19k) derived from E. coli curli and barnacle cement were fused and expressed as a fundamental building block of the bioadhesive. Utilizing the natural curli system of E. coli, fusion protein can be delivered to cell surface and self-assemble into an amyloid nanofibrous network. Then, the E. coli cells were incorporated into the molecular chain network of xanthan gum (XG) through covalent conjugation to produce a living-cell bioadhesive. The shear adhesive strength of the bioadhesive to the surface of the aluminum sheet reaches 278 ​kPa. Benefiting from living cells encapsulated inside, the bioadhesive can self-regenerate with adequate nutrients. This adhesive has low toxicity to organisms, strong resistance to the liquid environment in vivo, easy to pump, exhibiting potential application prospects in biomedical fields such as intestinal soft tissue repair.