Self-Assembly Behavior of Collagen and Its Composite Materials: Preparation, Characterizations, and Biomedical Engineering and Allied Applications
Abstract
:1. Introduction
2. Structures and Properties of Collagen
2.1. Biosynthesis and Extraction of Collagen
2.2. Structure of Collagen
2.3. Properties of Collagen
3. Self-Assembly Behavior of Collagen
3.1. Self-Assembly Mechanism of Collagen
3.2. Factors Affecting Collagen Self-Assembly
3.2.1. Collagen Concentration
3.2.2. Temperature
3.2.3. pH
3.2.4. Substrates
3.3. Characterization Methods of Collagen Self-Assembly
4. Collagen-Based Composite Materials
4.1. Preparation of Collagen-Based Composite Materials
4.1.1. Collagen-Based Fiber Materials
4.1.2. Collagen-Based Film Materials
4.1.3. Collagen-Based Scaffold Materials
4.2. Modification of Collagen-Based Composite Materials
4.3. Application of Collagen-Based Composite Materials
4.3.1. Biomedical Engineering
4.3.2. Food Engineering
4.3.3. Cosmetics
4.3.4. Others
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Sorushanova, A.; Delgado, L.M.; Wu, Z.; Shologu, N.; Kshirsagar, A.; Raghunath, R.; Mullen, A.M.; Bayon, Y.; Pandit, A.; Raghunath, M.; et al. The collagen suprafamily: From biosynthesis to advanced biomaterial development. Adv. Mater. 2019, 31, e1801651. [Google Scholar] [CrossRef] [PubMed]
- Ramachandran, G.N.; Kartha, G. Structure of collagen. Nature 1955, 176, 593–595. [Google Scholar] [CrossRef] [PubMed]
- Sherman, V.R.; Yang, W.; Meyers, M.A. The materials science of collagen. J. Mech. Behav. Biomed. Mater. 2015, 52, 22–50. [Google Scholar] [CrossRef] [PubMed]
- Gordon, M.K.; Hahn, R.A. Collagens. Cell Tissue Res. 2010, 339, 247–257. [Google Scholar] [CrossRef]
- Gross, J.; Schmitt, F.O. The structure of human skin collagen as studied with the electron microscope. J. Exp. Med. 1948, 88, 555. [Google Scholar] [CrossRef]
- Ricard-Blum, S. The collagen family. Cold Spring Harb. Perspect. Biol. 2011, 3, a004978. [Google Scholar] [CrossRef]
- Kavitha, O.; Thampan, R.V. Factors influencing collagen biosynthesis. J. Cell. Biochem. 2008, 104, 1150–1160. [Google Scholar] [CrossRef]
- Hulmes, D.J.S. Building collagen molecules, fibrils, and suprafibrillar structures. J. Struct. Biol. 2002, 137, 2–10. [Google Scholar] [CrossRef] [PubMed]
- Gelse, K.; Poschl, E.; Aigner, T. Collagens—Structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 2003, 55, 1531–1546. [Google Scholar] [CrossRef]
- Shoulders, M.D.; Raines, R.T. Collagen structure and stability. Annu. Rev. Biochem. 2009, 78, 929–958. [Google Scholar] [CrossRef]
- Kuwahara, J. Extraction of type I collagen from tilapia scales using acetic acid and ultrafine bubbles. Processes 2021, 9, 288. [Google Scholar] [CrossRef]
- Solazzo, C.; Courel, B.; Connan, J.; van Dongen, B.E.; Barden, H.; Penkman, K.; Taylor, S.; Demarchi, B.; Adam, P.; Schaeffer, P.; et al. Identification of the earliest collagen- and plant-based coatings from Neolithic artefacts (Nahal Hemar cave, Israel). Sci. Rep. 2016, 6, 31053. [Google Scholar] [CrossRef] [PubMed]
- Jafari, H.; Lista, A.; Siekapen, M.M.; Ghaffari-Bohlouli, P.; Nie, L.; Alimoradi, H.; Shavandi, A. Fish collagen: Extraction, characterization, and applications for biomaterials engineering. Polymers 2020, 12, 2230. [Google Scholar] [CrossRef]
- Noorzai, S.; Verbeek, C.J.R.; Lay, M.C.; Swan, J. Collagen extraction from various waste bovine hide sources. Waste Biomass Valorization 2020, 11, 5687–5698. [Google Scholar] [CrossRef]
- Rodriguez, F.; Moran, L.; Gonzalez, G.; Troncoso, E.; Zuniga, R.N. Collagen extraction from mussel byssus: A new marine collagen source with physicochemical properties of industrial interest. J. Food Sci. Technol.-Mysore 2017, 54, 1228–1238. [Google Scholar] [CrossRef]
- Ahmed, M.; Verma, A.K.; Patel, R. Collagen extraction and recent biological activities of collagen peptides derived from sea-food waste: A review. Sustain. Chem. Pharm. 2020, 18, 100315. [Google Scholar] [CrossRef]
- Zhang, L.; Li, Z.J.; Xiao, Y.L.; Liu, Z.J.; Pei, Y.; Wang, G.Z.; Tang, K.Y. Dissolution of collagen fibers from tannery solid wastes in salt aqueous solutions: Hofmeister series evaluation. J. Chem. Technol. Biotechnol. 2020, 95, 1225–1233. [Google Scholar] [CrossRef]
- Okur, H.I.; Hladilkova, J.; Rembert, K.B.; Cho, Y.; Heyda, J.; Dzubiella, J.; Cremer, P.S.; Jungwirth, P. Beyond the hofmeister series: Ion-specific effects on proteins and their biological functions. J. Phys. Chem. B 2017, 121, 1997–2014. [Google Scholar] [CrossRef]
- Kunz, W. Specific ion effects in colloidal and biological systems. Curr. Opin. Colloid Interface Sci. 2010, 15, 34–39. [Google Scholar] [CrossRef]
- Russell, A.E. Effect of pH on thermal stability of collagen in the dispersed and aggregated states. Biochem. J. 1974, 137, 599–602. [Google Scholar] [CrossRef]
- Adibzadeh, N.; Aminzadeh, S.; Jamili, S.; Karkhane, A.A.; Farrokhi, N. Purification and characterization of pepsin-solubilized collagen from skin of sea cucumber holothuria parva. Appl. Biochem. Biotechnol. 2014, 173, 143–154. [Google Scholar] [CrossRef] [PubMed]
- Olsen, D.; Jiang, J.; Chang, R.; Duffy, R.; Sakaguchi, M.; Leigh, S.; Lundgard, R.; Ju, J.; Buschman, F.; Truong-Le, V.; et al. Expression and characterization of a low molecular weight recombinant human gelatin: Development of a substitute for animal-derived gelatin with superior features. Protein Expr. Purif. 2005, 40, 346–357. [Google Scholar] [CrossRef] [PubMed]
- Luo, Y.e.; Mu, T.; Fan, D. Preparation of a low-cost minimal medium for engineered Escherichia coli with high yield of human-like collagen II. Pak. J. Pharm. Sci. 2014, 27, 663–669. [Google Scholar] [PubMed]
- Liu, X.H.; Zheng, C.; Luo, X.M.; Wang, X.C.; Jiang, H. Recent advances of collagen-based biomaterials: Multi-hierarchical structure, modification and biomedical applications. Mater. Sci. Eng. C-Mater. Biol. Appl. 2019, 99, 1509–1522. [Google Scholar] [CrossRef] [PubMed]
- Jones, E.Y.; Miller, A. Analysis of structural design features in collagen. J. Mol. Biol. 1991, 218, 209–219. [Google Scholar] [CrossRef]
- Zhu, S.; Yuan, Q.; Yin, T.; You, J.; Gu, Z.; Xiong, S.; Hu, Y. Self-assembly of collagen-based biomaterials: Preparation, characterizations and biomedical applications. J. Mater. Chem. B 2018, 6, 2650–2676. [Google Scholar] [CrossRef]
- Nomura, S.; Hiltner, A.; Lando, J.B.; Baer, E. Interaction of water with native collagen. Biopolymers 1977, 16, 231–246. [Google Scholar] [CrossRef]
- Znidarsic, W.J.; Chen, I.W.; Shastri, V.P. Zeta-potential characterization of collagen and bovine serum albumin modified silica nanoparticles: A comparative study. J. Mater. Sci. 2009, 44, 1374–1380. [Google Scholar] [CrossRef]
- Xu, J.; Liu, F.; Wang, T.; Goff, H.D.; Zhong, F. Fabrication of films with tailored properties by regulating the swelling of collagen fiber through pH adjustment. Food Hydrocoll. 2020, 108, 106016. [Google Scholar] [CrossRef]
- Bruckner, P.; Eikenberry, E.F.; Prockop, D.J. Formation of the Triple Helix of Type I Procollagen in cellulo. A Kinetic Model Based on cis-trans Isomerization of Peptide Bonds. Eur. J. Biochem. 1981, 118, 607–613. [Google Scholar] [CrossRef]
- Burjanadze, T.V.; Kisiriya, E.L. Dependence of thermal stability on the number of hydrogen bonds in water-bridged collagen structure. Biopolymers 1982, 21, 1695–1701. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.P.; Douglas, E.P. Effects of various salts on structural polymorphism of reconstituted type I collagen fibrils. Colloids Surf. B 2013, 112, 42–50. [Google Scholar] [CrossRef]
- Rai, R.K.; Singh, C.; Sinha, N. Predominant role of water in native collagen assembly inside the bone matrix. J. Phys. Chem. B 2015, 119, 201–211. [Google Scholar] [CrossRef] [PubMed]
- McGuinness, K.; Khan, I.J.; Nanda, V. Morphological diversity and polymorphism of self-assembling collagen peptides controlled by length of hydrophobic domains. ACS Nano 2014, 8, 12514–12523. [Google Scholar] [CrossRef]
- Sinthusamran, S.; Benjakul, S.; Kishimura, H. Comparative study on molecular characteristics of acid soluble collagens from skin and swim bladder of seabass (Lates calcarifer). Food Chem. 2013, 138, 2435–2441. [Google Scholar] [CrossRef]
- Liu, D.S.; Liang, L.; Regenstein, J.M.; Zhou, P. Extraction and characterisation of pepsin-solubilised collagen from fins, scales, skins, bones and swim bladders of bighead carp (Hypophthalmichthys nobilis). Food Chem. 2012, 133, 1441–1448. [Google Scholar] [CrossRef]
- Jarvinen, T.A.H.; Jarvinen, T.L.N.; Kannus, B.B.; Jozsa, L.; Jarvinen, M. Collagen fibres of the spontaneously ruptured human tendons display decreased thickness and crimp angle. J. Orthop. Res. 2004, 22, 1303–1309. [Google Scholar] [CrossRef]
- Franchi, M.; Trire, A.; Quaranta, M.; Orsini, E.; Ottani, V. Collagen structure of tendon relates to function. Sci. World J. 2007, 7, 404–420. [Google Scholar] [CrossRef] [PubMed]
- Reichenberger, E.; Olsen, B.R. Collagens as organizers of extracellular matrix during morphogenesis. Semin. Cell Dev. Biol. 1996, 7, 631–638. [Google Scholar] [CrossRef]
- Kurniawan, N.A.; Wong, L.H.; Rajagopalan, R. Early stiffening and softening of collagen: Interplay of deformation mechanisms in biopolymer networks. Biomacromolecules 2012, 13, 691–698. [Google Scholar] [CrossRef]
- Fratzl, P.; Misof, K.; Zizak, I.; Rapp, G.; Amenitsch, H.; Bernstorff, S. Fibrillar structure and mechanical properties of collagen. J. Struct. Biol. 1998, 122, 119–122. [Google Scholar] [CrossRef] [PubMed]
- Pins, G.D.; Christiansen, D.L.; Patel, R.; Silver, F.H. Self-assembly of collagen fibers. Influence of fibrillar alignment and decorin on mechanical properties. Biophys. J. 1997, 73, 2164–2172. [Google Scholar] [CrossRef] [PubMed]
- Wilks, B.T.; Evans, E.B.; Nakhla, M.N.; Morgan, J.R. Directing fibroblast self-assembly to fabricate highly-aligned, collagen-rich matrices. Acta Biomater. 2018, 81, 70–79. [Google Scholar] [CrossRef]
- Jiang, F.Z.; Horber, H.; Howard, J.; Muller, D.J. Assembly of collagen into microribbons: Effects of pH and electrolytes. J. Struct. Biol. 2004, 148, 268–278. [Google Scholar] [CrossRef]
- Elmi, F.; Elmi, M.M.; Amiri, F.N. Thermodynamic parameters and influence of kinetic factors on the self-assembly of acid-soluble collagen nanofibrils. Food Biophys. 2017, 12, 365–373. [Google Scholar] [CrossRef]
- Yue, C.; Ding, C.; Su, J.; Cheng, B. Effect of copper and zinc ions on type I collagen self-assembly. Int. J. Polym. Anal. Charact. 2022, 27, 394–408. [Google Scholar] [CrossRef]
- Li, Y.; Asadi, A.; Monroe, M.R.; Douglas, E.P. pH effects on collagen fibrillogenesis in vitro: Electrostatic interactions and phosphate binding. Mater. Sci. Eng. C 2009, 29, 1643–1649. [Google Scholar] [CrossRef]
- Yan, M.; Li, B.; Zhao, X.; Qin, S. Effect of concentration, pH and ionic strength on the kinetic self-assembly of acid-soluble collagen from walleye pollock (Theragra chalcogramma) skin. Food Hydrocoll. 2012, 29, 199–204. [Google Scholar] [CrossRef]
- Farber, S.; Garg, A.K.; Birk, D.E.; Silver, F.H. Collagen fibrillogenesis in vitro: Evidence for pre-nucleation and nucleation steps. Int. J. Biol. Macromol. 1986, 8, 37–42. [Google Scholar] [CrossRef]
- Wood, G.C.; Keech, M.K. The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: Kinetic and electron-microscope studies. Biochem. J. 1960, 75, 588–598. [Google Scholar] [CrossRef]
- Wood, G.C. The formation of fibrils from collagen solutions. 2. A mechanism for collagen-fibril formation. Biochem. J. 1960, 75, 598–605. [Google Scholar] [CrossRef] [PubMed]
- Wood, G.C. The formation of fibrils from collagen solutions. 3. Effect of chondroitin sulphate and some other naturally occurring polyanions on the rate of formation. Biochem. J. 1960, 75, 605–612. [Google Scholar] [CrossRef] [PubMed]
- Goh, M.C.; Paige, M.F.; Gale, M.A.; Yadegari, I.; Edirisinghe, M.; Strzelczyk, J. Fibril formation in collagen. Phys. A 1997, 239, 95–102. [Google Scholar] [CrossRef]
- Dan, W.H.; Chen, Y.N.; Dan, N.H.; Zheng, X.; Wang, L.; Yang, C.K.; Huang, Y.P.; Liu, X.H.; Hu, Y. Multi-level collagen aggregates and their applications in biomedical applications. Int. J. Polym. Anal. Charact. 2019, 24, 667–683. [Google Scholar] [CrossRef]
- Liu, X.H.; Zheng, M.H.; Wang, X.C.; Luo, X.M.; Hou, M.D.; Yue, O. Biofabrication and characterization of collagens with different hierarchical architectures. ACS Biomater. Sci. Eng. 2020, 6, 739–748. [Google Scholar] [CrossRef] [PubMed]
- Fang, M.; Goldstein, E.L.; Matich, E.K.; Orr, B.G.; Holl, M.M.B. Type I collagen self-assembly: The roles of substrate and concentration. Langmuir 2013, 29, 2330–2338. [Google Scholar] [CrossRef]
- Huelin, S.D.; Baker, H.R.; Poduska, K.M.; Erika, F.; Merschrod, S. Aggregation and adsorption of type I collagen near an electrified interface. Macromolecules 2007, 40, 8440–8444. [Google Scholar] [CrossRef]
- Noitup, P.; Morrissey, M.T.; Garnjanagoonchorn, W. In vitro self-assembly of silver-line grunt type I collagen: Effects of collagen concentrations, pH and temperatures on collagen self-assembly. J. Food Biochem. 2006, 30, 547–555. [Google Scholar] [CrossRef]
- Na, G.C.; Phillips, L.J.; Freire, E. In vitro collagen fibril assembly: Thermodynamic studies. Biochemistry 1989, 28, 7153–7161. [Google Scholar] [CrossRef]
- de Wild, M.; Pomp, W.; Koenderink, G.H. Thermal memory in self-assembled collagen fibril networks. Biophys. J. 2013, 105, 200–210. [Google Scholar] [CrossRef]
- Li, Y.L.; Qiao, C.D.; Shi, L.; Jiang, Q.W.; Li, T.D. Viscosity of collagen solutions: Influence of concentration, temperature, adsorption, and role of intermolecular interactions. J. Macromol. Sci. Part B Phys. 2014, 53, 893–901. [Google Scholar] [CrossRef]
- Meiners, F.; Ahlers, M.; Brand, I.; Wittstock, G. Impact of temperature and electrical potentials on the stability and structure of collagen adsorbed on the gold electrode. Surf. Sci. 2015, 631, 220–228. [Google Scholar] [CrossRef]
- Song, X.; Wang, Z.; Tao, S.; Li, G.; Zhu, J. Observing effects of calcium/magnesium ions and pH value on the self-assembly of extracted swine tendon collagen by atomic force microscopy. J. Food Qual. 2017, 2017, 925706. [Google Scholar] [CrossRef]
- Yadavalli, V.K.; Svintradze, D.V.; Pidaparti, R.M. Nanoscale measurements of the assembly of collagen to fibrils. Int. J. Biol. Macromol. 2010, 46, 458–464. [Google Scholar] [CrossRef]
- Dehsorkhi, A.; Castelletto, V.; Hamley, I.W.; Adamcik, J.; Mezzenga, R. The effect of pH on the self-assembly of a collagen derived peptide amphiphile. Soft Matter 2013, 9, 6033–6036. [Google Scholar] [CrossRef]
- Dupont-Gillain, C.C. Understanding and controlling type I collagen adsorption and assembly at interfaces, and application to cell engineering. Colloids Surf. B 2014, 124, 87–96. [Google Scholar] [CrossRef]
- Narayanan, B.; Gilmer, G.H.; Tao, J.; De Yoreo, J.J.; Ciobanu, C.V. Self-assembly of collagen on flat surfaces: The interplay of collagen-collagen and collagen-substrate interactions. Langmuir 2014, 30, 1343–1350. [Google Scholar] [CrossRef]
- Torbet, J.; Malbouyres, M.; Builles, N.; Justin, V.; Roulet, M.; Damour, O.; Oldberg, A.; Ruggieo, F.; Hulmes, D.J.S. Orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction. Biomaterials 2007, 28, 4268–4276. [Google Scholar] [CrossRef]
- Lowack, K.; Helm, C.A. Molecular mechanisms controlling the self-assembly process of polyelectrolyte multilayers. Macromolecules 1998, 31, 823–833. [Google Scholar] [CrossRef]
- Chung, E.J.; Jakus, A.E.; Shah, R.N. In situ forming collagen-hyaluronic acid membrane structures: Mechanism of self-assembly and applications in regenerative medicine. Acta Biomater. 2013, 9, 5153–5161. [Google Scholar] [CrossRef]
- Friess, W.; Schlapp, M. Effects of processing conditions on the rheological behavior of collagen dispersions. Eur. J. Pharm. Biopharm. 2001, 51, 259–265. [Google Scholar] [CrossRef] [PubMed]
- Yue, C.; Ding, C.; Cheng, B.; Du, X.; Su, J. Preparation of collagen/aspartic acid nanocomposite fibers and their self-assembly behaviors. J. Nat. Fibers 2022, 19, 8830–8841. [Google Scholar] [CrossRef]
- Yue, C.; Ding, C.; Du, X.; Wang, Y.; Su, J.; Cheng, B. Self-assembly of collagen fibrils on graphene oxide and their hybrid nanocomposite films. Int. J. Biol. Macromol. 2021, 193, 173–182. [Google Scholar] [CrossRef]
- Stylianou, A. Assessing collagen D-band periodicity with atomic force microscopy. Materials 2022, 15, 1608. [Google Scholar] [CrossRef]
- Stamov, D.R.; Stock, E.; Franz, C.M.; Jaehnke, T.; Haschke, H. Imaging collagen type I fibrillogenesis with high spatiotemporal resolution. Ultmi 2015, 149, 86–94. [Google Scholar] [CrossRef] [PubMed]
- Nudelman, F.; Pieterse, K.; George, A.; Bomans, P.P.; Friedrich, H.; Brylka, L.J.; Hilbers, P.A.J.; Sommerdijk, N.A.J.M. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. 2010, 9, 1004–1009. [Google Scholar] [CrossRef]
- Mesquita, J.P.d.; Patrício, P.S.d.O.; Donnici, C.L.; Petri, D.F.S.; Oliveira, L.C.A.; Pereira, F.V. Hybrid layer-by-layer assembly based on animal and vegetable structural materials: Multilayered films of collagen and cellulose nanowhiskers. Soft Matter 2011, 7, 4405–4413. [Google Scholar] [CrossRef]
- Krishnamoorthy, G.; Selvakumar, R.; Sastry, T.P.; Mandal, A.B.; Doble, M. Effect of D-amino acids on collagen fibrillar assembly and stability: Experimental and modelling studies. Biochem. Eng. J. 2013, 75, 92–100. [Google Scholar] [CrossRef]
- Kezwon, A.; Wojciechowski, K. Collagen-surfactant mixtures at fluid/fluid interfaces. Colloids Surf. A Physicochem. Eng. Asp. 2016, 509, 390–400. [Google Scholar] [CrossRef]
- Zeng, S.; Yin, J.; Yang, S.; Zhang, C.; Yang, P.; Wu, W. Structure and characteristics of acid and pepsin-solubilized collagens from the skin of cobia (Rachycentron canadum). Food Chem. 2012, 135, 1975–1984. [Google Scholar] [CrossRef]
- Pal, G.K.; Suresh, P.V. Comparative assessment of physico-chemical characteristics and fibril formation capacity of thermostable carp scales collagen. Mater. Sci. Eng. C-Mater. Biol. Appl. 2017, 70, 32–40. [Google Scholar] [CrossRef] [PubMed]
- Tonndorf, R.; Aibibu, D.; Cherif, C. Collagen multifilament spinning. Mater. Sci. Eng. C 2020, 106, 110105. [Google Scholar] [CrossRef] [PubMed]
- Bazrafshan, Z.; Stylios, G.K. Spinnability of collagen as a biomimetic material: A review. Int. J. Biol. Macromol. 2019, 129, 693–705. [Google Scholar] [CrossRef]
- DeFrates, K.G.; Moore, R.; Borgesi, J.; Lin, G.; Mulderig, T.; Beachley, V.; Hu, X. Protein-based fiber materials in medicine: A review. Nanomaterials 2018, 8, 457. [Google Scholar] [CrossRef] [PubMed]
- Yue, C.; Qin, X.; Hu, M.; Zhang, R.; Cheng, B. Microfluidic wet spinning of antibacterial collagen composite fibers supported by chelate effect of tannic acid with silver ions. React. Funct. Polym. 2024, 194, 105798. [Google Scholar] [CrossRef]
- Zhang, Z.; Zhao, X.Z.; Song, Z.Y.; Wang, L.; Gao, J. Electrospun collagen/chitosan composite fibrous membranes for accelerating wound healing. Biomed. Mater. 2024, 19, 055024. [Google Scholar] [CrossRef] [PubMed]
- Zhang, F.; Lu, Q.; Yue, X.; Zuo, B.; Qin, M.; Li, F.; Kaplan, D.L.; Zhang, X. Regeneration of high-quality silk fibroin fiber by wet spinning from CaCl2-formic acid solvent. Acta Biomater. 2015, 12, 139–145. [Google Scholar] [CrossRef]
- Green, E.C.; Zhang, Y.; Li, H.; Minus, M.L. Gel-spinning of mimetic collagen and collagen/nano-carbon fibers: Understanding multi-scale influences onmolecular ordering and fibril alignment. J. Mech. Behav. Biomed. Mater. 2017, 65, 552–564. [Google Scholar] [CrossRef] [PubMed]
- Ding, C.; Du, J.; Cao, Y.; Yue, C.; Cheng, B. Effects of the aspect ratio of multi-walled carbon nanotubes on the structure and properties of regenerated collagen fibers. Int. J. Biol. Macromol. 2019, 126, 595–602. [Google Scholar] [CrossRef]
- Yue, C.; Ding, C.; Du, X.; Cheng, B. Novel collagen/GO-MWNT hybrid fibers with improved strength and toughness by dry-jet wet spinning. Compos. Interfaces 2022, 29, 413–429. [Google Scholar] [CrossRef]
- Dems, D.; Rodrigues da Silva, J.; Hélary, C.; Wien, F.; Marchand, M.; Debons, N.; Muller, L.; Chen, Y.; Schanne-Klein, M.-C.; Laberty-Robert, C.; et al. Native collagen: Electrospinning of pure, cross-linker-free, self-supported membrane. ACS Appl. Bio Mater. 2020, 3, 2948–2957. [Google Scholar] [CrossRef] [PubMed]
- Zimba, B.L.; Wang, M.; Hao, J.; Yu, X.; Li, Y.; Chen, C.; Xiong, G.; Wu, Q. Preparation of collagen/carboxylated graphene oxide nanofibrous membranes by electrospinning and their hemocompatibilities. Mater. Res. Express 2019, 6, 105415. [Google Scholar] [CrossRef]
- Sun, J.; Chen, J.S.; Liu, K.; Zeng, H.B. Mechanically strong proteinaceous fibers: Engineered fabrication by microfluidics. Engineering 2021, 7, 615–623. [Google Scholar] [CrossRef]
- Kang, E.; Jeong, G.S.; Choi, Y.Y.; Lee, K.H.; Khademhosseini, A.; Lee, S.H. Digitally tunable physicochemical coding of material composition and topography in continuous microfibres. Nat. Mater. 2011, 10, 877–883. [Google Scholar] [CrossRef] [PubMed]
- Rosen, T.; Hsiao, B.S.; Soderberg, L.D. Elucidating the opportunities and challenges for nanocellulose spinning. Adv. Mater. 2021, 33, 2001238. [Google Scholar] [CrossRef]
- Du, X.-Y.; Li, Q.; Wu, G.; Chen, S. Multifunctional micro/nanoscale fibers based on microfluidic spinning technology. Adv. Mater. 2019, 31, 1903733. [Google Scholar] [CrossRef]
- Koster, S.; Evans, H.M.; Wong, J.Y.; Pfohl, T. An in situ study of collagen self-assembly processes. Biomacromolecules 2008, 9, 199–207. [Google Scholar] [CrossRef]
- Haynl, C.; Hofmann, E.; Pawar, K.; Foerster, S.; Scheibel, T. Microfluidics-produced collagen fibers show extraordinary mechanical properties. Nano Lett. 2016, 16, 5917–5922. [Google Scholar] [CrossRef]
- Suurs, P.; Barbut, S. Collagen use for co-extruded sausage casings—A review. Trends Food Sci. Technol. 2020, 102, 91–101. [Google Scholar] [CrossRef]
- Voicu, G.; Geanaliu-Nicolae, R.-E.; Pirvan, A.-A.; Andronescu, E.; Iordache, F. Synthesis, characterization and bioevaluation of drug-collagen hybrid materials for biomedical applications. Int. J. Pharm. 2016, 510, 474–484. [Google Scholar] [CrossRef]
- Peng, X.; Cui, Y.; Chen, J.; Gao, C.; Yang, Y.; Yu, W.; Rai, K.; Zhang, M.; Nian, R.; Bao, Z.; et al. High-strength collagen-based composite films regulated by water-soluble recombinant spider silk proteins and water annealing. ACS Biomater. Sci. Eng. 2022, 8, 3341–3353. [Google Scholar] [CrossRef]
- Jing, X.; Li, X.; Jiang, Y.F.; Zhao, R.H.; Ding, Q.J.; Han, W.J. Excellent coating of collagen fiber/chitosan-based materials that is water-and oil-resistant and fluorine-free. Carbohydr. Polym. 2021, 266, 118173. [Google Scholar] [CrossRef] [PubMed]
- Yue, C.; Ding, C.; Yang, N.; Luo, Y.; Su, J.; Cao, L.; Cheng, B. Strong and tough collagen/cellulose nanofibril composite films via the synergistic effect of hydrogen and metal–ligand bonds. Eur. Polym. J. 2022, 180, 111628. [Google Scholar] [CrossRef]
- Yang, S.; Shi, X.X.; Li, X.M.; Wang, J.F.; Wang, Y.L.; Luo, Y.F. Oriented collagen fiber membranes formed through counter-rotating extrusion and their application in tendon regeneration. Biomaterials 2019, 207, 61–75. [Google Scholar] [CrossRef] [PubMed]
- Lu, H.C.; Liu, Y.S.; Yang, Y.J.; Li, L. Preparation of poly (vinyl alcohol)/gelatin composites via in-situ thermal/mechanochemical degradation of collagen fibers during melt extrusion: Effect of extrusion temperature. J. Polym. Res. 2017, 24, 203. [Google Scholar] [CrossRef]
- Andonegi, M.; Heras, K.L.; Santos-Vizcaino, E.; Igartua, M.; Hernandez, R.M.; de la Caba, K.; Guerrero, P. Structure-properties relationship of chitosan/collagen films with potential for biomedical applications. Carbohydr. Polym. 2020, 237, 116159. [Google Scholar] [CrossRef]
- Perez-Puyana, V.; Romero, A.; Guerrero, A. Influence of collagen concentration and glutaraldehyde on collagen-based scaffold properties. J. Biomed. Mater. Res. Part A 2016, 104, 1462–1468. [Google Scholar] [CrossRef] [PubMed]
- Moxon, S.R.; Corbett, N.J.; Fisher, K.; Potjewyd, G.; Domingos, M.; Hooper, N.M. Blended alginate/collagen hydrogels promote neurogenesis and neuronal maturation. Mater. Sci. Eng. C-Mater. Biol. Appl. 2019, 104, 109904. [Google Scholar] [CrossRef]
- Bai, Z.X.; Wang, T.Y.; Zheng, X.; Huang, Y.P.; Chen, Y.N.; Dan, W.H. High strength and bioactivity polyvinyl alcohol/collagen composite hydrogel with tannic acid as cross-linker. Polym. Eng. Sci. 2021, 61, 278–287. [Google Scholar] [CrossRef]
- Ding, C.; Tian, M.; Feng, R.; Dang, Y.; Zhang, M. Novel self-healing hydrogel with injectable, pH-responsive, strain-sensitive, promoting wound-healing, and hemostatic properties based on collagen and chitosan. ACS Biomater. Sci. Eng. 2020, 6, 3855–3867. [Google Scholar] [CrossRef]
- Yue, C.; Xu, M.; Zhong, L.; Tang, S.; Cai, G.; Zhang, R.; Cheng, B. pH-responsive release features of collagen/carboxylated cellulose nanofiber composite aerogels through the incorporation of cyclodextrin/5-fluorouracil inclusion complexes. Eur. Polym. J. 2024, 207, 112807. [Google Scholar] [CrossRef]
- Zhang, W.B.; Pan, Z.Y.; Ma, J.Z.; Wei, L.F.; Chen, Z.; Wang, O. Degradable cross-linked collagen fiber/MXene composite aerogels as a high-performing sensitive pressure sensor. ACS Sustain. Chem. Eng. 2021, 10, 1408–1418. [Google Scholar] [CrossRef]
- Pot, M.W.; Faraj, K.A.; Adawy, A.; van Enckevort, W.J.P.; van Moerkerk, H.T.B.; Vlieg, E.; Daamen, W.F.; van Kuppevelt, T.H. Versatile wedge-based system for the construction of unidirectional collagen scaffolds by directional freezing: Practical and theoretical considerations. ACS Appl. Mater. Interfaces 2015, 7, 8495–8505. [Google Scholar] [CrossRef] [PubMed]
- Mekonnen, B.T.; Ragothaman, M.; Kalirajan, C.; Palanisamy, T. Conducting collagen-polypyrrole hybrid aerogels made from animal skin waste. RSC Adv. 2016, 6, 63071–63077. [Google Scholar] [CrossRef]
- Adamiak, K.; Sionkowska, A. Current methods of collagen cross-linking: Review. Int. J. Biol. Macromol. 2020, 161, 550–560. [Google Scholar] [CrossRef] [PubMed]
- Kikuchi, M.; Matsumoto, H.N.; Yamada, T.; Koyama, Y.; Takakuda, K.; Tanaka, J. Glutaraldehyde cross-linked hydroxyapatite/collagen self-organized nanocomposites. Biomaterials 2004, 25, 63–69. [Google Scholar] [CrossRef]
- Tian, Z.H.; Li, C.H.; Duan, L.; Li, G.Y. Physicochemical properties of collagen solutions cross-linked by glutaraldehyde. Connect. Tissue Res. 2014, 55, 239–247. [Google Scholar] [CrossRef]
- Sundararaghavan, H.G.; Monteiro, G.A.; Lapin, N.A.; Chabal, Y.J.; Miksan, J.R.; Shreiber, D.I. Genipin-induced changes in collagen gels: Correlation of mechanical properties to fluorescence. J. Biomed. Mater. Res. Part A 2008, 87A, 308–320. [Google Scholar] [CrossRef] [PubMed]
- Usha, R.; Sreeram, K.J.; Rajaram, A. Stabilization of collagen with EDC/NHS in the presence of L-lysine: A comprehensive study. Colloids Surf. B 2012, 90, 83–90. [Google Scholar] [CrossRef]
- Mu, C.; Liu, F.; Cheng, Q.; Li, H.; Wu, B.; Zhang, G.; Lin, W. Collagen cryogel cross-linked by dialdehyde starch. Macromol. Mater. Eng. 2010, 295, 100–107. [Google Scholar] [CrossRef]
- Haugh, M.G.; Jaasma, M.J.; O’Brien, F.J. The effect of dehydrothermal treatment on the mechanical and structural properties of collagen-GAG scaffolds. J. Biomed. Mater. Res. Part A 2009, 89A, 363–369. [Google Scholar] [CrossRef] [PubMed]
- Weadock, K.S.; Miller, E.J.; Bellincampi, L.D.; Zawadsky, J.P.; Dunn, M.G. Physical crosslinking of collagen fibers: Comparison of ultraviolet irradiation and dehydrothermal treatment. J. Biomed. Mater. Res. 1995, 29, 1373–1379. [Google Scholar] [CrossRef]
- Drexler, J.W.; Powell, H.M. Dehydrothermal crosslinking of electrospun collagen. Tissue Eng. Part C Methods 2010, 17, 9–17. [Google Scholar] [CrossRef] [PubMed]
- Song, X.; Dong, P.; Gravesande, J.; Cheng, B.; Xing, J. UV-mediated solid-state cross-linking of electrospinning nanofibers of modified collagen. Int. J. Biol. Macromol. 2018, 120, 2086–2093. [Google Scholar] [CrossRef] [PubMed]
- Reyna-Urrutia, V.A.; Mata-Haro, V.; Cauich-Rodriguez, J.V.; Herrera-Kao, W.A.; Cervantes-Uc, J.M. Effect of two crosslinking methods on the physicochemical and biological properties of the collagen-chitosan scaffolds. Eur. Polym. J. 2019, 117, 424–433. [Google Scholar] [CrossRef]
- Jafari-Sabet, M.; Nasiri, H.; Ataee, R. The effect of cross-linking agents and collagen concentrations on properties of collagen scaffolds. J. Arch. Mil. Med. 2016, 4, e42367. [Google Scholar] [CrossRef]
- Luo, X.; Guo, Z.; He, P.; Chen, T.; Li, L.; Ding, S.; Li, H. Study on structure, mechanical property and cell cytocompatibility of electrospun collagen nanofibers crosslinked by common agents. Int. J. Biol. Macromol. 2018, 113, 476–486. [Google Scholar] [CrossRef]
- Weadock, K.S.; Miller, E.J.; Keuffel, E.L.; Dunn, M.G. Effect of physical crosslinking methods on collagen-fiber durability in proteolytic solutions. J. Biomed. Mater. Res. 1996, 32, 221–226. [Google Scholar] [CrossRef]
- Ming-Che, W.; Pins, G.D.; Silver, F.H. Collagen fibres with improved strength for the repair of soft tissue injuries. Biomaterials 1994, 15, 507–512. [Google Scholar] [CrossRef]
- Hu, T.Y.; Lo, A.C.Y. Collagen-alginate composite hydrogel: Application in tissue engineering and biomedical sciences. Polymers 2021, 13, 1852. [Google Scholar] [CrossRef]
- Chen, Z.Y.; Fan, D.D.; Shang, L.J. Exploring the potential of the recombinant human collagens for biomedical and clinical applications: A short review. Biomed. Mater. 2021, 16, 012001. [Google Scholar] [CrossRef]
- Sionkowska, A.; Adamiak, K.; Musial, K.; Gadomska, M. Collagen based materials in cosmetic applications: A review. Materials 2020, 13, 4217. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez, M.I.A.; Barroso, L.G.R.; Sanchez, M.L. Collagen: A review on its sources and potential cosmetic applications. J. Cosmet. Dermatol. 2018, 17, 20–26. [Google Scholar] [CrossRef]
- Wang, Y.; Wang, Z.; Dong, Y. Collagen-based biomaterials for tissue engineering. ACS Biomater. Sci. Eng. 2023, 9, 1132–1150. [Google Scholar] [CrossRef] [PubMed]
- Xiao, H.; Wang, Y.; Hao, B.; Cao, Y.; Cui, Y.; Huang, X.; Shi, B. Collagen fiber-based advanced separation materials: Recent developments and future perspectives. Adv. Mater. 2022, 34, 2107891. [Google Scholar] [CrossRef]
- Zheng, M.H.; Wang, X.C.; Chen, Y.N.; Yue, O.Y.; Bai, Z.X.; Cui, B.Q.; Jiang, H.; Liu, X.H. A review of recent progress on collagen-based biomaterials. Adv. Healthc. Mater. 2022, 12, 2202042. [Google Scholar] [CrossRef] [PubMed]
- Lim, Y.S.; Ok, Y.J.; Hwang, S.Y.; Kwak, J.Y.; Yoon, S. Marine collagen as a promising biomaterial for biomedical applications. Mar. Drugs 2019, 17, 467. [Google Scholar] [CrossRef]
- Gu, L.S.; Shan, T.T.; Ma, Y.X.; Tay, F.R.; Niu, L.N. Novel biomedical applications of crosslinked collagen. Trends Biotechnol. 2019, 37, 464–491. [Google Scholar] [CrossRef] [PubMed]
- Coradin, T.; Wang, K.; Law, T.; Trichet, L. Type I collagen-fibrin mixed hydrogels: Preparation, properties and biomedical applications. Gels 2020, 6, 36. [Google Scholar] [CrossRef]
- Shekhter, A.B.; Fayzullin, A.L.; Vukolova, M.N.; Rudenko, T.G.; Osipycheva, V.D.; Litvitsky, P.F. Medical applications of collagen and collagen-based materials. Curr. Med. Chem. 2019, 26, 506–516. [Google Scholar] [CrossRef]
- Rahman, M.A. Collagen of extracellular matrix from marine invertebrates and its medical applications. Mar. Drugs 2019, 17, 118. [Google Scholar] [CrossRef] [PubMed]
- Law, J.X.; Liau, L.L.; Saim, A.; Yang, Y.; Idrus, R. Electrospun collagen nanofibers and their applications in skin tissue engineering. Tissue Eng. Regen. Med. 2017, 14, 699–718. [Google Scholar] [CrossRef] [PubMed]
- Kanungo, I.; Fathima, N.N.; Rao, J.R.; Nair, B.U. Influence of PCL on the material properties of collagen based biocomposites and in vitro evaluation of drug release. Mater. Sci. Eng. C-Mater. Biol. Appl. 2013, 33, 4651–4659. [Google Scholar] [CrossRef] [PubMed]
- Chattopadhyay, S.; Raines, R.T. Collagen-based biomaterials for wound healing. Biopolymers 2014, 101, 821–833. [Google Scholar] [CrossRef]
- Guo, B.; Dong, R.; Liang, Y.; Li, M. Haemostatic materials for wound healing applications. Nat. Rev. Chem. 2021, 5, 773–791. [Google Scholar] [CrossRef]
- Manon-Jensen, T.; Kjeld, N.G.; Karsdal, M.A. Collagen-mediated hemostasis. J. Thromb. Haemost. 2016, 14, 438–448. [Google Scholar] [CrossRef]
- Yan, X.; Chen, Y.; Dan, N.; Dan, W. A novel thermosensitive growth-promoting collagen fibers composite hemostatic gel. J. Mater. Chem. B 2022, 10, 4070–4082. [Google Scholar] [CrossRef]
- Chen, Q.-Z.; Harding, S.E.; Ali, N.N.; Lyon, A.R.; Boccaccini, A.R. Biomaterials in cardiac tissue engineering: Ten years of research survey. Mater. Sci. Eng. R Rep. 2008, 59, 1–37. [Google Scholar] [CrossRef]
- Subhan, F.; Hussain, Z.; Tauseef, I.; Shehzad, A.; Wahid, F. A review on recent advances and applications of fish collagen. Crit. Rev. Food Sci. Nutr. 2021, 61, 1027–1037. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Yan, H.; Zhang, J.; Tian, B.; Li, W.; Xiao, J. Agarose-collagen composite microsphere implants: A biocompatible and robust approach for skin tissue regeneration. Int. J. Biol. Macromol. 2024, 277, 134510. [Google Scholar] [CrossRef]
- Jin, H.; Zhu, X.; Liu, H.; Wang, L.; Liu, S.; Zhang, H. Type-I collagen polypeptide-based composite nanofiber membranes for fast and efficient bone regeneration. ACS Biomater. Sci. Eng. 2024, 10, 5632–5640. [Google Scholar] [CrossRef] [PubMed]
- Vijayalekha, A.; Anandasadagopan, S.K.; Pandurangan, A.K. An overview of collagen-based composite scaffold for bone tissue engineering. Appl. Biochem. Biotechnol. 2023, 195, 4617–4636. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Li, G. A biomimetic mineralized collagen hydrogel containing uniformly distributed and highly abundant dopamine-modified hydroxyapatite particles for bone tissue engineering. J. Appl. Polym. Sci. 2024, 141, e55567. [Google Scholar] [CrossRef]
- Balachandran Megha, K.; Syama, S.; Padmalayathil Sangeetha, V.; Vandana, U.; Oyane, A.; Valappil Mohanan, P. Development of a 3D multifunctional collagen scaffold impregnated with peptide LL-37 for vascularised bone tissue regeneration. Int. J. Pharm. 2024, 652, 123797. [Google Scholar] [CrossRef] [PubMed]
- Yao, L.Y.; Hu, Y.; Liu, Z.; Ding, X.; Tian, J.; Xiao, J.X. Luminescent lanthanide-collagen peptide framework for pH-controlled drug delivery. Mol. Pharm. 2019, 16, 846–855. [Google Scholar] [CrossRef]
- Kim, H.S.; Kim, S.J.; Kang, J.H.; Shin, U.S. Positively and negatively charged collagen nanohydrogels: pH-responsive drug-releasing characteristics. Bull. Korean Chem. Soc. 2018, 39, 477–482. [Google Scholar] [CrossRef]
- Yue, C.; Ding, C.; Hu, M.; Zhang, R.; Cheng, B. Collagen/functionalized cellulose nanofibril composite aerogels with pH-responsive characteristics for drug delivery system. Int. J. Biol. Macromol. 2024, 261, 129650. [Google Scholar] [CrossRef]
- Padekan, B.; Dadvand Koohi, A.; Akbari Dogolsar, M. Collagen-based hydrogel with incorporated nano-hydroxyapatite for the delivery of a poorly water-soluble drug. J. Macromol. Sci. Part B 2024, 1–20. [Google Scholar] [CrossRef]
- Princy; Kaur, D.; Kaur, A. Engineering of electrospun polycaprolactone/polyvinyl alcohol-collagen based 3D nano scaffolds and their drug release kinetics using cetirizine as a model drug. Int. J. Biol. Macromol. 2024, 268, 131847. [Google Scholar] [CrossRef]
- Leon-Lopez, A.; Morales-Penaloza, A.; Martinez-Juarez, V.M.; Vargas-Torres, A.; Zeugolis, D.I.; Aguirre-Alvarez, G. Hydrolyzed collagen-sources and applications. Molecules 2019, 24, 4031. [Google Scholar] [CrossRef]
- Nguyen, T.T.; Heimann, K.; Zhang, W. Protein recovery from underutilised marine bioresources for product development with nutraceutical and pharmaceutical bioactivities. Mar. Drugs 2020, 18, 391. [Google Scholar] [CrossRef] [PubMed]
- Irastorza, A.; Zarandona, I.; Andonegi, M.; Guerrero, P.; de la Caba, K. The versatility of collagen and chitosan: From food to biomedical applications. Food Hydrocoll. 2021, 116, 106633. [Google Scholar] [CrossRef]
- Mao, Q.; Zhuo, Y.; Luo, S.; Li, J.; Hu, F.; Zhao, Q. Preparation and characterisation of fish skin collagen–chitosan–cinnamon essential oil composite film. Int. J. Food Sci. Technol. 2024, 59, 6087–6101. [Google Scholar] [CrossRef]
- Mitura, S.; Sionkowska, A.; Jaiswal, A. Biopolymers for hydrogels in cosmetics: Review. J. Mater. Sci. Mater. Med. 2020, 31, 50. [Google Scholar] [CrossRef] [PubMed]
- Niu, J.; Shao, R.; Liu, M.; Zan, Y.; Dou, M.; Liu, J.; Zhang, Z.; Huang, Y.; Wang, F. Porous carbons derived from collagen-enriched biomass: Tailored design, synthesis, and application in electrochemical energy storage and conversion. Adv. Funct. Mater. 2019, 29, 1905095. [Google Scholar] [CrossRef]
- Liu, H.; Cao, Y.; Wang, F.; Huang, Y. Nitrogen-Doped Hierarchical Lamellar Porous Carbon Synthesized from the Fish Scale As Support Material for Platinum Nanoparticle Electrocatalyst toward the Oxygen Reduction Reaction. ACS Appl. Mater. Interfaces 2014, 6, 819–825. [Google Scholar] [CrossRef]
- Hooshvar, M.; Bagheri Marandi, G.; Taghvay Nakhjiri, M. Collagen-based hydrogel nanocomposite as adsorbent for methylene blue and crystal violet removal from aqueous solution: Isotherm, kinetic, and thermodynamic studies. Water Air Soil Pollut. 2024, 235, 161. [Google Scholar] [CrossRef]
- Zhou, J.; Du, X.; Lu, K.; Xiao, A. MXene@polydopamine/oxidized sodium alginate modified collagen composite aerogel as sustainable bio-adsorbent for heavy metal ion adsorption and solar driven water evaporation. Sep. Purif. Technol. 2025, 354, 129045. [Google Scholar] [CrossRef]
- Andonegi, M.; Correia, D.M.; Pereira, N.; Fernandes, M.M.; Costa, C.M.; Lanceros-Mendez, S.; de la Caba, K.; Guerrero, P. Sustainable antibacterial collagen composites with silver nanowires for resistive pressure sensor applications. Eur. Polym. J. 2023, 200, 112494. [Google Scholar] [CrossRef]
- Andonegi, M.; Correia, D.M.; Pereira, N.; Costa, C.M.; Lanceros-Mendez, S.; de la Caba, K.; Guerrero, P. Sustainable collagen composites with graphene oxide for bending resistive sensing. Polymers 2023, 15, 3855. [Google Scholar] [CrossRef]
Classification | Possible Mechanism | Ref. | |
---|---|---|---|
Chemical modification | GA | GA–protein cross-links are formed through reaction of ε-amine groups of lysine or hydroxylysine residues with the aldehyde group of GA. | [107,116,117] |
Genipin | (i) Fast nucleophilic attack of amine groups on lysine and arginine on the C3 atom of genipin, which leads to the formation of a heterocyclic compound of genipin connected with basic residues of proteins; (ii) Slow nucleophilic substitution of the ester groups in genipin which produces a secondary amide connection. | [118] | |
EDC/NHS | The cross-linking reaction of collagen with the use of EDC/NHS induces the formation of a covalent bond between carboxylic acid groups from aspartic and glutamic acid. | [119] | |
Dialdehyde starch | Dialdehyde starch aldehyde groups interact with the free amino group of collagen during the cross-linking reaction. | [120] | |
Physical modification | Dehydrothermal | Under vacuum conditions, water molecules are removed which causes the formation of intramolecular links (amide bonds) between collagen. | [121,122,123] |
UV light | This process involves the formation of free radicals on aromatic groups of tyrosine and phenylalanine, and radicals interact with each other and form chemical bonds form. | [124] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yue, C.; Ding, C.; Xu, M.; Hu, M.; Zhang, R. Self-Assembly Behavior of Collagen and Its Composite Materials: Preparation, Characterizations, and Biomedical Engineering and Allied Applications. Gels 2024, 10, 642. https://doi.org/10.3390/gels10100642
Yue C, Ding C, Xu M, Hu M, Zhang R. Self-Assembly Behavior of Collagen and Its Composite Materials: Preparation, Characterizations, and Biomedical Engineering and Allied Applications. Gels. 2024; 10(10):642. https://doi.org/10.3390/gels10100642
Chicago/Turabian StyleYue, Chengfei, Changkun Ding, Minjie Xu, Min Hu, and Ruquan Zhang. 2024. "Self-Assembly Behavior of Collagen and Its Composite Materials: Preparation, Characterizations, and Biomedical Engineering and Allied Applications" Gels 10, no. 10: 642. https://doi.org/10.3390/gels10100642
APA StyleYue, C., Ding, C., Xu, M., Hu, M., & Zhang, R. (2024). Self-Assembly Behavior of Collagen and Its Composite Materials: Preparation, Characterizations, and Biomedical Engineering and Allied Applications. Gels, 10(10), 642. https://doi.org/10.3390/gels10100642