Application of marine collagen for stem‑cell‑based therapy and tissue regeneration (Review)

Liu,Chao

doi:10.3892/mi.2021.5

Application of marine collagen for stem‑cell‑based therapy and tissue regeneration (Review)

Authors:
- Chao Liu
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Affiliations: Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, P.R. China
Published online on: June 23, 2021 https://doi.org/10.3892/mi.2021.5
Article Number: 6
Copyright: © Liu . This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Tissue engineering and regenerative medicine is becoming an important component in modern biological scientific research. Tissue engineering, a branch of regenerative medicine, is a field that is actively developing to meet the challenges presented in biomedical applications. This particularly applies to the research area of stem cells and biomaterials, due to both being pivotal determinants for the successful restoration or regeneration of damaged tissues and organs. Recently, the development of innovative marine collagen‑based biomaterials has attracted attention due to the reported environmentally friendly properties, the lack of zoonotic disease transmission, biocompatibility, bioactivity, the lack of ethics‑related concerns and cost‑effectiveness for manufacturing. The present review aimed to summarize the potential application and function of marine collagen in stem cell research in a medical and clinical setting. In addition, the present review cited recent studies regarding the latest research advances into using marine collagen for cartilage, bone, periodontal and corneal regeneration. It also characterized the distinct advantages of using marine collagen for stem cell‑based tissue repair and regeneration. In addition, the present review comprehensively discussed the most up to date information on stem cell biology, particularly the possibility of treating stem cells with marine collagen to maximize their multi‑directional differentiation capability, which highlights the potential use of marine collagen in regenerative medicine. Furthermore, recent research progress on the potential immunomodulatory capacity of mesenchymal stem cells following treatment with marine collagen to improve the understanding of cell‑matrix interactions was investigated. Finally, perspectives on the possible future research directions for the application of marine collagen in the area of regenerative medicine are provided.

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1	Caddeo S, Boffito M and Sartori S: Tissue engineering approaches in the design of healthy and pathological in vitro tissue models. Front Bioeng Biotechnol. 5(40)2017.PubMed/NCBI View Article : Google Scholar
2	Cossu G, Birchall M, Brown T, De Coppi P, Culme-Seymour E, Gibbon S, Hitchcock J, Mason C, Montgomery J, Morris S, et al: Lancet commission: Stem cells and regenerative medicine. Lancet. 391:883–910. 2018.PubMed/NCBI View Article : Google Scholar
3	La Noce M, Paino F, Spina A, Naddeo P, Montella R, Desiderio V, De Rosa A, Papaccio G, Tirino V and Laino L: Dental pulp stem cells: State of the art and suggestions for a true translation of research into therapy. J Dent. 42:761–768. 2014.PubMed/NCBI View Article : Google Scholar
4	Tsutsui TW: Dental pulp stem cells: Advances to applications. Stem Cells Cloning. 13:33–42. 2020.PubMed/NCBI View Article : Google Scholar
5	Glotzbach JP, Wong VW, Gurtner GC and Longaker MT: Regenerative medicine. Curr Probl Surg. 48:148–212. 2011.PubMed/NCBI View Article : Google Scholar
6	Subhan F, Hussain Z, Tauseef I, Shehzad A and Wahid F: A review on recent advances and applications of fish collagen. Crit Rev Food Sci Nutr. 61:1027–1037. 2021.PubMed/NCBI View Article : Google Scholar
7	Tziveleka LA, Ioannou E, Tsiourvas D, Berillis P, Foufa E and Roussis V: Collagen from the marine sponges Axinella Cannabina and Suberites Carnosus: Isolation and morphological, biochemical, and biophysical characterization. Mar Drugs. 15(152)2017.PubMed/NCBI View Article : Google Scholar
8	Jafari H, Lista A, Siekapen MM, Ghaffari-Bohlouli P, Nie L, Alimoradi H and Shavandi A: Fish collagen: Extraction, characterization, and applications for biomaterials engineering. Polymers (Basel). 12(2230)2020.PubMed/NCBI View Article : Google Scholar
9	Adamiak K, Lewandowska K and Sionkowska A: The infuence of salicin on rheological and film-forming properties of collagen. Molecules. 26(1661)2021.PubMed/NCBI View Article : Google Scholar
10	Liu C, Liu X, Xue Y, Ding TT and Sun J: Hydrolyzed tilapia fish collagen modulates the biological behavior of macrophages under inflammatory conditions. RSC Adv. 5:30727–30736. 2015.
11	Senaratne LS, Park PJ and Kim SK: Isolation and characterization of collagen from brown backed toadfish (Lagocephalus gloveri) skin. Bioresour Technol. 97:191–197. 2006.PubMed/NCBI View Article : Google Scholar
12	Alves A, Marques A, Martins E, Silva T and Reis R: Cosmetic potential of marine fish skin collagen. Cosmetics. 4(39)2017.
13	Muralidharan N, Jeya Shakila R, Sukumar D and Jeyasekaran G: Skin, bone and muscle collagen extraction from the trash fish, leather jacket (Odonus niger) and their characterization. J Food Sci Technol. 50:1106–1113. 2013.PubMed/NCBI View Article : Google Scholar
14	Aguirre-Cruz G, León-López A, Cruz-Gómez V, Jiménez-Alvarado R and Aguirre-Álvarez G: Collagen hydrolysates for skin protection: Oral administration and topical formulation. Antioxidants (Basel). 9(181)2020.PubMed/NCBI View Article : Google Scholar
15	Liu C, Xue Y and Sun J: Hydrolyzed fish collagen inhibits inflammatory cytokines secretion in lipopolysaccharide-induced HUVECs. Adv Materials Res. 1025-1026:570–573. 2014.
16	Nurilmala M, Hizbullah HH, Karnia E, Kusumaningtyas E and Ochiai Y: Characterization and antioxidant activity of collagen, gelatin, and the derived peptides from yellowfin tuna (Thunnus albacares) Skin. Mar Drugs. 18(98)2020.PubMed/NCBI View Article : Google Scholar
17	Liu C and Sun J: Marine based biomaterial-fish collagen enhances the polarization of human macrophage. IOP Conf Ser Mater Sci Eng. 1040(012006)2021.
18	Guo L, Harnedy PA, Zhang L, Li B, Zhang Z, Hou H, Zhao X and FitzGerald RJ: In vitro assessment of the multifunctional bioactive potential of Alaska pollock skin collagen following simulated gastrointestinal digestion. J Sci Food Agric. 95:1514–1520. 2015.PubMed/NCBI View Article : Google Scholar
19	Liu C and Sun J: Fish collagen promotes proliferation and inhibits the inflammation in human epidermal keratinocytes in vitro. BIBE2020: In: Proceedings of the Fourth International Conference on Biological Information and Biomedical Engineering. Association for Computing Machinery, New York, NY, 2020.
20	Meyer M: Processing of collagen based biomaterials and the resulting materials properties. Biomed Eng Online. 18(24)2019.PubMed/NCBI View Article : Google Scholar
21	Cumming MH, Hall B and Hofman K: Isolation and characterisation of major and minor collagens from hyaline cartilage of hoki (Macruronus novaezelandiae). Mar Drugs. 17(223)2019.PubMed/NCBI View Article : Google Scholar
22	Sripriya R and Kumar R: A novel enzymatic method for preparation and characterization of collagen film from swim bladder of fish rohu (Labeo rohita). Food Nutr Sci. 6:1468–1478. 2015.
23	Subhan F, Ikram M, Shehzad A and Ghafoor A: Marine Collagen: An emerging player in biomedical applications. J Food Sci Technol. 52:4703–4707. 2015.PubMed/NCBI View Article : Google Scholar
24	Avila Rodríguez MI, Rodríguez Barroso LG and Sánchez ML: Collagen: A review on its sources and potential cosmetic applications. J Cosmet Dermatol. 17:20–26. 2018.PubMed/NCBI View Article : Google Scholar
25	Bornes TD, Adesida AB and Jomha NM: Mesenchymal stem cells in the treatment of traumatic articular cartilage defects: A comprehensive review. Arthritis Res Ther. 16(432)2014.PubMed/NCBI View Article : Google Scholar
26	Armiento AR, Stoddart MJ, Alini M and Eglin D: Biomaterials for articular cartilage tissue engineering: Learning from biology. Acta Biomater. 65:1–20. 2018.PubMed/NCBI View Article : Google Scholar
27	Raabe O, Reich C, Wenisch S, Hild A, Burg-Roderfeld M, Siebert HC and Arnhold S: Hydrolyzed fish collagen induced chondrogenic differentiation of equine adipose tissue-derived stromal cells. Histochem Cell Biol. 134:545–554. 2010.PubMed/NCBI View Article : Google Scholar
28	Hoyer B, Bernhardt A, Lode A, Heinemann S, Sewing J, Klinger M, Notbohm H and Gelinsky M: Jellyfish collagen scaffolds for cartilage tissue engineering. Acta Biomater. 10:883–892. 2014.PubMed/NCBI View Article : Google Scholar
29	Pustlauk W, Paul B, Gelinsky M and Bernhardt A: Jellyfish collagen and alginate: Combined marine materials for superior chondrogenesis of hMSC. Mater Sci Eng C Mater Biol Appl. 64:190–198. 2016.PubMed/NCBI View Article : Google Scholar
30	Pugliano M, Vanbellinghen X, Schwinté P, Benkirane-Jessel N and Keller L: Combined jellyfish collagen type ii, human stem cells and tgf-Β3 as a therapeutic implant for cartilage repair. J Stem Cell Res Ther. 7(2)2017.
31	Wang J, He C, Cheng N, Yang Q, Chen M, You L and Zhang Q: Bone marrow stem cells response to Collagen/Single-Wall carbon nanotubes-COOHs nanocomposite films with transforming growth factor beta 1. J Nanosci Nanotechnol. 15:4844–4850. 2015.PubMed/NCBI View Article : Google Scholar
32	Diogo GS, Carneiro F, Freitas-Ribeiro S, Sotelo CG, Pérez-Martín RI, Pirraco RP, Reis RL and Silva TH: Prionace glauca skin collagen bioengineered constructs as a promising approach to trigger cartilage regeneration. Mater Sci Eng C Mater Biol Appl. 120(111587)2021.PubMed/NCBI View Article : Google Scholar
33	Hsu HH, Uemura T, Yamaguchi I, Ikoma T and Tanaka J: Chondrogenic differentiation of human mesenchymal stem cells on fish scale collagen. J Biosci Bioeng. 122:219–225. 2016.PubMed/NCBI View Article : Google Scholar
34	Pereira HF, Cengiz IF, Silva FS, Reis RL and Oliveira JM: Scaffolds and coatings for bone regeneration. J Mater Sci Mater Med. 31(27)2020.PubMed/NCBI View Article : Google Scholar
35	Safari B, Aghanejad A, Roshangar L and Davaran S: Osteogenic effects of the bioactive small molecules and minerals in the scaffold-based bone tissue engineering. Colloids Surf B Biointerfaces. 198(111462)2021.PubMed/NCBI View Article : Google Scholar
36	Jin S, Sun F, Zou Q, Huang J, Zuo Y, Li Y, Wang S, Cheng L, Man Y, Yang F and Li J: Fish collagen and hydroxyapatite reinforced poly(lactide-co-glycolide) Fibrous membrane for guided bone regeneration. Biomacromolecules. 20:2058–2067. 2019.PubMed/NCBI View Article : Google Scholar
37	Liu C and Sun J: Potential application of hydrolyzed fish collagen for inducing the multidirectional differentiation of rat bone marrow mesenchymal stem cells. Biomacromolecules. 15:436–443. 2014.PubMed/NCBI View Article : Google Scholar
38	Oh GW, Nguyen VT, Heo SY, Ko SC, Kim CS, Park WS, Choi IW and Jung WK: 3D PCL/fish collagen composite scaffolds incorporating osteogenic abalone protein hydrolysates for bone regeneration application: In vitro and in vivo studies. J Biomater Sci Polym Ed. 32:355–371. 2021.PubMed/NCBI View Article : Google Scholar
39	Matsumoto R, Uemura T, Xu Z, Yamaguchi I, Ikoma T and Tanaka J: Rapid oriented fibril formation of fish scale collagen facilitates early osteoblastic differentiation of human mesenchymal stem cells. J Biomed Mater Res A. 103:2531–2539. 2015.PubMed/NCBI View Article : Google Scholar
40	Oh HH, Uemura T, Yamaguchi I, Ikoma T and Tanaka J: Effect of enzymatically cross-linked tilapia scale collagen for osteoblastic differentiation of human mesenchymal stem cells. J Bioactive Compatible Polymers. 31:31–41. 2016.
41	Elango J, Saravanakumar K, Rahman SU, Henrotin Y, Regenstein JM, Wu W and Bao B: Chitosan-Collagen 3D matrix mimics trabecular bone and regulates RANKL-Mediated paracrine cues of differentiated osteoblast and mesenchymal stem cells for bone marrow macrophage-Derived osteoclastogenesis. Biomolecules. 9(173)2019.PubMed/NCBI View Article : Google Scholar
42	Hodgson EE, Wilson SM and Moore JW: Changing estuaries and impacts on juvenile salmon: A systematic review. Glob Chang Biol. 26:1986–2001. 2020.PubMed/NCBI View Article : Google Scholar
43	Hoyer B, Bernhardt A, Heinemann S, Stachel I, Meyer M and Gelinsky M: Biomimetically mineralized salmon collagen scaffolds for application in bone tissue engineering. Biomacromolecules. 13:1059–1066. 2012.PubMed/NCBI View Article : Google Scholar
44	Raftery RM, Woods B, Marques ALP, Moreira-Silva J, Silva TH, Cryan SA, Reis RL and O'Brien FJ: Multifunctional biomaterials from the sea: Assessing the effects of chitosan incorporation into collagen scaffolds on mechanical and biological functionality. Acta Biomater. 43:160–169. 2016.PubMed/NCBI View Article : Google Scholar
45	Bailleul D, Mackenzie A, Sacchi O, Poisson F, Bierne N and Arnaud-Haond S: Large-scale genetic panmixia in the blue shark (Prionace glauca): A single worldwide population, or a genetic lag-time effect of the ‘grey zone’ of differentiation? Evol Appl. 11:614–630. 2018.PubMed/NCBI View Article : Google Scholar
46	Blanco M, Sanz N, Valcarcel J, Pérez-Martín RI and Sotelo CG: Does Subunit Composition influence the intermolecular crosslinking of fish collagen? A Study with hake and blue shark skin collagens. Polymers (Basel). 12(1734)2020.PubMed/NCBI View Article : Google Scholar
47	Elango J, Lee JW, Wang S, Henrotin Y, de Val JEMS, M Regenstein J, Lim SY, Bao B and Wu W: Evaluation of differentiated bone cells proliferation by blue shark skin collagen via biochemical for bone tissue engineering. Mar Drugs. 16(350)2018.PubMed/NCBI View Article : Google Scholar
48	Elango J, Robinson J, Zhang J, Bao B, Ma N, de Val JEMS and Wu W: Collagen peptide Upregulates Osteoblastogenesis from bone marrow mesenchymal stem cells through MAPK-Runx2. Cells. 8(446)2019.PubMed/NCBI View Article : Google Scholar
49	d'Avanzo N, Bruno MC, Giudice A, Mancuso A, Gaetano F, Cristiano MC, Paolino D and Fresta M: Influence of materials properties on bio-physical features and effectiveness of 3D-Scaffolds for periodontal regeneration. Molecules. 26(1643)2021.PubMed/NCBI View Article : Google Scholar
50	Park CH: Biomaterial-based approaches for regeneration of periodontal ligament and cementum using 3D platforms. Int J Mol Sci. 20(4364)2019.PubMed/NCBI View Article : Google Scholar
51	Matichescu A, Ardelean LC, Rusu LC, Craciun D, Bratu EA, Babucea M and Leretter M: advanced biomaterials and techniques for oral tissue engineering and regeneration-a review. Materials (Basel). 13(5303)2020.PubMed/NCBI View Article : Google Scholar
52	Yunoki S, Nagai N, Suzuki T and Munekata M: Novel biomaterial from reinforced salmon collagen gel prepared by fibril formation and cross-linking. J Biosci Bioeng. 98:40–47. 2004.PubMed/NCBI View Article : Google Scholar
53	Liu C and Sun J: Hydrolyzed tilapia fish collagen induces osteogenic differentiation of human periodontal ligament cells. Biomed Mater. 10(065020)2015.PubMed/NCBI View Article : Google Scholar
54	Zhou T, Liu X, Sui B, Liu C, Mo X and Sun J: Development of fish collagen/bioactive glass/chitosan composite nanofibers as a GTR/GBR membrane for inducing periodontal tissue regeneration. Biomed Mater. 12(055004)2017.PubMed/NCBI View Article : Google Scholar
55	Nagai N, Mori K, Satoh Y, Takahashi N, Yunoki S, Tajima K and Munekata M: In vitro growth and differentiated activities of human periodontal ligament fibroblasts cultured on salmon collagen gel. J Biomed Mater Res A. 82:395–402. 2007.PubMed/NCBI View Article : Google Scholar
56	Kawase T, Okuda K, Kogami H, Nakayama H, Nagata M and Yoshie H: Osteogenic activity of human periosteal sheets cultured on salmon collagen-coated ePTFE meshes. J Mater Sci Mater Med. 21:731–739. 2010.PubMed/NCBI View Article : Google Scholar
57	Tidu A, Schanne-Klein MC and Borderie VM: Development, structure, and bioengineering of the human corneal stroma: A review of collagen-based implants. Exp Eye Res. 200(108256)2020.PubMed/NCBI View Article : Google Scholar
58	Mobaraki M, Abbasi R, Omidian Vandchali S, Ghaffari M, Moztarzadeh F and Mozafari M: Corneal repair and regeneration: Current concepts and future directions. Front Bioeng Biotechnol. 7(135)2019.PubMed/NCBI View Article : Google Scholar
59	van Essen TH, van Zijl L, Possemiers T, Mulder AA, Zwart SJ, Chou CH, Lin CC, Lai HJ, Luyten GPM, Tassignon MJ, et al: Biocompatibility of a fish scale-derived artificial cornea: Cytotoxicity, cellular adhesion and phenotype, and in vivo immunogenicity. Biomaterials. 81:36–45. 2016.PubMed/NCBI View Article : Google Scholar
60	Krishnan S, Sekar S, Katheem MF, Krishnakumar S and Sastry TP: Fish scale collagen-a novel material for corneal tissue engineering. Artif Organs. 36:829–835. 2012.PubMed/NCBI View Article : Google Scholar
61	Bordoni M, Scarian E, Rey F, Gagliardi S, Carelli S, Pansarasa O and Cereda C: Biomaterials in neurodegenerative disorders: A promising therapeutic approach. Int J Mol Sci. 21(3243)2020.PubMed/NCBI View Article : Google Scholar
62	Papadimitriou L, Manganas P, Ranella A and Stratakis E: Biofabrication for neural tissue engineering applications. Mater Today Bio. 6(100043)2020.PubMed/NCBI View Article : Google Scholar
63	Iwashita M, Ohta H, Fujisawa T, Cho M, Ikeya M, Kidoaki S and Kosodo Y: Brain-stiffness-mimicking tilapia collagen gel promotes the induction of dorsal cortical neurons from human pluripotent stem cells. Sci Rep. 9(3068)2019.PubMed/NCBI View Article : Google Scholar
64	Suzuki A, Kato H, Kawakami T, Kodama Y, Shiozawa M, Kuwae H, Miwa K, Hoshikawa E, Haga K, Shiomi A, et al: Development of microstructured fish scale collagen scaffolds to manufacture a tissue-engineered oral mucosa equivalent. J Biomater Sci Polym Ed. 31:578–600. 2020.PubMed/NCBI View Article : Google Scholar
65	Percival SL, McCarty S, Hunt JA and Woods EJ: The effects of pH on wound healing, biofilms, and antimicrobial efficacy. Wound Repair Regen. 22:174–186. 2014.PubMed/NCBI View Article : Google Scholar
66	Krzyszczyk P, Schloss R, Palmer A and Berthiaume F: The role of macrophages in acute and chronic wound healing and interventions to promote Pro-wound healing phenotypes. Front Physiol. 9(419)2018.PubMed/NCBI View Article : Google Scholar
67	Hesketh M, Sahin KB, West ZE and Murray RZ: Macrophage phenotypes regulate scar formation and chronic wound healing. Int J Mol Sci. 18(1545)2017.PubMed/NCBI View Article : Google Scholar
68	Feng X, Xu W, Li Z, Song W, Ding J and Chen X: Immunomodulatory Nanosystems. Adv Sci (Weinh). 6(1900101)2019.PubMed/NCBI View Article : Google Scholar
69	Liu C and Sun J: Osteogenically differentiated mesenchymal stem cells induced by hydrolyzed fish collagen maintain their immunomodulatory effects. Life Sci. 238(116970)2019.PubMed/NCBI View Article : Google Scholar
70	Pers YM, Bony C, Duroux-Richard I, Bernard L, Maumus M, Assou S, Barry F, Jorgensen C and Noël D: miR-155 Contributes to the immunoregulatory function of human mesenchymal stem cells. Front Immunol. 12(624024)2021.PubMed/NCBI View Article : Google Scholar
71	Abdi R, Fiorina P, Adra CN, Atkinson M and Sayegh MH: Immunomodulation by mesenchymal stem cells: A potential therapeutic strategy for type 1 diabetes. Diabetes. 57:1759–1767. 2008.PubMed/NCBI View Article : Google Scholar
72	Chávez-Galán L, Olleros ML, Vesin D and Garcia I: Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages. Front Immunol. 6(263)2015.PubMed/NCBI View Article : Google Scholar
73	Glenn JD and Whartenby KA: Mesenchymal stem cells: Emerging mechanisms of immunomodulation and therapy. World J Stem Cells. 6:526–539. 2014.PubMed/NCBI View Article : Google Scholar
74	Liu Y, Yin Z, Zhang R, Yan K, Chen L, Chen F, Huang W, Lv B, Sun C and Jiang X: MSCs inhibit bone marrow-derived DC maturation and function through the release of TSG-6. Biochem Biophys Res Commun. 450:1409–1415. 2014.PubMed/NCBI View Article : Google Scholar
75	Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC and Moretta L: Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: Role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 111:1327–1333. 2008.PubMed/NCBI View Article : Google Scholar
76	Aggarwal S and Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 105:1815–22. 2005.PubMed/NCBI View Article : Google Scholar
77	Glennie S, Soeiro I, Dyson PJ, Lam EW and Dazzi F: Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 105:2821–2827. 2005.PubMed/NCBI View Article : Google Scholar
78	Asari S, Itakura S, Ferreri K, Liu CP, Kuroda Y, Kandeel F and Mullen Y: Mesenchymal stem cells suppress B-cell terminal differentiation. Exp Hematol. 37:604–615. 2009.PubMed/NCBI View Article : Google Scholar
79	La Rocca G, Lo Iacono M, Corsello T, Corrao S, Farina F and Anzalone R: Human Wharton's jelly mesenchymal stem cells maintain the expression of key immunomodulatory molecules when subjected to osteogenic, adipogenic and chondrogenic differentiation in vitro: New perspectives for cellular therapy. Curr Stem Cell Res Ther. 8:100–113. 2013.PubMed/NCBI View Article : Google Scholar
80	Liu C and Sun J: Impact of Marine-based biomaterials on the immunoregulatory properties of bone marrow-derived mesenchymal stem cells: Potential Use of Fish Collagen in Bone Tissue Engineering. ACS Omega. 5:28360–28368. 2020.PubMed/NCBI View Article : Google Scholar
81	Ouyang L, Cao J, Dai Q and Qiu D: New insight of Immuno-engineering in osteoimmunomodulation for bone regeneration. Regen Ther. 18:24–29. 2021.PubMed/NCBI View Article : Google Scholar
82	Liu C and Sun J: Modulation of the secretion of mesenchymal stem cell immunoregulatory factors by hydrolyzed fish collagen. Exp Ther Med. 20:375–384. 2020.PubMed/NCBI View Article : Google Scholar
83	Hernández-Rangel A and Martin-Martinez ES: Collagen based electrospun materials for skin wounds treatment. J Biomed Mater Res A: Feb 27, 2021 (Epub ahead of print).
84	Shen XR, Chen XL, Xie HX, He Y, Chen W, Luo Q, Yuan WH, Tang X, Hou DY, Jiang DW and Wang QR: Beneficial effects of a novel shark-skin collagen dressing for the promotion of seawater immersion wound healing. Mil Med Res. 4(33)2017.PubMed/NCBI View Article : Google Scholar
85	Vigneswari S, Murugaiyah V, Kaur G, Abdul Khalil HP and Amirul AA: Biomacromolecule immobilization: Grafting of fish-scale collagen peptides onto aminolyzed P(3HB-co-4HB) scaffolds as a potential wound dressing. Biomed Mater. 11(055009)2016.PubMed/NCBI View Article : Google Scholar
86	Muthukumar T, Prabu P, Ghosh K and Sastry TP: Fish scale collagen sponge incorporated with Macrotyloma uniflorum plant extract as a possible wound/burn dressing material. Colloids Surf B Biointerfaces. 113:207–212. 2014.PubMed/NCBI View Article : Google Scholar
87	Michalska-Sionkowska M, Warżyńska O, Kaczmarek-Szczepańska B, Łukowicz K, Osyczka AM and Walczak M: Preparation and characterization of fish skin collagen material modified with β-glucan as potential wound dressing. Materials (Basel). 14(1322)2021.PubMed/NCBI View Article : Google Scholar
88	Hartinger JM, Lukáč P, Mlček M, Popková M, Suchý T, Šupová M, Chlup H, Horný L, Závora J, Adámková V, et al: Rifampin-releasing Triple-layer cross-linked fresh water fish collagen sponges as wound dressings. Biomed Res Int. 2020(3841861)2020.PubMed/NCBI View Article : Google Scholar
89	Feng X, Zhang X, Li S, Zheng Y, Shi X, Li F, Guo S and Yang J: Preparation of aminated fish scale collagen and oxidized sodium alginate hybrid hydrogel for enhanced full-thickness wound healing. Int J Biol Macromol. 164:626–637. 2020.PubMed/NCBI View Article : Google Scholar
90	Ge B, Wang H, Li J, Liu H, Yin Y, Zhang N and Qin S: Comprehensive assessment of Nile Tilapia Skin (Oreochromis niloticus) collagen hydrogels for wound dressings. Mar Drugs. 18(178)2020.PubMed/NCBI View Article : Google Scholar
91	Gómez-Guillén MC, Giménez B, López-Caballero ME and Montero MP: Functional and bioactive properties of collagen and gelatin from alternative sources: A review. Food Hydrocoll. 25:1813–1827. 2011.
92	Barczyk M, Carracedo S and Gullberg D: Integrins. Cell Tissue Res. 339:269–280. 2010.PubMed/NCBI View Article : Google Scholar
93	Sewing J, Klinger M and Notbohm H: Jellyfish collagen matrices conserve the chondrogenic phenotype in two- and three-dimensional collagen matrices. J Tissue Eng Regen Med. 11:916–925. 2017.PubMed/NCBI View Article : Google Scholar
94	Chiu LH, Lai WF, Chang SF, Wong CC, Fan CY, Fang CL and Tsai YH: The effect of type II collagen on MSC osteogenic differentiation and bone defect repair. Biomaterials. 35:2680–2691. 2014.PubMed/NCBI View Article : Google Scholar
95	Cho JK, Jin YG, Rha SJ, Kim SJ and Hwang JH: Biochemical characteristics of four marine fish skins in Korea. Food Chem. 159:200–207. 2014.PubMed/NCBI View Article : Google Scholar
96	Liu C and Sun J: The potential use of fish collagen as a new functional materials due to its good immune-compatibility. J Physics Conf Series. 1605(012174)2020.