Fabrication and characterization of the 3D-printed polycaprolactone/fish bone extract scaffolds for bone tissue regeneration
Seong-Yeong Heo
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorSeok-Chun Ko
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorGun-Woo Oh
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorNamwon Kim
Ingram School of Engineering, Texas State University, San Marcos, Texas
Search for more papers by this authorIl-Whan Choi
Department of Microbiology, Inje University College of Medicine, Busan, Republic of Korea
Search for more papers by this authorWon Sun Park
Department of Physiology, Kangwon National University School of Medicine, Chuncheon, Republic of Korea
Search for more papers by this authorCorresponding Author
Won-Kyo Jung
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Correspondence to: W.-K. Jung; e-mail address: e-mail: [email protected]Search for more papers by this authorSeong-Yeong Heo
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorSeok-Chun Ko
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorGun-Woo Oh
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Search for more papers by this authorNamwon Kim
Ingram School of Engineering, Texas State University, San Marcos, Texas
Search for more papers by this authorIl-Whan Choi
Department of Microbiology, Inje University College of Medicine, Busan, Republic of Korea
Search for more papers by this authorWon Sun Park
Department of Physiology, Kangwon National University School of Medicine, Chuncheon, Republic of Korea
Search for more papers by this authorCorresponding Author
Won-Kyo Jung
Department of Biomedical Engineering, and Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Republic of Korea
Marine-Integrated Bionics Research Center, Pukyong National University, Busan, Republic of Korea
Correspondence to: W.-K. Jung; e-mail address: e-mail: [email protected]Search for more papers by this authorAbstract
Fish bone extract (FBE) containing a trioligopeptide (FBP-KSA, Lys-Ser-Ala) isolated from Johnius belengerii could induce osteogenic activities on MC3T3-E1 pre-osteoblasts in our previous study. Regarding the osteogenic effect of FBE, in the present study, we fabricated the three-dimensional (3D) interconnected polycaprolactone (PCL)/FBE scaffolds for bone tissue regeneration. After fabrication of PCL scaffolds using 3D printing, FBE was coated on the surface of PCL scaffolds by self-assembly process. In the physical characteristic and mechanical property tests, the results demonstrated that the fabricated scaffolds have the strut diameter (between 340 and 345 μm), pore size (between 470 and 480 μm), porosity (between 50% and 55%), and tensile properties (Young's modulus: 9.18–9.42 MPa; max tensile strengths 82.3–87.4 MPa) were similar to those of PCL scaffold. In the cell proliferation and osteogenic assay, the results showed that PCL/FBE scaffolds could significantly induce cell proliferation, calcium deposition, and the expression of osteogenic phenotype markers such as alkaline phosphatase, osteopontin, osteocalcin, and bone morphogenetic protein-2 in the osteoblasts. These results suggest that FBE-coated PCL scaffolds are promising materials for use in biomedical application to promote bone tissue regeneration. © 2018 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater 107B: 1937–1944, 2019.
Supporting Information
Filename | Description |
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jbmb34286-sup-0001-FigureS1.tifTIFF image, 400.8 KB | Figure S1 Schematic diagram of purification of fish bone peptide (FBP-KSA) from fish bone extracts. |
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REFERENCES
- 1Feng X, McDonald JM. Disorders of bone remodeling. Annu Rev Pathol-Mech Dis 2011; 6: 121–145.
- 2Place ES, George JH, Williams CK, Stevens MM. Synthetic polymer scaffolds for tissue engineering. Chem Soc Rev 2009; 38(4): 1139–1151.
- 3Liu X, Ma PX. Polymeric scaffolds for bone tissue engineering. Ann Biomed Eng 2004; 32(3): 477–486.
- 4Sato T, Chen G, Ushida T, Ishii T, Ochiai N, Tateishi T, Tanaka J. Evaluation of PLLA-collagen hybrid sponge as a scaffold for cartilage tissue engineering. Mat Sci Eng C 2004; 24(3): 365–372.
- 5Poursamar SA, Hatami J, Lehner AN, da Silva CL, Ferreira FC, Antunes APM. Gelatin porous scaffolds fabricated using a modified gas foaming technique: characterisation and cytotoxicity assessment. Mat Sci Eng C 2015; 48: 63–70.
- 6Leong WS, Wu SC, Ng K, Tan LP. Electrospun 3D multi-scale fibrous scaffold for enhanced human dermal fibroblast infiltration. Int J Bioprinting 2016; 2(1): 81–92.
- 7Mikos AG, Bao Y, Cima LG, Ingber DE, Vacanti JP, Langer R. Preparation of poly (glycolic acid) bonded fiber structures for cell attachment and transplantation. J Biomed Mater Res A 1993; 27(2): 183–189.
- 8Lo H, Kadiyala S, Guggino S, Leong K. Poly (L-lactic acid) foams with cell seeding and controlled-release capacity. J Biomed Mater Res A 1996; 30(4): 475–484.
- 9Rücker M, Laschke MW, Junker D, Carvalho C, Schramm A, Mülhaupt R, Gellrich NC, Menger MD. Angiogenic and inflammatory response to biodegradable scaffolds in dorsal skinfold chambers of mice. Biomaterials 2006; 27(29): 5027–5038.
- 10Jang CH, Cho YB, Choi CH, Jang YS, Jung WK, Lee H, Kim GH. Effect of umbilical cord serum coated 3D PCL/alginate scaffold for mastoid obliteration. Int J Pediatr Otorhinolaryngol 2014; 78(7): 1061–1065.
- 11Je JY, Kim SY, Kim SK. Preparation and antioxidative activity of hoki frame protein hydrolysate using ultrafiltration membranes. Eur Food Res Technol 2005; 221: 157–162.
- 12Ennaas N, Hammami R, Beaulieu L, Fliss I. Purification and characterization of four antibacterial peptide from protamex hydrolysate of Atlantic mackerel (Scomber scombrus) by-products. Biochem Biophys Res Commun 2015; 462(3): 195–200.
- 13Heo SY, Ko SC, Nam SY, Oh J, Kim YM, Kim JI, Kim N, Yi M, Jung WK. Fish bone peptide promotes osteogenic differentiation of MC3T3-E1 pre-osteoblasts through upregulation of MAPKs and Smad pathways activated BMP-2 receptor. Cell Biochem Funct 2018; 36(3): 137–146.
- 14Gautam S, Dinda AK, Mishra NC. Fabrication and characterization of PCL/gelatin composite nanofibrous scaffold for tissue engineering applications by electrospinning method. Mater Sci Eng C 2013; 33(3): 1228–1235.
- 15Zhu H, Shen J, Feng X, Zhang H, Guo Y, Chen J. Fabrication and characterization of bioactive silk fibroin/wollastonite composite scaffolds. Mater Sci Eng C 2010; 30(1): 132–140.
- 16Wang X, Li Y, Wei J, De Groot K. Development of biomimetic nano-hydroxyapatite/poly (hexamethylene adipamide) composites. Biomaterials 2002; 23(24): 4787–4791.
- 17Zeng H, Lacefield WR. XPS, EDX and FTIR analysis of pulsed laser deposited calcium phosphate bioceramic coatings: the effects of various process parameters. Biomaterials 2000; 21(1): 23–30.
- 18Tangsadthakun C, Kanokpanont S, Sanchavanakit N, Banaprasert T, Damrongsakkul S. Properties of collagen/chitosan scaffolds for skin tissue engineering. J Met Mater Miner 2017; 16(1): 37–44.
- 19Maréchal A, Kido Y, Kita K, Moore AL, Rich PR. Three redox states of Trypanosoma brucei alternative oxidase identified by infrared spectroscopy and electrochemistry. J Biol Chem 2009; 284(46): 31827–31833.
- 20Pai Z, Tolstikov A, Berdnikova P, Kustova G, Khlebnikova T, Selivanova N, Shangina A, Kostrovskii V. Catalytic oxidation of olefins and alcohols with hydrogen peroxide in a two-phase system giving mono- and dicarboxylic acids. Russ Chem Bull 2005; 54(8): 1847–1854.
- 21Devi HS, Singh TD, Singh HP. Optically understanding the dependence of catalysis kinetics on work function of nanocatalyst. Bull Mater Sci 2017; 40(1): 163–170.
- 22Kim SK. Marine medicinal foods: implications and applications-animals and microbes. Oxford: Academic Press; 2012.
- 23Jung WK, Kim SK. Calcium-binding peptide derived from pepsinolytic hydrolysates of hoki (Johnius belengerii) frame. Eur Food Res Technol 2007; 224(6): 763–767.
- 24Jung WK, Lee BJ, Kim SK. Fish-bone peptide increases calcium solubility and bioavailability in ovariectomised rats. Br J Nutr 2006; 95(1): 124–128.
- 25Senthil R, Vedakumari SW, Sastry TP. Hydroxyapatite and demineralized bone matrix from marine food waste-a possible bone implant. Am J Mater Synth Process 2018; 3(1): 1.
- 26Chen J, Burger C, Krishnan CV, Chu B, Hsiao BS, Glimcher MJ. In vitro mineralization of collagen in deminveralized fish bone. Macromol Chem Phys 2005; 206(1): 43–51.
- 27Zhu Q, Ablikim Z, Chen T, Cai Q, Xia J, Jiang D, Wang S. The preparation and characterization of HA/β-TCP biphasic ceramics from fish bones. Ceram Int 2017; 43(15): 12213–12220.
- 28Yildirim ED, Besunder R, Pappas D, Allen F, Güçeri S, Sun W. Accelerated differentiation of osteoblast cells on polycaprolactone scaffolds driven by a combined effect of protein coating and plasma modification. Biofabrication 2010; 2(1): 014109.
- 29Kang SW, Bae JH, Park SA, Kim WD, Park MS, Ko YJ, Jang HS, Park JH. Combination therapy with BMP-2 and BMSCs enhances bone gealing efficacy of PCL scaffold fabricated using the 3D plotting system in a large segmental defect model. Biotechnol Lett 2012; 34: 263–267.
- 30Sousa I, Mendes A, Pereira RF, Bártolo PJ. Collagen surface modified poly (ε-caprolactone) scaffolds with improved hydrophilicity and cell adhesion properties. Mater Lett 2014; 134: 263–267.
- 31Lee K, Jin G, Jang CH, Jung WK, Kim G. Preparation and characterization of multi-layered poly (ε-caprolactone)/chitosan scaffolds fabricated with a combination of melt-plotting/in situ plasma treatment and a coating method for hard tissue regeneration. J Mater Chem B 2013; 1(42): 5831–5841.
- 32Yeo M, Jung WK, Kim G. Fabrication, characterization and biological activity of phlorotannin-conjugated PCL/ β-TCP composite scaffolds for bone tissue regeneration. J Mater Chem 2012; 22(8): 3568–3577.
- 33Kim TG, Park TG. Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly (D, L-lactic-co-glycolic acid) nanofiber mesh. Tissue Eng 2006; 12(2): 221–233.
- 34Kim M, Jung WK, Kim G. Bio-composites composed of a solid free-form fabricated poltcaprolactone and alginate-releasing bone morphogenic protein and bone formation peptide for bone tissue regeneration. Bioprocess Biosyst Eng 2013; 36(11): 1725–1734.
- 35Surmenev RA, Surmeneva MA, Lvanova AA. Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis-a review. Acta Biomater 2014; 10(2): 557–579.
- 36Beederman M, Lamplot JD, Nan G, Wang J, Liu X, Yin L, Li R, Shui W, Zhang H, Kim SH. BMP signaling in mesenchymal stem cell differentiation and bone formation. J Biomed Sci Eng 2013; 6(8A): 32–52.
- 37Nguyen MHT, Qian ZJ, Nguyen VT, Choi W, Heo SJ, Oh CH, Kang DH, Kim GH, Jung WK. Tetrameric peptide purified from hydrolysates of biodiesel byproducts of Nannochloropsis oculata induces osteoblastic differentiation through MAPK and Smad pathway on MG-63 and D1 cells. Process Biochem 2013; 48(9): 1387–1394.
- 38Beck GR, Sullivan EC, Moran E, Zerler B. Relationship between alkaline phosphatase levels, osteopontin expression, and mineralization in differentiating MC3T3-E1 osteoblasts. J Cell Biochem 1998; 68(2): 269–280.
10.1002/(SICI)1097-4644(19980201)68:2<269::AID-JCB13>3.0.CO;2-A CAS PubMed Web of Science® Google Scholar
- 39Aubin JE, Turksen K, Heersche JN. Osteoblastic cell lineage: cellular and molecular biology of bone. New York: Elsevier; 1993.
10.1016/B978-0-08-092500-4.50005-X Google Scholar
- 40Xie N, Li M, Wu T, Liu J, Wang B, Tang F. Does elevated osteopontin level play an important role in the development of scoliosis in bipedal mice? Spine J 2015; 15(7): 1660–1664.
- 41You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, Donahue HJ, Jacobs CR. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 2001; 276(16): 13365–13371.
- 42Oldknow KJ, Macrae VE, Farquharson C. Endocrine role of bone: recent and emerging perspectives beyond osteocalcin. J Endocrinol 2015; 225(1): R1–R19.
- 43Zouani OF, Rami L, Lei Y, Durrieu MC. Insights into the osteoblasts precursor differentiation towards mature osteoblasts induced by continuous BMP-2 signaling. Biol Open 2013; 2(9): 872–881.