Mineralization potential of cellulose-nanofibrils reinforced gelatine scaffolds for promoted calcium deposition by mesenchymal stem cells

Materials Science and Engineering C

Volumn 73, Issue , 2017, Pages 478-489

  Gorgieva, Selestina ^a   Girandon, Lenart ^b   Kokol, Vanja ^a  

^a UNIVERSITY OF MARIBOR   (Slovenia)

^b Educell Ltd   (Slovenia)

Author keywords

Calcium deposition; Cellulose nanofibrils; Gelatine; Mesenchymal stem cells; Mineralization; Scaffold

Indexed keywords

BIOMIMETIC PROCESSES; BIOMIMETICS; BONE; CALCIUM; CELL CULTURE; CELLULOSE; COMPRESSIVE STRENGTH; CROSSLINKING; DEPOSITION; MINERALOGY; NANOFIBERS; PORE SIZE; SCAFFOLDS; STEM CELLS; THAWING; TISSUE REGENERATION;

CALCIUM DEPOSITION; CELLULOSE NANOFIBRILS; GELATINE; MESENCHYMAL STEM CELL; MINERALIZATION;

SCAFFOLDS (BIOLOGY);

CALCIUM; CELLULOSE; DEPOSITION; SCAFFOLDS;

CALCIUM; CELLULOSE; GELATIN; NANOFIBER; PHOSPHORIC ACID;

ANIMAL; BONE MINERALIZATION; BOVINE; CELL SURVIVAL; CHEMISTRY; COMPRESSIVE STRENGTH; CYTOLOGY; DRUG EFFECTS; ELASTICITY; HUMAN; INFRARED SPECTROSCOPY; MESENCHYMAL STROMA CELL; METABOLISM; POROSITY; SURFACE PROPERTY; TISSUE SCAFFOLD; ULTRASTRUCTURE; VISCOSITY;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; CALCIUM; CATTLE; CELL SURVIVAL; CELLULOSE; COMPRESSIVE STRENGTH; ELASTICITY; GELATIN; HUMANS; MESENCHYMAL STROMAL CELLS; NANOFIBERS; PHOSPHORIC ACIDS; POROSITY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PROPERTIES; TISSUE SCAFFOLDS; VISCOSITY;

EID: 85008675626     PISSN: 09284931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.msec.2016.12.092     Document Type: Article

References (65)

1. [1] McMahon, R.E., Wang, L., Skoracki, R., Mathur, A.B., Development of nanomaterials for bone repair and regeneration. J. Biomed. Mater. Res. B Appl. Biomater. 101 (2013), 387–397.
2. [2] Saiz, E., Zimmermann, E.A., Lee, J.S., Wegst, U.G.K., Tomsia, A.P., Perspectives on the role of nanotechnology in bone tissue engineering. Dent. Mater. 29 (2013), 103–115.
3. [3] Westhrin, M., et al. Osteogenic differentiation of human mesenchymal stem cells in mineralized alginate matrices. PLoS One, 10, 2015, e0120374.
4. [4] Clarke, B., Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 3:Suppl. 3 (2008), S131–S139.
5. [5] Kepa, K., Coleman, R., Grøndahl, L., In vitro mineralization of functional polymers. Biosurf. Biotribol. 1 (2015), 214–227.
6. [6] Baek, J.-Y., et al. Fabrication and characterization of collagen-immobilized porous PHBV/HA nanocomposite scaffolds for bone tissue engineering. J. Nanomater. 2012 (2012), 1–11.
7. [7] Liu, X., Sun, J., Potential proinflammatory effects of hydroxyapatite nanoparticles on endothelial cells in a monocyte-endothelial cell coculture model. Int. J. Nanomedicine 9 (2014), 1261–1273.
8. [8] Huang, Z.-M., et al. Promotion of osteogenic differentiation of stem cells and increase of bone-bonding ability in vivo using urease-treated titanium coated with calcium phosphate and gelatin. Sci. Technol. Adv. Mater., 2016 http://www.tandfonline.com/doi/abs/10.1088/1468-6996/14/5/055001.
9. [9] Shuang, F., et al. Characterization of an injectable chitosan-demineralized bone matrix hybrid for healing critical-size long-bone defects in a rabbit model. Eur. Rev. Med. Pharmacol. Sci. 18 (2014), 740–752.
10. 3 microparticle templates. Mater. Lett. 80 (2012), 91–94.
11. [11] Ungaro, F., et al. Microsphere-integrated collagen scaffolds for tissue engineering: effect of microsphere formulation and scaffold properties on protein release kinetics. J. Control. Release 113 (2006), 128–136.
12. [12] Bao, M., et al. Electrospun biomimetic fibrous scaffold from shape memory polymer of PDLLA-co-TMC for bone tissue engineering. ACS Appl. Mater. Interfaces 6 (2014), 2611–2621.
13. [13] Bojar, W., et al. Bone regeneration potential of the new chitosan-based alloplastic biomaterial. J. Biomater. Appl. 28 (2014), 1060–1068.
14. [14] Lee, Y.M., et al. The bone regenerative effect of platelet-derived growth factor-BB delivered with a chitosan/tricalcium phosphate sponge carrier. J. Periodontol. 71 (2000), 418–424.
15. [15] Ghanaati, S., et al. An injectable bone substitute composed of beta-tricalcium phosphate granules, methylcellulose and hyaluronic acid inhibits connective tissue influx into its implantation bed in vivo. Acta Biomater. 7 (2011), 4018–4028.
16. [16] Keskar, V., Marion, N.W., Mao, J.J., Gemeinhart, R.A., In vitro evaluation of macroporous hydrogels to facilitate stem cell infiltration, growth, and mineralization. Tissue Eng. Part A 15 (2009), 1695–1707.
17. [17] Kolambkar, Y.M., et al. An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials 32 (2011), 65–74.
18. [18] Tampieri, A., et al. A conceptually new type of bio-hybrid scaffold for bone regeneration. Nanotechnology, 22, 2011, 015104.
19. [19] Zimmermann, K.A., LeBlanc, J.M., Sheets, K.T., Fox, R.W., Gatenholm, P., Biomimetic design of a bacterial cellulose/hydroxyapatite nanocomposite for bone healing applications. Mater. Sci. Eng. C 31 (2011), 43–49.
20. [20] Luo, Y., Lode, A., Akkineni, A.R., Gelinsky, M., Concentrated gelatin/alginate composites for fabrication of predesigned scaffolds with a favorable cell response by 3D plotting. RSC Adv. 5 (2015), 43480–43488.
21. [21] Sachot, N., Castaño, O., Mateos-Timoneda, M.A., Engel, E., Planell, J.A., Hierarchically engineered fibrous scaffolds for bone regeneration. J. R. Soc. Interface, 10, 2013, 20130684.
22. [22] Alexandrescu, L., Syverud, K., Gatti, A., Chinga-Carrasco, G., Cytotoxicity tests of cellulose nanofibril-based structures. Cellulose 20 (2013), 1765–1775.
23. [23] Manhas, N., Balasubramanian, K., Prajith, P., Rule, P., Nimje, S., PCL/PVA nanoencapsulated reinforcing fillers of steam exploded/autoclaved cellulose nanofibrils for tissue engineering applications. RSC Adv. 5 (2015), 23999–24008.
24. [24] Zander, N.E., Dong, H., Steele, J., Grant, J.T., Metal cation cross-linked nanocellulose hydrogels as tissue engineering substrates. ACS Appl. Mater. Interfaces 6 (2014), 18502–18510.
25. [25] Bhattacharya, M., et al. Nanofibrillar cellulose hydrogel promotes three-dimensional liver cell culture. J. Control. Release 164 (2012), 291–298.
26. [26] Kolakovic, R., Peltonen, L., Laukkanen, A., Hirvonen, J., Laaksonen, T., Nanofibrillar cellulose films for controlled drug delivery. Eur. J. Pharm. Biopharm. 82 (2012), 308–315 Off. J. Arbeitsgemeinschaft für Pharm. Verfahrenstechnik.
27. [27] Laurén, P., et al. Technetium-99 m-labeled nanofibrillar cellulose hydrogel for in vivo drug release. Eur. J. Pharm. Sci. 65 (2014), 79–88.
28. [28] Zhang, Y., et al. Cellulose nanofibrils. J. Renew. Mater. 1 (2013), 195–211.
29. [29] Lin, N., Dufresne, A., Nanocellulose in biomedicine: current status and future prospect. Eur. Polym. J. 59 (2014), 302–325.
30. [30] Čolić, M., Mihajlović, D., Mathew, A., Naseri, N., Kokol, V., Cytocompatibility and immunomodulatory properties of wood based nanofibrillated cellulose. Cellulose 22 (2014), 763–778.
31. [31] Naseri, N., et al. 3-Dimensional porous nanocomposite scaffolds based on cellulose nanofibers for cartilage tissue engineering: tailoring of porosity and mechanical performance. RSC Adv. 6 (2016), 5999–6007.
32. [32] Lin, N., Dufresne, A., Nanocellulose in biomedicine: current status and future prospect. Eur. Polym. J. 59 (2014), 302–325.
33. [33] El-Fiqi, A., Kim, J.H., Kim, H.W., Osteoinductive fibrous scaffolds of biopolymer/mesoporous bioactive glass nanocarriers with excellent bioactivity and long-term delivery of osteogenic drug. ACS Appl. Mater. Interfaces 7 (2015), 1140–1152.
34. [34] Gorgieva, S., Strancar, J., Kokol, V., Evaluation of surface/interface-related physicochemical and microstructural properties of gelatin 3D scaffolds, and their influence on fibroblast growth and morphology. J. Biomed. Mater. Res. A, 2014, 10.1002/jbm.a.35076.
35. [35] Gorgieva, S., Kokol, V., Processing of gelatin-based cryogels with improved thermomechanical resistance, pore size gradient, and high potential for sustainable protein drug release. J. Biomed. Mater. Res. A 103 (2015), 1119–1130.
36. [36] Marques, M.R.C., Loebenberg, R., Almukainzi, M., Simulated biological fluids with possible application in dissolution testing. Dissolut. Technol. 18 (2011), 15–28.
37. [37] Ye, C., Malak, S.T., Hu, K., Wu, W., Tsukruk, V.V., Cellulose nanocrystal microcapsules as tunable cages for nano- and microparticles. ACS Nano 9 (2015), 10887–10895.
38. [38] Saska, S., et al. Bacterial cellulose-hydroxyapatite nanocomposites for bone regeneration. Int. J. Biomater. 2011 (2011), 1–8.
39. [39] Quin, L.D., A Guide to Organophosphorus Chemistry. 2000, John Wiley & Sons https://books.google.com/books?id=3ATQyjZBjy0C&pgis=1.
40. [40] Gorgieva, S., Vogrinčič, R., Kokol, V., Polydispersity and assembling phenomena of native and reactive dye-labelled nanocellulose. Cellulose 22 (2015), 3541–3558.
41. [41] Verma, D., Katti, K.S., Katti, D.R., Osteoblast adhesion, proliferation and growth on polyelectrolyte complex-hydroxyapatite nanocomposites. Philos. Transact. A Math. Phys. Eng. Sci. 368 (2010), 2083–2097.
42. [42] Discher, D.E., Janmey, P., Wang, Y.-L., Tissue cells feel and respond to the stiffness of their substrate. Science 310 (2005), 1139–1143.
43. [43] Chen, G., et al. Matrix mechanics and fluid shear stress control stem cells fate in three dimensional microenvironment. Curr. Stem Cell Res. Ther. 8 (2013), 313–323.
44. [44] Ivanovska, I.L., Shin, J.-W., Swift, J., Discher, D.E., Stem cell mechanobiology: diverse lessons from bone marrow. Trends Cell Biol. 25 (2015), 523–532.
45. [45] Buxboim, A., Ivanovska, I.L., Discher, D.E., Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells ‘feel’ outside and in?. J. Cell Sci. 123 (2010), 297–308.
46. [46] Polo-Corrales, L., Latorre-Esteves, M., Ramirez-Vick, J.E., Scaffold design for bone regeneration. J. Nanosci. Nanotechnol. 14 (2014), 15–56.
47. [47] Plieva, F.M., Kirsebom, H., Mattiasson, B., Preparation of macroporous cryostructurated gel monoliths, their characterization and main applications. J. Sep. Sci. 34 (2011), 2164–2172.
48. [48] Allo, B.A., Costa, D.O., Dixon, S.J., Mequanint, K., Rizkalla, A.S., Bioactive and biodegradable nanocomposites and hybrid biomaterials for bone regeneration. J. Funct. Biomater. 3 (2012), 432–463.
49. [49] Nadeem, D., et al. Three-dimensional CaP/gelatin lattice scaffolds with integrated osteoinductive surface topographies for bone tissue engineering. Biofabrication, 7, 2015, 015005.
50. [50] Lyu, S., Huang, C., Yang, H., Zhang, X., Electrospun fibers as a scaffolding platform for bone tissue repair. J. Orthop. Res. 31 (2013), 1382–1389.
51. [51] Engler, A.J., Sen, S., Sweeney, H.L., Discher, D.E., Matrix elasticity directs stem cell lineage specification. Cell 126 (2006), 677–689.
52. [52] Ghasemi-Mobarakeh, L., et al. Structural properties of scaffolds: crucial parameters towards stem cells differentiation. J. Stem Cells 7 (2015), 728–744.
53. [53] Ten, E., Bahr, D.F., Li, B., Jiang, L., Wolcott, M.P., Effects of cellulose nanowhiskers on mechanical, dielectric, and rheological properties of poly(3-hydroxybutyrate-co-3-hydroxyvalerate)/cellulose nanowhisker composites. Ind. Eng. Chem. Res. 51 (2012), 2941–2951.
54. [54] Podlipec, R., et al. Molecular mobility of scaffolds’ biopolymers influences cell growth. ACS Appl. Mater. Interfaces 6 (2014), 15980–15990.
55. [55] Dash, R., Foston, M., Ragauskas, A.J., Improving the mechanical and thermal properties of gelatin hydrogels cross-linked by cellulose nanowhiskers. Carbohydr. Polym. 91 (2013), 638–645.
56. [56] Lukasheva, N.V., Tolmachev, D.A., Cellulose nanofibrils and mechanism of their mineralization in biomimetic synthesis of hydroxyapatite/native bacterial cellulose nanocomposites: molecular dynamics simulations. Langmuir 32 (2015), 125–134.
57. [57] Kokol, V., Božič, M., Vogrinčič, R., Mathew, A.P., Characterisation and properties of homo- and heterogenously phosphorylated nanocellulose. Carbohydr. Polym. 125 (2015), 301–313.
58. [58] Li, K., Wang, J., Liu, X., Xiong, X., Liu, H., Biomimetic growth of hydroxyapatite on phosphorylated electrospun cellulose nanofibers. Carbohydr. Polym. 90 (2012), 1573–1581.
59. [59] Liu, X.S., Zhang, X.H., Guo, X.E., Contributions of trabecular rods of various orientations in determining the elastic properties of human vertebral trabecular bone. Bone 45 (2009), 158–163.
60. [60] Pilia, M., Guda, T., Appleford, M., Development of composite scaffolds for load-bearing segmental bone defects. Biomed. Res. Int., 2013(458253), 2013.
61. [61] Birmingham, E., et al. Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur. Cell. Mater. 23 (2012), 13–27.
62. [62] Matsuoka, F., et al. Morphology-based prediction of osteogenic differentiation potential of human mesenchymal stem cells. PLoS One, 8, 2013, e55082.
63. [63] Silvent, J., et al. Collagen osteoid-like model allows kinetic gene expression studies of non-collagenous proteins in relation with mineral development to understand bone biomineralization. PLoS One, 8, 2013, e57344.
64. [64] Lausch, A.J., Quan, B.D., Miklas, J.W., Sone, E.D., Extracellular matrix control of collagen mineralization in vitro. Adv. Funct. Mater. 23 (2013), 4906–4912.
65. [65] Boonrungsiman, S., et al. The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 14170–14175.