Freeze-Thawed Hybridized Preparation with Biomimetic Self-Assembly for a Polyvinyl Alcohol/Collagen Hydrogel Created for Meniscus Tissue Engineering

Abstract:

Freeze-thawed hybridized preparation and the biomimetic self-assembly technique were used to fabricate hydrogel as tissue engineered scaffolds for meniscus tissue. Because of the advantages of both techniques, they were hybridized together as an interesting preparation for hydrogel. Three molecular weights (high, medium, and low) of PVA were prepared in a biomimetic solution before formation into hydrogel by freeze-thawing. The most suitable molecular weight PVA for hydrogel formation was chosen to be mixed with collagen. PVA, PVA/collagen, and collagen were prepared in biomimetic solutions and freeze-thawed into hydrogels. The hydrogels were analyzed and characterized by FTIR, DSC, and SEM. FTIR characterization indicated that high molecular weight PVA formed molecular interaction better than the other molecular weights, and PVA molecules formed molecular interaction with collagen molecules via –OH and C=O groups. DSC characterization showed that the hybridized preparation of freeze-thawing and biomimetic self-assembly kept the characteristics of PVA and collagen. SEM analysis demonstrated that the morphological formation of PVA/collagen was hybridized during freeze-thawing and collagen self-assembly. The morphological structure was organized into a porous network structure. The porous structure showed a rough wall that was formed by the hybridized structure of the crystal domain dispersed in amorphous and collagen self-assembly.

• Periodical: Journal of Biomimetics, Biomaterials and Biomedical Engineering (Volume 21)
• Pages: 17-33
• DOI: https://doi.org/10.4028/www.scientific.net/JBBBE.21.17
• Online since: August 2014
• Authors: Puttiporn Puttawibul, Soottawat Benjakul, Jirut Meesane
• Keywords: Biomimetic, Freeze-Thawing, Hydrogels, Polyvinyl Alcohol, Self-Assembly

References

[1] C. Scotti, M.T. Hirschmann, P. Antinolfi, I. Martin, G.M. Peretti, Meniscus repair and regeneration: review on current methods and research potential. Eur Cell Mater. 26(2013)150-70.

DOI: 10.22203/ecm.v026a11

[2] B. Haddad, Konan S. Konan, Adesida A. Adesida, Khan W.S. Khan, A systematic review of tissue engineered meniscus and replacement strategies: preclinical models. Curr Stem Cell Res Ther. 3(2013)232-42.

DOI: 10.2174/1574888x11308030008

[3] H. Pereira, A.M. Frias, J.M. Oliveira, J. Espregueira-Mendes, R.L. Reis, Tissue engineering and regenerative medicine strategies in meniscus lesions. Arthroscopy. 12(2011)1706-19.

DOI: 10.1016/j.arthro.2011.08.283

[4] J.J. Rongen, T.G. van Tienen, B. van Bochove, D.W. Grijpma, P. Buma, Biomaterials in search of a meniscus substitute. Biomaterials. 11(2014)3527-40.

DOI: 10.1016/j.biomaterials.2014.01.017

[5] A. Gloria, R. De Santis, L. Ambrosio, Polymer-based composite scaffolds for tissue engineering. J Appl Biomater Biomech. 2(2010)57-67.

[6] P. Buma, N.N. Ramrattan, T.G. van Tienen, R.P. Veth, Tissue engineering of the meniscus. Biomaterials. 9(2004)1523-32.

DOI: 10.1016/s0142-9612(03)00499-x

[7] J.L. Holloway, A.M. Lowman, G.R. Palmese, Mechanical evaluation of poly(vinyl alcohol)-based fibrous composites as biomaterials for meniscal tissue replacement. Acta Biomater 12(2010)4716-24.

DOI: 10.1016/j.actbio.2010.06.025

[8] M. Kobayashi, A study of polyvinyl alcohol-hydrogel (PVA-H) artificial meniscus in vivo. Biomed Mater Eng 4(2004)505-15.

[9] A.S. Hoffman, Hydrogels for biomedical applications. Advanced Drug Delivery Reviews 54(2002) 3-12.

[10] N.A. Peppas, J.J. Sahlin, Hydrogels as mucoadhesive and bioadhesive materials: a review. Biomaterials 17(1996)1553–1561.

DOI: 10.1016/0142-9612(95)00307-x

[11] R. Rizzi, C. Bearzi, A. Mauretti, S. Bernardini, S. Cannnata, C. Gargioli, Tissue engineering for skeletalmuscle regeneration. Muscles Ligaments Tendons J 2(2012)230-234.

[12] C. Wiltsey, P. Kubinski, T. Christiani, K. Toomer, Sheehan J. Sheehan, A. Branda, J. Kadlowec, C. Iftode, J. Vernege, Characterization of injectable hydrogels based on poly(N-isopropylacrylamide)-g-chondroitin sulfate with adhesive properties for nucleus pulposus tissue engineering. J Mater Sci Mater Med 4(2013).

DOI: 10.1007/s10856-013-4857-x

[13] G. Perale, F. Rossi, E. Sundstrom, S. Bacchiega, M. Masi, G. Forloni, P. Veglianese, Hydrogels in spinal cord injury repair strategies. ACS Chem Neurosci 2(2011)336-345.

DOI: 10.1021/cn200030w

[14] D. Macaya, M. Spector, Injectable hydrogel materials for spinal cord regeneration: a review. Biomed Mater 7(2012)1-22.

DOI: 10.1088/1748-6041/7/1/012001

[15] P. Fatehi, H. Xiao, Effect of cationic PVA characteristics on fiber and paper properties at saturation level of polymer adsorption. Carbohydrate Polymers 79(2010)423–428.

DOI: 10.1016/j.carbpol.2009.08.029

[16] T. Schuman, M. Wikstroem, M. Rigdahl, Coating of surface-modified papers with poly(vinyl alcohol). Surface and Coatings Technology 183(2004)96–105.

DOI: 10.1016/j.surfcoat.2003.09.059

[17] W.S. Lyoo, W.S. Ha Structure and properties of microfibrillar poly(vinyl alcohol) fibres prepared by saponification under shearing force of poly(vinyl pivalate). Polymer 37(1996) 3121–3129.

DOI: 10.1016/0032-3861(96)89414-6

[18] Y. Wang, Y.L. Hsieh, Immobilization of lipase enzyme in polyvinyl alcohol (PVA) nanofibrous membranes. Journal of Membrane Science 309(2008)73–81.

DOI: 10.1016/j.memsci.2007.10.008

[19] N.A. Peppas, J.E. Scott, Controlled release from poly (vinyl alcohol ) gels prepared by freezing-thawing processes. Journal of Controlled Release 18(1992) 95-100.

DOI: 10.1016/0168-3659(92)90178-t

[20] C.M. Hassan, J.E. Stewart, N.A. Peppas, Diffusional characteristics of freeze/thawed poly(vinyl alcohol) hydrogels: Applications to protein controlled release from multilaminate devices. European Journal of Pharmaceutics and Biopharmaceutics 49(2000).

DOI: 10.1016/s0939-6411(99)00056-9

[21] S. Jiang, S. Liu, W. Feng PVA hydrogel properties for biomedical application . Journal of the Mechanical Behavior of Biomedical Materials 4(2011)1228–1233.

DOI: 10.1016/j.jmbbm.2011.04.005

[22] J.L. Holloway, A.M. Lowman, G.R. Palmese, Aging behavior of PVA hydrogels for soft tissue applications after in vitro swelling using osmotic pressure solutions. Acta Biomaterials 9(2013)5013-5021.

DOI: 10.1016/j.actbio.2012.09.018

[23] W. Song, D.C. Markel, X. Jin, T. Shi, W. Ren Poly(vinylalcohol)/collagen/hydroxyapatite hydrogel: properties and in vitro cellular response. J Biomed Mater Res A 100(2012)3071-30719.

DOI: 10.1002/jbm.a.34240

[24] S. Lamponi, G. Leone, M. Consumi, G. Greco, A. Magnani, In vitro biocompatibility of new PVA-based hydrogels as vitreous body substitutes. J Biomater Sci Polym Ed 23(2012)555-575.

DOI: 10.1163/092050611x554499

[25] C. Hassan, N.A. Peppas, Biopolymers PVA Hydrogels, Anionic PolymerisationNanocomposites. Advances in Polymer Science 153(2000)37-65.

[26] K. Urayama,S. Ogasawara, T. Takigawa, Pure shear deformation of physical and chemical gels of poly(vinyl alcohol). Polymer 47(2006)6868-6873.

DOI: 10.1016/j.polymer.2006.07.021

[27] G.B. McKenna, F. Horkay, Effect of crosslinks on the thermodynamics of poly(vinyl alcohol) hydrogels. Polymer 35(1994)5737-5742.

DOI: 10.1016/s0032-3861(05)80049-7

[28] D.A. La Van, J.N. Cha, Approaches for biological and biomimetic energy conversion. PNAS 103(2006) 5251–5255.

[29] A. Menges, Biomimetic design processes in architecture: morphogenetic and evolutionary computational design. Bioinspir. Biomim 7(2012) 1-10.

DOI: 10.1088/1748-3182/7/1/015003

[30] M.E. Launey, E. Munch, D.H. Alsem, E. Saiz A.P. Tomsia, R.O. Ritchie, A novel biomimetic approach to the design of high-performance ceramic–metal composites. J. R. Soc. Interface 7 (2010)741–753.

DOI: 10.1098/rsif.2009.0331

[31] E.H. Lim, J.P. Sardinha, S. Myers, Nanotechnology Biomimetic Cartilage Regenerative Scaffolds. Arch Plast Surg 3(2014)231-240.

DOI: 10.5999/aps.2014.41.3.231

[32] E. Ko, S.W. Cho, Biomimetic Polymer Scaffolds to Promote Stem Cell-Mediated Osteogenesis. Int J Stem Cells. 2(2013)87-91.

DOI: 10.15283/ijsc.2013.6.2.87

[33] J. Ma, J. Wang, X. Ai, S. Zhang, Biomimetic self-assembly of apatite hybrid materials: From a single molecular template to bi-/multi-molecular templates. Biotechnol Adv 32(2014)744-760.

DOI: 10.1016/j.biotechadv.2013.10.014

[34] A. Diaz Lantada, B. Pareja Sanchez, C. Gomez Murillo, J. Urbieta Scotillo, Fractals in tissue engineering: toward biomimetic cell-culture matrices, microsystems and microstructured implants. Expert Rev Med Devices 10(2013)629-48.

DOI: 10.1586/17434440.2013.827506

[35] P.X. Ma Biomimetic Materials for Tissue Engineer. Adv Drug Deliv Rev 60(2008)184-198.

[36] S.C. Owen, M.S. Schoichet, Design of three-dimensional biomimetic scaffolds. Journal of Biomedical Materials Research A 94(2010)1321-1331.

[37] J. Pattersona, M.M. Martina, J.A. Hubbell, Biomimetic materials in tissue engineering. Materials Today 13(2010)14–22.

[38] T.G. Kim, H. Shin, D.W. Lim Biomimetic Scaffolds for Tissue Engineering . Advanced Functional Materials 22(2012)2446-2468.

DOI: 10.1002/adfm.201103083

[39] J. Zhu, L.J. Kaufman Collagen I self-assembly: revealing the developing structures that generate turbidity. Biophys J 106(2014): 1822-31.

DOI: 10.1016/j.bpj.2014.03.011

[40] W. Li, P. Zhao, C. Lin, X. Wen, E. Katsanevakis, D. Gero, O. Felix, Y. Liu Natural polyelectrolyte self-assembled multilayers based on collagen and alginate: stability and cytocompatibility. Biomacromolecules 14(2013): 2647-56.

DOI: 10.1021/bm4005063

[41] K. Zhang, J.A. Li, K. Deng, T. Liu, J.Y. Chen,N. Huang, The endothelialization and hemocompatibility of the functional multilayer on titanium surface constructed with type IV collagen and heparin. Colloids Surf B Biointerfaces 108(2013)295-304.

DOI: 10.1016/j.colsurfb.2012.12.053

[42] W.J. Chung, J.W. Oh, K. Kwak, B.Y. Lee, J. Meyer, E. Wang, A. Hexemer, S.W. Lee, Biomimetic self-templating supramolecular structures. Nature 2011; 478(7369): 364-8.

DOI: 10.1038/nature10513

[43] F. Jiang, H. Hoerber, J. Howard, Müller D.J. Mueller, Assembly of collagen into microribbons: effects of pH and electrolytes. J Struct Biol 2004; 148(3): 268-78.

DOI: 10.1016/j.jsb.2004.07.001

[44] D.A. Cisneros, C. Hung, C.M. Franz, D.J. Mueller, Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy. J Struct Biol 154(2006)232-45.

DOI: 10.1016/j.jsb.2006.02.006

[45] P. Kittiphattanabawon, S. Benjakul, W. Vissessanguan, H. Kishimura, F. Shahidi, Isolation and characterization of collagen from the skin of brownbanded bamboo shark (Chiloscyllium punctatum). Food Chemistry 199(2010)1519-1526.

DOI: 10.1016/j.foodchem.2009.09.037

[46] J.H. Bradt, M. Mertig,A. Teresiak, W. Pompe, Biomimetic Mineralization of Collagen by CombinedFibril Assembly and Calcium Phosphate Formation. Chem Mater 11(1999)2694-270.

DOI: 10.1021/cm991002p

[47] M.J. D Nugent, C.L. Higginbotham, Preparation of a novel freeze thawed poly(vinyl alcohol) composite hydrogel for drug delivery applications. European Journal of Pharmaceutics and Biopharmaceutics. 6: 377-386.

DOI: 10.1016/j.ejpb.2007.02.014

[48] A.K. Pramanick, S. Gupta, T. Mishra, A. Sinha, Topographical heterogeneity in transparent PVA hydrogels studied by AFM. Materials Science and Engineering: C 2012; 32: 222-227.

DOI: 10.1016/j.msec.2011.10.022

[49] U. Fumio, Y. Hiroshi, N. Kumiko, N. Sachihiko, S. Kenji, M. Yasunori, Swelling and mechanical properties of poly(vinyl alcohol) hydrogels. International Journal of Pharmaceutics 58(1990)135-142.

DOI: 10.1016/0378-5173(90)90251-x

[50] S.W. Tsai, R.L. Liu, F.Y. Hsu, C.C. Chen, A study of the influence of polysaccharides on collagen self-assembly: Nanostructure and kinetics. Biopolymers 83(2006)381–388.

DOI: 10.1002/bip.20568

[51] S. Hua, H. Ma, X. Li, H. Yang, A. Wang, pH-sensitive sodium alginate/poly(vinyl alcohol)hydrogel beads prepared by combined Ca2+ crosslinking and freeze-thawing cycles for controlled release of diclofenac sodium. International Journal of Biological Macromolecules 46(2010).

DOI: 10.1016/j.ijbiomac.2010.03.004

[52] S. Sigurgisladottir , H. Ingvarsdottir , Torrissen O.J. Torrissen , M. Cardinal , H. Hafsteinsson, Effect of freezing/thawing on the microstructure and the texture of smoked Atlantic salmon (Salmo salar). Food Research International 33(2000).

DOI: 10.1016/s0963-9969(00)00105-8

[53] P. Sriket, S. Benjakul, W. Visessanguan, K. Kijroongrojana, Comparative studies on the effect the freeze-thawing process on the physicochemical properties and microstructure of black tiger shrimp(Penaeus monodon) and white shrimp (Penaeus vanname) muscle. Food Chemistry 104(2007).

DOI: 10.1016/j.foodchem.2006.11.004

[54] C.M. Hassan, N.A. Peppas, Structure and morphology of Freeze/Thawed PVA hydrogels. Macromolecules 33(2000)2472-2479.

DOI: 10.1021/ma9907587

[55] E.M. Abdelrazek, I.S. Elashmawi, S. Labeeb, Chitosan filler effects on the experimental characterization, spectroscopic investigation and thermal studies of PVA/PVP blend films. Physica B 405(2010)2021–(2027).

DOI: 10.1016/j.physb.2010.01.095

[56] W. Kunz, Specific ion effects in colloidal and biological systems Current Opinion in Colloid & Interface Science 2010; 15(2010)34–39.

DOI: 10.1016/j.cocis.2009.11.008

[57] I.E. Gouve, W.A. S Judice, M.H. S Cerazi, M.A. Juliano, T. Juhz, Z. Szeltner,L. Polgr, L. Juliano, Kosmotropic salt activation and substrate specificity of poliovirus protease 3C. Biochemistry 45(2006)12083–12089.

DOI: 10.1021/bi060793n

[58] C. M Hassan, Peppas N.A. Peppas, Structure and morphology of Freeze/Thawed PVA hydrogels. Macromolecules 33(2000)2472-2479.

DOI: 10.1021/ma9907587

[59] Y. Zhang, Cremer P.S. Cremer, Interactions between macromolecules and ions: the Hofmeister series. Current Opinion in Chemical Biology 10(2006)658–663.

DOI: 10.1016/j.cbpa.2006.09.020

[60] J. Zhu, L.J. Kaufman, Collagen I self-assembly: revealing the developing structures that generate turbidity. Biophysical Journal 106(2004)1822-1831.

DOI: 10.1016/j.bpj.2014.03.011