Enhancement of adhesion and promotion of osteogenic differentiation of human adipose stem cells by poled electroactive poly(vinylidene fluoride)
Jenita Pärssinen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Search for more papers by this authorHenrik Hammarén
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorRolle Rahikainen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Search for more papers by this authorVitor Sencadas
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Instituto Politécnico do Cávado e do Ave, Campus do IPCA, Barcelos, 4750-810 Portugal
Search for more papers by this authorClarisse Ribeiro
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Search for more papers by this authorSari Vanhatupa
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorSusanna Miettinen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorSenentxu Lanceros-Méndez
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Search for more papers by this authorCorresponding Author
Vesa P. Hytönen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Correspondence to: V. P. Hytönen; e-mail: [email protected]Search for more papers by this authorJenita Pärssinen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Search for more papers by this authorHenrik Hammarén
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorRolle Rahikainen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Search for more papers by this authorVitor Sencadas
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Instituto Politécnico do Cávado e do Ave, Campus do IPCA, Barcelos, 4750-810 Portugal
Search for more papers by this authorClarisse Ribeiro
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Search for more papers by this authorSari Vanhatupa
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorSusanna Miettinen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Search for more papers by this authorSenentxu Lanceros-Méndez
Center/Department of Physics, University of Minho, Braga, 4710-057 Portugal
Search for more papers by this authorCorresponding Author
Vesa P. Hytönen
BioMediTech, University of Tampere, Tampere, 33014 Finland
Fimlab Laboratories Ltd., Tampere, 33520 Finland
Correspondence to: V. P. Hytönen; e-mail: [email protected]Search for more papers by this authorAbstract
Poly(vinylidene fluoride) (PVDF) is a biocompatible material with excellent electroactive properties. Nonelectroactive α-PVDF and electroactive β-PVDF were used to investigate the substrate polarization and polarity influence on the focal adhesion (FA) size and number as well as on human adipose stem cells (hASCs) differentiation. hASCs were cultured on different PVDF surfaces adsorbed with fibronectin and FA size and number, total adhesion area, cell size, cell aspect ratio and FA density were estimated using cells expressing vinculin fused to enhanced green fluorescent protein. Osteogenic differentiation was also determined using a quantitative alkaline phosphatase assay. The surface charge of the poled PVDF films (positive or negative) influenced the hydrophobicity of the samples, leading to variations in the conformation of adsorbed extracellular matrix proteins, which ultimately modulated the stem cell adhesion on the films and induced their osteogenic differentiation. © 2014 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 103A: 919–928, 2015.
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REFERENCES
- 1Bacakova L, Filova E, Parizek M, Ruml T, Svorcik V. Modulation of cell adhesion, proliferation and differentiation on materials designed for body implants. Biotechnol Adv 2011; 29: 739–767.
- 2Martins P, Lopes AC, Lanceros-Mendez S. Electroactive phases of poly(vinylidene fluoride): Determination, processing and applications. Prog Polym Sci 2014; 39: 683–706.
- 3Sencadas V, Ribeiro C, Bdikin IK, Kholkin AL, Lanceros-Mendez S. Local piezoelectric response of single poly(vinylidene fluoride) electrospun fibers. Phys Status Solidi A 2012; 209: 2605–2609.
- 4Ribeiro C, Sencadas V, Ribelles JLG, Lanceros-Méndez S. Influence of processing conditions on polymorphism and nanofiber morphology of electroactive poly(vinylidene fluoride) electrospun membranes. Soft Mater 2010; 8: 274–287.
- 5Baxter FR, Bowen CR, Turner IG, Dent ACE. Electrically active bioceramics: A review of interfacial responses. Ann Biomed Eng 2010; 38: 2079–2092.
- 6Guo HF, Li ZS, Dong SW, Chen WJ, Deng L, Wang YF, Ying DJ. Piezoelectric PU/PVDF electrospun scaffolds for wound healing applications. Colloids Surf B: Biointerfaces 2012; 96: 29–36.
- 7Laroche G, Marois Y, Guidoin R, King MW, Martin L, How T, Douville Y. Polyvinylidene fluoride (PVDF) as a biomaterial: From polymeric raw material to monofilament vascular suture. J Biomed Mater Res 1995; 29: 1525–1536.
- 8Lajnef N, Chakrabartty S, Elvin N, Elvin A. A sub-microwatt piezo-floating-gate sensor for long-term fatigue monitoring in biomechanical implants. In: 28th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS'06, New York, NY; 2006. p 5936–5939.
- 9Dadsetan M, Pumberger M, Casper ME, Shogren K, Giuliani M, Ruesink T, Hefferan TE, Currier BL, Yaszemski MJ. The effects of fixed electrical charge on chondrocyte behavior. Acta Biomater 2011; 7: 2080–2090.
- 10Weber N, Lee YS, Shanmugasundaram S, Jaffe M, Arinzeh TL. Characterization and in vitro cytocompatibility of piezoelectric electrospun scaffolds. Acta Biomater 2010; 6: 3550–3556.
- 11Ribeiro C, Moreira S, Correia V, Sencadas V, Rocha JG, Gama FM, Gómez Ribelles JL, Lanceros-Méndez S. Enhanced proliferation of pre-osteoblastic cells by dynamic piezoelectric stimulation. RSC Adv 2012; 2: 11504–11509.
- 12Schneider GB, English A, Abraham M, Zaharias R, Stanford C, Keller J. The effect of hydrogel charge density on cell attachment. Biomaterials 2004; 25: 3023–3028.
- 13Lee YS, Collins G, Livingston Arinzeh T. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomater 2011; 7: 3877–3886.
- 14Geiger B, Spatz JP, Bershadsky AD. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 2009; 10: 21–33.
- 15Stricker J, Aratyn-Schaus Y, Oakes Patrick W, Gardel Margaret L. Spatiotemporal constraints on the force-dependent growth of focal adhesions. Biophys J 2011; 100: 2883–2893.
- 16Jun I, Park KM, Lee DY, Park KD, Shin H. Control of adhesion, focal adhesion assembly, and differentiation of myoblasts by enzymatically crosslinked cell-interactive hydrogels. Macromol Res 2011; 19: 911–920.
- 17Ribeiro C, Panadero JA, Sencadas V, Lanceros-Méndez S, Tamaño MN, Moratal D, Salmerón-Sánchez M, Ribelles JLG. Fibronectin adsorption and cell response on electroactive poly(vinylidene fluoride) films. Biomed Mater 2012; 7: 035004.
- 18Lindroos B, Suuronen R, Miettinen S. The potential of adipose stem cells in regenerative medicine. Stem Cell Rev Rep 2011; 7: 269–291.
- 19Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13: 4279–4295.
- 20Fu RH, Wang YC, Liu SP, Huang CM, Kang YH, Tsai CH, Shyu WC, Lin SZ. Differentiation of stem cells: Strategies for modifying surface biomaterials. Cell Transplant 2011; 20: 37–47.
- 21Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677–689.
- 22Kilian KA, Bugarija B, Lahn BT, Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 2010; 107: 4872–4877.
- 23Kelly DJ, Jacobs CR. The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defects Res Part C—Embryo Today: Rev 2010; 90: 75–85.
- 24Fukada E, Yasuda I. On the piezoelectric effect of bone. J Phys Soc Japan 1957; 12: 1158–1162.
- 25Gomes J, Nunes JS, Sencadas V, Lanceros-Mendez S. Influence of the β-phase content and degree of crystallinity on the piezo- and ferroelectric properties of poly(vinylidene fluoride). Smart Mater Struct 2010; 19: 065010.
- 26Sencadas V, Gregorio R, Jr., Lanceros-Mendez S. Alpha to beta phase transformation and microestructural changes of PVDF films induced by uniaxial stretch. J Macromol Sci Part B Phys 2009; 48: 514–525.
- 27Lindroos B, Boucher S, Chase L, Kuokkanen H, Huhtala H, Haataja R, Vemuri M, Suuronen R, Miettinen S. Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro. Cytotherapy 2009; 11: 958–972.
- 28Gimble JM, Guilak F. Adipose-derived adult stem cells: Isolation, characterization, and differentiation potential. Cytotherapy 2003; 5: 362–369.
- 29Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS, Deans RJ, Keating A, Prockop DJ, Horwitz EM. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315–317.
- 30Kyllönen L, Haimi S, Mannerström B, Huhtala H, Rajala KM, Skottman H, Sándor GK, Miettinen S. Effects of different serum conditions on osteogenic differentiation of human adipose stem cells in vitro. Stem Cell Res Ther 2013; 4: 17. DOI:10.1186/scrt165.
- 31Cohen DM, Chen H, Johnson RP, Choudhury B, Craig SW. Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J Biol Chem 2005; 280: 17109–17117.
- 32Haimi S, Suuriniemi N, Haaparanta AM, Ellä V, Lindroos B, Huhtala H, Räty S, Kuokkanen H, Sándor GK, Kellomäki M and others. Growth and osteogenic differentiation of adipose stem cells on PLA/bioactive glass and PLA/β-TCP scaffolds. Tissue Eng Part A 2009; 15: 1473–1480.
- 33McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004; 6: 483–495.
- 34Peng R, Yao X, Ding J. Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. Biomaterials 2011; 32: 8048–8057.
- 35Yang TL, Hsiao YC, Lin SJ, Lee HW, Lou PJ, Ko JY, Young TH. Biomaterial mediated epithelial–mesenchymal interaction of salivary tissue under serum free condition. Biomaterials 2010; 31: 288–295.
- 36Marino AA, Rosson J, Gonzalez E, Jones L, Rogers S, Fukada E. Quasi-static charge interactions in bone. J Electrostatics 1988; 21: 347–360.
- 37Tan F, Xu X, Deng T, Yin M, Zhang X, Wang J. Fabrication of positively charged poly(ethylene glycol)-diacrylate hydrogel as a bone tissue engineering scaffold. Biomed Mater 2012; 7: 055009.
- 38Costa CM, Sencadas V, Mano JF, Lanceros-Méndez S. Effect of poling on the mechanical properties of β-poly(vinylidene fluoride). Mater Sci Forum 2006; 514: 951–955.
- 39van Wachem PB, Beugeling T, Feijen J, Bantjes A, Detmers JP, van Aken WG. Interaction of cultured human endothelial cells with polymeric surfaces of different wettabilities. Biomaterials 1985; 6: 403–408.
- 40Bradshaw MJ, Smith ML. Multiscale relationships between fibronectin structure and functional properties. Acta Biomater 2014; 10: 1524–1531. DOI:10.1016/j.actbio.2013.08.027.
- 41Rapuano BE, Lee JJE, MacDonald DE. Titanium alloy surface oxide modulates the conformation of adsorbed fibronectin to enhance its binding to α5β1 integrins in osteoblasts. Eur J Oral Sci 2012; 120: 185–194.
- 42Bergkvist M, Carlsson J, Oscarsson S. Surface-dependent conformations of human plasma fibronectin adsorbed to silica, mica, and hydrophobic surfaces, studied with use of atomic force microscopy. J Biomed Mater Res Part A 2003; 64A: 349–356.
- 43Chada D, Mather T, Nollert M. The synergy site of fibronectin is required for strong interaction with the platelet integrin αIIbβ3. Ann Biomed Eng 2006; 34: 1542–1552.
- 44De R, Zemel A, Safran SA. Chapter 7—Theoretical concepts and models of cellular mechanosensing. In: GV Shivashankar, editor. Methods in Cell Biology. Academic Press, Waltham, Massachusetts, USA; 2010. p 143–175.
- 45Rodríguez JP, González M, Ríos S, Cambiazo V. Cytoskeletal organization of human mesenchymal stem cells changes during their osteogenic differentiation. J Cell Biochem 2004; 93: 721–731.
- 46Elineni KK, Gallant ND. Regulation of cell adhesion strength by peripheral focal adhesion distribution. Biophys J 2011; 101: 2903–2911.
- 47Trichet L, Le Digabel J, Hawkins RJ, Vedula SRK, Gupta M, Ribrault C, Hersen P, Voituriez R, Ladoux B. Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. Proc Natl Acad Sci 2012; 109: 6933–6938.
- 48Beloti MM, De Oliveira PT, Gimenes R, Zaghete MA, Bertolini MJ, Rosa AL. In vitro biocompatibility of a novel membrane of the composite poly(vinylidene-trifluoroethylene)/barium titanate. J Biomed Mater Res Part A 2006; 79: 282–288.
- 49Costa R, Ribeiro C, Lopes AC, Martins P, Sencadas V, Soares R, Lanceros-Mendez S. Osteoblast, fibroblast and in vivo biological response to poly(vinylidene fluoride) based composite materials. J Mater Sci: Mater Med 2013; 24: 395–403.