Restricted accessResearch articleFirst published online 2014-02
Biodegradable Electrospun Scaffolds for Annulus Fibrosus Tissue Engineering: Effect of Scaffold Structure and Composition on Annulus Fibrosus Cells In Vitro
Electrospinning technology is an attractive process for the fabrication of a scaffold with an annulus fibrosus (AF)-like architecture for tissue engineering. Oriented and nonoriented electrospun scaffolds were prepared from poly(ester-urethane) (PU) and poly(ɛ-caprolactone) (PCL) as well as corresponding homogeneous films. Scaffolds' characteristics and mechanical properties were characterized by scanning electron microscopy, static water contact measurements, and dynamic mechanical analysis, respectively. The effect of scaffold architecture and polymer composition on bovine AF cells was investigated. PU and PCL films and scaffolds supported AF cell growth and extracellular matrix production and accumulation. Electrospun scaffolds increased the retention of collagen and glycosaminoglycan compared with films. Fiber orientation of the scaffolds promoted the AF cell phenotype with a trend toward an upregulation of matrix gene expression for oriented relative to nonoriented scaffolds. The higher yield strain of an oriented electrospun PU scaffold, compared with other scaffolds, will be advantageous for AF tissue engineering under a dynamic mechanical environment.
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References
1.
MillerJ.A., SchmatzC., and SchultzA.B.Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine (Phila Pa 1976), 13, 173, 1988.
2.
MooreA.J., ChiltonJ.D., and UttleyD.Long-term results of microlumbar discectomy. Br J Neurosurg, 8, 319, 1994.
3.
KimJ.M., LeeS.H., AhnY., YoonD.H., LeeC.D., and LimS.T.Recurrence after successful percutaneous endoscopic lumbar discectomy. Minim Invasive Neurosurg, 50, 82, 2007.
4.
SukK.S., LeeH.M., MoonS.H., and KimN.H.Recurrent lumbar disc herniation: results of operative management. Spine (Phila Pa 1976), 26, 672, 2001.
5.
VuceticN., AstrandP., GuntnerP., and SvenssonO.Diagnosis and prognosis in lumbar disc herniation. Clin Orthop Relat Res, 361, 116, 1999.
6.
MarchandF., and AhmedA.M.Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine (Phila Pa 1976), 15, 402, 1990.
7.
GuerinH.L., and ElliottD.M.Quantifying the contributions of structure to annulus fibrosus mechanical function using a nonlinear, anisotropic, hyperelastic model. J Orthop Res, 25, 508, 2007.
8.
SkaggsD.L., WeidenbaumM., IatridisJ.C., RatcliffeA., and MowV.C.Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine (Phila Pa 1976), 19, 1310, 1994.
9.
SatoM., et al.Tissue engineering of the intervertebral disc with cultured annulus fibrosus cells using atelocollagen honeycomb-shaped scaffold with a membrane seal (ACHMS scaffold). Med Biol Eng Comput, 41, 365, 2003.
10.
RongY., SugumaranG., SilbertJ.E., and SpectorM.Proteoglycans synthesized by canine intervertebral disc cells grown in a type I collagen-glycosaminoglycan matrix. Tissue Eng, 8, 1037, 2002.
11.
AliniM., LiW., MarkovicP., AebiM., SpiroR.C., and RoughleyP.J.The potential and limitations of a cell-seeded collagen/hyaluronan scaffold to engineer an intervertebral disc-like matrix. Spine (Phila Pa 1976), 28, 446, 2003.
12.
ChangG., KimH.J., KaplanD., Vunjak-NovakovicG., and KandelR.A.Porous silk scaffolds can be used for tissue engineering annulus fibrosus. Eur Spine J, 16, 1848, 2007.
13.
PhamQ.P., SharmaU., and MikosA.G.Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng, 12, 1197, 2006.
DahlinR.L., KasperF.K., and MikosA.G.Polymeric nanofibers in tissue engineering. Tissue Eng Part B, 17, 349, 2012.
16.
GuexA.G., BirrerD.L., FortunatoG., TevaearaiH.T., and GiraudM.N.Anisotropically oriented electrospun matrices with an imprinted periodic micropattern: a new scaffold for engineered muscle constructs. Biomed Mater, 8, 021001, 2013.
17.
GuexA.G., KocherF.M., FortunatoG., KoernerE., HegemannD., CarrelT.P., TevaearaiH.T., and GiraudM.N.Fine-tuning of substrate architecture and surface chemistry promotes muscle tissue development. Acta Biomater, 8, 1481, 2012.
18.
YangL., KandelR.A., ChangG., and SanterreJ.P.Polar surface chemistry of nanofibrous polyurethane scaffold affects annulus fibrosus cell attachment and early matrix accumulation. J Biomed Mater Res A, 91, 1089, 2009.
19.
AttiaM., et al.The response of annulus fibrosus cell to fibronectin-coated nanofibrous polyurethane-anionic dihydroxyoligomer scaffolds. Biomaterials, 32, 450–460, 2010.
20.
NerurkarN.L., ElliottD.M., and MauckR.L.Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res, 25, 1018, 2007.
21.
NerurkarN.L., MauckR.L., and ElliottD.M.ISSLS prize winner: integrating theoretical and experimental methods for functional tissue engineering of the annulus fibrosus. Spine (Phila Pa 1976), 33, 2691, 2008.
22.
KoepsellL., RemundT., BaoJ., NeufeldD., FongH., and DengY.Tissue engineering of annulus fibrosus using electrospun fibrous scaffolds with aligned polycaprolactone fibers. J Biomed Mater Res A, 99, 564, 2011.
23.
KoepsellL., et al.Electrospun nanofibrous polycaprolactone scaffolds for tissue engineering of annulus fibrosus. Macromol Biosci, 11, 391, 2011.
24.
VadalaG., MozeticP., RainerA., CentolaM., LoppiniM., TrombettaM., and DenaroV.Bioactive electrospun scaffold for annulus fibrosus repair and regeneration. Eur Spine J, 21Suppl 1, S20, 2012.
25.
NerurkarN.L., BakerB.M., SenS., WibleE.E., ElliottD.M., and MauckR.L.Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat Mater, 8, 986, 2009.
26.
YeganegiM., KandelR.A., and SanterreJ.P.Characterization of a biodegradable electrospun polyurethane nanofiber scaffold: Mechanical properties and cytotoxicity. Acta Biomater, 6, 3847, 2010.
27.
BoissardC.I., BourbanP.E., TamiA.E., AliniM., and EglinD.Nanohydroxyapatite/poly(ester urethane) scaffold for bone tissue engineering. Acta Biomater, 5, 3316, 2009.
28.
GornaK., and GogolewskiS.Biodegradable porous polyurethane scaffolds for tissue repair and regeneration. J Biomed Mater Res A, 79, 128, 2006.
29.
EglinD., GradS., GogolewskiS., and AliniM.Farsenol-modified biodegradable polyurethanes for cartilage tissue engineering. J Biomed Mater Res A, 92, 393, 2010.
30.
LaschkeM.W., StroheA., MengerM.D., AliniM., and EglinD.In vitro and in vivo evaluation of a novel nanosize hydroxyapatite. Acta Biomater, 6, 2020, 2010.
31.
LabarcaC., and PaigenK.A simple, rapid, and sensitive DNA assay procedure. Anal Biochem, 102, 344, 1980.
32.
FarndaleR.W., ButtleD.J., and BarrettA.J.Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta, 883, 173, 1986.
33.
WoessnerJ.F.The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys, 93, 440, 1961.
34.
NimniM.E.Collagen: structure, function, and metabolism in normal and fibrotic tissues. Semin Arthritis Rheum, 13, 1, 1983.
35.
TangZ.G., BlackR.A., CurranJ.M., HuntJ.A., RhodesN.P., and WilliamsD.F.Surface properties and biocompatibility of solvent-cast poly[ɛ-caprolactone] films. Biomaterials, 25, 4741, 2004.
36.
KimG.H.Electrospun PCL nanofibers with anisotropic mechanical properties as a biomedical scaffold. Biomed Mater, 3, 025010, 2008.
37.
FlemmingR.G., MurphyC.J., AbramsG.A., GoodmanS.L., and NealeyP.F.Effects of synthetic micro- and nano-structured surfaces on cell behaviour. Biomaterials, 20, 573, 1999.
38.
PhamQ.P., SharmaU., and MikosA.G.Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules, 7, 2796, 2006.
39.
BakerB.M., NathanA.S., GeeA.O., and MauckR.L.The influence of an aligned nanofibrous topography on human mesenchymal stem cell fibrochondrogenesis. Biomaterials, 31, 6190, 2010.
40.
MwaleF., RoughleyP., and AntoniouJ.Distinction between the extracellular matrix of the nucleus pulposus and hyaline cartilage: a requisite for tissue engineering of intervertebral disc. Eur Cell Mater, 8, 58, 2004.
41.
MizunoH.A., RoyK., VacantiC.A., KojimaK., UedaM., and BonassarL.J.Tissue-engineered composites of anulus fibrosus and nucleus pulposus for intervertebral disc replacement. Spine, 29, 1290, 2004.
42.
BakerB.M., and MauckR.L.The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials, 28, 1967, 2007.
43.
BronJ.L., HelderM.N., MeiselH.J., Van RoyenB.J., and SmitT.H.Repair, regenerative and supportive therapies of the annulus fibrosus: achievements and challenges. Eur Spine J, 18, 301, 2009.
44.
BakerB.M., et al.The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials, 29, 2348, 2008.
45.
BalguidA., MolA., van MarionM.H., BankR.A., BoutenC.V., and BaaijensF.P.Tailoring fiber diameter in electrospun poly(epsilon-caprolactone) scaffolds for optimal cellular infiltration in cardiovascular tissue engineering. Tissue Eng Part A, 15, 437, 2009.
46.
LeeJ.B., et al.Highly porous electrospun nanofibers enhanced by ultrasonication for improved cellular infiltration. Tissue Eng Part A, 17, 2695, 2011.
