Skip to main content
SpringerLink
Log in

A Review of Nanofiber Shish Kebabs and Their Potential in Creating Effective Biomimetic Bone Scaffolds

  • Review Paper
  • Published:
Regenerative Engineering and Translational Medicine Aims and scope Submit manuscript

Abstract

Synthetic scaffolds have emerged as a promising strategy in the field of tissue engineering and regenerative medicine due to their biocompatibility and resemblance of the extracellular matrix in tissues. Scaffolds can be tailored to specific architectures and have a controlled degradation based on their composition. However, one of the main drawbacks of synthetic scaffolds is that they are often limited due to their bioactivity. A novel technique that recently emerged for bone and mineralization applications has shown successful cellular bioactivity, which involves the polymer crystallization of nanofibers called nanofiber shish kebabs. These scaffolds allow for the formation of periodic kebab structure that is perpendicular to the nanofiber axis, which mimic mineralized collagen fibrils. They have attracted attention in bone tissue engineering because of their ability to direct biomimetic mineralization. Combined with block copolymer chemistry, the kebabs have the ability to attract Ca+2 and PO4−2 ions forming calcium phosphate minerals due to their negative charges. This review characterizes the nanofiber shish kebabs and similar systems in literature, investigates the biocompatibility and cellular response of these systems in vitro, and determines the ongoing and future research. Our purpose is to emphasize the potential and novelty of nanofiber shish kebabs as bone scaffolds, which closely mimic the hierarchical structure of bone.

Lay Summary

The current gold standard for bone tissue engineering is the use of autografts, the harvesting of the patient’s own healthy bone from a secondary location to replace the defect bone. This treatment is often painful and limited. This review discusses the potential of nanofiber shish kebabs as a bone scaffold for bone replacement. The purpose of this review is to summarize the research that have been done on nanofiber shish kebab scaffolds including material characterization and cellular behavior of different cell types on the scaffolds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000;371:10–27.

    Article  Google Scholar 

  2. Dawson JI, Oreffo RO. Bridging the regeneration gap: stem cells, biomaterials and clinical translation in bone tissue engineering. Arch Biochem Biophys. 2008;473(2):124–31.

    Article  CAS  Google Scholar 

  3. Stevens MM. Biomaterials for bone tissue engineering. Mater Today. 2008;11(5):18–25.

    Article  CAS  Google Scholar 

  4. Lohmann H, Grass G, Rangger C, Mathiak G. Economic impact of cancellous bone grafting in trauma surgery. Arch Orthop Trauma Surg. 2007;127(5):345–8.

    Article  Google Scholar 

  5. Greenwald AS, Boden SD, Goldberg VM, et al. Bone-graft substitutes: facts, fictions, and applications. J Bone Joint Surg Am. 2001;83-A(Suppl 2 Pt 2):98–103.

    Article  Google Scholar 

  6. Wong M, Eulenberger J, Schenk R, Hunziker E. Effect of surface topology on the osseointegration of implant materials in trabecular bone. J Biomed Mater Res. 1995;29(12):1567–75.

    Article  CAS  Google Scholar 

  7. Wang X, Xu S, Zhou S, Xu W, Leary M, Choong P, et al. Topological design and additive manufacturing of porous metals for bone scaffolds and orthopaedic implants: a review. Biomaterials. 2016;83:127–41.

    Article  CAS  Google Scholar 

  8. Kretlow JD, Mikos AG. Review: mineralization of synthetic polymer scaffolds for bone tissue engineering. Tissue Eng. 2007;13(5):927–38.

    Article  CAS  Google Scholar 

  9. Ambard AJ, Mueninghoff L. Calcium phosphate cement: review of mechanical and biological properties. J Prosthodont. 2006;15(5):321–8.

    Article  Google Scholar 

  10. Langer R, Vacanti JP. Tissue engineering. Science. 1993;260(5110):920–6.

    Article  CAS  Google Scholar 

  11. Mistry AS, Mikos AG. Tissue engineering strategies for bone regeneration. Adv Biochem Eng Biotechnol. 2005;94:1–22.

    Google Scholar 

  12. Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: state of the art and future trends. Macromol Biosci. 2004;4(8):743–65.

    Article  CAS  Google Scholar 

  13. Desai TA. Micro- and nanoscale structures for tissue engineering constructs. Med Eng Phys. 2000;22(9):595–606.

    Article  CAS  Google Scholar 

  14. Chen X, Gleeson SE, Yu T, Khan N, Yucha RW, Marcolongo M, et al. Hierarchically ordered polymer nanofiber shish kebabs as a bone scaffold material. J Biomed Mater Res A. 2017;105(6):1786–98.

    Article  CAS  Google Scholar 

  15. Song JH, Kim HE, Kim HW. Electrospun fibrous web of collagen-apatite precipitated nanocomposite for bone regeneration. J Mater Sci Mater Med. 2008;19(8):2925–32.

    Article  CAS  Google Scholar 

  16. Jang JH, Castano O, Kim HW. Electrospun materials as potential platforms for bone tissue engineering. Adv Drug Deliv Rev. 2009;61(12):1065–83.

    Article  CAS  Google Scholar 

  17. Jing X, Mi HY, Wang XC, Peng XF, Turng LS. Shish-kebab-structured poly(epsilon-caprolactone) nanofibers hierarchically decorated with chitosan-poly(epsilon-caprolactone) copolymers for bone tissue engineering. ACS Appl Mater Interfaces. 2015;7(12):6955–65.

    Article  CAS  Google Scholar 

  18. Wang X, Salick MR, Wang X, Cordie T, Han W, Peng Y, et al. Poly(epsilon-caprolactone) nanofibers with a self-induced nanohybrid shish-kebab structure mimicking collagen fibrils. Biomacromolecules. 2013;14(10):3557–69.

    Article  CAS  Google Scholar 

  19. Porter JR, Henson A, Popat KC. Biodegradable poly(epsilon-caprolactone) nanowires for bone tissue engineering applications. Biomaterials. 2009;30(5):780–8.

    Article  CAS  Google Scholar 

  20. San Thian E, Ahmad Z, Huang J, Edirisinghe MJ, Jayasinghe SN, Ireland DC, et al. The role of electrosprayed apatite nanocrystals in guiding osteoblast behaviour. Biomaterials. 2008;29(12):1833–43.

    Article  CAS  Google Scholar 

  21. Leeuwenburgh SC, Wolke JG, Siebers MC, Schoonman J, Jansen JA. In vitro and in vivo reactivity of porous, electrosprayed calcium phosphate coatings. Biomaterials. 2006;27(18):3368–78.

    Article  CAS  Google Scholar 

  22. Kumar R, Cheang P, Khor KA. Radio frequency (RF) suspension plasma sprayed ultra-fine hydroxyapatite (HA)/zirconia composite powders. Biomaterials. 2003;24(15):2611–21.

    Article  CAS  Google Scholar 

  23. Duncan RL, Turner CH. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int. 1995;57(5):344–58.

    Article  CAS  Google Scholar 

  24. Ducy P, Schinke T, Karsenty G. The osteoblast: a sophisticated fibroblast under central surveillance. Science. 2000;289(5484):1501–4.

    Article  CAS  Google Scholar 

  25. Hamed E, Jasiuk I. Multiscale damage and strength of lamellar bone modeled by cohesive finite elements. J Mech Behav Biomed Mater. 2013;28:94–110.

    Article  Google Scholar 

  26. Weiner S, Traub W. Bone structure: from angstroms to microns. FASEB J. 1992;6(3):879–85.

    Article  CAS  Google Scholar 

  27. Weiner S, Wagner HD. The material bone: structure-mechanical function relations. Annu Rev Mater Sci. 1998;28(1):271–98.

    Article  CAS  Google Scholar 

  28. Fratzl P, Weinkamer R. Nature’s hierarchical materials. Prog Mater Sci. 2007;52(8):1263–334.

    Article  CAS  Google Scholar 

  29. Hsu FY, Cheng YY, Tsai SW, Tsai WB. Fabrication and evaluation of a biodegradable cohesive plug based on reconstituted collagen/gamma-polyglutamic acid. J Biomed Mater Res B Appl Biomater. 2010;95((1):29–35.

    Article  CAS  Google Scholar 

  30. Hanagata N, Takemura T, Monkawa A, Ikoma T, Tanaka J. Pre-adsorbed type-I collagen structure-dependent changes in osteoblastic phenotype. Biochem Biophys Res Commun. 2006;344(4):1234–40.

    Article  CAS  Google Scholar 

  31. Wang CL, Miyata T, Weksler B, Rubin AL, Stenzel KH. Collagen-induced platelet aggregation and release. II Critical size and structural requirements of collagen. Biochim Biophys Acta. 1978;544(3):568–77.

    Article  CAS  Google Scholar 

  32. Traub W, Arad T, Weiner S. Origin of mineral crystal growth in collagen fibrils. Matrix. 1992;12(4):251–5.

    Article  CAS  Google Scholar 

  33. Goissis G, Da Silva Maginador SV, Da Conceição Amaro Martins V. Biomimetic mineralization of charged collagen matrices: in vitro and in vivo study. Artif Organs. 2003;27(5):437–43.

    Article  CAS  Google Scholar 

  34. Roach H. Why does bone matrix contain non-collagenous proteins? The possible roles of osteocalcin, osteonectin, osteopontin and bone sialoprotein in bone mineralisation and resorption. Cell Biol Int. 1994;18(6):617–28.

    Article  CAS  Google Scholar 

  35. Addadi L, Weiner S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci U S A. 1985;82(12):4110–4.

    Article  CAS  Google Scholar 

  36. He G, Dahl T, Veis A, George A. Nucleation of apatite crystals in vitro by self-assembled dentin matrix protein 1. Nat Mater. 2003;2(8):552–8.

    Article  CAS  Google Scholar 

  37. Hoang QQ, Sicheri F, Howard AJ, Yang DS. Bone recognition mechanism of porcine osteocalcin from crystal structure. Nature. 2003;425(6961):977–80.

    Article  CAS  Google Scholar 

  38. Harper RA, Posner AS. Measurement of non-crystalline calcium phosphate in bone mineral. Proc Soc Exp Biol Med. 1966;122(1):137–42.

    Article  CAS  Google Scholar 

  39. Termine JD, Wuthier RE, Posner AS. Amorphous-crystalline mineral changes during endochondral and periosteal bone formation. Proc Soc Exp Biol Med. 1967;125(1):4–9.

    Article  CAS  Google Scholar 

  40. Gu L, Kim YK, Liu Y, Ryou H, Wimmer CE, Dai L, et al. Biomimetic analogs for collagen biomineralization. J Dent Res. 2011;90(1):82–7.

    Article  CAS  Google Scholar 

  41. Olszta MJ, Odom DJ, Douglas EP, Gower LB. A new paradigm for biomineral formation: mineralization via an amorphous liquid-phase precursor. Connect Tissue Res. 2003;44(Suppl 1):326–34.

    Article  CAS  Google Scholar 

  42. Gower LB, Odom DJ. Deposition of calcium carbonate films by a polymer-induced liquid-precursor (PILP) process. J Cryst Growth. 2000;210(4):719–34.

    Article  CAS  Google Scholar 

  43. Dai LJ, Douglas EP, Gower LB. Compositional analysis of a polymer-induced liquid-precursor (PILP) amorphous CaCO3 phase. J Non-Cryst Solids. 2008;354(17):1845–54.

    Article  CAS  Google Scholar 

  44. Bewernitz MA, Gebauer D, Long J, Colfen H, Gower LB. A metastable liquid precursor phase of calcium carbonate and its interactions with polyaspartate. Faraday Discuss. 2012;159:291–312.

    Article  CAS  Google Scholar 

  45. Jee SS, Thula TT, Gower LB. Development of bone-like composites via the polymer-induced liquid-precursor (PILP) process. Part 1: influence of polymer molecular weight. Acta Biomater. 2010;6(9):3676–86.

    Article  CAS  Google Scholar 

  46. Thula TT, Rodriguez DE, Lee MH, Pendi L, Podschun J, Gower LB. In vitro mineralization of dense collagen substrates: a biomimetic approach toward the development of bone-graft materials. Acta Biomater. 2011;7(8):3158–69.

    Article  CAS  Google Scholar 

  47. Nurrohman H, Saeki K, Carneiro KMM, Chien YC, Djomehri S, Ho SP, et al. Repair of dentin defects from DSPP knockout mice by PILP mineralization. J Mater Res. 2016;31(3):321–7.

    Article  CAS  Google Scholar 

  48. Olszta MJ, Douglas EP, Gower LB. Scanning electron microscopic analysis of the mineralization of type I collagen via a polymer-induced liquid-precursor (PILP) process. Calcif Tissue Int. 2003;72(5):583–91.

    Article  CAS  Google Scholar 

  49. Tom S, Jin HE, Heo K, Lee SW. Engineered phage films as scaffolds for CaCO3 biomineralization. Nano. 2016;8(34):15696–701.

    CAS  Google Scholar 

  50. Liu Y, Kim YK, Dai L, Li N, Khan SO, Pashley DH, et al. Hierarchical and non-hierarchical mineralisation of collagen. Biomaterials. 2011;32(5):1291–300.

    Article  CAS  Google Scholar 

  51. Liu Y, Li N, Qi YP, Dai L, Bryan TE, Mao J, et al. Intrafibrillar collagen mineralization produced by biomimetic hierarchical nanoapatite assembly. Adv Mater. 2011;23(8):975–80.

    Article  CAS  Google Scholar 

  52. Gu LS, Kim YK, Liu Y, Takahashi K, Arun S, Wimmer CE, et al. Immobilization of a phosphonated analog of matrix phosphoproteins within cross-linked collagen as a templating mechanism for biomimetic mineralization. Acta Biomater. 2011;7(1):268–77.

    Article  CAS  Google Scholar 

  53. Gu LS, Kim J, Kim YK, Liu Y, Dickens SH, Pashley DH, et al. A chemical phosphorylation-inspired design for type I collagen biomimetic remineralization. Dent Mater. 2010;26(11):1077–89.

    Article  CAS  Google Scholar 

  54. Hartgerink JD, Beniash E, Stupp SI. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science. 2001;294(5547):1684–8.

    Article  CAS  Google Scholar 

  55. Spoerke ED, Anthony SG, Stupp SI. Enzyme directed templating of artificial bone mineral. Adv Mater. 2009;21(4):425–30.

    Article  CAS  Google Scholar 

  56. Mata A, Geng Y, Henrikson KJ, Aparicio C, Stock SR, Satcher RL, et al. Bone regeneration mediated by biomimetic mineralization of a nanofiber matrix. Biomaterials. 2010;31(23):6004–12.

    Article  CAS  Google Scholar 

  57. Wang F, Cao B, Mao C. Bacteriophage bundles with pre-aligned Ca initiate the oriented nucleation and growth of hydroxylapatite. Chem Mater. 2010;22(12):3630–6.

    Article  CAS  Google Scholar 

  58. Zhang X, Li Z, Zhu XX. Biomimetic mineralization induced by fibrils of polymers derived from a bile acid. Biomacromolecules. 2008;9(9):2309–14.

    Article  CAS  Google Scholar 

  59. Travaglini L, D’Annibale A, di Gregorio MC, et al. Between peptides and bile acids: self-assembly of phenylalanine substituted cholic acids. J Phys Chem B. 2013;117(31):9248–57.

    Article  CAS  Google Scholar 

  60. Ramakrishna S, Fujihara K, Teo W, Lim T-C, Ma Z. An introduction to electrospinning and nanofibers. Singapura: World Scientific Publishing Company; 2005.

    Book  Google Scholar 

  61. Reneker DH, Chun I. Nanometre diameter fibres of polymer, produced by electrospinning. Nanotechnology. 1996;7(3):216–23.

    Article  CAS  Google Scholar 

  62. Moghe A, Gupta B. Co-axial electrospinning for nanofiber structures: preparation and applications. Polym Rev. 2008;48(2):353–77.

    Article  CAS  Google Scholar 

  63. Schiffman JD, Schauer CL. Cross-linking chitosan nanofibers. Biomacromolecules. 2007;8(2):594–601.

    Article  CAS  Google Scholar 

  64. Shih YR, Chen CN, Tsai SW, Wang YJ, Lee OK. Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells. 2006;24(11):2391–7.

    Article  CAS  Google Scholar 

  65. Matthews JA, Wnek GE, Simpson DG, Bowlin GL. Electrospinning of collagen nanofibers. Biomacromolecules. 2002;3(2):232–8.

    Article  CAS  Google Scholar 

  66. Newton D, Mahajan R, Ayres C, Bowman JR, Bowlin GL, Simpson DG. Regulation of material properties in electrospun scaffolds: role of cross-linking and fiber tertiary structure. Acta Biomater. 2009;5(1):518–29.

    Article  CAS  Google Scholar 

  67. Dhand C, Ong ST, Dwivedi N, Diaz SM, Venugopal JR, Navaneethan B, et al. Bio-inspired in situ crosslinking and mineralization of electrospun collagen scaffolds for bone tissue engineering. Biomaterials. 2016;104:323–38.

    Article  CAS  Google Scholar 

  68. Zhou Y, Yao H, Wang J, Wang D, Liu Q, Li Z. Greener synthesis of electrospun collagen/hydroxyapatite composite fibers with an excellent microstructure for bone tissue engineering. Int J Nanomedicine. 2015;10:3203.

    Article  CAS  Google Scholar 

  69. Xie J, Peng C, Zhao Q, Wang X, Yuan H, Yang L, et al. Osteogenic differentiation and bone regeneration of iPSC-MSCs supported by a biomimetic nanofibrous scaffold. Acta Biomater. 2016;29:365–79.

    Article  CAS  Google Scholar 

  70. Iafisco M, Foltran I, Sabbatini S, Tosi G, Roveri N. Electrospun nanostructured fibers of collagen-biomimetic apatite on titanium alloy. Bioinorg Chem Appl. 2012;2012:123953.

    Article  CAS  Google Scholar 

  71. Liao S, Murugan R, Chan CK, Ramakrishna S. Processing nanoengineered scaffolds through electrospinning and mineralization suitable for biomimetic bone tissue engineering. J Mech Behav Biomed Mater. 2008;1(3):252–60.

    Article  Google Scholar 

  72. Li X, Xie J, Yuan X, Xia Y. Coating electrospun poly(epsilon-caprolactone) fibers with gelatin and calcium phosphate and their use as biomimetic scaffolds for bone tissue engineering. Langmuir. 2008;24(24):14145–50.

    Article  CAS  Google Scholar 

  73. Chen J, Chu B, Hsiao BS. Mineralization of hydroxyapatite in electrospun nanofibrous poly(L-lactic acid) scaffolds. J Biomed Mater Res A. 2006;79((2):307–17.

    Article  CAS  Google Scholar 

  74. Jin L, Feng Z-Q, Wang T, Ren Z, Ma S, Wu J, et al. A novel fluffy hydroxylapatite fiber scaffold with deep interconnected pores designed for three-dimensional cell culture. J Mater Chem B. 2014;2(1):129–36.

    Article  CAS  Google Scholar 

  75. Shalumon K, Binulal N, Selvamurugan N, et al. Electrospinning of carboxymethyl chitin/poly (vinyl alcohol) nanofibrous scaffolds for tissue engineering applications. Carbohydr Polym. 2009;77(4):863–9.

    Article  CAS  Google Scholar 

  76. Nirmala R, Nam KT, Navamathavan R, Park SJ, Kim HY. Hydroxyapatite mineralization on the calcium chloride blended polyurethane nanofiber via biomimetic method. Nanoscale Res Lett. 2010;6(1):2.

    CAS  Google Scholar 

  77. Choi MO, Kim Y-J. Fabrication of gelatin/calcium phosphate composite nanofibrous membranes by biomimetic mineralization. Int J Biol Macromol. 2012;50(5):1188–94.

    Article  CAS  Google Scholar 

  78. Li X, Xie J, Lipner J, Yuan X, Thomopoulos S, Xia Y. Nanofiber scaffolds with gradations in mineral content for mimicking the tendon-to-bone insertion site. Nano Lett. 2009;9(7):2763–8.

    Article  CAS  Google Scholar 

  79. Cui W, Li X, Xie C, Zhuang H, Zhou S, Weng J. Hydroxyapatite nucleation and growth mechanism on electrospun fibers functionalized with different chemical groups and their combinations. Biomaterials. 2010;31(17):4620–9.

    Article  CAS  Google Scholar 

  80. Li C, Jin H-J, Botsaris GD, Kaplan DL. Silk apatite composites from electrospun fibers. J Mater Res. 2005;20(12):3374–84.

    Article  CAS  Google Scholar 

  81. Yang D, Jin Y, Zhou Y, Ma G, Chen X, Lu F, et al. In situ mineralization of hydroxyapatite on electrospun chitosan-based nanofibrous scaffolds. Macromol Biosci. 2008;8(3):239–46.

    Article  CAS  Google Scholar 

  82. Wang B, Li B, Xiong J, Li CY. Hierarchically ordered polymer nanofibers via electrospinning and controlled polymer crystallization. Macromolecules. 2008;41(24):9516–21.

    Article  CAS  Google Scholar 

  83. Chen X, Dong B, Wang B, Shah R, Li CY. Crystalline block copolymer decorated, hierarchically ordered polymer nanofibers. Macromolecules. 2010;43(23):9918–27.

    Article  CAS  Google Scholar 

  84. Chen X, Wang W, Cheng S, Dong B, Li CY. Mimicking bone nanostructure by combining block copolymer self-assembly and 1D crystal nucleation. ACS Nano. 2013;7(9):8251–7.

    Article  CAS  Google Scholar 

  85. Li L, Li CY, Ni C. Polymer crystallization-driven, periodic patterning on carbon nanotubes. J Am Chem Soc. 2006;128(5):1692–9.

    Article  CAS  Google Scholar 

  86. Li B, Li L, Wang B, Li CY. Alternating patterns on single-walled carbon nanotubes. Nat Nanotechnol. 2009;4(6):358–62.

    Article  CAS  Google Scholar 

  87. Rodriguez K, Renneckar S, Gatenholm P. Biomimetic calcium phosphate crystal mineralization on electrospun cellulose-based scaffolds. ACS Appl Mater Interfaces. 2011;3(3):681–9.

    Article  CAS  Google Scholar 

  88. Prieto S, Shkilnyy A, Rumplasch C, Ribeiro A, Arias FJ, Rodríguez-Cabello JC, et al. Biomimetic calcium phosphate mineralization with multifunctional elastin-like recombinamers. Biomacromolecules. 2011;12(5):1480–6.

    Article  CAS  Google Scholar 

  89. Bigi A, Boanini E, Panzavolta S, Roveri N. Biomimetic growth of hydroxyapatite on gelatin films doped with sodium polyacrylate. Biomacromolecules. 2000;1(4):752–6.

    Article  CAS  Google Scholar 

  90. Yang X, Chen X, Wang H. Acceleration of osteogenic differentiation of preosteoblastic cells by chitosan containing nanofibrous scaffolds. Biomacromolecules. 2009;10(10):2772–8.

    Article  CAS  Google Scholar 

  91. Arras MM, Jana R, Mühlstädt M, et al. In situ formation of nanohybrid shish-kebabs during electrospinning for the creation of hierarchical shish-kebab structures. Macromolecules. 2016;49(9):3550–8.

    Article  CAS  Google Scholar 

  92. Jing X, Jin E, Mi H-Y, Li W-J, Peng X-F, Turng L-S. Hierarchically decorated electrospun poly( $$ \varepsilon $$ ε -caprolactone)/nanohydroxyapatite composite nanofibers for bone tissue engineering. J Mater Sci. 2015;50(12):4174–86.

    Article  CAS  Google Scholar 

  93. Jing X, Mi H-Y, Cordie TM, Salick MR, Peng X-F, Turng L-S. Fabrication of shish–kebab structured poly(ε-caprolactone) electrospun nanofibers that mimic collagen fibrils: effect of solvents and matrigel functionalization. Polymer. 2014;55(21):5396–406.

    Article  CAS  Google Scholar 

  94. LeBaron RG, Athanasiou KA. Extracellular matrix cell adhesion peptides: functional applications in orthopedic materials. Tissue Eng. 2000;6(2):85–103.

    Article  CAS  Google Scholar 

  95. Bettinger CJ, Langer R, Borenstein JT. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Ed Engl. 2009;48(30):5406–15.

    Article  CAS  Google Scholar 

  96. Curtis AS, Wilkinson CD. Reactions of cells to topography. J Biomater Sci Polym Ed. 1998;9(12):1313–29.

    Article  CAS  Google Scholar 

  97. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310(5751):1139–43.

    Article  CAS  Google Scholar 

  98. Pauly HM, Kelly DJ, Popat KC, Trujillo NA, Dunne NJ, McCarthy HO, et al. Mechanical properties and cellular response of novel electrospun nanofibers for ligament tissue engineering: effects of orientation and geometry. J Mech Behav Biomed Mater. 2016;61:258–70.

    Article  CAS  Google Scholar 

  99. Pascu EI, Cahill PA, Stokes J, McGuinness GB. Towards functional 3D-stacked electrospun composite scaffolds of PHBV, silk fibroin and nanohydroxyapatite: mechanical properties and surface osteogenic differentiation. J Biomater Appl. 2016;30(9):1334–49.

    Article  CAS  Google Scholar 

  100. Karazisis D, Petronis S, Agheli H, Emanuelsson L, Norlindh B, Johansson A, et al. The influence of controlled surface nanotopography on the early biological events of osseointegration. Acta Biomater. 2017;53:559–71.

    Article  CAS  Google Scholar 

  101. Doyle AD, Yamada KM. Mechanosensing via cell-matrix adhesions in 3D microenvironments. Exp Cell Res. 2016;343(1):60–6.

    Article  CAS  Google Scholar 

  102. Peng F, Yu X, Wei M. In vitro cell performance on hydroxyapatite particles/poly(L-lactic acid) nanofibrous scaffolds with an excellent particle along nanofiber orientation. Acta Biomater. 2011;7(6):2585–92.

    Article  CAS  Google Scholar 

  103. Linez-Bataillon P, Monchau F, Bigerelle M, Hildebrand HF. In vitro MC3T3 osteoblast adhesion with respect to surface roughness of Ti6Al4V substrates. Biomol Eng. 2002;19(2–6):133–41.

    Article  CAS  Google Scholar 

  104. Quarles LD, Yohay DA, Lever LW, Caton R, Wenstrup RJ. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. J Bone Miner Res: Off J Am Soc Bone Miner Res. 1992;7(6):683–92.

    Article  CAS  Google Scholar 

  105. Cao S, Li H, Li K, Lu J, Zhang L. In vitro mineralization of MC3T3-E1 osteoblast-like cells on collagen/nano-hydroxyapatite scaffolds coated carbon/carbon composites. J Biomed Mater Res A. 2016;104(2):533–43.

    Article  CAS  Google Scholar 

  106. Zhao H, Wang G, Hu S, Cui J, Ren N, Liu D, et al. In vitro biomimetic construction of hydroxyapatite-porcine acellular dermal matrix composite scaffold for MC3T3-E1 preosteoblast culture. Tissue Eng Part A. 2011;17(5–6):765–76.

    Article  CAS  Google Scholar 

  107. Wang K, Cai L, Zhang L, Dong J, Wang S. Biodegradable photo-crosslinked polymer substrates with concentric microgrooves for regulating MC3T3-E1 cell behavior. Adv Healthc Mater. 2012;1(3):292–301.

    Article  CAS  Google Scholar 

  108. Smith IO, McCabe LR, Baumann MJ. MC3T3-E1 osteoblast attachment and proliferation on porous hydroxyapatite scaffolds fabricated with nanophase powder. Int J Nanomedicine. 2006;1(2):189–94.

    Article  CAS  Google Scholar 

  109. Fang T, Wu Q, Mu S, Yang L, Liu S, Fu Q. Shikonin stimulates MC3T3-E1 cell proliferation and differentiation via the BMP-2/Smad5 signal transduction pathway. Mol Med Rep. 2016;14(2):1269–74.

    Article  CAS  Google Scholar 

  110. Wutticharoenmongkol P, Pavasant P, Supaphol P. Osteoblastic phenotype expression of MC3T3-E1 cultured on electrospun polycaprolactone fiber mats filled with hydroxyapatite nanoparticles. Biomacromolecules. 2007;8(8):2602–10.

    Article  CAS  Google Scholar 

  111. Zhang Z, Zhang YW, Gao H. On optimal hierarchy of load-bearing biological materials. Proc Biol Sci. 2011;278(1705):519–25.

    Article  Google Scholar 

  112. Ko EK, Jeong SI, Rim NG, Lee YM, Shin H, Lee B-K. In vitro osteogenic differentiation of human mesenchymal stem cells and in vivo bone formation in composite nanofiber meshes. Tissue Eng A. 2008;14(12):2105–19.

    Article  CAS  Google Scholar 

  113. Wu G, Pan M, Wang X, Wen J, Cao S, Li Z, et al. Osteogenesis of peripheral blood mesenchymal stem cells in self assembling peptide nanofiber for healing critical size calvarial bony defect. Sci Rep. 2015;5:16681.

  114. Daňková J, Buzgo M, Vejpravová J, Kubíčková S, Sovková V, Vysloužilová L, et al. Highly efficient mesenchymal stem cell proliferation on poly-ε-caprolactone nanofibers with embedded magnetic nanoparticles. Int J Nanomedicine. 2015;10:7307–17.

    Article  CAS  Google Scholar 

  115. Gugutkov D, Awaja F, Belemezova K, Keremidarska M, Krasteva N, Kyurkchiev S, et al. Osteogenic differentiation of mesenchymal stem cells using hybrid nanofibers with different configurations and dimensionality. J Biomed Mater Res A. 2017;105(7):2065–74.

    Article  CAS  Google Scholar 

  116. Shin H, Temenoff JS, Bowden GC, Zygourakis K, Farach-Carson MC, Yaszemski MJ, et al. Osteogenic differentiation of rat bone marrow stromal cells cultured on Arg-Gly-Asp modified hydrogels without dexamethasone and beta-glycerol phosphate. Biomaterials. 2005;26(17):3645–54.

    Article  CAS  Google Scholar 

  117. Niu B, Miao X-R, Chen J, Ji X, Zhong G-J, Li Z-M. Industrially scalable approach to nanohybrid shish kebabs by in situ nanofibrillation of isotactic poly(propylene). Macromol Chem Phys. 2015;216(23):2241–8.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Material Science and Engineering, Drexel University, Philadelphia, PA, USA

    Aria C. Attia, Tony Yu, Sarah E. Gleeson, Mark Petrovic, Christopher Y. Li & Michele Marcolongo

  2. College of Medicine, Drexel University, Philadelphia, PA, USA

    Aria C. Attia

  3. School of Biomedical Engineering, Science, and Health Systems, Drexel University, Philadelphia, PA, USA

    Tony Yu

Authors
  1. Aria C. Attia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tony Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah E. Gleeson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark Petrovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christopher Y. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michele Marcolongo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michele Marcolongo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Attia, A.C., Yu, T., Gleeson, S.E. et al. A Review of Nanofiber Shish Kebabs and Their Potential in Creating Effective Biomimetic Bone Scaffolds. Regen. Eng. Transl. Med. 4, 107–119 (2018). https://doi.org/10.1007/s40883-018-0053-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40883-018-0053-3

Keywords

Search

Navigation