Nanostructured Materials in Tissue Engineering

Chapter

Abstract

Over the past thirty years, interest in how mammalian cells interact with materials has exploded, with applications ranging from diagnostic in vitro testing, to bioprocess engineering with microcarriers, and to tissue engineering. This interest has paralleled a revolution in material processing methods which allow scientists and engineers to create an enormous variety of micro- and nanotopological features. By studying aspects of cell behavior such as gene expression, viability, motility, and fate when cells are presented with simple architectural elements, biomedical engineers hope to build a toolbox of topological features that can be deployed to solve specific tissue engineering problems. In this chapter, we first discuss fundamental molecular biology-based mechanisms behind cell–material interactions and then focus specifically on mammalian cell interactions with nanofibers, nanofibrous microspheres, nanogrooves, nanopits, nanotubes, and nanopillars, along with their applications in tissue engineering.

Keywords

Mechanotransduction Nanostructured materials Nanofibrous materials Thermally induced phase separation Injectable tissue engineering 

Notes

Acknowledgements

This work was supported by the Tissue Engineering and Regeneration Training Grant through the National Institutes of Health (5T32DE007057-39).

References

  1. 1.
    Wall SP, Plunkett C, Caplan A (2015) A potential solution to the shortage of solid organs for transplantation. JAMA 313(23):2321–2322.  https://doi.org/10.1001/jama.2015.5328 CrossRefGoogle Scholar
  2. 2.
    Scotta C, Fanelli G, Hoong SJ, Romano M, Lamperti EN, Sukthankar M, Guggino G, Fazekasova H, Ratnasothy K, Becker PD, Afzali B, Lechler RI, Lombardi G (2016) Impact of immunosuppressive drugs on the therapeutic efficacy of ex vivo expanded human regulatory T cells. Haematologica 101(1):91–100.  https://doi.org/10.3324/haematol.2015.128934 CrossRefGoogle Scholar
  3. 3.
    Claas FH (2003) Towards clinical transplantation tolerance. Lancet 361(9368):1489–1490.  https://doi.org/10.1016/S0140-6736(03)13220-5 CrossRefGoogle Scholar
  4. 4.
    Sachlos E, Czernuszka JT (2003) Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur Cells Mater 5:29–39; discussion 39–40Google Scholar
  5. 5.
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872.  https://doi.org/10.1016/j.cell.2007.11.019
  6. 6.
    Marion NW, Mao JJ (2006) Mesenchymal stem cells and tissue engineering. In: Methods in Enzymology, vol 420. Academic Press, Cambridge, pp 339–361.  https://doi.org/10.1016/S0076-6879(06)20016-8
  7. 7.
    O’Brien FJ (2011) Biomaterials & scaffolds for tissue engineering. Mater Today 14(3):88–95.  https://doi.org/10.1016/S1369-7021(11)70058-X
  8. 8.
    Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quarto N, Contag CH, Wu B, Longaker MT (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22(5):560–567.  https://doi.org/10.1038/nbt958 CrossRefGoogle Scholar
  9. 9.
    Mansbridge J, Liu K, Patch R, Symons K, Pinney E (1998) Three-dimensional fibroblast culture implant for the treatment of diabetic foot ulcers: metabolic activity and therapeutic range. Tissue Eng 4(4):403–414.  https://doi.org/10.1089/ten.1998.4.403 CrossRefGoogle Scholar
  10. 10.
    Marijnissen WJCM, van Osch GJVM, Aigner J, van der Veen SW, Hollander AP, Verwoerd-Verhoef HL, Verhaar JAN (2002) Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering. Biomaterials 23(6):1511–1517.  https://doi.org/10.1016/S0142-9612(01)00281-2 CrossRefGoogle Scholar
  11. 11.
    Gattazzo F, Urciuolo A (1840) Bonaldo P (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochem Biophys Acta 8:2506–2519.  https://doi.org/10.1016/j.bbagen.2014.01.010 Google Scholar
  12. 12.
    Ross AM, Jiang Z, Bastmeyer M, Lahann J (2012) Physical aspects of cell culture substrates: topography, roughness, and elasticity. Small 8(3):336–355.  https://doi.org/10.1002/smll.201100934 CrossRefGoogle Scholar
  13. 13.
    Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475(7356):316–323.  https://doi.org/10.1038/nature10316 CrossRefGoogle Scholar
  14. 14.
    Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689.  https://doi.org/10.1016/j.cell.2006.06.044 CrossRefGoogle Scholar
  15. 15.
    Edmondson R, Broglie JJ, Adcock AF, Yang L (2014) Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol 12(4):207–218.  https://doi.org/10.1089/adt.2014.573 CrossRefGoogle Scholar
  16. 16.
    Daxer A, Misof K, Grabner B, Ettl A, Fratzl P (1998) Collagen fibrils in the human corneal stroma: structure and aging. Invest Ophthalmol Vis Sci 39(3):644–648Google Scholar
  17. 17.
    Ushiki T (2002) Collagen fibers, reticular fibers and elastic fibers. A comprehensive understanding from a morphological viewpoint. Arch Histol Cytol 65(2):109–126.  https://doi.org/10.1679/aohc.65.109 CrossRefGoogle Scholar
  18. 18.
    Yim EKF, Leong KW (2005) Significance of synthetic nanostructures in dictating cellular response. Nanomed Nanotechnol Biol Med 1(1):10–21.  https://doi.org/10.1016/j.nano.2004.11.008 CrossRefGoogle Scholar
  19. 19.
    Chan BP, Leong KW (2008) Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J 17(Suppl 4):467–479.  https://doi.org/10.1007/s00586-008-0745-3 CrossRefGoogle Scholar
  20. 20.
    Deng X, Eyster TW, Elkasabi Y, Lahann J (2012) Bio-orthogonal polymer coatings for co-presentation of biomolecules. Macromol Rapid Commun 33(8):640–645.  https://doi.org/10.1002/marc.201100819 CrossRefGoogle Scholar
  21. 21.
    Davis ME, Hsieh PCH, Takahashi T, Song Q, Zhang S, Kamm RD, Grodzinsky AJ, Anversa P, Lee RT (2006) Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci 103(21):8155–8160.  https://doi.org/10.1073/pnas.0602877103 CrossRefGoogle Scholar
  22. 22.
    Wang W, Dang M, Zhang Z, Hu J, Eyster TW, Ni L, Ma PX (2016) Dentin regeneration by stem cells of apical papilla on injectable nanofibrous microspheres and stimulated by controlled BMP-2 release. Acta Biomater 36:63–72.  https://doi.org/10.1016/j.actbio.2016.03.015 CrossRefGoogle Scholar
  23. 23.
    Wei G, Jin Q, Giannobile WV, Ma PX (2006) Nano-fibrous scaffold for controlled delivery of recombinant human PDGF-BB. J Control Release: Official J Control Release Soc 112(1):103–110.  https://doi.org/10.1016/j.jconrel.2006.01.011 CrossRefGoogle Scholar
  24. 24.
    Wei G, Jin Q, Giannobile WV, Ma PX (2007) The enhancement of osteogenesis by nano-fibrous scaffolds incorporating rhBMP-7 nanospheres. Biomaterials 28(12):2087–2096.  https://doi.org/10.1016/j.biomaterials.2006.12.028 CrossRefGoogle Scholar
  25. 25.
    Wei G, Ma PX (2008) Nanostructured biomaterials for regeneration. Adv Funct Mater 18(22):3566–3582.  https://doi.org/10.1002/adfm.200800662 CrossRefGoogle Scholar
  26. 26.
    Ma PX (2008) Biomimetic materials for tissue engineering. Adv Drug Deliv Rev 60(2):184–198.  https://doi.org/10.1016/j.addr.2007.08.041 CrossRefGoogle Scholar
  27. 27.
    Kim D-H, Provenzano PP, Smith CL, Levchenko A (2012) Matrix nanotopography as a regulator of cell function. J Cell Biol 197(3):351–360.  https://doi.org/10.1083/jcb.201108062 CrossRefGoogle Scholar
  28. 28.
    Nagata I, Kawana A, Nakatsuji N (1993) Perpendicular contact guidance of CNS neuroblasts on artificial microstructures. Development 117(1):401–408Google Scholar
  29. 29.
    Gauvin R, Chen Y-C, Lee JW, Soman P, Zorlutuna P, Nichol JW, Bae H, Chen S, Khademhosseini A (2012) Microfabrication of complex porous tissue engineering scaffolds using 3D projection stereolithography. Biomaterials 33(15):3824–3834.  https://doi.org/10.1016/j.biomaterials.2012.01.048 CrossRefGoogle Scholar
  30. 30.
    Givant-Horwitz V, Davidson B, Reich R (2005) Laminin-induced signaling in tumor cells. Cancer Lett 223(1):1–10.  https://doi.org/10.1016/j.canlet.2004.08.030 CrossRefGoogle Scholar
  31. 31.
    Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326(5957):1216–1219.  https://doi.org/10.1126/science.1176009 CrossRefGoogle Scholar
  32. 32.
    Ma PX, Zhang R (1999) Synthetic nano-scale fibrous extracellular matrix. J Biomed Mater Res 46(1):60–72. https://doi.org/10.1002/(sici)1097-4636(199907)46:1<60:aid-jbm7>3.0.co;2-h CrossRefGoogle Scholar
  33. 33.
    Woo KM, Chen VJ, Ma PX (2003) Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment. J Biomed Mater Res, Part A 67A(2):531–537.  https://doi.org/10.1002/jbm.a.10098 CrossRefGoogle Scholar
  34. 34.
    Wei G, Ma PX (2004) Structure and properties of nano-hydroxyapatite/polymer composite scaffolds for bone tissue engineering. Biomaterials 25(19):4749–4757.  https://doi.org/10.1016/j.biomaterials.2003.12.005 CrossRefGoogle Scholar
  35. 35.
    Li X, Xie J, Lipner J, Yuan X, Thomopoulos S, Xia Y (2009) Nanofiber scaffolds with gradations in mineral content for mimicking the tendon-to-bone insertion site. Nano Lett 9(7):2763–2768.  https://doi.org/10.1021/nl901582f CrossRefGoogle Scholar
  36. 36.
    Liu X, Won Y, Ma PX (2006) Porogen-induced surface modification of nano-fibrous poly(l-lactic acid) scaffolds for tissue engineering. Biomaterials 27(21):3980–3987.  https://doi.org/10.1016/j.biomaterials.2006.03.008 CrossRefGoogle Scholar
  37. 37.
    Armentano I, Dottori M, Fortunati E, Mattioli S, Kenny JM (2010) Biodegradable polymer matrix nanocomposites for tissue engineering: a review. Polym Degrad Stab 95(11):2126–2146.  https://doi.org/10.1016/j.polymdegradstab.2010.06.007 CrossRefGoogle Scholar
  38. 38.
    Yang S-M, Jang SG, Choi D-G, Kim S, Yu HK (2006) Nanomachining by colloidal lithography. Small 2(4):458–475.  https://doi.org/10.1002/smll.200500390 CrossRefGoogle Scholar
  39. 39.
    Rubin PJ, Yaremchuk MJ (1997) Complications and toxicities of implantable biomaterials used in facial reconstructive and aesthetic surgery: a comprehensive review of the literature. Plast Reconstr Surg 100(5):1336–1353CrossRefGoogle Scholar
  40. 40.
    Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(5761):622–627.  https://doi.org/10.1126/science.1114397 CrossRefGoogle Scholar
  41. 41.
    Shvedova AA, Kisin ER, Mercer R, Murray AR, Johnson VJ, Potapovich AI, Tyurina YY, Gorelik O, Arepalli S, Schwegler-Berry D, Hubbs AF, Antonini J, Evans DE, Ku B-K, Ramsey D, Maynard A, Kagan VE, Castranova V, Baron P (2005) Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am J Physiol - Lung Cell Mol Physiol 289(5):L698–L708.  https://doi.org/10.1152/ajplung.00084.2005 CrossRefGoogle Scholar
  42. 42.
    Kalita SJ, Bhardwaj A, Bhatt HA (2007) Nanocrystalline calcium phosphate ceramics in biomedical engineering. Mater Sci Eng, C 27(3):441–449.  https://doi.org/10.1016/j.msec.2006.05.018 CrossRefGoogle Scholar
  43. 43.
    Popat KC, Leoni L, Grimes CA, Desai TA (2007) Influence of engineered titania nanotubular surfaces on bone cells. Biomaterials 28(21):3188–3197.  https://doi.org/10.1016/j.biomaterials.2007.03.020 CrossRefGoogle Scholar
  44. 44.
    Harrison BS, Atala A (2007) Carbon nanotube applications for tissue engineering. Biomaterials 28(2):344–353.  https://doi.org/10.1016/j.biomaterials.2006.07.044 CrossRefGoogle Scholar
  45. 45.
    Gunatillake PA, Adhikari R (2003) Biodegradable synthetic polymers for tissue engineering. Eur Cells Mater 5(1):1–16Google Scholar
  46. 46.
    Liu H, Slamovich EB, Webster TJ (2006) Less harmful acidic degradation of poly(lactic-co-glycolic acid) bone tissue engineering scaffolds through titania nanoparticle addition. Int J Nanomed 1(4):541–545CrossRefGoogle Scholar
  47. 47.
    Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials 21(24):2529–2543.  https://doi.org/10.1016/S0142-9612(00)00121-6 CrossRefGoogle Scholar
  48. 48.
    Kim JH, Choung P-H, Kim IY, Lim KT, Son HM, Choung Y-H, Cho C-S, Chung JH (2009) Electrospun nanofibers composed of poly(ε-caprolactone) and polyethylenimine for tissue engineering applications. Mater Sci Eng, C 29(5):1725–1731.  https://doi.org/10.1016/j.msec.2009.01.023 CrossRefGoogle Scholar
  49. 49.
    Klein Gunnewiek M, Benetti EM, Di Luca A, van Blitterswijk CA, Moroni L, Vancso GJ (2013) Thin polymer brush decouples biomaterial’s micro-/nanotopology and stem cell adhesion. Langmuir 29(45):13843–13852.  https://doi.org/10.1021/la403360r CrossRefGoogle Scholar
  50. 50.
    Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis ASG (2004) Changes in fibroblast morphology in response to nano-columns produced by colloidal lithography. Biomaterials 25(23):5415–5422.  https://doi.org/10.1016/j.biomaterials.2003.12.049 CrossRefGoogle Scholar
  51. 51.
    Caracciolo PC, Thomas V, Vohra YK, Buffa F, Abraham GA (2009) Electrospinning of novel biodegradable poly(ester urethane)s and poly(ester urethane urea)s for soft tissue-engineering applications. J Mater Sci - Mater Med 20(10):2129–2137.  https://doi.org/10.1007/s10856-009-3768-3 CrossRefGoogle Scholar
  52. 52.
    Park J-C, Ito T, Kim K-O, Kim K-W, Kim B-S, Khil M-S, Kim H-Y, Kim I-S (2010) Electrospun poly(vinyl alcohol) nanofibers: effects of degree of hydrolysis and enhanced water stability. Polym J 42(3):273–276CrossRefGoogle Scholar
  53. 53.
    Matthews JA, Wnek GE, Simpson DG, Bowlin GL (2002) Electrospinning of collagen nanofibers. Biomacromol 3(2):232–238.  https://doi.org/10.1021/bm015533u CrossRefGoogle Scholar
  54. 54.
    Elsabee MZ, Naguib HF, Morsi RE (2012) Chitosan based nanofibers, review. Mater Sci Eng, C 32(7):1711–1726.  https://doi.org/10.1016/j.msec.2012.05.009 CrossRefGoogle Scholar
  55. 55.
    Bonino CA, Krebs MD, Saquing CD, Jeong SI, Shearer KL, Alsberg E, Khan SA (2011) Electrospinning alginate-based nanofibers: from blends to crosslinked low molecular weight alginate-only systems. Carbohyd Polym 85(1):111–119.  https://doi.org/10.1016/j.carbpol.2011.02.002 CrossRefGoogle Scholar
  56. 56.
    Holzwarth JM, Ma PX (2011) Biomimetic nanofibrous scaffolds for bone tissue engineering. Biomaterials 32(36):9622–9629.  https://doi.org/10.1016/j.biomaterials.2011.09.009 CrossRefGoogle Scholar
  57. 57.
    Zhang Z, Eyster TW, Ma PX (2016) Nanostructured injectable cell microcarriers for tissue regeneration. Nanomedicine 11(12):1611–1628.  https://doi.org/10.2217/nnm-2016-0083 CrossRefGoogle Scholar
  58. 58.
    Nair LS, Laurencin CT (2006) Polymers as biomaterials for tissue engineering and controlled drug delivery. In: Lee K, Kaplan D (eds) Tissue engineering I. Springer, Berlin, pp 47–90.  https://doi.org/10.1007/b137240
  59. 59.
    Plachetka U, Bender M, Fuchs A, Vratzov B, Glinsner T, Lindner F, Kurz H (2004) Wafer scale patterning by soft UV-nanoimprint lithography. Microelectron Eng 73–74:167–171.  https://doi.org/10.1016/j.mee.2004.02.035 CrossRefGoogle Scholar
  60. 60.
    Chou SY, Krauss PR, Renstrom PJ (1996) Nanoimprint lithography. J Vac Sci Technol B: Microelectron Nanometer Struct 14(6):4129–4133CrossRefGoogle Scholar
  61. 61.
    Denis FA, Hanarp P, Sutherland DS, Dufrêne YF (2002) Fabrication of nanostructured polymer surfaces using colloidal lithography and spin-coating. Nano Lett 2(12):1419–1425.  https://doi.org/10.1021/nl025750g CrossRefGoogle Scholar
  62. 62.
    Wood MA (2007) Colloidal lithography and current fabrication techniques producing in-plane nanotopography for biological applications. J R Soc Interface 4(12):1–17.  https://doi.org/10.1098/rsif.2006.0149 CrossRefGoogle Scholar
  63. 63.
    Sutherland DS, Broberg M, Nygren H, Kasemo B (2001) Influence of nanoscale surface topography and chemistry on the functional behaviour of an adsorbed model macromolecule. Macromol Biosci 1(6):270–273. https://doi.org/10.1002/1616-5195(20010801)1:6<270:aid-mabi270>3.0.co;2-3 CrossRefGoogle Scholar
  64. 64.
    Truskett VN, Watts MPC (2006) Trends in imprint lithography for biological applications. Trends Biotechnol 24(7):312–317.  https://doi.org/10.1016/j.tibtech.2006.05.005 CrossRefGoogle Scholar
  65. 65.
    Gilles S, Meier M, Prömpers M, Avd Hart, Kügeler C, Offenhäusser A, Mayer D (2009) UV nanoimprint lithography with rigid polymer molds. Microelectron Eng 86(4–6):661–664.  https://doi.org/10.1016/j.mee.2008.12.051 CrossRefGoogle Scholar
  66. 66.
    Bucaro MA, Vasquez Y, Hatton BD, Aizenberg J (2012) Fine-tuning the degree of stem cell polarization and alignment on ordered arrays of high-aspect-ratio nanopillars. ACS Nano 6(7):6222–6230.  https://doi.org/10.1021/nn301654e CrossRefGoogle Scholar
  67. 67.
    Eliason MT, Charest JL, Simmons BA, Garcia AJ, King WP (2007) Nanoimprint fabrication of polymer cell substrates with combined microscale and nanoscale topography. J Vac Sci Technol, B 25(4):L31–L34.  https://doi.org/10.1116/1.2748792 CrossRefGoogle Scholar
  68. 68.
    Wang Y, Angelatos AS, Caruso F (2008) Template synthesis of nanostructured materials via layer-by-layer assembly. Chem Mater 20(3):848–858.  https://doi.org/10.1021/cm7024813 CrossRefGoogle Scholar
  69. 69.
    Richardson JJ, Björnmalm M, Caruso F (2015) Technology-driven layer-by-layer assembly of nanofilms. Science 348(6233).  https://doi.org/10.1126/science.aaa2491
  70. 70.
    Seo J, Schattling P, Lang T, Jochum F, Nilles K, Theato P, Char K (2010) Covalently bonded layer-by-layer assembly of multifunctional thin films based on activated esters. Langmuir 26(3):1830–1836.  https://doi.org/10.1021/la902574z CrossRefGoogle Scholar
  71. 71.
    Jiang C, Tsukruk VV (2006) Freestanding nanostructures via layer-by-layer assembly. Adv Mater 18(7):829–840.  https://doi.org/10.1002/adma.200502444 CrossRefGoogle Scholar
  72. 72.
    Liang Z, Susha AS, Yu A, Caruso F (2003) Nanotubes prepared by layer-by-layer coating of porous membrane templates. Adv Mater 15(21):1849–1853.  https://doi.org/10.1002/adma.200305580 CrossRefGoogle Scholar
  73. 73.
    Johnston APR, Cortez C, Angelatos AS, Caruso F (2006) Layer-by-layer engineered capsules and their applications. Curr Opin Colloid Interface Sci 11(4):203–209.  https://doi.org/10.1016/j.cocis.2006.05.001 CrossRefGoogle Scholar
  74. 74.
    Gupta R, Mcclelland JJ, Jabbour ZJ, Celotta RJ (1995) Nanofabrication of a 2-dimensional array using laser-focused atomic deposition. Appl Phys Lett 67(10):1378–1380.  https://doi.org/10.1063/1.115539
  75. 75.
    Bigi A, Bracci B, Cuisinier F, Elkaim R, Fini M, Mayer I, Mihailescu IN, Socol G, Sturba L, Torricelli P (2005) Human osteoblast response to pulsed laser deposited calcium phosphate coatings. Biomaterials 26(15):2381–2389.  https://doi.org/10.1016/j.biomaterials.2004.07.057 CrossRefGoogle Scholar
  76. 76.
    Thissen H, Hayes JP, Kingshott P, Johnson G, Harvey EC, Griesser HJ (2002) Nanometer thickness laser ablation for spatial control of cell attachment. Smart Mater Struct 11(5):792CrossRefGoogle Scholar
  77. 77.
    Meschede D, Metcalf H (2003) Atomic nanofabrication: atomic deposition and lithography by laser and magnetic forces. J Phys D Appl Phys 36(3):R17CrossRefGoogle Scholar
  78. 78.
    Sun H-B, Kawata S (2004) Two-photon photopolymerization and 3D lithographic microfabrication. In: NMR • 3D Analysis • Photopolymerization. Springer, Berlin, pp 169–273.  https://doi.org/10.1007/b94405
  79. 79.
    Lee K-S, Yang D-Y, Park SH, Kim RH (2006) Recent developments in the use of two-photon polymerization in precise 2D and 3D microfabrications. Polym Adv Technol 17(2):72–82.  https://doi.org/10.1002/pat.664 CrossRefGoogle Scholar
  80. 80.
    Marino A, Ciofani G, Filippeschi C, Pellegrino M, Pellegrini M, Orsini P, Pasqualetti M, Mattoli V, Mazzolai B (2013) Two-photon polymerization of sub-micrometric patterned surfaces: investigation of cell-substrate interactions and improved differentiation of neuron-like cells. ACS Appl Mater Interfaces 5(24):13012–13021.  https://doi.org/10.1021/am403895k CrossRefGoogle Scholar
  81. 81.
    Benjamin H, Kartik B, Michael P, Lijie Grace Z (2016) A synergistic approach to the design, fabrication and evaluation of 3D printed micro and nano featured scaffolds for vascularized bone tissue repair. Nanotechnology 27(6):064001CrossRefGoogle Scholar
  82. 82.
    Horii A, Wang X, Gelain F, Zhang S (2007) Biological designer self-assembling peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3-D migration. PLoS ONE 2(2):e190.  https://doi.org/10.1371/journal.pone.0000190 CrossRefGoogle Scholar
  83. 83.
    Choi C-H, Hagvall SH, Wu BM, Dunn JCY, Beygui RE, “Cj” Kim C-J (2007) Cell interaction with three-dimensional sharp-tip nanotopography. Biomaterials 28(9):1672–1679.  https://doi.org/10.1016/j.biomaterials.2006.11.031
  84. 84.
    Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6(12):997–1003. http://www.nature.com/nmat/journal/v6/n12/suppinfo/nmat2013_S1.html
  85. 85.
    Martínez E, Engel E, Planell JA, Samitier J (2009) Effects of artificial micro- and nano-structured surfaces on cell behaviour. Ann Anat - Anatomischer Anz 191(1):126–135.  https://doi.org/10.1016/j.aanat.2008.05.006 CrossRefGoogle Scholar
  86. 86.
    Larsen M, Artym VV, Green JA, Yamada KM (2006) The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol 18(5):463–471.  https://doi.org/10.1016/j.ceb.2006.08.009 CrossRefGoogle Scholar
  87. 87.
    Giancotti FG, Ruoslahti E (1999) Integrin Signaling. Science 285(5430):1028–1033.  https://doi.org/10.1126/science.285.5430.1028 CrossRefGoogle Scholar
  88. 88.
    Siebers MC, ter Brugge PJ, Walboomers XF, Jansen JA (2005) Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials 26(2):137–146.  https://doi.org/10.1016/j.biomaterials.2004.02.021 CrossRefGoogle Scholar
  89. 89.
    Burkin DJ, Kaufman SJ (1999) The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res 296(1):183–190CrossRefGoogle Scholar
  90. 90.
    Danen EHJ, Sonneveld P, Brakebusch C, Fässler R, Sonnenberg A (2002) The fibronectin-binding integrins α5β1 and αvβ3 differentially modulate RhoA–GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J Cell Biol 159(6):1071–1086.  https://doi.org/10.1083/jcb.200205014 CrossRefGoogle Scholar
  91. 91.
    Wozniak MA, Modzelewska K, Kwong L, Keely PJ (2004) Focal adhesion regulation of cell behavior. Biochimica et Biophysica Acta (BBA) - Molecular. Cell Res 1692(2–3):103–119.  https://doi.org/10.1016/j.bbamcr.2004.04.007 Google Scholar
  92. 92.
    Kim S-J, Park K-H, Park Y-G, Lee S-W, Kang Y-G (2013) Compressive stress induced the up-regulation of M-CSF, RANKL, TNF-α expression and the down-regulation of OPG expression in PDL cells via the integrin-FAK pathway. Arch Oral Biol 58(6):707–716.  https://doi.org/10.1016/j.archoralbio.2012.11.003 CrossRefGoogle Scholar
  93. 93.
    Barberis L, Wary KK, Fiucci G, Liu F, Hirsch E, Brancaccio M, Altruda F, Tarone G, Giancotti FG (2000) Distinct roles of the adaptor protein Shc and focal adhesion kinase in integrin signaling to ERK. J Biol Chem 275(47):36532–36540.  https://doi.org/10.1074/jbc.M002487200 CrossRefGoogle Scholar
  94. 94.
    Schwartz MA, Shattil SJ (2000) Signaling networks linking integrins and Rho family GTPases. Trends Biochem Sci 25(8):388–391.  https://doi.org/10.1016/s0968-0004(00)01605-4
  95. 95.
    Kaibuchi K, Kuroda S, Amano M (1999) Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem 68(1):459–486.  https://doi.org/10.1146/annurev.biochem.68.1.459 CrossRefGoogle Scholar
  96. 96.
    Thodeti CK, Albrechtsen R, Grauslund M, Asmar M, Larsson C, Takada Y, Mercurio AM, Couchman JR, Wewer UM (2003) ADAM12/Syndecan-4 signaling promotes β1Integrin-dependent cell spreading through protein kinase Cα and RhoA. J Biol Chem 278(11):9576–9584.  https://doi.org/10.1074/jbc.M208937200 CrossRefGoogle Scholar
  97. 97.
    Buhl AM, Johnson NL, Dhanasekaran N, Johnson GL (1995) Gα12 and Gα13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J Biol Chem 270(42):24631–24634.  https://doi.org/10.1074/jbc.270.42.24631 CrossRefGoogle Scholar
  98. 98.
    McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6(4):483–495.  https://doi.org/10.1016/S1534-5807(04)00075-9 CrossRefGoogle Scholar
  99. 99.
    Cukierman E, Pankov R, Yamada KM (2002) Cell interactions with three-dimensional matrices. Curr Opin Cell Biol 14(5):633–640.  https://doi.org/10.1016/S0955-0674(02)00364-2 CrossRefGoogle Scholar
  100. 100.
    Biggs MJP, Richards RG, McFarlane S, Wilkinson CDW, Oreffo ROC, Dalby MJ (2008) Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330 nm deep microgrooves. J R Soc Interface 5(27):1231–1242.  https://doi.org/10.1098/rsif.2008.0035 CrossRefGoogle Scholar
  101. 101.
    Bettinger CJ, Langer R, Borenstein JT (2009) Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Ed 48(30):5406–5415.  https://doi.org/10.1002/anie.200805179 CrossRefGoogle Scholar
  102. 102.
    Patel KD, Mahapatra C, Jin G-Z, Singh RK, Kim H-W (2015) Biocompatible mesoporous nanotubular structured surface to control cell behaviors and deliver bioactive molecules. ACS Appl Mater Interfaces 7(48):26850–26859.  https://doi.org/10.1021/acsami.5b09114 CrossRefGoogle Scholar
  103. 103.
    Ohta Y, Suzuki N, Nakamura S, Hartwig JH, Stossel TP (1999) The small GTPase RalA targets filamin to induce filopodia. Proc Natl Acad Sci 96(5):2122–2128.  https://doi.org/10.1073/pnas.96.5.2122 CrossRefGoogle Scholar
  104. 104.
    Dalby MJ, Gadegaard N, Riehle MO, Wilkinson CDW, Curtis ASG (2004) Investigating filopodia sensing using arrays of defined nano-pits down to 35 nm diameter in size. Int J Biochem Cell Biol 36(10):2005–2015.  https://doi.org/10.1016/j.biocel.2004.03.001 CrossRefGoogle Scholar
  105. 105.
    Albuschies J, Vogel V (2013) The role of filopodia in the recognition of nanotopographies. Sci Reports 3:1658.  https://doi.org/10.1038/srep01658 CrossRefGoogle Scholar
  106. 106.
    Alberts B, Johnson A, Lewis J, Morgan D, Raff MC, Roberts K, Walter P, Wilson JH, Hunt T (2015) Molecular biology of the cell. Sixth editionGoogle Scholar
  107. 107.
    Small JV, Stradal T, Vignal E, Rottner K (2002) The lamellipodium: where motility begins. Trends Cell Biol 12(3):112–120.  https://doi.org/10.1016/S0962-8924(01)02237-1 CrossRefGoogle Scholar
  108. 108.
    Wang H-R, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH, Wrana JL (2003) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302(5651):1775–1779.  https://doi.org/10.1126/science.1090772 CrossRefGoogle Scholar
  109. 109.
    Brammer KS, Oh S, Gallagher JO, Jin S (2008) Enhanced cellular mobility guided by TiO2 nanotube surfaces. Nano Lett 8(3):786–793.  https://doi.org/10.1021/nl072572o CrossRefGoogle Scholar
  110. 110.
    Alberts B, Johnson A, Lewis J, Morgan D, Raff MC, Roberts K, Walter P, Wilson JH, Hunt T Molecular biology of the cell. Sixth editionGoogle Scholar
  111. 111.
    Dalby MJ, Biggs MJP, Gadegaard N, Kalna G, Wilkinson CDW, Curtis ASG (2007) Nanotopographical stimulation of mechanotransduction and changes in interphase centromere positioning. J Cell Biochem 100(2):326–338.  https://doi.org/10.1002/jcb.21058 CrossRefGoogle Scholar
  112. 112.
    Bloom S, Lockard VG, Bloom M (1996) Intermediate filament-mediated stretch-induced changes in chromatin: a hypothesis for growth initiation in cardiac myocytes. J Mol Cell Cardiol 28(10):2123–2127.  https://doi.org/10.1006/jmcc.1996.0204 CrossRefGoogle Scholar
  113. 113.
    Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 6(6):468–473.  https://doi.org/10.1038/nphys1613 CrossRefGoogle Scholar
  114. 114.
    Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci 107(11):4872–4877.  https://doi.org/10.1073/pnas.0903269107 CrossRefGoogle Scholar
  115. 115.
    Oh S, Brammer KS, Li YSJ, Teng D, Engler AJ, Chien S, Jin S (2009) Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci 106(7):2130–2135.  https://doi.org/10.1073/pnas.0813200106 CrossRefGoogle Scholar
  116. 116.
    Hu J, Liu X, Ma PX (2008) Induction of osteoblast differentiation phenotype on poly(l-lactic acid) nanofibrous matrix. Biomaterials 29(28):3815–3821.  https://doi.org/10.1016/j.biomaterials.2008.06.015 CrossRefGoogle Scholar
  117. 117.
    Brammer KS, Choi C, Frandsen CJ, Oh S, Jin S (2011) Hydrophobic nanopillars initiate mesenchymal stem cell aggregation and osteo-differentiation. Acta Biomater 7(2):683–690.  https://doi.org/10.1016/j.actbio.2010.09.022 CrossRefGoogle Scholar
  118. 118.
    Zhang YZ, Su B, Venugopal J, Ramakrishna S, Lim CT (2007) Biomimetic and bioactive nanofibrous scaffolds from electrospun composite nanofibers. Int J Nanomed 2(4):623–638Google Scholar
  119. 119.
    Subramony SD, Dargis BR, Castillo M, Azeloglu EU, Tracey MS, Su A, Lu HH (2013) The guidance of stem cell differentiation by substrate alignment and mechanical stimulation. Biomaterials 34(8):1942–1953.  https://doi.org/10.1016/j.biomaterials.2012.11.012 CrossRefGoogle Scholar
  120. 120.
    Smith LA, Ma PX (2004) Nano-fibrous scaffolds for tissue engineering. Colloids Surf, B 39(3):125–131.  https://doi.org/10.1016/j.colsurfb.2003.12.004 CrossRefGoogle Scholar
  121. 121.
    Di Lullo GA, Sweeney SM, Korkko J, Ala-Kokko L, San Antonio JD (2002) Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J Biol Chem 277(6):4223–4231.  https://doi.org/10.1074/jbc.M110709200 CrossRefGoogle Scholar
  122. 122.
    Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17(3):319–336.  https://doi.org/10.1007/s00198-005-2035-9 CrossRefGoogle Scholar
  123. 123.
    Finlay HM, McCullough L, Canham PB (1995) Three-dimensional collagen organization of human brain arteries at different transmural pressures. J Vasc Res 32(5):301–312CrossRefGoogle Scholar
  124. 124.
    Giraud-Guille MM (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3):167–180.  https://doi.org/10.1007/bf02556330 CrossRefGoogle Scholar
  125. 125.
    Provenzano PP, Vanderby R Jr (2006) Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25(2):71–84.  https://doi.org/10.1016/j.matbio.2005.09.005 CrossRefGoogle Scholar
  126. 126.
    Bancelin S, Aimé C, Gusachenko I, Kowalczuk L, Latour G, Coradin T, Schanne-Klein M-C (2014) Determination of collagen fibril size via absolute measurements of second-harmonic generation signals. Nat Commun 5.  https://doi.org/10.1038/ncomms5920
  127. 127.
    Cui W, Zhou Y, Chang J (2010) Electrospun nanofibrous materials for tissue engineering and drug delivery. Sci Technol Adv Mater 11(1):014108.  https://doi.org/10.1088/1468-6996/11/1/014108 CrossRefGoogle Scholar
  128. 128.
    Huang Z-M, Zhang YZ, Kotaki M, Ramakrishna S (2003) A review on polymer nanofibers by electrospinning and their applications in nanocomposites. Compos Sci Technol 63(15):2223–2253.  https://doi.org/10.1016/S0266-3538(03)00178-7 CrossRefGoogle Scholar
  129. 129.
    Yan X, Gevelber M (2010) Investigation of electrospun fiber diameter distribution and process variations. J Electrostat 68(5):458–464.  https://doi.org/10.1016/j.elstat.2010.06.009 CrossRefGoogle Scholar
  130. 130.
    Beachley V, Wen X (2009) Effect of electrospinning parameters on the nanofiber diameter and length. Mater Sci Eng C, Mater Biol Appl 29(3):663–668.  https://doi.org/10.1016/j.msec.2008.10.037 CrossRefGoogle Scholar
  131. 131.
    Cho H, Min S-Y, Lee T-W (2013) Electrospun organic nanofiber electronics and photonics. Macromol Mater Eng 298(5):475–486.  https://doi.org/10.1002/mame.201200364 CrossRefGoogle Scholar
  132. 132.
    Lee S, Obendorf SK (2007) Use of electrospun nanofiber web for protective textile materials as barriers to liquid penetration. Text Res J 77(9):696–702.  https://doi.org/10.1177/0040517507080284 CrossRefGoogle Scholar
  133. 133.
    Lannutti J, Reneker D, Ma T, Tomasko D, Farson D (2007) Electrospinning for tissue engineering scaffolds. Mater Sci Eng, C 27(3):504–509.  https://doi.org/10.1016/j.msec.2006.05.019 CrossRefGoogle Scholar
  134. 134.
    Meng ZX, Wang YS, Ma C, Zheng W, Li L, Zheng YF (2010) Electrospinning of PLGA/gelatin randomly-oriented and aligned nanofibers as potential scaffold in tissue engineering. Mater Sci Eng, C 30(8):1204–1210.  https://doi.org/10.1016/j.msec.2010.06.018 CrossRefGoogle Scholar
  135. 135.
    Jin H-J, Chen J, Karageorgiou V, Altman GH, Kaplan DL (2004) Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials 25(6):1039–1047.  https://doi.org/10.1016/S0142-9612(03)00609-4 CrossRefGoogle Scholar
  136. 136.
    Yang F, Murugan R, Wang S, Ramakrishna S (2005) Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 26(15):2603–2610.  https://doi.org/10.1016/j.biomaterials.2004.06.051 CrossRefGoogle Scholar
  137. 137.
    Yin Z, Chen X, Chen JL, Shen WL, Hieu Nguyen TM, Gao L, Ouyang HW (2010) The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 31(8):2163–2175.  https://doi.org/10.1016/j.biomaterials.2009.11.083 CrossRefGoogle Scholar
  138. 138.
    Liu W, Wei Y, Zhang X, Xu M, Yang X, Deng X (2013) Lower extent but similar rhythm of osteogenic behavior in hBMSCs cultured on nanofibrous scaffolds versus induced with osteogenic supplement. ACS Nano 7(8):6928–6938.  https://doi.org/10.1021/nn402118s CrossRefGoogle Scholar
  139. 139.
    Zhang Y, Venugopal JR, El-Turki A, Ramakrishna S, Su B, Lim CT (2008) Electrospun biomimetic nanocomposite nanofibers of hydroxyapatite/chitosan for bone tissue engineering. Biomaterials 29(32):4314–4322.  https://doi.org/10.1016/j.biomaterials.2008.07.038 CrossRefGoogle Scholar
  140. 140.
    Feng ZQ, Leach MK, Chu XH, Wang YC, Tian T, Shi XL, Ding YT, Gu ZZ (2010) Electrospun chitosan nanofibers for hepatocyte culture. J Biomed Nanotechnol 6(6):658–666CrossRefGoogle Scholar
  141. 141.
    Ebrahimi-Barough S, Norouzi Javidan A, Saberi H, Joghataei MT, Rahbarghazi R, Mirzaei E, Faghihi F, Shirian S, Ai A, Ai J (2015) Evaluation of motor neuron-like cell differentiation of hEnSCs on biodegradable PLGA nanofiber scaffolds. Mol Neurobiol 52(3):1704–1713.  https://doi.org/10.1007/s12035-014-8931-2 CrossRefGoogle Scholar
  142. 142.
    Chen J-P, Su C-H (2011) Surface modification of electrospun PLLA nanofibers by plasma treatment and cationized gelatin immobilization for cartilage tissue engineering. Acta Biomater 7(1):234–243.  https://doi.org/10.1016/j.actbio.2010.08.015 CrossRefGoogle Scholar
  143. 143.
    Xie J, Willerth SM, Li X, Macewan MR, Rader A, Sakiyama-Elbert SE, Xia Y (2009) The differentiation of embryonic stem cells seeded on electrospun nanofibers into neural lineages. Biomaterials 30(3):354–362.  https://doi.org/10.1016/j.biomaterials.2008.09.046 CrossRefGoogle Scholar
  144. 144.
    Uyar T, Balan A, Toppare L, Besenbacher F (2009) Electrospinning of cyclodextrin functionalized poly(methyl methacrylate) (PMMA) nanofibers. Polymer 50(2):475–480.  https://doi.org/10.1016/j.polymer.2008.11.021 CrossRefGoogle Scholar
  145. 145.
    Bhattarai N, Edmondson D, Veiseh O, Matsen FA, Zhang M (2005) Electrospun chitosan-based nanofibers and their cellular compatibility. Biomaterials 26(31):6176–6184.  https://doi.org/10.1016/j.biomaterials.2005.03.027 CrossRefGoogle Scholar
  146. 146.
    Kriegel C, Kit KM, McClements DJ, Weiss J (2009) Electrospinning of chitosan–poly(ethylene oxide) blend nanofibers in the presence of micellar surfactant solutions. Polymer 50(1):189–200.  https://doi.org/10.1016/j.polymer.2008.09.041 CrossRefGoogle Scholar
  147. 147.
    Zhang Y, Huang Z-M, Xu X, Lim CT, Ramakrishna S (2004) Preparation of core–shell structured PCL-r-Gelatin Bi-component nanofibers by coaxial electrospinning. Chem Mater 16(18):3406–3409.  https://doi.org/10.1021/cm049580f CrossRefGoogle Scholar
  148. 148.
    Mandal S, Bhaskar S, Lahann J (2009) Micropatterned fiber scaffolds for spatially controlled cell adhesion. Macromol Rapid Commun 30(19):1638–1644.  https://doi.org/10.1002/marc.200900340 CrossRefGoogle Scholar
  149. 149.
    Liu X, Ma PX (2009) Phase separation, pore structure, and properties of nanofibrous gelatin scaffolds. Biomaterials 30(25):4094–4103.  https://doi.org/10.1016/j.biomaterials.2009.04.024 CrossRefGoogle Scholar
  150. 150.
    Woo KM, Jun J-H, Chen VJ, Seo J, Baek J-H, Ryoo H-M, Kim G-S, Somerman MJ, Ma PX (2007) Nano-fibrous scaffolding promotes osteoblast differentiation and biomineralization. Biomaterials 28(2):335–343.  https://doi.org/10.1016/j.biomaterials.2006.06.013 CrossRefGoogle Scholar
  151. 151.
    Wang Y, Hu J, Jiao J, Liu Z, Zhou Z, Zhao C, Chang L-J, Chen YE, Ma PX, Yang B (2014) Engineering vascular tissue with functional smooth muscle cells derived from human iPS cells and nanofibrous scaffolds. Biomaterials 35(32):8960–8969.  https://doi.org/10.1016/j.biomaterials.2014.07.011 CrossRefGoogle Scholar
  152. 152.
    Hu J, Feng K, Liu X, Ma PX (2009) Chondrogenic and osteogenic differentiations of human bone marrow-derived mesenchymal stem cells on a nanofibrous scaffold with designed pore network. Biomaterials 30(28):5061–5067.  https://doi.org/10.1016/j.biomaterials.2009.06.013 CrossRefGoogle Scholar
  153. 153.
    Smith LA, Liu X, Hu J, Ma PX (2009) The influence of three-dimensional nanofibrous scaffolds on the osteogenic differentiation of embryonic stem cells. Biomaterials 30(13):2516–2522.  https://doi.org/10.1016/j.biomaterials.2009.01.009 CrossRefGoogle Scholar
  154. 154.
    Feng G, Zhang Z, Jin X, Hu J, Gupte MJ, Holzwarth JM, Ma PX (2012) Regenerating nucleus pulposus of the intervertebral disc using biodegradable nanofibrous polymer scaffolds. Tissue Eng Part A 18(21–22):2231–2238.  https://doi.org/10.1089/ten.tea.2011.0747 CrossRefGoogle Scholar
  155. 155.
    Hu J, Sun X, Ma H, Xie C, Chen YE, Ma PX (2010) Porous nanofibrous PLLA scaffolds for vascular tissue engineering. Biomaterials 31(31):7971–7977.  https://doi.org/10.1016/j.biomaterials.2010.07.028 CrossRefGoogle Scholar
  156. 156.
    Khatiwala CB, Kim PD, Peyton SR, Putnam AJ (2009) ECM compliance regulates osteogenesis by influencing MAPK signaling downstream of RhoA and ROCK. J Bone Miner Res: Official J Am Soc Bone Miner Res 24(5):886–898.  https://doi.org/10.1359/jbmr.081240 CrossRefGoogle Scholar
  157. 157.
    Eda H, Kulig KM, Steiner TA, Shimada H, Patel K, Park E, Kim ES, Borenstein JT, Neville CM, Keller BT (2012) A nanofiber membrane maintains the quiescent phenotype of hepatic stellate cells. Dig Dis Sci 57(5):1152–1162.  https://doi.org/10.1007/s10620-012-2084-9 CrossRefGoogle Scholar
  158. 158.
    Hofmeister LH, Costa L, Balikov DA, Crowder SW, Terekhov A, Sung HJ, Hofmeister WH (2015) Patterned polymer matrix promotes stemness and cell-cell interaction of adult stem cells. J Biol Eng 9:18.  https://doi.org/10.1186/s13036-015-0016-x CrossRefGoogle Scholar
  159. 159.
    Erisken C, Zhang X, Moffat KL, Levine WN, Lu HH (2013) Scaffold fiber diameter regulates human tendon fibroblast growth and differentiation. Tissue Eng Part A 19(3–4):519–528.  https://doi.org/10.1089/ten.tea.2012.0072 CrossRefGoogle Scholar
  160. 160.
    Bashur CA, Shaffer RD, Dahlgren LA, Guelcher SA, Goldstein AS (2009) Effect of fiber diameter and alignment of electrospun polyurethane meshes on mesenchymal progenitor cells. Tissue Eng Part A 15(9):2435–2445.  https://doi.org/10.1089/ten.tea.2008.0295 CrossRefGoogle Scholar
  161. 161.
    Chen Y, Zeng D, Ding L, Li X-L, Liu X-T, Li W-J, Wei T, Yan S, Xie J-H, Wei L, Zheng Q-S (2015) Three-dimensional poly-(ε-caprolactone) nanofibrous scaffolds directly promote the cardiomyocyte differentiation of murine-induced pluripotent stem cells through Wnt/β-catenin signaling. BMC Cell Biol 16(1):1–13.  https://doi.org/10.1186/s12860-015-0067-3 CrossRefGoogle Scholar
  162. 162.
    Wang Y, Yao M, Zhou J, Zheng W, Zhou C, Dong D, Liu Y, Teng Z, Jiang Y, Wei G, Cui X (2011) The promotion of neural progenitor cells proliferation by aligned and randomly oriented collagen nanofibers through β1 integrin/MAPK signaling pathway. Biomaterials 32(28):6737–6744.  https://doi.org/10.1016/j.biomaterials.2011.05.075 CrossRefGoogle Scholar
  163. 163.
    Sivashanmugam A, Arun Kumar R, Vishnu Priya M, Nair SV, Jayakumar R (2015) An overview of injectable polymeric hydrogels for tissue engineering. Eur Polymer J 72:543–565.  https://doi.org/10.1016/j.eurpolymj.2015.05.014 CrossRefGoogle Scholar
  164. 164.
    Balakrishnan B, Banerjee R (2011) Biopolymer-based hydrogels for cartilage tissue engineering. Chem Rev 111(8):4453–4474.  https://doi.org/10.1021/cr100123h CrossRefGoogle Scholar
  165. 165.
    Srouji S, Rachmiel A, Blumenfeld I, Livne E (2005) Mandibular defect repair by TGF-β and IGF-1 released from a biodegradable osteoconductive hydrogel. J Cranio-Maxillofac Surg 33(2):79–84.  https://doi.org/10.1016/j.jcms.2004.09.003 CrossRefGoogle Scholar
  166. 166.
    Hern DL, Hubbell JA (1998) Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J Biomed Mater Res 39(2):266–276. https://doi.org/10.1002/(sici)1097-4636(199802)39:2<266:aid-jbm14>3.0.co;2-b CrossRefGoogle Scholar
  167. 167.
    Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24(24):4337–4351.  https://doi.org/10.1016/S0142-9612(03)00340-5 CrossRefGoogle Scholar
  168. 168.
    Cui FZ, Tian WM, Hou SP, Xu QY, Lee I-S (2006) Hyaluronic acid hydrogel immobilized with RGD peptides for brain tissue engineering. J Mater Sci - Mater Med 17(12):1393–1401.  https://doi.org/10.1007/s10856-006-0615-7 CrossRefGoogle Scholar
  169. 169.
    Oyen ML (2014) Mechanical characterisation of hydrogel materials. Int Mater Rev 59(1):44–59.  https://doi.org/10.1179/1743280413y.0000000022 CrossRefGoogle Scholar
  170. 170.
    Hong Y, Huber A, Takanari K, Amoroso NJ, Hashizume R, Badylak SF, Wagner WR (2011) Mechanical properties and in vivo behavior of a biodegradable synthetic polymer microfiber–extracellular matrix hydrogel biohybrid scaffold. Biomaterials 32(13):3387–3394.  https://doi.org/10.1016/j.biomaterials.2011.01.025 CrossRefGoogle Scholar
  171. 171.
    Liu X, Jin X, Ma PX (2011) Nanofibrous hollow microspheres self-assembled from star-shaped polymers as injectable cell carriers for knee repair. Nat Mater 10(5):398–406. http://www.nature.com/nmat/journal/v10/n5/abs/nmat2999.html#supplementary-information
  172. 172.
    Lutolf MP, Lauer-Fields JL, Schmoekel HG, Metters AT, Weber FE, Fields GB, Hubbell JA (2003) Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci 100(9):5413–5418.  https://doi.org/10.1073/pnas.0737381100 CrossRefGoogle Scholar
  173. 173.
    Qutachi O, Vetsch JR, Gill D, Cox H, Scurr DJ, Hofmann S, Müller R, Quirk RA, Shakesheff KM, Rahman CV (2014) Injectable and porous PLGA microspheres that form highly porous scaffolds at body temperature. Acta Biomater 10(12):5090–5098.  https://doi.org/10.1016/j.actbio.2014.08.015 CrossRefGoogle Scholar
  174. 174.
    Garkhal K, Verma S, Tikoo K, Kumar N (2007) Surface modified poly(L-lactide-co-ε-caprolactone) microspheres as scaffold for tissue engineering. J Biomed Mater Res, Part A 82A(3):747–756.  https://doi.org/10.1002/jbm.a.31150 CrossRefGoogle Scholar
  175. 175.
    Qiu Q-Q, Ducheyne P, Ayyaswamy PS (2000) New bioactive, degradable composite microspheres as tissue engineering substrates. J Biomed Mater Res 52(1):66–76. https://doi.org/10.1002/1097-4636(200010)52:1<66:aid-jbm9>3.0.co;2-2 CrossRefGoogle Scholar
  176. 176.
    Zhang Z, Gupte MJ, Jin X, Ma PX (2015) Injectable peptide decorated functional nanofibrous hollow microspheres to direct stem cell differentiation and tissue regeneration. Adv Func Mater 25(3):350–360.  https://doi.org/10.1002/adfm.201402618 CrossRefGoogle Scholar
  177. 177.
    Zhang Z, Marson RL, Ge Z, Glotzer SC, Ma PX (2015) Simultaneous nano- and microscale control of nanofibrous microspheres self-assembled from star-shaped polymers. Adv Mater 27(26):3947–3952.  https://doi.org/10.1002/adma.201501329 CrossRefGoogle Scholar
  178. 178.
    Kuang R, Zhang Z, Jin X, Hu J, Gupte MJ, Ni L, Ma PX (2015) Nanofibrous spongy microspheres enhance odontogenic differentiation of human dental pulp stem cells. Adv Healthc Mater 4(13):1993–2000.  https://doi.org/10.1002/adhm.201500308 CrossRefGoogle Scholar
  179. 179.
    Flemming RG, Murphy CJ, Abrams GA, Goodman SL, Nealey PF (1999) Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials 20(6):573–588.  https://doi.org/10.1016/S0142-9612(98)00209-9 CrossRefGoogle Scholar
  180. 180.
    Walboomers XF, Croes HJE, Ginsel LA, Jansen JA (1998) Growth behavior of fibroblasts on microgrooved polystyrene. Biomaterials 19(20):1861–1868.  https://doi.org/10.1016/S0142-9612(98)00093-3 CrossRefGoogle Scholar
  181. 181.
    Dalton BA, Walboomers XF, Dziegielewski M, Evans MDM, Taylor S, Jansen JA, Steele JG (2001) Modulation of epithelial tissue and cell migration by microgrooves. J Biomed Mater Res 56(2):195–207. https://doi.org/10.1002/1097-4636(200108)56:2<195:aid-jbm1084>3.0.co;2-7 CrossRefGoogle Scholar
  182. 182.
    Matsuzaka K, Walboomers F, De Ruijter A, Jansen JA (2000) Effect of microgrooved poly-l-lactic (PLA) surfaces on proliferation, cytoskeletal organization, and mineralized matrix formation of rat bone marrow cells. Clin Oral Implant Res 11(4):325–333.  https://doi.org/10.1034/j.1600-0501.2000.011004325.x CrossRefGoogle Scholar
  183. 183.
    den Braber ET, de Ruijter JE, Smits HTJ, Ginsel LA, von Recum AF, Jansen JA (1996) Quantitative analysis of cell proliferation and orientation on substrata with uniform parallel surface micro-grooves. Biomaterials 17(11):1093–1099.  https://doi.org/10.1016/0142-9612(96)85910-2 CrossRefGoogle Scholar
  184. 184.
    Zhu B, Lu Q, Yin J, Hu J, Wang Z (2005) Alignment of osteoblast-like cells and cell-produced collagen matrix induced by nanogrooves. Tissue Eng 11(5–6):825–834.  https://doi.org/10.1089/ten.2005.11.825 CrossRefGoogle Scholar
  185. 185.
    Gomez N, Lu Y, Chen S, Schmidt CE (2007) Immobilized nerve growth factor and microtopography have distinct effects on polarization versus axon elongation in hippocampal cells in culture. Biomaterials 28(2):271–284.  https://doi.org/10.1016/j.biomaterials.2006.07.043 CrossRefGoogle Scholar
  186. 186.
    Lamers E, Frank Walboomers X, Domanski M, te Riet J, van Delft FCMJM, Luttge R, Winnubst LAJA, Gardeniers HJGE, Jansen JA (2010) The influence of nanoscale grooved substrates on osteoblast behavior and extracellular matrix deposition. Biomaterials 31(12):3307–3316.  https://doi.org/10.1016/j.biomaterials.2010.01.034 CrossRefGoogle Scholar
  187. 187.
    Frimat JP, Xie SJ, Bastiaens A, Schurink B, Wolbers F, den Toonder J, Luttge R (2015) Advances in 3D neuronal cell culture. J Vac Sci Technol B 33(6):06f902.  https://doi.org/10.1116/1.4931636
  188. 188.
    Kim MS, Kim AY, Jang KJ, Kim JH, Kim JB, Suh KY (2011) Effect of nanogroove geometry on adipogenic differentiation. Nanotechnology 22(49):494017CrossRefGoogle Scholar
  189. 189.
    Yim EKF, Pang SW, Leong KW (2007) Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 313(9):1820–1829.  https://doi.org/10.1016/j.yexcr.2007.02.031 CrossRefGoogle Scholar
  190. 190.
    Wilkinson A, Hewitt RN, McNamara LE, McCloy D, Dominic Meek RM, Dalby MJ (2011) Biomimetic microtopography to enhance osteogenesis in vitro. Acta Biomater 7(7):2919–2925.  https://doi.org/10.1016/j.actbio.2011.03.026 CrossRefGoogle Scholar
  191. 191.
    Shibakawa A, Yudoh K, Masuko-Hongo K, Kato T, Nishioka K, Nakamura H (2005) The role of subchondral bone resorption pits in osteoarthritis: MMP production by cells derived from bone marrow. Osteoarthritis and Cartilage 13(8):679–687.  https://doi.org/10.1016/j.joca.2005.04.010 CrossRefGoogle Scholar
  192. 192.
    Rumpler M, Würger T, Roschger P, Zwettler E, Sturmlechner I, Altmann P, Fratzl P, Rogers MJ, Klaushofer K (2013) Osteoclasts on bone and dentin in vitro: mechanism of trail formation and comparison of resorption behavior. Calcif Tissue Int 93(6):526–539.  https://doi.org/10.1007/s00223-013-9786-7 CrossRefGoogle Scholar
  193. 193.
    Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol: CJASN 3(Suppl 3):S131–S139.  https://doi.org/10.2215/cjn.04151206 CrossRefGoogle Scholar
  194. 194.
    Davison MJ, McMurray RJ, Smith C-A, Dalby MJ, Meek RMD (2016) Nanopit-induced osteoprogenitor cell differentiation: the effect of nanopit depth. J Tissue Eng 7:2041731416652778.  https://doi.org/10.1177/2041731416652778 CrossRefGoogle Scholar
  195. 195.
    Biggs MJP, Richards RG, Gadegaard N, Wilkinson CDW, Dalby MJ (2007) The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading. J Mater Sci - Mater Med 18(2):399–404.  https://doi.org/10.1007/s10856-006-0705-6 CrossRefGoogle Scholar
  196. 196.
    Ni S, Sun L, Ercan B, Liu L, Ziemer K, Webster TJ (2014) A mechanism for the enhanced attachment and proliferation of fibroblasts on anodized 316L stainless steel with nano-pit arrays. J Biomed Mater Res B Appl Biomater 102(6):1297–1303.  https://doi.org/10.1002/jbm.b.33127 CrossRefGoogle Scholar
  197. 197.
    Gadegaard N, Mosler S, Larsen NB (2003) Biomimetic Polymer Nanostructures by Injection Molding. Macromol Mater Eng 288(1):76–83.  https://doi.org/10.1002/mame.200290037 CrossRefGoogle Scholar
  198. 198.
    Dalby MJ, McCloy D, Robertson M, Agheli H, Sutherland D, Affrossman S, Oreffo ROC (2006) Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27(15):2980–2987.  https://doi.org/10.1016/j.biomaterials.2006.01.010 CrossRefGoogle Scholar
  199. 199.
    Curtis ASG, Casey B, Gallagher JO, Pasqui D, Wood MA, Wilkinson CDW (2001) Substratum nanotopography and the adhesion of biological cells. Are symmetry or regularity of nanotopography important? Biophys Chem 94(3):275–283.  https://doi.org/10.1016/S0301-4622(01)00247-2 CrossRefGoogle Scholar
  200. 200.
    Brammer KS, Choi C, Frandsen CJ, Oh S, Johnston G, Jin S (2011) Comparative cell behavior on carbon-coated TiO2 nanotube surfaces for osteoblasts vs. osteo-progenitor cells. Acta Biomater 7(6):2697–2703.  https://doi.org/10.1016/j.actbio.2011.02.039 CrossRefGoogle Scholar
  201. 201.
    Park J, Bauer S, von der Mark K, Schmuki P (2007) Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett 7(6):1686–1691.  https://doi.org/10.1021/nl070678d CrossRefGoogle Scholar
  202. 202.
    Oh S-H, Finõnes RR, Daraio C, Chen L-H, Jin S (2005) Growth of nano-scale hydroxyapatite using chemically treated titanium oxide nanotubes. Biomaterials 26(24):4938–4943.  https://doi.org/10.1016/j.biomaterials.2005.01.048 CrossRefGoogle Scholar
  203. 203.
    Lee J-H, Shim W, Choolakadavil Khalid N, Kang W-S, Lee M, Kim H-S, Choi J, Lee G, Kim J-H (2015) Random networks of single-walled carbon nanotubes promote mesenchymal stem cell’s proliferation and differentiation. ACS Appl Mater Interfaces 7(3):1560–1567.  https://doi.org/10.1021/am506833q CrossRefGoogle Scholar
  204. 204.
    Bauer S, Park J, Kvd Mark, Schmuki P (2008) Improved attachment of mesenchymal stem cells on super-hydrophobic TiO2 nanotubes. Acta Biomater 4(5):1576–1582.  https://doi.org/10.1016/j.actbio.2008.04.004 CrossRefGoogle Scholar
  205. 205.
    Sniadecki NJ (2009) Cellular mechanotransduction studies using microposts, nanoposts and magnetic posts. In: Proceedings of the Asme Summer Bioengineering Conference 2008, Pts A and B:1047–1048Google Scholar
  206. 206.
    Kim D-H, Kim P, Song I, Cha JM, Lee SH, Kim B, Suh KY (2006) Guided three-dimensional growth of functional cardiomyocytes on polyethylene glycol nanostructures. Langmuir 22(12):5419–5426.  https://doi.org/10.1021/la060283u CrossRefGoogle Scholar
  207. 207.
    Rasmussen CH, Reynolds PM, Petersen DR, Hansson M, McMeeking RM, Dufva M, Gadegaard N (2016) Nanostructures: enhanced differentiation of human embryonic stem cells toward definitive endoderm on ultrahigh aspect ratio nanopillars (Adv. Funct. Mater. 6/2016). Adv Func Mater 26(6):814.  https://doi.org/10.1002/adfm.201670038 CrossRefGoogle Scholar
  208. 208.
    Migliorini E, Ban J, Grenci G, Andolfi L, Pozzato A, Tormen M, Torre V, Lazzarino M (2013) Nanomechanics controls neuronal precursors adhesion and differentiation. Biotechnol Bioeng 110(8):2301–2310.  https://doi.org/10.1002/bit.24880 CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Biologic and Materials SciencesUniversity of MichiganAnn ArborUSA
  2. 2.Department of Biomedical EngineeringUniversity of MichiganAnn ArborUSA
  3. 3.Macromolecular Science and Engineering CenterUniversity of MichiganAnn ArborUSA

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