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Cellular Response to Surface Topography and Substrate Stiffness

  • Qi Zhang
  • Shiyun Lin
  • Qianshun Li
  • Dan Zhao
  • Xiaoxiao CaiEmail author
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Materials can dominate stem cell fate by chemical, biological, topographical and mechanical approaches. Cell feel the cues provided by biomaterial surfaces at both micrometer and nanometer scale, which leads to a series of signal pathways changing dominated by integrin. In addition, as an irregular pattern, the influence of substrate roughness on cellular behavior is also considered in this chapter. Another mechanical cue that affected cell behavior is the stiffness of substrate. Through an understanding of micro/nano-patterns and substrate stiffness that regulate cell behavior and decide stem cells’ fates, a more superior design of biomaterials will be employed in tissue engineering and regenerative medicine.

Keywords

Stiffness Roughness Tissue engineering Stem cell 

Notes

Acknowledgements

This work was funded by National Natural Science Foundation of China (81201211, 81471803).

Conflict of Interest: There are no any financial or other relationships with other people or organizations that might lead to a conflict of interest.

References

  1. 1.
    Mano JF, Silva GA, Azevedo HS, Malafaya PB, Sousa RA, Silva SS, Boesel LF, Oliveira JM, Santos TC, Marques AP. Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface. 2008;4:999–1030.CrossRefGoogle Scholar
  2. 2.
    Wang L, Shansky J, Borselli C, Mooney D, Vandenburgh H. Design and fabrication of a biodegradable, covalently crosslinked shape-memory alginate scaffold for cell and growth factor delivery. Tissue Eng A. 2012;18:2000–7.CrossRefGoogle Scholar
  3. 3.
    Bi H, Jin Y. Current progress of skin tissue engineering: seed cells, bioscaffolds, and construction strategies. Burns Trauma. 2013;1:63–72.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Alves NM, Pashkuleva I, Rui LR, Mano JF. Controlling cell behavior through the design of polymer surfaces. Small. 2010;6:2208–20.PubMedCrossRefGoogle Scholar
  5. 5.
    Griffin MF, Butler PE, Seifalian AM, Kalaskar DM. Control of stem cell fate by engineering their micro and nanoenvironment. World J Stem Cells. 2015;7:37–50.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310:1139–43.PubMedCrossRefGoogle Scholar
  7. 7.
    Pelham Jr RJ, Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A. 1997;94:13661–5.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–89.PubMedCrossRefGoogle Scholar
  9. 9.
    Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009;326:1216–9.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Montanaro L, Campoccia D, Arciola CR. Nanostructured materials for inhibition of bacterial adhesion in orthopedic implants: a minireview. Int J Artif Organs. 2008;31:771–6.PubMedGoogle Scholar
  11. 11.
    Mavrogenis AF, Dimitriou R, Parvizi J, Babis GC. Biology of implant osseointegration. J Musculoskelet Nueronal Interact. 2009;9:61–71.Google Scholar
  12. 12.
    Tobiasch E. Differentiation potential of adult human mesenchymal stem cells. Berlin: Springer; 2011.CrossRefGoogle Scholar
  13. 13.
    Deng S, Huang R, Wang J, Zhang S, Chen Z, Wu S, Jiang Y, Peng Q, Cai X, Lin Y. Miscellaneous animal models accelerate the application of mesenchymal stem cells for cartilage regeneration. Curr Stem Cell Res Ther. 2014;9:223–33.PubMedCrossRefGoogle Scholar
  14. 14.
    Carter SB. Haptotactic islands: a method of confining single cells to study individual cell reactions and clone formation. Exp Cell Res. 1967;48:189–93.PubMedCrossRefGoogle Scholar
  15. 15.
    Kaneda S, Fujii T. Micro/nano fabrication technique by soft lithography. 2004;53:341.Google Scholar
  16. 16.
    Ruiz SA, Chen CS. Microcontact printing: a tool to pattern. Soft Matter. 2007;3:168–77.CrossRefGoogle Scholar
  17. 17.
    Park TH, Shuler ML. Integration of cell culture and microfabrication technology. Biotechnol Prog. 2003;19:243–53.PubMedCrossRefGoogle Scholar
  18. 18.
    Otsuka H. Nanofabrication of nonfouling surfaces for micropatterning of cell and microtissue. Molecules. 2010;15:5525–46.PubMedCrossRefGoogle Scholar
  19. 19.
    Haushalter RC, Vetcha S. Microcontact printing device. US, US 20080066634 A1[P]. 2008.Google Scholar
  20. 20.
    Théry M. Micropatterning as a tool to decipher cell morphogenesis and functions. J Cell Sci. 2010;123:4201–13.PubMedCrossRefGoogle Scholar
  21. 21.
    Bernard A, Renault JP, Michel B, Bosshard HR, Delamarche E. Microcontact printing of proteins. Adv Mater. 2000;12:1067–70.CrossRefGoogle Scholar
  22. 22.
    Karp JM, Yeo Y, Geng W, Cannizarro C, Yan K, Kohane DS, Vunjak-Novakovic G, Langer RS, Radisic M. A photolithographic method to create cellular micropatterns. Biomaterials. 2006;27:4755–64.PubMedCrossRefGoogle Scholar
  23. 23.
    Itoga K, Kobayashi J, Yamato M, Kikuchi A, Okano T. Maskless liquid-crystal-display projection photolithography for improved design flexibility of cellular micropatterns. Biomaterials. 2006;27:3005–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Ruiz A, Zychowicz M, Buzanska L, Mehn D, Mills CA, Martinez E, Coecke S, Samitier J, Colpo P, Rossi F. Single stem cell positioning on polylysine and fibronectin microarrays. Micro Nanosyst. 2009;1:50–6(7).CrossRefGoogle Scholar
  25. 25.
    Kim M, Choi JC, Jung HR, Katz JS, Kim MG, Doh J. Addressable micropatterning of multiple proteins and cells by microscope projection photolithography based on a protein friendly photoresist. Langmuir. 2010;26:12112–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Kikuchi Y, Nakanishi J, Nakayama H, Shimizu T, Yoshino Y, Yamaguchi K, Yoshida Y, Horiike Y. Grafting poly(ethylene glycol) to a glass surface via a photocleavable linker for light-induced cell micropatterning and cell proliferation control. Chem Lett. 2008;37:1062–3.CrossRefGoogle Scholar
  27. 27.
    Falconnet D, Koenig A, Assi F, Textor M. A combined photolithographic and molecular-assembly approach to produce functional micropatterns for applications in the biosciences. Adv Funct Mater. 2004;14:749–56.CrossRefGoogle Scholar
  28. 28.
    Kozak J, Rajurkar KP, Makkar Y. Selected problems of micro-electrochemical machining. J Mater Process Technol. 2004;149:426–31.CrossRefGoogle Scholar
  29. 29.
    Khademhosseini A, Eng G, Yeh J, Kucharczyk PA, Langer R, Vunjak-Novakovic G, Radisic M. Microfluidic patterning for fabrication of contractile cardiac organoids. Biomed Microdevices. 2007;9:149–57.PubMedCrossRefGoogle Scholar
  30. 30.
    Khetani SR, Bhatia SN. Microscale culture of human liver cells for drug development. Nat Biotechnol. 2008;26:120–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Tan W, Desai TA. Microfluidic patterning of cells in extracellular matrix biopolymers: effects of channel size, cell type, and matrix composition on pattern integrity. Tissue Eng. 2003;9:255–67.PubMedCrossRefGoogle Scholar
  32. 32.
    Zheng C, Wang J, Pang Y, Wang J, Li W, Ge Z, Huang Y. High-throughput immunoassay through in-channel microfluidic patterning. Lab Chip. 2012;12:2487–90.PubMedCrossRefGoogle Scholar
  33. 33.
    Sun J, Zhou Y, Deng J, Zhao J. Effect of hybrid texture combining micro-pits and micro-grooves on cutting performance of WC/Co-based tools. Int J Adv Manuf Technol. 2016;86:1–12.Google Scholar
  34. 34.
    Schoen I, Wei H, Klotzsch E, Vogel V. Probing cellular traction forces by micropillar arrays: contribution of substrate warping to pillar deflection. Nano Lett. 2010;10:1823–30.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Wilkinson CDW, Riehle M, Wood M, Gallagher J, Curtis ASG. The use of materials patterned on a nano- and micro-metric scale in cellular engineering. Mater Sci Eng C. 2002;19:263–9.CrossRefGoogle Scholar
  36. 36.
    Rong P, Xiang Y, Ding J. Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. Biomaterials. 2011;32:8048–57.CrossRefGoogle Scholar
  37. 37.
    Kumar G, Ho CC, Co CC. Cell-substrate interactions feedback to direct cell migration along or against morphological polarization. PLoS One. 2015;10:e0133117.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Sayin E, Türker BE, Hasirci V. Osteogenic differentiation of adipose derived stem cells on high and low aspect ratio micropatterns. J Biomater Sci Polym Ed. 2015;26:1–44.CrossRefGoogle Scholar
  39. 39.
    Hu J, Hardy C, Chen CM, Yang S, Voloshin AS, Liu Y. Enhanced cell adhesion and alignment on micro-wavy patterned surfaces. PLoS One. 2014;9:e104502.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Abagnale G, Steger M, Nguyen VH, Hersch N, Sechi A, Joussen S, Denecke B, Merkel R, Hoffmann B, Dreser A. Surface topography enhances differentiation of mesenchymal stem cells towards osteogenic and adipogenic lineages. Biomaterials. 2015;61:316–26.PubMedCrossRefGoogle Scholar
  41. 41.
    Carvalho A, Pelaezvargas A, Hansford DJ, Fernandes MH, Monteiro FJ. Effects of line and pillar array microengineered SiO2 thin films on the osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. Langmuir. 2016;32(4):1091–100.PubMedCrossRefGoogle Scholar
  42. 42.
    Jeon H, Hidai H, Hwang DJ, Healy KE, Grigoropoulos CP. The effect of micronscale anisotropic cross patterns on fibroblast migration. Biomaterials. 2010;31:4286–95.PubMedCrossRefGoogle Scholar
  43. 43.
    Lim JY. Topographic control of cell response to synthetic materials. Tissue Eng Regen Med. 6:365–70.Google Scholar
  44. 44.
    Wang PY, Li WT, Yu J, Tsai WB. Modulation of osteogenic, adipogenic and myogenic differentiation of mesenchymal stem cells by submicron grooved topography. J Mater Sci Mater Med. 2012;23:3015–28.PubMedCrossRefGoogle Scholar
  45. 45.
    Engel E, Martínez E, Mills CA, Funes M, Planell JA, Samitier J. Mesenchymal stem cell differentiation on microstructured poly (methyl methacrylate) substrates. Ann Anat. 2009;191:136–44.PubMedCrossRefGoogle Scholar
  46. 46.
    Yang Y, Kusano K, Frei H, Rossi F, Brunette DM, Putnins EE. Microtopographical regulation of adult bone marrow progenitor cells chondrogenic and osteogenic gene and protein expressions. J Biomed Mater Res A. 2010;95:294–304.PubMedCrossRefGoogle Scholar
  47. 47.
    Hamilton DW, Wong KS, Brunette DM. Microfabricated discontinuous-edge surface topographies influence osteoblast adhesion, migration, cytoskeletal organization, and proliferation and enhance matrix and mineral deposition in vitro. Calcif Tissue Int. 2006;78:314–25.PubMedCrossRefGoogle Scholar
  48. 48.
    Poellmann MJ, Harrell PA, King WP, Johnson AJW. Geometric microenvironment directs cell morphology on topographically patterned hydrogel substrates. Acta Biomater. 2010;6:3514–23.PubMedCrossRefGoogle Scholar
  49. 49.
    Davis KA, Burke KA, Mather PT, Henderson JH. Dynamic cell behavior on shape memory polymer substrates. Biomaterials. 2011;32:2285–93.PubMedCrossRefGoogle Scholar
  50. 50.
    Le DM, Kulangara K, Adler AF, Leong KW, Ashby VS. Dynamic topographical control of mesenchymal stem cells by culture on responsive poly(ε-caprolactone) surfaces. Adv Mater. 2011;23:3278–83.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Tao G, Zhao K, Yang G, Li J, Chen H, Chen Y, Zhou S. Tissue engineering: the control of mesenchymal stem cell differentiation using dynamically tunable surface microgrooves (Adv. Healthcare Mater. 10/2014). Adv Healthcare Mater. 2014;3:397–8.Google Scholar
  52. 52.
    Park S, Im GI. Stem cell responses to nanotopography. J Biomed Mater Res A. 2015;103:1238–45.PubMedCrossRefGoogle Scholar
  53. 53.
    Abrams GA, Goodman SL, Nealey PF, Franco M, Murphy CJ. Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res. 2000;299:39–46.PubMedCrossRefGoogle Scholar
  54. 54.
    Gerecht S, Bettinger CJ, Zhang Z, Borenstein JT, Vunjak-Novakovic G, Langer R. The effect of actin disrupting agents on contact guidance of human embryonic stem cells. Biomaterials. 2007;28:4068–77.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Yim EKF, Darling EM, Kulangara K, Guilak F, Leong KW. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials. 2010;31:1299–306.PubMedCrossRefGoogle Scholar
  56. 56.
    Kafi MA, El-Said WA, Kim TH, Choi JW. Cell adhesion, spreading, and proliferation on surface functionalized with RGD nanopillar arrays. Biomaterials. 2012;33:731–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Cha KJ, Hong JM, Cho DW, Kim DS. Enhanced osteogenic fate and function of MC3T3-E1 cells on nanoengineered polystyrene surfaces with nanopillar and nanopore arrays. Biofabrication. 2013;5:1297–307.CrossRefGoogle Scholar
  58. 58.
    Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells ☆. Exp Cell Res. 1998;238:265–72.PubMedCrossRefGoogle Scholar
  59. 59.
    Wu YN, Yang Z, Hui JHP, Ouyang HW, Lee EH. Cartilaginous ECM component-modification of the micro-bead culture system for chondrogenic differentiation of mesenchymal stem cells. Biomaterials. 2007;28:4056–67.PubMedCrossRefGoogle Scholar
  60. 60.
    Varghese S, Hwang NS, Canver AC, Theprungsirikul P, Lin DW, Elisseeff J. Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol. 2008;27:12–21.PubMedCrossRefGoogle Scholar
  61. 61.
    Wu YN, Law JB, He AY, Low HY, Hui JH, Lim CT, Yang Z, Lee EH. Substrate topography determines the fate of chondrogenesis from human mesenchymal stem cells resulting in specific cartilage phenotype formation. Nanomed Nanotechnol Biol Med. 2014;10:1507–16.CrossRefGoogle Scholar
  62. 62.
    Kaivosoja E, Suvanto P, Barreto G, Aura S, Soininen A, Franssila S, Konttinen YT. Cell adhesion and osteogenic differentiation on three-dimensional pillar surfaces †. J Biomed Mater Res A. 2013;101A:842–52.CrossRefGoogle Scholar
  63. 63.
    van den Dolder J, Bancroft GN, Sikavitsas VI, Spauwen PH, Mikos AG, Jansen JA. Effect of fibronectin- and collagen I-coated titanium fiber mesh on proliferation and differentiation of osteogenic cells. Tissue Eng. 2003;9:505–15.PubMedCrossRefGoogle Scholar
  64. 64.
    Park JW, Kim YJ, Chan HP, Lee DH, Ko YG, Jang JH, Chong SL. Enhanced osteoblast response to an equal channel angular pressing-processed pure titanium substrate with microrough surface topography. Acta Biomater. 2009;5:3272–80.PubMedCrossRefGoogle Scholar
  65. 65.
    Guéhennec LL, Soueidan A, Layrolle P, Amouriq Y. Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater. 2007;23:844–54.PubMedCrossRefGoogle Scholar
  66. 66.
    Anselme K, Bigerelle M, Noël B, Iost A, Hardouin P. Effect of grooved titanium substratum on human osteoblastic cell growth. J Biomed Mater Res. 2002;60:529–40.PubMedCrossRefGoogle Scholar
  67. 67.
    Lincks J, Boyan BD, Blanchard CR, Lohmann CH, Liu Y, Cochran DL, Dean DD, Schwartz Z. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials. 1998;19:2219–32.PubMedCrossRefGoogle Scholar
  68. 68.
    Brett PM, Harle J, Salih V, Mihoc R, Olsen I, Jones FH, Tonetti M. Roughness response genes in osteoblasts. Bone. 2004;35:124–33.PubMedCrossRefGoogle Scholar
  69. 69.
    Borsari V, Giavaresi G, Fini M, Torricelli P, Tschon M, Chiesa R, Chiusoli L, Salito A, Volpert A, Giardino R. Comparative in vitro study on a ultra-high roughness and dense titanium coating. Biomaterials. 2005;26:4948–55.PubMedCrossRefGoogle Scholar
  70. 70.
    Guehennec LL, Lopez-Heredia MA, Enkel B, Weiss P, Amouriq Y, Layrolle P. Osteoblastic cell behavior on different titanium implant surfaces. Acta Biomater. 2008;4:535–43.PubMedCrossRefGoogle Scholar
  71. 71.
    Schwartz Z, Olivares-Navarrete R, Wieland M, Cochran DL, Boyan BD. Mechanisms regulating increased production of osteoprotegerin by osteoblasts cultured on microstructured titanium surfaces. Biomaterials. 2009;30:3390–6.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Mandracci P, Mussano F, Rivolo P, Carossa S. Surface treatments and functional coatings for biocompatibility improvement and bacterial adhesion reduction in dental implantology. Coatings. 2016;6:7.CrossRefGoogle Scholar
  73. 73.
    Jäger M, Zilkens C, Zanger K, Krauspe R. Significance of nano- and microtopography for cell-surface interactions in orthopaedic implants. Biomed Res Int. 2007;2007:69036.Google Scholar
  74. 74.
    Stevens MM. Exploring and engineering the cell-surface interface. Science. 2005;310:1135–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Marinucci L, Balloni S, Becchetti E, Belcastro S, Guerra M, Calvitti M, Lilli C, Calvi E, Locci P. Effect of titanium surface roughness on human osteoblast proliferation and gene expression in vitro. Int J Oral Maxillofac Implants. 2006;21:719–25.PubMedGoogle Scholar
  76. 76.
    Qu Z, Andrukhov O, Laky M, Ulm C. Effect of enamel matrix derivative on proliferation and differentiation of osteoblast cells grown on the titanium implant surface. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;111:517–22.PubMedCrossRefGoogle Scholar
  77. 77.
    Arnold JW, Boothe DH, Bailey GW. Parameters of treated stainless steel surfaces important for resistance to bacterial contamination. 2001;44:347–356.Google Scholar
  78. 78.
    Bollen CML, Papaioanno W, Van Eldere J, Schepers E, Quirynen M, Van Steenberghe D. The influence of abutment surface roughness on plaque accumulation and peri-implant mucositis. Clin Oral Implants Res. 1996;7:201–11.PubMedCrossRefGoogle Scholar
  79. 79.
    Harris LG, Richards RG. Staphylococci and implant surfaces: a review. Injury. 2006;37:S3–14.PubMedCrossRefGoogle Scholar
  80. 80.
    Whitehead KA, Verran J. The effect of surface topography on the retention of microorganisms. Food Bioprod Process. 2007;84:253–9.CrossRefGoogle Scholar
  81. 81.
    Wu Y, Zitelli JP, Tenhuisen KS, Yu X, Libera MR. Differential response of Staphylococci and osteoblasts to varying titanium surface roughness. Biomaterials. 2011;32:951–60.PubMedCrossRefGoogle Scholar
  82. 82.
    Liu X, Chu PK, Ding C. Surface modification of titanium, titanium alloys, and related materials for biomedical applications. Mater Sci Eng R Rep. 2004;47:49–121.CrossRefGoogle Scholar
  83. 83.
    Hayakawa T, Kiba H, Yasuda S, Yamamoto H, Nemoto K. A histologic and histomorphometric evaluation of two types of retrieved human titanium implants. Int J Periodontics Restorative Dent. 2002;22:164–71.PubMedGoogle Scholar
  84. 84.
    Valiev RZ, Semenova IP, Latysh VV, Rack H, Lowe TC, Petruzelka J, Dluhos L, Hrusak D, Sochova J. Nanostructured titanium for biomedical applications. Adv Eng Mater. 2008;10:B15–7.CrossRefGoogle Scholar
  85. 85.
    Estrin Y, Kasper C, Diederichs S, Lapovok R. Accelerated growth of preosteoblastic cells on ultrafine grained titanium. J Biomed Mater Res A. 2009;90A:1239–42.CrossRefGoogle Scholar
  86. 86.
    Sader MS, Balduino A, Soares GDA, Borojevic R. Effect of three distinct treatments of titanium surface on osteoblast attachment, proliferation, and differentiation. Clin Oral Implants Res. 2005;16:667–75.PubMedCrossRefGoogle Scholar
  87. 87.
    Yuasa T, Miyamoto Y, Ishikawa K, Takechi M, Momota Y, Tatehara S, Nagayama M. Effects of apatite cements on proliferation and differentiation of human osteoblasts in vitro. Biomaterials. 2004;25:1159–66.PubMedCrossRefGoogle Scholar
  88. 88.
    Junker R, Dimakis A, Thoneick M, Jansen JA. Effects of implant surface coatings and composition on bone integration: a systematic review. Clin Oral Implants Res. 2009;20:185–206.PubMedCrossRefGoogle Scholar
  89. 89.
    Ferraz EP, Sa JC, Oliveira PT, Alves C, Beloti MM, Rosa AL. The effect of plasma-nitrided titanium surfaces on osteoblastic cell adhesion, proliferation, and differentiation. J Biomed Mater Res A. 2014;102:991–8.PubMedCrossRefGoogle Scholar
  90. 90.
    Hayes JS, Czekanska EM, Richards RG. The cell–surface interaction. Adv Biochem Eng Biotechnol. 2012;126:1–31.PubMedGoogle Scholar
  91. 91.
    Wall I, Donos N, Carlqvist K, Jones F, Brett P. Modified titanium surfaces promote accelerated osteogenic differentiation of mesenchymal stromal cells in vitro. Bone. 2009;45:17–26.PubMedCrossRefGoogle Scholar
  92. 92.
    Price RL, Ellison K, Haberstroh KM, Webster TJ. Nanometer surface roughness increases select osteoblast adhesion on carbon nanofiber compacts. J Biomed Mater Res A. 2004;70:129–38.PubMedCrossRefGoogle Scholar
  93. 93.
    Depprich R, Ommerborn M, Zipprich H, Naujoks C, Handschel J, Wiesmann HP, Kübler NR, Meyer U. Behavior of osteoblastic cells cultured on titanium and structured zirconia surfaces. Head Face Med. 2008;4:1–9.CrossRefGoogle Scholar
  94. 94.
    Li Z, Gong Y, Sun S, Du Y, Lü D, Liu X, Long M. Differential regulation of stiffness, topography, and dimension of substrates in rat mesenchymal stem cells. Biomaterials. 2013;34:7616–25.PubMedCrossRefGoogle Scholar
  95. 95.
    Wells RG. The role of matrix stiffness in regulating cell behavior. Hepatology. 2008;47:1394–400.PubMedCrossRefGoogle Scholar
  96. 96.
    Park JS, Chu JS, Tsou AD, Diop R, Tang Z, Wang A, Li S. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β. Biomaterials. 2011;32:3921–30.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Lee J, Abdeen AA, Kilian KA. Rewiring mesenchymal stem cell lineage specification by switching the biophysical microenvironment. Sci Rep. 2014;4:182.Google Scholar
  98. 98.
    Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracellular matrix—cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001;2:793–805.PubMedCrossRefGoogle Scholar
  99. 99.
    Janmey PA, Mcculloch CA. Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng. 2007;9:1–34.PubMedCrossRefGoogle Scholar
  100. 100.
    Chen W, Villadiaz LG, Sun Y, Weng S, Kim JK, Lam RH, Han L, Fan R, Krebsbach PH, Fu J. Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells. ACS Nano. 2012;6:4094–103.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Trappmann B, Gautrot JE, Connelly JT, Strange DG, Li Y, Oyen ML, Cohen Stuart MA, Boehm H, Li B, Vogel V, Spatz JP, Watt FM, Huck WT. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater. 2012;11:642–9.PubMedCrossRefGoogle Scholar
  102. 102.
    Hwang JH, Byun MR, Kim AR, Kim KM, Cho HJ, Lee YH, Kim J, Jeong MG, Hwang ES, Hong JH. Extracellular matrix stiffness regulates osteogenic differentiation through MAPK activation. PLoS One. 2015;10:e0135519.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le DJ, Forcato M, Bicciato S. Role of YAP/TAZ in mechanotransduction. Nature. 2011;474:179–83.PubMedCrossRefGoogle Scholar
  104. 104.
    Pek YS, Wan AJ. The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials. 2010;31:385–91.PubMedCrossRefGoogle Scholar
  105. 105.
    Chen G, Dong C, Yang L, Lv Y. 3D scaffolds with different stiffness but the same microstructure for bone tissue engineering. ACS Appl Mater Interfaces. 2015;7:15790–802.PubMedCrossRefGoogle Scholar
  106. 106.
    US Department of Commerce. Effect of 3D hydrogel scaffold stiffness on human bone marrow stromal cell differentiation. 2010.Google Scholar
  107. 107.
    Breuls RG, Jiya TU, Smit TH. Scaffold stiffness influences cell behavior: opportunities for skeletal tissue engineering. Open Orthop J. 2008;2:103–9.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Dalby MJ, Riehle MO, Johnstone H, Affrossman S, Curtis ASG. Investigating the limits of filopodial sensing: a brief report using SEM to image the interaction between 10 nm high nano-topography and fibroblast filopodia. Cell Biol Int. 2004;28:229–36.PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  • Qi Zhang
    • 1
  • Shiyun Lin
    • 1
  • Qianshun Li
    • 1
  • Dan Zhao
    • 1
  • Xiaoxiao Cai
    • 1
    Email author
  1. 1.State Key Laboratory of Oral DiseasesWest China Hospital of Stomatology, Sichuan UniversityChengduChina

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