Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 619-633 , October 2010

Nanotopographical modification: a regulator of cellular function through focal adhesions

  • Manus Jonathan Paul Biggs, PhD

      Affiliations

    • Nanotechnology Center for Mechanics in Regenerative Medicine, Department of Applied Physics and Applied Mathematics, Columbia University, New York, New York, USA
    • Centre for Cell Engineering, Institute of Biomedical and Life Sciences, Joseph Black Building, University of Glasgow, Glasgow, United Kingdom
    • Corresponding Author InformationCorresponding author: Nanotechnology Center for Mechanics in Regenerative Medicine, Department of Applied Physics and Applied Mathematics, Columbia University, New York, NY 10027, USA.
    • ,
  • R. Geoff Richards, PhD

      Affiliations

    • AO Research Institute, AO Foundation, Davos Platz, Switzerland
    • ,
  • Matthew J. Dalby, PhD

      Affiliations

    • Centre for Cell Engineering, Institute of Biomedical and Life Sciences, Joseph Black Building, University of Glasgow, Glasgow, United Kingdom

Received 6 June 2009 ,Accepted 7 January 2010.

References 

  1. Hench LL, Polak JM. Third-generation biomedical materials. Science. 2002;295:1014–1017
  2. Curtis A. Tutorial on the biology of nanotopography. IEEE Trans Nanobiosci. 2004;3:293–295
  3. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD. Topographical control of cell behaviour. I. Simple step cues. Development. 1987;99:439–448
  4. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD. Cell guidance by ultrafine topography in vitro. J Cell Sci. 1991;99(Pt 1):73–77
  5. Tanaka M, Takayama A, Ito E, Sunami H, Yamamoto S, Shimomura M. Effect of pore size of self-organized honeycomb-patterned polymer films on spreading, focal adhesion, proliferation, and function of endothelial cells. J Nanosci Nanotechnol. 2007;7:763–772
  6. Karuri NW, Liliensiek S, Teixeira AI, Abrams G, Campbell S, Nealey PF, et al. Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells. J Cell Sci. 2004;117:3153–3164
  7. Brody S, Anilkumar T, Liliensiek S, Last JA, Murphy CJ, Pandit A. Characterizing nanoscale topography of the aortic heart valve basement membrane for tissue engineering heart valve scaffold design. Tissue Eng. 2006;12:413–421
  8. Wolter JR, Meyer RF. Sessile macrophages forming clear endothelium-like membrane on inside of successful keratoprosthesis. Trans Am Ophthalmol Soc. 1984;82:187–202
  9. Tabata Y. Recent progress in tissue engineering. Drug Discov Today. 2001;6:483–487
  10. Marwick C. Implant recommendations. JAMA. 2000;283:869
  11. Tabata Y. Tissue regeneration based on tissue engineering technology. Congenit Anom (Kyoto). 2004;44:111–124
  12. Soon-Shiong P, Heintz RE, Merideth N, Yao QX, Yao Z, Zheng T, et al. Insulin independence in a type 1 diabetic patient after encapsulated islet transplantation. Lancet. 1994;343:950–951
  13. Honkanen PB, Kellomaki M, Konttinen YT, Makela S, Lehto MU. A midterm follow-up study of bioreconstructive polylactide scaffold implants in metacarpophalangeal joint arthroplasty in rheumatoid arthritis patients. J Hand Surg Eur Vol. 2009;34:179–185
  14. Darouiche RO. Treatment of infections associated with surgical implants. N Engl J Med. 2004;350:1422–1429
  15. Suska F, Emanuelsson L, Johansson A, Tengvall P, Thomsen P. Fibrous capsule formation around titanium and copper. J Biomed Mater Res A. 2007;85:888–896
  16. Andersson M, Suska F, Johansson A, Berglin M, Emanuelsson L, Elwing H, et al. Effect of molecular mobility of polymeric implants on soft tissue reactions: an in vivo study in rats. J Biomed Mater Res A. 2007;84A:652–660
  17. Baxter LC, Frauchiger V, Textor M, ap Gwynn I, Richards RG. Fibroblast and osteoblast adhesion and morphology on calcium phosphate surfaces. Eur Cell Mater. 2002;4:1–17
  18. Oleschuk RD, McComb ME, Chow A, Ens W, Standing KG, Perreault H, et al. Characterization of plasma proteins adsorbed onto biomaterials. By MALDI-TOFMS. Biomaterials. 2000;21:1701–1710
  19. Suh CW, Kim MY, Choo JB, Kim JK, Kim HK, Lee EK. Analysis of protein adsorption characteristics to nano-pore silica particles by using confocal laser scanning microscopy. J Biotechnol. 2004;112:267–277
  20. Dettin M, Conconi MT, Gambaretto R, Bagno A, Di Bello C, Menti AM, et al. Effect of synthetic peptides on osteoblast adhesion. Biomaterials. 2005;26:4507–4515
  21. Keselowsky BG, Collard DM, Garcia AJ. Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials. 2004;25:5947–5954
  22. Wan Y, Wang Y, Liu Z, Qu X, Han B, Bei J, et al. Adhesion and proliferation of OCT-1 osteoblast-like cells on micro- and nano-scale topography structured poly(l-lactide). Biomaterials. 2005;26:4453–4459
  23. Yamaguchi M, Shinbo T, Kanamori T, Wang PC, Niwa M, Kawakami H, et al. Surface modification of poly(l-lactic acid) affects initial cell attachment, cell morphology, and cell growth. J Artif Organs. 2004;7:187–193
  24. Marchisio M, Di Carmine M, Pagone R, Piattelli A, Miscia S. Implant surface roughness influences osteoclast proliferation and differentiation. J Biomed Mater Res B. Appl Biomater. 2005;75:251–256
  25. Zhao H, Van Humbeeck J, Sohier J, De Scheerder I. Electrochemical polishing of 316L stainless steel slotted tube coronary stents. J Mater Sci Mater Med. 2002;13:911–916
  26. Chen MC, Chang Y, Liu CT, Lai WY, Peng SF, Hung YW, et al. The characteristics and in vivo suppression of neointimal formation with sirolimus-eluting polymeric stents. Biomaterials. 2008;30:79–88
  27. Bertrand OF, Sipehia R, Mongrain R, Rodes J, Tardif JC, Bilodeau L, et al. Biocompatibility aspects of new stent technology. J Am Coll Cardiol. 1998;32:562–571
  28. Leu HJ, Feigl W, Susani M, Odermatt B. Differentiation of mononuclear blood cells into macrophages, fibroblasts and endothelial cells in thrombus organization. Exp Cell Biol. 1988;56:201–210
  29. Schwarz US, Erdmann T, Bischofs IB. Focal adhesions as mechanosensors: the two-spring model. Biosystems. 2006;83:225–232
  30. Triplett JW, Pavalko FM. Disruption of α-actinin-integrin interactions at focal adhesions renders osteoblasts susceptible to apoptosis. Am J Physiol Cell Physiol. 2006;291:C909–921
  31. Zinger O, Anselme K, Denzer A, Habersetzer P, Wieland M, Jeanfils J, et al. Time-dependent morphology and adhesion of osteoblastic cells on titanium model surfaces featuring scale-resolved topography. Biomaterials. 2004;25:2695–2711
  32. Dalby MJ, Riehle MO, Johnstone H, Affrossman S, Curtis AS. 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;28:229–236
  33. Abercrombie M, Heaysman JE, Pegrum SM. The locomotion of fibroblasts in culture. 3. Movements of particles on the dorsal surface of the leading lamella. Exp Cell Res. 1970;62:389–398
  34. Bershadsky AD, Ballestrem C, Carramusa L, Zilberman Y, Gilquin B, Khochbin S, et al. Assembly and mechanosensory function of focal adhesions: experiments and models. Eur J Cell Biol. 2006;85:165–173
  35. Lim JY, Dreiss AD, Zhou Z, Hansen JC, Siedlecki CA, Hengstebeck RW, et al. The regulation of integrin-mediated osteoblast focal adhesion and focal adhesion kinase expression by nanoscale topography. Biomaterials. 2007;28:1787–1797
  36. Cohen M, Joester D, Geiger B, Addadi L. Spatial and temporal sequence of events in cell adhesion: from molecular recognition to focal adhesion assembly. Chembiochem. 2004;5:1393–1399
  37. Garcia AJ. Get a grip: integrins in cell-biomaterial interactions. Biomaterials. 2005;26:7525–7529
  38. Zimerman B, Volberg T, Geiger B. Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil Cytoskeleton. 2004;58:143–159
  39. Burridge K, Fath K, Kelly T, Nuckolls G, Turner C. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu Rev Cell Biol. 1988;4:487–525
  40. Ward MD, Hammer DA. A theoretical analysis for the effect of focal contact formation on cell-substrate attachment strength. Biophys J. 1993;64:936–959
  41. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol. 2001;3:466–472
  42. Besser A, Safran SA. Force-induced adsorption and anisotropic growth of focal adhesions. Biophys J. 2006;90:3469–3484
  43. Takagi J, Petre BM, Walz T, Springer TA. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell. 2002;110:599–611
  44. Norman JJ, Desai TA. Methods for fabrication of nanoscale topography for tissue engineering scaffolds. Ann Biomed Eng. 2006;34:89–101
  45. Wood MA. Colloidal lithography and current fabrication techniques producing in-plane nanotopography for biological applications. J R Soc Interface. 2007;4:1–17
  46. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater. 2007;6:997–1003
  47. Martines E, Seunarine K, Morgan H, Gadegaard N, Wilkinson CD, Riehle MO. Superhydrophobicity and superhydrophilicity of regular nanopatterns. Nano Lett. 2005;5:2097–2103
  48. Andersson AS, Brink J, Lidberg U, Sutherland DS. Influence of systematically varied nanoscale topography on the morphology of epithelial cells. IEEE Trans Nanobiosci. 2003;2:49–57
  49. Dalby MJ, Gadegaard N, Wilkinson CD. The response of fibroblasts to hexagonal nanotopography fabricated by electron beam lithography. J Biomed Mater Res A. 2008;84:973–979
  50. Mack PJ, Kaazempur-Mofrad MR, Karcher H, Lee RT, Kamm RD. Force-induced focal adhesion translocation: effects of force amplitude and frequency. Am J Physiol Cell Physiol. 2004;287:C954–962
  51. Biggs MJ, Richards RG, Gadegaard N, McMurray RJ, Affrossman S, Wilkinson CD, et al. Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. J Biomed Mater Res A. 2009;91:195–208
  52. Curtis AS, Casey B, Gallagher JO, Pasqui D, Wood MA, Wilkinson CD. Substratum nanotopography and the adhesion of biological cells. Are symmetry or regularity of nanotopography important. Biophys Chem. 2001;94:275–283
  53. Sato M, Aslani A, Sambito MA, Kalkhoran NM, Slamovich EB, Webster TJ. Nanocrystalline hydroxyapatite/titania coatings on titanium improves osteoblast adhesion. J Biomed Mater Res A. 2008;84:265–272
  54. Selhuber-Unkel C, Lopez-Garcia M, Kessler H, Spatz JP. Cooperativity in adhesion cluster formation during initial cell adhesion. Biophys J. 2008;95:5424–5431
  55. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol. 2003;200:423–428
  56. Bozec L, Horton MA. Skeletal tissues as nanomaterials. J Mater Sci Mater Med. 2006;17:1043–1048
  57. Tsuprun V, Santi P. Ultrastructure and immunohistochemical identification of the extracellular matrix of the chinchilla cochlea. Hear Res. 1999;129:35–49
  58. Osawa T, Feng XY, Nozaka Y. Scanning electron microscopic observations of the basement membranes with dithiothreitol separation. Med Electron Microsc. 2003;36:132–138
  59. Schvartzman M, Nguyen K, Palma M, Abramson J, Sable J, Hone J, et al. Fabrication of nanoscale bioarrays for the study of cytoskeletal protein binding interactions using nanoimprint lithography. J Vac Sci Technol B Microelectron Nanometer Struct Process Meas Phenom. 2009;27:61–65
  60. Hanarp P, Sutherland D, Gold J, Kasemo B. Nanostructured model biomaterial surfaces prepared by colloidal lithography. Nanostruct Mater. 1999;12:429–432
  61. Affrosman S, Henn G, O' Niell SA, Pethrick RA, Stamm M. Surface topography and composition of deuterated polystyrene-poly(bromostyrene) blends. Macromolecules. 1996;29:5010–5016
  62. Sjostrom T, Dalby MJ, Hart A, Tare R, Oreffo RO, Su B. Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. Acta Biomater. 2009;5:1433–1441
  63. Wilkinson CD. Making structures for cell engineering. Eur Cell Mater. 2004;8:21–26
  64. Milner KR, Siedlecki CA. Submicron poly(l-lactic acid) pillars affect fibroblast adhesion and proliferation. J Biomed Mater Res A. 2007;82:80–91
  65. Lim JY, Hansen JC, Siedlecki CA, Runt J, Donahue HJ. Human foetal osteoblastic cell response to polymer-demixed nanotopographic interfaces. J R Soc Interface. 2005;2:97–108
  66. Lee J, Chu BH, Chen KH, Ren F, Lele TP. Randomly oriented, upright SiO2 coated nanorods for reduced adhesion of mammalian cells. Biomaterials. 2009;30:4488–4493
  67. Dalby MJ, Childs S, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS. Fibroblast reaction to island topography: changes in cytoskeleton and morphology with time. Biomaterials. 2003;24:927–935
  68. Berry CC, Dalby MJ, Oreffo RO, McCloy D, Affrosman S. The interaction of human bone marrow cells with nanotopographical features in three dimensional constructs. J Biomed Mater Res A. 2006;79:431–439
  69. Dalby MJ, Yarwood SJ, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS. Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. Exp Cell Res. 2002;276:1–9
  70. Lim JY, Hansen JC, Siedlecki CA, Hengstebeck RW, Cheng J, Winograd N, et al. Osteoblast adhesion on poly(l-lactic acid)/polystyrene demixed thin film blends: effect of nanotopography, surface chemistry, and wettability. Biomacromolecules. 2005;6:3319–3327
  71. Dalby MJ, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS. Nonadhesive nanotopography: fibroblast response to poly(n-butyl methacrylate)-poly(styrene) demixed surface features. J Biomed Mater Res A. 2003;67:1025–1032
  72. Dulgar-Tulloch AJ, Bizios R, Siegel RW. Human mesenchymal stem cell adhesion and proliferation in response to ceramic chemistry and nanoscale topography. J Biomed Mater Res A. 2008;90:586–594
  73. Gallagher JO, McGhee KF, Wilkinson CD, Riehle MO. Interaction of animal cells with ordered nanotopography. IEEE Trans Nanobiosci. 2002;1:24–28
  74. Heydarkhan-Hagvall S, Choi CH, Dunn J, Heydarkhan S, Schenke-Layland K, MacLellan WR, et al. Influence of systematically varied nano-scale topography on cell morphology and adhesion. Cell Commun Adhes. 2007;14:181–194
  75. Lee J, Kang BS, Hicks B, Chancellor TF, Chu BH, Wang HT, et al. The control of cell adhesion and viability by zinc oxide nanorods. Biomaterials. 2008;29:3743–3749
  76. Kim DH, Kim P, Suh K, Kyu Choi S, Ho Lee S, Kim B. Modulation of adhesion and growth of cardiac myocytes by surface nanotopography. Conf Proc IEEE Eng Med Biol Soc. 2005;4:4091–4094
  77. 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
  78. Liliensiek SJ, Nealey P, Murphy CJ. Characterization of endothelial basement membrane nanotopography in rhesus macaque as a guide for vessel tissue engineering. Tissue Eng Part A. 2009;15:2643–2651
  79. Biggs MJP, Richards RG, Gadegaard N, Wilkinson CDW, Dalby MJ. Regulation of implant surface cell adhesion: characterization and quantification of S-phase primary osteoblast adhesions on biomimetic nanoscale substrates. J Orthop Res. 2007;25:273–282
  80. Biggs MJP, Richards RG, Gadegaard N, Wilkinson CDW, Dalby MJ. The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading. J Mater Sci Mater Med. 2007;18:399–404
  81. Hart A, Gadegaard N, Wilkinson CD, Oreffo RO, Dalby MJ. Osteoprogenitor response to low-adhesion nanotopographies originally fabricated by electron beam lithography. J Mater Sci Mater Med. 2007;18:1211–1218
  82. Dalby MJ, Biggs MJ, Gadegaard N, Kalna G, Wilkinson CD, Curtis AS. Nanotopographical stimulation of mechanotransduction and changes in interphase centromere positioning. J Cell Biochem. 2006;100:326–338
  83. Franz CM, Muller DJ. Analyzing focal adhesion structure by atomic force microscopy. J Cell Sci. 2005;118:5315–5323
  84. Krasteva N, Seifert B, Albrecht W, Weigel T, Schossig M, Altankov G, et al. Influence of polymer membrane porosity on C3A hepatoblastoma cell adhesive interaction and function. Biomaterials. 2004;25:2467–2476
  85. Park J, Bauer S, von der Mark K, Schmuki P. Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett. 2007;7:1686–1691
  86. Zhu B, Zhang Q, Lu Q, Xu Y, Yin J, Hu J, et al. Nanotopographical guidance of C6 glioma cell alignment and oriented growth. Biomaterials. 2004;25:4215–4223
  87. Diehl KA, Foley JD, Nealey PF, Murphy CJ. Nanoscale topography modulates corneal epithelial cell migration. J Biomed Mater Res A. 2005;75:603–611
  88. Dalby MJ, McCloy D, Robertson M, Wilkinson CD, Oreffo RO. Osteoprogenitor response to defined topographies with nanoscale depths. Biomaterials. 2006;27:1306–1315
  89. Zhu B, Lu Q, Yin J, Hu J, Wang Z. Alignment of osteoblast-like cells and cell-produced collagen matrix induced by nanogrooves. Tissue Eng. 2005;11:825–834
  90. Kannus P. Structure of the tendon connective tissue. Scand J Med Sci Sports. 2000;10:312–320
  91. Dalby MJ, Riehle MO, Yarwood SJ, Wilkinson CD, Curtis AS. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res. 2003;284:274–282
  92. Lenhert S, Meier MB, Meyer U, Chi L, Wiesmann HP. Osteoblast alignment, elongation and migration on grooved polystyrene surfaces patterned by Langmuir-Blodgett lithography. Biomaterials. 2005;26:563–570
  93. Yim EK, Pang SW, Leong KW. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res. 2007;313:1820–1829
  94. Chou L, Firth JD, Uitto VJ, Brunette DM. Substratum surface topography alters cell shape and regulates fibronectin mRNA level, mRNA stability, secretion and assembly in human fibroblasts. J Cell Sci. 1995;108(Pt 4):1563–1573
  95. Dalby MJ, Hart A, Yarwood SJ. The effect of the RACK1 signalling protein on the regulation of cell adhesion and cell contact guidance on nanometric grooves. Biomaterials. 2008;29:282–289
  96. Jin CY, Zhu BS, Wang XF, Lu QH, Chen WT, Zhou XJ. Nanoscale surface topography enhances cell adhesion and gene expression of Madin Darby canine kidney cells. J Mater Sci Mater Med. 2008;19:2215–2222
  97. Teixeira AI, Nealey PF, Murphy CJ. Responses of human keratocytes to micro- and nanostructured substrates. J Biomed Mater Res A. 2004;71:369–376
  98. den Braber ET, de Ruijter JE, Ginsel LA, von Recum AF, Jansen JA. Orientation of ECM protein deposition, fibroblast cytoskeleton, and attachment complex components on silicone microgrooved surfaces. J Biomed Mater Res. 1998;40:291–300
  99. Fujita S, Ohshima M, Iwata H. Time-lapse observation of cell alignment on nanogrooved patterns. J R Soc Interface. 2009;6(Suppl 3):S269–S277
  100. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD. Topographical control of cell behaviour: II. Multiple grooved substrata. Development. 1990;108:635–644
  101. Loesberg WA, te Riet J, van Delft FC, Schon P, Figdor CG, Speller S, et al. The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion. Biomaterials. 2007;28:3944–3951
  102. Crouch AS, Miller D, Luebke KJ, Hu W. Correlation of anisotropic cell behaviors with topographic aspect ratio. Biomaterials. 2009;30:1560–1567
  103. Teixeira AI, Abrams GA, Bertics PJ, Murphy CJ, Nealey PF. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci. 2003;116:1881–1892
  104. Matsuzaka K, Walboomers F, de Ruijter A, Jansen JA. Effect of microgrooved poly-l-lactic (PLA) surfaces on proliferation, cytoskeletal organization, and mineralized matrix formation of rat bone marrow cells. Clin Oral Implants Res. 2000;11:325–333
  105. Teixeira AI, McKie GA, Foley JD, Bertics PJ, Nealey PF, Murphy CJ. The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials. 2006;27:3945–3954
  106. Biggs M, Richards G, Dalby M. The use of nanoscale topography to modulate the dynamics of adhesion formation in primary osteoblasts and ERK/MAPK signalling in STRO-1+ enriched skeletal stem cells. Biomaterials. 2009;30:5094–5103
  107. Biela SA, Su Y, Spatz JP, Kemkemer R. Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater. 2009;5:2460–2466
  108. Pavalko FM, Norvell SM, Burr DB, Turner CH, Duncan RL, Bidwell JP. A model for mechanotransduction in bone cells: the load-bearing mechanosomes. J Cell Biochem. 2003;88:104–112
  109. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB. Parsons JT. pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci U S A. 1992;89:5192–5196
  110. Kurenova E, Xu LH, Yang X, Baldwin AS, Craven RJ, Hanks SK, et al. Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol Cell Biol. 2004;24:4361–4371
  111. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY. Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol. 1996;134:793–799
  112. Saleem S, Li J, Yee SP, Fellows GF, Goodyer CG, Wang R. β1 integrin/FAK/ERK signalling pathway is essential for human fetal islet cell differentiation and survival. J Pathol. 2009;219:182–192
  113. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110:673–687
  114. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem. 2000;275:9645–9652
  115. Klees RF, Salasznyk RM, Kingsley K, Williams WA, Boskey A, Plopper GE. Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway. Mol Biol Cell. 2005;16:881–890
  116. Ge C, Xiao G, Jiang D, Franceschi RT. Critical role of the extracellular signal-regulated kinase-MAPK pathway in osteoblast differentiation and skeletal development. J Cell Biol. 2007;176:709–718
  117. Salasznyk RM, Klees RF, Williams WA, Boskey A, Plopper GE. Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp Cell Res. 2007;313:22–37
  118. Kim JY, Khang D, Lee JE, Webster TJ. Decreased macrophage density on carbon nanotube patterns on polycarbonate urethane. J Biomed Mater Res A. 2009;88:419–426
  119. Jakobsen SS, Larsen A, Stoltenberg M, Bruun JM, Soballe K. Hydroxyapatite coatings did not increase TGF-β and BMP-2 secretion in murine J774A.1 macrophages, but induced a pro-inflammatory cytokine response. J Biomater Sci Polym Ed. 2009;20:455–465
  120. Wojciak-Stothard B, Curtis A, Monaghan W, MacDonald K, Wilkinson C. Guidance and activation of murine macrophages by nanometric scale topography. Exp Cell Res. 1996;223:426–435
  121. Whitney GS, Chan PY, Blake J, Cosand WL, Neubauer MG, Aruffo A, et al. Human T and B lymphocytes express a structurally conserved focal adhesion kinase, pp125FAK. DNA Cell Biol. 1993;12:823–830
  122. Torres AJ, Vasudevan L, Holowka D, Baird BA. Focal adhesion proteins connect IgE receptors to the cytoskeleton as revealed by micropatterned ligand arrays. Proc Natl Acad Sci U S A. 2008;105:17238–17244
  123. Hocde SA, Hyrien O, Waugh RE. Cell adhesion molecule distribution relative to neutrophil surface topography assessed by TIRFM. Biophys J. 2009;97:379–387
  124. Bhattacharyya SP, Mekori YA, Hoh D, Paolini R, Metcalfe DD, Bianchine PJ. Both adhesion to immobilized vitronectin and FcɛRI cross-linking cause enhanced focal adhesion kinase phosphorylation in murine mast cells. Immunology. 1999;98:357–362
  125. Kasorn A, Alcaide P, Jia Y, Subramanian KK, Sarraj B, Li Y, et al. Focal adhesion kinase regulates pathogen-killing capability and life span of neutrophils via mediating both adhesion-dependent and -independent cellular signals. J Immunol. 2009;183:1032–1043
  126. Cohen-Hillel E, Mintz R, Meshel T, Garty BZ, Ben-Baruch A. Cell migration to the chemokine CXCL8: paxillin is activated and regulates adhesion and cell motility. Cell Mol Life Sci. 2009;66:884–899
  127. Zhu J, Wang YS, Zhang J, Zhao W, Yang XM, Li X, et al. Focal adhesion kinase signaling pathway participates in the formation of choroidal neovascularization and regulates the proliferation and migration of choroidal microvascular endothelial cells by acting through HIF-1 and VEGF expression in RPE cells. Exp Eye Res. 2009;88:910–918
  128. Sheta EA, Harding MA, Conaway MR, Theodorescu D. Focal adhesion kinase, Rap1, and transcriptional induction of vascular endothelial growth factor. J Natl Cancer Inst. 2000;92:1065–1073
  129. Pezzatini S, Morbidelli L, Solito R, Paccagnini E, Boanini E, Bigi A, et al. Nanostructured HA crystals up-regulate FGF-2 expression and activity in microvascular endothelium promoting angiogenesis. Bone. 2007;41:523–534
  130. Hood JD, Frausto R, Kiosses WB, Schwartz MA, Cheresh DA. Differential αv integrin-mediated Ras-ERK signaling during two pathways of angiogenesis. J Cell Biol. 2003;162:933–943
  131. Blaschke F, Stawowy P, Kappert K, Goetze S, Kintscher U, Wollert-Wulf B, et al. Angiotensin II-augmented migration of VSMCs towards PDGF-BB involves Pyk2 and ERK 1/2 activation. Basic Res Cardiol. 2002;97:334–342
  132. Tanaka K, Abe M, Sato Y. Roles of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in the signal transduction of basic fibroblast growth factor in endothelial cells during angiogenesis. Jpn J Cancer Res. 1999;90:647–654
  133. Dalby MJ, Marshall GE, Johnstone HJ, Affrossman S, Riehle MO. Interactions of human blood and tissue cell types with 95-nm-high nanotopography. IEEE Trans Nanobiosci. 2002;1:18–23
  134. Park J, Bauer S, Schlegel KA, Neukam FW, von der Mark K, Schmuki P. TiO2 nanotube surfaces: 15 nm--an optimal length scale of surface topography for cell adhesion and differentiation. Small. 2009;5:666–671
  135. Karuri NW, Porri TJ, Albrecht RM, Murphy CJ, Nealey PF. Nano- and microscale holes modulate cell-substrate adhesion, cytoskeletal organization, and -beta1 integrin localization in SV40 human corneal epithelial cells. IEEE Trans Nanobioscience. 2006;5:273–280
  136. Hajicharalambous CS, Lichter J, Hix WT, Swierczewska M, Rubner MF, Rajagopalan P. Nano- and sub-micron porous polyelectrolyte multilayer assemblies: biomimetic surfaces for human corneal epithelial cells. Biomaterials. 2009;30:4029–4036
  137. Curtis ASG, Gadegaard N, Dalby MJ, Riehle MO, Wilkinson CDW, Aitchison G. Cells react to nanoscale order and symmetry in their surroundings. IEEE Trans Nanobioscience. 2004;3:61–65
  138. Biggs MJ, Richards RG, McFarlane S, Wilkinson CD, Oreffo RO, Dalby MJ. Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330nm deep microgrooves. J R Soc Interface. 2008;5:1231–1242
  139. Lu J, Rao MP, MacDonald NC, Khang D, Webster TJ. Improved endothelial cell adhesion and proliferation on patterned titanium surfaces with rationally designed, micrometer to nanometer features. Acta Biomater. 2008;4:192–201

 This work was funded by the AO Research Fund, Switzerland (grant no. 04-D81) and The U.S. National Institutes of Health, Nanomedicine Roadmap Initiative (grant no. PN2EY016586). M.J.D. is supported by the Biology and Biological Sciences Research Council.

PII: S1549-9634(10)00016-X

doi: 10.1016/j.nano.2010.01.009

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 619-633 , October 2010

Article Tools

* Image Usage & Resolution