Cell and Tissue Research

, 339:131 | Cite as

Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix

  • Klaus von der MarkEmail author
  • Jung Park
  • Sebastian Bauer
  • Patrik Schmuki


The ultimate goal in the design of biomimetic materials for use in tissue engineering as permanent or resorbable tissue implants is to generate biocompatible scaffolds with appropriate biomechanical and chemical properties to allow the adhesion, ingrowth, and survival of cells. Recent efforts have therefore focused on the construction and modification of biomimetic surfaces targeted to support tissue-specific cell functions including adhesion, growth, differentiation, motility, and the expression of tissue-specific genes. Four decades of extensive research on the structure and biological influence of the extracellular matrix (ECM) on cell behavior and cell fate have shown that three types of information from the ECM are relevant for the design of biomimetic surfaces: (1) physical properties (elasticity, stiffness, resilience of the cellular environment), (2) specific chemical signals from peptide epitopes contained in a wide variety of extracelluar matrix molecules, and (3) the nanoscale topography of microenvironmental adhesive sites. Initial physical and chemical approaches aimed at improving the adhesiveness of biomaterial surfaces by sandblasting, particle coating, or etching have been supplemented by attempts to increase the bioactivity of biomaterials by coating them with ECM macromolecules, such as fibronectin, elastin, laminin, and collagens, or their integrin-binding epitopes including RGD, YIGSR, and GFOGER. Recently, the development of new nanotechnologies such as photo- or electron-beam nanolithography, polymer demixing, nano-imprinting, compression molding, or the generation of TiO2 nanotubes of defined diameters (15–200 nm), has opened up the possibility of constructing biomimetic surfaces with a defined nanopattern, eliciting tissue-specific cellular responses by stimulating integrin clustering. This development has provided new input into the design of novel biomaterials. The new technologies allowing the construction of a geometrically defined microenvironment for cells at the nanoscale should facilitate the investigation of nanotopography-dependent mechanisms of integrin-mediated cell signaling.


Extracellular matrix Biomimetic materials Tissue engineering Nanotechnology Nanotopography 


  1. Akiyama SK, Yamada KM (1987) Fibronectin. Adv Enzymol Relat Areas Mol Biol 59:1–57PubMedGoogle Scholar
  2. Al-Munajjed AA, Plunkett NA, Gleeson JP, Weber T, Jungreuthmayer C, Levingstone T, Hammer J, O'Brien FJ (2009) Development of a biomimetic collagen-hydroxyapatite scaffold for bone tissue engineering using a SBF immersion technique. J Biomed Mater Res B Appl Biomater 90:584–591PubMedGoogle Scholar
  3. Andreiotelli M, Kohal RJ (2009) Fracture strength of zirconia implants after artificial aging. Clin Implant Dent Relat Res 11:158–166PubMedGoogle Scholar
  4. Arnaout MA, Goodman SL, Xiong JP (2002) Integrin structure: new twists and turns in dynamic cell adhesion. Immunol Rev 186:125–140PubMedGoogle Scholar
  5. Arnaout MA, Mahalingam B, Xiong JP (2005) Integrin structure, allostery, and bidirectional signaling. Annu Rev Cell Dev Biol 21:381–410PubMedGoogle Scholar
  6. Arnaout MA, Goodman SL, Xiong JP (2007) Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 19:495–507PubMedGoogle Scholar
  7. Arnold M, Cavalcanti-Adam EA, Glass R, Blummel J, Eck W, Kantlehner M, Kessler H, Spatz JP (2004) Activation of integrin function by nanopatterned adhesive interfaces. Chemphyschem 5:383–388PubMedGoogle Scholar
  8. Arnold M, Hirschfeld-Warneken VC, Lohmuller T, Heil P, Blummel J, Cavalcanti-Adam EA, Lopez-Garcia M, Walther P, Kessler H, Geiger B, et al (2008) Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett 8:2063–2069PubMedGoogle Scholar
  9. Aumailley M, Timpl R, Sonnenberg A (1990) Antibody to integrin alpha6 subunit specifically inhibits cell- binding to laminin fragment 8. Exp Cell Res 188:55–60PubMedGoogle Scholar
  10. Ayad S, Boot-Handford RP, Humpries MJ, Kadler KE, Shuttleworth CA (1998) The extracellular matrix factsbook, 2nd edn. Academic Press, LondonGoogle Scholar
  11. Babensee JE, McIntire LV, Mikos AG (2000) Growth factor delivery for tissue engineering. Pharm Res 17:497–504PubMedGoogle Scholar
  12. Bard JBL, Hay ED (1975) The behavior of fibroblasts from the developing avian cornea. Morphology and movement in situ and in vitro. J Cell Biol 67:400–418PubMedGoogle Scholar
  13. Bauer S, Kleber S, Schmuki P (2006) Tailoring the geometry in H3PO4/HF electrolytes. Electrochem Commun 8:1321–1325Google Scholar
  14. Bax DV, Rodgers UR, Bilek MM, Weiss AS (2009) Cell adhesion to tropoelastin is mediated via the C-terminal GRKRK motif and integrin alphaVbeta3. J Biol Chem 284:28616–28623PubMedGoogle Scholar
  15. Becker U, Fietzek PP, Furthmayr H, Timpl R (1975) Non-helical sequences of rabbit collagen. Correlation with antigenic determinants detected by rabbit antibodies in homologous regions of rat and calf collagen. Eur J Biochem 54:359–366PubMedGoogle Scholar
  16. Belyanskaya L, Weigel S, Hirsch C, Tobler U, Krug HF, Wick P (2009) Effects of carbon nanotubes on primary neurons and glial cells. Neurotoxicology 30:702–711PubMedGoogle Scholar
  17. Biggs MJ, Richards RG, Gadegaard N, Wilkinson CD, Dalby MJ (2007) The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading. J Mater Sci Mater Med 18:399–404PubMedGoogle Scholar
  18. Binder PS, Rock ME, Schmidt KC, Anderson JA (1991) High-voltage electron microscopy of normal human cornea. Invest Ophthalmol Vis Sci 32:2234–43PubMedGoogle Scholar
  19. Birk DE, Trelstad RL (1986) Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J Cell Biol 103:231–240PubMedGoogle Scholar
  20. Bornstein P (2001) Thrombospondins as matricellular modulators of cell function. J Clin Invest 107:929–934PubMedGoogle Scholar
  21. Brammer KS, Oh S, Gallagher JO, Jin S (2008) Enhanced cellular mobility guided by TiO2 nanotube surfaces. Nano Lett 8:786–793PubMedGoogle Scholar
  22. Brandley BK, Schnaar RL (1988) Covalent attachment of an Arg-Gly-Asp sequence peptide to derivatizable polyacrylamide surfaces: support of fibroblast adhesion and long-term growth. Anal Biochem 172:270–278PubMedGoogle Scholar
  23. Brinckmann J, Notbohm H, Müller P (2005) Collagen—primer in structure, processing and assembly. Springer, BerlinGoogle Scholar
  24. Burgeson RE (1988) New collagens, new concepts. Annu Rev Cell Biol 4:551–577PubMedGoogle Scholar
  25. Burridge K, Chrzanowska-Wodnicka M (1996) Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12:463–518PubMedGoogle Scholar
  26. Camper L, Hellman U, Lundgren-Akerlund E (1998) Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem 273:20383–20389PubMedGoogle Scholar
  27. Cavalcanti-Adam EA, Tomakidi P, Bezler M, Spatz JP (2005) Geometric organization of the extracellular matrix in the control of integrin-mediated adhesion and cell function in osteoblasts. Prog Orthod 6:232–237PubMedGoogle Scholar
  28. Cavalcanti-Adam EA, Micoulet A, Blummel J, Auernheimer J, Kessler H, Spatz JP (2006) Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly. Eur J Cell Biol 85:219–224PubMedGoogle Scholar
  29. Cavalcanti-Adam EA, Volberg T, Micoulet A, Kessler H, Geiger B, Spatz JP (2007) Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys J 92:2964–2974PubMedGoogle Scholar
  30. Cavalcanti-Adam EA, Aydin D, Hirschfeld-Warneken VC, Spatz JP (2008) Cell adhesion and response to synthetic nanopatterned environments by steering receptor clustering and spatial location. HFSP J 2:276–285PubMedGoogle Scholar
  31. Cen L, Liu W, Cui L, Zhang W, Cao Y (2008) Collagen tissue engineering: development of novel biomaterials and applications. Pediatr Res 63:492–496PubMedGoogle Scholar
  32. Chajra H, Rousseau CF, Cortial D, Ronziere MC, Herbage D, Mallein-Gerin F, Freyria AM (2008) Collagen-based biomaterials and cartilage engineering. Application to osteochondral defects. Biomed Mater Eng 18 (1 Suppl):S33–S45PubMedGoogle Scholar
  33. Chambard M, Gabrion J, Mauchamp J (1981) Influence of collagen gel on the orientation of epithelial cell polarity: follicle formation from isolated thyroid cells and from preformed monolayers. J Cell Biol 91:157–166PubMedGoogle Scholar
  34. Cheng S, Craig WS, Mullen D, Tschopp JF, Dixon D, Pierschbacher MD (1994) Design and synthesis of novel cyclic RGD-containing peptides as highly potent and selective integrin alpha IIb beta 3 antagonists. J Med Chem 37:1–8PubMedGoogle Scholar
  35. Chesnutt BM, Yuan Y, Buddington K, Haggard WO, Bumgardner JD (2009) Composite chitosan/nano-hydroxyapatite scaffolds induce osteocalcin production by osteoblasts in vitro and support bone formation in vivo. Tissue Eng Part A 15:2571–2579PubMedGoogle Scholar
  36. Chiquet-Ehrismann R (2004) Tenascins. Int J Biochem Cell Biol 36:986–990PubMedGoogle Scholar
  37. Chong EJ, Phan TT, Lim IJ, Zhang YZ, Bay BH, Ramakrishna S, Lim CT (2007) Evaluation of electrospun PCL/gelatin nanofibrous scaffold for wound healing and layered dermal reconstitution. Acta Biomater 3:321–330PubMedGoogle Scholar
  38. Choudhary S, Berhe M, Haberstroh KM, Webster TJ (2006) Increased endothelial and vascular smooth muscle cell adhesion on nanostructured titanium and CoCrMo. Int J Nanomedicine 1:41–49PubMedGoogle Scholar
  39. Chung S, Moghe AK, Montero GA, Kim SH, King MW (2009) Nanofibrous scaffolds electrospun from elastomeric biodegradable poly(L-lactide-co-epsilon-caprolactone) copolymer. Biomed Mater 4:15019PubMedGoogle Scholar
  40. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213–234PubMedGoogle Scholar
  41. Conner KA, Sabatini R, Mealey BL, Takacs VJ, Mills MP, Cochran DL (2003) Guided bone regeneration around titanium plasma-sprayed, acid-etched, and hydroxyapatite-coated implants in the canine model. J Periodontol 74:658–668PubMedGoogle Scholar
  42. Cook AD, Hrkach JS, Gao NN, Johnson IM, Pajvani UB, Cannizzaro SM, Langer R (1997) Characterization and development of RGD-peptide-modified poly(lactic acid-co-lysine) as an interactive, resorbable biomaterial. J Biomed Mater Res 35:513–523PubMedGoogle Scholar
  43. Couchman JR (2003) Syndecans: proteoglycan regulators of cell-surface microdomains? Nat Rev Mol Cell Biol 4:926–937PubMedGoogle Scholar
  44. Cukierman E, Pankov R, Yamada KM (2002) Cell interactions with three-dimensional matrices. Curr Opin Cell Biol 14:633–639PubMedGoogle Scholar
  45. Cunningham LW (ed) (1987) Structural and contractile proteins. Part D: Extracellular matrix. Academic Press, LondonGoogle Scholar
  46. Curtis AS, Dalby MJ, Gadegaard N (2006) Nanoprinting onto cells. J R Soc Interface 3:393–398PubMedGoogle Scholar
  47. Dailey L, Laplantine E, Priore R, Basilico C (2003) A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol 161:1053–1066PubMedGoogle Scholar
  48. Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis AS (2004) Use of nanotopography to study mechanotransduction in fibroblasts–methods and perspectives. Eur J Cell Biol 83:159–169PubMedGoogle Scholar
  49. Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis AS (2005) Morphological and microarray analysis of human fibroblasts cultured on nanocolumns produced by colloidal lithography. Eur Cell Mater 9:1–8PubMedGoogle Scholar
  50. Dalby MJ, McCloy D, Robertson M, Agheli H, Sutherland D, Affrossman S, Oreffo RO (2006) Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27:2980–2987PubMedGoogle Scholar
  51. Dalby MJ, Gadegaard N, Curtis AS, Oreffo RO (2007a) Nanotopographical control of human osteoprogenitor differentiation. Curr Stem Cell Res Ther 2:129–138PubMedGoogle Scholar
  52. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CD, Oreffo RO (2007b) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6:997–1003PubMedGoogle Scholar
  53. Davies JE (1996) In vitro modeling of the bone/implant interface. Anat Rec 245:426–445PubMedGoogle Scholar
  54. Den Dunnen WF, Van der Lei B, Schakenraad JM, Blaauw EH, Stokroos I, Pennings AJ, Robinson PH (1993) Long-term evaluation of nerve regeneration in a biodegradable nerve guide. Microsurgery 14:508–515Google Scholar
  55. Doi M, Thyboll J, Kortesmaa J, Jansson K, Iivanainen A, Parvardeh M, Timpl R, Hedin U, Swedenborg J, Tryggvason K (2002) Recombinant human laminin-10 (alpha5beta1gamma1). Production, purification, and migration-promoting activity on vascular endothelial cells. J Biol Chem 277:12741–12748PubMedGoogle Scholar
  56. Eble JA (2001) The molecular basis of integrin-extracellular matrix interactions. Osteoarthritis Cartilage 9(Suppl A):S131–S140PubMedGoogle Scholar
  57. Ekaputra AK, Zhou Y, Cool S, Hutmacher DW (2009) Composite electrospun scaffolds for engineering tubular bone grafts. Tissue Eng Part A (in press)Google Scholar
  58. Elias KL, Price RL, Webster TJ (2002) Enhanced functions of osteoblasts on nanometer diameter carbon fibers. Biomaterials 23:3279–3287PubMedGoogle Scholar
  59. Elsdale T, Bard J (1972) Collagen substrate for studies on cell behavior. J Cell Biol 54:626–637PubMedGoogle Scholar
  60. Emerich DF, Thanos CG (2007) Targeted nanoparticle-based drug delivery and diagnosis. J Drug Target 15:163–183PubMedGoogle Scholar
  61. Emsley J, Knight CG, Farndale RW, Barnes MJ (2004) Structure of the integrin alpha2beta1-binding collagen peptide. J Mol Biol 335:1019–1028PubMedGoogle Scholar
  62. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689PubMedGoogle Scholar
  63. Engler AJ, Sweeney HL, Discher DE, Schwarzbauer JE (2007) Extracellular matrix elasticity directs stem cell differentiation. J Musculoskelet Neuronal Interact 7:335PubMedGoogle Scholar
  64. Ergun C, Liu H, Webster TJ (2009) Osteoblast adhesion on novel machinable calcium phosphate/lanthanum phosphate composites for orthopedic applications. J Biomed Mater Res A 89:727–733PubMedGoogle Scholar
  65. Fratzl P (2008) Collagen: structure and mechanics. Springer, BerlinGoogle Scholar
  66. Friedl P, Zanker KS, Brocker EB (1998) Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc Res Tech 43:369–378PubMedGoogle Scholar
  67. Fuerer C, Habib SJ, Nusse R (2009) A study on the interactions between heparan sulfate proteoglycans and Wnt proteins. Dev Dyn (in press)Google Scholar
  68. Fujihara K, Huang ZM, Ramakrishna S, Satknanantham K, Hamada H (2004) Feasibility of knitted carbon/PEEK composites for orthopedic bone plates. Biomaterials 25:3877–3885PubMedGoogle Scholar
  69. Gahmberg CG, Tolvanen M, Kotovuori P (1997) Leukocyte adhesion–structure and function of human leukocyte beta2-integrins and their cellular ligands. Eur J Biochem 245:215–232PubMedGoogle Scholar
  70. Geiger B, Spatz JP, Bershadsky AD (2009) Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 10:21–33PubMedGoogle Scholar
  71. Ghicov A, Albu SP, Macak JM, Schmuki P (2008) High-contrast electrochromic switching using transparent lift-off layers of self-organized TiO2 nanotubes. Small 4:1063–1066PubMedGoogle Scholar
  72. Giancotti FG (2003) A structural view of integrin activation and signaling. Dev Cell 4:149–151PubMedGoogle Scholar
  73. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028–1032PubMedGoogle Scholar
  74. Glowacki J, Mizuno S (2008) Collagen scaffolds for tissue engineering. Biopolymers 89:338–344PubMedGoogle Scholar
  75. Goodman SL, Risse G, Mark K von der (1989) The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix. J Cell Biol 109:799–809PubMedGoogle Scholar
  76. Goodman SB, Gomez Barrena E, Takagi M, Konttinen YT (2009) Biocompatibility of total joint replacements: a review. J Biomed Mater Res A 90:603–618PubMedGoogle Scholar
  77. Graf J, Ogle RC, Robey FA, Sasaki M, Martin GR, Yamada Y, Kleinman HK (1987) A pentapeptide from the laminin-B1 chain mediates cell-adhesion and binds the 67000-laminin receptor. Biochemistry 26:6896–6900PubMedGoogle Scholar
  78. Grant DS, Tashiro K-I, Segui-Real B, Yamada Y, Martin GR, Kleinman HK (1989) Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell 58:933–943PubMedGoogle Scholar
  79. Grashoff C, Aszodi A, Sakai T, Hunziker EB, Fassler R (2003) Integrin-linked kinase regulates chondrocyte shape and proliferation. EMBO Rep 4:432–438PubMedGoogle Scholar
  80. Guo W, Giancotti FG (2004) Integrin signalling during tumour progression. Nat Rev Mol Cell Biol 5:816–826PubMedGoogle Scholar
  81. Habraken WJ, Wolke JG, Jansen JA (2007) Ceramic composites as matrices and scaffolds for drug delivery in tissue engineering. Adv Drug Deliv Rev 59:234–248PubMedGoogle Scholar
  82. Hafemann B, Ensslen S, Erdmann C, Niedballa R, Zuhlke A, Ghofrani K, Kirkpatrick CJ (1999) Use of a collagen/elastin-membrane for the tissue engineering of dermis. Burns 25:373–384PubMedGoogle Scholar
  83. Hall HG, Farson DA, Bissell MJ (1982) Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture. Proc Natl Acad Sci USA 79:4672–4676PubMedGoogle Scholar
  84. Hanawa T, Kamiura Y, Yamamoto S, Kohgo T, Amemiya A, Ukai H, Murakami K, Asaoka K (1997) Early bone formation around calcium-ion-implanted titanium inserted into rat tibia. J Biomed Mater Res 36:131–136PubMedGoogle Scholar
  85. Hardingham T, Bayliss M (1990) Proteoglycans of articular cartilage: changes in aging and in joint disease. Semin Arthritis Rheum 20 (3 Suppl 1):12–33PubMedGoogle Scholar
  86. Harris AK, Stopak D, Wild P (1981) Fibroblast traction as a mechanism for collagen morphogenesis. Nature 290:249–251PubMedGoogle Scholar
  87. Hattori K, Tomita N, Tamai S, Ikada Y (2000) Bioabsorbable thread for tight tying of bones. J Orthop Sci 5:57–63PubMedGoogle Scholar
  88. Hausser H, Groning A, Hasilik A, Schonherr E, Kresse H (1994) Selective inactivity of TGF-beta/decorin complexes. FEBS Lett 353:243–245PubMedGoogle Scholar
  89. Hay ED (1983) Cell and extracellular matrix: their organization and mutual dependence. Mod Cell Biol 2:509–548Google Scholar
  90. Hedbom E, Heinegard D (1993) Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J Biol Chem 268:27307–27312PubMedGoogle Scholar
  91. Heinegard D, Sommarin Y (1987) Proteoglycans: an overview. Methods Enzymol 144:305–319PubMedGoogle Scholar
  92. Heinl P, Muller L, Korner C, Singer RF, Muller FA (2008) Cellular Ti-6Al-4V structures with interconnected macro porosity for bone implants fabricated by selective electron beam melting. Acta Biomater 4:1536–1544PubMedGoogle Scholar
  93. Hirschfeld-Warneken VC, Arnold M, Cavalcanti-Adam A, Lopez-Garcia M, Kessler H, Spatz JP (2008) Cell adhesion and polarisation on molecularly defined spacing gradient surfaces of cyclic RGDfK peptide patches. Eur J Cell Biol 87:743–750PubMedGoogle Scholar
  94. Hocking AM, Shinomura T, McQuillan DJ (1998) Leucine-rich repeat glycoproteins of the extracellular matrix. Matrix Biol 17:1–19PubMedGoogle Scholar
  95. Hsiong SX, Boontheekul T, Huebsch N, Mooney DJ (2009) Cyclic arginine-glycine-aspartate peptides enhance three-dimensional stem cell osteogenic differentiation. Tissue Eng Part A 15:263–272PubMedGoogle Scholar
  96. Hu J, Liu X, Ma PX (2008) Induction of osteoblast differentiation phenotype on poly(L-lactic acid) nanofibrous matrix. Biomaterials 29:3815–3821PubMedGoogle Scholar
  97. Hubbell JA, Massia SP, Desai NP, Drumheller PD (1991) Endothelial cell-selective materials for tissue engineering in the vascular graft via a new receptor. Biotechnology (N Y) 9:568–572Google Scholar
  98. Hubmacher D, Tiedemann K, Reinhardt DP (2006) Fibrillins: from biogenesis of microfibrils to signaling functions. Curr Top Dev Biol 75:93–123PubMedGoogle Scholar
  99. Humphries MJ, Akiyama SK, Komoriya A, Olden K, Yamada KM (1986) Identification of an alternatively spliced site in human plasma fibronectin that mediates cell type-specific adhesion. J Cell Biol 103:2637–2647PubMedGoogle Scholar
  100. Humphries MJ, Obara M, Olden K, Yamada KM (1989) Role of fibronectin in adhesion, migration, and metastasis. Cancer Invest 7:373–393PubMedGoogle Scholar
  101. Humphries MJ, McEwan PA, Barton SJ, Buckley PA, Bella J, Mould AP (2003) Integrin structure: heady advances in ligand binding, but activation still makes the knees wobble. Trends Biochem Sci 28:313–320PubMedGoogle Scholar
  102. Humphries JD, Byron A, Humphries MJ (2006) Integrin ligands at a glance. J Cell Sci 119:3901–3903PubMedGoogle Scholar
  103. Hunziker EB, Wagner J, Studer D (1996) Vitrified articular cartilage reveals novel ultra-structural features respecting extracellular matrix architecture. Histochem Cell Biol 106:375–382PubMedGoogle Scholar
  104. Huo F, Zheng Z, Zheng G, Giam LR, Zhang H, Mirkin CA (2008) Polymer pen lithography. Science 321:1658–1660PubMedGoogle Scholar
  105. Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11–25PubMedGoogle Scholar
  106. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609–652PubMedGoogle Scholar
  107. Iozzo RV (2005) Basement membrane proteoglycans: from cellar to ceiling. Nat Rev Mol Cell Biol 6:646–656PubMedGoogle Scholar
  108. Isacke CM, Yarwood H (2002) The hyaluronan receptor, CD44. Int J Biochem Cell Biol 34:718–721PubMedGoogle Scholar
  109. Jalali S, Pozo MA del, Chen K, Miao H, Li Y, Schwartz MA, Shyy JY, Chien S (2001) Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc Natl Acad Sci USA 98:1042–1046PubMedGoogle Scholar
  110. Jokinen J, Dadu E, Nykvist P, Kapyla J, White DJ, Ivaska J, Vehvilainen P, Reunanen H, Larjava H, Hakkinen L, et al (2004) Integrin-mediated cell adhesion to type I collagen fibrils. J Biol Chem 279:31956–31963PubMedGoogle Scholar
  111. Kariya Y, Ishida K, Tsubota Y, Nakashima Y, Hirosaki T, Ogawa T, Miyazaki K (2002) Efficient expression system of human recombinant laminin-5. J Biochem 132:607–612PubMedGoogle Scholar
  112. Karlinsey RL, Yi K, Duhn CW (2006) Nucleation and growth of apatite by a self-assembled polycrystalline bioceramic. Bioinspir Biomim 1:12–19PubMedGoogle Scholar
  113. Kay S, Thapa A, Haberstroh KM, Webster TJ (2002) Nanostructured polymer/nanophase ceramic composites enhance osteoblast and chondrocyte adhesion. Tissue Eng 8:753–761PubMedGoogle Scholar
  114. Keeney M, Collin E, Pandit A (2009) Multi-channelled collagen-calcium phosphate scaffolds: their physical properties and human cell response. Tissue Eng Part C Methods 15:265–273PubMedGoogle Scholar
  115. Keselowsky BG, Collard DM, Garcia AJ (2003) Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion. J Biomed Mater Res A 66:247–259PubMedGoogle Scholar
  116. Keselowsky BG, Collard DM, Garcia AJ (2005) Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation. Proc Natl Acad Sci USA 102:5953–5957PubMedGoogle Scholar
  117. Khakbaznejad A, Chehroudi B, Brunette DM (2004) Effects of titanium-coated micromachined grooved substrata on orienting layers of osteoblast-like cells and collagen fibers in culture. J Biomed Mater Res A 70:206–218PubMedGoogle Scholar
  118. Khang D, Sato M, Price RL, Ribbe AE, Webster TJ (2006) Selective adhesion and mineral deposition by osteoblasts on carbon nanofiber patterns. Int J Nanomed 1:65–72Google Scholar
  119. Khang D, Carpenter J, Chun YW, Pareta R, Webster TJ (2008) Nanotechnology for regenerative medicine. Biomed Microdevices 19:19Google Scholar
  120. Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71:357–370PubMedGoogle Scholar
  121. Kielty CM (2006) Elastic fibres in health and disease. Expert Rev Mol Med 8:1–23PubMedGoogle Scholar
  122. Kielty CM, Grant ME (2002) The collagen family: structure, assembly, and organisation in the extracellular matrix. In: Royce PM, Steinmann B (eds) Connective tisssue and its heritable disorders. Wiley-Liss, New York, pp 159–221Google Scholar
  123. Kielty CM, Sherratt MJ, Marson A, Baldock C (2005) Fibrillin microfibrils. Adv Protein Chem 70:405–436PubMedGoogle Scholar
  124. Kim HW, Kang W, Jeon E, Jang JH (2009) Construction and expression of a recombinant fibronectin(III)10 protein for integrin-mediated cell adhesion. Biotechnol Lett (in press)Google Scholar
  125. King SR, Hickerson WL, Proctor KG (1991) Beneficial actions of exogenous hyaluronic acid on wound healing. Surgery 109:76–84PubMedGoogle Scholar
  126. Knabe C, Berger G, Gildenhaar R, Klar F, Zreiqat H (2004) The modulation of osteogenesis in vitro by calcium titanium phosphate coatings. Biomaterials 25:4911–4919PubMedGoogle Scholar
  127. Knight CG, Morton LF, Onley DJ, Peachey AR, Messent AJ, Smethurst PA, Tuckwell DS, Farndale RW, Barnes MJ (1998) Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. J Biol Chem 273:33287–33294PubMedGoogle Scholar
  128. Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ (2000) The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35–40PubMedGoogle Scholar
  129. Knudson CB, Knudson W (2004) Hyaluronan and CD44: modulators of chondrocyte metabolism. Clin Orthop Relat Res 427 (Suppl):S152-S162PubMedGoogle Scholar
  130. Kortesmaa J, Yurchenco P, Tryggvason K (2000) Recombinant laminin-8 (alpha(4)beta(1)gamma(1)). Production, purification, and interactions with integrins. J Biol Chem 275:14853–14859PubMedGoogle Scholar
  131. Koziel L, Kunath M, Kelly OG, Vortkamp A (2004) Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev Cell 6:801–813PubMedGoogle Scholar
  132. Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107:1589–1598PubMedGoogle Scholar
  133. Kühn K (1986) The collagen family—variations in the molecular and supramolecular structure. In: Kühn K, Krieg T (eds) Rheumatology, vol 10. Connective tissue: biological and clinical aspects. Karger, Basel, pp 29–69Google Scholar
  134. Kumagai H, Tajima M, Ueno Y, Giga-Hama Y, Ohba M (1991) Effect of cyclic RGD peptide on cell adhesion and tumor metastasis. Biochem Biophys Res Commun 177:74–82PubMedGoogle Scholar
  135. Kuo SC, Lauffenburger DA (1993) Relationship between receptor/ligand binding affinity and adhesion strength. Biophys J 65:2191–2200PubMedGoogle Scholar
  136. Kwan APL, Cummings CE, Chapman JA, Grant ME (1991) Macromolecular organization of chicken type X collagen in vitro. J Cell Biol 114:597–605PubMedGoogle Scholar
  137. Kyriakides TR, Bornstein P (2003) Matricellular proteins as modulators of wound healing and the foreign body response. Thromb Haemost 90:986–992PubMedGoogle Scholar
  138. Langholz O, Rockel D, Mauch C, Kozlowska E, Bank I, Krieg T, Eckes B (1995) Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by alpha 1 beta 1 and alpha 2 beta 1 integrins. J Cell Biol 131:1903–1915PubMedGoogle Scholar
  139. Larsen M, Artym VV, Green JA, Yamada KM (2006) The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol 18:463–471PubMedGoogle Scholar
  140. Larsson S (2006) Cement augmentation in fracture treatment. Scand J Surg 95:111–118PubMedGoogle Scholar
  141. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359–369PubMedGoogle Scholar
  142. Laurent TC, Fraser JR (1992) Hyaluronan. FASEB J 6:2397–2404PubMedGoogle Scholar
  143. Leahy DJ, Aukhil I, Erickson HP (1996) 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell 84:155–164PubMedGoogle Scholar
  144. LeBaron RG, Athanasiou KA (2000) Extracellular matrix cell adhesion peptides: functional applications in orthopedic materials. Tissue Eng 6:85–103PubMedGoogle Scholar
  145. Lee EY, Lee WH, Kaetzel CS, Parry G, Bissell MJ (1985) Interaction of mouse mammary epithelial cells with collagen substrata: regulation of caseni gene expression and secretion. Proc Natl Acad Sci USA 82:1419–1423PubMedGoogle Scholar
  146. Lee SW, OB, Sanedrin RG, Salaita K, Fujigaya T, Mirkin CA (2006) Biologically active protein nanoarrays generated using parallel dip-pen nanolithography. Adv Mater 18:1133–1136Google Scholar
  147. Lee KY, Jeong L, Kang YO, Lee SJ, Park WH (2009) Electrospinning of polysaccharides for regenerative medicine. Adv Drug Deliv Rev 61:1020–1032PubMedGoogle Scholar
  148. Legate KR, Wickstrom SA, Fassler R (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23:397–418PubMedGoogle Scholar
  149. Lehnert D, Wehrle-Haller B, David C, Weiland U, Ballestrem C, Imhof BA, Bastmeyer M (2004) Cell behaviour on micropatterned substrata: limits of extracellular matrix geometry for spreading and adhesion. J Cell Sci 117:41–52PubMedGoogle Scholar
  150. Li M, Mondrinos MJ, Gandhi MR, Ko FK, Weiss AS, Lelkes PI (2005a) Electrospun protein fibers as matrices for tissue engineering. Biomaterials 26:5999–6008PubMedGoogle Scholar
  151. Li WJ, Tuli R, Okafor C, Derfoul A, Danielson KG, Hall DJ, Tuan RS (2005b) A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 26:599–609PubMedGoogle Scholar
  152. Li M, Mondrinos MJ, Chen X, Gandhi MR, Ko FK, Lelkes PI (2006) Co-electrospun poly(lactide-co-glycolide), gelatin, and elastin blends for tissue engineering scaffolds. J Biomed Mater Res A 79:963–973PubMedGoogle Scholar
  153. Li J, Ding M, Fu Q, Tan H, Xie X, Zhong Y (2008) A novel strategy to graft RGD peptide on biomaterials surfaces for endothelization of small-diamater vascular grafts and tissue engineering blood vessel. J Mater Sci Mater Med 19:2595–2603PubMedGoogle Scholar
  154. Liao E, Yaszemski M, Krebsbach P, Hollister S (2007) Tissue-engineered cartilage constructs using composite hyaluronic acid/collagen I hydrogels and designed poly(propylene fumarate) scaffolds. Tissue Eng 13:537–550PubMedGoogle Scholar
  155. Lin CH, Su JM, Hsu SH (2008) Evaluation of type II collagen scaffolds reinforced by poly(epsilon-caprolactone) as tissue-engineered trachea. Tissue Eng Part C Methods 14:69–77PubMedGoogle Scholar
  156. Lind M, Larsen A (2008) Equal cartilage repair response between autologous chondrocytes in a collagen scaffold and minced cartilage under a collagen scaffold: an in vivo study in goats. Connect Tissue Res 49:437–442PubMedGoogle Scholar
  157. Liu C, Han Z, Czernuszka JT (2009a) Gradient collagen/nanohydroxyapatite composite scaffold: development and characterization. Acta Biomater 5:661–669PubMedGoogle Scholar
  158. Liu J, Yue Z, Fong H (2009b) Continuous nanoscale carbon fibers with superior mechanical strength. Small 5:536–542PubMedGoogle Scholar
  159. Lu J, Rao MP, MacDonald NC, Khang D, Webster TJ (2008) Improved endothelial cell adhesion and proliferation on patterned titanium surfaces with rationally designed, micrometer to nanometer features. Acta Biomater 4:192–201PubMedGoogle Scholar
  160. Ma PX (2008) Biomimetic materials for tissue engineering. Adv Drug Deliv Rev 60:184–198PubMedGoogle Scholar
  161. Macak JM, Tsuchiya H, Schmuki P (2005) High-aspect-ratio TiO2 nanotubes by anodization of titanium. Angew Chem Int Ed Engl 44:2100–2102PubMedGoogle Scholar
  162. Macak JM, Zlamal M, Krysa J, Schmuki P (2007) Self-organized TiO2 nanotube layers as highly efficient photocatalysts. Small 3:300–304PubMedGoogle Scholar
  163. Maheshwari G, Brown G, Lauffenburger DA, Wells A, Griffith LG (2000) Cell adhesion and motility depend on nanoscale RGD clustering. J Cell Sci 113:1677–1686PubMedGoogle Scholar
  164. Malicev E, Radosavljevic D, Velikonja NK (2007) Fibrin gel improved the spatial uniformity and phenotype of human chondrocytes seeded on collagen scaffolds. Biotechnol Bioeng 96:364–370PubMedGoogle Scholar
  165. Massia SP, Hubbell JA (1991) An RGD spacing of 440 nm is sufficient for integrin alpha V beta 3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation. J Cell Biol 114:1089–1100PubMedGoogle Scholar
  166. Massia SP, Rao SS, Hubbell JA (1993) Covalently immobilized laminin peptide Tyr-Ile-Gly-Ser-Arg (YIGSR) supports cell spreading and co-localization of the 67-kilodalton laminin receptor with alpha-actinin and vinculin. J Biol Chem 268:8053–8059PubMedGoogle Scholar
  167. Mauch C, Adelmann-Grill B, Hatamochi A, Krieg T (1989) Collagenase gene expression in fibroblasts is regulated by a three-dimensional contact with collagen. FEBS Lett 250:301–305PubMedGoogle Scholar
  168. Miller DC, Haberstroh KM, Webster TJ (2005) Mechanism(s) of increased vascular cell adhesion on nanostructured poly(lactic-co-glycolic acid) films. J Biomed Mater Res A 73:476–484PubMedGoogle Scholar
  169. Millward-Sadler SJ, Salter DM (2004) Integrin-dependent signal cascades in chondrocyte mechanotransduction. Ann Biomed Eng 32:435–446PubMedGoogle Scholar
  170. Miner JH, Yurchenco PD (2004) Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20:255–284PubMedGoogle Scholar
  171. Mithieux SM, Rasko JE, Weiss AS (2004) Synthetic elastin hydrogels derived from massive elastic assemblies of self-organized human protein monomers. Biomaterials 25:4921–4927PubMedGoogle Scholar
  172. Mohri H, Hashimoto Y, Ohba M, Kumagai H, Ohkubo T (1991) Novel effect of cyclicization of the Arg-Gly-Asp-containing peptide on vitronectin binding to platelets. Am J Hematol 37:14–19PubMedGoogle Scholar
  173. Montesano R, Orci L, Vassalli P (1983) In vitro rapid organization of endothelial cells into capillary-like networks is promoted by collagen matrices. J Cell Biol 97:1648–1652PubMedGoogle Scholar
  174. Morris NP, Keene DR, Horton WA (2002) Morphology and chemical composition of connective tissue: cartilage. In: Royce PM, Steinmann B (eds) Connective tissue and its heritable disorders. Wiley-Liss, New York, pp 41–66Google Scholar
  175. Muller LJ, Pels E, Schurmans LR, Vrensen GF (2004) A new three-dimensional model of the organization of proteoglycans and collagen fibrils in the human corneal stroma. Exp Eye Res 78:493–501PubMedGoogle Scholar
  176. Muller FA, Muller L, Hofmann I, Greil P, Wenzel MM, Staudenmaier R (2006) Cellulose-based scaffold materials for cartilage tissue engineering. Biomaterials 27:3955–3963PubMedGoogle Scholar
  177. Nomizu M, Yamamura K, Kleinman HK, Yamada Y, Grant DS, Kinsella JL, Fridman R, Auerbach R, Piasecki BA, Zain M (1993) Multimeric forms of Tyr-Ile-Gly-Ser-Arg (YIGSR) peptide enhance the inhibition of tumor growth and metastasis. Cancer Res 53:3459–3461PubMedGoogle Scholar
  178. Oh IH, Nomura N, Chiba A, Murayama Y, Masahashi N, Lee BT, Hanada S (2005) Microstructures and bond strengths of plasma-sprayed hydroxyapatite coatings on porous titanium substrates. J Mater Sci Mater Med 16:635–640PubMedGoogle Scholar
  179. Oh S, Daraio C, Chen LH, Pisanic TR, Finones RR, Jin S (2006) Significantly accelerated osteoblast cell growth on aligned TiO2 nanotubes. J Biomed Mater Res A 78:97–103PubMedGoogle Scholar
  180. Oldberg A, Antonsson P, Hedbom E, Heinegard D (1990) Structure and function of extracellular matrix proteoglycans. Biochem Soc Trans 18:789–792PubMedGoogle Scholar
  181. Oliveira PT de, Nanci A (2004) Nanotexturing of titanium-based surfaces upregulates expression of bone sialoprotein and osteopontin by cultured osteogenic cells. Biomaterials 25:403–413PubMedGoogle Scholar
  182. Olsen D, Yang C, Bodo M, Chang R, Leigh S, Baez J, Carmichael D, Perala M, Hamalainen ER, Jarvinen M, et al (2003) Recombinant collagen and gelatin for drug delivery. Adv Drug Deliv Rev 55:1547–1567PubMedGoogle Scholar
  183. Pacifici M, Shimo T, Gentili C, Kirsch T, Freeman TA, Enomoto-Iwamoto M, Iwamoto M, Koyama E (2005) Syndecan-3: a cell-surface heparan sulfate proteoglycan important for chondrocyte proliferation and function during limb skeletogenesis. J Bone Miner Metab 23:191–199PubMedGoogle Scholar
  184. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385:537–540PubMedGoogle Scholar
  185. Park SN, Lee HJ, Lee KH, Suh H (2003) Biological characterization of EDC-crosslinked collagen-hyaluronic acid matrix in dermal tissue restoration. Biomaterials 24:1631–1641PubMedGoogle Scholar
  186. Park J, Bauer S, Mark K von der, Schmuki P (2007) Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett 7:1686–1691PubMedGoogle Scholar
  187. Park J, Bauer S, Schlegel KA, Neukam FW, Mark K von der, Schmuki P (2009a) TiO2 nanotube surfaces: 15 nm—an optimal length scale of surface topography for cell adhesion and differentiation. Small 5:666–671PubMedGoogle Scholar
  188. Park J, Bauer S, Schmuki P, Mark K von der (2009b) Narrow window in nanoscale dependent activation of endothelial cell growth and differentiation on TiO2 nanotube surfaces. Nano Lett 9:3157–3164PubMedGoogle Scholar
  189. Peng L, Eltgroth ML, LaTempa TJ, Grimes CA, Desai TA (2009) The effect of TiO2 nanotubes on endothelial function and smooth muscle proliferation. Biomaterials 30:1268–1272PubMedGoogle Scholar
  190. Pfaff M, Tangemann K, Muller B, Gurrath M, Muller G, Kessler H, Timpl R, Engel J (1994) Selective recognition of cyclic RGD peptides of NMR defined conformation by alpha IIb beta 3, alpha V beta 3, and alpha 5 beta 1 integrins. J Biol Chem 269:20233–20238PubMedGoogle Scholar
  191. Ponader S, Vairaktaris E, Heinl P, Wilmowsky CV, Rottmair A, Korner C, Singer RF, Holst S, Schlegel KA, Neukam FW, et al (2008) Effects of topographical surface modifications of electron beam melted Ti-6Al-4 V titanium on human fetal osteoblasts. J Biomed Mater Res A 84:1111–1119PubMedGoogle Scholar
  192. Popat KC, Chatvanichkul KI, Barnes GL, Latempa TJ Jr, Grimes CA, Desai TA (2006) Osteogenic differentiation of marrow stromal cells cultured on nanoporous alumina surfaces. J Biomed Mater Res A 80:955–964Google Scholar
  193. Popat KC, Leoni L, Grimes CA, Desai TA (2007) Influence of engineered titania nanotubular surfaces on bone cells. Biomaterials 28:3188–3197PubMedGoogle Scholar
  194. Popova SN, Barczyk M, Tiger CF, Beertsen W, Zigrino P, Aszodi A, Miosge N, Forsberg E, Gullberg D (2007) Alpha11 beta1 integrin-dependent regulation of periodontal ligament function in the erupting mouse incisor. Mol Cell Biol 27:4306–4316PubMedGoogle Scholar
  195. Price RL, Ellison K, Haberstroh KM, Webster TJ (2004) Nanometer surface roughness increases select osteoblast adhesion on carbon nanofiber compacts. J Biomed Mater Res A 70:129–138PubMedGoogle Scholar
  196. Pytela R, Pierschbacher MD, Ruoslahti E (1985) Identification and isolation of a 140-kD cell-surface glycoprotein with properties expected of a fibronectin receptor. Cell 40:191–198PubMedGoogle Scholar
  197. Pytela R, Pierschbacher MD, Argraves S, Suzuki S, Ruoslahti E (1987) Arginine-glycine-aspartic acid adhesion receptors. Methods Enzymol 144:475–489PubMedGoogle Scholar
  198. Raja PM, Connolley J, Ganesan GP, Ci L, Ajayan PM, Nalamasu O, Thompson DM (2007) Impact of carbon nanotube exposure, dosage and aggregation on smooth muscle cells. Toxicol Lett 169:51–63PubMedGoogle Scholar
  199. Ranieri JP, Bellamkonda R, Bekos EJ, Vargo TG, Gardella JA Jr, Aebischer P (1995) Neuronal cell attachment to fluorinated ethylene propylene films with covalently immobilized laminin oligopeptides YIGSR and IKVAV. II. J Biomed Mater Res 29:779–785PubMedGoogle Scholar
  200. Rapraeger AC (2001) Molecular interactions of syndecans during development. Semin Cell Dev Biol 12:107–116PubMedGoogle Scholar
  201. Responte DJ, Natoli RM, Athanasiou KA (2007) Collagens of articular cartilage: structure, function, and importance in tissue engineering. Crit Rev Biomed Eng 35:363–411PubMedGoogle Scholar
  202. Reyes CD, Garcia AJ (2004) Alpha2beta1 integrin-specific collagen-mimetic surfaces supporting osteoblastic differentiation. J Biomed Mater Res 69A:591–600Google Scholar
  203. Rezania A, Healy KE (2000) The effect of peptide surface density on mineralization of a matrix deposited by osteogenic cells. J Biomed Mater Res 52:595–600PubMedGoogle Scholar
  204. Richardson TP, Murphy WL, Mooney DJ (2001) Polymeric delivery of proteins and plasmid DNA for tissue engineering and gene therapy. Crit Rev Eukaryot Gene Expr 11:47–58PubMedGoogle Scholar
  205. Rnjak J, Li Z, Maitz PK, Wise SG, Weiss AS (2009) Primary human dermal fibroblast interactions with open weave three-dimensional scaffolds prepared from synthetic human elastin. Biomaterials 30:6469–6477PubMedGoogle Scholar
  206. Robinson PS, Huang TF, Kazam E, Iozzo RV, Birk DE, Soslowsky LJ (2005) Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J Biomech Eng 127:181–185PubMedGoogle Scholar
  207. Rotter N, Bucheler M, Haisch A, Wollenberg B, Lang S (2007) Cartilage tissue engineering using resorbable scaffolds. J Tissue Eng Regen Med 1:411–416PubMedGoogle Scholar
  208. Royce PM, Steinmann B (2002) Connective tissue and its heritable sisorders. Wiley Liss, New YorkGoogle Scholar
  209. Ruggiero F, Koch M (2008) Making recombinant extracellular matrix proteins. Methods 45:75–85PubMedGoogle Scholar
  210. Ruoslahti E, Pierschbacher MD (1987) New perspectives in cell adhesion: RGD and integrins. Science 238:491–497PubMedGoogle Scholar
  211. Ruszczak Z, Schwartz RA (1999) Collagen uses in dermatology—an update. Dermatology 199:285–289PubMedGoogle Scholar
  212. Ryan G, Pandit A, Apatsidis DP (2006) Fabrication methods of porous metals for use in orthopaedic applications. Biomaterials 27:2651–2670PubMedGoogle Scholar
  213. Salter DM, Robb JE, Wright MO (1997) Electrophysiological responses of human bone cells to mechanical stimulation: evidence for specific integrin function in mechanotransduction. J Bone Miner Res 12:1133–1141PubMedGoogle Scholar
  214. Sargeant TD, Rao MS, Koh CY, Stupp SI (2008) Covalent functionalization of NiTi surfaces with bioactive peptide amphiphile nanofibers. Biomaterials 29:1085–1098PubMedGoogle Scholar
  215. Sasaki T, Timpl R (2001) Domain IVa of laminin alpha5 chain is cell-adhesive and binds beta1 and alphaVbeta3 integrins through Arg-Gly-Asp. FEBS Lett 509:181–185PubMedGoogle Scholar
  216. Sato M, Aslani A, Sambito MA, Kalkhoran NM, Slamovich EB, Webster TJ (2008) Nanocrystalline hydroxyapatite/titania coatings on titanium improves osteoblast adhesion. J Biomed Mater Res A 84:265–272PubMedGoogle Scholar
  217. Schaefer L, Iozzo RV (2008) Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J Biol Chem 283:21305–21309PubMedGoogle Scholar
  218. Schenk RK, Buser D (1998) Osseointegration: a reality. Periodontology 2000:22–35Google Scholar
  219. Schenk RKHW, Felix R (2002) Morphology and chemical compoition of connective tissue: bone. In: Royce PM, Steinmann B (eds) Connective tisssue and its heritable disorders. Wiley-Liss, New York, pp 67–120Google Scholar
  220. Schmidt RC, Healy KE (2009) Controlling biological interfaces on the nanometer length scale. J Biomed Mater Res A 90:1252–1261PubMedGoogle Scholar
  221. Schwartz MA, DeSimone DW (2008) Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 20:551–556PubMedGoogle Scholar
  222. Schwartz Z, Nasazky E, Boyan BD (2005) Surface microtopography regulates osteointegration: the role of implant surface microtopography in osteointegration. Alpha Omegan 98:9–19PubMedGoogle Scholar
  223. Senior RM, Griffin GL, Mecham RP (1980) Chemotactic activity of elastin-derived peptides. J Clin Invest 66:859–862PubMedGoogle Scholar
  224. Shapiro HS, Chen J, Wrana JL, Zhang Q, Blum M, Sodek J (1993) Characterization of porcine bone sialoprotein: primary structure and cellular expression. Matrix 13:431–440PubMedGoogle Scholar
  225. Shin H, Jo S, Mikos AG (2003) Biomimetic materials for tissue engineering. Biomaterials 24:4353–4364PubMedGoogle Scholar
  226. Silva GA (2009) Nanomedicine: shorting neurons with nanotubes. Nat Nanotechnol 4:82–83PubMedGoogle Scholar
  227. Simionescu DT, Lu Q, Song Y, Lee JS, Rosenbalm TN, Kelley C, Vyavahare NR (2006) Biocompatibility and remodeling potential of pure arterial elastin and collagen scaffolds. Biomaterials 27:702–713PubMedGoogle Scholar
  228. Singh R, Lillard JW Jr (2009) Nanoparticle-based targeted drug delivery. Exp Mol Pathol 86:215–223PubMedGoogle Scholar
  229. Spadaccio C, Rainer A, Trombetta M, Vadala G, Chello M, Covino E, Denaro V, Toyoda Y, Genovese JA (2009) Poly-L-lactic acid/hydroxyapatite electrospun nanocomposites induce chondrogenic differentiation of human MSC. Ann Biomed Eng 37:1376–1389PubMedGoogle Scholar
  230. Spatz JP (2004) Cell-nanostructure interactions. In: Niemeyer CM, Mirkin CA (eds) Nanobiotechnology. Wiley-VCH, Weinheim, pp 53–65Google Scholar
  231. Stark HJ, Baur M, Breitkreutz D, Mirancea N, Fusenig NE (1999) Organotypic keratinocyte cocultures in defined medium with regular epidermal morphogenesis and differentiation. J Invest Dermatol 112:681–691PubMedGoogle Scholar
  232. Staunton D, Millard CJ, Aricescu AR, Campbell ID (2009) Preparation of recombinant fibronectin fragments for functional and structural studies. Methods Mol Biol 522:73–99PubMedGoogle Scholar
  233. Stevens MM, George JH (2005) Exploring and engineering the cell surface interface. Science 310:1135–1138PubMedGoogle Scholar
  234. Still J, Glat P, Silverstein P, Griswold J, Mozingo D (2003) The use of a collagen sponge/living cell composite material to treat donor sites in burn patients. Burns 29:837–841PubMedGoogle Scholar
  235. Stoddart MJ, Grad S, Eglin D, Alini M (2009) Cells and biomaterials in cartilage tissue engineering. Regen Med 4:81–98PubMedGoogle Scholar
  236. Streuli CH, Bissell MJ (1990) Expression of extracellular matrix components is regulated by substratum. J Cell Biol 110:1405–1415PubMedGoogle Scholar
  237. Sun X, Skorstengaard K, Mosher DF (1992) Disulfides modulate RGD-inhibitable cell adhesive activity of thrombospondin. J Cell Biol 118:693–701PubMedGoogle Scholar
  238. Svensson L, Aszodi A, Reinholt FP, Fassler R, Heinegard D, Oldberg A (1999) Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem 274:9636–9647PubMedGoogle Scholar
  239. Takagi M, Santavirta S, Ida H, Ishii M, Takei I, Niissalo S, Ogino T, Konttinen YT (2001) High-turnover periprosthetic bone remodeling and immature bone formation around loose cemented total hip joints. J Bone Miner Res 16:79–88PubMedGoogle Scholar
  240. Takagi J, Petre BM, Walz T, Springer TA (2002) Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110:599–611PubMedGoogle Scholar
  241. Tang S, Spector M (2007) Incorporation of hyaluronic acid into collagen scaffolds for the control of chondrocyte-mediated contraction and chondrogenesis. Biomed Mater 2:S135–S141PubMedGoogle Scholar
  242. Tashiro K, Sephel GC, Weeks B, Sasaki M, Martin GR, Kleinman HK, Yamada Y (1989) A synthetic peptide containing the IKVAV sequence from the A chain of laminin mediates cell attachment, migration, and neurite outgrowth. J Biol Chem 264:16174–16182PubMedGoogle Scholar
  243. Tashiro K, Sephel GC, Greatorex D, Sasaki M, Shirashi N, Martin GR, Kleinman HK, Yamada Y (1991) The RGD containing site of the mouse laminin A chain is active for cell attachment, spreading, migration and neurite outgrowth. J Cell Physiol 146:451–459PubMedGoogle Scholar
  244. Thomas CH, McFarland CD, Jenkins ML, Rezania A, Steele JG, Healy KE (1997) The role of vitronectin in the attachment and spatial distribution of bone-derived cells on materials with patterned surface chemistry. J Biomed Mater Res 37:81–93PubMedGoogle Scholar
  245. Tiitu V, Pulkkinen HJ, Valonen P, Kiviranta O, Kiekara T, Kiviranta I, Lammi MJ (2008) Recombinant human collagens as scaffold materials for chondrocyte cultures. Biomed Mater Eng 18:225–229PubMedGoogle Scholar
  246. Timpl R, Brown J (1994) The laminins (minireview). Matrix Biol 14:275–281PubMedGoogle Scholar
  247. Tortelli F, Cancedda R (2009) Three-dimensional cultures of osteogenic and chondrogenic cells: a tissue engineering approach to mimic bone and cartilage in vitro. Eur Cell Mater 17:1–14PubMedGoogle Scholar
  248. Tryggvason K (1993) The laminin family. Curr Biol 5:877–882Google Scholar
  249. Tsuchiya H, Macak JM, Sieber I, Schmuki P (2005) Self-organized high-aspect-ratio nanoporous zirconium oxides prepared by electrochemical anodization. Small 1:722–725PubMedGoogle Scholar
  250. Tulla M, Pentikainen OT, Viitasalo T, Kapyla J, Impola U, Nykvist P, Nissinen L, Johnson MS, Heino J (2001) Selective binding of collagen subtypes by integrin alpha 1I, alpha 2I, and alpha 10I domains. J Biol Chem 276:48206–48212PubMedGoogle Scholar
  251. Underwood PA, Bennett FA (1989) A comparison of the biological activities of the cell-adhesive proteins vitronectin and fibronectin. J Cell Sci 93:641–649PubMedGoogle Scholar
  252. Varghese OK, Mor GK, Grimes CA, Paulose M, Mukherjee N (2004) A titania nanotube-array room-temperature sensor for selective detection of hydrogen at low concentrations. J Nanosci Nanotechnol 4:733–737PubMedGoogle Scholar
  253. Vigny M, Ollier-Hartmann MP, Lavigne M, Fayein N, Jeanny JC, Laurent M, Courtois Y (1988) Specific binding of basic fibroblast growth factor to basement membrane-like structures and to purified heparan sulfate proteoglycan of the EHS tumor. J Cell Physiol 137:321–328PubMedGoogle Scholar
  254. Vogel WF, Abdulhussein R, Ford CE (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18:1108–1116PubMedGoogle Scholar
  255. Volpi N, Schiller J, Stern R, Soltes L (2009) Role, metabolism, chemical modifications and applications of hyaluronan. Curr Med Chem 16:1718–1745PubMedGoogle Scholar
  256. von der Mark K, Sorokin L (2002) Adhesive glycoproteins. In: Royce PM, Steinmann B (eds) Connective tissue and its heritable disorders. Wiley-Liss, New York, pp 293–328Google Scholar
  257. von der Mark H, Williams I, Wendler O, Sorokin L, von der Mark K, Poschl E (2002) Alternative splice variants of alpha 7 beta 1 integrin selectively recognize different laminin isoforms. J Biol Chem 277:6012–6016PubMedGoogle Scholar
  258. von der Mark H, Poschl E, Lanig H, Sasaki T, Deutzman R, von der Mark K (2007) Distinct acidic clusters and hydrophobic residues in the alternative splice domains X1 and X2 of alpha7 integrins define specificity for laminin isoforms. J Mol Biol 371:1188–1203PubMedGoogle Scholar
  259. Wagener R, Ehlen HW, Ko YP, Kobbe B, Mann HH, Sengle G, Paulsson M (2005) The matrilins–adaptor proteins in the extracellular matrix. FEBS Lett 579:3323–3329PubMedGoogle Scholar
  260. Wang HB, Mullins ME, Cregg JM, Hurtado A, Oudega M, Trombley MT, Gilbert RJ (2009) Creation of highly aligned electrospun poly-L-lactic acid fibers for nerve regeneration applications. J Neural Eng 6:016001PubMedGoogle Scholar
  261. Ward BC, Webster TJ (2006) The effect of nanotopography on calcium and phosphorus deposition on metallic materials in vitro. Biomaterials 27:3064–3074PubMedGoogle Scholar
  262. Webster TJ, Ahn ES (2007) Nanostructured biomaterials for tissue engineering bone. Adv Biochem Eng Biotechnol 103:275–308PubMedGoogle Scholar
  263. Whitaker MJ, Quirk RA, Howdle SM, Shakesheff KM (2001) Growth factor release from tissue engineering scaffolds. J Pharm Pharmacol 53:1427–1437PubMedGoogle Scholar
  264. Wilson K, Stuart SJ, Garcia A, Latour RA Jr (2004) A molecular modeling study of the effect of surface chemistry on the adsorption of a fibronectin fragment spanning the 7–10th type III repeats. J Biomed Mater Res 15:686–698Google Scholar
  265. Xiong JP, Stehle T, Zhang R, Joachimiak A, Frech M, Goodman SL, Arnaout MA (2002) Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 296:151–155PubMedGoogle Scholar
  266. Xiong JY, Li YC, Wang XJ, Hodgson PD, Wen CE (2008) Titanium-nickel shape memory alloy foams for bone tissue engineering. J Mech Behav Biomed Mater 1:269–273PubMedGoogle Scholar
  267. Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610PubMedGoogle Scholar
  268. Yao C, Webster TJ (2006) Anodization: a promising nano-modification technique of titanium implants for orthopedic applications. J Nanosci Nanotechnol 6:2682–2692PubMedGoogle Scholar
  269. Yao C, Slamovich EB, Webster TJ (2008) Enhanced osteoblast functions on anodized titanium with nanotube-like structures. J Biomed Mater Res A 85:157–166PubMedGoogle Scholar
  270. Yeo IS, Oh JE, Jeong L, Lee TS, Lee SJ, Park WH, Min BM (2008) Collagen-based biomimetic nanofibrous scaffolds: preparation and characterization of collagen/silk fibroin bicomponent nanofibrous structures. Biomacromolecules 9:1106–1116PubMedGoogle Scholar
  271. Yurchenco PD, Schittny JC (1990) Molecular architecture of basement membranes. FASEB J 4:1577–1590PubMedGoogle Scholar
  272. Zhang G, Young BB, Ezura Y, Favata M, Soslowsky LJ, Chakravarti S, Birk DE (2005) Development of tendon structure and function: regulation of collagen fibrillogenesis. J Musculoskelet Neuronal Interact 5:5–21PubMedGoogle Scholar
  273. Zhou QH, You YZ, Wu C, Huang Y, Oupicky D (2009) Cyclic RGD-targeting of reversibly stabilized DNA nanoparticles enhances cell uptake and transfection in vitro. J Drug Target 17:364–373PubMedGoogle Scholar
  274. Zinger O, Anselme K, Denzer A, Habersetzer P, Wieland M, Jeanfils J, Hardouin P, Landolt D (2004) Time-dependent morphology and adhesion of osteoblastic cells on titanium model surfaces featuring scale-resolved topography. Biomaterials 25:2695–2711PubMedGoogle Scholar
  275. Zong X, Bien H, Chung CY, Yin L, Fang D, Hsiao BS, Chu B, Entcheva E (2005) Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials 26:5330–5338PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Klaus von der Mark
    • 1
    Email author
  • Jung Park
    • 1
  • Sebastian Bauer
    • 2
  • Patrik Schmuki
    • 2
  1. 1.Department of Experimental Medicine I, Nikolaus Fiebiger Center of Molecular MedicineFriedrich Alexander University at Erlangen-NurembergErlangenGermany
  2. 2.Department of Materials Science, Institute for Surface Chemistry and Corrosion (LKO)Friedrich Alexander University at Erlangen-NurembergErlangenGermany

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