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Regenerative Medicine

Integrating mechanical and biological control of cell proliferation through bioinspired multieffector materials

    Joaquin Seras-Franzoso

    Departament de Genètica & de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Institut de Biotecnologia & de Biomedicina, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    Authors contributed equally

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    ,
    Witold I Tatkiewicz

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Department of Molecular Nanoscience & Organic Materials, Institut de Ciència de Materials de Barcelona (CSIC), Bellaterra, 08193 Barcelona, Spain

    Authors contributed equally

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    ,
    Esther Vazquez

    Departament de Genètica & de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Institut de Biotecnologia & de Biomedicina, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    ,
    Elena García-Fruitós

    Departament de Genètica & de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Institut de Biotecnologia & de Biomedicina, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    ,
    Imma Ratera

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Department of Molecular Nanoscience & Organic Materials, Institut de Ciència de Materials de Barcelona (CSIC), Bellaterra, 08193 Barcelona, Spain

    ,
    Jaume Veciana

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Department of Molecular Nanoscience & Organic Materials, Institut de Ciència de Materials de Barcelona (CSIC), Bellaterra, 08193 Barcelona, Spain

    &
    Antonio Villaverde

    *Author for correspondence:

    E-mail Address: antoni.villaverde@uab.es

    Departament de Genètica & de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    CIBER de Bioingeniería, Biomateriales & Nanomedicina (CIBER-BBN), Bellaterra, 08193 Barcelona, Spain

    Institut de Biotecnologia & de Biomedicina, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain

    Published Online:https://doi.org/10.2217/nnm.15.5

    In nature, cells respond to complex mechanical and biological stimuli whose understanding is required for tissue construction in regenerative medicine. However, the full replication of such bimodal effector networks is far to be reached. Engineering substrate roughness and architecture allows regulating cell adhesion, positioning, proliferation, differentiation and survival, and the external supply of soluble protein factors (mainly growth factors and hormones) has been long applied to promote growth and differentiation. Further, bioinspired scaffolds are progressively engineered as reservoirs for the in situ sustained release of soluble protein factors from functional topographies. We review here how research progresses toward the design of integrative, holistic scaffold platforms based on the exploration of individual mechanical and biological effectors and their further combination.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1 Dalby MJ. Nanostructured surfaces: cell engineering and cell biology. Nanomedicine (Lond.) 4(3), 247–248 (2009).
    • 2 Griffith LG, Naughton G. Tissue engineering: current challenges and expanding opportunities. Science 295(5557), 1009–1014 (2002).
    • 3 Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 23(1), 47–55 (2005).
    • 4 Vagaska B, Bacakova L, Filova E, Balik K. Osteogenic cells on bio-inspired materials for bone tissue engineering. Physiol. Res. 59(3), 309–322 (2010).
    • 5 Biggs MJ, Richards RG, Dalby MJ. Nanotopographical modification: a regulator of cellular function through focal adhesions. Nanomedicine 6(5), 619–633 (2010).
    • 6 Martinez E, Engel E, Planell JA, Samitier J. Effects of artificial micro- and nano-structured surfaces on cell behaviour. Ann. Anat. 191(1), 126–135 (2009).
    • 7 Wojciak-Stothard B, Madeja Z, Korohoda W, Curtis A, Wilkinson C. Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol. Int. 19(6), 485–490 (1995).
    • 8 Wood A. Contact guidance on microfabricated substrata: the response of teleost fin mesenchyme cells to repeating topographical patterns. J. Cell Sci. 90(Pt 4), 667–681 (1988).
    • 9 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. 284(2), 274–282 (2003).
    • 10 Wojciak-Stothard B, Curtis A, Monaghan W, MacDonald K, Wilkinson C. Guidance and activation of murine macrophages by nanometric scale topography. Exp. Cell Res. 223(2), 426–435 (1996).
    • 11 Rajnicek AM, Foubister LE, McCaig CD. Prioritising guidance cues: directional migration induced by substratum contours and electrical gradients is controlled by a rho/cdc42 switch. Dev. Biol. 312(1), 448–460 (2007).
    • 12 Teixeira AI, Abrams GA, Bertics PJ, Murphy CJ, Nealey PF. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J. Cell Sci. 116(Pt 10), 1881–1892 (2003).•• Documents that epithelial cell behavior is profoundly affected by biologic length-scale topographic features.
    • 13 Meyle J, Gultig K, Nisch W. Variation in contact guidance by human cells on a microstructured surface. J. Biomed. Mater. Res. 29(1), 81–88 (1995).
    • 14 Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108(4), 635–644 (1990).• One of the first uses of photolithography for preparation of grooved substrates with controlled geometry on the cell guidance.
    • 15 Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis AS. Changes in fibroblast morphology in response to nano-columns produced by colloidal lithography. Biomaterials 25(23), 5415–5422 (2004).
    • 16 Dalby MJ, Gadegaard N, Riehlea MO, Wilkinson CDW, Curtis ASG. Investigating filopodia sensing using arrays of defined nano-pits down to 35 nm diameter in size. Int. J. Biochem. Cell Biol. 36(10), 2005–2015 (2004).
    • 17 Curtis AS, Gadegaard N, Dalby MJ, Riehle MO, Wilkinson CD, Aitchison G. Cells react to nanoscale order and symmetry in their surroundings. IEEE Trans. Nanobioscience 3(1), 61–65 (2004).
    • 18 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. 94(3), 275–283 (2001).
    • 19 Recknor JB, Recknor JC, Sakaguchi DS, Mallapragada SK. Oriented astroglial cell growth on micropatterned polystyrene substrates. Biomaterials 25(14), 2753–2767 (2004).
    • 20 Loesberg WA, te Riet J, van Delft FC et al. The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion. Biomaterials 28(27), 3944–3951 (2007).
    • 21 Matsuzaka K, Walboomers XF, Yoshinari M, Inoue T, Jansen JA. The attachment and growth behavior of osteoblast-like cells on microtextured surfaces. Biomaterials 24(16), 2711–2719 (2003).
    • 22 Bruinink A, Wintermantel E. Grooves affect primary bone marrow but not osteoblastic MC3T3-E1 cell cultures. Biomaterials 22(18), 2465–2473 (2001).
    • 23 Wang X, Ohlin CA, Lu Q, Hu J. Cell directional migration and oriented division on three-dimensional laser-induced periodic surface structures on polystyrene. Biomaterials 29(13), 2049–2059 (2008).
    • 24 Rebollar E, Frischauf I, Olbrich M et al. Proliferation of aligned mammalian cells on laser-nanostructured polystyrene. Biomaterials 29(12), 1796–1806 (2008).
    • 25 Dalton BA, Walboomers XF, Dziegielewski M et al. Modulation of epithelial tissue and cell migration by microgrooves. J. Biomed. Mater. Res. 56(2), 195–207 (2001).
    • 26 Nomura S, Kojima H, Ohyabu Y, Kuwabara K, Miyauchi A, Uemura T. Nanopillar sheets as a new type of cell culture dish: detailed study of HeLa cells cultured on nanopillar sheets. J. Artif. Organs 9(2), 90–96 (2006).
    • 27 Dalby MJ, Riehle MO, Johnstone H, Affrossman S, Curtis AS. In vitro reaction of endothelial cells to polymer demixed nanotopography. Biomaterials 23(14), 2945–2954 (2002).• Study of endothelial cell response to nanotopography obtained by polymer demixing. It is demonstrated, that morphological and cytoskeletal response depends on topographical feature size.
    • 28 Charest JL, Bryant LE, Garcia AJ, King WP. Hot embossing for micropatterned cell substrates. Biomaterials 25(19), 4767–4775 (2004).
    • 29 Miller C, Shanks H, Witt A, Rutkowski G, Mallapragada S. Oriented Schwann cell growth on micropatterned biodegradable polymer substrates. Biomaterials 22(11), 1263–1269 (2001).
    • 30 Thapa A, Webster TJ, Haberstroh KM. Polymers with nano-dimensional surface features enhance bladder smooth muscle cell adhesion. J. Biomed. Mater. Res. A 67(4), 1374–1383 (2003).
    • 31 Meyle J, Wolburg H, von Recum AF. Surface micromorphology and cellular interactions. J. Biomater. Appl. 7(4), 362–374 (1993).
    • 32 Matsuzaka K, Walboomers XF, de Ruijter JE, Jansen JA. The effect of poly-L-lactic acid with parallel surface micro groove on osteoblast-like cells in vitro. Biomaterials 20(14), 1293–1301 (1999).
    • 33 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 28(28), 4068–4077 (2007).
    • 34 Green AM, Jansen JA, van der Waerden JP, von Recum AF. Fibroblast response to microtextured silicone surfaces: texture orientation into or out of the surface. J. Biomed. Mater. Res. 28(5), 647–653 (1994).
    • 35 Bettinger CJ, Zhang Z, Gerecht S, Borenstein JT, Langer R. Enhancement of in vitro capillary tube formation by substrate nanotopography. Adv. Mater. 20(1), 99–103 (2008).
    • 36 Yim EK, Pang SW, Leong KW. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp. Cell Res. 313(9), 1820–1829 (2007).
    • 37 Dalby MJ, Gadegaard N, Tare R et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 6(12), 997–1003 (2007).•• Demonstrates the proper use of nanoscale modification of scaffolds stimulates human mesenchymal stem cells to produce bone minerals in vitro, in the absence of osteogenic supplements.
    • 38 Dalby MJ, McCloy D, Robertson M et al. Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27(15), 2980–2987 (2006).
    • 39 Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis AS. Fibroblast response to a controlled nanoenvironment produced by colloidal lithography. J. Biomed. Mater. Res. A 69(2), 314–322 (2004).
    • 40 Yim EK, Reano RM, Pang SW, Yee AF, Chen CS, Leong KW. Nanopattern-induced changes in morphology and motility of smooth muscle cells. Biomaterials 26(26), 5405–5413 (2005).•• Study of proliferation, motility and morphology of cells growing on poly(methylmethacrylate) and poly-dimethyl siloxane substrates with developed nanotopography. It is proposed that used nanoimprinting technology will provide a valuable platform for studies in cell–substrate interactions and for development of medical devices with nanoscale features.
    • 41 Miller DC, Thapa A, Haberstroh KM, Webster TJ. Endothelial and vascular smooth muscle cell function on poly(lactic-co-glycolic acid) with nano-structured surface features. Biomaterials 25(1), 53–61 (2004).
    • 42 Kim DH, Kim P, Suh K, Kyu CS, Ho LS, Kim B. Modulation of adhesion and growth of cardiac myocytes by surface nanotopography. Conf. Proc. IEEE Eng. Med. Biol. Soc. 4, 4091–4094 (2005).
    • 43 Kim P, Kim DH, Kim B et al. Fabrication of nanostructures of polyethylene glycol for applications to protein adsorption and cell adhesion. Nanotechnology 16(10), 2420–2426 (2005).
    • 44 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. 18(6), 1211–1218 (2007).
    • 45 Biggs MJ, Richards RG, Gadegaard N, Wilkinson CD, Dalby MJ. The effects of nanoscale pits on primary human osteoblast adhesion formation and cellular spreading. J. Mater. Sci. Mater. Med. 18(2), 399–404 (2007).
    • 46 Bettinger CJ, Orrick B, Misra A, Langer R, Borenstein JT. Microfabrication of poly (glycerol-sebacate) for contact guidance applications. Biomaterials 27(12), 2558–2565 (2006).
    • 47 Choi CH, Hagvall SH, Wu BM, Dunn JC, Beygui RE, Kim CJ. Cell interaction with three-dimensional sharp-tip nanotopography. Biomaterials 28(9), 1672–1679 (2007).
    • 48 Foley JD, Grunwald EW, Nealey PF, Murphy CJ. Cooperative modulation of neuritogenesis by PC12 cells by topography and nerve growth factor. Biomaterials 26(17), 3639–3644 (2005).
    • 49 Karuri NW, Liliensiek S, Teixeira AI et al. Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells. J. Cell Sci. 117(Pt 15), 3153–3164 (2004).
    • 50 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. 108(Pt 4), 1563–1573 (1995).
    • 51 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. 4(1), 192–201 (2008).
    • 52 Andersson AS, Backhed F, von EA, Richter-Dahlfors A, Sutherland D, Kasemo B. Nanoscale features influence epithelial cell morphology and cytokine production. Biomaterials 24(20), 3427–3436 (2003).
    • 53 Popat KC, Chatvanichkul KI, Barnes GL, Latempa TJ Jr, Grimes CA, Desai TA. Osteogenic differentiation of marrow stromal cells cultured on nanoporous alumina surfaces. J. Biomed. Mater. Res. A 80(4), 955–964 (2007).
    • 54 Kunzler TP, Huwiler C, Drobek T, Voros J, Spencer ND. Systematic study of osteoblast response to nanotopography by means of nanoparticle-density gradients. Biomaterials 28(33), 5000–5006 (2007).
    • 55 Kantawong F, Burgess KE, Jayawardena K et al. Whole proteome analysis of osteoprogenitor differentiation induced by disordered nanotopography and mediated by ERK signalling. Biomaterials 30(27), 4723–4731 (2009).
    • 56 Kantawong F, Burchmore R, Gadegaard N, Oreffo RO, Dalby MJ. Proteomic analysis of human osteoprogenitor response to disordered nanotopography. J. R. Soc. Interface 6(40), 1075–1086 (2009).
    • 57 Heydarkhan-Hagvall S, Choi CH, Dunn J et al. Influence of systematically varied nano-scale topography on cell morphology and adhesion. Cell Commun. Adhes. 14(5), 181–194 (2007).
    • 58 Uttayarat P, Toworfe GK, Dietrich F, Lelkes PI, Composto RJ. Topographic guidance of endothelial cells on silicone surfaces with micro- to nanogrooves: orientation of actin filaments and focal adhesions. J. Biomed Mater. Res. A 75(3), 668–680 (2005).
    • 59 McKee CT, Raghunathan VK, Nealey PF, Russell P, Murphy CJ. Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells. Biophys. J. 101(9), 2139–2146 (2011).
    • 60 Lange SA, Benes V, Kern DP, Horber JK, Bernard A. Microcontact printing of DNA molecules. Anal. Chem. 76(6), 1641–1647 (2004).
    • 61 Falconnet D, Csucs G, Grandin HM, Textor M. Surface engineering approaches to micropattern surfaces for cell-based assays. Biomaterials 27(16), 3044–3063 (2006).
    • 62 Mrksich M, Dike LE, Tien J, Ingber DE, Whitesides GM. Using microcontact printing to pattern the attachment of mammalian cells to self-assembled monolayers of alkanethiolates on transparent films of gold and silver. Exp. Cell Res. 235(2), 305–313 (1997).
    • 63 Zhang S, Yan L, Altman M et al. Biological surface engineering: a simple system for cell pattern formation. Biomaterials 20(13), 1213–1220 (1999).
    • 64 Raghavan S, Desai RA, Kwon Y, Mrksich M, Chen CS. Micropatterned dynamically adhesive substrates for cell migration. Langmuir 26(22), 17733–17738 (2010).
    • 65 Yan X, Yao J, Lu G, Chen X, Zhang K, Yang B. Microcontact printing of colloidal crystals. J. Am. Chem. Soc. 126(34), 10510–10511 (2004).
    • 66 Weibel DB, Lee A, Mayer M et al. Bacterial printing press that regenerates its ink: contact-printing bacteria using hydrogel stamps. Langmuir 21(14), 6436–6442 (2005).
    • 67 Keefer EW, Botterman BR, Romero MI, Rossi AF, Gross GW. Carbon nanotube coating improves neuronal recordings. Nat. Nanotechnol. 3(7), 434–439 (2008).
    • 68 Lipski AM, Pino CJ, Haselton FR, Chen IW, Shastri VP. The effect of silica nanoparticle-modified surfaces on cell morphology, cytoskeletal organization and function. Biomaterials 29, 3836–3846 (2008).
    • 69 Ludden MJ, Mulder A, Tampe R, Reinhoudt DN, Huskens J. Molecular printboards as a general platform for protein immobilization: a supramolecular solution to nonspecific adsorption. Angew. Chem. Int. Ed. Engl. 46(22), 4104–4107 (2007).
    • 70 Samaroo HD, Lu J, Webster TJ. Enhanced endothelial cell density on NiTi surfaces with sub-micron to nanometer roughness. Int. J. Nanomedicine 3(1), 75–82 (2008).
    • 71 Park J, Bauer S, von der MK, Schmuki P. Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett. 7(6), 1686–1691 (2007).
    • 72 Namgung S, Baik KY, Park J, Hong S. Controlling the growth and differentiation of human mesenchymal stem cells by the arrangement of individual carbon nanotubes. ACS Nano 5(9), 7383–7390 (2011).
    • 73 Charest JL, Eliason MT, Garcia AJ, King WP. Combined microscale mechanical topography and chemical patterns on polymer cell culture substrates. Biomaterials 27(11), 2487–2494 (2006).
    • 74 Feinberg AW, Wilkerson WR, Seegert CA, Gibson AL, Hoipkemeier-Wilson L, Brennan AB. Systematic variation of microtopography, surface chemistry and elastic modulus and the state dependent effect on endothelial cell alignment. J. Biomed. Mater. Res. A 86(2), 522–534 (2008).
    • 75 Recknor JB, Sakaguchi DS, Mallapragada SK. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 27(22), 4098–4108 (2006).
    • 76 García-Fruitós E, Rodríguez-Carmona E, Díez-Gil C et al. Surface cell growth engineering assisted by a novel bacterial nanomaterial. Adv. Mater. 21, 4249–4253 (2009).
    • 77 Diez-Gil C, Krabbenborg S, Garcia-Fruitos E et al. The nanoscale properties of bacterial inclusion bodies and their effect on mammalian cell proliferation. Biomaterials 31(22), 5805–5812 (2010).
    • 78 Seras-Franzoso J, Diez-Gil C, Vazquez E et al. Bioadhesiveness and efficient mechanotransduction stimuli synergistically provided by bacterial inclusion bodies as scaffolds for tissue engineering. Nanomedicine (Lond.) 7(1), 79–93 (2012).
    • 79 Tatkiewicz WI, Seras-Franzoso J, Garcia-Fruitos E et al. Two-dimensional microscale engineering of protein-based nanoparticles for cell guidance. ACS Nano 7(6), 4774–4784 (2013).
    • 80 Khang D, Carpenter J, Chun YW, Pareta R, Webster TJ. Nanotechnology for regenerative medicine. Biomed. Microdevices 12(4), 575–587 (2010).
    • 81 Navarro M, Michiardi A, Castano O, Planell JA. Biomaterials in orthopaedics. J. R. Soc. Interface 5(27), 1137–1158 (2008).
    • 82 Bonzani IC, George JH, Stevens MM. Novel materials for bone and cartilage regeneration. Curr. Opin. Chem. Biol. 10(6), 568–575 (2006).
    • 83 Hollister SJ. Porous scaffold design for tissue engineering. Nat. Mater. 4(7), 518–524 (2005).
    • 84 Huang D, Zuo Y, Li J et al. Bioactive composite gradient coatings of nano-hydroxyapatite/polyamide66 fabricated on polyamide66 substrates. J. R. Soc. Interface 9(72), 1450–1457 (2012).
    • 85 Su B, Peng X, Jiang D et al. In vitro and in vivo evaluations of nano-hydroxyapatite/polyamide 66/glass fibre (n-HA/PA66/GF) as a novel bioactive bone screw. PLoS ONE 8(7), e68342 (2013).
    • 86 Huang D, Zuo Y, Zou Q et al. Antibacterial chitosan coating on nano-hydroxyapatite/polyamide66 porous bone scaffold for drug delivery. J. Biomater. Sci. Polym. Ed. 22(7), 931–944 (2011).
    • 87 Shekaran A, Garcia AJ. Extracellular matrix-mimetic adhesive biomaterials for bone repair. J. Biomed. Mater. Res. A 96(1), 261–272 (2011).
    • 88 Vroman L, Adams AL. Identification of rapid changes at plasma-solid interfaces. J. Biomed. Mater. Res. 3(1), 43–67 (1969).
    • 89 Wilson K, Stuart SJ, Garcia A, Latour RA Jr. 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. A 69(4), 686–698 (2004).
    • 90 Kaufmann D, Fiedler A, Junger A, Auernheimer J, Kessler H, Weberskirch R. Chemical conjugation of linear and cyclic RGD moieties to a recombinant elastin-mimetic polypeptide: a versatile approach towards bioactive protein hydrogels. Macromol. Biosci. 8(6), 577–588 (2008).
    • 91 Webster TJ, Ahn ES. Nanostructured biomaterials for tissue engineering bone. Adv. Biochem. Eng. Biotechnol. 103, 275–308 (2007).
    • 92 Hong JM, Kim BJ, Shim JH et al. Enhancement of bone regeneration through facile surface functionalization of solid freeform fabrication-based three-dimensional scaffolds using mussel adhesive proteins. Acta Biomater. 8(7), 2578–2586 (2012).
    • 93 Zhang X, Baughman CB, Kaplan DL. In vitro evaluation of electrospun silk fibroin scaffolds for vascular cell growth. Biomaterials 29(14), 2217–2227 (2008).
    • 94 Dao MA, Hashino K, Kato I, Nolta JA. Adhesion to fibronectin maintains regenerative capacity during ex vivo culture and transduction of human hematopoietic stem and progenitor cells. Blood 92(12), 4612–4621 (1998).
    • 95 Miyazaki T, Futaki S, Suemori H et al. Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nat. Commun. 3, 1236 (2012).
    • 96 Salasznyk RM, Williams WA, Boskey A, Batorsky A, Plopper GE. Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells. J. Biomed. Biotechnol. 2004(1), 24–34 (2004).
    • 97 Wojtowicz AM, Shekaran A, Oest ME et al. Coating of biomaterial scaffolds with the collagen-mimetic peptide GFOGER for bone defect repair. Biomaterials 31(9), 2574–2582 (2010).
    • 98 Unterman SA, Gibson M, Lee JH et al. Hyaluronic acid-binding scaffold for articular cartilage repair. Tissue Eng. Part A 18(23–24), 2497–2506 (2012).
    • 99 Martinez-Osorio H, Juarez-Campo M, Diebold Y et al. Genetically engineered elastin-like polymer as a substratum to culture cells from the ocular surface. Curr. Eye Res. 34(1), 48–56 (2009).
    • 100 Forsprecher J, Wang Z, Goldberg HA, Kaartinen MT. Transglutaminase-mediated oligomerization promotes osteoblast adhesive properties of osteopontin and bone sialoprotein. Cell Adh. Migr. 5(1), 65–72 (2011).
    • 101 Jensen T, Baas J, Dolathshahi-Pirouz A et al. Osteopontin functionalization of hydroxyapatite nanoparticles in a PDLLA matrix promotes bone formation. J. Biomed. Mater Res. A 99(1), 94–101 (2011).
    • 102 Jung H, Park JS, Yeom J et al. 3D tissue engineered supramolecular hydrogels for controlled chondrogenesis of human mesenchymal stem cells. Biomacromolecules 15(3), 707–714 (2014).
    • 103 Porter AM, Klinge CM, Gobin AS. Biomimetic hydrogels with VEGF induce angiogenic processes in both hUVEC and hMEC. Biomacromolecules 12(1), 242–246 (2011).
    • 104 Zieris A, Chwalek K, Prokoph S et al. Dual independent delivery of pro-angiogenic growth factors from starPEG-heparin hydrogels. J. Control. Release 156(1), 28–36 (2011).
    • 105 Gnavi S, di Blasio L, Tonda-Turo C et al. Gelatin-based hydrogel for vascular endothelial growth factor release in peripheral nerve tissue engineering. J. Tissue Eng. Regen. Med. doi:10.1002/term.1936 (2014) (Epub ahead of print).
    • 106 Stukel J, Thompson S, Simon L, Willits R. Polyethlyene glycol microgels to deliver bioactive nerve growth factor. J. Biomed. Mater. Res. A doi:10.1002/jbm.a.35209 (2014) (Epub ahead of print).• Interesting in vivo example of the use of hydrogels as delivery platforms of growth factors with promising results in nerve tissue regeneration.
    • 107 Seras-Franzoso J, Peebo K, Garcia-Fruitos E, Vazquez E, Rinas U, Villaverde A. Improving protein delivery of fibroblast growth factor-2 from bacterial inclusion bodies used as cell culture substrates. Acta Biomater. 10, 1354–1359 (2013).
    • 108 Simmons CA, Alsberg E, Hsiong S, Kim WJ, Mooney DJ. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35(2), 562–569 (2004).
    • 109 Smith EL, Kanczler JM, Gothard D et al. Evaluation of skeletal tissue repair, part 1: assessment of novel growth-factor-releasing hydrogels in an ex vivo chick femur defect model. Acta Biomater. 10(10), 4186–4196 (2014).•• Describes the use of a new and improved type of hydrogel for tissue engineering applications. This hydrogel has been combined, for the first time, with decellularized and demineralized extracellular matrix- and microparticle-containing growth factors with the aim to successfully mimic both the biological and physico-chemical functions of the extracellular environment.
    • 110 Smith EL, Kanczler JM, Gothard D et al. Evaluation of skeletal tissue repair, part 2: enhancement of skeletal tissue repair through dual-growth-factor-releasing hydrogels within an ex vivo chick femur defect model. Acta Biomater. 10(10), 4197–4205 (2014).•• Describes the use of a new and improved type of hydrogel for tissue engineering applications. This hydrogel has been combined, for the first time, with decellularized and demineralized extracellular matrix- and microparticle- containing growth factors with the aim to successfully mimic both the biological and physico-chemical functions of the extracellular environment.
    • 111 Luo J, Cao S, Chen X et al. Super long-term glycemic control in diabetic rats by glucose-sensitive LbL films constructed of supramolecular insulin assembly. Biomaterials 33(33), 8733–8742 (2012).
    • 112 Maji SK, Schubert D, Rivier C, Lee S, Rivier JE, Riek R. Amyloid as a depot for the formulation of long-acting drugs. PLoS Biol. 6(2), e17 (2008).
    • 113 Chun J, Bhak G, Lee SG et al. Kappa-Casein-based hierarchical suprastructures and their use for selective temporal and spatial control over neuronal differentiation. Biomacromolecules 13(9), 2731–2738 (2012).
    • 114 Davis ME, Hsieh PC, Takahashi T et al. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl Acad. Sci. USA 103(21), 8155–8160 (2006).
    • 115 Seras-Franzoso J, Steurer C, Roldan M et al. Functionalization of 3D scaffolds with protein-releasing biomaterials for intracellular delivery. J. Control. Release 171(1), 63–72 (2013).
    • 116 Berns EJ, Sur S, Pan L et al. Aligned neurite outgrowth and directed cell migration in self-assembled monodomain gels. Biomaterials 35(1), 185–195 (2014).
    • 117 Yang H, Qu T, Yang H et al. Self-assembling nanofibers improve cognitive impairment in a transgenic mice model of Alzheimer's disease. Neurosci. Lett. 556, 63–68 (2013).• Interesting in vivo example of peptide amphiphile nanofibers functionalization with the IKVAV motif.
    • 118 Massia SP, Holecko MM, Ehteshami GR et al. In vitro assessment of bioactive coatings for neural implant applications. J. Biomed. Mater. Res. A 68(1), 177–186 (2004).
    • 119 von der MK, Park J, Bauer S, Schmuki P. Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res. 339(1), 131–153 (2010).
    • 120 Reichl S. Films based on human hair keratin as substrates for cell culture and tissue engineering. Biomaterials 30(36), 6854–6866 (2009).• Seminal article on the use of human hair keratin as a coating material for cell culture using novel methods for film generation and performing an exhaustive study on cell growth and epithelial tightness of different cell types.
    • 121 Almine JF, Bax DV, Mithieux SM et al. Elastin-based materials. Chem. Soc. Rev. 39(9), 3371–3379 (2010).
    • 122 Kundu B, Rajkhowa R, Kundu SC, Wang X. Silk fibroin biomaterials for tissue regenerations. Adv. Drug Deliv. Rev. 65(4), 457–470 (2013).
    • 123 Min BM, Lee G, Kim SH, Nam YS, Lee TS, Park WH. Electrospinning of silk fibroin nanofibers and its effect on the adhesion and spreading of normal human keratinocytes and fibroblasts in vitro. Biomaterials 25(7–8), 1289–1297 (2004).
    • 124 Jin HJ, Chen J, Karageorgiou V, Altman GH, Kaplan DL. Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials 25(6), 1039–1047 (2004).
    • 125 Yang Z, Tu Q, Zhu Y et al. Mussel-inspired coating of polydopamine directs endothelial and smooth muscle cell fate for re-endothelialization of vascular devices. Adv. Healthc. Mater. 1(5), 548–559 (2012).• Nice example on the use of polydopamine, a mussel-adhesive protein-inspired coating, as a vascular stent surface to promote endothelial function with a deep biocompatibility analysis.
    • 126 Sreejalekshmi KG, Nair PD. Biomimeticity in tissue engineering scaffolds through synthetic peptide modifications-altering chemistry for enhanced biological response. J. Biomed. Mater. Res. A 96(2), 477–491 (2011).
    • 127 Chatakun P, Nunez-Toldra R, Díaz López EJ et al. The effect of five proteins on stem cells used for osteoblast differentiation and proliferation: a current review of the literature. Cell Mol. Life Sci. 71(1), 113–142 (2014).
    • 128 Kopecek J, Yang J. Smart self-assembled hybrid hydrogel biomaterials. Angew. Chem. Int. Ed. Engl. 51(30), 7396–7417 (2012).
    • 129 Chen FM, Zhang M, Wu ZF. Toward delivery of multiple growth factors in tissue engineering. Biomaterials 31(24), 6279–6308 (2010).• The authors introduce the concept of dual and multiple delivery of growth factors for tissue engineering using several examples already published.
    • 130 Jiang Y, Chen J, Deng C, Suuronen EJ, Zhong Z. Click hydrogels, microgels and nanogels: emerging platforms for drug delivery and tissue engineering. Biomaterials 35(18), 4969–4985 (2014).
    • 131 Ladewig K. Drug delivery in soft tissue engineering. Expert Opin. Drug Deliv. 8(9), 1175–1188 (2011).
    • 132 Lienemann PS, Lutolf MP, Ehrbar M. Biomimetic hydrogels for controlled biomolecule delivery to augment bone regeneration. Adv. Drug Deliv. Rev. 64(12), 1078–1089 (2012).
    • 133 Kempen DH, Lu L, Heijink A et al. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 30(14), 2816–2825 (2009).
    • 134 Thomas AM, Gomez AJ, Palma JL, Yap WT, Shea LD. Heparin-chitosan nanoparticle functionalization of porous poly(ethylene glycol) hydrogels for localized lentivirus delivery of angiogenic factors. Biomaterials 35(30), 8687–8693 (2014).
    • 135 Knowles TP, Buehler MJ. Nanomechanics of functional and pathological amyloid materials. Nat. Nanotechnol. 6(8), 469–479 (2011).
    • 136 Mitraki A. Protein aggregation from inclusion bodies to amyloid and biomaterials. Adv. Protein Chem. Struct. Biol. 79, 89–125 (2010).
    • 137 Maji SK, Perrin MH, Sawaya MR et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325(5938), 328–332 (2009).•• The authors unveil for the first time a number of peptide hormones being stored in releasable amyloids in the pituitary secretory granules. These functional amyloids evidence the need of rethinking the relationship between amyloids and amyloidal toxicity.
    • 138 Measey TJ, Gai F. Light-triggered disassembly of amyloid fibrils. Langmuir 28(34), 12588–12592 (2012).
    • 139 Cano-Garrido O, Rodriguez-Carmona E, Díez-Gil C et al. Supramolecular organization of protein-releasing functional amyloids solved in bacterial inclusion bodies. Acta Biomater. 9(4), 6134–6142 (2013).
    • 140 Seras-Franzoso J, Peebo K, Corchero JL et al. A nanostructured bacterial bio-scaffold for the sustained bottom–up delivery of protein drugs. Nanomedicine (Lond.) 8(10), 1587–1599 (2013).
    • 141 Seras-Franzoso J, Tsimbouri PM, Burgess KV et al. Topographically targeted osteogenesis of mesenchymal stem cells stimulated by inclusion bodies attached to polycaprolactone surfaces. Nanomedicine (Lond.) 9, 207–220 (2014).
    • 142 Mankar S, Anoop A, Sen S, Maji SK. Nanomaterials: amyloids reflect their brighter side. Nano Rev. 2, 6032 (2011).
    • 143 Vazquez E, Corchero JL, Burgueno JF et al. Functional inclusion bodies produced in bacteria as naturally occurring nanopills for advanced cell therapies. Adv. Mater. 24(13), 1742–1747 (2012).
    • 144 Rueda F, Cano-Garrido O, Mamat U et al. Production of functional inclusion bodies in endotoxin-free Escherichia coli. Appl. Microbiol. Biotechnol. 98(22), 9229–9238 (2014).
    • 145 Ghadiri MR, Granja JR, Milligan RA, McRee DE, Khazanovich N. Self-assembling organic nanotubes based on a cyclic peptide architecture. Nature 366(6453), 324–327 (1993).
    • 146 Claussen RC, Rabatic BM, Stupp SI. Aqueous self-assembly of unsymmetric peptide bolaamphiphiles into nanofibers with hydrophilic cores and surfaces. J. Am. Chem. Soc. 125(42), 12680–12681 (2003).
    • 147 Vauthey S, Santoso S, Gong H, Watson N, Zhang S. Molecular self-assembly of surfactant-like peptides to form nanotubes and nanovesicles. Proc. Natl Acad. Sci. USA 99(8), 5355–5360 (2002).
    • 148 Reches M, Gazit E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300(5619), 625–627 (2003).