Advanced nanobiomaterial strategies for the development of organized tissue engineering constructs.

Nanobiomaterials, a field at the interface of biomaterials and nanotechnologies, when applied to tissue engineering applications, are usually perceived to resemble the cell microenvironment components or as a material strategy to instruct cells and alter cell behaviors. Therefore, they provide a clear understanding of the relationship between nanotechnologies and resulting cellular responses. This review will cover recent advances in nanobiomaterial research for applications in tissue engineering. In particular, recent developments in nanofibrous scaffolds, nanobiomaterial composites, hydrogel systems, laser-fabricated nanostructures and cell-based bioprinting methods to produce scaffolds with nanofeatures for tissue engineering are discussed. As in native niches of cells, where nanofeatures are constantly interacting and influencing cellular behavior, new generations of scaffolds will need to have these features to enable more desirable engineered tissues. Moving forward, tissue engineering will also have to address the issues of complexity and organization in tissues and organs.

[1]  Xiaohong Li,et al.  Electrospun fibrous mats with high porosity as potential scaffolds for skin tissue engineering. , 2008, Biomacromolecules.

[2]  GeunHyung Kim,et al.  Hybrid Process for Fabricating 3D Hierarchical Scaffolds Combining Rapid Prototyping and Electrospinning , 2008 .

[3]  Elise M. Stewart,et al.  A Single Component Conducting Polymer Hydrogel as a Scaffold for Tissue Engineering , 2012 .

[4]  Eben Alsberg,et al.  Three-dimensional electrospun alginate nanofiber mats via tailored charge repulsions. , 2012, Small.

[5]  Shyni Varghese,et al.  PEG/clay nanocomposite hydrogel: a mechanically robust tissue engineering scaffold , 2010 .

[6]  Masayuki Yamato,et al.  Tissue Engineering Based on Cell Sheet Technology , 2007 .

[7]  R. Narayan,et al.  Laser direct writing of micro- and nano-scale medical devices , 2010, Expert review of medical devices.

[8]  L. Ghasemi‐Mobarakeh,et al.  Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. , 2008, Biomaterials.

[9]  Casey K. Chan,et al.  Fabrication and characterization of hierarchically organized nanoparticle-reinforced nanofibrous composite scaffolds. , 2011, Acta biomaterialia.

[10]  R. Wyrwa,et al.  Two‐Photon Polymerization of Biocompatible Photopolymers for Microstructured 3D Biointerfaces , 2011 .

[11]  Michael Olbrich,et al.  Proliferation of aligned mammalian cells on laser-nanostructured polystyrene. , 2008, Biomaterials.

[12]  Peng Chen,et al.  Interfacing live cells with nanocarbon substrates. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[13]  Saulius Juodkazis,et al.  Two-photon lithography of nanorods in SU-8 photoresist , 2005 .

[14]  V Mironov,et al.  Biofabrication: a 21st century manufacturing paradigm , 2009, Biofabrication.

[15]  Shaochen Chen,et al.  Femtosecond laser nanofabrication of hydrogel biomaterial , 2011 .

[16]  Michael J Yaszemski,et al.  Poly(propylene fumarate) bone tissue engineering scaffold fabrication using stereolithography: effects of resin formulations and laser parameters. , 2007, Biomacromolecules.

[17]  Jun Wang,et al.  New Photoactivators for Multiphoton Excited Three-dimensional Submicron Cross-linking of Proteins: Bovine Serum Albumin and Type 1 Collagen¶,† , 2002, Photochemistry and photobiology.

[18]  Lei Yang,et al.  Nanobiomaterials: State of the Art and Future Trends , 2011 .

[19]  C. Lim,et al.  Fabrication of large pores in electrospun nanofibrous scaffolds for cellular infiltration: a review. , 2012, Tissue engineering. Part B, Reviews.

[20]  Boris N. Chichkov,et al.  Rapid prototyping of ossicular replacement prostheses , 2007 .

[21]  A. Gaharwar,et al.  Mechanically Tough Pluronic F127/Laponite Nanocomposite Hydrogels from Covalently and Physically Cross-Linked Networks , 2011 .

[22]  Tahlia L. Weis,et al.  Surfaces modified with nanometer-thick silver-impregnated polymeric films that kill bacteria but support growth of mammalian cells. , 2010, Biomaterials.

[23]  Costas Fotakis,et al.  Laser-based micro/nanoengineering for biological applications , 2009 .

[24]  L. Niklason,et al.  Scaffold-free vascular tissue engineering using bioprinting. , 2009, Biomaterials.

[25]  K. Chennazhi,et al.  Biocompatible β-chitin hydrogel/nanobioactive glass ceramic nanocomposite scaffolds for periodontal bone regeneration , 2011 .

[26]  Cato T. Laurencin,et al.  Electrospun poly(lactic acid-co-glycolic acid) scaffolds for skin tissue engineering. , 2008, Biomaterials.

[27]  C. Chen,et al.  Preparation and Properties of Poly(lactide-co-glycolide) (PLGA)/ Nano-Hydroxyapatite (NHA) Scaffolds by Thermally Induced Phase Separation and Rabbit MSCs Culture on Scaffolds , 2008, Journal of biomaterials applications.

[28]  D. Norris,et al.  Thermally Stable Organic–Inorganic Hybrid Photoresists for Fabrication of Photonic Band Gap Structures with Direct Laser Writing , 2008 .

[29]  Changqing Xie,et al.  Porous nanofibrous PLLA scaffolds for vascular tissue engineering. , 2010, Biomaterials.

[30]  Seth R. Marder,et al.  Two-photon polymerization initiators for three-dimensional optical data storage and microfabrication , 1999, Nature.

[31]  R. Cancedda,et al.  Three-dimensional cultures of osteogenic and chondrogenic cells: a tissue engineering approach to mimic bone and cartilage in vitro. , 2009, European cells & materials.

[32]  S. Ramakrishna,et al.  Nanobioengineered electrospun composite nanofibers and osteoblasts for bone regeneration. , 2008, Artificial organs.

[33]  Yan Liu,et al.  Myogenic differentiation of human bone marrow mesenchymal stem cells on a 3D nano fibrous scaffold for bladder tissue engineering. , 2010, Biomaterials.

[34]  Seeram Ramakrishna,et al.  Electrospun biomimetic nanocomposite nanofibers of hydroxyapatite/chitosan for bone tissue engineering. , 2008, Biomaterials.

[35]  Peter X Ma,et al.  Structure and properties of nano-hydroxyapatite/polymer composite scaffolds for bone tissue engineering. , 2004, Biomaterials.

[36]  James J. Yoo,et al.  Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. , 2013, Biomaterials.

[37]  Yen Chang,et al.  Electrical coupling of isolated cardiomyocyte clusters grown on aligned conductive nanofibrous meshes for their synchronized beating. , 2013, Biomaterials.

[38]  Say Chye Joachim Loo,et al.  Cellular behavior of human mesenchymal stem cells cultured on single-walled carbon nanotube film , 2010 .

[39]  R. T. Hill,et al.  Direct electrochemical and spectroscopic assessment of heme integrity in multiphoton photo-cross-linked cytochrome C structures. , 2007, Analytical chemistry.

[40]  Jun Hu,et al.  Cell directional migration and oriented division on three-dimensional laser-induced periodic surface structures on polystyrene. , 2008, Biomaterials.

[41]  Stefan Jockenhoevel,et al.  Fabrication of fibrin scaffolds with controlled microscale architecture by a two-photon polymerization–micromolding technique , 2012, Biofabrication.

[42]  B. Chichkov,et al.  Multi-focus two-photon polymerization technique based on individually controlled phase modulation. , 2010, Optics express.

[43]  R. T. Hill,et al.  Microfabrication of three-dimensional bioelectronic architectures. , 2005, Journal of the American Chemical Society.

[44]  X. Mo,et al.  Aligned natural-synthetic polyblend nanofibers for peripheral nerve regeneration. , 2011, Acta biomaterialia.

[45]  M. Kotaki,et al.  Aligned biodegradable nanofibrous structure: a potential scaffold for blood vessel engineering. , 2004, Biomaterials.

[46]  J. Ai,et al.  Preparation of a biomimetic nanocomposite scaffold for bone tissue engineering via mineralization of gelatin hydrogel and study of mineral transformation in simulated body fluid. , 2012, Journal of biomedical materials research. Part A.

[47]  Aleksandr Ovsianikov,et al.  Two Photon Polymerization‐Micromolding of Polyethylene Glycol‐Gentamicin Sulfate Microneedles , 2010, Advanced engineering materials.

[48]  F. Guillemot,et al.  Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. , 2010, Biomaterials.

[49]  K. Akiyoshi,et al.  Nanogel engineering for new nanobiomaterials: from chaperoning engineering to biomedical applications. , 2010, Chemical record.

[50]  Tianyi Yang,et al.  Bio‐Inspired Nacre‐like Composite Films Based on Graphene with Superior Mechanical, Electrical, and Biocompatible Properties , 2012, Advanced materials.

[51]  Malcolm N. Cooke,et al.  Use of stereolithography to manufacture critical-sized 3D biodegradable scaffolds for bone ingrowth. , 2003, Journal of biomedical materials research. Part B, Applied biomaterials.

[52]  R. T. Hill,et al.  Direct-write fabrication of functional protein matrixes using a low-cost Q-switched laser. , 2006, Analytical chemistry.

[53]  Shantikumar V. Nair,et al.  Preparation and characterization of novel β-chitin/nanosilver composite scaffolds for wound dressing applications , 2010 .

[54]  L. Koch,et al.  Laser printing of cells into 3D scaffolds , 2010, Biofabrication.

[55]  Hae-Won Kim,et al.  Electrospun materials as potential platforms for bone tissue engineering. , 2009, Advanced drug delivery reviews.

[56]  Paul J. Campagnola,et al.  Submicron Multiphoton Free-Form Fabrication of Proteins and Polymers: Studies of Reaction Efficiencies and Applications in Sustained Release , 2000 .

[57]  H. Mirzadeh,et al.  Laser-modified nanostructures of PET films and cell behavior. , 2011, Journal of biomedical materials research. Part A.

[58]  C. Fotakis,et al.  Ultra-low shrinkage hybrid photosensitive material for two-photon polymerization microfabrication. , 2008, ACS nano.

[59]  V Mironov,et al.  Scalable robotic biofabrication of tissue spheroids , 2011, Biofabrication.

[60]  D. Lim,et al.  Cell infiltration and growth in a low density, uncompressed three-dimensional electrospun nanofibrous scaffold. , 2011, Biomaterials.

[61]  Nobuyuki Magome,et al.  Electrospun nanofibers as a tool for architecture control in engineered cardiac tissue. , 2011, Biomaterials.

[62]  Seeram Ramakrishna,et al.  Mesenchymal stem cell differentiation to neuronal cells on electrospun nanofibrous substrates for nerve tissue engineering. , 2009, Biomaterials.

[63]  Boris N. Chichkov,et al.  Microreplication of laser-fabricated surface and three-dimensional structures , 2010 .

[64]  J. Fallas,et al.  Multi-hierarchical self-assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel. , 2011, Nature chemistry.

[65]  Christine E Schmidt,et al.  Nanostructured scaffolds for neural applications. , 2008, Nanomedicine.

[66]  Jos Malda,et al.  A Printable Photopolymerizable Thermosensitive p(HPMAm‐lactate)‐PEG Hydrogel for Tissue Engineering , 2011 .

[67]  R. Baughman,et al.  Electrical Stimulation of Myoblast Proliferation and Differentiation on Aligned Nanostructured Conductive Polymer Platforms , 2012, Advanced healthcare materials.

[68]  L. Ghasemi‐Mobarakeh,et al.  Electrical stimulation of nerve cells using conductive nanofibrous scaffolds for nerve tissue engineering. , 2009, Tissue engineering. Part A.

[69]  Masayuki Yamato,et al.  Cell sheet engineering for heart tissue repair. , 2008, Advanced drug delivery reviews.

[70]  Aleksandr Ovsianikov,et al.  Multiphoton microscopy of transdermal quantum dot delivery using two photon polymerization-fabricated polymer microneedles. , 2011, Faraday discussions.

[71]  R. Marchant,et al.  Design and synthesis of biomimetic hydrogel scaffolds with controlled organization of cyclic RGD peptides. , 2009, Bioconjugate chemistry.

[72]  K. Leong,et al.  Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. , 2003, Biomaterials.

[73]  T. Notomi,et al.  Nanogel-based scaffold delivery of prostaglandin E(2) receptor-specific agonist in combination with a low dose of growth factor heals critical-size bone defects in mice. , 2011, Arthritis and rheumatism.

[74]  Costas Fotakis,et al.  Three-dimensional biodegradable structures fabricated by two-photon polymerization. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[75]  Lorenzo Moroni,et al.  3D Fiber‐Deposited Electrospun Integrated Scaffolds Enhance Cartilage Tissue Formation , 2008 .

[76]  B. Chichkov,et al.  Two photon induced polymerization of organic-inorganic hybrid biomaterials for microstructured medical devices. , 2006, Acta biomaterialia.

[77]  P. Bandaru,et al.  Toxicity issues in the application of carbon nanotubes to biological systems. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[78]  Anthony Atala,et al.  In situ bioprinting of the skin for burns , 2010 .

[79]  Mitsuo Umezu,et al.  Fabrication of functional three-dimensional tissues by stacking cell sheets in vitro , 2012, Nature Protocols.

[80]  T. Webster,et al.  Nanotechnology and nanomaterials: Promises for improved tissue regeneration , 2009 .

[81]  M. Prabhakaran,et al.  Mechanical properties and in vitro behavior of nanofiber–hydrogel composites for tissue engineering applications , 2012, Nanotechnology.

[82]  K. Matyjaszewski,et al.  Synthesis by AGET ATRP of degradable nanogel precursors for in situ formation of nanostructured hyaluronic acid hydrogel. , 2009, Biomacromolecules.

[83]  E. Fortunati,et al.  Biodegradable polymer matrix nanocomposites for tissue engineering: A review , 2010 .

[84]  S. Ramakrishna,et al.  Nanostructured biocomposite substrates by electrospinning and electrospraying for the mineralization of osteoblasts. , 2009, Biomaterials.

[85]  A. Mikos,et al.  Electrospinning of polymeric nanofibers for tissue engineering applications: a review. , 2006, Tissue engineering.

[86]  G. Oberdörster,et al.  Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology , 2010, Journal of internal medicine.

[87]  D. Gray,et al.  Two-photon polymerization of titanium-containing sol–gel composites for three-dimensional structure fabrication , 2010 .

[88]  Aleksandr Ovsianikov,et al.  Two‐photon polymerization technique for microfabrication of CAD‐designed 3D scaffolds from commercially available photosensitive materials , 2007, Journal of tissue engineering and regenerative medicine.

[89]  Masaki Noda,et al.  Osteoblastic bone formation is induced by using nanogel‐crosslinking hydrogel as novel scaffold for bone growth factor , 2009, Journal of cellular physiology.

[90]  K Sternberg,et al.  Three-dimensional laser micro- and nano-structuring of acrylated poly(ethylene glycol) materials and evaluation of their cytoxicity for tissue engineering applications. , 2011, Acta biomaterialia.

[91]  F. Baaijens,et al.  Advanced maturation by electrical stimulation: Differences in response between C2C12 and primary muscle progenitor cells , 2011, Journal of tissue engineering and regenerative medicine.

[92]  J Malda,et al.  Bioprinting of hybrid tissue constructs with tailorable mechanical properties , 2011, Biofabrication.

[93]  Peter Dubruel,et al.  A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. , 2012, Biomaterials.

[94]  K. Leong,et al.  Scaffold development using selective laser sintering of polyetheretherketone-hydroxyapatite biocomposite blends. , 2003, Biomaterials.