Nanomaterial-based bone regeneration.

Bone diseases/injuries have been driving an urgent quest for bone substitutes for bone regeneration. Nanoscaled materials with bone-mimicking characteristics may create suitable microenvironments to guide effective bone regeneration. In this review, the natural hierarchical architecture of bone and its regeneration mechanisms are elucidated. Recent progress in the development of nanomaterials which can promote bone regeneration through bone-healing mimicry (e.g., compositional, nanocrystal formation, structural, and growth factor-related mimicking) is summarized. The nanoeffects of nanomaterials on the regulation of bone-related biological functions are highlighted. How to prepare nanomaterials with combinative bone-biomimicry features according to the bone healing process is prospected in order to achieve rapid bone regeneration in situ.

[1]  Yuan Yuan,et al.  Calcium ion-induced formation of β-sheet/-turn structure leading to alteration of osteogenic activity of bone morphogenetic protein-2 , 2015, Scientific Reports.

[2]  Hiroki Yamamoto,et al.  Controlled arrangement of nanoparticles capped with protecting ligand on Au nanopatterns , 2014 .

[3]  J. Coleman,et al.  Structure and mechanism of alkaline phosphatase. , 1992, Annual review of biophysics and biomolecular structure.

[4]  Xinlong Wang,et al.  Gold nanoparticle size and shape influence on osteogenesis of mesenchymal stem cells. , 2016, Nanoscale.

[5]  E. Hunziker,et al.  Osseointegration: the slow delivery of BMP-2 enhances osteoinductivity. , 2012, Bone.

[6]  Carl G Simon,et al.  Injectable and strong nano-apatite scaffolds for cell/growth factor delivery and bone regeneration. , 2008, Dental materials : official publication of the Academy of Dental Materials.

[7]  Jun Komotori,et al.  Preparation of hierarchically organized calcium phosphate–organic polymer composites by calcification of hydrogel , 2006 .

[8]  D. Deamer,et al.  Relation between the Inorganic Chemistry and Biochemistry of Bone Mineralization , 1961, Science.

[9]  Andrés J. García,et al.  Biomaterial strategies for engineering implants for enhanced osseointegration and bone repair. , 2015, Advanced drug delivery reviews.

[10]  B. Boyan,et al.  Response of Musculoskeletal Cells to Biomaterials , 2006, The Journal of the American Academy of Orthopaedic Surgeons.

[11]  Julian H. George,et al.  Exploring and Engineering the Cell Surface Interface , 2005, Science.

[12]  Junmin Lee,et al.  Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. , 2013, Biomaterials.

[13]  B. Boyan,et al.  Implant osseointegration and the role of microroughness and nanostructures: lessons for spine implants. , 2014, Acta biomaterialia.

[14]  G. Cuniberti,et al.  Unveiling the Atomic Structure of Single‐Wall Boron Nanotubes , 2014, 1404.4489.

[15]  D. Kurniawan,et al.  Preparation of Natural Hydroxyapatite from Bovine Femur Bones Using Calcination at Various Temperatures , 2015 .

[16]  Hongyi Li,et al.  The nanoscale geometry of TiO2 nanotubes influences the osteogenic differentiation of human adipose-derived stem cells by modulating H3K4 trimethylation. , 2015, Biomaterials.

[17]  H. M. Jamil,et al.  TGF-β/BMP signaling and other molecular events: regulation of osteoblastogenesis and bone formation , 2015, Bone Research.

[18]  L. Griffith,et al.  Tissue Engineering--Current Challenges and Expanding Opportunities , 2002, Science.

[19]  Yuan Yuan,et al.  Strontium attenuates rhBMP-2-induced osteogenic differentiation via formation of Sr-rhBMP-2 complex and suppression of Smad-dependent signaling pathway. , 2016, Acta biomaterialia.

[20]  J. Vacanti,et al.  Tissue engineering : Frontiers in biotechnology , 1993 .

[21]  M. Glimcher,et al.  Shape and size of isolated bone mineralites measured using atomic force microscopy , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[22]  Françoise Peyrin,et al.  Spatial distribution of tissue level properties in a human femoral cortical bone. , 2012, Journal of biomechanics.

[23]  Changsheng Liu,et al.  The Horizon of Materiobiology: A Perspective on Material-Guided Cell Behaviors and Tissue Engineering. , 2017, Chemical reviews.

[24]  Yuan Yuan,et al.  Surface-induced conformational and functional changes of bone morphogenetic protein-2 adsorbed onto single-walled carbon nanotubes. , 2013, Biochemical and biophysical research communications.

[25]  J. Jansen,et al.  Facilitating the mineralization of oligo(poly(ethylene glycol) fumarate) hydrogel by incorporation of hydroxyapatite nanoparticles. , 2012, Journal of biomedical materials research. Part A.

[26]  Tingting Wang,et al.  Modulation of macrophage phenotype by cell shape , 2013, Proceedings of the National Academy of Sciences.

[27]  R. Ritchie,et al.  Bioinspired structural materials. , 2014, Nature Materials.

[28]  Alexander G Robling,et al.  Biomechanical and molecular regulation of bone remodeling. , 2006, Annual review of biomedical engineering.

[29]  P. Fratzl,et al.  The bone mineralization density distribution as a fingerprint of the mineralization process. , 2007, Bone.

[30]  Xiaofeng Chen,et al.  Biocompatibility and osteogenesis of biomimetic Bioglass-Collagen-Phosphatidylserine composite scaffolds for bone tissue engineering. , 2011, Biomaterials.

[31]  H. Cölfen,et al.  A crystal-clear view , 2010 .

[32]  R O Ritchie,et al.  The true toughness of human cortical bone measured with realistically short cracks. , 2008, Nature materials.

[33]  D. Benoit,et al.  Local and targeted drug delivery for bone regeneration. , 2016, Current opinion in biotechnology.

[34]  Changsheng Liu,et al.  Facilitated receptor-recognition and enhanced bioactivity of bone morphogenetic protein-2 on magnesium-substituted hydroxyapatite surface , 2016, Scientific Reports.

[35]  Shihe Yang,et al.  Bio-inspired synthesis: understanding and exploitation of the crystallization process from amorphous precursors. , 2012, Nanoscale.

[36]  Yuan Yuan,et al.  Magnesium modification up-regulates the bioactivity of bone morphogenetic protein-2 upon calcium phosphate cement via enhanced BMP receptor recognition and Smad signaling pathway. , 2016, Colloids and surfaces. B, Biointerfaces.

[37]  T. Webster,et al.  Enhanced osteoclast-like cell functions on nanophase ceramics. , 2001, Biomaterials.

[38]  H. Fleisch,et al.  Mechanism of Calcification: Inhibitory Role of Pyrophosphate , 1962, Nature.

[39]  S. Goodman,et al.  Inflammation, fracture and bone repair. , 2016, Bone.

[40]  D. Kaplan,et al.  Porosity of 3D biomaterial scaffolds and osteogenesis. , 2005, Biomaterials.

[41]  Xiao-juan Luo,et al.  Biomimetic Intrafibrillar Mineralization of Type I Collagen with Intermediate Precursors-loaded Mesoporous Carriers , 2015, Scientific Reports.

[42]  H. Redmond,et al.  Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[43]  S. Dorozhkin.  Self-Setting Calcium Orthophosphate Formulations , 2013, Journal of functional biomaterials.

[44]  Yuan Yuan,et al.  β-Tricalcium phosphate/poly(glycerol sebacate) scaffolds with robust mechanical property for bone tissue engineering. , 2015, Materials science & engineering. C, Materials for biological applications.

[45]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[46]  Dan Lin,et al.  Enhancement of VEGF-Mediated Angiogenesis by 2-N,6-O-Sulfated Chitosan-Coated Hierarchical PLGA Scaffolds. , 2015, ACS applied materials & interfaces.

[47]  Changsheng Liu,et al.  Functionalized mesoporous bioactive glass scaffolds for enhanced bone tissue regeneration , 2016, Scientific Reports.

[48]  R. Chen,et al.  Biomaterials Act as Enhancers of Growth Factors in Bone Regeneration , 2016 .

[49]  Akon Higuchi,et al.  Physical cues of biomaterials guide stem cell differentiation fate. , 2013, Chemical reviews.

[50]  D. Puleo,et al.  In vitro effects of combined and sequential delivery of two bone growth factors. , 2004, Biomaterials.

[51]  W. Marsden.  I and J , 2012 .

[52]  C. Laurencin,et al.  Studies of bone morphogenetic protein-based surgical repair. , 2012, Advanced drug delivery reviews.

[53]  G. H. Nancollas,et al.  Size-effects in the dissolution of hydroxyapatite: an understanding of biological demineralization , 2004 .

[54]  Dan Lin,et al.  Fabrication and clinical application of easy-to-operate pre-cured CPC/rhBMP-2 micro-scaffolds for bone regeneration. , 2016, American journal of translational research.

[55]  H. Kim,et al.  Capacity of mesoporous bioactive glass nanoparticles to deliver therapeutic molecules. , 2012, Nanoscale.

[56]  S. Ramakrishna,et al.  Controlled release of drugs in electrosprayed nanoparticles for bone tissue engineering. , 2015, Advanced drug delivery reviews.

[57]  B. Boyan,et al.  Integrin α2β1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates , 2008, Proceedings of the National Academy of Sciences.

[58]  O. Suzuki.  Octacalcium phosphate: osteoconductivity and crystal chemistry. , 2010, Acta biomaterialia.

[59]  Biqiong Chen,et al.  Synthesis and characterization of biomimetic hydroxyapatite/sepiolite nanocomposites. , 2011, Nanoscale.

[60]  Eduardo Saiz,et al.  A new approach to mineralization of biocompatible hydrogel scaffolds: an efficient process toward 3-dimensional bonelike composites. , 2003, Journal of the American Chemical Society.

[61]  Lei Cai,et al.  Exposed hydroxyapatite particles on the surface of photo-crosslinked nanocomposites for promoting MC3T3 cell proliferation and differentiation. , 2011, Acta biomaterialia.

[62]  M. Z. Mughal,et al.  Protein adsorption on nano-patterned hydrogenated amorphous carbon model surfaces , 2016 .

[63]  Dan Lin,et al.  Magnesium modification of a calcium phosphate cement alters bone marrow stromal cell behavior via an integrin-mediated mechanism. , 2015, Biomaterials.

[64]  K. Chennazhi,et al.  Fabrication of electrospun poly (lactide-co-glycolide)-fibrin multiscale scaffold for myocardial regeneration in vitro. , 2013, Tissue engineering. Part A.

[65]  W. Tan,et al.  A combinatorial variation in surface chemistry and pore size of three-dimensional porous poly(ε-caprolactone) scaffolds modulates the behaviors of mesenchymal stem cells. , 2016, Materials science & engineering. C, Materials for biological applications.

[66]  Reine Bareille,et al.  Altered nanofeature size dictates stem cell differentiation , 2012, Journal of Cell Science.

[67]  R. G. Richards,et al.  Nanotopographical modification: a regulator of cellular function through focal adhesions. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[68]  Rui L Reis,et al.  Natural‐Based Nanocomposites for Bone Tissue Engineering and Regenerative Medicine: A Review , 2015, Advanced materials.

[69]  Y. Huang,et al.  Micro-/nano- sized hydroxyapatite directs differentiation of rat bone marrow derived mesenchymal stem cells towards an osteoblast lineage. , 2012, Nanoscale.

[70]  P. Dubruel,et al.  Enzymatic mineralization of hydrogels for bone tissue engineering by incorporation of alkaline phosphatase. , 2012, Macromolecular bioscience.

[71]  Changsheng Liu,et al.  Effect of crystal seeding on the hydration of calcium phosphate cement , 1997, Journal of materials science. Materials in medicine.

[72]  Richard O.C. Oreffo,et al.  Biofabrication of bone tissue: approaches, challenges and translation for bone regeneration. , 2016, Biomaterials.

[73]  F. Mauri,et al.  Magnesium incorporation into hydroxyapatite. , 2011, Biomaterials.

[74]  K. Chennazhi,et al.  Role of nanostructured biopolymers and bioceramics in enamel, dentin and periodontal tissue regeneration , 2013 .

[75]  John P Fisher,et al.  Influence of 3D printed porous architecture on mesenchymal stem cell enrichment and differentiation. , 2016, Acta biomaterialia.

[76]  Yuan Yuan,et al.  Nanostructured hydroxyapatite surfaces-mediated adsorption alters recognition of BMP receptor IA and bioactivity of bone morphogenetic protein-2. , 2015, Acta biomaterialia.

[77]  A. Khademhosseini,et al.  Bioactive Silicate Nanoplatelets for Osteogenic Differentiation of Human Mesenchymal Stem Cells , 2013, Advanced materials.

[78]  B. Park,et al.  Self-renewal of embryonic stem cells through culture on nanopattern polydimethylsiloxane substrate. , 2012, Biomaterials.

[79]  Aaas News,et al.  Book Reviews , 1893, Buffalo Medical and Surgical Journal.

[80]  Robert Langer,et al.  A decade of progress in tissue engineering , 2016, Nature Protocols.

[81]  Changsheng Liu,et al.  Kinetics of hydroxyapatite precipitation at pH 10 to 11. , 2001, Biomaterials.

[82]  Lingzhou Zhao,et al.  The osteogenic activity of strontium loaded titania nanotube arrays on titanium substrates. , 2013, Biomaterials.

[83]  J. Y. Lim,et al.  Cell sensing and response to micro- and nanostructured surfaces produced by chemical and topographic patterning. , 2007, Tissue engineering.

[84]  D. Heymann,et al.  Mechanisms of bone repair and regeneration. , 2009, Trends in molecular medicine.

[85]  R. Skoracki,et al.  Development of nanomaterials for bone repair and regeneration. , 2013, Journal of biomedical materials research. Part B, Applied biomaterials.

[86]  J. Pasteris,et al.  A mineralogical perspective on the apatite in bone , 2005 .

[87]  S. Weiner.  Transient precursor strategy in mineral formation of bone. , 2006, Bone.

[88]  Peter X Ma,et al.  Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment. , 2003, Journal of biomedical materials research. Part A.

[89]  C. Wilkinson,et al.  The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. , 2007, Nature materials.

[90]  M. Bostrom,et al.  Potential Role of Bone Morphogenetic Proteins in Fracture Healing , 1998, Clinical orthopaedics and related research.

[91]  Changsheng Liu,et al.  Vascularization and bone regeneration in a critical sized defect using 2-N,6-O-sulfated chitosan nanoparticles incorporating BMP-2. , 2014, Biomaterials.

[92]  Jan Henkel,et al.  Bone Regeneration Based on Tissue Engineering Conceptions — A 21st Century Perspective , 2013, Bone Research.

[93]  Yurong Cai,et al.  Effect of proteins on the synthesis and assembly of calcium phosphate nanomaterials. , 2010, Nanoscale.

[94]  Yan Liu,et al.  Hierarchical Structures of Bone and Bioinspired Bone Tissue Engineering. , 2016, Small.

[95]  Neng Li,et al.  Three-dimensional micro/nanoscale architectures: fabrication and applications. , 2015, Nanoscale.

[96]  Chengtie Wu,et al.  Nanoporous microstructures mediate osteogenesis by modulating the osteo-immune response of macrophages. , 2017, Nanoscale.

[97]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

[98]  Nongyue He,et al.  Recent advances in nano scaffolds for bone repair , 2016, Bone Research.

[99]  H. Kim,et al.  Gene delivery nanocarriers of bioactive glass with unique potential to load BMP2 plasmid DNA and to internalize into mesenchymal stem cells for osteogenesis and bone regeneration. , 2016, Nanoscale.

[100]  Dan Lin,et al.  Bioinspired trimodal macro/micro/nano-porous scaffolds loading rhBMP-2 for complete regeneration of critical size bone defect. , 2016, Acta biomaterialia.

[101]  Lauren M. Cross,et al.  Nanoengineered biomaterials for repair and regeneration of orthopedic tissue interfaces. , 2016, Acta biomaterialia.

[102]  Ying E. Zhang,et al.  Smad-dependent and Smad-independent pathways in TGF-β family signalling , 2003, Nature.

[103]  S. Walrand,et al.  Skeletal muscle regeneration and impact of aging and nutrition , 2016, Ageing Research Reviews.

[104]  Changsheng Liu,et al.  In vitro degradability, bioactivity and cell responses to mesoporous magnesium silicate for the induction of bone regeneration. , 2014, Colloids and surfaces. B, Biointerfaces.

[105]  Bo Liedberg,et al.  Protein adsorption and surface patterning , 2010 .

[106]  M. Grynpas,et al.  Relationships between polyphosphate chemistry, biochemistry and apatite biomineralization. , 2008, Chemical reviews.

[107]  L. Rasmusson,et al.  The influence of controlled surface nanotopography on the early biological events of osseointegration. , 2017, Acta biomaterialia.

[108]  Suck Won Hong,et al.  Reduced graphene oxide-coated hydroxyapatite composites stimulate spontaneous osteogenic differentiation of human mesenchymal stem cells. , 2015, Nanoscale.

[109]  Yuan Yuan,et al.  RhBMP-2-loaded calcium silicate/calcium phosphate cement scaffold with hierarchically porous structure for enhanced bone tissue regeneration. , 2013, Biomaterials.

[110]  H. Chong,et al.  Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level. , 2013, Journal of the mechanical behavior of biomedical materials.