Diatom‐Inspired Silica Nanostructure Coatings with Controllable Microroughness Using an Engineered Mussel Protein Glue to Accelerate Bone Growth on Titanium‐Based Implants

Silica nanoparticles (SiNPs) have been utilized to construct bioactive nanostructures comprising surface topographic features and bioactivity that enhances the activity of bone cells onto titanium-based implants. However, there have been no previous attempts to create microrough surfaces based on SiNP nanostructures even though microroughness is established as a characteristic that provides beneficial effects in improving the biomechanical interlocking of titanium implants. Herein, a protein-based SiNP coating is proposed as an osteopromotive surface functionalization approach to create microroughness on titanium implant surfaces. A bioengineered recombinant mussel adhesive protein fused with a silica-precipitating R5 peptide (R5-MAP) enables direct control of the microroughness of the surface through the multilayer assembly of SiNP nanostructures under mild conditions. The assembled SiNP nanostructure significantly enhances the in vitro osteogenic cellular behaviors of preosteoblasts in a roughness-dependent manner and promotes the in vivo bone tissue formation on a titanium implant within a calvarial defect site. Thus, the R5-MAP-based SiNP nanostructure assembly could be practically applied to accelerate bone-tissue growth to improve the stability and prolong the lifetime of medical implantable devices.

[1]  Maxence Bigerelle,et al.  Effect of grooved titanium substratum on human osteoblastic cell growth. , 2002, Journal of biomedical materials research.

[2]  Qing Shen,et al.  Structure and properties of layer-by-layer self-assembled chitosan/lignosulfonate multilayer film. , 2012, Materials science & engineering. C, Materials for biological applications.

[3]  M. Vallet‐Regí,et al.  Mechanical properties of organically modified silicates for bone regeneration , 2009, Journal of materials science. Materials in medicine.

[4]  K. Komvopoulos,et al.  Nanomechanical Properties of Polymers Determined From Nanoindentation Experiments , 2001 .

[5]  Carole C. Perry,et al.  Biosilicification: the role of the organic matrix in structure control , 2000, JBIC Journal of Biological Inorganic Chemistry.

[6]  Richard M Day,et al.  Bioactive glass stimulates the secretion of angiogenic growth factors and angiogenesis in vitro. , 2005, Tissue engineering.

[7]  T. Albrektsson,et al.  Osteoinduction, osteoconduction and osseointegration , 2001, European Spine Journal.

[8]  Chun-Hway Hsueh Effects of Aspect Ratios of Ellipsoidal Inclusions on Elastic Stress Transfer of Ceramic Composites , 1989 .

[9]  Zi-kui Liu Thermodynamic calculations and phase diagrams for magnesium and its alloys: Part II , 2008 .

[10]  P. Layrolle,et al.  Surface treatments of titanium dental implants for rapid osseointegration. , 2007, Dental materials : official publication of the Academy of Dental Materials.

[11]  J. Waite,et al.  Polyphenolic Substance of Mytilus edulis: Novel Adhesive Containing L-Dopa and Hydroxyproline. , 1981, Science.

[12]  E. Vuorio,et al.  Silica-based bioactive glasses modulate expression of bone morphogenetic protein-2 mRNA in Saos-2 osteoblasts in vitro. , 2001, Biomaterials.

[13]  C. Stanford,et al.  Effects of Implant Microtopography on Osteoblast Cell Attachment , 2003, Implant dentistry.

[14]  Chirathodi Vayalappil Muraleedharan,et al.  Laser surface modification of titanium substrate for pulsed laser deposition of highly adherent hydroxyapatite , 2011, Journal of materials science. Materials in medicine.

[15]  E. Chang,et al.  Influence of residual stress on bonding strength and fracture of plasma-sprayed hydroxyapatite coatings on Ti-6Al-4V substrate. , 2001, Biomaterials.

[16]  David L Cochran,et al.  Osteoblast maturation and new bone formation in response to titanium implant surface features are reduced with age , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[17]  Bum Jin Kim,et al.  Surface-independent antibacterial coating using silver nanoparticle-generating engineered mussel glue. , 2014, ACS applied materials & interfaces.

[18]  J. Pou,et al.  Micro- and nano-testing of calcium phosphate coatings produced by pulsed laser deposition. , 2003, Biomaterials.

[19]  H. Cha,et al.  Development of bioadhesives from marine mussels , 2008, Biotechnology journal.

[20]  Cong Zhou,et al.  Bioengineered mussel glue incorporated with a cell recognition motif as an osteostimulating bone adhesive for titanium implants. , 2015, Journal of materials chemistry. B.

[21]  J. J. Mecholsky,et al.  Fracture toughness of manatee rib and bovine femur using a chevron-notched beam test. , 2006, Journal of biomechanics.

[22]  Eduardo Saiz,et al.  Nanotechnology Approaches for Better Dental Implants , 2011 .

[23]  V. Shastri,et al.  The effect of silica nanoparticle-modified surfaces on cell morphology, cytoskeletal organization and function. , 2008, Biomaterials.

[24]  Hee Young Yoo,et al.  Recombinant mussel coating protein fused with cell adhesion recognition motif enhanced cell proliferation , 2015, Biotechnology and Bioprocess Engineering.

[25]  Byung Hoon Jo,et al.  Recent developments and applications of bioinspired silicification , 2016, Korean Journal of Chemical Engineering.

[26]  M. Sumper,et al.  Silica Biomineralisation in Diatoms: The Model Organism Thalassiosira pseudonana , 2008, Chembiochem : a European journal of chemical biology.

[27]  G S Stein,et al.  Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. , 1993, Endocrine reviews.

[28]  Ann Wennerberg,et al.  Oral implant surfaces: Part 1--review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. , 2004, The International journal of prosthodontics.

[29]  H. Rack,et al.  Titanium alloys in total joint replacement--a materials science perspective. , 1998, Biomaterials.

[30]  Kemin Wang,et al.  Bionanotechnology based on silica nanoparticles , 2004, Medicinal research reviews.

[31]  K. Rottner,et al.  Interplay between Rac and Rho in the control of substrate contact dynamics , 1999, Current Biology.

[32]  Chaobin He,et al.  Star-shaped polyhedral oligomeric silsesquioxane-polycaprolactone-polyurethane as biomaterials for tissue engineering application , 2014 .

[33]  Zhiyong Tang,et al.  Biomedical Applications of Layer‐by‐Layer Assembly: From Biomimetics to Tissue Engineering , 2006 .

[34]  M. Kreutzer,et al.  Contact mechanics of highly porous oxide nanoparticle agglomerates , 2016, Journal of Nanoparticle Research.

[35]  R. Assoian,et al.  Growth control by intracellular tension and extracellular stiffness. , 2008, Trends in cell biology.

[36]  N. Forest,et al.  Sequential Expression of Bone Matrix Proteins During Rat Calvaria Osteoblast Differentiation and Bone Nodule Formation In Vitro , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[37]  Alan Hall,et al.  Rho GTPases: biochemistry and biology. , 2005, Annual review of cell and developmental biology.

[38]  Seung Min Yeo,et al.  Micromechanical properties of polymeric coatings , 2013 .

[39]  Taeheon Kang,et al.  Titanium mesh as an alternative to a membrane for ridge augmentation. , 2012, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[40]  J. Wennström,et al.  Clinical characteristics at implants with a history of progressive bone loss. , 2008, Clinical oral implants research.

[41]  Joachim Bill,et al.  Nanomechanical Properties of Bioinspired Organic–Inorganic Composite Films , 2007 .

[42]  J. Granjeiro,et al.  Basic research methods and current trends of dental implant surfaces. , 2009, Journal of biomedical materials research. Part B, Applied biomaterials.

[43]  J. Parsons,et al.  Focal adhesion kinase: the first ten years , 2003, Journal of Cell Science.

[44]  K. Burridge,et al.  Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. , 2000, Experimental cell research.

[45]  P. Branemark,et al.  Osseointegrated titanium fixtures in the treatment of edentulousness. , 1983, Biomaterials.

[46]  Wei Huang,et al.  Signaling and transcriptional regulation in osteoblast commitment and differentiation. , 2007, Frontiers in bioscience : a journal and virtual library.

[47]  Siddharth V. Patwardhan,et al.  Biomimetic and bioinspired silica: recent developments and applications. , 2011, Chemical communications.

[48]  A. Raucci,et al.  Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways , 2008, Journal of cellular physiology.

[49]  J. Morenza,et al.  Characterization of calcium phosphate coatings deposited by Nd:YAG laser ablation at 355 nm: influence of thickness. , 2002, Biomaterials.

[50]  H. Cha,et al.  Cell adhesion biomaterial based on mussel adhesive protein fused with RGD peptide. , 2007, Biomaterials.

[51]  J. García-Ruíz,et al.  Nanostructured Porous Silicon: The Winding Road from Photonics to Cell Scaffolds – A Review , 2015, Front. Bioeng. Biotechnol..

[52]  Bong-Hyuk Choi,et al.  Facile surface functionalization with glycosaminoglycans by direct coating with mussel adhesive protein. , 2012, Tissue engineering. Part C, Methods.

[53]  S. Lorenz,et al.  Self-Assembly of Highly Phosphorylated Silaffins and Their Function in Biosilica Morphogenesis , 2002, Science.

[54]  Richard O. Hynes,et al.  Integrin-mediated Signals Regulated by Members of the Rho Family of GTPases , 1998, The Journal of cell biology.

[55]  Andrés J. García,et al.  Focal adhesion kinase modulates cell adhesion strengthening via integrin activation. , 2009, Molecular biology of the cell.

[56]  J. Pemberton,et al.  Ultrathin silica films immobilized on gold supports: fabrication, characterization, and modification. , 2007, Langmuir.

[57]  C. Becker,et al.  Modified silaffin R5 peptides enable encapsulation and release of cargo molecules from biomimetic silica particles. , 2013, Bioorganic & medicinal chemistry.

[58]  Hyung Joon Cha,et al.  Practical recombinant hybrid mussel bioadhesive fp-151. , 2007, Biomaterials.

[59]  J. Brugge,et al.  Integrins and signal transduction pathways: the road taken. , 1995, Science.

[60]  N. Moody,et al.  Determining fracture toughness of vitreous silica glass , 1995 .