Mineralized self-assembled peptides on 3D laser-made scaffolds: a new route toward ‘scaffold on scaffold’ hard tissue engineering

In this study, we propose a new approach to hard tissue regeneration based on the mineralization of 3D scaffolds made using lasers. To this end, we report the rational design of aspartate-containing self-assembling peptides targeted for calcium binding. We further investigate the suitability of these peptides to support cell attachment and proliferation when coupled on a hybrid organic-inorganic structurable material, and evaluate the response of pre-osteoblastic cells on functionalized 3D scaffolds and material surfaces. Our results show that the mineralized peptide, when immobilized on a hybrid photo-structurable material strongly supports cell adhesion, a proliferation increase after three and seven days in culture, and exhibits a statistically significant increase of biomineralization. We propose this strategy as a 'scaffold on scaffold' approach for hard tissue regeneration.

[1]  Ashutosh Chilkoti,et al.  Peptide-based Biopolymers in Biomedicine and Biotechnology. , 2008, Materials science & engineering. R, Reports : a review journal.

[2]  Bin Duan,et al.  Selective laser sintering and its application in biomedical engineering , 2011 .

[3]  Phanourios Tamamis,et al.  Amyloid-like self-assembly of peptide sequences from the adenovirus fiber shaft: insights from molecular dynamics simulations. , 2009, The journal of physical chemistry. B.

[4]  J. Rodríguez‐Cabello,et al.  “Recombinamers” as advanced materials for the post-oil age , 2009 .

[5]  R. Yukna,et al.  Bone and bone substitutes. , 1999, Periodontology 2000.

[6]  S. Mann.  Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry , 2002 .

[7]  S. Hollister.  Porous scaffold design for tissue engineering , 2005, Nature materials.

[8]  Ehud Gazit,et al.  Design of metal‐binding sites onto self‐assembled peptide fibrils , 2009, Biopolymers.

[9]  A. Khademhosseini,et al.  Microscale technologies for tissue engineering and biology. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Theodore S. Drakakis,et al.  Construction of three-dimensional biomolecule structures employing femtosecond lasers , 2006 .

[11]  V. Trevor Forsyth,et al.  Amyloid Fibril Formation from Sequences of a Natural β-Structured Fibrous Protein, the Adenovirus Fiber* , 2005, Journal of Biological Chemistry.

[12]  L. Komuves,et al.  Expression and Signal Transduction of Calcium-Sensing Receptors in Cartilage and Bone1. , 1999, Endocrinology.

[13]  L. Serpell,et al.  X-ray fiber diffraction of amyloid fibrils. , 1999, Methods in enzymology.

[14]  Shuguang Zhang,et al.  Designer Self-Assembling Peptide Nanofiber Biological Materials , 2010 .

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

[16]  Costas Fotakis,et al.  Directed three-dimensional patterning of self-assembled peptide fibrils. , 2008, Nano letters.

[17]  David L Kaplan,et al.  Natural and Genetically Engineered Proteins for Tissue Engineering. , 2012, Progress in polymer science.

[18]  E. Brown,et al.  Extracellular calcium-sensing-receptor (CaR)-mediated opening of an outward K(+) channel in murine MC3T3-E1 osteoblastic cells: evidence for expression of a functional CaR. , 2000, Bone.

[19]  D. Prockop,et al.  An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. , 2004, Analytical biochemistry.

[20]  F. Hughes,et al.  The effects of bone morphogenetic protein-2, -4, and -6 on differentiation of rat osteoblast cells in vitro. , 1995, Endocrinology.

[21]  Fabrizio Gelain,et al.  Designer self-assembling peptide scaffolds for 3-d tissue cell cultures and regenerative medicine. , 2007, Macromolecular bioscience.

[22]  F. Melchels,et al.  A review on stereolithography and its applications in biomedical engineering. , 2010, Biomaterials.

[23]  Harald Giessen,et al.  Three‐Dimensional Bichiral Plasmonic Crystals Fabricated by Direct Laser Writing and Electroless Silver Plating , 2011, Advanced materials.

[24]  C. Charitidis,et al.  Pre-osteoblastic cell response on three-dimensional, organic-inorganic hybrid material scaffolds for bone tissue engineering. , 2013, Journal of biomedical materials research. Part A.

[25]  A. Boskey,et al.  Mineralization of Bones and Teeth , 2007 .

[26]  John T. Fourkas,et al.  Cover Picture: Multiphoton Fabrication (Angew. Chem. Int. Ed. 33/2007) , 2007 .

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

[28]  M. Vamvakaki,et al.  Metal Nanocrystals Embedded within Polymeric Nanostructures: Effect of Polymer-Metal Compound Interactions , 2009 .

[29]  D. Hutmacher,et al.  Scaffolds in tissue engineering bone and cartilage. , 2000, Biomaterials.

[30]  Ehud Gazit,et al.  Self‐Assembled Peptide Nanostructures: The Design of Molecular Building Blocks and Their Technological Utilization , 2007 .

[31]  S. Weiner,et al.  Control and Design Principles in Biological Mineralization , 1992 .

[32]  Kurt Busch,et al.  Three‐Dimensional Nanostructures for Photonics , 2010 .

[33]  Arnold Gillner,et al.  Fabrication of 2D protein microstructures and 3D polymer–protein hybrid microstructures by two-photon polymerization , 2011, Biofabrication.

[34]  E. Ogata,et al.  Inhibition ofin vitro mineralization by aluminum in a clonal osteoblastlike cell line, MC3T3-E1 , 1986, Calcified Tissue International.

[35]  H. Jennissen,et al.  Peri-implant reactivity and osteoinductive potential of immobilized rhBMP-2 on titanium carriers. , 2010, Acta biomaterialia.

[36]  R. Osellame,et al.  Integrated three-dimensional filter separates nanoscale from microscale elements in a microfluidic chip. , 2012, Lab on a chip.

[37]  S. Stupp,et al.  Self-Assembly and Mineralization of Peptide-Amphiphile Nanofibers , 2001, Science.

[38]  C. Fotakis,et al.  Pico- and femtosecond laser-induced crosslinking of protein microstructures: evaluation of processability and bioactivity , 2011, Biofabrication.

[39]  D. Talham.  Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry Stephen Mann. Oxford University Press, New York, 2001. , 2002 .

[40]  Steve Weiner,et al.  Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. , 2006, Journal of structural biology.

[41]  Samuel I. Stupp,et al.  Biomimetic Systems for Hydroxyapatite Mineralization Inspired by Bone and Enamel , 2009 .

[42]  J. Schneider,et al.  Self assembled bi-functional peptide hydrogels with biomineralization-directing peptides. , 2010, Biomaterials.

[43]  A. Aggeli,et al.  Self-assembling Peptide Scaffolds Promote Enamel Remineralization , 2007, Journal of dental research.

[44]  A. Mitraki,et al.  Silica biotemplating by self‐assembling peptides via serine residues activated by the peptide amino terminal group , 2012, Biopolymers.

[45]  A Ranella,et al.  Direct laser writing of 3D scaffolds for neural tissue engineering applications , 2011, Biofabrication.

[46]  Tommaso Baldacchini,et al.  Multiphoton fabrication. , 2007, Angewandte Chemie.

[47]  G. Arlaud,et al.  A peptide from the adenovirus fiber shaft forms amyloid‐type fibrils , 2000, FEBS letters.

[48]  C M Stanford,et al.  Rapidly Forming Apatitic Mineral in an Osteoblastic Cell Line (UMR 10601 BSP) (*) , 1995, The Journal of Biological Chemistry.

[49]  M. R. Nilsson.  Techniques to study amyloid fibril formation in vitro. , 2004, Methods.

[50]  Thomas Scheibel,et al.  Recombinant spider silk proteins for applications in biomaterials. , 2010, Macromolecular bioscience.

[51]  L. Komuves,et al.  Expression and signal transduction of calcium-sensing receptors in cartilage and bone. , 1999, Endocrinology.

[52]  D. Riccardi,et al.  Ca2+ as an extracellular signal in bone. , 2004, Cell calcium.

[53]  Struther Arnott,et al.  New CCP13 software and the strategy behind further developments: stripping and modelling of fibre diffraction data , 2003 .

[54]  Pierre Weiss,et al.  Behaviour of mesenchymal stem cells, fibroblasts and osteoblasts on smooth surfaces. , 2011, Acta biomaterialia.

[55]  K. Shakesheff,et al.  Three‐Dimensional Bioactive and Biodegradable Scaffolds Fabricated by Surface‐Selective Laser Sintering , 2005, Advanced materials.

[56]  Aleksandr Ovsianikov,et al.  Engineering 3D cell-culture matrices: multiphoton processing technologies for biological and tissue engineering applications , 2012, Expert review of medical devices.