Self-Assembled Peptides: Characterisation and In Vivo Response

The fabrication of tissue engineering scaffolds is a well-established field that has gained recent prominence for the in vivo repair of a variety of tissue types. Recently, increasing levels of sophistication have been engineered into adjuvant scaffolds facilitating the concomitant presentation of a variety of stimuli (both physical and biochemical) to create a range of favourable cellular microenvironments. It is here that self-assembling peptide scaffolds have shown considerable promise as functional biomaterials, as they are not only formed from peptides that are physiologically relevant, but through molecular recognition can offer synergy between the presentation of biochemical and physio-chemical cues. This is achieved through the utilisation of a unique, highly ordered, nano- to microscale 3-D morphology to deliver mechanical and topographical properties to improve, augment or replace physiological function. Here, we will review the structures and forces underpinning the formation of self-assembling scaffolds, and their application in vivo for a variety of tissue types.

[1]  Derek N. Woolfson,et al.  Engineering nanoscale order into a designed protein fiber , 2007, Proceedings of the National Academy of Sciences.

[2]  Derek N. Woolfson,et al.  Engineering Increased Stability into Self‐Assembled Protein Fibers , 2006 .

[3]  I. Hamley,et al.  Hydrogelation and self-assembly of Fmoc-tripeptides: unexpected influence of sequence on self-assembled fibril structure, and hydrogel modulus and anisotropy. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[4]  J. Stendahl,et al.  Intermolecular Forces in the Self‐Assembly of Peptide Amphiphile Nanofibers , 2006 .

[5]  E. Ingham,et al.  The internal dynamic modes of charged self-assembled peptide fibrils. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[6]  Jangwook P. Jung,et al.  Modulating the mechanical properties of self-assembled peptide hydrogels via native chemical ligation. , 2008, Biomaterials.

[7]  A. Mata,et al.  Self-Assembly of Large and Small Molecules into Hierarchically Ordered Sacs and Membranes , 2008, Science.

[8]  J. West,et al.  Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. , 2008, Current topics in medicinal chemistry.

[9]  D. Pochan,et al.  Injectable solid hydrogel: mechanism of shear-thinning and immediate recovery of injectable β-hairpin peptide hydrogels. , 2010, Soft matter.

[10]  Xuebin B. Yang,et al.  Biomimetic self-assembling peptides as injectable scaffolds for hard tissue engineering. , 2006, Nanomedicine.

[11]  E. Furst,et al.  Gelation Kinetics of β-Hairpin Peptide Hydrogel Networks , 2006 .

[12]  Rein V. Ulijn,et al.  Peptide-based stimuli-responsive biomaterials. , 2006, Soft matter.

[13]  Samuel I Stupp,et al.  Heparin binding nanostructures to promote growth of blood vessels. , 2006, Nano letters.

[14]  A. J. Grodzinsky,et al.  Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: Implications for cartilage tissue repair , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  S. Stupp,et al.  Supramolecular Materials: Self-Organized Nanostructures , 1997, Science.

[16]  Bing Xu,et al.  Supramolecular hydrogels respond to ligand-receptor interaction. , 2003, Journal of the American Chemical Society.

[17]  Riccardo Ferracini,et al.  IL-7 Up-Regulates TNF-α-Dependent Osteoclastogenesis in Patients Affected by Solid Tumor , 2006, PloS one.

[18]  Mi Zhou,et al.  Self-assembled peptide-based hydrogels as scaffolds for anchorage-dependent cells. , 2009, Biomaterials.

[19]  Huanxing Su,et al.  Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold. , 2007, Nanomedicine : nanotechnology, biology, and medicine.

[20]  David A Tirrell,et al.  Protein engineering approaches to biomaterials design. , 2005, Current opinion in biotechnology.

[21]  D. Woolfson,et al.  Kinking the coiled coil--negatively charged residues at the coiled-coil interface. , 2007, Journal of molecular biology.

[22]  Valerie M. Weaver,et al.  The extracellular matrix at a glance , 2010, Journal of Cell Science.

[23]  J. Hubbell,et al.  Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering , 2005, Nature Biotechnology.

[24]  Huanxing Su,et al.  Self-assembling peptide nanofiber scaffold promotes the reconstruction of acutely injured brain. , 2009, Nanomedicine : nanotechnology, biology, and medicine.

[25]  Jangwook P. Jung,et al.  Co-assembling peptides as defined matrices for endothelial cells. , 2009, Biomaterials.

[26]  Takatoshi Kinoshita,et al.  Dynamic reassembly of peptide RADA16 nanofiber scaffold. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  I. Hamley,et al.  Hydrogelation of self-assembling RGD-based peptides , 2011 .

[28]  S. Stupp,et al.  Enzyme Directed Templating of Artificial Bone Mineral , 2009, Advanced materials.

[29]  George C Schatz,et al.  Atomistic molecular dynamics simulations of peptide amphiphile self-assembly into cylindrical nanofibers. , 2011, Journal of the American Chemical Society.

[30]  J. H. Kim,et al.  In Vivo Biocompatibility Study of Electrospun Chitosan Microfiber for Tissue Engineering , 2010, International journal of molecular sciences.

[31]  Michael S. Arnold,et al.  Peptide amphiphile nanostructure-heparin interactions and their relationship to bioactivity. , 2008, Biomaterials.

[32]  N. Wagner,et al.  The effect of protein structure on their controlled release from an injectable peptide hydrogel. , 2010, Biomaterials.

[33]  A. Aggeli,et al.  Self-assembly and structure transformations in living polymers forming fibrils , 2000 .

[34]  D. Woolfson,et al.  The non-covalent decoration of self-assembling protein fibers. , 2010, Biomaterials.

[35]  A. Grodzinsky,et al.  Effect of self-assembling peptide, chondrogenic factors, and bone marrow-derived stromal cells on osteochondral repair. , 2010, Osteoarthritis and cartilage.

[36]  Shuguang Zhang,et al.  Design of molecular biological materials using peptide motifs , 2004 .

[37]  M. Horne,et al.  Review Paper: A Review of the Cellular Response on Electrospun Nanofibers for Tissue Engineering , 2009, Journal of biomaterials applications.

[38]  P. Hartley,et al.  The in vivo performance of an enzyme-assisted self-assembled peptide/protein hydrogel. , 2011, Biomaterials.

[39]  Stephen Marshall,et al.  Biocatalytic induction of supramolecular order , 2010, Nature Chemistry.

[40]  Joel H Collier,et al.  Enzymatic modification of self-assembled peptide structures with tissue transglutaminase. , 2003, Bioconjugate chemistry.

[41]  M. Horne,et al.  Implantation of functionalized thermally gelling xyloglucan hydrogel within the brain: associated neurite infiltration and inflammatory response. , 2010, Tissue engineering. Part A.

[42]  D. Pochan,et al.  De novo design of strand-swapped beta-hairpin hydrogels. , 2008, Journal of the American Chemical Society.

[43]  S. Stupp,et al.  Peptide amphiphile nanofibers with conjugated polydiacetylene backbones in their core. , 2008, Journal of the American Chemical Society.

[44]  H. Börner,et al.  A modular approach towards functional decoration of peptide-polymer nanotapes. , 2010, Chemical communications.

[45]  R. Ulijn,et al.  Exploiting biocatalysis in peptide self‐assembly , 2010, Biopolymers.

[46]  C. J. Bell,et al.  Self-assembling peptides as injectable lubricants for osteoarthritis. , 2006, Journal of biomedical materials research. Part A.

[47]  C James Kirkpatrick,et al.  Dynamic in vivo biocompatibility of angiogenic peptide amphiphile nanofibers. , 2009, Biomaterials.

[48]  A. Mata,et al.  Hybrid bone implants: self-assembly of peptide amphiphile nanofibers within porous titanium. , 2008, Biomaterials.

[49]  A. Rich,et al.  Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Y. Chau,et al.  Neural differentiation directed by self-assembling peptide scaffolds presenting laminin-derived epitopes. , 2010, Journal of biomedical materials research. Part A.

[51]  Carlos E Semino,et al.  The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function. , 2005, Biomaterials.

[52]  Matthew Pilarz,et al.  Controlling hydrogelation kinetics by peptide design for three-dimensional encapsulation and injectable delivery of cells , 2007, Proceedings of the National Academy of Sciences.

[53]  J. Hartgerink,et al.  Biomimetic self-assembled nanofibers. , 2006, Soft matter.

[54]  J. Hartgerink,et al.  Enzyme‐Mediated Degradation of Peptide‐Amphiphile Nanofiber Networks , 2005 .

[55]  Samuel I Stupp,et al.  Presentation of RGDS epitopes on self-assembled nanofibers of branched peptide amphiphiles. , 2006, Biomacromolecules.

[56]  Andrew M. Smith,et al.  Fmoc-diphenylalanine self-assembly mechanism induces apparent pKa shifts. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[57]  Derek N Woolfson,et al.  Preferred side-chain constellations at antiparallel coiled-coil interfaces , 2008, Proceedings of the National Academy of Sciences.

[58]  Rein V Ulijn,et al.  Enzyme-triggered self-assembly of peptide hydrogels via reversed hydrolysis. , 2006, Journal of the American Chemical Society.

[59]  Krista L. Niece,et al.  Self-assembly combining two bioactive peptide-amphiphile molecules into nanofibers by electrostatic attraction. , 2003, Journal of the American Chemical Society.

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

[61]  M. Horne,et al.  Interaction of embryonic cortical neurons on nanofibrous scaffolds for neural tissue engineering , 2007, Journal of neural engineering.

[62]  A. Rich,et al.  Self-complementary oligopeptide matrices support mammalian cell attachment. , 1995, Biomaterials.

[63]  Rein V Ulijn,et al.  Enzyme-assisted self-assembly under thermodynamic control. , 2009, Nature nanotechnology.

[64]  Rein V. Ulijn,et al.  Fmoc‐Diphenylalanine Self Assembles to a Hydrogel via a Novel Architecture Based on π–π Interlocked β‐Sheets , 2008 .

[65]  G. Whitesides,et al.  Self-Assembly at All Scales , 2002, Science.

[66]  C. Anfinsen Principles that govern the folding of protein chains. , 1973, Science.

[67]  D. Seliktar,et al.  Self-assembled Fmoc-peptides as a platform for the formation of nanostructures and hydrogels. , 2009, Biomacromolecules.

[68]  M. Wiberg,et al.  BD™ PuraMatrix™ peptide hydrogel seeded with Schwann cells for peripheral nerve regeneration , 2010, Brain Research Bulletin.

[69]  Derek N. Woolfson,et al.  Sticky-end assembly of a designed peptide fiber provides insight into protein fibrillogenesis. , 2000 .

[70]  Kwok-Fai So,et al.  Nano hemostat solution: immediate hemostasis at the nanoscale. , 2006, Nanomedicine : nanotechnology, biology, and medicine.

[71]  Krista L. Niece,et al.  Phase diagram for assembly of biologically-active peptide amphiphiles. , 2008, The journal of physical chemistry. B.

[72]  J. Hartgerink,et al.  Self-assembly of peptide-amphiphile nanofibers: the roles of hydrogen bonding and amphiphilic packing. , 2006, Journal of the American Chemical Society.

[73]  Michael C. Giano,et al.  Controlled biodegradation of self-assembling β-hairpin peptide hydrogels by proteolysis with matrix metalloproteinase-13. , 2011, Biomaterials.

[74]  David A Winkler,et al.  Tripeptide motifs in biology: targets for peptidomimetic design. , 2011, Journal of medicinal chemistry.

[75]  A. Rich,et al.  Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Malcolm K Horne,et al.  Three-dimensional nanofibrous scaffolds incorporating immobilized BDNF promote proliferation and differentiation of cortical neural stem cells. , 2010, Stem cells and development.

[77]  Lisa Pakstis,et al.  Responsive hydrogels from the intramolecular folding and self-assembly of a designed peptide. , 2002, Journal of the American Chemical Society.

[78]  Derek N Woolfson,et al.  Engineering the morphology of a self-assembling protein fibre , 2003, Nature materials.

[79]  Differentiation of mouse embryonic stem cells in self-assembling peptide scaffolds. , 2011, Methods in molecular biology.

[80]  Rutledge Ellis-Behnke,et al.  At the nanoscale: nanohemostat, a new class of hemostatic agent. , 2011, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[81]  Richard T. Lee,et al.  Injectable Self-Assembling Peptide Nanofibers Create Intramyocardial Microenvironments for Endothelial Cells , 2005, Circulation.

[82]  Steve F. A. Acquah,et al.  Polar assembly in a designed protein fiber. , 2004, Angewandte Chemie.

[83]  A. Grodzinsky,et al.  Growth Factor Delivery Through Self-assembling Peptide Scaffolds , 2011, Clinical orthopaedics and related research.

[84]  Andrew M. Smith,et al.  Controlling stiffness in nanostructured hydrogels produced by enzymatic dephosphorylation. , 2009, Biochemical Society transactions.

[85]  G. Schneider,et al.  Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Yadong Wang,et al.  Materials for central nervous system regeneration: bioactive cues , 2011 .

[87]  R. Zhuo,et al.  Peptide hydrogel as an intraocular drug delivery system for inhibition of postoperative scarring formation. , 2010, ACS applied materials & interfaces.

[88]  Robert Langer,et al.  Incorporation of a matrix metalloproteinase-sensitive substrate into self-assembling peptides - a model for biofunctional scaffolds. , 2008, Biomaterials.

[89]  M. Shoichet,et al.  Biomaterials for Brain Tissue Engineering , 2010 .

[90]  Michael G. Fehlings,et al.  Self-Assembling Nanofibers Inhibit Glial Scar Formation and Promote Axon Elongation after Spinal Cord Injury , 2008, The Journal of Neuroscience.

[91]  S. Radford,et al.  Responsive gels formed by the spontaneous self-assembly of peptides into polymeric β-sheet tapes , 1997, Nature.

[92]  Krista L. Niece,et al.  Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers , 2004, Science.

[93]  Bing Xu,et al.  In vitro and in vivo enzymatic formation of supramolecular hydrogels based on self-assembled nanofibers of a beta-amino acid derivative. , 2007, Small.

[94]  Shuguang Zhang Fabrication of novel biomaterials through molecular self-assembly , 2003, Nature Biotechnology.

[95]  Matthias P. Lutolf,et al.  Designing materials to direct stem-cell fate , 2009, Nature.

[96]  M. Horne,et al.  Neural tissue engineering of the CNS using hydrogels. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[97]  A. N. Semenov,et al.  Hierarchical self-assembly of chiral rod-like molecules as a model for peptide β-sheet tapes, ribbons, fibrils, and fibers , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[98]  D. Pochan,et al.  Salt-Triggered Peptide Folding and Consequent Self-Assembly into Hydrogels with Tunable Modulus , 2004 .

[99]  Tomohiro Matsumoto,et al.  Osteogenic Differentiation of Mesenchymal Stem Cells/Polymer Composites with HA In Vitro , 2011 .

[100]  C. Fishwick,et al.  Self-assembling β-Sheet Tape Forming Peptides , 2006 .

[101]  Malcolm K Horne,et al.  Neurite infiltration and cellular response to electrospun polycaprolactone scaffolds implanted into the brain. , 2009, Biomaterials.

[102]  J. Fisher,et al.  Effect of ionic strength on the self-assembly, morphology and gelation of pH responsive β-sheet tape-forming peptides , 2007 .

[103]  Meital Reches,et al.  Formation of Closed-Cage Nanostructures by Self-Assembly of Aromatic Dipeptides , 2004 .

[104]  Samuel I Stupp,et al.  Peptide-amphiphile nanofibers: A versatile scaffold for the preparation of self-assembling materials , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[105]  Meital Reches,et al.  Rigid, Self‐Assembled Hydrogel Composed of a Modified Aromatic Dipeptide , 2006 .