Self‐Assembling Peptides as Cell‐Interactive Scaffolds

Cell and tissue engineering therapies for regenerative medicine as well as cell-based assays require an understanding of the interactions between cells with the surrounding microenvironment at the nanoscale. Engineering a cell-interactive scaffold therefore entails control over the nanostructure of the biomaterial. Peptides that are able to self-assemble into 3D scaffolds have emerged as interesting biomaterials for directing cell behavior, with desirable properties such as the capability of tuning the nanostructure by modulating the amino acid composition. Here, an overview of the development of self-assembling peptide hydrogels as functional cell scaffolds is presented, highlighting recent work on incorporating features such as bioactive ligands, growth factor delivery, controlled degradation, and formulation into microgels for defined cell microenvironments.

[1]  S. Radford,et al.  pH as a trigger of peptide beta-sheet self-assembly and reversible switching between nematic and isotropic phases. , 2003, Journal of the American Chemical Society.

[2]  R. C. Dutta,et al.  Comprehension of ECM-cell dynamics: a prerequisite for tissue regeneration. , 2010, Biotechnology advances.

[3]  Richard T. Lee,et al.  Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Fabrizio Gelain,et al.  Biological Designer Self-Assembling Peptide Nanofiber Scaffolds Significantly Enhance Osteoblast Proliferation, Differentiation and 3-D Migration , 2007, PloS one.

[5]  A. G. Fadeev,et al.  Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells , 2010, Nature Biotechnology.

[6]  Fabrizio Gelain,et al.  Designer Self-Assembling Peptide Nanofiber Scaffolds for Adult Mouse Neural Stem Cell 3-Dimensional Cultures , 2006, PloS one.

[7]  J. Collier,et al.  Fibrillized peptide microgels for cell encapsulation and 3D cell culture. , 2011, Soft matter.

[8]  W. Hennink,et al.  In situ gelling hydrogels for pharmaceutical and biomedical applications. , 2008, International journal of pharmaceutics.

[9]  J. Schneider,et al.  Self-assembling peptides and proteins for nanotechnological applications. , 2004, Current opinion in structural biology.

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

[11]  Ranjna C Dutta,et al.  Cell-interactive 3D-scaffold; advances and applications. , 2009, Biotechnology advances.

[12]  D. Pochan,et al.  In vitro assessment of the pro-inflammatory potential of beta-hairpin peptide hydrogels. , 2008, Biomaterials.

[13]  Joel L Berry,et al.  A hybrid biomimetic nanomatrix composed of electrospun polycaprolactone and bioactive peptide amphiphiles for cardiovascular implants. , 2011, Acta biomaterialia.

[14]  Jangwook P. Jung,et al.  Fibrillar peptide gels in biotechnology and biomedicine , 2010, Biopolymers.

[15]  Fabrizio Gelain,et al.  Slow and sustained release of active cytokines from self-assembling peptide scaffolds. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

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

[17]  Qixin Zheng,et al.  Biocompatibility of KLD-12 peptide hydrogel as a scaffold in tissue engineering of intervertebral discs in rabbits , 2010, Journal of Huazhong University of Science and Technology. Medical sciences = Hua zhong ke ji da xue xue bao. Yi xue Ying De wen ban = Huazhong keji daxue xuebao. Yixue Yingdewen ban.

[18]  P. Menasché Cellular transplantation: hurdles remaining before widespread clinical use , 2004, Current opinion in cardiology.

[19]  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.

[20]  A. Khademhosseini,et al.  Hydrogels in Regenerative Medicine , 2009, Advanced materials.

[21]  Andrea Bagno,et al.  Electrospun scaffolds of self-assembling peptides with poly(ethylene oxide) for bone tissue engineering. , 2011, Acta biomaterialia.

[22]  Toshifumi Ozaki,et al.  PuraMatrix™ Facilitates Bone Regeneration in Bone Defects of Calvaria in Mice. , 2006, Cell transplantation.

[23]  Shoji Takeuchi,et al.  Monodisperse cell-encapsulating peptide microgel beads for 3D cell culture. , 2010, Langmuir : the ACS journal of surfaces and colloids.

[24]  T. Mamo,et al.  Amino Acid Pairing for De Novo Design of Self‐Assembling Peptides and Their Drug Delivery Potential , 2011 .

[25]  Gottfried Schmalz,et al.  Self-assembling peptide amphiphile nanofibers as a scaffold for dental stem cells. , 2008, Tissue engineering. Part A.

[26]  S. Doglia,et al.  BMHP1-derived self-assembling peptides: hierarchically assembled structures with self-healing propensity and potential for tissue engineering applications. , 2011, ACS nano.

[27]  Jaesoon Choi,et al.  The enhancement of mature vessel formation and cardiac function in infarcted hearts using dual growth factor delivery with self-assembling peptides. , 2011, Biomaterials.

[28]  Xuejun Wen,et al.  Polymer nanofibrous structures: Fabrication, biofunctionalization, and cell interactions. , 2010, Progress in polymer science.

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

[30]  Hisatoshi Kobayashi,et al.  Osteogenic differentiation of mesenchymal stem cells in self-assembled peptide-amphiphile nanofibers. , 2006, Biomaterials.

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

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

[33]  Rena N. D'Souza,et al.  Self-assembling multidomain peptide hydrogels: designed susceptibility to enzymatic cleavage allows enhanced cell migration and spreading. , 2010, Journal of the American Chemical Society.

[34]  A. Grodzinsky,et al.  Controlled delivery of transforming growth factor β1 by self-assembling peptide hydrogels induces chondrogenesis of bone marrow stromal cells and modulates Smad2/3 signaling. , 2011, Tissue engineering. Part A.

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

[36]  H. Kong,et al.  The interplay between cell adhesion cues and curvature of cell adherent alginate microgels in multipotent stem cell culture. , 2011, Tissue engineering. Part A.

[37]  Glenn D Prestwich,et al.  Simplifying the extracellular matrix for 3‐D cell culture and tissue engineering: A pragmatic approach , 2007, Journal of cellular biochemistry.

[38]  Larisa C Wu,et al.  Hybrid hydrogels self-assembled from graft copolymers containing complementary β-sheets as hydroxyapatite nucleation scaffolds. , 2011, Biomaterials.

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

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

[41]  M. McPherson,et al.  Recombinant self-assembling peptides as biomaterials for tissue engineering , 2010, Biomaterials.

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

[43]  H. Wadley,et al.  The limits of solid state foaming , 2001 .

[44]  Shuguang Zhang,et al.  Functionalized scaffolds of shorter self-assembling peptides containing MMP-2 cleavable motif promote fibroblast proliferation and significantly accelerate 3-D cell migration independent of scaffold stiffness , 2010 .

[45]  F. Albericio,et al.  Amphiphilic peptides and their cross-disciplinary role as building blocks for nanoscience. , 2010, Chemical Society reviews.

[46]  Richard B. Sessions,et al.  Designed alpha-helical tectons for constructing multicomponent synthetic biological systems. , 2009, Journal of the American Chemical Society.

[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]  Long Zhao,et al.  Support of human adipose-derived mesenchymal stem cell multipotency by a poloxamer-octapeptide hybrid hydrogel. , 2010, Biomaterials.

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

[51]  Shuguang Zhang,et al.  Significant Type I and Type III Collagen Production from Human Periodontal Ligament Fibroblasts in 3D Peptide Scaffolds without Extra Growth Factors , 2010, PloS one.

[52]  Ali Khademhosseini,et al.  Interface-directed self-assembly of cell-laden microgels. , 2010, Small.

[53]  Shuguang Zhang,et al.  Designer self-assembling peptide nanofiber biological materials. , 2010, Chemical Society reviews.

[54]  R. Lal,et al.  Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. , 2011, Biomaterials.

[55]  S. Stupp,et al.  Regeneration of the cavernous nerve by Sonic hedgehog using aligned peptide amphiphile nanofibers. , 2011, Biomaterials.

[56]  David J. Mooney,et al.  Growth Factors, Matrices, and Forces Combine and Control Stem Cells , 2009, Science.

[57]  Zahra N Mahmoud,et al.  Bioorthogonal dual functionalization of self-assembling peptide fibers. , 2011, Biomaterials.

[58]  Yihua Loo,et al.  Natural tri- to hexapeptides self-assemble in water to amyloid β-type fiber aggregates by unexpected α-helical intermediate structures , 2011, Proceedings of the National Academy of Sciences.

[59]  Honggang Cui,et al.  Self‐assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials , 2010, Biopolymers.

[60]  S. Stupp,et al.  Self-assembling nanostructures to deliver angiogenic factors to pancreatic islets. , 2010, Biomaterials.

[61]  I. Hamachi,et al.  Rational Molecular Design of Stimulus‐Responsive Supramolecular Hydrogels Based on Dipeptides , 2011, Advanced materials.

[62]  Jennifer A. Craig,et al.  Self-assembly and applications of biomimetic and bioactive peptide-amphiphiles. , 2006, Soft matter.

[63]  Ali Khademhosseini,et al.  Nanoscale tissue engineering: spatial control over cell-materials interactions , 2011, Nanotechnology.

[64]  Eileen Ingham,et al.  Production of self-assembling biomaterials for tissue engineering , 2009, Trends in biotechnology.

[65]  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.

[66]  L. Lock,et al.  Stem/Progenitor cell sources of insulin-producing cells for the treatment of diabetes. , 2007, Tissue engineering.

[67]  Yihua Loo,et al.  Ultrasmall natural peptides self-assemble to strong temperature-resistant helical fibers in scaffolds suitable for tissue engineering , 2011 .

[68]  S. Stupp,et al.  Interfacial self-assembly of cell-like filamentous microcapsules. , 2011, Angewandte Chemie.

[69]  D. Hao,et al.  Compatibility of neural stem cells with functionalized self-assembling peptide scaffold in vitro , 2010 .

[70]  C T Laurencin,et al.  Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system. , 2001, Journal of biomedical materials research.

[71]  E. Bakota,et al.  Injectable multidomain peptide nanofiber hydrogel as a delivery agent for stem cell secretome. , 2011, Biomacromolecules.

[72]  J. Lu,et al.  Molecular self-assembly and applications of designer peptide amphiphiles. , 2010, Chemical Society reviews.

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

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

[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]  Qixin Zheng,et al.  Culture of nucleus pulposus cells from intervertebral disc on self-assembling KLD-12 peptide hydrogel scaffold , 2010 .

[77]  Ali Khademhosseini,et al.  Bioinspired materials for controlling stem cell fate. , 2010, Accounts of chemical research.

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

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

[80]  Derek N. Woolfson,et al.  Rational design and application of responsive α-helical peptide hydrogels , 2009, Nature materials.

[81]  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.

[82]  Stuart R Stock,et al.  Bone regeneration mediated by biomimetic mineralization of a nanofiber matrix. , 2010, Biomaterials.

[83]  R. Shah,et al.  Supramolecular design of self-assembling nanofibers for cartilage regeneration , 2010, Proceedings of the National Academy of Sciences of the United States of America.

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

[85]  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.

[86]  R. Bitton,et al.  A bioactive self-assembled membrane to promote angiogenesis. , 2011, Biomaterials.

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

[88]  Robin A Felder,et al.  3D cell culture opens new dimensions in cell-based assays. , 2009, Drug discovery today.

[89]  Y. Hosaka,et al.  Construction of synthetic dermis and skin based on a self-assembled peptide hydrogel scaffold. , 2009, Tissue engineering. Part A.

[90]  J. Vacanti,et al.  Engineering extracellular matrix through nanotechnology , 2010, Journal of The Royal Society Interface.

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

[92]  Samuel I. Stupp,et al.  A Self-Assembly Pathway to Aligned Monodomain Gels , 2010, Nature materials.

[93]  Xiaojun Zhao,et al.  A 3D model of ovarian cancer cell lines on peptide nanofiber scaffold to explore the cell–scaffold interaction and chemotherapeutic resistance of anticancer drugs , 2011, International journal of nanomedicine.

[94]  Zhang Shuguang,et al.  Designer self-assembling peptide nanomaterials , 2009 .

[95]  A. Cohen,et al.  Spectroscopy in sculpted fields , 2009 .