Peptide-Based Stimuli-Responsive Biomaterials

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Peptide-Based Stimuli-Responsive Biomaterials View Article Online / Journal Homepage / Table of Contents for this issue REVIEW www.rsc.org/softmatter | Soft Matter Peptide-based stimuli-responsive biomaterials Robert J. Mart,a Rachel D. Osborne,b Molly M. Stevens*b and Rein V. Ulijn*a Received 31st May 2006, Accepted 31st July 2006 First published as an Advance Article on the web 25th August 2006 DOI: 10.1039/b607706d This article explores recent advances in the design and engineering of materials wholly or principally constructed from peptides. We focus on materials that are able to respond to changes in their environment (pH, ionic strength, temperature, light, oxidation/reduction state, presence of small molecules or the catalytic activity of enzymes) by altering their macromolecular structure. Such peptide-based responsive biomaterials have exciting prospects for a variety of biomedical and bionanotechnology applications in drug delivery, bio-sensing and regenerative medicine. 1. Introduction biomedical applications. For example, physical or chemical hydrogels loaded with drug molecules may release their Materials that change properties in response to local environ- payload, only when and where required, in response to mental stimuli are increasingly being studied in the context of changes in the local environmental conditions, such as pH, temperature, presence of small molecules or enzymes, and oxidising/reducing environment, among others.1 Another key aSchool of Materials and Manchester Interdisciplinary Biocentre (MIB), Grosvenor Street, Manchester, UK M1 7HS. application is injectable gels for minimal invasive surgery. E-mail: [email protected]; Fax: +44 161 3068877; These materials may be applied through a syringe, and Tel: +44 161 3065986 undergo a solution-to-gel transition when triggered by b Department of Materials and Institute for Biomedical Engineering, temperature, pH, ionic strength, oxidative species or enzymes Imperial College of Science, Technology and Medicine, Prince Consort Road, London, UK SW7 2AZ. E-mail: [email protected]; at the site of injury to act as a scaffold for tissue regrowth. A Fax: +44 20 7594 6757; Tel: +44 20 7594 6804 third area is in bio-sensing, where small chemical or physical Robert Mart received a Rachel Osborne read for a Masters degree from UMIST, Masters in Materials, before completing a PhD on Economics and Management asymmetric organic catalysis of at Oxford University before the Morita-Baylis–Hillman spending a year as a reaction with Dr D. J. Marketing Co-ordinator for Berrisford. He then spent a L’Occitane in New York. Published on 25 August 2006. Downloaded by University of California - Santa Barbara 03/02/2016 22:03:39. year as a postdoctoral research Despite all the free lunches associate with Dr S. J. Webb in she wanted to pursue science the newly created University of and under the direction of Dr Manchester studying vesicle– M. M. Stevens she is currently vesicle interactions before join- undertaking a PhD looking at ing the Ulijn group where he the bio-functionalization of synthesises enzyme responsive gold nanoparticles at Imperial Robert Mart biomaterials. Rachel Osborne College, London. Molly Stevens received her Rein Ulijn received his Masters PhD from The University of from Wageningen University, Nottingham and spent 2.5 years PhD from The University of as a postdoctoral researcher at Strathclyde and spent 2 years MIT. She is currently a reader as a postdoctoral researcher at at Imperial College London. the University of Edinburgh. She has recently been recog- He is currently an advanced nised by Technology Review’s research fellow and senior TR100 Young Innovators lecturer in biomedical Award (2004) and the Philip materials at the University of Leverhulme Prize for Manchester. His research is Engineering (2005) for her interdisciplinary and focuses research in regenerative medi- on the design, characterisation cine and nanotechnology. and application of responsive Molly Stevens Rein Ulijn molecular biomaterials. 822 | Soft Matter, 2006, 2, 822–835 This journal is ß The Royal Society of Chemistry 2006 View Article Online changes in the sensing environment trigger macroscopically amino acids), hydrophobic, p-stacking (aromatic amino acids), observable changes in material properties, thereby reporting hydrogen bonding (polar amino acids) as well as covalent them, for example by gelation or nanoparticle (dis)-assembly. (disulfide) bonds and steric contributions (strand directing These responsive biomaterials contain molecular building amino acids). While individually these interactions are quite blocks that undergo molecular level changes which result in weak (see Fig. 1), collectively they can give rise to very stable altered non-covalent interactions that, in turn, translate into structures. Crucially, each of these interactions depend in macroscopic responses. different ways on environmental conditions such as ionic In this Review Article, we focus on recent (since 2000) strength, pH and temperature. In addition, specific short reports on responsive biomaterials that use peptides as their peptide sequences can introduce responsiveness via small stimuli-responsive elements. Peptides are ideally suited for this molecule recognition. Enzyme responsiveness can be pro- purpose because of the range of distinct physical properties grammed into these materials by incorporation of peptide available from the naturally occurring amino acids (Fig. 1). sequences that are known substrates for proteases, kinases, or This diversity allows for rational incorporation of non- phosphatases.1n The dynamic nature of these interactions then covalent interactions including electrostatic (acidic and basic allows the molecular organisation to be altered in response to Published on 25 August 2006. Downloaded by University of California - Santa Barbara 03/02/2016 22:03:39. Fig. 1 Schematic descriptions of different classes of amino acids and the types of peptide interactions they are involved in. This journal is ß The Royal Society of Chemistry 2006 Soft Matter, 2006, 2, 822–835 | 823 View Article Online changes in the direct environment. Each type of interaction has dichroism shows that, as expected, the trans to cis photo- different requirements, for example hydrogen bonding requires isomerism of the azobenzene linker increases the a-helical precisely positioned and directed residues with the donor and content for the i, i + 4 and i, i + 7 peptides as the over-long acceptor approximately 2.8 A˚ apart. p–p stacking interactions cross-linking molecule is effectively shortened. Conversely, require the overlap of two p systems approximately 3.4 A˚ there is a decrease in the a-helical content for the i, i +11 apart. In contrast, electrostatic interactions are generally not peptide as the cross-linker becomes too short to permit ready directional and tend to be more flexible regarding the distance helix formation. between the participating charges, although this depends An important a-helix based quaternary structure of peptides strongly on the ionic strength of the solution. Hydrophobic is the coiled-coil. Characterised by two or more a-helices interactions are even less geometrically constrained. In nature, organised into a supercoil, each peptide length contains a 3, 4 responsive peptide based materials, for example, enzymes heptad motif repeat (abcdefg). The interhelical interactions and motor-proteins, use a combination of these individually are captured by pairwise interactions by four key positions; weak interactions, which work cooperatively to dynamically a, d, e, g (see top panel, Fig. 2). Hydrophobic residues found at organise the secondary, tertiary and quaternary structures of positions a and d form the hydrophobic core of a coiled-coil. proteins. Positions e and g are either side of the hydrophobic core and It is a major challenge for scientists and engineers to can participate in electrostatic interhelical contacts and also incorporate these design concepts into useful peptide based alter core hydrophobicity. Changing the nature of these materials and devices. The following sections examine contacts by introducing responsive amino acids can alter the strategies which involve the design of a peptide macro- stability of the conformation and provide a mechanism for monomer consisting of a primary sequence that is either control of dynamic materials. amphiphilic or forms a known secondary structural motif The use of acidic and basic amino acids that can be (a-helix, b-sheet, b-turn, elastin-like sequence), in which protonated or deprotonated by a change in pH allows dynamic responsive elements are rationally incorporated. control over the secondary structure of the peptides and can be Macroscopically observed transitions in response to external used to control the assembly of coiled-coils. For example, a stimuli are then achieved by further quaternary interactions coiled-coil a-helix with leucine at position d and glutamic between individual peptides. The resulting switchable assem- acid residues at positions e and g (Table 1, entry 2) forms blies may take the shape of nanometre sized fibres, spheres homodimeric coiled-coils which are destabilised in basic or tubes (consisting of superhelices, coiled-coils, amphiphilic solutions.3 This leucine zipper amino acid sequence was assemblies such as micelles). In other examples, peptide covalently bonded to a gold-substrate via the formation of a motifs are used as responsive elements in multi component gold–thiolate bond to form a monolayer. An extended version
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