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From Infection to Healing: the Use of Plant Viruses in Bioactive Hydrogels

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From Infection to Healing: the Use of Plant Viruses in Bioactive Hydrogels Received: 4 February 2020 Revised: 8 June 2020 Accepted: 23 June 2020 DOI: 10.1002/wnan.1662 ADVANCED REVIEW From infection to healing: The use of plant viruses in bioactive hydrogels Christina Dickmeis | Louisa Kauth | Ulrich Commandeur Institute for Molecular Biotechnology, RWTH Aachen University, Aachen, Abstract Germany Plant viruses show great diversity in shape and size, but each species forms unique nucleoprotein particles that are symmetrical and monodisperse. The Correspondence Christina Dickmeis, Institute for genetically programed structure of plant viruses allows them to be modified by Molecular Biotechnology, RWTH Aachen genetic engineering, bioconjugation, or encapsulation to form virus University, Aachen, Germany. nanoparticles (VNPs) that are suitable for a broad range of applications. Plant Email: christina.dickmeis@molbiotech. rwth-aachen.de VNPs can be used to present foreign proteins or epitopes, to construct inor- ganic hybrid materials, or to carry molecular cargos, allowing their utilization Funding information as imaging reagents, immunomodulators, therapeutics, nanoreactors, and bio- Deutsche Forschungsgemeinschaft, Grant/ Award Number: 654127; RWTH Aachen sensors. The medical applications of plant viruses benefit from their inability University to infect and replicate in human cells. The structural properties of plant viruses also make them useful as components of hydrogels for tissue engineering. Hydrogels are three-dimensional networks composed of hydrophilic polymers that can absorb large amounts of water. They are used as supports for tissue regeneration, as reservoirs for controlled drug release, and are found in contact lenses, many wound healing materials, and hygiene products. They are also useful in ecological applications such as wastewater treatment. Hydrogel-based matrices are structurally similar to the native extracellular matrix (ECM) and provide a scaffold for the attachment of cells. To fully replicate the functions of the ECM it is necessary to augment hydrogels with biological cues that regu- late cellular interactions. This can be achieved by incorporating functionalized VNPs displaying ligands that influence the mechanical characteristics of hydrogels and their biological properties, promoting the survival, proliferation, migration, and differentiation of embedded cells. This article is categorized under: Implantable Materials and Surgical Technologies > Nanomaterials and Implants Biology-Inspired Nanomaterials > Protein and Virus-Based Structures Implantable Materials and Surgical Technologies > Nanotechnology in Tissue Repair and Replacement This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. WIREs Nanomedicine and Nanobiotechnology published by Wiley Periodicals LLC. WIREs Nanomed Nanobiotechnol. 2020;e1662. wires.wiley.com/nanomed 1of32 https://doi.org/10.1002/wnan.1662 2of32 DICKMEIS ET AL. KEYWORDS hydrogels, nanoparticles, plant viruses, tissue engineering 1 | INTRODUCTION Virus nanoparticles (VNPs) are nanomaterials based on augmented natural viruses. They have many advantages for applications in the biomedical and material sciences, including their uniformity and versatility. VNPs are uniform because they are genetically encoded, therefore the particles are identical, symmetrical, and monodisperse. They are versatile because they can be functionalized by genetic engineering, bioconjugation, and/or encapsulation. VNPs based on plant viruses have the added advantages of safety and inexpensive production. Most plant-based food products con- tain plant viruses (Latham & Wilson, 2008; Lesemann & Winter, 2002; Rochow, 1972) and some species are even propa- gated in fog and clouds (Castello et al., 1995) and in cigarettes (Liu, Vaishnav, Roberts, & Friedland, 2013; Wetter, 1975). People are exposed to plant viruses constantly but are never infected. The corresponding VNPs are also noninfectious, and because they are nucleoprotein structures they are also biocompatible and biodegradable (Czapar et al., 2016; van Kan-Davelaar, van Hest, Cornelissen, & Koay, 2014). Plant VNPs are inexpensive to produce because, like the native virus, they replicate naturally in plants. VNPs produced in plants may carry plant glycans (Lomonossoff & D'Aoust, 2016; Sack, Hofbauer, Fischer, & Stoger, 2015). If this is undesirable, specialized plant lines are available that have been engineered to eliminate plant glycans or produce oligosaccharides similar to those synthesized in human cells (Schoberer & Strasser, 2018). Based on these advantages, plant VNPs have been used to develop inorganic hybrid materials (Lee, Lim, & Harris, 2012; Wen & Steinmetz, 2016) and modified to carry drugs, contrast and imaging reagents, immunomodulators, enzymes, and biosensors (Chen, Butler, Chen, & Suh, 2019; Cormode, Jarzyna, Mulder, & Fayad, 2010; Koudelka, Pitek, Manchester, & Steinmetz, 2015; Lam & Steinmetz, 2018; Manchester & Singh, 2006; Wen & Steinmetz, 2016; Wu, Wu, Nakagawa, & Gao, 2019; Young, Debbie, Uchida, & Douglas, 2008). The programma- bility of viruses allows their use as targeted drug delivery vehicles. Some plant VNPs have a natural tendency to accu- mulate in tumors, a property influenced by the particle shape and distribution of surface charges, which affect the enhanced permeability and retention effect (Lee et al., 2013; Shukla et al., 2015). Targeting can also be engineered by modifying the surface charge and chemistry or by adding specific targeting peptides or shielding molecules such as polyethylene glycol (PEG) (Pitek, Wen, Shukla, & Steinmetz, 2016). For example, new forms of cancer therapy have been developed based on potato virus X (PVX) modified to deliver doxorubicin (Le, Lee, Shukla, Commandeur, & Stein- metz, 2017) and tobacco mosaic virus (TMV) modified to deliver phenanthriplatin (Czapar et al., 2016). The capsids pro- vide a scaffold that can simultaneously encapsulate drugs while presenting targeting ligands on the external surface (Hovlid et al., 2014). Capsids can also be used to encapsulate imaging reagents or to display them externally. For exam- ple, PVX particles displaying fluorescent markers such as mCherry or green fluorescent protein have been used for imaging in plants, preclinical animal models, and human cells (Shukla et al., 2014). Many of the advantages of plant viruses are shared by bacteriophages, but the latter are contaminated with lipopolysaccharides when produced in bacte- ria, and additional purification steps are thus needed during downstream processing (Szermer-Olearnik & Boratynski, 2015). The well-defined structures of plant VNPs make them particularly suitable for tissue-engineering applications, pro- viding an alternative strategy where there is a lack of donor tissue or a risk of rejection after implantation. Hydrogels are colloidal gels in which a liquid is dispersed in a three-dimensional (3D) network of hydrophilic polymer chains, all- owing the adsorption of large quantities of water or biological fluids (El-Sherbiny & Yacoub, 2013). This contrasts with other colloidal gels in which the liquid is dispersed among solid particles. Hydrogels can be used to support organs or tissue implants, or as a matrix to embed cells for the regrowth of tissues de novo (El-Sherbiny & Yacoub, 2013). They can also be developed as controlled drug-release systems (Kim, Lee, et al., 2015; Merino, Martín, Kostarelos, Prato, & Vázquez, 2015), wound healing materials (Gupta, Agarwal, & Alam, 2011), superabsorbent materials for hygiene prod- ucts such as diapers (Zohuriaan-Mehr, Omidian, Doroudiani, & Kabiri, 2010), and the filling of contact lenses (Michalek, Hobzova, Pradny, & Duskova, 2010). They have also been used in agriculture (Abobatta, 2018) and for wastewater treatment (Ali Shah & Ali Khan, 2019). The construction of hydrogels has been comprehensively reviewed by Mantha et al. (2019). In tissue engineering, hydrogels provide a support scaffold for implanted cells and therefore mimic the mechanical properties of the extracellular matrix (ECM). However, to support tissue regeneration they must also provide the appropriate biological signals that control cell behavior (Luckanagul et al., 2012). Bioactive scaffolds DICKMEIS ET AL. 3of32 can be developed by incorporating plant VNPs into hydrogels, allowing the presentation of peptides that promote cell proliferation, adhesion, migration, or differentiation. A recent review covering plant virus-based materials for biomedi- cal applications included a brief description of VNP-based hydrogels (Eiben et al., 2019). Here we expand on this specific theme by describing the use of plant viruses for the creation of composite hydrogels in more detail, focusing on the strategies used to produce VNP-augmented hydrogels and the novel functions conferred by plant VNPs in the context of tissue engineering. 2 | PLANT VIRUSES Plant viruses are natural supramolecular structures ranging in size from tens to hundreds of nanometers. They are com- posed of multiple copies of one or more identical coat protein subunits that self-assemble to form a capsid enclosing the virus genome, allowing them to be adapted into nanocarriers. VNPs derived from plant viruses remain stable when exposed to high temperatures, extreme pH and many solvents (Pokorski & Steinmetz, 2011). Structurally, there are two major classes of plant viruses—those with icosahedral capsids and those with
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