Virus-derived materials: bury the hatchet with old foes.

Although enormous attempts are being made to develop synthetic materials for biomedical applications, more and more attention has been paid to bioderived materials due to their natural properties, including mammalian cells, bacteria, and viruses. Attributed to their symmetrical, monodisperse, and polyvalent architectures, viruses present remarkable flexibility in functionalization for biomedical applications. In this review, modification strategies including bioconjugation chemistry, encapsulation, mineralization and genetic engineering, and several related methods for construction of virus-derived materials are introduced. Through rational design, virus-derived materials show great potential in cargo delivery, imaging and therapy. Particularly, virus-derived materials can serve as versatile platforms for immune modulation via various pathways. However, safety concerns of viruses and their immunogenicity are major obstacles for virus-derived materials to be exploited in critical clinical applications, which need to be addressed urgently.

[1]  Quanyin Hu,et al.  Platelet for drug delivery. , 2019, Current opinion in biotechnology.

[2]  Y. C. Shin,et al.  Virus-Incorporated Biomimetic Nanocomposites for Tissue Regeneration , 2019, Nanomaterials.

[3]  Jung Weon Lee,et al.  In Situ Nanoadjuvant-Assembled Tumor Vaccine for Preventing Long-Term Recurrence. , 2019, ACS nano.

[4]  N. Steinmetz,et al.  Cowpea Mosaic Virus Promotes Anti‐Tumor Activity and Immune Memory in a Mouse Ovarian Tumor Model , 2019, Advanced therapeutics.

[5]  T. Hyeon,et al.  Ferrimagnetic Nanochains‐Based Mesenchymal Stem Cell Engineering for Highly Efficient Post‐Stroke Recovery , 2019, Advanced Functional Materials.

[6]  N. Steinmetz,et al.  A Viral Nanoparticle Cancer Vaccine Delays Tumor Progression and Prolongs Survival in a HER2+ Tumor Mouse Model , 2019, Advanced therapeutics.

[7]  A. Hemminki,et al.  Oncolytic adenoviruses: a game changer approach in the battle between cancer and the immune system. , 2019, Expert opinion on biological therapy.

[8]  N. Steinmetz,et al.  CD47 Blockade and Cowpea Mosaic Virus Nanoparticle In Situ Vaccination Triggers Phagocytosis and Tumor Killing , 2019, Advanced healthcare materials.

[9]  H. V. von Recum,et al.  Let There Be Light: Targeted Photodynamic Therapy Using High Aspect Ratio Plant Viral Nanoparticles. , 2019, Macromolecular bioscience.

[10]  Jianqing Gao,et al.  Recent strategies on targeted delivery of thrombolytics , 2019, Asian journal of pharmaceutical sciences.

[11]  N. Steinmetz,et al.  Presentation and Delivery of Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand via Elongated Plant Viral Nanoparticle Enhances Antitumor Efficacy. , 2019, ACS nano.

[12]  Y. Tabata,et al.  Neural Stem Cells Transfected with Reactive Oxygen Species–Responsive Polyplexes for Effective Treatment of Ischemic Stroke , 2019, Advanced materials.

[13]  Y. Tabata,et al.  Mesenchymal stem cell-based drug delivery strategy: from cells to biomimetic. , 2019, Journal of controlled release : official journal of the Controlled Release Society.

[14]  Nicole F Steinmetz,et al.  Tobacco Mosaic Virus-Functionalized Mesoporous Silica Nanoparticles, a Wool-Ball-like Nanostructure for Drug Delivery. , 2018, Langmuir : the ACS journal of surfaces and colloids.

[15]  D. Ling,et al.  Uniformly sized iron oxide nanoparticles for efficient gene delivery to mesenchymal stem cells , 2018, International journal of pharmaceutics.

[16]  Kanyi Pu,et al.  Recent Advances in Cell Membrane-Camouflaged Nanoparticles for Cancer Phototherapy. , 2018, Small.

[17]  Andrzej S Pitek,et al.  Cancer Theranostic Applications of Albumin-Coated Tobacco Mosaic Virus Nanoparticles. , 2018, ACS applied materials & interfaces.

[18]  N. Steinmetz,et al.  Delivery of mitoxantrone using a plant virus-based nanoparticle for the treatment of glioblastomas. , 2018, Journal of materials chemistry. B.

[19]  Andrzej S Pitek,et al.  Delivery of thrombolytic therapy using rod-shaped plant viral nanoparticles decreases the risk of hemorrhage. , 2018, Nanoscale.

[20]  N. Steinmetz,et al.  Tobacco mosaic virus delivery of mitoxantrone for cancer therapy. , 2018, Nanoscale.

[21]  Youngho Seo,et al.  Vascular Cell Adhesion Molecule-Targeted MS2 Viral Capsids for the Detection of Early-Stage Atherosclerotic Plaques. , 2018, Bioconjugate chemistry.

[22]  Ronnie H. Fang,et al.  Cell Membrane Coating Nanotechnology , 2018, Advanced materials.

[23]  N. Steinmetz,et al.  In Situ Vaccination with Cowpea vs Tobacco Mosaic Virus against Melanoma. , 2018, Molecular pharmaceutics.

[24]  Trevor Douglas,et al.  Protein cage assembly across multiple length scales. , 2018, Chemical Society reviews.

[25]  N. Steinmetz,et al.  Radiation Therapy Combined with Cowpea Mosaic Virus Nanoparticle in Situ Vaccination Initiates Immune-Mediated Tumor Regression , 2018, ACS omega.

[26]  T. Douglas,et al.  Templated Assembly of a Functional Ordered Protein Macromolecular Framework from P22 Virus-like Particles. , 2018, ACS nano.

[27]  T. Douglas,et al.  Stimuli Responsive Hierarchical Assembly of P22 Virus-like Particles , 2018 .

[28]  Frank A. Veliz,et al.  Slow‐Release Formulation of Cowpea Mosaic Virus for In Situ Vaccine Delivery to Treat Ovarian Cancer , 2018, Advanced science.

[29]  Zhen Gu,et al.  Red Blood Cells for Drug Delivery , 2017 .

[30]  M. Fukuto,et al.  Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis. , 2017, ACS nano.

[31]  Paul L. Chariou,et al.  Physalis Mottle Virus-Like Particles as Nanocarriers for Imaging Reagents and Drugs. , 2017, Biomacromolecules.

[32]  Ronnie H. Fang,et al.  A facile approach to functionalizing cell membrane‐coated nanoparticles with neurotoxin‐derived peptide for brain‐targeted drug delivery , 2017, Journal of controlled release : official journal of the Controlled Release Society.

[33]  Y. Tabata,et al.  Peptide modified mesenchymal stem cells as targeting delivery system transfected with miR-133b for the treatment of cerebral ischemia. , 2017, International journal of pharmaceutics.

[34]  Nicole F Steinmetz,et al.  Elongated Plant Virus-Based Nanoparticles for Enhanced Delivery of Thrombolytic Therapies. , 2017, Molecular pharmaceutics.

[35]  N. Steinmetz,et al.  Tobacco Mosaic Virus-Delivered Cisplatin Restores Efficacy in Platinum-Resistant Ovarian Cancer Cells. , 2017, Molecular pharmaceutics.

[36]  Xin Yu,et al.  Dysprosium-Modified Tobacco Mosaic Virus Nanoparticles for Ultra-High-Field Magnetic Resonance and Near-Infrared Fluorescence Imaging of Prostate Cancer. , 2017, ACS nano.

[37]  N. Steinmetz,et al.  Viral nanoparticles decorated with novel EGFL7 ligands enable intravital imaging of tumor neovasculature. , 2017, Nanoscale.

[38]  T. Douglas,et al.  Modular interior loading and exterior decoration of a virus-like particle. , 2017, Nanoscale.

[39]  Paul Krugler,et al.  Sortase-Mediated Ligation as a Modular Approach for the Covalent Attachment of Proteins to the Exterior of the Bacteriophage P22 Virus-like Particle. , 2017, Bioconjugate chemistry.

[40]  Ronnie H. Fang,et al.  Cell membrane-derived nanomaterials for biomedical applications. , 2017, Biomaterials.

[41]  Jian-Qing Gao,et al.  Exosomes as novel bio-carriers for gene and drug delivery. , 2017, International journal of pharmaceutics.

[42]  Y. Tabata,et al.  Design of magnetic gene complexes as effective and serum resistant gene delivery systems for mesenchymal stem cells. , 2017, International journal of pharmaceutics.

[43]  Paul L. Chariou,et al.  Delivery of Pesticides to Plant Parasitic Nematodes Using Tobacco Mild Green Mosaic Virus as a Nanocarrier. , 2017, ACS nano.

[44]  A. Levine,et al.  Plant viral nanoparticles-based HER2 vaccine: Immune response influenced by differential transport, localization and cellular interactions of particulate carriers. , 2017, Biomaterials.

[45]  N. Steinmetz,et al.  Potato virus X, a filamentous plant viral nanoparticle for doxorubicin delivery in cancer therapy. , 2017, Nanoscale.

[46]  Y. Tabata,et al.  Peptide-Tethered Hydrogel Scaffold Promotes Recovery from Spinal Cord Transection via Synergism with Mesenchymal Stem Cells. , 2017, ACS applied materials & interfaces.

[47]  Y. Duan,et al.  Oncolytic Adenovirus Complexes Coated with Lipids and Calcium Phosphate for Cancer Gene Therapy. , 2016, ACS nano.

[48]  B. Graham,et al.  Viruslike Particles Encapsidating Respiratory Syncytial Virus M and M2 Proteins Induce Robust T Cell Responses. , 2016, ACS biomaterials science & engineering.

[49]  Jianqing Gao,et al.  Integration of antimicrobial peptides with gold nanoparticles as unique non-viral vectors for gene delivery to mesenchymal stem cells with antibacterial activity. , 2016, Biomaterials.

[50]  Youngho Seo,et al.  Biodistribution of Antibody-MS2 Viral Capsid Conjugates in Breast Cancer Models. , 2016, Molecular pharmaceutics.

[51]  Nicole F Steinmetz,et al.  Design of virus-based nanomaterials for medicine, biotechnology, and energy. , 2016, Chemical Society reviews.

[52]  N. Steinmetz,et al.  Tobacco mosaic virus-based protein nanoparticles and nanorods for chemotherapy delivery targeting breast cancer. , 2016, Journal of controlled release : official journal of the Controlled Release Society.

[53]  Frank A. Veliz,et al.  Utilizing Viral Nanoparticle/Dendron Hybrid Conjugates in Photodynamic Therapy for Dual Delivery to Macrophages and Cancer Cells. , 2016, Bioconjugate chemistry.

[54]  N. Steinmetz,et al.  High Aspect Ratio Nanotubes Formed by Tobacco Mosaic Virus for Delivery of Photodynamic Agents Targeting Melanoma. , 2016, ACS biomaterials science & engineering.

[55]  Andrzej S Pitek,et al.  The Protein Corona of Plant Virus Nanoparticles Influences their Dispersion Properties, Cellular Interactions, and In Vivo Fates. , 2016, Small.

[56]  S. Lippard,et al.  Tobacco Mosaic Virus Delivery of Phenanthriplatin for Cancer therapy. , 2016, ACS nano.

[57]  B. Wiedenheft,et al.  Programmed Self-Assembly of an Active P22-Cas9 Nanocarrier System. , 2016, Molecular pharmaceutics.

[58]  Paul C Jordan,et al.  Self-assembling biomolecular catalysts for hydrogen production. , 2016, Nature chemistry.

[59]  P. Lizotte,et al.  In situ vaccination with cowpea mosaic virus nanoparticles suppresses metastatic cancer , 2015, Nature nanotechnology.

[60]  Daniel L. Popkin,et al.  Tropism of CPMV to Professional Antigen Presenting Cells Enables a Platform to Eliminate Chronic Infections. , 2015, ACS biomaterials science & engineering.

[61]  Rui Tian,et al.  Virus-mimetic nanovesicles as a versatile antigen-delivery system , 2015, Proceedings of the National Academy of Sciences.

[62]  H. Kaufman,et al.  Oncolytic viruses: a new class of immunotherapy drugs , 2015, Nature Reviews Drug Discovery.

[63]  A. Rynda-Apple,et al.  Symmetry Controlled, Genetic Presentation of Bioactive Proteins on the P22 Virus-like Particle Using an External Decoration Protein. , 2015, ACS nano.

[64]  Ronnie H. Fang,et al.  Engineered nanoparticles mimicking cell membranes for toxin neutralization. , 2015, Advanced drug delivery reviews.

[65]  Kai Jiang,et al.  Shaping bio-inspired nanotechnologies to target thrombosis for dual optical-magnetic resonance imaging. , 2015, Journal of materials chemistry. B.

[66]  Y. Tabata,et al.  Synergistic effects of co-administration of suicide gene expressing mesenchymal stem cells and prodrug-encapsulated liposome on aggressive lung melanoma metastases in mice. , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[67]  P. Levkin,et al.  ScreenFect A: an efficient and low toxic liposome for gene delivery to mesenchymal stem cells. , 2015, International journal of pharmaceutics.

[68]  G. Dubyak,et al.  Stealth filaments: Polymer chain length and conformation affect the in vivo fate of PEGylated potato virus X. , 2015, Acta biomaterialia.

[69]  G. Khang,et al.  β-Cyclodextrin-Linked Polyethylenimine Nanoparticles Facilitate Gene Transfer and Enhance the Angiogenic Capacity of Mesenchymal Stem Cells for Wound Repair and Regeneration. , 2015, Journal of biomedical nanotechnology.

[70]  M. Francis,et al.  Chemical strategies for the covalent modification of filamentous phage , 2014, Front. Microbiol..

[71]  R. Tang,et al.  Nanomodification of living organisms by biomimetic mineralization , 2014, Nano Research.

[72]  T. Douglas,et al.  Constructing catalytic antimicrobial nanoparticles by encapsulation of hydrogen peroxide producing enzyme inside the P22 VLP. , 2014, Journal of materials chemistry. B.

[73]  Jian-Qing Gao,et al.  TAT conjugated cationic noble metal nanoparticles for gene delivery to epidermal stem cells. , 2014, Biomaterials.

[74]  N. Steinmetz,et al.  Molecular farming of fluorescent virus-based nanoparticles for optical imaging in plants, human cells and mouse models. , 2014, Biomaterials science.

[75]  T. Gedeon,et al.  Encapsulation of an enzyme cascade within the bacteriophage P22 virus-like particle. , 2014, ACS chemical biology.

[76]  Kai Jiang,et al.  Dual-Modal Magnetic Resonance and Fluorescence Imaging of Atherosclerotic Plaques in Vivo Using VCAM-1 Targeted Tobacco Mosaic Virus , 2014, Nano letters.

[77]  Y. Tabata,et al.  Reversal of tumor growth by gene modification of mesenchymal stem cells using spermine-pullulan/DNA nanoparticles. , 2014, Journal of biomedical nanotechnology.

[78]  N. Steinmetz,et al.  Infusion of imaging and therapeutic molecules into the plant virus-based carrier cowpea mosaic virus: cargo-loading and delivery. , 2013, Journal of controlled release : official journal of the Controlled Release Society.

[79]  P. Prevelige,et al.  Location of the bacteriophage P22 coat protein C-terminus provides opportunities for the design of capsid-based materials. , 2013, Biomacromolecules.

[80]  P. Prevelige,et al.  Stabilizing viral nano-reactors for nerve-agent degradation. , 2013, Biomaterials science.

[81]  X. Chen,et al.  Epidermal stem cells manipulated by pDNA-VEGF165/CYD-PEI nanoparticles loaded gelatin/β-TCP matrix as a therapeutic agent and gene delivery vehicle for wound healing. , 2013, Molecular pharmaceutics.

[82]  A. Rynda-Apple,et al.  Biomimetic antigenic nanoparticles elicit controlled protective immune response to influenza. , 2013, ACS nano.

[83]  Kai Jiang,et al.  Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. , 2013, Journal of materials chemistry. B.

[84]  M. Francis,et al.  Controlled integration of gold nanoparticles and organic fluorophores using synthetically modified MS2 viral capsids. , 2013, Journal of the American Chemical Society.

[85]  P. Prevelige,et al.  P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. , 2013, Molecular pharmaceutics.

[86]  J. O’Neil,et al.  PET Imaging and biodistribution of chemically modified bacteriophage MS2. , 2013, Molecular pharmaceutics.

[87]  N. Steinmetz Viral nanoparticles in drug delivery and imaging. , 2013, Molecular pharmaceutics.

[88]  M. Francis,et al.  Osmolyte-mediated encapsulation of proteins inside MS2 viral capsids. , 2012, ACS nano.

[89]  P. Prevelige,et al.  Use of the interior cavity of the P22 capsid for site-specific initiation of atom-transfer radical polymerization with high-density cargo loading. , 2012, Nature chemistry.

[90]  Y. Tabata,et al.  Mesenchymal stem cells as therapeutic agents and potential targeted gene delivery vehicle for brain diseases. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[91]  Y. Tabata,et al.  Mesenchymal stem cells as a novel carrier for targeted delivery of gene in cancer therapy based on nonviral transfection. , 2012, Molecular pharmaceutics.

[92]  N. Steinmetz,et al.  Photodynamic activity of viral nanoparticles conjugated with C60. , 2012, Chemical communications.

[93]  P. Prevelige,et al.  Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. , 2012, ACS nano.

[94]  Nicole F Steinmetz,et al.  Engineering of Brome mosaic virus for biomedical applications. , 2012, RSC advances.

[95]  N. Steinmetz,et al.  A potential nanobiotechnology platform based on infectious bursal disease subviral particles. , 2012, RSC advances.

[96]  P. Prevelige,et al.  Site-directed coordination chemistry with P22 virus-like particles. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[97]  Nicole F Steinmetz,et al.  Applications of viral nanoparticles in medicine. , 2011, Current opinion in biotechnology.

[98]  M. Francis,et al.  Using synthetically modified proteins to make new materials. , 2011, Accounts of chemical research.

[99]  P. Prevelige,et al.  Genetically programmed in vivo packaging of protein cargo and its controlled release from bacteriophage P22. , 2011, Angewandte Chemie.

[100]  N. Steinmetz,et al.  Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells. , 2011, Nanomedicine.

[101]  P. Prevelige,et al.  Templated assembly of organic-inorganic materials using the core shell structure of the P22 bacteriophage. , 2011, Chemical communications.

[102]  T. Douglas,et al.  Structure and photoelectrochemistry of a virus capsid-TiO2 nanocomposite. , 2011, Nanoscale.

[103]  Nicole F Steinmetz,et al.  The art of engineering viral nanoparticles. , 2011, Molecular pharmaceutics.

[104]  Y. Tabata,et al.  Mesenchymal stem cells: a promising targeted-delivery vehicle in cancer gene therapy. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[105]  N. Steinmetz Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[106]  N. Stephanopoulos,et al.  Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. , 2010, ACS nano.

[107]  Nicole F Steinmetz,et al.  Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles , 2010, Nature Protocols.

[108]  N. Steinmetz,et al.  Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. , 2010, Nano letters.

[109]  Yu Zhao,et al.  Functional single-virus-polyelectrolyte hybrids make large-scale applications of viral nanoparticles more efficient. , 2010, Small.

[110]  John E. Johnson,et al.  Potato virus X as a novel platform for potential biomedical applications. , 2010, Nano letters.

[111]  N. Steinmetz,et al.  Virus-templated silica nanoparticles. , 2009, Small.

[112]  Young Keun Kim,et al.  A highly sensitive and selective diagnostic assay based on virus nanoparticles. , 2009, Nature nanotechnology.

[113]  M. Young,et al.  Biomimetic synthesis of β-TiO2 inside a viral capsid , 2008 .

[114]  Y. Tsutsumi,et al.  Combination of two fiber-mutant adenovirus vectors, one encoding the chemokine FKN and another encoding cytokine interleukin 12, elicits notably enhanced anti-tumor responses , 2008, Cancer Immunology, Immunotherapy.

[115]  Trevor Douglas,et al.  Viral capsids as MRI contrast agents , 2007, Magnetic resonance in medicine.

[116]  M. Young,et al.  Targeting and photodynamic killing of a microbial pathogen using protein cage architectures functionalized with a photosensitizer. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[117]  Y. Yoshioka,et al.  Effective tumor targeted gene transfer using PEGylated adenovirus vector via systemic administration. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[118]  Trevor Douglas,et al.  Biological Containers: Protein Cages as Multifunctional Nanoplatforms , 2007 .

[119]  Jianqing Gao,et al.  Enhanced immune responses induced by vaccine using Sendai virosomes as carrier. , 2007, International journal of pharmaceutics.

[120]  Y. Tsutsumi,et al.  Cotransduction of CCL27 gene can improve the efficacy and safety of IL-12 gene therapy for cancer , 2007, Gene Therapy.

[121]  Trevor Douglas,et al.  Viruses: Making Friends with Old Foes , 2006, Science.

[122]  N. Steinmetz,et al.  Decoration of cowpea mosaic virus with multiple, redox-active, organometallic complexes. , 2006, Small.

[123]  Trevor Douglas,et al.  Paramagnetic viral nanoparticles as potential high‐relaxivity magnetic resonance contrast agents , 2005, Magnetic resonance in medicine.

[124]  Y. Tsutsumi,et al.  Anti-tumor responses induced by chemokine CCL19 transfected into an ovarian carcinoma model via fiber-mutant adenovirus vector. , 2005, Biological & pharmaceutical bulletin.

[125]  Y. Tsutsumi,et al.  PEGylated adenovirus vectors containing RGD peptides on the tip of PEG show high transduction efficiency and antibody evasion ability , 2005, The journal of gene medicine.

[126]  Y. Tsutsumi,et al.  A single intratumoral injection of a fiber-mutant adenoviral vector encoding interleukin 12 induces remarkable anti-tumor and anti-metastatic activity in mice with Meth-A fibrosarcoma. , 2005, Biochemical and biophysical research communications.

[127]  Takao Hayakawa,et al.  Neutralizing antibody evasion ability of adenovirus vector induced by the bioconjugation of methoxypolyethylene glycol succinimidyl propionate (MPEG-SPA). , 2004, Biological & pharmaceutical bulletin.

[128]  M. Young,et al.  2-D array formation of genetically engineered viral cages on au surfaces and imaging by atomic force microscopy. , 2003, Journal of the American Chemical Society.

[129]  Y. Tsutsumi,et al.  Antitumor effect by interleukin-11 receptor alpha-locus chemokine/CCL27, introduced into tumor cells through a recombinant adenovirus vector. , 2003, Cancer research.

[130]  M. Young,et al.  Chemical modification of a viral cage for multivalent presentation. , 2002, Chemical communications.

[131]  Trevor Douglas,et al.  VIRUS PARTICLES AS TEMPLATES FOR MATERIALS SYNTHESIS , 1999 .

[132]  G. Stubbs,et al.  Inorganic–Organic Nanotube Composites from Template Mineralization of Tobacco Mosaic Virus , 1999 .

[133]  H. Ouyang,et al.  Transplantation of BDNF Gene Recombinant Mesenchymal Stem Cells and Adhesive Peptide-modified Hydrogel Scaffold for Spinal Cord Repair. , 2018, Current gene therapy.

[134]  Y. Tabata,et al.  Gene recombinant bone marrow mesenchymal stem cells as a tumor-targeted suicide gene delivery vehicle in pulmonary metastasis therapy using non-viral transfection. , 2014, Nanomedicine : nanotechnology, biology, and medicine.

[135]  A. Rynda-Apple,et al.  Immunopathology and Infectious Diseases Virus-Like Particle-Induced Protection Against MRSA Pneumonia Is Dependent on IL-13 and Enhancement of Phagocyte Function , 2012 .