Virus capsid assembly across different length scales inspire the development of virus-based biomaterials

Selivanovitch, Ekaterina; Douglas, Trevor

doi:10.1016/j.coviro.2019.02.010

Title: Virus capsid assembly across different length scales inspire the development of virus-based biomaterials

Journal Article · Mon May 06 00:00:00 EDT 2019 · Current Opinion in Virology

DOI:https://doi.org/10.1016/j.coviro.2019.02.010· OSTI ID:1716723

Selivanovitch, Ekaterina ^[1];

^[1]

Indiana Univ., Bloomington, IN (United States)

In biology, there are an abundant number of self-assembled structures organized according to hierarchical levels of complexity. In some examples, the assemblies formed at each level exhibit unique properties and behaviors not present in individual components. Viruses are an example of such where first individual subunits come together to form a capsid structure, some utilizing a scaffolding protein to template or catalyze the capsid formation. Increasing the level of complexity, the viral capsids can then be used as building blocks of higher-level assemblies. This has inspired scientists to design and construct virus capsid-based functional nano-materials. In conclusion, this review provides some insight into the assembly of virus capsids across several length scales, and certain properties that arise at different levels, providing examples found in naturally occurring systems and those that are synthetically designed.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Indiana Univ., Bloomington, IN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division

Grant/Contract Number:: SC0016155

OSTI ID:: 1716723

Journal Information:: Current Opinion in Virology, Vol. 36, Issue C; ISSN 1879-6257

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 13 works

Citation information provided by
Web of Science

References (88)

Materials Aspects of Photonic Crystals López, C. Advanced Materials, Vol. 15, Issue 20 https://doi.org/10.1002/adma.200300386	journal	October 2003
Nanoreactors by Programmed Enzyme Encapsulation Inside the Capsid of the Bacteriophage P22 Patterson, Dustin P.; Prevelige, Peter E.; Douglas, Trevor ACS Nano, Vol. 6, Issue 6 https://doi.org/10.1021/nn300545z	journal	May 2012
Assembly of a Bacteriophage-Based Template for the Organization of Materials into Nanoporous Networks Courchesne, Noémie-Manuelle Dorval; Klug, Matthew T.; Chen, Po-Yen Advanced Materials, Vol. 26, Issue 21 https://doi.org/10.1002/adma.201305928	journal	March 2014
Assembly of a nucleus-like structure during viral replication in bacteria Chaikeeratisak, Vorrapon; Nguyen, Katrina; Khanna, Kanika Science, Vol. 355, Issue 6321 https://doi.org/10.1126/science.aal2130	journal	January 2017
Ordered association of tobacco mosaic virus in the presence of divalent metal ions Nedoluzhko, Aleksey; Douglas, Trevor Journal of Inorganic Biochemistry, Vol. 84, Issue 3-4 https://doi.org/10.1016/S0162-0134(01)00174-X	journal	April 2001
Bacteriophage φ29 scaffolding protein gp7 before and after prohead assembly Morais, Marc C.; Kanamaru, Shuji; Badasso, Mohammed O. Nature Structural & Molecular Biology, Vol. 10, Issue 7 https://doi.org/10.1038/nsb939	journal	June 2003
Virus factories: associations of cell organelles for viral replication and morphogenesis Novoa, Reyes R.; Calderita, Gloria; Arranz, Rocío Biology of the Cell, Vol. 97, Issue 2 https://doi.org/10.1042/BC20040058	journal	February 2005
The Structure of an Infectious P22 Virion Shows the Signal for Headful DNA Packaging Lander, G. C. Science, Vol. 312, Issue 5781 https://doi.org/10.1126/science.1127981	journal	June 2006
A proposed structure of bacteriophage T4 gene product 22—A major prohead scaffolding core protein Mesyanzhinov, Vadim V.; Sobolev, Boris N.; Marusich, Elena I. Journal of Structural Biology, Vol. 104, Issue 1-3 https://doi.org/10.1016/1047-8477(90)90053-F	journal	July 1990
Assembly of T7 Capsids from Independently Expressed and Purified Head Protein and Scaffolding Protein Cerritelli, Mario E.; Studier, William F. Journal of Molecular Biology, Vol. 258, Issue 2 https://doi.org/10.1006/jmbi.1996.0250	journal	May 1996
Structure and Assembly of the Capsid of Bacteriophage P22 King, J.; Botstein, D.; Casjens, S. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 276, Issue 943 https://doi.org/10.1098/rstb.1976.0096	journal	November 1976
Stimuli Responsive Hierarchical Assembly of P22 Virus-like Particles Aumiller, William M.; Uchida, Masaki; Biner, Daniel W. Chemistry of Materials, Vol. 30, Issue 7 https://doi.org/10.1021/acs.chemmater.7b04964	journal	March 2018
Internal proteins of bacteriophage T7 Serwer, Philip Journal of Molecular Biology, Vol. 107, Issue 3 https://doi.org/10.1016/S0022-2836(76)80005-8	journal	November 1976
Molecular Dissection of Ø29 Scaffolding Protein Function in an in Vitro Assembly System Fu, Chi-yu; Morais, Marc C.; Battisti, Anthony J. Journal of Molecular Biology, Vol. 366, Issue 4 https://doi.org/10.1016/j.jmb.2006.11.091	journal	March 2007
Preparation and magnetoviscosity of nanotube ferrofluids by viral scaffolding and ALD on porous templates Wu, Zhenyu; Zierold, Robert; Mueller, Anna physica status solidi (b), Vol. 247, Issue 10 https://doi.org/10.1002/pssb.201046208	journal	September 2010
Virus particle assembly into crystalline domains enabled by the coffee ring effect Gebhardt, Ronald; Teulon, Jean-Marie; Pellequer, Jean-Luc Soft Matter, Vol. 10, Issue 30 https://doi.org/10.1039/C4SM00414K	journal	January 2014
Virus-based piezoelectric energy generation Lee, Byung Yang; Zhang, Jinxing; Zueger, Chris Nature Nanotechnology, Vol. 7, Issue 6 https://doi.org/10.1038/nnano.2012.69	journal	May 2012
Coconfinement of Fluorescent Proteins: Spatially Enforced Communication of GFP and mCherry Encapsulated within the P22 Capsid O’Neil, Alison; Prevelige, Peter E.; Basu, Gautam Biomacromolecules, Vol. 13, Issue 12 https://doi.org/10.1021/bm301347x	journal	November 2012
Collective Infectious Units in Viruses Sanjuán, Rafael Trends in Microbiology, Vol. 25, Issue 5 https://doi.org/10.1016/j.tim.2017.02.003	journal	May 2017
Virus engineering: functionalization and stabilization Mateu, M. G. Protein Engineering Design and Selection, Vol. 24, Issue 1-2 https://doi.org/10.1093/protein/gzq069	journal	October 2010
Formation of supercrystals through self-assembly of polyhedral nanocrystals Huang, Michael H.; Thoka, Subashchandrabose Nano Today, Vol. 10, Issue 1 https://doi.org/10.1016/j.nantod.2015.01.006	journal	February 2015
Templated Assembly of a Functional Ordered Protein Macromolecular Framework from P22 Virus-like Particles McCoy, Kimberly; Uchida, Masaki; Lee, Byeongdu ACS Nano, Vol. 12, Issue 4 https://doi.org/10.1021/acsnano.8b00528	journal	March 2018
Emergent properties from organisms to ecosystems: towards a realistic approach Ponge, Jean-François Biological Reviews, Vol. 80, Issue 03 https://doi.org/10.1017/S146479310500672X	journal	April 2005
Biomimetic virus-based colourimetric sensors Oh, Jin-Woo; Chung, Woo-Jae; Heo, Kwang Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4043	journal	January 2014
Why large icosahedral viruses need scaffolding proteins Li, Siyu; Roy, Polly; Travesset, Alex Proceedings of the National Academy of Sciences, Vol. 115, Issue 43 https://doi.org/10.1073/pnas.1807706115	journal	October 2018
Alignment of biological assemblies using magnetic fluids — A review Charles, Stuart W. Journal of Magnetism and Magnetic Materials, Vol. 85, Issue 1-3 https://doi.org/10.1016/0304-8853(90)90066-Y	journal	April 1990
Functional Virus-Based Polymer–Protein Nanoparticles by Atom Transfer Radical Polymerization Pokorski, Jonathan K.; Breitenkamp, Kurt; Liepold, Lars O. Journal of the American Chemical Society, Vol. 133, Issue 24 https://doi.org/10.1021/ja203286n	journal	June 2011
DNA-controlled assembly of a NaTl lattice structure from gold nanoparticles and protein nanoparticles Cigler, Petr; Lytton-Jean, Abigail K. R.; Anderson, Daniel G. Nature Materials, Vol. 9, Issue 11, p. 918-922 https://doi.org/10.1038/nmat2877	journal	October 2010
Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus Chen, D. -H.; Baker, M. L.; Hryc, C. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1015739108	journal	January 2011
The isotropic–nematic transition and the phase separation of the tobacco mosaic virus particles with polysaccharide Urakami, Naohito; Imai, Masayuki; Sano, Yoh The Journal of Chemical Physics, Vol. 111, Issue 5 https://doi.org/10.1063/1.479503	journal	August 1999
Structure and interaction in 2D assemblies of tobacco mosaic viruses Yang, Lin; Wang, Suntao; Fukuto, Masafumi Soft Matter, Vol. 5, Issue 24 https://doi.org/10.1039/b911894b	journal	January 2009
TPPP/p25 Promotes Tubulin Acetylation by Inhibiting Histone Deacetylase 6 Tőkési, Natália; Lehotzky, Attila; Horváth, István Journal of Biological Chemistry, Vol. 285, Issue 23 https://doi.org/10.1074/jbc.M109.096578	journal	June 2010
Tubulin Polymerization Promoting Protein 1 (Tppp1) Phosphorylation by Rho-associated Coiled-coil Kinase (Rock) and Cyclin-dependent Kinase 1 (Cdk1) Inhibits Microtubule Dynamics to Increase Cell Proliferation Schofield, Alice V.; Gamell, Cristina; Suryadinata, Randy Journal of Biological Chemistry, Vol. 288, Issue 11 https://doi.org/10.1074/jbc.M112.441048	journal	March 2013
Self-Assembly at All Scales Whitesides, George M.; Grzybowski, Bartosz Science, Vol. 295, Issue 5564, p. 2418-2421 https://doi.org/10.1126/science.1070821	journal	March 2002
Assembly ofWiseanaIridovirus: Viruses for Colloidal Photonic Crystals Juhl, S. B.; Chan, E. P.; Ha, Y. -H. Advanced Functional Materials, Vol. 16, Issue 8 https://doi.org/10.1002/adfm.200500682	journal	May 2006
Bio-Inspired Synthesis of Minerals for Energy, Environment, and Medicinal Applications Kim, Sungjin; Park, Chan Beum Advanced Functional Materials, Vol. 23, Issue 1 https://doi.org/10.1002/adfm.201201994	journal	September 2012
The Concept of Integrative Levels and Biology Novikoff, A. B. Science, Vol. 101, Issue 2618 https://doi.org/10.1126/science.101.2618.209	journal	March 1945
Electrostatic Interactions Drive Scaffolding/Coat Protein Binding and Procapsid Maturation in Bacteriophage P22 Parker, Matthew H.; Prevelige, Peter E. Virology, Vol. 250, Issue 2 https://doi.org/10.1006/viro.1998.9386	journal	October 1998
Invertebrate Iridoviruses: A Glance over the Last Decade İnce, İkbal; Özcan, Orhan; Ilter-Akulke, Ayca Viruses, Vol. 10, Issue 4 https://doi.org/10.3390/v10040161	journal	March 2018
Bio-inspired, bioengineered and biomimetic drug delivery carriers Yoo, Jin-Wook; Irvine, Darrell J.; Discher, Dennis E. Nature Reviews Drug Discovery, Vol. 10, Issue 7 https://doi.org/10.1038/nrd3499	journal	July 2011
Encapsulation of an Enzyme Cascade within the Bacteriophage P22 Virus-Like Particle Patterson, Dustin P.; Schwarz, Benjamin; Waters, Ryan S. ACS Chemical Biology, Vol. 9, Issue 2 https://doi.org/10.1021/cb4006529	journal	November 2013
Virus factories: biogenesis and structural design: Biogenesis and architecture of virus factories de Castro, Isabel Fernández; Volonté, Luca; Risco, Cristina Cellular Microbiology, Vol. 15, Issue 1 https://doi.org/10.1111/cmi.12029	journal	October 2012
Superlattice of Rodlike Virus Particles Formed in Aqueous Solution through Like-Charge Attraction Li, Tao; Winans, Randall E.; Lee, Byeongdu Langmuir, Vol. 27, Issue 17 https://doi.org/10.1021/la202121s	journal	September 2011
Self-assembling biomolecular catalysts for hydrogen production Jordan, Paul C.; Patterson, Dustin P.; Saboda, Kendall N. Nature Chemistry, Vol. 8, Issue 2 https://doi.org/10.1038/nchem.2416	journal	December 2015
The Structure of Cells During Tobacco Mosaic Virus Reproduction Kolehmainen, L.; Zech, H.; von Wettstein, D. Journal of Cell Biology, Vol. 25, Issue 3 https://doi.org/10.1083/jcb.25.3.77	journal	June 1965
Host–guest encapsulation of materials by assembled virus protein cages Douglas, Trevor; Young, Mark Nature, Vol. 393, Issue 6681 https://doi.org/10.1038/30211	journal	May 1998
Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid Patterson, Dustin P.; Schwarz, Benjamin; El-Boubbou, Kheireddine Soft Matter, Vol. 8, Issue 39 https://doi.org/10.1039/c2sm26485d	journal	January 2012
Bacteriophage Assembly Aksyuk, Anastasia A.; Rossmann, Michael G. Viruses, Vol. 3, Issue 3 https://doi.org/10.3390/v3030172	journal	February 2011
Sequence of Morphological Changes in Epithelial cell Cultures Infected with Poliovirus Reissig, Magdalena; Howes, David W.; Melnick, Joseph L. Journal of Experimental Medicine, Vol. 104, Issue 3 https://doi.org/10.1084/jem.104.3.289	journal	September 1956
Biomimetic self-templating supramolecular structures Chung, Woo-Jae; Oh, Jin-Woo; Kwak, Kyungwon Nature, Vol. 478, Issue 7369 https://doi.org/10.1038/nature10513	journal	October 2011
Collective motion Vicsek, Tamás; Zafeiris, Anna Physics Reports, Vol. 517, Issue 3-4 https://doi.org/10.1016/j.physrep.2012.03.004	journal	August 2012
Regions of the Herpes Simplex Virus Scaffolding Protein That Are Important for Intermolecular Self-Interaction Preston, Valerie G.; McDougall, Iris M. Journal of Virology, Vol. 76, Issue 2 https://doi.org/10.1128/JVI.76.2.673-687.2002	journal	January 2002
Self-Assembly of Electrostatic Cocrystals from Supercharged Fusion Peptides and Protein Cages Korpi, Antti; Ma, Chao; Liu, Kai ACS Macro Letters, Vol. 7, Issue 3 https://doi.org/10.1021/acsmacrolett.8b00023	journal	February 2018
Two-dimensional nanoarchitectonics based on self-assembly Ariga, Katsuhiko; Lee, Michael V.; Mori, Taizo Advances in Colloid and Interface Science, Vol. 154, Issue 1-2 https://doi.org/10.1016/j.cis.2010.01.005	journal	February 2010
Biomimetism and bioinspiration as tools for the design of innovative materials and systems Sanchez, Clément; Arribart, Hervé; Giraud Guille, Marie Madeleine Nature Materials, Vol. 4, Issue 4 https://doi.org/10.1038/nmat1339	journal	April 2005
Two-Phase Formation in Solutions of Tobacco Mosaic Virus and the Problem of Long-Range Forces Oster, G. The Journal of General Physiology, Vol. 33, Issue 5 https://doi.org/10.1085/jgp.33.5.445	journal	May 1950
Phage-Based Structural Color Sensors and Their Pattern Recognition Sensing System Lee, Ju Hun; Fan, Benson; Samdin, Tuan D. ACS Nano, Vol. 11, Issue 4 https://doi.org/10.1021/acsnano.6b07942	journal	April 2017
Electrostatic interactions govern both nucleation and elongation during phage P22 procapsid assembly Parent, Kristin N.; Doyle, Shannon M.; Anderson, Eric Virology, Vol. 340, Issue 1 https://doi.org/10.1016/j.virol.2005.06.018	journal	September 2005
Brain-Specific p25 Protein Binds to Tubulin and Microtubules and Induces Aberrant Microtubule Assemblies at Substoichiometric Concentrations ^† Hlavanda, Emma; Kovács, János; Oláh, Judit Biochemistry, Vol. 41, Issue 27 https://doi.org/10.1021/bi020140g	journal	July 2002
The structure and properties of nanocrystalline materials: Issues and concerns Suryanarayana, C. JOM, Vol. 54, Issue 9 https://doi.org/10.1007/BF02709088	journal	September 2002
Fabrication of novel biomaterials through molecular self-assembly Zhang, Shuguang Nature Biotechnology, Vol. 21, Issue 10 https://doi.org/10.1038/nbt874	journal	September 2003
Folding of Newly Translated Proteins In Vivo: The Role of Molecular Chaperones Frydman, Judith Annual Review of Biochemistry, Vol. 70, Issue 1 https://doi.org/10.1146/annurev.biochem.70.1.603	journal	June 2001
Filamentous Viruses as Building Blocks for Hierarchical Self-Assembly toward Functional Soft Materials Sawada, Toshiki; Serizawa, Takeshi Bulletin of the Chemical Society of Japan, Vol. 91, Issue 3 https://doi.org/10.1246/bcsj.20170428	journal	March 2018
Molecular Genetics of Bacteriophage P22 Scaffolding Protein's Functional Domains Weigele, Peter R.; Sampson, Laura; Winn-Stapley, Danella Journal of Molecular Biology, Vol. 348, Issue 4 https://doi.org/10.1016/j.jmb.2005.03.004	journal	May 2005
Transient self-templating assembly of M13 bacteriophage for enhanced biopiezoelectric devices Heo, Kwang; Jin, Hyo-Eon; Kim, Han Nano Energy, Vol. 56 https://doi.org/10.1016/j.nanoen.2018.11.084	journal	February 2019
P22 morphogenesis I: Catalytic scaffolding protein in capsid assembly Casjens, Sherwood; King, Jonathan Journal of Supramolecular Structure, Vol. 2, Issue 2-4 https://doi.org/10.1002/jss.400020215	journal	January 1974
Modular interior loading and exterior decoration of a virus-like particle Sharma, Jhanvi; Uchida, Masaki; Miettinen, Heini M. Nanoscale, Vol. 9, Issue 29 https://doi.org/10.1039/C7NR03018E	journal	January 2017
Natural Nanochemical Building Blocks: Icosahedral Virus Particles Organized by Attached Oligonucleotides Strable, Erica; Johnson, John E.; Finn, M. G. Nano Letters, Vol. 4, Issue 8 https://doi.org/10.1021/nl0493850	journal	August 2004
Diverse Bacterial Microcompartment Organelles Chowdhury, C.; Sinha, S.; Chun, S. Microbiology and Molecular Biology Reviews, Vol. 78, Issue 3 https://doi.org/10.1128/MMBR.00009-14	journal	September 2014
Self-assembly of biomolecular soft matter Stupp, Samuel I.; Zha, R. Helen; Palmer, Liam C. Faraday Discussions, Vol. 166 https://doi.org/10.1039/c3fd00120b	journal	January 2013
Structure and function of bacteriophage T4 Yap, Moh Lan; Rossmann, Michael G. Future Microbiology, Vol. 9, Issue 12 https://doi.org/10.2217/fmb.14.91	journal	December 2014
Head morphogenesis of complex double-stranded deoxyribonucleic acid bacteriophages. Murialdo, H.; Becker, A. Microbiological Reviews, Vol. 42, Issue 3 https://doi.org/10.1128/MMBR.42.3.529-576.1978	journal	January 1978
Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis Uchida, Masaki; McCoy, Kimberly; Fukuto, Masafumi ACS Nano, Vol. 12, Issue 2 https://doi.org/10.1021/acsnano.7b06049	journal	November 2017
Virus-Based Fabrication of Micro- and Nanofibers Using Electrospinning Lee, Seung-Wuk; Belcher, Angela M. Nano Letters, Vol. 4, Issue 3 https://doi.org/10.1021/nl034911t	journal	March 2004
Genetically Programmed In Vivo Packaging of Protein Cargo and Its Controlled Release from Bacteriophage P22 O'Neil, Alison; Reichhardt, Courtney; Johnson, Benjamin Angewandte Chemie International Edition, Vol. 50, Issue 32 https://doi.org/10.1002/anie.201102036	journal	June 2011
Active tension network model suggests an exotic mechanical state realized in epithelial tissues Noll, Nicholas; Mani, Madhav; Heemskerk, Idse Nature Physics, Vol. 13, Issue 12 https://doi.org/10.1038/nphys4219	journal	August 2017
Self-Assembly of Rodlike Virus to Superlattices Li, Tao; Zan, Xingjie; Sun, Yong Langmuir, Vol. 29, Issue 41 https://doi.org/10.1021/la402933q	journal	October 2013
Recent advances in coarse-grained modeling of virus assembly Hagan, Michael F.; Zandi, Roya Current Opinion in Virology, Vol. 18 https://doi.org/10.1016/j.coviro.2016.02.012	journal	June 2016
Compartmentalized supramolecular hydrogels based on viral nanocages towards sophisticated cargo administration Yang, Liulin; Liu, Aijie; de Ruiter, Mark V. Nanoscale, Vol. 10, Issue 8 https://doi.org/10.1039/C7NR07718A	journal	January 2018
Principles of electrostatic interactions and self-assembly in lipid/peptide/DNA systems: Applications to gene delivery Berezhnoy, Nikolay V.; Korolev, Nikolay; Nordenskiöld, Lars Advances in Colloid and Interface Science, Vol. 205 https://doi.org/10.1016/j.cis.2013.08.008	journal	March 2014
Tobacco Mosaic Virus Liquid Crystals as Templates for the Interior Design of Silica Mesophases and Nanoparticles Fowler, C. E.; Shenton, W.; Stubbs, G. Advanced Materials, Vol. 13, Issue 16 https://doi.org/10.1002/1521-4095(200108)13:16<1266::AID-ADMA1266>3.0.CO;2-9	journal	August 2001
Scaffolding proteins and their role in viral assembly Dokland, T. Cellular and Molecular Life Sciences (CMLS), Vol. 56, Issue 7-8 https://doi.org/10.1007/s000180050455	journal	November 1999
Functional architectures based on self-assembly of bio-inspired dipeptides: Structure modulation and its photoelectronic applications Chen, Chengjun; Liu, Kai; Li, Junbai Advances in Colloid and Interface Science, Vol. 225 https://doi.org/10.1016/j.cis.2015.09.001	journal	November 2015
Biomolecular Assembly of Thermoresponsive Superlattices of the Tobacco Mosaic Virus with Large Tunable Interparticle Distances Li, Tao; Zan, Xingjie; Winans, Randall E. Angewandte Chemie, Vol. 125, Issue 26 https://doi.org/10.1002/ange.201209299	journal	May 2013
Self-assembly and applications of anisotropic nanomaterials: A review Thorkelsson, Kari; Bai, Peter; Xu, Ting Nano Today, Vol. 10, Issue 1 https://doi.org/10.1016/j.nantod.2014.12.005	journal	February 2015
Electrostatic assembly of binary nanoparticle superlattices using protein cages Kostiainen, Mauri A.; Hiekkataipale, Panu; Laiho, Ari Nature Nanotechnology, Vol. 8, Issue 1 https://doi.org/10.1038/nnano.2012.220	journal	December 2012
The purification and properties of the scaffolding protein of bacteriophage lambda. Ziegelhoffer, T.; Yau, P.; Chandrasekhar, G. N. Journal of Biological Chemistry, Vol. 267, Issue 1 https://doi.org/10.1016/S0021-9258(18)48516-X	journal	January 1992
Head morphogenesis of complex double-stranded deoxyribonucleic acid bacteriophages Murialdo, H.; Becker, A. Microbiological Reviews, Vol. 42, Issue 3 https://doi.org/10.1128/MR.42.3.529-576.1978	journal	September 1978

Cited By (2)

Tuning the catalytic properties of P22 nanoreactors through compositional control Sharma, Jhanvi; Douglas, Trevor Nanoscale, Vol. 12, Issue 1 https://doi.org/10.1039/c9nr08348k	journal	January 2020
From stars to stripes: RNA‐directed shaping of plant viral protein templates—structural synthetic virology for smart biohybrid nanostructures Wege, Christina; Koch, Claudia WIREs Nanomedicine and Nanobiotechnology, Vol. 12, Issue 2 https://doi.org/10.1002/wnan.1591	journal	October 2019

Similar Records

RNA nanotechnology to build a dodecahedral genome of single-stranded RNA virus

Journal Article · Thu Apr 29 00:00:00 EDT 2021 · RNA Biology · OSTI ID:1716723

Li, Hui; Zhang, Kaiming; Binzel, Daniel W.; +4 more

Self-Assembly of Virus Particle Based Materials for Hydrogen Catalysis

Technical Report · Sun Nov 22 00:00:00 EST 2020 · OSTI ID:1716723

Douglas, Trevor; Uchida, Masaki

Photonics and plasmonics go viral: self-assembly of hierarchical metamaterials

Journal Article · Thu Mar 05 00:00:00 EST 2015 · Rendiconti Lincei · OSTI ID:1716723

Wen, Amy M.; Podgornik, Rudolf; Strangi, Giuseppe; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Virus capsid assembly across different length scales inspire the development of virus-based biomaterials

Citation Formats

References (88)

Cited By (2)

Similar Records

Related Subjects