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

Li, Hui; Zhang, Kaiming; Binzel, Daniel W.; Shlyakhtenko, Lyudmila S.; Lyubchenko, Yuri L.; Chiu, Wah; Guo, Peixuan

doi:10.1080/15476286.2021.1915620

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

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

DOI:https://doi.org/10.1080/15476286.2021.1915620· OSTI ID:1788247

Li, Hui ^[1]; Zhang, Kaiming ^[2]; Binzel, Daniel W. ^[1]; Shlyakhtenko, Lyudmila S. ^[3]; Lyubchenko, Yuri L. ^[3]; Chiu, Wah ^[4]; ^[1]

The Ohio State Univ., Columbus, OH (United States). Center for RNA Nanobiotechnology and Nanomedicine, James Comprehensive Cancer Center, and Dorothy M. Davis Heart and Lung Research Institute
Stanford Univ., CA (United States). James H. Clark Center
Univ. of Nebraska Medical Center, Omaha, NE (United States)
Stanford Univ., CA (United States). James H. Clark Center; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

The quest for artificial RNA viral complexes with authentic structure while being non-replicative is on its way for the development of viral vaccines. RNA viruses contain capsid proteins that interact with the genome during morphogenesis. The sequence and properties of the protein and genome determine the structure of the virus. For example, the Pariacoto virus ssRNA genome assembles into a dodecahedron. Virus-inspired nanotechnology has progressed remarkably due to the unique structural and functional properties of viruses, which can inspire the design of novel nanomaterials. RNA is a programmable biopolymer able to self-assemble sophisticated 3D structures with rich functionalities. RNA dodecahedrons mimicking the Pariacoto virus quasi-icosahedral genome structures were constructed from both native and 2'-F modified RNA oligos. The RNA dodecahedron easily self-assembled using the stable pRNA three-way junction of bacteriophage phi29 as building blocks. The RNA dodecahedron cage was further characterized by cryo-electron microscopy and atomic force microscopy, confirming the spontaneous and homogenous formation of the RNA cage. The reported RNA dodecahedron cage will likely provide further studies on the mechanisms of interaction of the capsid protein with the viral genome while providing a template for further construction of the viral RNA scaffold to add capsid proteins for the assembly of the viral nucleocapsid as a model. Understanding the self-assembly and RNA folding of this RNA cage may offer new insights into the 3D organization of viral RNA genomes. Finally, the reported RNA cage also has the potential to be explored as a novel virus-inspired nanocarrier.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1788247

Journal Information:: RNA Biology, Journal Name: RNA Biology Journal Issue: 12 Vol. 18; ISSN 1547-6286

Publisher:: Taylor & FrancisCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Icosahedral Virus Particles as Addressable Nanoscale Building Blocks Wang, Qian; Lin, Tianwei; Tang, Liang Angewandte Chemie International Edition, Vol. 41, Issue 3 https://doi.org/10.1002/1521-3773(20020201)41:3<459::AID-ANIE459>3.0.CO;2-O	journal	January 2002
Controllable Self-Assembly of RNA Tetrahedrons with Precise Shape and Size for Cancer Targeting Li, Hui; Zhang, Kaiming; Pi, Fengmei Advanced Materials, Vol. 28, Issue 34 https://doi.org/10.1002/adma.201601976	journal	June 2016
Fabrication of RNA 3D Nanoprisms for Loading and Protection of Small RNAs and Model Drugs Khisamutdinov, Emil F.; Jasinski, Daniel L.; Li, Hui Advanced Materials, Vol. 28, Issue 45 https://doi.org/10.1002/adma.201603180	journal	October 2016
RNA Nanotechnology to Solubilize Hydrophobic Antitumor Drug for Targeted Delivery Piao, Xijun; Yin, Hongran; Guo, Sijin Advanced Science, Vol. 6, Issue 22 https://doi.org/10.1002/advs.201900951	journal	September 2019
Integrating open‐source software applications to build molecular dynamics systems Allen, Bruce M.; Predecki, Paul K.; Kumosa, Maciej Journal of Computational Chemistry, Vol. 35, Issue 9 https://doi.org/10.1002/jcc.23537	journal	February 2014
Theoretical aspects of virus capsid assembly Zlotnick, Adam Journal of Molecular Recognition, Vol. 18, Issue 6 https://doi.org/10.1002/jmr.754	journal	January 2005
The structure and folding of kink turns in RNA: Kink turns in RNA structure Lilley, David M. J. Wiley Interdisciplinary Reviews: RNA, Vol. 3, Issue 6 https://doi.org/10.1002/wrna.1136	journal	September 2012
Introduction: Principles, perspectives and potential applications in viral assembly Guo, Peixuan Seminars in Virology, Vol. 5, Issue 1 https://doi.org/10.1006/smvy.1994.1001	journal	February 1994
Evolution of Viral Structure Bamford, Dennis H.; Burnett, Roger M.; Stuart, David I. Theoretical Population Biology, Vol. 61, Issue 4 https://doi.org/10.1006/tpbi.2002.1591	journal	June 2002
Photo-controlled release of paclitaxel and model drugs from RNA pyramids Xu, Congcong; Li, Hui; Zhang, Kaiming Nano Research, Vol. 12, Issue 1 https://doi.org/10.1007/s12274-018-2174-x	journal	September 2018
Shape-controllable Synthesis of Functional Nanomaterials on DNA Templates Zhu, Jinjin; Shang, Yingxu; Yu, Haiyin Chemical Research in Chinese Universities, Vol. 36, Issue 2 https://doi.org/10.1007/s40242-020-9035-3	journal	January 2020
Structure of Dengue Virus Kuhn, Richard J.; Zhang, Wei; Rossmann, Michael G. Cell, Vol. 108, Issue 5 https://doi.org/10.1016/S0092-8674(02)00660-8	journal	March 2002
The role of Vif during HIV-1 infection: interaction with novel host cellular factors Lake, Julie-anne; Carr, Jillian; Feng, Feng Journal of Clinical Virology, Vol. 26, Issue 2 https://doi.org/10.1016/S1386-6532(02)00113-0	journal	February 2003
Structural Proteins in Severe Acute Respiratory Syndrome Coronavirus-2 Satarker, Sairaj; Nampoothiri, Madhavan Archives of Medical Research, Vol. 51, Issue 6 https://doi.org/10.1016/j.arcmed.2020.05.012	journal	August 2020
Bio-inspired engineering of cell- and virus-like nanoparticles for drug delivery Parodi, Alessandro; Molinaro, Roberto; Sushnitha, Manuela Biomaterials, Vol. 147 https://doi.org/10.1016/j.biomaterials.2017.09.020	journal	December 2017
Automated prediction of three-way junction topological families in RNA secondary structures Lamiable, Alexis; Barth, Dominique; Denise, Alain Computational Biology and Chemistry, Vol. 37 https://doi.org/10.1016/j.compbiolchem.2011.11.001	journal	April 2012
A modelling paradigm for RNA virus assembly Twarock, Reidun; Bingham, Richard J.; Dykeman, Eric C. Current Opinion in Virology, Vol. 31 https://doi.org/10.1016/j.coviro.2018.07.003	journal	August 2018
The Assembly Pathway of an Icosahedral Single-Stranded RNA Virus Depends on the Strength of Inter-Subunit Attractions Garmann, Rees F.; Comas-Garcia, Mauricio; Gopal, Ajaykumar Journal of Molecular Biology, Vol. 426, Issue 5 https://doi.org/10.1016/j.jmb.2013.10.017	journal	March 2014
The Kink Turn, a Key Architectural Element in RNA Structure Huang, Lin; Lilley, David M. J. Journal of Molecular Biology, Vol. 428, Issue 5 https://doi.org/10.1016/j.jmb.2015.09.026	journal	February 2016
Retroviral Gag protein–RNA interactions: Implications for specific genomic RNA packaging and virion assembly Olson, Erik D.; Musier-Forsyth, Karin Seminars in Cell & Developmental Biology, Vol. 86 https://doi.org/10.1016/j.semcdb.2018.03.015	journal	February 2019
Virus assembly, allostery and antivirals Zlotnick, Adam; Mukhopadhyay, Suchetana Trends in Microbiology, Vol. 19, Issue 1 https://doi.org/10.1016/j.tim.2010.11.003	journal	January 2011
Influenza virus assembly and budding Rossman, Jeremy S.; Lamb, Robert A. Virology, Vol. 411, Issue 2 https://doi.org/10.1016/j.virol.2010.12.003	journal	March 2011
Imaging of nucleic acids with atomic force microscopy Lyubchenko, Yuri L.; Shlyakhtenko, Luda S.; Ando, Toshio Methods, Vol. 54, Issue 2 https://doi.org/10.1016/j.ymeth.2011.02.001	journal	June 2011
Integration of Cell-Penetrating Peptides with Rod-like Bionanoparticles: Virus-Inspired Gene-Silencing Technology Tian, Ye; Zhou, Mengxue; Shi, Haigang Nano Letters, Vol. 18, Issue 9 https://doi.org/10.1021/acs.nanolett.8b01805	journal	August 2018
RNA Nanoparticles as Rubber for Compelling Vessel Extravasation to Enhance Tumor Targeting and for Fast Renal Excretion to Reduce Toxicity Ghimire, Chiran; Wang, Hongzhi; Li, Hui ACS Nano, Vol. 14, Issue 10 https://doi.org/10.1021/acsnano.0c04863	journal	September 2020
Systemic Delivery of Anti-miRNA for Suppression of Triple Negative Breast Cancer Utilizing RNA Nanotechnology Shu, Dan; Li, Hui; Shu, Yi ACS Nano, Vol. 9, Issue 10 https://doi.org/10.1021/acsnano.5b02471	journal	September 2015
Advancement of the Emerging Field of RNA Nanotechnology Jasinski, Daniel; Haque, Farzin; Binzel, Daniel W. ACS Nano, Vol. 11, Issue 2 https://doi.org/10.1021/acsnano.6b05737	journal	February 2017
RNA Self-Assembly and RNA Nanotechnology Grabow, Wade W.; Jaeger, Luc Accounts of Chemical Research, Vol. 47, Issue 6 https://doi.org/10.1021/ar500076k	journal	May 2014
Virus-Inspired Function in Engineered Protein Cages Edwardson, Thomas G. W.; Hilvert, Donald Journal of the American Chemical Society, Vol. 141, Issue 24 https://doi.org/10.1021/jacs.9b03705	journal	April 2019
A Boost for the Emerging Field of RNA Nanotechnology: Report on the First International Conference on RNA Nanotechnology Shukla, Girish C.; Haque, Farzin; Tor, Yitzhak ACS Nano, Vol. 5, Issue 5 https://doi.org/10.1021/nn200989r	journal	April 2011
RNA as a Boiling-Resistant Anionic Polymer Material To Build Robust Structures with Defined Shape and Stoichiometry Khisamutdinov, Emil F.; Jasinski, Daniel L.; Guo, Peixuan ACS Nano, Vol. 8, Issue 5 https://doi.org/10.1021/nn5006254	journal	April 2014
Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve In Vivo Stability Perrault, Steven D.; Shih, William M. ACS Nano, Vol. 8, Issue 5 https://doi.org/10.1021/nn5011914	journal	April 2014
Physicochemically Tunable Polyfunctionalized RNA Square Architecture with Fluorogenic and Ribozymatic Properties Jasinski, Daniel L.; Khisamutdinov, Emil F.; Lyubchenko, Yuri L. ACS Nano, Vol. 8, Issue 8 https://doi.org/10.1021/nn502160s	journal	July 2014
Engineering RNA–Protein Complexes with Different Shapes for Imaging and Therapeutic Applications Osada, Eriko; Suzuki, Yuki; Hidaka, Kumi ACS Nano, Vol. 8, Issue 8 https://doi.org/10.1021/nn502253c	journal	July 2014
Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy Conway, J. F.; Cheng, N.; Zlotnick, A. Nature, Vol. 386, Issue 6620 https://doi.org/10.1038/386091a0	journal	March 1997
Distribution and three-dimensional structure of AIDS virus envelope spikes Zhu, Ping; Liu, Jun; Bess, Julian Nature, Vol. 441, Issue 7095 https://doi.org/10.1038/nature04817	journal	May 2006
Icosahedral bacteriophage ΦX174 forms a tail for DNA transport during infection Sun, Lei; Young, Lindsey N.; Zhang, Xinzheng Nature, Vol. 505, Issue 7483 https://doi.org/10.1038/nature12816	journal	December 2013
Adenovirus dodecahedron, a new vector for human gene transfer Fender, Pascal; Ruigrok, Rob W. H.; Gout, Evelyne Nature Biotechnology, Vol. 15, Issue 1 https://doi.org/10.1038/nbt0197-52	journal	January 1997
Mechanisms of assembly and genome packaging in an RNA virus revealed by high-resolution cryo-EM Hesketh, Emma L.; Meshcheriakova, Yulia; Dent, Kyle C. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms10113	journal	December 2015
An influenza virus-inspired polymer system for the timed release of siRNA Truong, Nghia P.; Gu, Wenyi; Prasadam, Indira Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2905	journal	May 2013
Construction of RNA nanocages by re-engineering the packaging RNA of Phi29 bacteriophage Hao, Chenhui; Li, Xiang; Tian, Cheng Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4890	journal	May 2014
The emerging field of RNA nanotechnology Guo, Peixuan Nature Nanotechnology, Vol. 5, Issue 12 https://doi.org/10.1038/nnano.2010.231	journal	November 2010
Thermodynamically stable RNA three-way junction for constructing multifunctional nanoparticles for delivery of therapeutics Shu, Dan; Shu, Yi; Haque, Farzin Nature Nanotechnology, Vol. 6, Issue 10 https://doi.org/10.1038/nnano.2011.105	journal	September 2011
Fabrication of pRNA nanoparticles to deliver therapeutic RNAs and bioactive compounds into tumor cells Shu, Yi; Shu, Dan; Haque, Farzin Nature Protocols, Vol. 8, Issue 9 https://doi.org/10.1038/nprot.2013.097	journal	August 2013
The ins and outs of hepatitis C virus entry and assembly Lindenbach, Brett D.; Rice, Charles M. Nature Reviews Microbiology, Vol. 11, Issue 10 https://doi.org/10.1038/nrmicro3098	journal	September 2013
Construction of spherical virus-inspired peptide nanoassemblies Matsuura, Kazunori Polymer Journal, Vol. 44, Issue 6 https://doi.org/10.1038/pj.2012.16	journal	March 2012
Ultra-thermostable RNA nanoparticles for solubilizing and high-yield loading of paclitaxel for breast cancer therapy Guo, Sijin; Vieweger, Mario; Zhang, Kaiming Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14780-5	journal	February 2020
Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid Reguera, J.; Carreira, A.; Riolobos, L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 9 https://doi.org/10.1073/pnas.0307748101	journal	February 2004
Molecular architecture of the prolate head of bacteriophage T4 Fokine, A.; Chipman, P. R.; Leiman, P. G. Proceedings of the National Academy of Sciences, Vol. 101, Issue 16 https://doi.org/10.1073/pnas.0400444101	journal	April 2004
The nucleocapsid protein specifically anneals tRNALys-3 onto a noncomplementary primer binding site within the HIV-1 RNA genome in vitro Chan, B.; Musier-Forsyth, K. Proceedings of the National Academy of Sciences, Vol. 94, Issue 25 https://doi.org/10.1073/pnas.94.25.13530	journal	December 1997
Enhancing immunomodulation on innate immunity by shape transition among RNA triangle, square and pentagon nanovehicles Khisamutdinov, Emil F.; Li, Hui; Jasinski, Daniel L. Nucleic Acids Research, Vol. 42, Issue 15 https://doi.org/10.1093/nar/gku516	journal	August 2014
The tobacco mosaic virus particle: structure and assembly Klug, A. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 354, Issue 1383 https://doi.org/10.1098/rstb.1999.0404	journal	March 1999
Crystal structure of Junin virus nucleoprotein Zhang, Yinjie; Li, Le; Liu, Xiang Journal of General Virology, Vol. 94, Issue 10 https://doi.org/10.1099/vir.0.055053-0	journal	October 2013
Physical Principles in the Construction of Regular Viruses Caspar, D. L. D.; Klug, A. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 27, Issue 0 https://doi.org/10.1101/SQB.1962.027.001.005	journal	January 1962
Icosahedral Packing of RNA Viral Genomes Rudnick, Joseph; Bruinsma, Robijn Physical Review Letters, Vol. 94, Issue 3 https://doi.org/10.1103/PhysRevLett.94.038101	journal	January 2005
Viral nanomotors for packaging of dsDNA and dsRNA Guo, Peixuan; Lee, Tae Jin Molecular Microbiology, Vol. 64, Issue 4 https://doi.org/10.1111/j.1365-2958.2007.05706.x	journal	May 2007
Structure of West Nile Virus Mukhopadhyay, S. Science, Vol. 302, Issue 5643 https://doi.org/10.1126/science.1089316	journal	October 2003
Self-assembled RNA nanostructures Leontis, N. B.; Westhof, E. Science, Vol. 345, Issue 6198 https://doi.org/10.1126/science.1257989	journal	August 2014
X-ray Crystallographic Structure of the Norwalk Virus Capsid Prasad, B. V. V. Science, Vol. 286, Issue 5438 https://doi.org/10.1126/science.286.5438.287	journal	October 1999
The 3.8 A resolution cryo-EM structure of Zika virus Sirohi, D.; Chen, Z.; Sun, L. Science, Vol. 352, Issue 6284 https://doi.org/10.1126/science.aaf5316	journal	March 2016
Cryo-EM structure of a herpesvirus capsid at 3.1 Å Yuan, Shuai; Wang, Jialing; Zhu, Dongjie Science, Vol. 360, Issue 6384 https://doi.org/10.1126/science.aao7283	journal	April 2018
Assembly of Adenoviruses Sundquist, Bo; Everitt, Einar; Philipson, Lennart Journal of Virology, Vol. 11, Issue 3 https://doi.org/10.1128/JVI.11.3.449-459.1973	journal	March 1973
Herpesvirus Assembly and Egress Mettenleiter, Thomas C. Journal of Virology, Vol. 76, Issue 4 https://doi.org/10.1128/JVI.76.4.1537-1547.2002	journal	February 2002
Flavivirus Capsid Is a Dimeric Alpha-Helical Protein Jones, Christopher T.; Ma, Lixin; Burgner, John W. Journal of Virology, Vol. 77, Issue 12 https://doi.org/10.1128/JVI.77.12.7143-7149.2003	journal	June 2003
Adenovirus Dodecahedron Allows Large Multimeric Protein Transduction in Human Cells Fender, P.; Schoehn, G.; Foucaud-Gamen, J. Journal of Virology, Vol. 77, Issue 8 https://doi.org/10.1128/JVI.77.8.4960-4964.2003	journal	April 2003
Assembly of Adenoviruses Sundquist, Bo; Everitt, Einar; Philipson, Lennart Journal of Virology, Vol. 11, Issue 3 https://doi.org/10.1128/jvi.11.3.449-459.1973	journal	March 1973
Mechanisms of Virus Assembly Perlmutter, Jason D.; Hagan, Michael F. Annual Review of Physical Chemistry, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-physchem-040214-121637	journal	April 2015
Properties and Functions of the Dengue Virus Capsid Protein Byk, Laura A.; Gamarnik, Andrea V. Annual Review of Virology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-virology-110615-042334	journal	September 2016
Icosahedral RNA Virus Structure Rossmann, M. G.; Johnson, J. E. Annual Review of Biochemistry, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.bi.58.070189.002533	journal	June 1989
HIV-1: Fifteen Proteins and an RNA Frankel, Alan D.; Young, John A. T. Annual Review of Biochemistry, Vol. 67, Issue 1 https://doi.org/10.1146/annurev.biochem.67.1.1	journal	June 1998
The Structural and Functional Role of RNA in Icosahedral Virus Assembly Schneemann, Anette Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142304	journal	October 2006
RNA Nanotechnology: Engineering, Assembly and Applications in Detection, Gene Delivery and Therapy Guo, Peixuan Journal of Nanoscience and Nanotechnology, Vol. 5, Issue 12 https://doi.org/10.1166/jnn.2005.446	journal	December 2005
Role of RNA-binding proteins during the late stages of Flavivirus replication cycle Diosa-Toro, Mayra; Prasanth, K. Reddisiva; Bradrick, Shelton S. Virology Journal, Vol. 17, Issue 1 https://doi.org/10.1186/s12985-020-01329-7	journal	April 2020
Crystal structure of 3WJ core revealing divalent ion-promoted thermostability and assembly of the Phi29 hexameric motor pRNA Zhang, H.; Endrizzi, J. A.; Shu, Y. RNA, Vol. 19, Issue 9 https://doi.org/10.1261/rna.037077.112	journal	July 2013
Visualizing the global secondary structure of a viral RNA genome with cryo-electron microscopy Garmann, Rees F.; Gopal, Ajaykumar; Athavale, Shreyas S. RNA, Vol. 21, Issue 5 https://doi.org/10.1261/rna.047506.114	journal	March 2015
Assessment and comparison of thermal stability of phosphorothioate-DNA, DNA, RNA, 2′-F RNA, and LNA in the context of Phi29 pRNA 3WJ Piao, Xijun; Wang, Hongzhi; Binzel, Daniel W. RNA, Vol. 24, Issue 1 https://doi.org/10.1261/rna.063057.117	journal	October 2017
Virus-Inspired Design Principles of Nanoparticle-Based Bioagents Yuan, Hongyan; Huang, Changjin; Zhang, Sulin PLoS ONE, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pone.0013495	journal	October 2010
Engineered RNA Nanodesigns for Applications in RNA Nanotechnology Afonin, Kirill A.; Lindsay, Brian; Shapiro, Bruce A. DNA and RNA Nanotechnology, Vol. 1, Issue 1 https://doi.org/10.2478/rnan-2013-0001	journal	January 2013
Monitoring HIV-1 Assembly in Living Cells: Insights from Dynamic and Single Molecule Microscopy Inamdar, Kaushik; Floderer, Charlotte; Favard, Cyril Viruses, Vol. 11, Issue 1 https://doi.org/10.3390/v11010072	journal	January 2019
Foamy Virus Assembly with Emphasis on Pol Encapsidation Lee, Eun-Gyung; Stenbak, Carolyn; Linial, Maxine Viruses, Vol. 5, Issue 3 https://doi.org/10.3390/v5030886	journal	March 2013

Similar Records

Structure of a Venezuelan equine encephalitis virus assembly intermediate isolated from infected cells

Journal Article · Mon Oct 25 00:00:00 EDT 2010 · Virology · OSTI ID:21460281

Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus

Journal Article · Wed Apr 13 20:00:00 EDT 2016 · PLoS Pathogens · OSTI ID:1438860

An alphavirus temperature-sensitive capsid mutant reveals stages of nucleocapsid assembly

Journal Article · Thu Oct 15 00:00:00 EDT 2015 · Virology · OSTI ID:22470195

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
RNA nanostructures
RNA nanotechnology
cage
dodecahedral viral genome

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

Citation Formats

References (80)

Similar Records

Related Subjects