Stimuli Responsive Hierarchical Assembly of P22 Virus-like Particles

Aumiller, Jr., William M.; Uchida, Masaki; Biner, Daniel W.; Miettinen, Heini M.; Lee, Byeongdu; Douglas, Trevor

doi:10.1021/acs.chemmater.7b04964

Stimuli Responsive Hierarchical Assembly of P22 Virus-like Particles

Journal Article · Thu Mar 15 04:00:00 EDT 2018 · Chemistry of Materials

DOI:https://doi.org/10.1021/acs.chemmater.7b04964· OSTI ID:1461344

^[1]; ^[1]; Biner, Daniel W. ^[1]; Miettinen, Heini M. ^[2]; ^[3]; ^[1]

Indiana Univ., Bloomington, IN (United States)
Montana State Univ., Bozeman, MT (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)

Biomimetic systems responsive to environmental stimuli are of growing interest due to their useful, intriguing, and sometimes unexpected properties. Hierarchical self-assembly of biological building blocks has emerged as a powerful means of creating biomaterials with collective properties. Here, we show P22 virus-like particles (VLPs) functionalized with a spider silk protein derivative on the capsid exterior assemble into a hierarchical structure due to spider silk/spider silk interactions at low pH and reversibly dissemble upon raising the pH. We also show that the capsid arrays can be assembled through electrostatic interaction between the negatively charged capsids and a positively supercharged GFP mutant and can be reversed by raising the ionic strength. Most notably, we found that the supercharged GFP could bind to the hierarchically assembled material under high salt conditions but not to the individual capsids under the same high salt conditions. As a result, the binding of the charged macromolecule under high salt conditions demonstrates a collective behavior of the hierarchically assembled system that is not present with the unassembled, individual components of the system.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1461344

Journal Information:: Chemistry of Materials, Journal Name: Chemistry of Materials Journal Issue: 7 Vol. 30; ISSN 0897-4756

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (50)

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
Higher Order Assembly of Virus-like Particles (VLPs) Mediated by Multi-valent Protein Linkers Uchida, Masaki; LaFrance, Ben; Broomell, Chris C. Small, Vol. 11, Issue 13 https://doi.org/10.1002/smll.201402067	journal	January 2015
Assembly, stability and dynamics of virus capsids Mateu, Mauricio G. Archives of Biochemistry and Biophysics, Vol. 531, Issue 1-2 https://doi.org/10.1016/j.abb.2012.10.015	journal	March 2013
Coordination and collective properties of molecular motors: theory Guérin, Thomas; Prost, Jacques; Martin, Pascal Current Opinion in Cell Biology, Vol. 22, Issue 1 https://doi.org/10.1016/j.ceb.2009.12.012	journal	February 2010
Atom transfer radical polymerization on the interior of the P22 capsid and incorporation of photocatalytic monomer crosslinks Lucon, Janice; Edwards, Ethan; Qazi, Shefah European Polymer Journal, Vol. 49, Issue 10 https://doi.org/10.1016/j.eurpolymj.2013.06.010	journal	October 2013
Hydrogels in a historical perspective: From simple networks to smart materials Buwalda, Sytze J.; Boere, Kristel W. M.; Dijkstra, Pieter J. Journal of Controlled Release, Vol. 190 https://doi.org/10.1016/j.jconrel.2014.03.052	journal	September 2014
pH‐Dependent Dimerization of Spider Silk N-Terminal Domain Requires Relocation of a Wedged Tryptophan Side Chain Jaudzems, Kristaps; Askarieh, Glareh; Landreh, Michael Journal of Molecular Biology, Vol. 422, Issue 4 https://doi.org/10.1016/j.jmb.2012.06.004	journal	September 2012
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
Regular pattern formation in real ecosystems Rietkerk, Max; van de Koppel, Johan Trends in Ecology & Evolution, Vol. 23, Issue 3 https://doi.org/10.1016/j.tree.2007.10.013	journal	March 2008
Small Angle X-ray Scattering for Nanoparticle Research Li, Tao; Senesi, Andrew J.; Lee, Byeongdu Chemical Reviews, Vol. 116, Issue 18 https://doi.org/10.1021/acs.chemrev.5b00690	journal	April 2016
Programmed Self-Assembly of an Active P22-Cas9 Nanocarrier System Qazi, Shefah; Miettinen, Heini M.; Wilkinson, Royce A. Molecular Pharmaceutics, Vol. 13, Issue 3 https://doi.org/10.1021/acs.molpharmaceut.5b00822	journal	January 2016
Combining Protein Cages and Polymers: from Understanding Self-Assembly to Functional Materials Maassen, Stan J.; van der Ham, Anne M.; Cornelissen, Jeroen J. L. M. ACS Macro Letters, Vol. 5, Issue 8 https://doi.org/10.1021/acsmacrolett.6b00509	journal	August 2016
Symmetry Controlled, Genetic Presentation of Bioactive Proteins on the P22 Virus-like Particle Using an External Decoration Protein Schwarz, Benjamin; Madden, Patrick; Avera, John ACS Nano, Vol. 9, Issue 9 https://doi.org/10.1021/acsnano.5b03360	journal	August 2015
Electrostatic Self-Assembly of Soft Matter Nanoparticle Cocrystals with Tunable Lattice Parameters Liljeström, Ville; Seitsonen, Jani; Kostiainen, Mauri A. ACS Nano, Vol. 9, Issue 11 https://doi.org/10.1021/acsnano.5b04912	journal	October 2015
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
Structural Properties of Recombinant Nonrepetitive and Repetitive Parts of Major Ampullate Spidroin 1 from Euprosthenops australis : Implications for Fiber Formation Hedhammar, My; Rising, Anna; Grip, Stefan Biochemistry, Vol. 47, Issue 11 https://doi.org/10.1021/bi702432y	journal	February 2008
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
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
Hydrolysis of D-glucono-.delta.-lactone. I. General acid-base catalysis, solvent deuterium isotope effects, and transition state characterization Pocker, Y.; Green, Edmond. Journal of the American Chemical Society, Vol. 95, Issue 1 https://doi.org/10.1021/ja00782a019	journal	January 1973
Self-Assembly Mechanism for a Naphthalene−Dipeptide Leading to Hydrogelation Chen, Lin; Morris, Kyle; Laybourn, Andrea Langmuir, Vol. 26, Issue 7 https://doi.org/10.1021/la903694a	journal	November 2009
Dual-Surface Modified Virus Capsids for Targeted Delivery of Photodynamic Agents to Cancer Cells Stephanopoulos, Nicholas; Tong, Gary J.; Hsiao, Sonny C. ACS Nano, Vol. 4, Issue 10 https://doi.org/10.1021/nn1014769	journal	September 2010
Structural diversity in binary nanoparticle superlattices Shevchenko, Elena V.; Talapin, Dmitri V.; Kotov, Nicholas A. Nature, Vol. 439, Issue 7072, p. 55-59 https://doi.org/10.1038/nature04414	journal	January 2006
Self-assembly of spider silk proteins is controlled by a pH-sensitive relay Askarieh, Glareh; Hedhammar, My; Nordling, Kerstin Nature, Vol. 465, Issue 7295 https://doi.org/10.1038/nature08962	journal	May 2010
Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo Zuris, John A.; Thompson, David B.; Shu, Yilai Nature Biotechnology, Vol. 33, Issue 1 https://doi.org/10.1038/nbt.3081	journal	October 2014
Use of the interior cavity of the P22 capsid for site-specific initiation of atom-transfer radical polymerization with high-density cargo loading Lucon, Janice; Qazi, Shefah; Uchida, Masaki Nature Chemistry, Vol. 4, Issue 10 https://doi.org/10.1038/nchem.1442	journal	August 2012
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
Self-assembly and optically triggered disassembly of hierarchical dendron–virus complexes Kostiainen, Mauri A.; Kasyutich, Oksana; Cornelissen, Jeroen J. L. M. Nature Chemistry, Vol. 2, Issue 5 https://doi.org/10.1038/nchem.592	journal	March 2010
Toward spinning artificial spider silk Rising, Anna; Johansson, Jan Nature Chemical Biology, Vol. 11, Issue 5 https://doi.org/10.1038/nchembio.1789	journal	April 2015
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
Sequential pH-driven dimerization and stabilization of the N-terminal domain enables rapid spider silk formation Kronqvist, Nina; Otikovs, Martins; Chmyrov, Volodymyr Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4254	journal	February 2014
Emerging applications of stimuli-responsive polymer materials Stuart, Martien A. Cohen; Huck, Wilhelm T. S.; Genzer, Jan Nature Materials, Vol. 9, Issue 2, p. 101-113 https://doi.org/10.1038/nmat2614	journal	January 2010
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
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
A general strategy for the DNA-mediated self-assembly of functional nanoparticles into heterogeneous systems Zhang, Yugang; Lu, Fang; Yager, Kevin G. Nature Nanotechnology, Vol. 8, Issue 11 https://doi.org/10.1038/nnano.2013.209	journal	October 2013
Biofilms: an emergent form of bacterial life Flemming, Hans-Curt; Wingender, Jost; Szewzyk, Ulrich Nature Reviews Microbiology, Vol. 14, Issue 9 https://doi.org/10.1038/nrmicro.2016.94	journal	August 2016
Bacterial biofilms: from the Natural environment to infectious diseases Hall-Stoodley, Luanne; Costerton, J. William; Stoodley, Paul Nature Reviews Microbiology, Vol. 2, Issue 2, p. 95-108 https://doi.org/10.1038/nrmicro821	journal	February 2004
CO ₂ -Responsive polymer materials Liu, Hanbin; Lin, Shaojian; Feng, Yujun Polymer Chemistry, Vol. 8, Issue 1 https://doi.org/10.1039/C6PY01101B	journal	January 2017
Stimuli-responsive polymers and their applications Wei, Menglian; Gao, Yongfeng; Li, Xue Polymer Chemistry, Vol. 8, Issue 1 https://doi.org/10.1039/C6PY01585A	journal	January 2017
pH-Responsive polymers Kocak, G.; Tuncer, C.; Bütün, V. Polymer Chemistry, Vol. 8, Issue 1 https://doi.org/10.1039/C6PY01872F	journal	January 2017
UV light- and thermo-responsive hierarchical assemblies based on the inclusion complexation of β-cyclodextrin and azobenzene Zou, Hui; Lu, Yeqiang; Yuan, Weizhong Polymer Chemistry, Vol. 8, Issue 4 https://doi.org/10.1039/C6PY02016J	journal	January 2017
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
pH-Responsive polymers: synthesis, properties and applications Dai, Sheng; Ravi, Palaniswamy; Tam, Kam Chiu Soft Matter, Vol. 4, Issue 3 https://doi.org/10.1039/b714741d	journal	January 2008
Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles Liu, Zhi; Qiao, Jing; Niu, Zhongwei Chemical Society Reviews, Vol. 41, Issue 18 https://doi.org/10.1039/c2cs35108k	journal	January 2012
DNA-mediated engineering of multicomponent enzyme crystals Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A. Proceedings of the National Academy of Sciences, Vol. 112, Issue 15 https://doi.org/10.1073/pnas.1503533112	journal	March 2015
The concept of self-organization in cellular architecture Misteli, Tom The Journal of Cell Biology, Vol. 155, Issue 2 https://doi.org/10.1083/jcb.200108110	journal	October 2001
What drives bacteria to produce a biofilm? Jefferson, Kimberly K. FEMS Microbiology Letters, Vol. 236, Issue 2 https://doi.org/10.1111/j.1574-6968.2004.tb09643.x	journal	July 2004
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
Viruses: Making Friends with Old Foes Douglas, T. Science, Vol. 312, Issue 5775 https://doi.org/10.1126/science.1123223	journal	May 2006
Directed Evolution of a Protein Container Worsdorfer, B.; Woycechowsky, K. J.; Hilvert, D. Science, Vol. 331, Issue 6017 https://doi.org/10.1126/science.1199081	journal	February 2011
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

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