Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions
Abstract
Self-assembly of molecular building blocks into higher-order structures is exploited in living systems to create functional complexity and represents a powerful strategy for constructing new materials. As nanoscale building blocks, proteins offer unique advantages, including monodispersity and atomically tunable interactions. Yet, control of protein self-assembly has been limited compared to inorganic or polymeric nanoparticles, which lack such attributes. Here, we report modular self-assembly of an engineered protein into four physicochemically distinct, precisely patterned 2D crystals via control of four classes of interactions spanning Ångström to several-nanometer length scales. We relate the resulting structures to the underlying free-energy landscape by combining in-situ atomic force microscopy observations of assembly with thermodynamic analyses of protein-protein and -surface interactions. Our results demonstrate rich phase behavior obtainable from a single, highly patchy protein when interactions acting over multiple length scales are exploited and predict unusual bulk-scale properties for protein-based materials that ensue from such control.
- Authors:
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Univ. of Washington, Seattle, WA (United States); Univ. of California, San Diego, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division; National Science Foundation (NSF)
- OSTI Identifier:
- 1643727
- Alternate Identifier(s):
- OSTI ID: 1650710; OSTI ID: 1668312; OSTI ID: 1781109
- Report Number(s):
- PNNL-SA-153945
Journal ID: ISSN 2041-1723; 3770; PII: 17562
- Grant/Contract Number:
- SC0019288; SC0003844; AC05-76RL01830
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; atomic force microscopy; biomaterials; biophysics; nanoscale materials; surface assembly
Citation Formats
Zhang, Shuai, Alberstein, Robert G., De Yoreo, James J., and Tezcan, F. Akif. Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-17562-1.
Zhang, Shuai, Alberstein, Robert G., De Yoreo, James J., & Tezcan, F. Akif. Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions. United Kingdom. https://doi.org/10.1038/s41467-020-17562-1
Zhang, Shuai, Alberstein, Robert G., De Yoreo, James J., and Tezcan, F. Akif. Tue .
"Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions". United Kingdom. https://doi.org/10.1038/s41467-020-17562-1.
@article{osti_1643727,
title = {Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions},
author = {Zhang, Shuai and Alberstein, Robert G. and De Yoreo, James J. and Tezcan, F. Akif},
abstractNote = {Self-assembly of molecular building blocks into higher-order structures is exploited in living systems to create functional complexity and represents a powerful strategy for constructing new materials. As nanoscale building blocks, proteins offer unique advantages, including monodispersity and atomically tunable interactions. Yet, control of protein self-assembly has been limited compared to inorganic or polymeric nanoparticles, which lack such attributes. Here, we report modular self-assembly of an engineered protein into four physicochemically distinct, precisely patterned 2D crystals via control of four classes of interactions spanning Ångström to several-nanometer length scales. We relate the resulting structures to the underlying free-energy landscape by combining in-situ atomic force microscopy observations of assembly with thermodynamic analyses of protein-protein and -surface interactions. Our results demonstrate rich phase behavior obtainable from a single, highly patchy protein when interactions acting over multiple length scales are exploited and predict unusual bulk-scale properties for protein-based materials that ensue from such control.},
doi = {10.1038/s41467-020-17562-1},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Tue Jul 28 00:00:00 EDT 2020},
month = {Tue Jul 28 00:00:00 EDT 2020}
}
https://doi.org/10.1038/s41467-020-17562-1
Web of Science
Works referenced in this record:
Dipole−Dipole Interactions in Nanoparticle Superlattices
journal, May 2007
- Talapin, Dmitri V.; Shevchenko, Elena V.; Murray, Christopher B.
- Nano Letters, Vol. 7, Issue 5, p. 1213-1219
Self-assembly: From nanoscale to microscale colloids
journal, January 2004
- Glotzer, S. C.; Solomon, M. J.; Kotov, N. A.
- AIChE Journal, Vol. 50, Issue 12
Orientation-Averaged Pair Potentials between Dipolar Proteins or Colloids
journal, March 2002
- Bratko, D.; Striolo, A.; Wu, J. Z.
- The Journal of Physical Chemistry B, Vol. 106, Issue 10
Piezoelectric properties in two-dimensional materials: Simulations and experiments
journal, July 2018
- Hinchet, Ronan; Khan, Usman; Falconi, Christian
- Materials Today, Vol. 21, Issue 6
CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data
journal, July 2013
- Huang, Jing; MacKerell, Alexander D.
- Journal of Computational Chemistry, Vol. 34, Issue 25
Detecting Ligand-Binding Events and Free Energy Landscape while Imaging Membrane Receptors at Subnanometer Resolution
journal, April 2017
- Pfreundschuh, Moritz; Harder, Daniel; Ucurum, Zöhre
- Nano Letters, Vol. 17, Issue 5
Controlling protein assembly on inorganic crystals through designed protein interfaces
journal, July 2019
- Pyles, Harley; Zhang, Shuai; De Yoreo, James J.
- Nature, Vol. 571, Issue 7764
Scalable molecular dynamics with NAMD
journal, January 2005
- Phillips, James C.; Braun, Rosemary; Wang, Wei
- Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
Inorganic Nanoparticles as Protein Mimics
journal, October 2010
- Kotov, Nicholas A.
- Science, Vol. 330, Issue 6001
Crystallization by particle attachment in synthetic, biogenic, and geologic environments
journal, July 2015
- De Yoreo, J. J.; Gilbert, P. U. P. A.; Sommerdijk, N. A. J. M.
- Science, Vol. 349, Issue 6247
Stern Layer Structure and Energetics at Mica–Water Interfaces
journal, April 2017
- Bourg, Ian C.; Lee, Sang Soo; Fenter, Paul
- The Journal of Physical Chemistry C, Vol. 121, Issue 17
Multilevel Summation Method for Electrostatic Force Evaluation
journal, January 2015
- Hardy, David J.; Wu, Zhe; Phillips, James C.
- Journal of Chemical Theory and Computation, Vol. 11, Issue 2
Solid–Liquid Interface Structure of Muscovite Mica in CsCl and RbBr Solutions
journal, November 2016
- Pintea, Stelian; de Poel, Wester; de Jong, Aryan E. F.
- Langmuir, Vol. 32, Issue 49
Accurate design of megadalton-scale two-component icosahedral protein complexes
journal, July 2016
- Bale, J. B.; Gonen, S.; Liu, Y.
- Science, Vol. 353, Issue 6297
Structure, Dynamics, Assembly, and Evolution of Protein Complexes
journal, June 2015
- Marsh, Joseph A.; Teichmann, Sarah A.
- Annual Review of Biochemistry, Vol. 84, Issue 1
Control of Pathways and Yields of Protein Crystallization through the Interplay of Nonspecific and Specific Attractions
journal, August 2010
- Whitelam, Stephen
- Physical Review Letters, Vol. 105, Issue 8
Direct observation of kinetic traps associated with structural transformations leading to multiple pathways of S-layer assembly
journal, July 2012
- Shin, S. -H.; Chung, S.; Sanii, B.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 32
Excess chemical potential of dilute solutions of spherical polyelectrolytes
journal, April 1974
- Phillies, George D. J.
- The Journal of Chemical Physics, Vol. 60, Issue 7
New Monte Carlo method to compute the free energy of arbitrary solids. Application to the fcc and hcp phases of hard spheres
journal, October 1984
- Frenkel, Daan; Ladd, Anthony J. C.
- The Journal of Chemical Physics, Vol. 81, Issue 7
Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays
journal, March 2012
- Brodin, Jeffrey D.; Ambroggio, X. I.; Tang, Chunyan
- Nature Chemistry, Vol. 4, Issue 5
Reprogramming an ATP-driven protein machine into a light-gated nanocage
journal, November 2013
- Hoersch, Daniel; Roh, Soung-Hun; Chiu, Wah
- Nature Nanotechnology, Vol. 8, Issue 12
Engineering Crystal Morphology
journal, July 2013
- Dandekar, Preshit; Kuvadia, Zubin B.; Doherty, Michael F.
- Annual Review of Materials Research, Vol. 43, Issue 1
Anisotropy of building blocks and their assembly into complex structures
journal, August 2007
- Glotzer, Sharon C.; Solomon, Michael J.
- Nature Materials, Vol. 6, Issue 8, p. 557-562
Immunoactive two-dimensional self-assembly of monoclonal antibodies in aqueous solution revealed by atomic force microscopy
journal, January 2014
- Ido, Shinichiro; Kimiya, Hirokazu; Kobayashi, Kei
- Nature Materials, Vol. 13, Issue 3
The crystallographically determined structures of atypical strained disulfides engineered into subtilisin.
journal, November 1986
- Katz, B. A.; Kossiakoff, A.
- Journal of Biological Chemistry, Vol. 261, Issue 33
New Look at Hemoglobin Allostery
journal, January 2015
- Yuan, Yue; Tam, Ming F.; Simplaceanu, Virgil
- Chemical Reviews, Vol. 115, Issue 4
Thermodynamically Consistent Force Fields for the Assembly of Inorganic, Organic, and Biological Nanostructures: The INTERFACE Force Field
journal, January 2013
- Heinz, Hendrik; Lin, Tzu-Jen; Kishore Mishra, Ratan
- Langmuir, Vol. 29, Issue 6
S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays
journal, November 2002
- Moll, D.; Huber, C.; Schlegel, B.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
Determination of protein structural flexibility by microsecond force spectroscopy
journal, June 2009
- Dong, Mingdong; Husale, Sudhir; Sahin, Ozgur
- Nature Nanotechnology, Vol. 4, Issue 8
Control of Calcium Phosphate Nucleation and Transformation through Interactions of Enamelin and Amelogenin Exhibits the “Goldilocks Effect”
journal, October 2018
- Tao, Jinhui; Fijneman, Andreas; Wan, Jiaqi
- Crystal Growth & Design, Vol. 18, Issue 12
Water-induced correlation between single ions imaged at the solid–liquid interface
journal, July 2014
- Ricci, Maria; Spijker, Peter; Voïtchovsky, Kislon
- Nature Communications, Vol. 5, Issue 1
Local Electronic Structure of Molecular Heterojunctions in a Single‐Layer 2D Covalent Organic Framework
journal, September 2018
- Joshi, Trinity; Chen, Chen; Li, Huifang
- Advanced Materials, Vol. 31, Issue 3
PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical p K a Predictions
journal, December 2010
- Olsson, Mats H. M.; Søndergaard, Chresten R.; Rostkowski, Michal
- Journal of Chemical Theory and Computation, Vol. 7, Issue 2
Piezoelectricity in cellular electret films
journal, January 2000
- Hillenbrand, J.; Sessler, G. M.
- IEEE Transactions on Dielectrics and Electrical Insulation, Vol. 7, Issue 4
Analysis of solvent content and oligomeric states in protein crystals-does symmetry matter?
journal, April 2008
- Chruszcz, Maksymilian; Potrzebowski, Wojciech; Zimmerman, Matthew D.
- Protein Science, Vol. 17, Issue 4
A server and database for dipole moments of proteins
journal, May 2007
- Felder, C. E.; Prilusky, J.; Silman, I.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Guided hierarchical co-assembly of soft patchy nanoparticles
journal, November 2013
- Gröschel, André H.; Walther, Andreas; Löbling, Tina I.
- Nature, Vol. 503, Issue 7475
Two-step mechanism for the nucleation of crystals from solution
journal, February 2005
- Vekilov, Peter G.
- Journal of Crystal Growth, Vol. 275, Issue 1-2
Energetic landscape of α-lytic protease optimizes longevity through kinetic stability
journal, January 2002
- Jaswal, Sheila S.; Sohl, Julie L.; Davis, Jonathan H.
- Nature, Vol. 415, Issue 6869
Principles for designing ideal protein structures
journal, November 2012
- Koga, Nobuyasu; Tatsumi-Koga, Rie; Liu, Gaohua
- Nature, Vol. 491, Issue 7423
Self-Assembly of Proteins into Designed Networks
journal, October 2003
- Ringler, P.
- Science, Vol. 302, Issue 5642
Crystal Potential Formula for the Calculation of Crystal Lattice Sums 1
journal, May 1998
- Steiger, Don; Ahlbrandt, Calvin; Glaser, Rainer
- The Journal of Physical Chemistry B, Vol. 102, Issue 22
Crystallization at Inorganic-organic Interfaces: Biominerals and Biomimetic Synthesis
journal, September 1993
- Mann, S.; Archibald, D. D.; Didymus, J. M.
- Science, Vol. 261, Issue 5126
Why protein crystals favour some space-groups over others
journal, December 1995
- Wukovitz, Stephanie W.; Yeates, Todd O.
- Nature Structural & Molecular Biology, Vol. 2, Issue 12
Do hierarchical structures assemble best via hierarchical pathways?
journal, January 2013
- Haxton, Thomas K.; Whitelam, Stephen
- Soft Matter, Vol. 9, Issue 29
THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method
journal, October 1992
- Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal
- Journal of Computational Chemistry, Vol. 13, Issue 8
Identification of Single Adsorbed Cations on Mica–Liquid Interfaces by 3D Force Microscopy
journal, November 2017
- Martin-Jimenez, Daniel; Garcia, Ricardo
- The Journal of Physical Chemistry Letters, Vol. 8, Issue 23
S-layers: principles and applications
journal, September 2014
- Sleytr, Uwe B.; Schuster, Bernhard; Egelseer, Eva-Maria
- FEMS Microbiology Reviews, Vol. 38, Issue 5
Supercharging enables organized assembly of synthetic biomolecules
journal, January 2019
- Simon, Anna J.; Zhou, Yi; Ramasubramani, Vyas
- Nature Chemistry, Vol. 11, Issue 3
Geometric Principles for Designing Highly Symmetric Self-Assembling Protein Nanomaterials
journal, May 2017
- Yeates, Todd O.
- Annual Review of Biophysics, Vol. 46, Issue 1
Engineering the entropy-driven free-energy landscape of a dynamic nanoporous protein assembly
journal, April 2018
- Alberstein, Robert; Suzuki, Yuta; Paesani, Francesco
- Nature Chemistry, Vol. 10, Issue 7
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite
journal, October 2017
- Jurrus, Elizabeth; Engel, Dave; Star, Keith
- Protein Science, Vol. 27, Issue 1
Convergence and error estimation in free energy calculations using the weighted histogram analysis method
journal, November 2011
- Zhu, Fangqiang; Hummer, Gerhard
- Journal of Computational Chemistry, Vol. 33, Issue 4
Self-Assembly of CdTe Nanocrystals into Free-Floating Sheets
journal, October 2006
- Tang, Z.; Zhang, Z.; Wang, Y.
- Science, Vol. 314, Issue 5797
Imaging α-Hemolysin with Molecular Dynamics: Ionic Conductance, Osmotic Permeability, and the Electrostatic Potential Map
journal, June 2005
- Aksimentiev, Aleksij; Schulten, Klaus
- Biophysical Journal, Vol. 88, Issue 6
Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals
journal, May 2016
- Suzuki, Yuta; Cardone, Giovanni; Restrepo, David
- Nature, Vol. 533, Issue 7603
Determination of Alkali and Halide Monovalent Ion Parameters for Use in Explicitly Solvated Biomolecular Simulations
journal, July 2008
- Joung, In Suk; Cheatham, Thomas E.
- The Journal of Physical Chemistry B, Vol. 112, Issue 30
Monte Carlo Computer Simulation of Chain Formation from Nanoparticles
journal, April 2006
- Sinyagin, Alex Y.; Belov, Artem; Tang, Zhioyng
- The Journal of Physical Chemistry B, Vol. 110, Issue 14
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1
Self-assembly and applications of anisotropic nanomaterials: A review
journal, February 2015
- Thorkelsson, Kari; Bai, Peter; Xu, Ting
- Nano Today, Vol. 10, Issue 1
Electrostatic assembly of binary nanoparticle superlattices using protein cages
journal, December 2012
- Kostiainen, Mauri A.; Hiekkataipale, Panu; Laiho, Ari
- Nature Nanotechnology, Vol. 8, Issue 1
Design and Construction of Functional Supramolecular Metalloprotein Assemblies
journal, January 2019
- Churchfield, Lewis A.; Tezcan, F. Akif
- Accounts of Chemical Research, Vol. 52, Issue 2