Designed 2D protein crystals as dynamic molecular gatekeepers for a solid-state device

Vijayakumar, Sanahan; Alberstein, Robert G.; Zhang, Zhiyin; Lu, Yi-Sheng; Chan, Adriano; Wahl, Charlotte E.; Ha, James S.; Hunka, Deborah E.; Boss, Gerry R.; Sailor, Michael J.; Tezcan, F. Akif

doi:10.1038/s41467-024-50567-8

Title: Designed 2D protein crystals as dynamic molecular gatekeepers for a solid-state device

Journal Article · 27 July 2024 · Nature Communications

DOI: https://doi.org/10.1038/s41467-024-50567-8 · OSTI ID:2406987

Vijayakumar, Sanahan; Alberstein, Robert G.; Zhang, Zhiyin; Lu, Yi-Sheng; Chan, Adriano; Wahl, Charlotte E.; Ha, James S.;

; Boss, Gerry R.;

;

Abstract The sensitivity and responsiveness of living cells to environmental changes are enabled by dynamic protein structures, inspiring efforts to construct artificial supramolecular protein assemblies. However, despite their sophisticated structures, designed protein assemblies have yet to be incorporated into macroscale devices for real-life applications. We report a 2D crystalline protein assembly of ^C98/E57/E66 L-rhamnulose-1-phosphate aldolase ( ^CEE RhuA) that selectively blocks or passes molecular species when exposed to a chemical trigger. ^CEE RhuA crystals are engineered via cobalt(II) coordination bonds to undergo a coherent conformational change from a closed state (pore dimensions <1 nm) to an ajar state (pore dimensions ~4 nm) when exposed to an HCN(g) trigger. When layered onto a mesoporous silicon (pSi) photonic crystal optical sensor configured to detect HCN _(g) , the 2D ^CEE RhuA crystal layer effectively blocks interferents that would otherwise result in a false positive signal. The 2D ^CEE RhuA crystal layer opens in selective response to low-ppm levels of HCN _(g) , allowing analyte penetration into the pSi sensor layer for detection. These findings illustrate that designed protein assemblies can function as dynamic components of solid-state devices in non-aqueous environments.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0003844; SC0019288

OSTI ID:: 2406987

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (69)

Cyano Compounds, Inorganic Gail, Ernst; Gos, Stephen; Kulzer, Rupprecht Ullmann's Encyclopedia of Industrial Chemistry https://doi.org/10.1002/14356007.a08_159.pub3	book	January 2011
Porous Silicon‐Based Optical Microsensors for Volatile Organic Analytes: Effect of Surface Chemistry on Stability and Specificity Ruminski, Anne M.; King, Brian H.; Salonen, Jarno Advanced Functional Materials, Vol. 20, Issue 17 https://doi.org/10.1002/adfm.201000575	journal	September 2010
Internally Referenced Remote Sensors for HF and Cl₂ Using Reactive Porous Silicon Photonic Crystals Ruminski, Anne M.; Barillaro, Giuseppe; Chaffin, Charles Advanced Functional Materials, Vol. 21, Issue 8 https://doi.org/10.1002/adfm.201002037	journal	March 2011
Covalent Organic Frameworks: Structures, Synthesis, and Applications Lohse, Maria S.; Bein, Thomas Advanced Functional Materials, Vol. 28, Issue 33 https://doi.org/10.1002/adfm.201705553	journal	July 2018
Internally Referenced Ammonia Sensor Based on an Electrochemically Prepared Porous SiO2 Photonic Crystal King, B. H.; Gramada, A.; Link, J. R. Advanced Materials, Vol. 19, Issue 22 https://doi.org/10.1002/adma.200602860	journal	November 2007
25th Anniversary Article: MXenes: A New Family of Two-Dimensional Materials Naguib, Michael; Mochalin, Vadym N.; Barsoum, Michel W. Advanced Materials, Vol. 26, Issue 7, p. 992-1005 https://doi.org/10.1002/adma.201304138	journal	December 2013
Ultrathin Membranes for Separations: A New Era Driven by Advanced Nanotechnology Zhang, Shiyu; Shen, Liang; Deng, Hao Advanced Materials, Vol. 34, Issue 21 https://doi.org/10.1002/adma.202108457	journal	March 2022
Recent Progress of Protein‐Based Data Storage and Neuromorphic Devices Wang, Junjie; Qian, Fangsheng; Huang, Shenming Advanced Intelligent Systems, Vol. 3, Issue 1 https://doi.org/10.1002/aisy.202000180	journal	November 2020
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data Huang, Jing; MacKerell, Alexander D. Journal of Computational Chemistry, Vol. 34, Issue 25 https://doi.org/10.1002/jcc.23354	journal	July 2013
UCSF ChimeraX : Structure visualization for researchers, educators, and developers Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Protein Science, Vol. 30, Issue 1 https://doi.org/10.1002/pro.3943	journal	October 2020
The Vitamin B12 Analog Cobinamide Is an Effective Antidote for Oral Cyanide Poisoning Lee, Jangwoen; Mahon, Sari B.; Mukai, David Journal of Medical Toxicology, Vol. 12, Issue 4 https://doi.org/10.1007/s13181-016-0566-4	journal	September 2016
Neurotransmitter action: Opening of ligand-gated ion channels Unwin, Nigel Cell, Vol. 72 https://doi.org/10.1016/S0092-8674(05)80026-1	journal	January 1993
Cobinamide chemistries for photometric cyanide determination. A merging zone liquid core waveguide cyanide analyzer using cyanoaquacobinamide Ma, Jian; Dasgupta, Purnendu K.; Zelder, Felix H. Analytica Chimica Acta, Vol. 736 https://doi.org/10.1016/j.aca.2012.05.028	journal	July 2012
Elucidation of flexible metal-organic frameworks: Research progresses and recent developments Lee, Jae Hwa; Jeoung, Sungeun; Chung, Yongchul G. Coordination Chemistry Reviews, Vol. 389 https://doi.org/10.1016/j.ccr.2019.03.008	journal	June 2019
Two-dimensional material membrane fabrication: progress and challenges Tian, Shengji; Pan, Qingqing; Li, Haowen Current Opinion in Chemical Engineering, Vol. 39 https://doi.org/10.1016/j.coche.2023.100900	journal	March 2023
Development of a cobinamide-based end-of-service-life indicator for detection of hydrogen cyanide gas Greenawald, Lee A.; Snyder, Jay L.; Fry, Nicole L. Sensors and Actuators B: Chemical, Vol. 221 https://doi.org/10.1016/j.snb.2015.06.085	journal	December 2015
Mechanosensitive Channels: What Can They Do and How Do They Do It? Haswell, Elizabeth S.; Phillips, Rob; Rees, Douglas C. Structure, Vol. 19, Issue 10 https://doi.org/10.1016/j.str.2011.09.005	journal	October 2011
Two-Dimensional Metal-Organic Framework Materials: Synthesis, Structures, Properties and Applications Chakraborty, Gouri; Park, In-Hyeok; Medishetty, Raghavender Chemical Reviews, Vol. 121, Issue 7 https://doi.org/10.1021/acs.chemrev.0c01049	journal	February 2021
Protein Assembly by Design Zhu, Jie; Avakyan, Nicole; Kakkis, Albert Chemical Reviews, Vol. 121, Issue 22 https://doi.org/10.1021/acs.chemrev.1c00308	journal	August 2021
Layer-Structured Anisotropic Metal Chalcogenides: Recent Advances in Synthesis, Modulation, and Applications Giri, Anupam; Park, Gyeongbae; Jeong, Unyong Chemical Reviews, Vol. 123, Issue 7 https://doi.org/10.1021/acs.chemrev.2c00455	journal	January 2023
MXenes: Two-Dimensional Building Blocks for Future Materials and Devices Gogotsi, Yury; Huang, Qing ACS Nano, Vol. 15, Issue 4 https://doi.org/10.1021/acsnano.1c03161	journal	April 2021
Remote Detection of HCN, HF, and Nerve Agent Vapors Based on Self-Referencing, Dye-Impregnated Porous Silicon Photonic Crystals Lu, Yi-Sheng; Vijayakumar, Sanahan; Chaix, Arnaud ACS Sensors, Vol. 6, Issue 2 https://doi.org/10.1021/acssensors.0c01931	journal	December 2020
Structure and Catalytic Mechanism of l-Rhamnulose-1-phosphate Aldolase^, Kroemer, Markus; Merkel, Iris; Schulz, Georg E. Biochemistry, Vol. 42, Issue 36 https://doi.org/10.1021/bi0349266	journal	August 2003
Multilevel Summation Method for Electrostatic Force Evaluation Hardy, David J.; Wu, Zhe; Phillips, James C. Journal of Chemical Theory and Computation, Vol. 11, Issue 2 https://doi.org/10.1021/ct5009075	journal	January 2015
A Crystalline Imine-Linked 3-D Porous Covalent Organic Framework Uribe-Romo, Fernando J.; Hunt, Joseph R.; Furukawa, Hiroyasu Journal of the American Chemical Society, Vol. 131, Issue 13, p. 4570-4571 https://doi.org/10.1021/ja8096256	journal	April 2009
Tunable and Cooperative Thermomechanical Properties of Protein–Metal–Organic Frameworks Bailey, Jake B.; Tezcan, F. Akif Journal of the American Chemical Society, Vol. 142, Issue 41 https://doi.org/10.1021/jacs.0c07835	journal	September 2020
Covalent Chemistry beyond Molecules Jiang, Juncong; Zhao, Yingbo; Yaghi, Omar M. Journal of the American Chemical Society, Vol. 138, Issue 10 https://doi.org/10.1021/jacs.5b10666	journal	February 2016
Facile Surface Modification of Hydroxylated Silicon Nanostructures Using Heterocyclic Silanes Kim, Dokyoung; Zuidema, Jonathan M.; Kang, Jinyoung Journal of the American Chemical Society, Vol. 138, Issue 46 https://doi.org/10.1021/jacs.6b08614	journal	November 2016
Guest-Dependent Dynamics in a 3D Covalent Organic Framework Chen, Yichong; Shi, Zhao-Lin; Wei, Lei Journal of the American Chemical Society, Vol. 141, Issue 7 https://doi.org/10.1021/jacs.8b13691	journal	January 2019
Biomolecular Electronics: Protein-Based Associative Processors and Volumetric Memories Birge, Robert R.; Gillespie, Nathan B.; Izaguirre, Enrique W. The Journal of Physical Chemistry B, Vol. 103, Issue 49 https://doi.org/10.1021/jp991883n	journal	November 1999
Antibody arrays for high-throughput screening of antibody–antigen interactions de Wildt, Ruud M. T.; Mundy, Chris R.; Gorick, Barbara D. Nature Biotechnology, Vol. 18, Issue 9 https://doi.org/10.1038/79494	journal	September 2000
Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals Suzuki, Yuta; Cardone, Giovanni; Restrepo, David Nature, Vol. 533, Issue 7603 https://doi.org/10.1038/nature17633	journal	May 2016
Beyond natural antibodies: the power of in vitro display technologies Bradbury, Andrew R. M.; Sidhu, Sachdev; Dübel, Stefan Nature Biotechnology, Vol. 29, Issue 3 https://doi.org/10.1038/nbt.1791	journal	March 2011
Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays Brodin, Jeffrey D.; Ambroggio, X. I.; Tang, Chunyan Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1290	journal	March 2012
Soft porous crystals Horike, Satoshi; Shimomura, Satoru; Kitagawa, Susumu Nature Chemistry, Vol. 1, Issue 9, p. 695-704 https://doi.org/10.1038/nchem.444	journal	November 2009
Continuous base identification for single-molecule nanopore DNA sequencing Clarke, James; Wu, Hai-Chen; Jayasinghe, Lakmal Nature Nanotechnology, Vol. 4, Issue 4, p. 265-270 https://doi.org/10.1038/nnano.2009.12	journal	February 2009
Solid-state nanopores towards single-molecule DNA sequencing Goto, Yusuke; Akahori, Rena; Yanagi, Itaru Journal of Human Genetics, Vol. 65, Issue 1 https://doi.org/10.1038/s10038-019-0655-8	journal	August 2019
Assembly of a patchy protein into variable 2D lattices via tunable multiscale interactions Zhang, Shuai; Alberstein, Robert G.; De Yoreo, James J. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17562-1	journal	July 2020
Engineering the entropy-driven free-energy landscape of a dynamic nanoporous protein assembly Alberstein, Robert; Suzuki, Yuta; Paesani, Francesco Nature Chemistry, Vol. 10, Issue 7 https://doi.org/10.1038/s41557-018-0053-4	journal	April 2018
Constructing protein polyhedra via orthogonal chemical interactions Golub, Eyal; Subramanian, Rohit H.; Esselborn, Julian Nature, Vol. 578, Issue 7793 https://doi.org/10.1038/s41586-019-1928-2	journal	January 2020
Design of biologically active binary protein 2D materials Ben-Sasson, Ariel J.; Watson, Joseph L.; Sheffler, William Nature, Vol. 589, Issue 7842 https://doi.org/10.1038/s41586-020-03120-8	journal	January 2021
Discoveries in structure and physiology of mechanically activated ion channels Kefauver, J. M.; Ward, A. B.; Patapoutian, A. Nature, Vol. 587, Issue 7835 https://doi.org/10.1038/s41586-020-2933-1	journal	November 2020
2D materials: to graphene and beyond Mas-Ballesté, Rubén; Gómez-Navarro, Cristina; Gómez-Herrero, Julio Nanoscale, Vol. 3, Issue 1 https://doi.org/10.1039/C0NR00323A	journal	January 2011
Flexible metal–organic frameworks Schneemann, A.; Bon, V.; Schwedler, I. Chem. Soc. Rev., Vol. 43, Issue 16 https://doi.org/10.1039/C4CS00101J	journal	January 2014
Protein self-assembly via supramolecular strategies Bai, Yushi; Luo, Quan; Liu, Junqiu Chemical Society Reviews, Vol. 45, Issue 10 https://doi.org/10.1039/C6CS00004E	journal	January 2016
Silkworm silk-based materials and devices generated using bio-nanotechnology Huang, Wenwen; Ling, Shengjie; Li, Chunmei Chemical Society Reviews, Vol. 47, Issue 17 https://doi.org/10.1039/C8CS00187A	journal	January 2018
Two-dimensional metal–organic framework nanosheets: synthesis and applications Zhao, Meiting; Huang, Ying; Peng, Yongwu Chemical Society Reviews, Vol. 47, Issue 16 https://doi.org/10.1039/C8CS00268A	journal	January 2018
Two-dimensional material membranes for critical separations Liu, Pengchao; Hou, Junjun; Zhang, Yi Inorganic Chemistry Frontiers, Vol. 7, Issue 13 https://doi.org/10.1039/D0QI00307G	journal	January 2020
2D framework materials for energy applications Schneemann, Andreas; Dong, Renhao; Schwotzer, Friedrich Chemical Science, Vol. 12, Issue 5 https://doi.org/10.1039/D0SC05889K	journal	January 2021
Single-molecular protein-based bioelectronicsviaelectronic transport: fundamentals, devices and applications Jiang, Tao; Zeng, Biao-Feng; Zhang, Bintian Chemical Society Reviews, Vol. 52, Issue 17 https://doi.org/10.1039/D2CS00519K	journal	January 2023
Applications of peptide and protein-based materials in bionanotechnology de la Rica, Roberto; Matsui, Hiroshi Chemical Society Reviews, Vol. 39, Issue 9 https://doi.org/10.1039/b917574c	journal	January 2010
Enzyme entrapment in electrically conducting polymers. Immobilisation of glucose oxidase in polypyrrole and its application in amperometric glucose sensors Foulds, Nicola C.; Lowe, Christopher R. Journal of the Chemical Society, Faraday Transactions 1: Physical Chemistry in Condensed Phases, Vol. 82, Issue 4 https://doi.org/10.1039/f19868201259	journal	January 1986
Biological membranes Watson, Helen Essays in Biochemistry, Vol. 59 https://doi.org/10.1042/bse0590043	journal	October 2015
Two-dimensional atomic crystals Novoselov, K. S.; Jiang, D.; Schedin, F. Proceedings of the National Academy of Sciences, Vol. 102, Issue 30, p. 10451-10453 https://doi.org/10.1073/pnas.0502848102	journal	July 2005
Membrane protein-based biosensors Misawa, Nobuo; Osaki, Toshihisa; Takeuchi, Shoji Journal of The Royal Society Interface, Vol. 15, Issue 141 https://doi.org/10.1098/rsif.2017.0952	journal	April 2018
Glucose sensors: a review of current and emerging technology Oliver, N. S.; Toumazou, C.; Cass, A. E. G. Diabetic Medicine, Vol. 26, Issue 3 https://doi.org/10.1111/j.1464-5491.2008.02642.x	journal	March 2009
Designing and defining dynamic protein cage nanoassemblies in solution Lai, Yen-Ting; Hura, Greg L.; Dyer, Kevin N. Science Advances, Vol. 2, Issue 12 https://doi.org/10.1126/sciadv.1501855	journal	December 2016
Electric Field Effect in Atomically Thin Carbon Films Novoselov, K. S. Science, Vol. 306, Issue 5696, p. 666-669 https://doi.org/10.1126/science.1102896	journal	October 2004
A designed supramolecular protein assembly with in vivo enzymatic activity Song, Woon Ju; Tezcan, F. Akif Science, Vol. 346, Issue 6216 https://doi.org/10.1126/science.1259680	journal	December 2014
A Porous Silicon-Based Optical Interferometric Biosensor Lin, V. S. Science, Vol. 278, Issue 5339 https://doi.org/10.1126/science.278.5339.840	journal	October 1997
Design of ordered two-dimensional arrays mediated by noncovalent protein-protein interfaces Gonen, S.; DiMaio, F.; Gonen, T. Science, Vol. 348, Issue 6241 https://doi.org/10.1126/science.aaa9897	journal	June 2015
Weaving of organic threads into a crystalline covalent organic framework Liu, Y.; Ma, Y.; Zhao, Y. Science, Vol. 351, Issue 6271 https://doi.org/10.1126/science.aad4011	journal	January 2016
Accurate design of megadalton-scale two-component icosahedral protein complexes Bale, J. B.; Gonen, S.; Liu, Y. Science, Vol. 353, Issue 6297 https://doi.org/10.1126/science.aaf8818	journal	July 2016
Reconfigurable asymmetric protein assemblies through implicit negative design Sahtoe, Danny D.; Praetorius, Florian; Courbet, Alexis Science, Vol. 375, Issue 6578 https://doi.org/10.1126/science.abj7662	journal	January 2022
Top-down design of protein architectures with reinforcement learning Lutz, Isaac D.; Wang, Shunzhi; Norn, Christoffer Science, Vol. 380, Issue 6642 https://doi.org/10.1126/science.adf6591	journal	April 2023
TRP Channels and Pain Julius, David Annual Review of Cell and Developmental Biology, Vol. 29, Issue 1 https://doi.org/10.1146/annurev-cellbio-101011-155833	journal	October 2013
Structure and Function of Voltage-Gated Ion Channels Catterall, William A. Annual Review of Biochemistry, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.bi.64.070195.002425	journal	June 1995
Structure and Function of Cyclic Nucleotide-Gated Channels Zagotta, W. N.; Siegelbaum, S. A. Annual Review of Neuroscience, Vol. 19, Issue 1 https://doi.org/10.1146/annurev.ne.19.030196.001315	journal	March 1996

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