Large-scale design and refinement of stable proteins using sequence-only models

Singer, Jedediah M.; Novotney, Scott; Strickland, Devin; Haddox, Hugh K.; Leiby, Nicholas; Rocklin, Gabriel J.; Chow, Cameron M.; Roy, Anindya; Bera, Asim K.; Motta, Francis C.; Cao, Longxing; Strauch, Eva-Maria; Chidyausiku, Tamuka M.; Ford, Alex; Ho, Ethan; Zaitzeff, Alexander; Mackenzie, Craig O.; Eramian, Hamed; DiMaio, Frank; Grigoryan, Gevorg; Vaughn, Matthew; Stewart, Lance J.; Baker, David; Klavins, Eric

doi:10.1371/journal.pone.0265020

Title: Large-scale design and refinement of stable proteins using sequence-only models

Journal Article · 01 March 2022 · PLoS One

DOI:https://doi.org/10.1371/journal.pone.0265020· OSTI ID:1878389

Singer, Jedediah M.; Novotney, Scott; Strickland, Devin; Haddox, Hugh K.; Leiby, Nicholas; Rocklin, Gabriel J.; Chow, Cameron M.; Roy, Anindya; Bera, Asim K.; Motta, Francis C.; Cao, Longxing; Strauch, Eva-Maria; Chidyausiku, Tamuka M.; Ford, Alex; Ho, Ethan; Zaitzeff, Alexander; Mackenzie, Craig O.; Eramian, Hamed; DiMaio, Frank; Grigoryan, Gevorg more »

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: DOE - Office Of Science; Defense Advanced Research Projects Agency (DARPA)

OSTI ID:: 1878389

Journal Information:: PLoS One, Vol. 17, Issue (3)

Country of Publication:: United States

Language:: ENGLISH

References (64)

Massively parallel de novo protein design for targeted therapeutics Chevalier, Aaron; Silva, Daniel-Adriano; Rocklin, Gabriel J. Nature, Vol. 550, Issue 7674 https://doi.org/10.1038/nature23912	journal	September 2017
De Novo Computational Design of Retro-Aldol Enzymes Jiang, L.; Althoff, E. A.; Clemente, F. R. Science, Vol. 319, Issue 5868 https://doi.org/10.1126/science.1152692	journal	March 2008
Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy King, N. P.; Sheffler, W.; Sawaya, M. R. Science, Vol. 336, Issue 6085 https://doi.org/10.1126/science.1219364	journal	May 2012
The Rosetta All-Atom Energy Function for Macromolecular Modeling and Design Alford, Rebecca F.; Leaver-Fay, Andrew; Jeliazkov, Jeliazko R. Journal of Chemical Theory and Computation, Vol. 13, Issue 6 https://doi.org/10.1021/acs.jctc.7b00125	journal	May 2017
Protein stability: computation, sequence statistics, and new experimental methods Magliery, Thomas J. Current Opinion in Structural Biology, Vol. 33 https://doi.org/10.1016/j.sbi.2015.09.002	journal	August 2015
Machine learning for protein folding and dynamics Noé, Frank; De Fabritiis, Gianni; Clementi, Cecilia Current Opinion in Structural Biology, Vol. 60 https://doi.org/10.1016/j.sbi.2019.12.005	journal	February 2020
End-to-End Differentiable Learning of Protein Structure AlQuraishi, Mohammed Cell Systems, Vol. 8, Issue 4 https://doi.org/10.1016/j.cels.2019.03.006	journal	April 2019
Improved protein structure prediction using potentials from deep learning Senior, Andrew W.; Evans, Richard; Jumper, John Nature, Vol. 577, Issue 7792 https://doi.org/10.1038/s41586-019-1923-7	journal	January 2020
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Machine learning-assisted directed protein evolution with combinatorial libraries Wu, Zachary; Kan, S. B. Jennifer; Lewis, Russell D. Proceedings of the National Academy of Sciences, Vol. 116, Issue 18 https://doi.org/10.1073/pnas.1901979116	journal	April 2019
Unified rational protein engineering with sequence-based deep representation learning Alley, Ethan C.; Khimulya, Grigory; Biswas, Surojit Nature Methods, Vol. 16, Issue 12 https://doi.org/10.1038/s41592-019-0598-1	journal	October 2019
MAESTRO - multi agent stability prediction upon point mutations Laimer, Josef; Hofer, Heidi; Fritz, Marko BMC Bioinformatics, Vol. 16, Issue 1 https://doi.org/10.1186/s12859-015-0548-6	journal	April 2015
Machine Learning Enables Selection of Epistatic Enzyme Mutants for Stability Against Unfolding and Detrimental Aggregation Li, Guangyue; Qin, Youcai; Fontaine, Nicolas T. ChemBioChem, Vol. 22, Issue 5 https://doi.org/10.1002/cbic.202000612	journal	November 2020
Recurrent Neural Network Model for Constructive Peptide Design Müller, Alex T.; Hiss, Jan A.; Schneider, Gisbert Journal of Chemical Information and Modeling, Vol. 58, Issue 2 https://doi.org/10.1021/acs.jcim.7b00414	journal	January 2018
An evolution-based model for designing chorismate mutase enzymes Russ, William P.; Figliuzzi, Matteo; Stocker, Christian Science, Vol. 369, Issue 6502 https://doi.org/10.1126/science.aba3304	journal	July 2020
ProThermDB: thermodynamic database for proteins and mutants revisited after 15 years Nikam, Rahul; Kulandaisamy, A.; Harini, K. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1035	journal	November 2020
Measuring and increasing protein stability Pace, C. Trends in Biotechnology, Vol. 8 https://doi.org/10.1016/0167-7799(90)90146-O	journal	January 1990
Protein stability engineering insights revealed by domain-wide comprehensive mutagenesis Nisthal, Alex; Wang, Connie Y.; Ary, Marie L. Proceedings of the National Academy of Sciences, Vol. 116, Issue 33 https://doi.org/10.1073/pnas.1903888116	journal	August 2019
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
UniProt: a worldwide hub of protein knowledge Consortium, The UniProt Nucleic Acids Research https://doi.org/10.1093/nar/gky1049		November 2018
Networks of bZIP Protein-Protein Interactions Diversified Over a Billion Years of Evolution Reinke, A. W.; Baek, J.; Ashenberg, O. Science, Vol. 340, Issue 6133 https://doi.org/10.1126/science.1233465	journal	May 2013
Global analysis of protein folding using massively parallel design, synthesis, and testing Rocklin, Gabriel J.; Chidyausiku, Tamuka M.; Goreshnik, Inna Science, Vol. 357, Issue 6347 https://doi.org/10.1126/science.aan0693	journal	July 2017
A Deep Neural Network for Predicting and Engineering Alternative Polyadenylation Bogard, Nicholas; Linder, Johannes; Rosenberg, Alexander B. Cell, Vol. 178, Issue 1 https://doi.org/10.1016/j.cell.2019.04.046	journal	June 2019
Learning the Sequence Determinants of Alternative Splicing from Millions of Random Sequences Rosenberg, Alexander B.; Patwardhan, Rupali P.; Shendure, Jay Cell, Vol. 163, Issue 3 https://doi.org/10.1016/j.cell.2015.09.054	journal	October 2015
Deep learning enables rapid identification of potent DDR1 kinase inhibitors Zhavoronkov, Alex; Ivanenkov, Yan A.; Aliper, Alex Nature Biotechnology, Vol. 37, Issue 9 https://doi.org/10.1038/s41587-019-0224-x	journal	September 2019
Deciphering interaction fingerprints from protein molecular surfaces using geometric deep learning Gainza, P.; Sverrisson, F.; Monti, F. Nature Methods, Vol. 17, Issue 2 https://doi.org/10.1038/s41592-019-0666-6	journal	December 2019
A general-purpose protein design framework based on mining sequence–structure relationships in known protein structures Zhou, Jianfu; Panaitiu, Alexandra E.; Grigoryan, Gevorg Proceedings of the National Academy of Sciences, Vol. 117, Issue 2 https://doi.org/10.1073/pnas.1908723117	journal	December 2019
De Novo Design of Helical Bundles as Models for Understanding Protein Folding and Function Hill, R. Blake; Raleigh, Daniel P.; Lombardi, Angela Accounts of Chemical Research, Vol. 33, Issue 11 https://doi.org/10.1021/ar970004h	journal	November 2000
Deep learning to predict the lab-of-origin of engineered DNA Nielsen, Alec A. K.; Voigt, Christopher A. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05378-z	journal	August 2018
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Stabilization of the Cold Shock Protein CspB from Bacillus subtilis by Evolutionary Optimization of Coulombic Interactions Wunderlich, Michael; Martin, Andreas; Schmid, Franz X. Journal of Molecular Biology, Vol. 347, Issue 5, p. 1063-1076 https://doi.org/10.1016/j.jmb.2005.02.014	journal	April 2005
Amino-acid substitutions in a surface turn modulate protein stability Predki, Paul F.; Agrawal, Vishal; Brünger, Axel T. Nature Structural Biology, Vol. 3, Issue 1 https://doi.org/10.1038/nsb0196-54	journal	January 1996
Contribution of individual side-chains to the stability of BPTI examined by alanine-scanning mutagenesis Yu, Myeong-Hee; Weissman, Jonathan S.; Kim, Peter S. Journal of Molecular Biology, Vol. 249, Issue 2 https://doi.org/10.1006/jmbi.1995.0304	journal	January 1995
Protein stability effects of a complete set of alanine substitutions in Arc repressor Milla, Marcos E.; Brown, Bronwen M.; Sauer, Robert T. Nature Structural Biology, Vol. 1, Issue 8 https://doi.org/10.1038/nsb0894-518	journal	August 1994
Molecular Determinants of Mutant Phenotypes, Inferred from Saturation Mutagenesis Data Tripathi, Arti; Gupta, Kritika; Khare, Shruti Molecular Biology and Evolution, Vol. 33, Issue 11 https://doi.org/10.1093/molbev/msw182	journal	August 2016
Stability, activity and flexibility in α-lactalbumin Greene, Lesley H.; Grobler, Jay A.; Malinovskii, Vladimir A. Protein Engineering, Design and Selection, Vol. 12, Issue 7 https://doi.org/10.1093/protein/12.7.581	journal	July 1999
Protein fragments as models for events in protein folding pathways: Protein engineering analysis of the association of two complementary fragments of the barley chymotrypsin inhibitor 2 (CI-2) Ruiz-Sanz, Javier; de Gay, Gonzalo; Otzen, Daniel E. Biochemistry, Vol. 34, Issue 5 https://doi.org/10.1021/bi00005a026	journal	February 1995
Effective Approaches to Attention-based Neural Machine Translation Luong, Thang; Pham, Hieu; Manning, Christopher D. Proceedings of the 2015 Conference on Empirical Methods in Natural Language Processing https://doi.org/10.18653/v1/D15-1166	conference	January 2015
Minimum error rate training in statistical machine translation Och, Franz Josef Proceedings of the 41st Annual Meeting on Association for Computational Linguistics - ACL '03 https://doi.org/10.3115/1075096.1075117	conference	January 2003
A Convolutional Encoder Model for Neural Machine Translation Gehring, Jonas; Auli, Michael; Grangier, David Proceedings of the 55th Annual Meeting of the Association for Computational Linguistics (Volume 1: Long Papers) https://doi.org/10.18653/v1/P17-1012	conference	January 2017
Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Kabsch, Wolfgang; Sander, Christian Biopolymers, Vol. 22, Issue 12 https://doi.org/10.1002/bip.360221211	journal	December 1983
Perplexity—a measure of the difficulty of speech recognition tasks Jelinek, F.; Mercer, R. L.; Bahl, L. R. The Journal of the Acoustical Society of America, Vol. 62, Issue S1 https://doi.org/10.1121/1.2016299	journal	December 1977
Frequencies of amino acid strings in globular protein sequences indicate suppression of blocks of consecutive hydrophobic residues Schwartz, Russell; Istrail, Sorin; King, Jonathan Protein Science, Vol. 10, Issue 5 https://doi.org/10.1110/ps.33201	journal	May 2001
Tryptophan zippers: Stable, monomeric -hairpins Cochran, A. G.; Skelton, N. J.; Starovasnik, M. A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 10 https://doi.org/10.1073/pnas.091100898	journal	May 2001
Improved protein structure prediction using predicted interresidue orientations Yang, Jianyi; Anishchenko, Ivan; Park, Hahnbeom Proceedings of the National Academy of Sciences, Vol. 117, Issue 3 https://doi.org/10.1073/pnas.1914677117	journal	January 2020
Automated selection of stabilizing mutations in designed and natural proteins Borgo, B.; Havranek, J. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1115172109	journal	January 2012
The Crucial Role of Methodology Development in Directed Evolution of Selective Enzymes Qu, Ge; Li, Aitao; Acevedo‐Rocha, Carlos G. Angewandte Chemie International Edition, Vol. 59, Issue 32 https://doi.org/10.1002/anie.201901491	journal	March 2020
De novo design of picomolar SARS-CoV-2 miniprotein inhibitors Cao, Longxing; Goreshnik, Inna; Coventry, Brian Science, Vol. 370, Issue 6515 https://doi.org/10.1126/science.abd9909	journal	September 2020
Accurate prediction of protein structures and interactions using a three-track neural network Baek, Minkyung; DiMaio, Frank; Anishchenko, Ivan Science, Vol. 373, Issue 6557 https://doi.org/10.1126/science.abj8754	journal	July 2021
An enumerative algorithm for de novo design of proteins with diverse pocket structures Basanta, Benjamin; Bick, Matthew J.; Bera, Asim K. Proceedings of the National Academy of Sciences, Vol. 117, Issue 36 https://doi.org/10.1073/pnas.2005412117	journal	August 2020
An mRNA Vaccine against SARS-CoV-2 — Preliminary Report Jackson, Lisa A.; Anderson, Evan J.; Rouphael, Nadine G. New England Journal of Medicine, Vol. 383, Issue 20 https://doi.org/10.1056/NEJMoa2022483	journal	November 2020
Phase I/II study of COVID-19 RNA vaccine BNT162b1 in adults Mulligan, Mark J.; Lyke, Kirsten E.; Kitchin, Nicholas Nature, Vol. 586, Issue 7830 https://doi.org/10.1038/s41586-020-2639-4	journal	August 2020
Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation Wrapp, Daniel; Wang, Nianshuang; Corbett, Kizzmekia S. Science, Vol. 367, Issue 6483 https://doi.org/10.1126/science.abb2507	journal	February 2020
Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen Pallesen, Jesper; Wang, Nianshuang; Corbett, Kizzmekia S. Proceedings of the National Academy of Sciences, Vol. 114, Issue 35 https://doi.org/10.1073/pnas.1707304114	journal	August 2017
Protein stability promotes evolvability Bloom, J. D.; Labthavikul, S. T.; Otey, C. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15, p. 5869-5874 https://doi.org/10.1073/pnas.0510098103	journal	March 2006
Multitask Learning Caruana, Rich Machine Learning, Vol. 28, Issue 1, p. 41-75 https://doi.org/10.1023/A:1007379606734	journal	January 1997
fairseq: A Fast, Extensible Toolkit for Sequence Modeling Ott, Myle; Edunov, Sergey; Baevski, Alexei Proceedings of the 2019 Conference of the North https://doi.org/10.18653/v1/N19-4009	conference	January 2019
Using circular dichroism spectra to estimate protein secondary structure Greenfield, Norma J Nature Protocols, Vol. 1, Issue 6, p. 2876-2890 https://doi.org/10.1038/nprot.2006.202	journal	January 2007
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017

Similar Records

Large-scale design and refinement of stable proteins using sequence-only models

Journal Article · 2022 · PLoS One · OSTI ID:1878389

Singer, Jedediah M.; Novotney, Scott; Strickland, Devin; +21 more

Monomer-scale design of functional protein polymers using consensus repeat sequences

Journal Article · 2021 · Journal of Polymer Science · OSTI ID:1878389

Chang, Marina P.; Huang, Winnie; Mai, Danielle J.

pGraph: Efficient Parallel Construction of Large-Scale Protein Sequence Homology Graphs

Journal Article · 2012 · IEEE Transactions on Parallel and Distributed Systems, 23(10):1923-1933 · OSTI ID:1878389

Wu, Changjun; Kalyanaraman, Anantharaman; Cannon, William R

Title: Large-scale design and refinement of stable proteins using sequence-only models

Citation Formats

References (64)

Similar Records

Related Subjects