Improved protein structure prediction using potentials from deep learning

Nature - Tập 577 Số 7792 - Trang 706-710 - 2020
Andrew Senior1, Richard Evans1, John Jumper1, James Kirkpatrick1, Laurent Sifre1, Tim Green1, Chongli Qin1, Augustin Žídek1, Alexander Nelson1, Alex Bridgland1, Hugo Penedones1, Stig Petersen1, Karen Simonyan1, Steve Crossan1, Pushmeet Kohli1, David T. Jones2, David Silver1, Koray Kavukcuoglu1, Demis Hassabis1
1DeepMind, London, UK
2The Francis Crick Institute, London, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Dill, K. A., Ozkan, S. B., Shell, M. S. & Weikl, T. R. The protein folding problem. Annu. Rev. Biophys. 37, 289–316 (2008).

Dill, K. A. & MacCallum, J. L. The protein-folding problem, 50 years on. Science 338, 1042–1046 (2012).

Schaarschmidt, J., Monastyrskyy, B., Kryshtafovych, A. & Bonvin, A. M. J. J. Assessment of contact predictions in CASP12: co-evolution and deep learning coming of age. Proteins 86, 51–66 (2018).

Kirkwood, J. Statistical mechanics of fluid mixtures. J. Chem. Phys. 3, 300–313 (1935).

Kryshtafovych, A., Schwede, T., Topf, M., Fidelis, K. & Moult, J. Critical assessment of methods of protein structure prediction (CASP)—Round XIII. Proteins 87, 1011–1020 (2019).

Zhang, Y. & Skolnick, J. Scoring function for automated assessment of protein structure template quality. Proteins 57, 702–710 (2004).

Zhang, Y. Protein structure prediction: when is it useful? Curr. Opin. Struct. Biol. 19, 145–155 (2009).

Senior, A. W. et al. Protein structure prediction using multiple deep neural networks in the 13th Critical Assessment of Protein Structure Prediction (CASP13). Proteins 87, 1141–1148 (2019).

Das, R. & Baker, D. Macromolecular modeling with Rosetta. Annu. Rev. Biochem. 77, 363–382 (2008).

Jones, D. T. Predicting novel protein folds by using FRAGFOLD. Proteins 45, 127–132 (2001).

Zhang, C., Mortuza, S. M., He, B., Wang, Y. & Zhang, Y. Template-based and free modeling of I-TASSER and QUARK pipelines using predicted contact maps in CASP12. Proteins 86, 136–151 (2018).

Kirkpatrick, S., Gelatt, C. D. Jr & Vecchi, M. P. Optimization by simulated annealing. Science 220, 671–680 (1983).

Berman, H. M. et al. The Protein Data Bank. Nucleic Acids Res. 28, 235–242 (2000).

Altschuh, D., Lesk, A. M., Bloomer, A. C. & Klug, A. Correlation of co-ordinated amino acid substitutions with function in viruses related to tobacco mosaic virus. J. Mol. Biol. 193, 693–707 (1987).

Ovchinnikov, S., Kamisetty, H. & Baker, D. Robust and accurate prediction of residue–residue interactions across protein interfaces using evolutionary information. eLife 3, e02030 (2014).

Seemayer, S., Gruber, M. & Söding, J. CCMpred—fast and precise prediction of protein residue–residue contacts from correlated mutations. Bioinformatics 30, 3128–3130 (2014).

Morcos, F. et al. Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc. Natl Acad. Sci. USA 108, E1293–E1301 (2011).

Jones, D. T., Buchan, D. W., Cozzetto, D. & Pontil, M. PSICOV: precise structural contact prediction using sparse inverse covariance estimation on large multiple sequence alignments. Bioinformatics 28, 184–190 (2012).

Skwark, M. J., Raimondi, D., Michel, M. & Elofsson, A. Improved contact predictions using the recognition of protein like contact patterns. PLOS Comput. Biol. 10, e1003889 (2014).

Jones, D. T., Singh, T., Kosciolek, T. & Tetchner, S. MetaPSICOV: combining coevolution methods for accurate prediction of contacts and long range hydrogen bonding in proteins. Bioinformatics 31, 999–1006 (2015).

Wang, S., Sun, S., Li, Z., Zhang, R. & Xu, J. Accurate de novo prediction of protein contact map by ultra-deep learning model. PLOS Comput. Biol. 13, e1005324 (2017).

Jones, D. T. & Kandathil, S. M. High precision in protein contact prediction using fully convolutional neural networks and minimal sequence features. Bioinformatics 34, 3308–3315 (2018).

Ovchinnikov, S. et al. Improved de novo structure prediction in CASP11 by incorporating coevolution information into Rosetta. Proteins 84, 67–75 (2016).

Aszódi, A. & Taylor, W. R. Estimating polypeptide α-carbon distances from multiple sequence alignments. J. Math. Chem. 17, 167–184 (1995).

Zhao, F. & Xu, J. A position-specific distance-dependent statistical potential for protein structure and functional study. Structure 20, 1118–1126 (2012).

Xu, J. & Wang, S. Analysis of distance-based protein structure prediction by deep learning in CASP13. Proteins 87, 1069–1081 (2019).

Aszódi, A., Gradwell, M. J. & Taylor, W. R. Global fold determination from a small number of distance restraints. J. Mol. Biol. 251, 308–326 (1995).

Kandathil, S. M., Greener, J. G. & Jones, D. T. Prediction of interresidue contacts with DeepMetaPSICOV in CASP13. Proteins 87, 1092–1099 (2019).

He, K., Zhang, X., Ren, S. & Sun, J. Deep residual learning for image recognition. In Proc. IEEE Conference on Computer Vision and Pattern Recognition 770–778 (2016).

Simons, K. T., Kooperberg, C., Huang, E. & Baker, D. Assembly of protein tertiary structures from fragments with similar local sequences using simulated annealing and Bayesian scoring functions. J. Mol. Biol. 268, 209–225 (1997).

Liu, D. C. & Nocedal, J. On the limited memory BFGS method for large scale optimization. Math. Program. 45, 503–528 (1989).

Li, Y., Zhang, C., Bell, E. W., Yu, D.-J. & Zhang, Y. Ensembling multiple raw coevolutionary features with deep residual neural networks for contact-map prediction in CASP13. Proteins 87, 1082–1091 (2019).

Konagurthu, A. S., Lesk, A. M. & Allison, L. Minimum message length inference of secondary structure from protein coordinate data. Bioinformatics 28, i97–i105 (2012).

Dawson, N. L. et al. CATH: an expanded resource to predict protein function through structure and sequence. Nucleic Acids Res. 45, D289–D295 (2017).

Mirdita, M. et al. Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res. 45, D170–D176 (2017).

Remmert, M., Biegert, A., Hauser, A. & Söding, J. HHblits: lightning-fast iterative protein sequence searching by HMM–HMM alignment. Nat. Methods 9, 173–175 (2012).

Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).

Yu, F. & Koltun, V. Multi-scale context aggregation by dilated convolutions. Preprint at arXiv https://arxiv.org/abs/1511.07122 (2015).

Oord, A. d. et al. Wavenet: a generative model for raw audio. Preprint at arXiv https://arxiv.org/abs/1609.03499 (2016).

Clevert, D.-A., Unterthiner, T. & Hochreiter, S. Fast and accurate deep network learning by exponential linear units (ELUs). Preprint at arXiv https://arxiv.org/abs/1511.07289 (2015).

Srivastava, N., Hinton, G., Krizhevsky, A., Sutskever, I. & Salakhutdinov, R. Dropout: a simple way to prevent neural networks from overfitting. J. Mach. Learn. Res. 15, 1929–1958 (2014).

Kabsch, W. & Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577–2637 (1983).

Yang, Y. et al. Sixty-five years of the long march in protein secondary structure prediction: the final stretch? Briefings Bioinf. 19, 482–494 (2018).

Zemla, A., Venclovas, C., Moult, J. & Fidelis, K. Processing and analysis of CASP3 protein structure predictions. Proteins 37, 22–29 (1999).

Mariani, V., Biasini, M., Barbato, A. & Schwede, T. lDDT: a local superposition-free score for comparing protein structures and models using distance difference tests. Bioinformatics 29, 2722–2728 (2013).

Abriata, L. A., Tamo, G. E. & Dal Peraro, M. A further leap of improvement in tertiary structure prediction in CASP13 prompts new routes for future assessments. Proteins 87, 1100–1112 (2019).

Kayikci, M. et al. Visualization and analysis of non-covalent contacts using the Protein Contacts Atlas. Nat. Struct. Mol. Biol. 25, 185–194 (2018).

Croll, T. I. et al. Evaluation of template-based modeling in CASP13. Proteins 87, 1113–1127 (2019).

Sundararajan, M., Taly, A. & Yan, Q. Axiomatic attribution for deep networks. In Proc. 34th International Conference on Machine Learning Vol. 70, 3319–3328 (2017).

Abadi, M. et al. Tensorflow: a system for large-scale machine learning. In Proc. 12th USENIX Symposium on Operating Systems Design and Implementation (OSDI 16) 265–283 (2016).

Söding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244–W248 (2005).

Cong, Q. et al. An automatic method for CASP9 free modeling structure prediction assessment. Bioinformatics 27, 3371–3378 (2011).

Zhang, Y. & Skolnick, J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33, 2302–2309 (2005).

Tovchigrechko, A., Wells, C. A. & Vakser, I. A. Docking of protein models. Protein Sci. 11, 1888–1896 (2002).

Audet, M. et al. Crystal structure of misoprostol bound to the labor inducer prostaglandin E2 receptor. Nat. Chem. Biol. 15, 11–17 (2019).