Deep Learning-Based Prediction of Protein Structure from Sequence Data

Authors

  • Petr Dubois Department of Biotechnology and Molecular Biology, Delta University Center for Bioinformatics, Netherlands Author
  • Claire Havlicek Department of Biotechnology and Molecular Biology, Delta University Center for Bioinformatics, Netherlands Author
  • Astrid Fernandez Department of Biomedical and Health Sciences, Baltic Institute of Biomedical Research, Sweden Author

DOI:

https://doi.org/10.5281/zenodo.22688031

Keywords:

protein structure prediction, AlphaFold, deep learning, ESMFold, protein language models, CASP, structural bioinformatics

Abstract

Predicting a protein's three-dimensional structure from its amino acid sequence was, for five decades, the kind of
problem that structural biologists cited as a benchmark of how far computational methods still had to travel. That
situation changed abruptly between the thirteenth and fourteenth Critical Assessment of Structure Prediction
(CASP) experiments, when deep-learning systems built around attention-based neural architectures began
producing models whose backbone accuracy rivalled experimental structures for a large share of single-domain
targets. This systematic review synthesises 68 primary research articles and method papers published between
January 2018 and March 2024, identified through a structured search of five bibliographic databases, covering the
architectural lineage from early contact-map convolutional networks through AlphaFold2, RoseTTAFold and their
open derivatives, to protein-language-model-based single-sequence predictors such as ESMFold and
OmegaFold. We extracted and compared reported accuracy on CASP14, CASP15 and continuous CAMEO
benchmarks, computational cost, multiple-sequence-alignment dependence, and reported performance on three
categories of hard target: intrinsically disordered regions, novel folds with no close structural homologue, and
multi-chain protein complexes. Across the reviewed literature, mean backbone accuracy (GDT-TS) on
single-domain CASP14/15 targets rose from approximately 40 in pre-2020 deep learning methods to above 90 for
AlphaFold2-class predictors, while complex and disordered-region prediction remained substantially harder, with
median accuracy gains over pre-deep-learning baselines of roughly half the magnitude seen for single-domain
folding. We conclude that the field has largely solved single-chain, well-conserved-fold structure prediction, that
language-model-based single-sequence methods offer a meaningful speed-accuracy trade-off for large-scale
proteome annotation, and that complex assembly, disorder-to-order transitions and function prediction from
structure remain the primary open problems guiding the next generation of methods.

References

Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181(4096):223-230. https://doi.org/10.1126/science.181.4096.223

Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Research 28(1):235-242. https://doi.org/10.1093/nar/28.1.235

UniProt Consortium (2023) UniProt: the Universal Protein Knowledgebase in 2023. Nucleic Acids Research 51(D1):D523-D531. https://doi.org/10.1093/nar/gkac1052

Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology 234(3):779-815. https://doi.org/10.1006/jmbi.1993.1626

Das R, Baker D (2008) Macromolecular modeling with Rosetta. Annual Review of Biochemistry 77:363-382. https:/ /doi.org/10.1146/annurev.biochem.77.062906.171838

Kim DE, Chivian D, Baker D (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Research 32(suppl_2):W526-W531. https://doi.org/10.1093/nar/gkh468

Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, Zecchina R, Sander C (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS ONE 6(12):e28766. https://doi.org/10.1371/journal.pone.0028766

Wang S, Sun S, Li Z, Zhang R, Xu J (2017) Accurate de novo prediction of protein contact map by ultra-deep learning model. PLoS Computational Biology 13(1):e1005324. https://doi.org/10.1371/journal.pcbi.1005324

Senior AW, Evans R, Jumper J, Kirkpatrick J, Sifre L, Green T, Qin C, Zidek A, Nelson AWR, Bridgland A, Penedones H (2020) Improved protein structure prediction using potentials from deep learning. Nature 577(7792):706-710. https://doi.org/10.1038/s41586-019-1923-7

Kryshtafovych A, Schwede T, Topf M, Fidelis K, Moult J (2021) Critical assessment of methods of protein structure prediction (CASP)-Round XIV. Proteins 89(12):1607-1617. https://doi.org/10.1002/prot.26237

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Zidek A, Potapenko A, Bridgland A (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596(7873):583-589. https://doi.org/10.1038/s41586-021-03819-2

Callaway E (2020) 'It will change everything': DeepMind's AI makes gigantic leap in solving protein structures. Nature 588(7837):203-204. https://doi.org/10.1038/d41586-020-03348-4

Mirdita M, Schutze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M (2022) ColabFold: making protein folding accessible to all. Nature Methods 19(6):679-682. https://doi.org/10.1038/s41592-022-01488-1

Ahdritz G, Bouatta N, Floristean C, Kadyan S, Xia Q, Gerecke W, O'Donnell TJ, Berenberg D, Fisk I, Zanichelli N, Zhang B (2024) OpenFold: retraining AlphaFold2 yields new insights into its learning mechanisms and capacity for generalization. Nature Methods 21(8):1514-1524. https://doi.org/10.1038/s41592-024-02272-z

Lin Z, Akin H, Rao R, Hie B, Zhu Z, Lu W, Smetanin N, Verkuil R, Kabeli O, Shmueli Y, dos Santos Costa A (2023) Evolutionary-scale prediction of atomic-level protein structure with a language model. Science 379(6637):1123-1130. https://doi.org/10.1126/science.ade2574

Wu R, Ding F, Wang R, Shen R, Zhang X, Luo S, Su C, Wu Z, Xie Q, Berger B, Ma J (2022) High-resolution de novo structure prediction from primary sequence. bioRxiv preprint. https://doi.org/10.1101/2022.07.21.500999

Kryshtafovych A, Moult J, Billings WM, Williams CJ, Schaeffer RD, Fidelis K, Topf M (2023) Assessment of predictions submitted for the CASP15 protein and RNA structure prediction challenge. Proteins 91(12):1539-1549. https://doi.org/10.1002/prot.26602

Haas J, Barbato A, Behringer D, Studer G, Roth S, Bertoni M, Mostaguir K, Gumienny R, Schwede T (2018) Continuous automated model evaluation (CAMEO) complementing the critical assessment of structure prediction in CASP12. Proteins 86(Suppl 1):387-398. https://doi.org/10.1002/prot.25431

Necci M, Piovesan D, Predictors of Intrinsic Disorder CAID, Tosatto SCE (2021) Critical assessment of protein intrinsic disorder prediction. Nature Methods 18(5):472-481. https://doi.org/10.1038/s41592-021-01117-3

Ruff KM, Pappu RV (2021) AlphaFold and implications for intrinsically disordered proteins. Journal of Molecular Biology 433(20):167208. https://doi.org/10.1016/j.jmb.2021.167208

Evans R, O'Neill M, Pritzel A, Antropova N, Senior A, Green T, Zidek A, Bates R, Blackwell S, Yim J, Ronneberger O (2022) Protein complex prediction with AlphaFold-Multimer. bioRxiv preprint. https://doi.org/10.1101/2021.10.04.463034

Baek M, DiMaio F, Anishchenko I, Dauparas J, Ovchinnikov S, Lee GR, Wang J, Cong Q, Kinch LN, Schaeffer RD, Millan C (2021) Accurate prediction of protein structures and interactions using a three-track neural network. Science 373(6557):871-876. https://doi.org/10.1126/science.abj8754

Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, Zidek A (2022) AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Research 50(D1):D439-D444. https://doi.org/10.1093/nar/gkab1061

Bryant P, Pozzati G, Elofsson A (2022) Improved prediction of protein-protein interactions using AlphaFold2. Nature Communications 13:1265. https://doi.org/10.1038/s41467-022-28865-w

Tunyasuvunakool K, Adler J, Wu Z, Green T, Zielinski M, Zidek A, Bridgland A, Cowie A, Meyer C, Laydon A, Velankar S (2021) Highly accurate protein structure prediction for the human proteome. Nature 596(7873):590-596. https://doi.org/10.1038/s41586-021-03828-1

Skolnick J, Gao M, Zhou H, Singh S (2021) AlphaFold 2: why it works and its implications for understanding the relationships of protein sequence, structure, and function. Journal of Chemical Information and Modeling 61(10):4827-4831. https://doi.org/10.1021/acs.jcim.1c01114

Akdel M, Pires DEV, Pardo EP, Janes J, Zalevsky AO, Meszaros B, Bryant P, Good LL, Laskowski RA, Pozzati G, Shenoy A (2022) A structural biology community assessment of AlphaFold2 applications. Nature Structural & Molecular Biology 29(11):1056-1067. https://doi.org/10.1038/s41594-022-00849-w

Rives A, Meier J, Sercu T, Goyal S, Lin Z, Liu J, Guo D, Ott M, Zitnick CL, Ma J, Fergus R (2021) Biological structure and function emerge from scaling unsupervised learning to 250 million protein sequences. PNAS 118(15):e2016239118. https://doi.org/10.1073/pnas.2016239118

Elnaggar A, Heinzinger M, Dallago C, Rehawi G, Wang Y, Jones L, Gibbs T, Feher T, Angerer C, Steinegger M, Bhowmik D (2022) ProtTrans: toward understanding the language of life through self-supervised learning. IEEE Transactions on Pattern Analysis and Machine Intelligence 44(10):7112-7127. https://doi.org/10.1109/TPAMI.2021.3095381

Yang J, Anishchenko I, Park H, Peng Z, Ovchinnikov S, Baker D (2020) Improved protein structure prediction using predicted interresidue orientations. PNAS 117(3):1496-1503. https://doi.org/10.1073/pnas.1914677117

Xu J (2019) Distance-based protein folding powered by deep learning. PNAS 116(34):16856-16865. https://doi.org/10.1073/pnas.1821309116

AlQuraishi M (2019) AlphaFold at CASP13. Bioinformatics 35(22):4862-4865. https://doi.org/10.1093/bioinformatics/btz422

Pearce R, Zhang Y (2021) Deep learning techniques have significantly impacted protein structure prediction and protein design. Current Opinion in Structural Biology 68:194-207. https://doi.org/10.1016/j.sbi.2021.01.007

Baker D (2019) What has de novo protein design taught us about protein folding and biophysics? Protein Science 28(4):678-683. https://doi.org/10.1002/pro.3588

Watson JL, Juergens D, Bennett NR, Trippe BL, Yim J, Eisenach HE, Ahern W, Borst AJ, Ragotte RJ, Milles LF, Wicky BIM (2023) De novo design of protein structure and function with RFdiffusion. Nature 620(7976):1089-1100. https://doi.org/10.1038/s41586-023-06415-8

Wu KE, Yang KK, van den Berg R, Zou JY, Lu AX, Amini AP (2022) Protein structure generation via folding diffusion. arXiv preprint. https://doi.org/10.48550/arXiv.2209.15611

Abramson J, Adler J, Dunger J, Evans R, Green T, Pritzel A, Ronneberger O, Willmore L, Ballard AJ, Bambrick J, Bodenstein SW (2024) Accurate structure prediction of biomolecular interactions with AlphaFold3. Nature 630(8016):493-500. https://doi.org/10.1038/s41586-024-07487-w

Ozden B, Kryshtafovych A, Karaca E (2023) The impact of AI-based modeling on the future of cryo-EM structure determination. Structure 31(11):1414-1423. https://doi.org/10.1016/j.str.2023.09.010

Zhang Y, Skolnick J (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Research 33(7):2302-2309. https://doi.org/10.1093/nar/gki524

Basu S, Wallner B (2016) DockQ: a quality measure for protein-protein docking models. PLoS ONE 11(8):e0161879. https://doi.org/10.1371/journal.pone.0161879

Ruffolo JA, Chu LS, Mahajan SP, Gray JJ (2023) Fast, accurate antibody structure prediction from deep learning on massive set of natural antibodies. Nature Communications 14:2389. https://doi.org/10.1038/s41467-023-38063-x

Terwilliger TC, Liebschner D, Croll TI, Williams CJ, McCoy AJ, Poon BK, Afonine PV, Oeffner RD, Richardson JS, Read RJ, Adams PD (2024) AlphaFold predictions are valuable hypotheses and accelerate but do not replace experimental structure determination. Nature Methods 21(1):110-116. https://doi.org/10.1038/s41592-023-02087-4

David A, Islam S, Tankhilevich E, Sternberg MJE (2022) The AlphaFold database of protein structures: a biologist's guide. Journal of Molecular Biology 434(15):167336. https://doi.org/10.1016/j.jmb.2021.167336

Kuhlman B, Bradley P (2019) Advances in protein structure prediction and design. Nature Reviews Molecular Cell Biology 20(11):681-697. https://doi.org/10.1038/s41580-019-0163-x

Stahl K, Graziadei A, Dau T, Brock O, Rappsilber J (2023) Protein structure prediction with in-cell photo-crosslinking mass spectrometry and deep learning. Nature Biotechnology 41(12):1810-1819. https://doi.org/10.1038/s41587-023-01704-z

Perrakis A, Sixma TK (2021) AI revolutions in biology: the joys and perils of AlphaFold. EMBO Reports 22(11):e54046. https://doi.org/10.15252/embr.202154046

Thornton JM, Laskowski RA, Borkakoti N (2021) AlphaFold heralds a data-driven revolution in biology and medicine. Nature Medicine 27(10):1666-1669. https://doi.org/10.1038/s41591-021-01533-0

Guo Z, Liu J, Wang J, Chen S, Gong Y, Wu J (2023) Diffusion models in bioinformatics and computational biology. Nature Reviews Bioengineering 2:136-154. https://doi.org/10.1038/s44222-023-00114-9

Yang J, Zhang Y (2015) I-TASSER server: new development for protein structure and function predictions. Nucleic Acids Research 43(W1):W174-W181. https://doi.org/10.1093/nar/gkv342

Vaswani A, Shazeer N, Parmar N, Uszkoreit J, Jones L, Gomez AN, Kaiser L, Polosukhin I (2017) Attention is all you need. Advances in Neural Information Processing Systems 30:5998-6008. https://doi.org/10.5555/3295222.3295349

Ovchinnikov S, Kamisetty H, Baker D (2014) Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. eLife 3:e02030. https://doi.org/10.7554/eLife.02030

Pakhrin SC, Shrestha B, Adhikari B, KC DB (2021) Deep learning-based advances in protein structure prediction. International Journal of Molecular Sciences 22(11):5553. https://doi.org/10.3390/ijms22115553

Steinegger M, Meier M, Mirdita M, Vohringer H, Haunsberger SJ, Soding J (2019) HH-suite3 for fast remote homology detection and deep protein annotation. BMC Bioinformatics 20:473. https://doi.org/10.1186/s12859-019-3019-7

Bertoline LMF, Lima AN, Krieger JE, Teixeira SK (2023) Before and after AlphaFold2: an overview of protein structure prediction. Frontiers in Bioinformatics 3:1120370. https://doi.org/10.3389/fbinf.2023.1120370

Torrisi M, Pollastri G, Le Q (2020) Deep learning methods in protein structure prediction. Computational and Structural Biotechnology Journal 18:1301-1310. https://doi.org/10.1016/j.csbj.2019.12.011

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Published

2024-12-21