PreprintCited by 68Genomics and Rare DiseasesGenetic Associations and EpidemiologyCancer Genomics and Diagnostics

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

Cross-protein transfer learning substantially improves disease variant prediction

Open access

Preprint — published as 10.1186/s13059-023-03024-6

Abstract

Genetic variation in the human genome is a major determinant of individual disease risk, but the vast majority of missense variants have unknown etiological effects. Here, we present a robust learning framework for leveraging saturation mutagenesis experiments to construct accurate computational predictors of proteome-wide missense variant pathogenicity. We train cross-protein transfer (CPT) models using deep mutational scanning data from only five proteins and achieve state-of-the-art performance on clinical variant interpretation for unseen proteins across the human proteome. High sensitivity is crucial for clinical applications and our model CPT-1 particularly excels in this regime. For instance, at 95% sensitivity of detecting human disease variants annotated in ClinVar, CPT-1 improves specificity to 68%, from 27% for ESM-1v and 55% for EVE. Furthermore, for genes not used to train REVEL, a supervised method widely used by clinicians, we show that CPT-1 compares favorably with REVEL. Our framework combines predictive features derived from general protein sequence models, vertebrate sequence alignments, and AlphaFold2 structures, and it is adaptable to the future inclusion of other sources of information. We find that vertebrate alignments, albeit rather shallow with only 100 genomes, provide a strong signal for variant pathogenicity prediction that is complementary to recent deep learning-based models trained on massive amounts of protein sequence data. We release predictions for all possible missense variants in 90% of human genes. Our results demonstrate the utility of mutational scanning data for learning properties of variants that transfer to unseen proteins.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1101/2022.11.15.516532

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 52

  1. 10.1093/nar/gkv1222 · DOI · Paper page
  2. 10.1038/s41586-020-2308-7 · DOI · Paper page
  3. 10.1002/humu.10212 · DOI
  4. 10.1038/s41586-020-2853-0 · DOI · Paper page
  5. 2014, Deep mutational scanning: a new style of protein science, Nature Methods, 11, 801, 10.1038/nmeth.3027 · DOI · Paper page
  6. 2020, Using deep mutational scanning to benchmark variant effect predictors and identify disease mutations, Molecular Systems Biology, 16, e9380, 10.15252/msb.20199380 · DOI
  7. 10.15252/msb.20177908 · DOI · Paper page
  8. 10.1038/s41586-021-04043-8 · DOI · Paper page
  9. 2021, Language models enable zero-shot prediction of the effects of mutations on protein function, Advances in Neural Information Processing Systems, 34, 29287
  10. 10.1016/j.ajhg.2016.08.016 · DOI · Paper page
  11. 10.1093/nar/gky1016 · DOI · Paper page
  12. 2017, DEOGEN2: prediction and interactive visualization of single amino acid variant deleteriousness in human proteins, Nucleic Acids Research, 45, W201, 10.1093/nar/gkx390 · DOI
  13. 2010, A method and server for predicting damaging missense mutations, Nature Methods, 7, 248, 10.1038/nmeth0410-248 · DOI · Paper page
  14. 2018, Deep generative models of genetic variation capture the effects of mutations, Nature Methods, 15, 816, 10.1038/s41592-018-0138-4 · DOI · Paper page
  15. 10.1038/ng.3703 · DOI
  16. 10.1038/nbt.2419 · DOI · Paper page
  17. 10.1073/pnas.1314045110 · DOI
  18. 10.1073/pnas.1111471108 · DOI · Paper page
  19. Roshan Rao , Joshua Meier , Tom Sercu , Sergey Ovchinnikov , and Alexander Rives . Transformer protein language models are unsupervised structure learners. Biorxiv, 2020.
  20. 10.1126/science.ade2574 · DOI · Paper page
  21. 2021, Informed training set design enables efficient machine learning-assisted directed protein evolution, Cell Systems, 12, 1026, 10.1016/j.cels.2021.07.008 · DOI
  22. Chloe Hsu , Hunter Nisonoff , Clara Fannjiang , and Jennifer Listgarten . Learning protein fitness models from evolutionary and assay-labeled data. Nature Biotechnology, pages 1–9, 2022. · DOI
  23. 10.1016/j.sbi.2021.01.008 · DOI
  24. 10.1002/humu.22768 · DOI · Paper page
  25. Benjamin J Livesey and Joseph A Marsh . Updated benchmarking of variant effect predictors using deep mutational scanning. bioRxiv, pages 2022–11, 2022. · DOI
  26. 2018, Quantitative missense variant effect prediction using large-scale mutagenesis data, Cell systems, 6, 116, 10.1016/j.cels.2017.11.003 · DOI
  27. 2022, Embeddings from protein language models predict conservation and variant effects, Human genetics, 141, 1629, 10.1007/s00439-021-02411-y · DOI
  28. 10.1038/nature10530 · DOI · Paper page
  29. 10.1101/gr.229102. Article published online before print in May 2002 · DOI · Paper page
  30. 2021, Highly accurate protein structure prediction for the human proteome, Nature, 596, 590, 10.1038/s41586-021-03828-1 · DOI · Paper page
  31. 2021, Shifting landscapes of human MTHFR missense-variant effects, The American Journal of Human Genetics, 108, 1283, 10.1016/j.ajhg.2021.05.009 · DOI
  32. Pascal Notin , Mafalda Dias , Jonathan Frazer , Javier Marchena Hurtado , Aidan N Gomez , Debora Marks , and Yarin Gal . Tranception: protein fitness prediction with autoregressive transformers and inference-time retrieval. In International Conference on Machine Learning, pages 16990–17017. PMLR, 2022.
  33. 10.1101/gr.1933104 · DOI · Paper page
  34. 10.1101/gr.097857.109 · DOI · Paper page
  35. Adam Siepel , Katherine S Pollard , and David Haussler . New methods for detecting lineagespecific selection. In Annual International Conference on Research in Computational Molecular Biology, pages 190–205. Springer, 2006. · DOI
  36. 10.1093/bioinformatics/bty966 · DOI
  37. 2022, The impact of AlphaFold2 one year on, Nature Methods, 19, 15, 10.1038/s41592-021-01365-3 · DOI
  38. Axel Schmidt , Sebastian Röner , Karola Mai , Hannah Klinkhammer , Martin Kircher , and Kerstin U Ludwig . Predicting the pathogenicity of missense variants using features derived from AlphaFold2. bioRxiv, 2022. · DOI · Paper page
  39. 2022, The 3D mutational constraint on amino acid sites in the human proteome, Nature Communications, 13, 1
  40. Justas Dauparas , Ivan Anishchenko , Nathaniel Bennett , Hua Bai , Robert J Ragotte , Lukas F Milles , Basile IM Wicky , Alexis Courbet , Rob J de Haas , Neville Bethel , et al. Robust deep learning–based protein sequence design using ProteinMPNN. Science, page eadd2187, 2022. · DOI · Paper page
  41. 10.1038/s41586-021-03451-0 · DOI · Paper page
  42. James P Roney and Sergey Ovchinnikov . State-of-the-art estimation of protein model accuracy using AlphaFold. BioRxiv, 2022. · DOI · Paper page
  43. 10.1038/s41586-020-2188-x · DOI · Paper page
  44. 10.1006/jmbi.1998.2400 · DOI
  45. 10.1093/nar/gky1049 · DOI · Paper page
  46. 2015, Peptides: a package for data mining of antimicrobial peptides, Small, 12, 44
  47. 2004, Peptide studies by means of principal properties of amino acids derived from MIF descriptors, Journal of Chemometrics, 18, 146, 10.1002/cem.856 · DOI
  48. 2005, A new set of amino acid descriptors and its application in peptide QSARs, Peptide Science: Original Research on Biomolecules, 80, 775, 10.1002/bip.20296 · DOI
  49. 10.1021/jm9700575 · DOI
  50. 10.1007/s00726-009-0287-y · DOI
  51. 2013, Benchmarking of protein descriptor sets in proteochemometric modeling (part 1): comparative study of 13 amino acid descriptor sets, Journal of Cheminformatics, 5, 1
  52. 10.1089/cmb.2008.0173 · DOI

Metadata

Authors
Jagota, M., Ye, C., Albors, C., Rastogi, R., Koehl, A., Ioannidis, N., & Song, Y. S.
Affiliations
  • University of California, Berkeley (US)
  • Chan Zuckerberg Biohub San Francisco (US)
Corresponding author
Song, Yun S.
Venue
Genome biology
Publisher
openRxiv
Published
2022-11-17
Volume
24
Issue
1
Pages
182-182
ISSN
1465-6906 (ISSN-L)
OpenAlex
W4385637034
Cited by
68
References
2
Citations by year
2026: 15 · 2025: 29 · 2024: 18 · 2023: 5 · 2022: 1
FWCI
11.12
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Genome biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Tel Aviv University
  • National Institutes of Health
  • National Human Genome Research Institute (R00HG009677)
  • National Institute of General Medical Sciences (R35GM134922)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomics and Rare Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Keywords
deep mutational scanning, saturation mutagenesis, clinical variant interpretation, ClinVar, AlphaFold protein structure, carnitine palmitoyltransferase 1
MeSH terms
Machine Learning, Amino Acid Sequence, Humans, Mutation, Computational Biology, Mutation, Missense, Proteome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review