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Imputation of label-free quantitative mass spectrometry-based proteomics data using self-supervised deep learning

Author

Listed:
  • Henry Webel

    (University of Copenhagen
    University of Copenhagen)

  • Lili Niu

    (University of Copenhagen)

  • Annelaura Bach Nielsen

    (University of Copenhagen)

  • Marie Locard-Paulet

    (University of Copenhagen
    Université de Toulouse, CNRS, Université Toulouse III - Paul Sabatier (UT3))

  • Matthias Mann

    (University of Copenhagen
    Max Planck Institute of Biochemistry)

  • Lars Juhl Jensen

    (University of Copenhagen)

  • Simon Rasmussen

    (University of Copenhagen
    University of Copenhagen
    Broad Institute of MIT and Harvard)

Abstract

Imputation techniques provide means to replace missing measurements with a value and are used in almost all downstream analysis of mass spectrometry (MS) based proteomics data using label-free quantification (LFQ). Here we demonstrate how collaborative filtering, denoising autoencoders, and variational autoencoders can impute missing values in the context of LFQ at different levels. We applied our method, proteomics imputation modeling mass spectrometry (PIMMS), to an alcohol-related liver disease (ALD) cohort with blood plasma proteomics data available for 358 individuals. Removing 20 percent of the intensities we were able to recover 15 out of 17 significant abundant protein groups using PIMMS-VAE imputations. When analyzing the full dataset we identified 30 additional proteins (+13.2%) that were significantly differentially abundant across disease stages compared to no imputation and found that some of these were predictive of ALD progression in machine learning models. We, therefore, suggest the use of deep learning approaches for imputing missing values in MS-based proteomics on larger datasets and provide workflows for these.

Suggested Citation

  • Henry Webel & Lili Niu & Annelaura Bach Nielsen & Marie Locard-Paulet & Matthias Mann & Lars Juhl Jensen & Simon Rasmussen, 2024. "Imputation of label-free quantitative mass spectrometry-based proteomics data using self-supervised deep learning," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48711-5
    DOI: 10.1038/s41467-024-48711-5
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    as
    1. van Buuren, Stef & Groothuis-Oudshoorn, Karin, 2011. "mice: Multivariate Imputation by Chained Equations in R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 45(i03).
    2. Mathias Wilhelm & Daniel P. Zolg & Michael Graber & Siegfried Gessulat & Tobias Schmidt & Karsten Schnatbaum & Celina Schwencke-Westphal & Philipp Seifert & Niklas Andrade Krätzig & Johannes Zerweck &, 2021. "Deep learning boosts sensitivity of mass spectrometry-based immunopeptidomics," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Mathias Wilhelm & Daniel P. Zolg & Michael Graber & Siegfried Gessulat & Tobias Schmidt & Karsten Schnatbaum & Celina Schwencke-Westphal & Philipp Seifert & Niklas Andrade Krätzig & Johannes Zerweck &, 2021. "Author Correction: Deep learning boosts sensitivity of mass spectrometry-based immunopeptidomics," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    4. Erwin M. Schoof & Benjamin Furtwängler & Nil Üresin & Nicolas Rapin & Simonas Savickas & Coline Gentil & Eric Lechman & Ulrich auf dem Keller & John E. Dick & Bo T. Porse, 2021. "Quantitative single-cell proteomics as a tool to characterize cellular hierarchies," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    5. Valentin Todorov & Matthias Templ & Peter Filzmoser, 2011. "Detection of multivariate outliers in business survey data with incomplete information," Advances in Data Analysis and Classification, Springer;German Classification Society - Gesellschaft für Klassifikation (GfKl);Japanese Classification Society (JCS);Classification and Data Analysis Group of the Italian Statistical Society (CLADAG);International Federation of Classification Societies (IFCS), vol. 5(1), pages 37-56, April.
    6. Runmin Wei & Jingye Wang & Erik Jia & Tianlu Chen & Yan Ni & Wei Jia, 2018. "GSimp: A Gibbs sampler based left-censored missing value imputation approach for metabolomics studies," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-14, January.
    7. Kowarik, Alexander & Templ, Matthias, 2016. "Imputation with the R Package VIM," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 74(i07).
    8. Ruedi Aebersold & Matthias Mann, 2016. "Mass-spectrometric exploration of proteome structure and function," Nature, Nature, vol. 537(7620), pages 347-355, September.
    9. Jonathan Frazer & Pascal Notin & Mafalda Dias & Aidan Gomez & Joseph K. Min & Kelly Brock & Yarin Gal & Debora S. Marks, 2021. "Disease variant prediction with deep generative models of evolutionary data," Nature, Nature, vol. 599(7883), pages 91-95, November.
    10. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    11. Rebecca C. Poulos & Peter G. Hains & Rohan Shah & Natasha Lucas & Dylan Xavier & Srikanth S. Manda & Asim Anees & Jennifer M. S. Koh & Sadia Mahboob & Max Wittman & Steven G. Williams & Erin K. Sykes , 2020. "Strategies to enable large-scale proteomics for reproducible research," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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