IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48868-z.html
   My bibliography  Save this article

DOT: a flexible multi-objective optimization framework for transferring features across single-cell and spatial omics

Author

Listed:
  • Arezou Rahimi

    (Heidelberg University & Heidelberg University Hospital
    GlaxoSmithKline)

  • Luis A. Vale-Silva

    (GlaxoSmithKline)

  • Maria Fälth Savitski

    (GlaxoSmithKline)

  • Jovan Tanevski

    (Heidelberg University & Heidelberg University Hospital
    Jožef Stefan Institute)

  • Julio Saez-Rodriguez

    (Heidelberg University & Heidelberg University Hospital)

Abstract

Single-cell transcriptomics and spatially-resolved imaging/sequencing technologies have revolutionized biomedical research. However, they suffer from lack of spatial information and a trade-off of resolution and gene coverage, respectively. We propose DOT, a multi-objective optimization framework for transferring cellular features across these data modalities, thus integrating their complementary information. DOT uses genes beyond those common to the data modalities, exploits the local spatial context, transfers spatial features beyond cell-type information, and infers absolute/relative abundance of cell populations at tissue locations. Thus, DOT bridges single-cell transcriptomics data with both high- and low-resolution spatially-resolved data. Moreover, DOT combines practical aspects related to cell composition, heterogeneity, technical effects, and integration of prior knowledge. Our fast implementation based on the Frank-Wolfe algorithm achieves state-of-the-art or improved performance in localizing cell features in high- and low-resolution spatial data and estimating the expression of unmeasured genes in low-coverage spatial data.

Suggested Citation

  • Arezou Rahimi & Luis A. Vale-Silva & Maria Fälth Savitski & Jovan Tanevski & Julio Saez-Rodriguez, 2024. "DOT: a flexible multi-objective optimization framework for transferring features across single-cell and spatial omics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48868-z
    DOI: 10.1038/s41467-024-48868-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48868-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48868-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Wright, Marvin N. & Ziegler, Andreas, 2017. "ranger: A Fast Implementation of Random Forests for High Dimensional Data in C++ and R," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 77(i01).
    2. Alma Andersson & Ludvig Larsson & Linnea Stenbeck & Fredrik Salmén & Anna Ehinger & Sunny Z. Wu & Ghamdan Al-Eryani & Daniel Roden & Alex Swarbrick & Åke Borg & Jonas Frisén & Camilla Engblom & Joakim, 2021. "Spatial deconvolution of HER2-positive breast cancer delineates tumor-associated cell type interactions," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Nikolaus Rajewsky & Geneviève Almouzni & Stanislaw A. Gorski & Stein Aerts & Ido Amit & Michela G. Bertero & Christoph Bock & Annelien L. Bredenoord & Giacomo Cavalli & Susanna Chiocca & Hans Clevers , 2020. "LifeTime and improving European healthcare through cell-based interceptive medicine," Nature, Nature, vol. 587(7834), pages 377-386, November.
    4. Gneiting, Tilmann & Raftery, Adrian E., 2007. "Strictly Proper Scoring Rules, Prediction, and Estimation," Journal of the American Statistical Association, American Statistical Association, vol. 102, pages 359-378, March.
    5. Anjali Rao & Dalia Barkley & Gustavo S. França & Itai Yanai, 2021. "Exploring tissue architecture using spatial transcriptomics," Nature, Nature, vol. 596(7871), pages 211-220, August.
    6. Meng Zhang & Stephen W. Eichhorn & Brian Zingg & Zizhen Yao & Kaelan Cotter & Hongkui Zeng & Hongwei Dong & Xiaowei Zhuang, 2021. "Spatially resolved cell atlas of the mouse primary motor cortex by MERFISH," Nature, Nature, vol. 598(7879), pages 137-143, October.
    7. Marguerite Frank & Philip Wolfe, 1956. "An algorithm for quadratic programming," Naval Research Logistics Quarterly, John Wiley & Sons, vol. 3(1‐2), pages 95-110, March.
    8. Amanda Janesick & Robert Shelansky & Andrew D. Gottscho & Florian Wagner & Stephen R. Williams & Morgane Rouault & Ghezal Beliakoff & Carolyn A. Morrison & Michelli F. Oliveira & Jordan T. Sicherman &, 2023. "High resolution mapping of the tumor microenvironment using integrated single-cell, spatial and in situ analysis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
    10. Zizhen Yao & Hanqing Liu & Fangming Xie & Stephan Fischer & Ricky S. Adkins & Andrew I. Aldridge & Seth A. Ament & Anna Bartlett & M. Margarita Behrens & Koen Berge & Darren Bertagnolli & Hector Roux , 2021. "A transcriptomic and epigenomic cell atlas of the mouse primary motor cortex," Nature, Nature, vol. 598(7879), pages 103-110, October.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Rongbo Shen & Lin Liu & Zihan Wu & Ying Zhang & Zhiyuan Yuan & Junfu Guo & Fan Yang & Chao Zhang & Bichao Chen & Wanwan Feng & Chao Liu & Jing Guo & Guozhen Fan & Yong Zhang & Yuxiang Li & Xun Xu & Ji, 2022. "Spatial-ID: a cell typing method for spatially resolved transcriptomics via transfer learning and spatial embedding," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Kian Kalhor & Chien-Ju Chen & Ho Suk Lee & Matthew Cai & Mahsa Nafisi & Richard Que & Carter R. Palmer & Yixu Yuan & Yida Zhang & Xuwen Li & Jinghui Song & Amanda Knoten & Blue B. Lake & Joseph P. Gau, 2024. "Mapping human tissues with highly multiplexed RNA in situ hybridization," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Xinrui Zhou & Wan Yi Seow & Norbert Ha & Teh How Cheng & Lingfan Jiang & Jeeranan Boonruangkan & Jolene Jie Lin Goh & Shyam Prabhakar & Nigel Chou & Kok Hao Chen, 2024. "Highly sensitive spatial transcriptomics using FISHnCHIPs of multiple co-expressed genes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Reza Mirzazadeh & Zaneta Andrusivova & Ludvig Larsson & Phillip T. Newton & Leire Alonso Galicia & Xesús M. Abalo & Mahtab Avijgan & Linda Kvastad & Alexandre Denadai-Souza & Nathalie Stakenborg & Ale, 2023. "Spatially resolved transcriptomic profiling of degraded and challenging fresh frozen samples," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Ian Covert & Rohan Gala & Tim Wang & Karel Svoboda & Uygar Sümbül & Su-In Lee, 2023. "Predictive and robust gene selection for spatial transcriptomics," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Gennady Gorin & John J. Vastola & Meichen Fang & Lior Pachter, 2022. "Interpretable and tractable models of transcriptional noise for the rational design of single-molecule quantification experiments," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Wenyi Yang & Pingping Wang & Shouping Xu & Tao Wang & Meng Luo & Yideng Cai & Chang Xu & Guangfu Xue & Jinhao Que & Qian Ding & Xiyun Jin & Yuexin Yang & Fenglan Pang & Boran Pang & Yi Lin & Huan Nie , 2024. "Deciphering cell–cell communication at single-cell resolution for spatial transcriptomics with subgraph-based graph attention network," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Wei Feng & Abha Bais & Haoting He & Cassandra Rios & Shan Jiang & Juan Xu & Cindy Chang & Dennis Kostka & Guang Li, 2022. "Single-cell transcriptomic analysis identifies murine heart molecular features at embryonic and neonatal stages," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Lulu Shang & Xiang Zhou, 2022. "Spatially aware dimension reduction for spatial transcriptomics," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    10. Honglei Ren & Benjamin L. Walker & Zixuan Cang & Qing Nie, 2022. "Identifying multicellular spatiotemporal organization of cells with SpaceFlow," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Andree,Bo Pieter Johannes & Chamorro Elizondo,Andres Fernando & Kraay,Aart C. & Spencer,Phoebe Girouard & Wang,Dieter, 2020. "Predicting Food Crises," Policy Research Working Paper Series 9412, The World Bank.
    12. Jongsu Choi & Jin Li & Salma Ferdous & Qingnan Liang & Jeffrey R. Moffitt & Rui Chen, 2023. "Spatial organization of the mouse retina at single cell resolution by MERFISH," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Zhiyuan Yuan, 2024. "MENDER: fast and scalable tissue structure identification in spatial omics data," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    14. Maia, Mateus & Murphy, Keefe & Parnell, Andrew C., 2024. "GP-BART: A novel Bayesian additive regression trees approach using Gaussian processes," Computational Statistics & Data Analysis, Elsevier, vol. 190(C).
    15. Hao Xu & Shuyan Wang & Minghao Fang & Songwen Luo & Chunpeng Chen & Siyuan Wan & Rirui Wang & Meifang Tang & Tian Xue & Bin Li & Jun Lin & Kun Qu, 2023. "SPACEL: deep learning-based characterization of spatial transcriptome architectures," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Schratz, Patrick & Muenchow, Jannes & Iturritxa, Eugenia & Richter, Jakob & Brenning, Alexander, 2019. "Hyperparameter tuning and performance assessment of statistical and machine-learning algorithms using spatial data," Ecological Modelling, Elsevier, vol. 406(C), pages 109-120.
    17. Haoyang Li & Yingxin Lin & Wenjia He & Wenkai Han & Xiaopeng Xu & Chencheng Xu & Elva Gao & Hongyu Zhao & Xin Gao, 2024. "SANTO: a coarse-to-fine alignment and stitching method for spatial omics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    18. Xiaohang Fu & Yingxin Lin & David M. Lin & Daniel Mechtersheimer & Chuhan Wang & Farhan Ameen & Shila Ghazanfar & Ellis Patrick & Jinman Kim & Jean Y. H. Yang, 2024. "BIDCell: Biologically-informed self-supervised learning for segmentation of subcellular spatial transcriptomics data," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    19. Zhiyuan Liu & Dafei Wu & Weiwei Zhai & Liang Ma, 2023. "SONAR enables cell type deconvolution with spatially weighted Poisson-Gamma model for spatial transcriptomics," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    20. Wendy Xueyi Wang & Julie L. Lefebvre, 2022. "Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons," Nature Communications, Nature, vol. 13(1), pages 1-21, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48868-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.