IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40068-5.html
   My bibliography  Save this article

Robust phenotyping of highly multiplexed tissue imaging data using pixel-level clustering

Author

Listed:
  • Candace C. Liu

    (Stanford University)

  • Noah F. Greenwald

    (Stanford University)

  • Alex Kong

    (Stanford University)

  • Erin F. McCaffrey

    (Stanford University)

  • Ke Xuan Leow

    (Stanford University)

  • Dunja Mrdjen

    (Stanford University)

  • Bryan J. Cannon

    (Stanford University)

  • Josef Lorenz Rumberger

    (Max-Delbrueck-Center for Molecular Medicine
    Charité University Medicine)

  • Sricharan Reddy Varra

    (Stanford University)

  • Michael Angelo

    (Stanford University)

Abstract

While technologies for multiplexed imaging have provided an unprecedented understanding of tissue composition in health and disease, interpreting this data remains a significant computational challenge. To understand the spatial organization of tissue and how it relates to disease processes, imaging studies typically focus on cell-level phenotypes. However, images can capture biologically important objects that are outside of cells, such as the extracellular matrix. Here, we describe a pipeline, Pixie, that achieves robust and quantitative annotation of pixel-level features using unsupervised clustering and show its application across a variety of biological contexts and multiplexed imaging platforms. Furthermore, current cell phenotyping strategies that rely on unsupervised clustering can be labor intensive and require large amounts of manual cluster adjustments. We demonstrate how pixel clusters that lie within cells can be used to improve cell annotations. We comprehensively evaluate pre-processing steps and parameter choices to optimize clustering performance and quantify the reproducibility of our method. Importantly, Pixie is open source and easily customizable through a user-friendly interface.

Suggested Citation

  • Candace C. Liu & Noah F. Greenwald & Alex Kong & Erin F. McCaffrey & Ke Xuan Leow & Dunja Mrdjen & Bryan J. Cannon & Josef Lorenz Rumberger & Sricharan Reddy Varra & Michael Angelo, 2023. "Robust phenotyping of highly multiplexed tissue imaging data using pixel-level clustering," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40068-5
    DOI: 10.1038/s41467-023-40068-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40068-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40068-5?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. Ovijit Chaudhuri & Justin Cooper-White & Paul A. Janmey & David J. Mooney & Vivek B. Shenoy, 2020. "Effects of extracellular matrix viscoelasticity on cellular behaviour," Nature, Nature, vol. 584(7822), pages 535-546, August.
    2. Alex Baranski & Idan Milo & Shirley Greenbaum & John-Paul Oliveria & Dunja Mrdjen & Michael Angelo & Leeat Keren, 2021. "MAUI (MBI Analysis User Interface)—An image processing pipeline for Multiplexed Mass Based Imaging," PLOS Computational Biology, Public Library of Science, vol. 17(4), pages 1-16, April.
    3. André F. Rendeiro & Hiranmayi Ravichandran & Yaron Bram & Vasuretha Chandar & Junbum Kim & Cem Meydan & Jiwoon Park & Jonathan Foox & Tyler Hether & Sarah Warren & Youngmi Kim & Jason Reeves & Steven , 2021. "The spatial landscape of lung pathology during COVID-19 progression," Nature, Nature, vol. 593(7860), pages 564-569, May.
    4. Peng Qiu, 2020. "Embracing the dropouts in single-cell RNA-seq analysis," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    5. Hartland W. Jackson & Jana R. Fischer & Vito R. T. Zanotelli & H. Raza Ali & Robert Mechera & Savas D. Soysal & Holger Moch & Simone Muenst & Zsuzsanna Varga & Walter P. Weber & Bernd Bodenmiller, 2020. "The single-cell pathology landscape of breast cancer," Nature, Nature, vol. 578(7796), pages 615-620, February.
    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. Peng Lu & Karolyn A. Oetjen & Diane E. Bender & Marianna B. Ruzinova & Daniel A. C. Fisher & Kevin G. Shim & Russell K. Pachynski & W. Nathaniel Brennen & Stephen T. Oh & Daniel C. Link & Daniel L. J., 2023. "IMC-Denoise: a content aware denoising pipeline to enhance Imaging Mass Cytometry," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Yunhao Bai & Bokai Zhu & John-Paul Oliveria & Bryan J. Cannon & Dorien Feyaerts & Marc Bosse & Kausalia Vijayaragavan & Noah F. Greenwald & Darci Phillips & Christian M. Schürch & Samuel M. Naik & Edw, 2023. "Expanded vacuum-stable gels for multiplexed high-resolution spatial histopathology," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Thomas Hu & Mayar Allam & Shuangyi Cai & Walter Henderson & Brian Yueh & Aybuke Garipcan & Anton V. Ievlev & Maryam Afkarian & Semir Beyaz & Ahmet F. Coskun, 2023. "Single-cell spatial metabolomics with cell-type specific protein profiling for tissue systems biology," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Yael Amitay & Yuval Bussi & Ben Feinstein & Shai Bagon & Idan Milo & Leeat Keren, 2023. "CellSighter: a neural network to classify cells in highly multiplexed images," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Juan Du & Junlei Zhang & Lin Wang & Xun Wang & Yaxing Zhao & Jiaoying Lu & Tingmin Fan & Meng Niu & Jie Zhang & Fei Cheng & Jun Li & Qi Zhu & Daoqiang Zhang & Hao Pei & Guang Li & Xingguang Liang & He, 2023. "Selective oxidative protection leads to tissue topological changes orchestrated by macrophage during ulcerative colitis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    7. Huimin He & Xi Wei & Bin Yang & Hongzhen Liu & Mingze Sun & Yanran Li & Aixin Yan & Chuyang Y. Tang & Yuan Lin & Lizhi Xu, 2022. "Ultrastrong and multifunctional aerogels with hyperconnective network of composite polymeric nanofibers," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    8. Rui Chen & Jiasu Xu & Boqian Wang & Yi Ding & Aynur Abdulla & Yiyang Li & Lai Jiang & Xianting Ding, 2024. "SpiDe-Sr: blind super-resolution network for precise cell segmentation and clustering in spatial proteomics imaging," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Kaiwen Wang & Yuqiu Yang & Fangjiang Wu & Bing Song & Xinlei Wang & Tao Wang, 2023. "Comparative analysis of dimension reduction methods for cytometry by time-of-flight data," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Yangteng Ou & Shixiang Cao & Yang Zhang & Hongjia Zhu & Chengzhi Guo & Wei Yan & Fengxue Xin & Weiliang Dong & Yanli Zhang & Masashi Narita & Ziyi Yu & Tuomas P. J. Knowles, 2023. "Bioprinting microporous functional living materials from protein-based core-shell microgels," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Yingxin Lin & Yue Cao & Elijah Willie & Ellis Patrick & Jean Y. H. Yang, 2023. "Atlas-scale single-cell multi-sample multi-condition data integration using scMerge2," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Zhao Wang & Jan Lauko & Amanda W. Kijas & Elliot P. Gilbert & Petri Turunen & Ramanathan Yegappan & Dongxiu Zou & Jitendra Mata & Alan E. Rowan, 2023. "Snake venom-defined fibrin architecture dictates fibroblast survival and differentiation," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. 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.
    14. Zhiyuan Yuan & Yisi Li & Minglei Shi & Fan Yang & Juntao Gao & Jianhua Yao & Michael Q. Zhang, 2022. "SOTIP is a versatile method for microenvironment modeling with spatial omics data," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    15. Stefanie Hiltbrunner & Lena Cords & Sabrina Kasser & Sandra N. Freiberger & Susanne Kreutzer & Nora C. Toussaint & Linda Grob & Isabelle Opitz & Michael Messerli & Martin Zoche & Alex Soltermann & Mar, 2023. "Acquired resistance to anti-PD1 therapy in patients with NSCLC associates with immunosuppressive T cell phenotype," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Jingyang Qian & Jie Liao & Ziqi Liu & Ying Chi & Yin Fang & Yanrong Zheng & Xin Shao & Bingqi Liu & Yongjin Cui & Wenbo Guo & Yining Hu & Hudong Bao & Penghui Yang & Qian Chen & Mingxiao Li & Bing Zha, 2023. "Reconstruction of the cell pseudo-space from single-cell RNA sequencing data with scSpace," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    17. Ronja Mothes & Anna Pascual-Reguant & Ralf Koehler & Juliane Liebeskind & Alina Liebheit & Sandy Bauherr & Lars Philipsen & Carsten Dittmayer & Michael Laue & Regina Manitius & Sefer Elezkurtaj & Pawe, 2023. "Distinct tissue niches direct lung immunopathology via CCL18 and CCL21 in severe COVID-19," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Darci Phillips & Magdalena Matusiak & Belén Rivero Gutierrez & Salil S. Bhate & Graham L. Barlow & Sizun Jiang & Janos Demeter & Kimberly S. Smythe & Robert H. Pierce & Steven P. Fling & Nirasha Ramch, 2021. "Immune cell topography predicts response to PD-1 blockade in cutaneous T cell lymphoma," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    19. Tabea M. Eser & Olga Baranov & Manuel Huth & Mohammed I. M. Ahmed & Flora Deák & Kathrin Held & Luming Lin & Kami Pekayvaz & Alexander Leunig & Leo Nicolai & Georgios Pollakis & Marcus Buggert & David, 2023. "Nucleocapsid-specific T cell responses associate with control of SARS-CoV-2 in the upper airways before seroconversion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Xiaofang Jia & Jingwen Song & Wenyan Lv & Jonathan P. Hill & Jun Nakanishi & Katsuhiko Ariga, 2022. "Adaptive liquid interfaces induce neuronal differentiation of mesenchymal stem cells through lipid raft assembly," Nature Communications, Nature, vol. 13(1), pages 1-10, 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:14:y:2023:i:1:d:10.1038_s41467-023-40068-5. 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.