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Cross-tissue immune cell analysis reveals tissue-specific adaptations and clonal architecture in humans

C Domínguez Conde, C Xu, LB Jarvis, T Gomes, SK Howlett, DB Rainbow, O Suchanek, HW King, L Mamanova, K Polanski, N Huang, ES Fasouli, KT Mahbubani, M Prete, L Tuck, N Richoz, ZK Tuong, L Campos, HS Mousa, EJ Needham, S Pritchard, T Li, R Elmentaite, J Park, DK Menon, OA Bayraktar, LK James, KB Meyer, MR Clatworthy, K Saeb-Parsy, JL Jones, SA Teichmann
doi: https://doi.org/10.1101/2021.04.28.441762
C Domínguez Conde
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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C Xu
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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LB Jarvis
2Department of Clinical Neurosciences, University of Cambridge
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T Gomes
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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SK Howlett
2Department of Clinical Neurosciences, University of Cambridge
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DB Rainbow
2Department of Clinical Neurosciences, University of Cambridge
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O Suchanek
3Molecular Immunity Unit, Department of Medicine, University of Cambridge, Cambridge, UK
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HW King
4Centre for Immunobiology, Blizard Institute, Queen Mary University of London, London, UK
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L Mamanova
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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K Polanski
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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N Huang
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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ES Fasouli
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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KT Mahbubani
5Department of Surgery, University of Cambridge and NIHR Cambridge Biomedical Research Centre, Cambridge, UK
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M Prete
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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L Tuck
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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N Richoz
3Molecular Immunity Unit, Department of Medicine, University of Cambridge, Cambridge, UK
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ZK Tuong
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
3Molecular Immunity Unit, Department of Medicine, University of Cambridge, Cambridge, UK
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L Campos
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
6West Suffolk Hospital NHS Trust, Bury Saint Edmunds, UK
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HS Mousa
2Department of Clinical Neurosciences, University of Cambridge
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EJ Needham
2Department of Clinical Neurosciences, University of Cambridge
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S Pritchard
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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T Li
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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R Elmentaite
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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J Park
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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DK Menon
7Department of Anaesthesia, University of Cambridge, Cambridge, UK
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OA Bayraktar
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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LK James
4Centre for Immunobiology, Blizard Institute, Queen Mary University of London, London, UK
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KB Meyer
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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MR Clatworthy
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
3Molecular Immunity Unit, Department of Medicine, University of Cambridge, Cambridge, UK
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K Saeb-Parsy
5Department of Surgery, University of Cambridge and NIHR Cambridge Biomedical Research Centre, Cambridge, UK
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  • For correspondence: st9@sanger.ac.uk jls53@medschl.cam.ac.uk ks10014@cam.ac.uk
JL Jones
2Department of Clinical Neurosciences, University of Cambridge
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  • For correspondence: st9@sanger.ac.uk jls53@medschl.cam.ac.uk ks10014@cam.ac.uk
SA Teichmann
1Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
8Theory of Condensed Matter, Cavendish Laboratory, Department of Physics, University of Cambridge, JJ Thomson Ave, Cambridge CB3 0HE, UK
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  • For correspondence: st9@sanger.ac.uk jls53@medschl.cam.ac.uk ks10014@cam.ac.uk
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Abstract

Despite their crucial role in health and disease, our knowledge of immune cells within human tissues remains limited. Here, we surveyed the immune compartment of 15 tissues of six deceased adult donors by single-cell RNA sequencing and paired VDJ sequencing. To systematically resolve immune cell heterogeneity across tissues, we developed CellTypist, a machine learning tool for rapid and precise cell type annotation. Using this approach, combined with detailed curation, we determined the tissue distribution of 45 finely phenotyped immune cell types and states, revealing hitherto unappreciated tissue-specific features and clonal architecture of T and B cells. In summary, our multi-tissue approach lays the foundation for identifying highly resolved immune cell types by leveraging a common reference dataset, tissue-integrated expression analysis and antigen receptor sequencing.

One Sentence Summary We provide an immune cell atlas, including antigen receptor repertoire profiling, across lymphoid and non-lymphoid human tissues.

Competing Interest Statement

In the past three years, S.A.T has worked as a consultant for Genentech and Roche, and is a remunerated member of the Scientific Advisory Boards of Biogen, GlaxoSmithKline and Foresite Labs.

Footnotes

  • ↵# Co-first authors

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted July 20, 2021.
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Cross-tissue immune cell analysis reveals tissue-specific adaptations and clonal architecture in humans
C Domínguez Conde, C Xu, LB Jarvis, T Gomes, SK Howlett, DB Rainbow, O Suchanek, HW King, L Mamanova, K Polanski, N Huang, ES Fasouli, KT Mahbubani, M Prete, L Tuck, N Richoz, ZK Tuong, L Campos, HS Mousa, EJ Needham, S Pritchard, T Li, R Elmentaite, J Park, DK Menon, OA Bayraktar, LK James, KB Meyer, MR Clatworthy, K Saeb-Parsy, JL Jones, SA Teichmann
bioRxiv 2021.04.28.441762; doi: https://doi.org/10.1101/2021.04.28.441762
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Cross-tissue immune cell analysis reveals tissue-specific adaptations and clonal architecture in humans
C Domínguez Conde, C Xu, LB Jarvis, T Gomes, SK Howlett, DB Rainbow, O Suchanek, HW King, L Mamanova, K Polanski, N Huang, ES Fasouli, KT Mahbubani, M Prete, L Tuck, N Richoz, ZK Tuong, L Campos, HS Mousa, EJ Needham, S Pritchard, T Li, R Elmentaite, J Park, DK Menon, OA Bayraktar, LK James, KB Meyer, MR Clatworthy, K Saeb-Parsy, JL Jones, SA Teichmann
bioRxiv 2021.04.28.441762; doi: https://doi.org/10.1101/2021.04.28.441762

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