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An integrated cell atlas of the human lung in health and disease

View ORCID ProfileL Sikkema, View ORCID ProfileD Strobl, View ORCID ProfileL Zappia, E Madissoon, View ORCID ProfileNS Markov, View ORCID ProfileL Zaragosi, M Ansari, View ORCID ProfileM Arguel, L Apperloo, View ORCID ProfileC Bécavin, View ORCID ProfileM Berg, E Chichelnitskiy, M Chung, A Collin, ACA Gay, View ORCID ProfileB Hooshiar Kashani, View ORCID ProfileM Jain, T Kapellos, View ORCID ProfileTM Kole, C Mayr, View ORCID ProfileM von Papen, L Peter, C Ramírez-Suástegui, View ORCID ProfileJ Schniering, C Taylor, T Walzthoeni, View ORCID ProfileC Xu, LT Bui, View ORCID ProfileC de Donno, View ORCID ProfileL Dony, View ORCID ProfileM Guo, AJ Gutierrez, View ORCID ProfileL Heumos, View ORCID ProfileN Huang, View ORCID ProfileI Ibarra, N Jackson, View ORCID ProfileP Kadur Lakshminarasimha Murthy, View ORCID ProfileM Lotfollahi, T Tabib, View ORCID ProfileC Talavera-Lopez, View ORCID ProfileK Travaglini, A Wilbrey-Clark, View ORCID ProfileKB Worlock, View ORCID ProfileM Yoshida, Lung Biological Network Consortium, View ORCID ProfileT Desai, View ORCID ProfileO Eickelberg, View ORCID ProfileC Falk, View ORCID ProfileN Kaminski, View ORCID ProfileM Krasnow, View ORCID ProfileR Lafyatis, View ORCID ProfileM Nikolíc, View ORCID ProfileJ Powell, View ORCID ProfileJ Rajagopal, O Rozenblatt-Rosen, MA Seibold, D Sheppard, View ORCID ProfileD Shepherd, View ORCID ProfileSA Teichmann, View ORCID ProfileA Tsankov, J Whitsett, View ORCID ProfileY Xu, View ORCID ProfileNE Banovich, View ORCID ProfileP Barbry, View ORCID ProfileTE Duong, View ORCID ProfileKB Meyer, View ORCID ProfileJA Kropski, View ORCID ProfileD Pe’er, View ORCID ProfileHB Schiller, View ORCID ProfilePR Tata, View ORCID ProfileJL Schultze, View ORCID ProfileAV Misharin, View ORCID ProfileMC Nawijn, View ORCID ProfileMD Luecken, View ORCID ProfileF Theis
doi: https://doi.org/10.1101/2022.03.10.483747
L Sikkema
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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D Strobl
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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L Zappia
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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E Madissoon
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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NS Markov
3Division of Pulmonary and Critical Care Medicine, Feinberg School of Medicine, Northwestern University
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L Zaragosi
4Universite Cote d’Azur and CNRS, IPMC, 06560 Sophia Antipolis, France
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M Ansari
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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M Arguel
4Universite Cote d’Azur and CNRS, IPMC, 06560 Sophia Antipolis, France
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L Apperloo
5Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen
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C Bécavin
4Universite Cote d’Azur and CNRS, IPMC, 06560 Sophia Antipolis, France
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M Berg
5Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen
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E Chichelnitskiy
6Genomics & Immunoregulation, Life and Medical Sciences (LIMES) Institute, University of Bonn, Bonn, Germany
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M Chung
7Translational Genomics Research Institute, 445 N 5th St. Phoenix, AZ 85016
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A Collin
4Universite Cote d’Azur and CNRS, IPMC, 06560 Sophia Antipolis, France
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ACA Gay
5Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen
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B Hooshiar Kashani
8Institute of Lung Health and Immunity and Comprehensive Pneumology Center with the CPC-M bioArchive; Helmholtz Zentrum Munich; Member of the German Center for Lung Research (DZL), Munich, Germany
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M Jain
3Division of Pulmonary and Critical Care Medicine, Feinberg School of Medicine, Northwestern University
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T Kapellos
9Medizinische Hochschule Hannover, Hannover Germany
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TM Kole
10Department of Pulmonary Diseases, University of Groningen, University Medical Center Groningen
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C Mayr
8Institute of Lung Health and Immunity and Comprehensive Pneumology Center with the CPC-M bioArchive; Helmholtz Zentrum Munich; Member of the German Center for Lung Research (DZL), Munich, Germany
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M von Papen
11Research, Development & Innovation; Comma Soft AG; Bonn; Germany
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L Peter
7Translational Genomics Research Institute, 445 N 5th St. Phoenix, AZ 85016
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C Ramírez-Suástegui
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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J Schniering
8Institute of Lung Health and Immunity and Comprehensive Pneumology Center with the CPC-M bioArchive; Helmholtz Zentrum Munich; Member of the German Center for Lung Research (DZL), Munich, Germany
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C Taylor
12Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN
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T Walzthoeni
13Core Facility Genomics, Helmholtz Zentrum Munich, Munich, Germany
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C Xu
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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LT Bui
7Translational Genomics Research Institute, 445 N 5th St. Phoenix, AZ 85016
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C de Donno
14Institute of Computational Biology, Helmholtz Zentrum Munich, Munich, Germany
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L Dony
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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M Guo
15Division of Neonatology and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center, University of Cincinnati College of Medicine
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AJ Gutierrez
7Translational Genomics Research Institute, 445 N 5th St. Phoenix, AZ 85016
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L Heumos
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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N Huang
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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I Ibarra
14Institute of Computational Biology, Helmholtz Zentrum Munich, Munich, Germany
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N Jackson
16Center for Genes, Environment, and Health, National Jewish Health; Denver, CO, USA
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P Kadur Lakshminarasimha Murthy
17Department of Cell Biology, Duke University School of Medicine, Durham, NC, United States 27710
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M Lotfollahi
14Institute of Computational Biology, Helmholtz Zentrum Munich, Munich, Germany
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T Tabib
18Division of Rheumatology and Clinical Immunology, Department of Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA, USA
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C Talavera-Lopez
14Institute of Computational Biology, Helmholtz Zentrum Munich, Munich, Germany
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K Travaglini
19Department of Biochemistry, Stanford University School of Medicine
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A Wilbrey-Clark
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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KB Worlock
20UCL Respiratory, Division of Medicine, University College London, London, UK
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M Yoshida
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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T Desai
21Department of Medicine, Stanford University School of Medicine, Stanford, CA USA
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O Eickelberg
22Division of Pulmonary, Allergy and Critical Care Medicine, University of Pittsburgh, Pittsburgh, PA, USA
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C Falk
9Medizinische Hochschule Hannover, Hannover Germany
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N Kaminski
23Pulmonary, critical Care and Sleep Medicine, Yale School of Medicine
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M Krasnow
19Department of Biochemistry, Stanford University School of Medicine
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R Lafyatis
18Division of Rheumatology and Clinical Immunology, Department of Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA, USA
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M Nikolíc
20UCL Respiratory, Division of Medicine, University College London, London, UK
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J Powell
24Garvan Institute of Medical Research, Sydney, Australia; UNSW Cellular Genomics Futures Institute, UNSW, Sydney, Australia
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J Rajagopal
25Center for Regenerative Medicine, Massachusetts General Hospital, Harvard Medical School
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O Rozenblatt-Rosen
26Klarman Cell Observatory, Broad Institute of Harvard and MIT, Cambridge, MA, USA
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MA Seibold
16Center for Genes, Environment, and Health, National Jewish Health; Denver, CO, USA
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D Sheppard
27Division of Pulmonary, Critical Care, Allergy and Sleep, University of California, San Francisco
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D Shepherd
28Department of Physics and Center for Biological Physics, Arizona State University, Tempe, Az
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SA Teichmann
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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A Tsankov
29Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY, USA
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J Whitsett
30Division of Neonatology and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center
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Y Xu
30Division of Neonatology and Pulmonary Biology, Cincinnati Children’s Hospital Medical Center
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NE Banovich
7Translational Genomics Research Institute, 445 N 5th St. Phoenix, AZ 85016
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P Barbry
4Universite Cote d’Azur and CNRS, IPMC, 06560 Sophia Antipolis, France
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TE Duong
31Department of Pediatrics, Division of Respiratory Medicine, University of California San Diego, La Jolla, CA 92093, USA
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KB Meyer
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK
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JA Kropski
12Division of Allergy, Pulmonary and Critical Care Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN
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D Pe’er
32Computational and Systems Biology program, Sloan Kettering Institute, MSKCC
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HB Schiller
8Institute of Lung Health and Immunity and Comprehensive Pneumology Center with the CPC-M bioArchive; Helmholtz Zentrum Munich; Member of the German Center for Lung Research (DZL), Munich, Germany
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PR Tata
17Department of Cell Biology, Duke University School of Medicine, Durham, NC, United States 27710
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JL Schultze
33Systems Medicine, Deutsches Zentrum fur Neurodegenerative Erkrankungen (DZNE)
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AV Misharin
3Division of Pulmonary and Critical Care Medicine, Feinberg School of Medicine, Northwestern University
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  • For correspondence: malte.luecken@helmholtz-muenchen.de
MC Nawijn
5Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen
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  • For correspondence: malte.luecken@helmholtz-muenchen.de
MD Luecken
1Institute of Computational Biology, Department of Computational Health, Helmholtz Munich, Germany
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  • ORCID record for MD Luecken
  • For correspondence: malte.luecken@helmholtz-muenchen.de
F Theis
34Institute of Computational Biology, Helmholtz Center Munich, Neuherberg, Germany
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  • ORCID record for F Theis
  • For correspondence: malte.luecken@helmholtz-muenchen.de
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ABSTRACT

Organ- and body-scale cell atlases have the potential to transform our understanding of human biology. To capture the variability present in the population, these atlases must include diverse demographics such as age and ethnicity from both healthy and diseased individuals. The growth in both size and number of single-cell datasets, combined with recent advances in computational techniques, for the first time makes it possible to generate such comprehensive large-scale atlases through integration of multiple datasets. Here, we present the integrated Human Lung Cell Atlas (HLCA) combining 46 datasets of the human respiratory system into a single atlas spanning over 2.2 million cells from 444 individuals across health and disease. The HLCA contains a consensus re-annotation of published and newly generated datasets, resolving under- or misannotation of 59% of cells in the original datasets. The HLCA enables recovery of rare cell types, provides consensus marker genes for each cell type, and uncovers gene modules associated with demographic covariates and anatomical location within the respiratory system. To facilitate the use of the HLCA as a reference for single-cell lung research and allow rapid analysis of new data, we provide an interactive web portal to project datasets onto the HLCA. Finally, we demonstrate the value of the HLCA reference for interpreting disease-associated changes. Thus, the HLCA outlines a roadmap for the development and use of organ-scale cell atlases within the Human Cell Atlas.

Competing Interest Statement

PRT serves as a consultant for Surrozen Inc., Cellarity Inc., and Celldom Inc. and currently acting CEO of Iolux Inc. FJT consults for Immunai Inc., Singularity Bio B.V., CytoReason Ltd, and Omniscope Ltd, and has ownership interest in Dermagnostix GmbH and Cellarity. JAK reports grants/contracts from Boehringer Ingleheim, Bristol-Myers-Squibb, consulting fees from Janssen and Boehringer Ingelheim, study support from Genentech, and is a member of the scientific advisory board of APIE Therapeutics. SAT, in the past three years, has received remuneration for consulting and Scientific Advisory Board Membership from Genentech, Roche, Biogen, GlaxoSmithKline, Foresite Labs and Qiagen. SAT is a co-founder, board member and holds equity in Transition Bio. DS is a founder of Pliant Therapeutics, a member of the Genentech Scientific Advisory Board and has a sponsored research agreement with Abbvie. OE serves in advisory capacity to Pieris Pharmaceuticals, Blade Therapeutics, Delta 4 and YAP Therapeutics. NK served as a consultant to Boehringer Ingelheim, Third Rock, Pliant, Samumed, NuMedii, Theravance, LifeMax, Three Lake Partners, Optikira, Astra Zeneca, RohBar, Veracyte, Augmanity, CSL Behring, Galapagos, and Thyron over the last 3 years, reports Equity in Pliant and Thyron, and a grant from Veracyte, Boehringer Ingelheim, BMS and non-financial support from MiRagen and Astra Zeneca. NK has IP on novel biomarkers and therapeutics in IPF licensed to Biotech. OR is a co-inventor on patent applications filed by the Broad Institute for inventions related to single cell genomics. ORR is an employee of Genentech since October 19, 2020.

Footnotes

  • https://beta.fastgenomics.org/p/hlca

  • https://cellxgene.cziscience.com/collections/6f6d381a-7701-4781-935c-db10d30de293

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-ND 4.0 International license.
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An integrated cell atlas of the human lung in health and disease
L Sikkema, D Strobl, L Zappia, E Madissoon, NS Markov, L Zaragosi, M Ansari, M Arguel, L Apperloo, C Bécavin, M Berg, E Chichelnitskiy, M Chung, A Collin, ACA Gay, B Hooshiar Kashani, M Jain, T Kapellos, TM Kole, C Mayr, M von Papen, L Peter, C Ramírez-Suástegui, J Schniering, C Taylor, T Walzthoeni, C Xu, LT Bui, C de Donno, L Dony, M Guo, AJ Gutierrez, L Heumos, N Huang, I Ibarra, N Jackson, P Kadur Lakshminarasimha Murthy, M Lotfollahi, T Tabib, C Talavera-Lopez, K Travaglini, A Wilbrey-Clark, KB Worlock, M Yoshida, Lung Biological Network Consortium, T Desai, O Eickelberg, C Falk, N Kaminski, M Krasnow, R Lafyatis, M Nikolíc, J Powell, J Rajagopal, O Rozenblatt-Rosen, MA Seibold, D Sheppard, D Shepherd, SA Teichmann, A Tsankov, J Whitsett, Y Xu, NE Banovich, P Barbry, TE Duong, KB Meyer, JA Kropski, D Pe’er, HB Schiller, PR Tata, JL Schultze, AV Misharin, MC Nawijn, MD Luecken, F Theis
bioRxiv 2022.03.10.483747; doi: https://doi.org/10.1101/2022.03.10.483747
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An integrated cell atlas of the human lung in health and disease
L Sikkema, D Strobl, L Zappia, E Madissoon, NS Markov, L Zaragosi, M Ansari, M Arguel, L Apperloo, C Bécavin, M Berg, E Chichelnitskiy, M Chung, A Collin, ACA Gay, B Hooshiar Kashani, M Jain, T Kapellos, TM Kole, C Mayr, M von Papen, L Peter, C Ramírez-Suástegui, J Schniering, C Taylor, T Walzthoeni, C Xu, LT Bui, C de Donno, L Dony, M Guo, AJ Gutierrez, L Heumos, N Huang, I Ibarra, N Jackson, P Kadur Lakshminarasimha Murthy, M Lotfollahi, T Tabib, C Talavera-Lopez, K Travaglini, A Wilbrey-Clark, KB Worlock, M Yoshida, Lung Biological Network Consortium, T Desai, O Eickelberg, C Falk, N Kaminski, M Krasnow, R Lafyatis, M Nikolíc, J Powell, J Rajagopal, O Rozenblatt-Rosen, MA Seibold, D Sheppard, D Shepherd, SA Teichmann, A Tsankov, J Whitsett, Y Xu, NE Banovich, P Barbry, TE Duong, KB Meyer, JA Kropski, D Pe’er, HB Schiller, PR Tata, JL Schultze, AV Misharin, MC Nawijn, MD Luecken, F Theis
bioRxiv 2022.03.10.483747; doi: https://doi.org/10.1101/2022.03.10.483747

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