An integrated cell atlas of the lung in health and disease

single-cell
rna-seq
lung
atlas
Authors

Lisa Sikkema

Ciro Ramírez-Suástegui

Daniel C. Strobl

Tessa E. Gillett

Luke Zappia

Elo Madissoon

Nikolay S. Markov

Laure-Emmanuelle Zaragosi

Yuge Ji

Meshal Ansari

Marie-Jeanne Arguel

Leonie Apperloo

Martin Banchero

Christophe Bécavin

Marijn Berg

Evgeny Chichelnitskiy

Mei-i Chung

Antoine Collin

Aurore C. A. Gay

Janine Gote-Schniering

Baharak Hooshiar Kashani

Kemal Inecik

Manu Jain

Theodore S. Kapellos

Tessa M. Kole

Sylvie Leroy

Christoph H. Mayr

Amanda J. Oliver

Michael von Papen

Lance Peter

Chase J. Taylor

Thomas Walzthoeni

Chuan Xu

Linh T. Bui

Carlo De Donno

Leander Dony

Alen Faiz

Minzhe Guo

Austin J. Gutierrez

Lukas Heumos

Ni Huang

Ignacio L. Ibarra

Nathan D. Jackson

Preetish Kadur Lakshminarasimha Murthy

Mohammad Lotfollahi

Tracy Tabib

Carlos Talavera-López

Kyle J. Travaglini

Anna Wilbrey-Clark

Kaylee B. Worlock

Masahiro Yoshida

Lung Biological Network Consortium

Maarten van den Berge

Yohan Bossé

Tushar J. Desai

Oliver Eickelberg

Naftali Kaminski

Mark A. Krasnow

Robert Lafyatis

Marko Z. Nikolic

Joseph E. Powell

Jayaraj Rajagopal

Mauricio Rojas

Orit Rozenblatt-Rosen

Max A. Seibold

Dean Sheppard

Douglas P. Shepherd

Don D. Sin

Wim Timens

Alexander M. Tsankov

Jeffrey Whitsett

Yan Xu

Nicholas E. Banovich

Pascal Barbry

Thu Elizabeth Duong

Christine S. Falk

Kerstin B. Meyer

Jonathan A. Kropski

Dana Pe’er

Herbert B. Schiller

Purushothama Rao Tata

Joachim L. Schultze

Sara A. Teichmann

Alexander V. Misharin

Martijn C. Nawijn

Malte D. Luecken

Fabian J. Theis

Date

August 6, 2023

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Abstract

Single-cell technologies have transformed our understanding of human tissues. Yet, studies typically capture only a limited number of donors and disagree on cell type definitions. Integrating many single-cell datasets can address these limitations of individual studies and capture the variability present in the population. Here we present the integrated Human Lung Cell Atlas (HLCA), combining 49 datasets of the human respiratory system into a single atlas spanning over 2.4 million cells from 486 individuals. The HLCA presents a consensus cell type re-annotation with matching marker genes, including annotations of rare and previously undescribed cell types. Leveraging the number and diversity of individuals in the HLCA, we identify gene modules that are associated with demographic covariates such as age, sex and body mass index, as well as gene modules changing expression along the proximal-to-distal axis of the bronchial tree. Mapping new data to the HLCA enables rapid data annotation and interpretation. Using the HLCA as a reference for the study of disease, we identify shared cell states across multiple lung diseases, including SPP1+ profibrotic monocyte-derived macrophages in COVID-19, pulmonary fibrosis and lung carcinoma. Overall, the HLCA serves as an example for the development and use of large-scale, cross-dataset organ atlases within the Human Cell Atlas.

Citation

BibTeX citation:
@article{sikkema2023,
  author = {Sikkema, Lisa and Ramírez-Suástegui, Ciro and C. Strobl,
    Daniel and E. Gillett, Tessa and Zappia, Luke and Madissoon, Elo and
    S. Markov, Nikolay and Zaragosi, Laure-Emmanuelle and Ji, Yuge and
    Ansari, Meshal and Arguel, Marie-Jeanne and Apperloo, Leonie and
    Banchero, Martin and Bécavin, Christophe and Berg, Marijn and
    Chichelnitskiy, Evgeny and Chung, Mei-i and Collin, Antoine and C.
    A. Gay, Aurore and Gote-Schniering, Janine and Hooshiar Kashani,
    Baharak and Inecik, Kemal and Jain, Manu and S. Kapellos, Theodore
    and M. Kole, Tessa and Leroy, Sylvie and H. Mayr, Christoph and J.
    Oliver, Amanda and von Papen, Michael and Peter, Lance and J.
    Taylor, Chase and Walzthoeni, Thomas and Xu, Chuan and T. Bui, Linh
    and De Donno, Carlo and Dony, Leander and Faiz, Alen and Guo, Minzhe
    and J. Gutierrez, Austin and Heumos, Lukas and Huang, Ni and L.
    Ibarra, Ignacio and D. Jackson, Nathan and Kadur Lakshminarasimha
    Murthy, Preetish and Lotfollahi, Mohammad and Tabib, Tracy and
    Talavera-López, Carlos and J. Travaglini, Kyle and Wilbrey-Clark,
    Anna and B. Worlock, Kaylee and Yoshida, Masahiro and Biological
    Network Consortium, Lung and van den Berge, Maarten and Bossé, Yohan
    and J. Desai, Tushar and Eickelberg, Oliver and Kaminski, Naftali
    and A. Krasnow, Mark and Lafyatis, Robert and Z. Nikolic, Marko and
    E. Powell, Joseph and Rajagopal, Jayaraj and Rojas, Mauricio and
    Rozenblatt-Rosen, Orit and A. Seibold, Max and Sheppard, Dean and P.
    Shepherd, Douglas and D. Sin, Don and Timens, Wim and M. Tsankov,
    Alexander and Whitsett, Jeffrey and Xu, Yan and E. Banovich,
    Nicholas and Barbry, Pascal and Elizabeth Duong, Thu and S. Falk,
    Christine and B. Meyer, Kerstin and A. Kropski, Jonathan and Pe’er,
    Dana and B. Schiller, Herbert and Rao Tata, Purushothama and L.
    Schultze, Joachim and A. Teichmann, Sara and V. Misharin, Alexander
    and C. Nawijn, Martijn and D. Luecken, Malte and J. Theis, Fabian},
  title = {An Integrated Cell Atlas of the Lung in Health and Disease},
  journal = {Nature Medicine},
  volume = {29},
  number = {6},
  pages = {1563-1577},
  date = {2023-08-06},
  url = {https://lazappi.id.au/publications/2023-sikkema-HLCA/},
  doi = {10.1038/s41591-023-02327-2},
  issn = {1078-8956},
  langid = {en},
  abstract = {Single-cell technologies have transformed our
    understanding of human tissues. Yet, studies typically capture only
    a limited number of donors and disagree on cell type definitions.
    Integrating many single-cell datasets can address these limitations
    of individual studies and capture the variability present in the
    population. Here we present the integrated Human Lung Cell Atlas
    (HLCA), combining 49 datasets of the human respiratory system into a
    single atlas spanning over 2.4 million cells from 486 individuals.
    The HLCA presents a consensus cell type re-annotation with matching
    marker genes, including annotations of rare and previously
    undescribed cell types. Leveraging the number and diversity of
    individuals in the HLCA, we identify gene modules that are
    associated with demographic covariates such as age, sex and body
    mass index, as well as gene modules changing expression along the
    proximal-to-distal axis of the bronchial tree. Mapping new data to
    the HLCA enables rapid data annotation and interpretation. Using the
    HLCA as a reference for the study of disease, we identify shared
    cell states across multiple lung diseases, including SPP1+
    profibrotic monocyte-derived macrophages in COVID-19, pulmonary
    fibrosis and lung carcinoma. Overall, the HLCA serves as an example
    for the development and use of large-scale, cross-dataset organ
    atlases within the Human Cell Atlas.}
}
For attribution, please cite this work as:
Sikkema, Lisa, Ciro Ramírez-Suástegui, Daniel C. Strobl, Tessa E. Gillett, Luke Zappia, Elo Madissoon, Nikolay S. Markov, et al. 2023. “An Integrated Cell Atlas of the Lung in Health and Disease.” Nature Medicine 29 (6): 1563–77. https://doi.org/10.1038/s41591-023-02327-2.