Cell Reports (Jan 2023)
Single-cell RNA sequencing identifies a population of human liver-type ILC1s
- Benjamin Krämer,
- Ansel P. Nalin,
- Feiyang Ma,
- Sarah Eickhoff,
- Philipp Lutz,
- Sonia Leonardelli,
- Felix Goeser,
- Claudia Finnemann,
- Gudrun Hack,
- Jan Raabe,
- Michael ToVinh,
- Sarah Ahmad,
- Christoph Hoffmeister,
- Kim M. Kaiser,
- Steffen Manekeller,
- Vittorio Branchi,
- Tobias Bald,
- Michael Hölzel,
- Robert Hüneburg,
- Hans Dieter Nischalke,
- Alexander Semaan,
- Bettina Langhans,
- Dominik J. Kaczmarek,
- Brooke Benner,
- Matthew R. Lordo,
- Jesse Kowalski,
- Adam Gerhardt,
- Jörg Timm,
- Marieta Toma,
- Raphael Mohr,
- Andreas Türler,
- Arthur Charpentier,
- Tobias van Bremen,
- Georg Feldmann,
- Arne Sattler,
- Katja Kotsch,
- Ali T. Abdallah,
- Christian P. Strassburg,
- Ulrich Spengler,
- William E. Carson, III,
- Bethany L. Mundy-Bosse,
- Matteo Pellegrini,
- Timothy E. O’Sullivan,
- Aharon G. Freud,
- Jacob Nattermann
Affiliations
- Benjamin Krämer
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany; Corresponding author
- Ansel P. Nalin
- Medical Scientist Training Program, The Ohio State University, Columbus, OH 43210, USA; Biomedical Sciences Graduate Program, The Ohio State University, Columbus, OH 43210, USA
- Feiyang Ma
- Molecular Cell and Developmental Biology, College of Life Sciences, University of California Los Angeles, Los Angeles, CA 90095, USA
- Sarah Eickhoff
- Institute of Experimental Oncology (IEO), Medical Faculty, University Hospital Bonn, University of Bonn, 53127 Bonn, Germany
- Philipp Lutz
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Sonia Leonardelli
- Institute of Experimental Oncology (IEO), Medical Faculty, University Hospital Bonn, University of Bonn, 53127 Bonn, Germany
- Felix Goeser
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Claudia Finnemann
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Gudrun Hack
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Jan Raabe
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Michael ToVinh
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Sarah Ahmad
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Christoph Hoffmeister
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Kim M. Kaiser
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Steffen Manekeller
- Department of Surgery, University of Bonn, 53127 Bonn, Germany
- Vittorio Branchi
- Department of Surgery, University of Bonn, 53127 Bonn, Germany
- Tobias Bald
- Institute of Experimental Oncology (IEO), Medical Faculty, University Hospital Bonn, University of Bonn, 53127 Bonn, Germany
- Michael Hölzel
- Institute of Experimental Oncology (IEO), Medical Faculty, University Hospital Bonn, University of Bonn, 53127 Bonn, Germany
- Robert Hüneburg
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany
- Hans Dieter Nischalke
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany
- Alexander Semaan
- Department of Surgery, University of Bonn, 53127 Bonn, Germany
- Bettina Langhans
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Dominik J. Kaczmarek
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany
- Brooke Benner
- Biomedical Sciences Graduate Program, The Ohio State University, Columbus, OH 43210, USA
- Matthew R. Lordo
- Medical Scientist Training Program, The Ohio State University, Columbus, OH 43210, USA; Biomedical Sciences Graduate Program, The Ohio State University, Columbus, OH 43210, USA
- Jesse Kowalski
- Nationwide Children’s Hospital, Columbus, OH, USA
- Adam Gerhardt
- College of Medicine, University of Cincinnati, Cincinnati, OH 45221, USA
- Jörg Timm
- Institute of Virology, University of Duesseldorf, 40225 Düsseldorf, Germany
- Marieta Toma
- Department of Pathology, University of Bonn, 53127 Bonn, Germany
- Raphael Mohr
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany
- Andreas Türler
- General and Visceral Surgery, Johanniter Hospital, 53113 Bonn, Germany
- Arthur Charpentier
- Department of Otorhinolaryngology/Head and Neck Surgery, University of Bonn, 53127 Bonn, Germany; Department of Otorhinolaryngology, Head and Neck Surgery, Medical Faculty, University of Cologne, 50931 Cologne, Germany
- Tobias van Bremen
- Department of Otorhinolaryngology/Head and Neck Surgery, University of Bonn, 53127 Bonn, Germany
- Georg Feldmann
- Department of Internal Medicine III, University of Bonn, 53127 Bonn, Germany
- Arne Sattler
- Clinic for Surgery, Transplant Immunology Lab, Charité University Hospital Berlin, 10117 Berlin, Germany
- Katja Kotsch
- Clinic for Surgery, Transplant Immunology Lab, Charité University Hospital Berlin, 10117 Berlin, Germany
- Ali T. Abdallah
- Interdisciplinary Center for Clinical Research, RWTH Aachen University, 52074 Aachen, Germany
- Christian P. Strassburg
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany
- Ulrich Spengler
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- William E. Carson, III
- Division of Surgical Oncology, Department of Surgery, Comprehensive Cancer Center and The James Cancer Hospital and Solove Research Institute, Columbus, OH 43210, USA
- Bethany L. Mundy-Bosse
- Division of Hematology, Department of Internal Medicine, Comprehensive Cancer Center, The James Cancer Hospital and Solove Research Institute, The Ohio State University, Columbus, OH 43210, USA
- Matteo Pellegrini
- Molecular Cell and Developmental Biology, College of Life Sciences, University of California Los Angeles, Los Angeles, CA 90095, USA
- Timothy E. O’Sullivan
- Department of Microbiology, Immunology, and Molecular Genetics, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA 900953, USA
- Aharon G. Freud
- Department of Pathology, Comprehensive Cancer Center, The James Cancer Hospital and Solove Research Institute, The Ohio State University, Columbus, OH 43210, USA; Corresponding author
- Jacob Nattermann
- Department of Internal Medicine I, University of Bonn, 53127 Bonn, Germany; German Center for Infection Research (DZIF), 53127 Bonn, Germany
- Journal volume & issue
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Vol. 42,
no. 1
p. 111937
Abstract
Summary: Group 1 innate lymphoid cells (ILCs) comprise a heterogeneous family of cytotoxic natural killer (NK) cells and ILC1s. We identify a population of “liver-type” ILC1s with transcriptional, phenotypic, and functional features distinct from those of conventional and liver-resident NK cells as well as from other previously described human ILC1 subsets. LT-ILC1s are CD49a+CD94+CD200R1+, express the transcription factor T-BET, and do not express the activating receptor NKp80 or the transcription factor EOMES. Similar to NK cells, liver-type ILC1s produce IFN-γ, TNF-α, and GM-CSF; however, liver-type ILC1s also produce IL-2 and lack perforin and granzyme-B. Liver-type ILC1s are expanded in cirrhotic liver tissues, and they can be produced from blood-derived ILC precursors in vitro in the presence of TGF-β1 and liver sinusoidal endothelial cells. Cells with similar signature and function can also be found in tonsil and intestinal tissues. Collectively, our study identifies and classifies a population of human cross-tissue ILC1s.
