Early human lung immune cell development and its role in epithelial cell fate-Reference-Cited by-同舟云学术

Early human lung immune cell development and its role in epithelial cell fate

Published:2023-12-22 Issue:90 Volume:8 Page:
ISSN:2470-9468
Container-title:Science Immunology
language:en
Short-container-title:Sci. Immunol.

Author:

Barnes Josephine L.¹^ORCID,Yoshida Masahiro¹²^ORCID,He Peng³⁴^ORCID,Worlock Kaylee B.¹,Lindeboom Rik G.H.³⁵^ORCID,Suo Chenqu³^ORCID,Pett J. Patrick³^ORCID,Wilbrey-Clark Anna³^ORCID,Dann Emma³^ORCID,Mamanova Lira³⁶^ORCID,Richardson Laura³^ORCID,Polanski Krzysztof³^ORCID,Pennycuick Adam¹^ORCID,Allen-Hyttinen Jessica¹^ORCID,Herczeg Iván T.¹^ORCID,Arzili Romina¹^ORCID,Hynds Robert E.⁷⁸^ORCID,Teixeira Vitor H.¹^ORCID,Haniffa Muzlifah³⁹¹⁰^ORCID,Lim Kyungtae¹¹¹²^ORCID,Sun Dawei¹¹^ORCID,Rawlins Emma L.¹¹^ORCID,Oliver Amanda J.³^ORCID,Lyons Paul A.¹³¹⁴^ORCID,Marioni John C.³⁴¹⁵^ORCID,Ruhrberg Christiana¹⁶^ORCID,Tuong Zewen Kelvin³¹³¹⁷^ORCID,Clatworthy Menna R.³¹³^ORCID,Reading James L.⁸¹⁸^ORCID,Janes Sam M.¹⁸¹⁹^ORCID,Teichmann Sarah A.³¹⁰²⁰^ORCID,Meyer Kerstin B.³^ORCID,Nikolić Marko Z.¹¹⁹^ORCID

Affiliation:

1. UCL Respiratory, Division of Medicine, University College London, London, UK.

2. Division of Respiratory Diseases, Department of Internal Medicine, Jikei University School of Medicine, Tokyo, Japan.

3. Wellcome Sanger Institute, Wellcome Genome Campus, Cambridge, UK.

4. European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Cambridge, UK.

5. Netherlands Cancer Institute, Amsterdam, Netherlands.

6. Enhanc3D Genomics Ltd, Cambridge, UK.

7. Epithelial Cell Biology in ENT Research (EpiCENTR) Group, Developmental Biology and Cancer Department, Great Ormond Street UCL Institute of Child Health, University College London, London, UK.

8. CRUK Lung Cancer Centre Of Excellence, UCL Cancer Institute, University College London, London, UK.

9. Biosciences Institute, Newcastle University, Newcastle upon Tyne, UK.

10. Department of Dermatology and NIHR Newcastle Biomedical Research Centre, Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK.

11. Wellcome Trust/CRUK Gurdon Institute and Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.

12. Department of Life Sciences, Korea University, Seoul, Republic of Korea.

13. Department of Medicine, University of Cambridge, Cambridge Biomedical Campus, Cambridge, UK.

14. Cambridge Institute of Therapeutic Immunology and Infectious Disease, Jeffrey Cheah Biomedical Centre, Cambridge Biomedical Campus, Cambridge, UK.

15. CRUK Cambridge Institute, University of Cambridge, Cambridge, UK.

16. UCL Institute of Ophthalmology, University College London, London, UK.

17. Ian Frazer Centre for Children's Immunotherapy Research, Child Health Research Centre, Faculty of Medicine, University of Queensland, Brisbane, QLD, Australia.

18. Tumour Immunodynamics and Interception Laboratory, Cancer Institute, University College London, London, UK.

19. University College London Hospitals NHS Foundation Trust, London, UK.

20. Department of Physics/Cavendish Laboratory, University of Cambridge, Cambridge, UK.

Abstract

Studies of human lung development have focused on epithelial and mesenchymal cell types and function, but much less is known about the developing lung immune cells, even though the airways are a major site of mucosal immunity after birth. An unanswered question is whether tissue-resident immune cells play a role in shaping the tissue as it develops in utero. Here, we profiled human embryonic and fetal lung immune cells using scRNA-seq, smFISH, and immunohistochemistry. At the embryonic stage, we observed an early wave of innate immune cells, including innate lymphoid cells, natural killer cells, myeloid cells, and lineage progenitors. By the canalicular stage, we detected naive T lymphocytes expressing high levels of cytotoxicity genes and the presence of mature B lymphocytes, including B-1 cells. Our analysis suggests that fetal lungs provide a niche for full B cell maturation. Given the presence and diversity of immune cells during development, we also investigated their possible effect on epithelial maturation. We found that IL-1β drives epithelial progenitor exit from self-renewal and differentiation to basal cells in vitro. In vivo, IL-1β–producing myeloid cells were found throughout the lung and adjacent to epithelial tips, suggesting that immune cells may direct human lung epithelial development.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

General Medicine,Immunology

Link

https://www.science.org/doi/pdf/10.1126/sciimmunol.adf9988

Reference84 articles.

1. Human lung development: recent progress and new challenges

2. National Heart, Lung, and Blood Institute and Building Respiratory Epithelium and Tissue for Health (BREATH) Consortium Workshop Report: Moving Forward in Lung Regeneration

3. World Health Organization Noncommunicable diseases (2021); www.who.int/news-room/fact-sheets/detail/noncommunicable-diseases.

4. Human embryonic lung epithelial tips are multipotent progenitors that can be expanded in vitro as long-term self-renewing organoids

5. Embryonic and Early Fetal Development of Human Lung Vasculature and Its Functional Implications

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