Structural cells are key regulators of organ-specific immune responses

Thomas Krausgruber, Nikolaus Fortelny, Victoria Fife-Gernedl, Martin Senekowitsch, Linda C. Schuster, Alexander Lercher, Amelie Nemc, Christian Schmidl, André F. Rendeiro, Andreas Bergthaler and Christoph Bock ()
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Thomas Krausgruber: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Nikolaus Fortelny: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Victoria Fife-Gernedl: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Martin Senekowitsch: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Linda C. Schuster: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Alexander Lercher: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Amelie Nemc: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Christian Schmidl: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
André F. Rendeiro: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Andreas Bergthaler: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences
Christoph Bock: CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences

Nature, 2020, vol. 583, issue 7815, 296-302

Abstract: Abstract The mammalian immune system implements a remarkably effective set of mechanisms for fighting pathogens1. Its main components are haematopoietic immune cells, including myeloid cells that control innate immunity, and lymphoid cells that constitute adaptive immunity2. However, immune functions are not unique to haematopoietic cells, and many other cell types display basic mechanisms of pathogen defence3–5. To advance our understanding of immunology outside the haematopoietic system, here we systematically investigate the regulation of immune genes in the three major types of structural cells: epithelium, endothelium and fibroblasts. We characterize these cell types across twelve organs in mice, using cellular phenotyping, transcriptome sequencing, chromatin accessibility profiling and epigenome mapping. This comprehensive dataset revealed complex immune gene activity and regulation in structural cells. The observed patterns were highly organ-specific and seem to modulate the extensive interactions between structural cells and haematopoietic immune cells. Moreover, we identified an epigenetically encoded immune potential in structural cells under tissue homeostasis, which was triggered in response to systemic viral infection. This study highlights the prevalence and organ-specific complexity of immune gene activity in non-haematopoietic structural cells, and it provides a high-resolution, multi-omics atlas of the epigenetic and transcriptional networks that regulate structural cells in the mouse.

Date: 2020
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DOI: 10.1038/s41586-020-2424-4

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