Origin and differentiation trajectories of fibroblastic reticular cells in the splenic white pulp

Hung-Wei Cheng, Lucas Onder, Mario Novkovic, Charlotte Soneson, Mechthild Lütge, Natalia Pikor, Elke Scandella, Mark D. Robinson, Jun-ichi Miyazaki, Anne Tersteegen, Ursula Sorg, Klaus Pfeffer, Thomas Rülicke, Thomas Hehlgans and Burkhard Ludewig ()
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Hung-Wei Cheng: Institute of Immunobiology, Kantonsspital St. Gallen
Lucas Onder: Institute of Immunobiology, Kantonsspital St. Gallen
Mario Novkovic: Institute of Immunobiology, Kantonsspital St. Gallen
Charlotte Soneson: Institute of Molecular Life Sciences and SIB Swiss Institute of Bioinformatics, University of Zurich
Mechthild Lütge: Institute of Immunobiology, Kantonsspital St. Gallen
Natalia Pikor: Institute of Immunobiology, Kantonsspital St. Gallen
Elke Scandella: Institute of Immunobiology, Kantonsspital St. Gallen
Mark D. Robinson: Institute of Molecular Life Sciences and SIB Swiss Institute of Bioinformatics, University of Zurich
Jun-ichi Miyazaki: Division of Stem Cell Regulation Research, Osaka University Medical School
Anne Tersteegen: Institute of Medical Microbiology and Hospital Hygiene, University of Düsseldorf
Ursula Sorg: Institute of Medical Microbiology and Hospital Hygiene, University of Düsseldorf
Klaus Pfeffer: Institute of Medical Microbiology and Hospital Hygiene, University of Düsseldorf
Thomas Rülicke: Institute of Laboratory Animal Science, University of Veterinary Medicine Vienna
Thomas Hehlgans: Institute of Immunology, Regensburg Center for Interventional Immunology (RCI) and University Medical Center of Regensburg
Burkhard Ludewig: Institute of Immunobiology, Kantonsspital St. Gallen

Nature Communications, 2019, vol. 10, issue 1, 1-14

Abstract: Abstract The splenic white pulp is underpinned by poorly characterized stromal cells that demarcate distinct immune cell microenvironments. Here we establish fibroblastic reticular cell (FRC)-specific fate-mapping in mice to define their embryonic origin and differentiation trajectories. Our data show that all reticular cell subsets descend from multipotent progenitors emerging at embryonic day 19.5 from periarterial progenitors. Commitment of FRC progenitors is concluded during the first week of postnatal life through occupation of niches along developing central arterioles. Single cell transcriptomic analysis facilitated deconvolution of FRC differentiation trajectories and indicated that perivascular reticular cells function both as adult lymphoid organizer cells and mural cell progenitors. The lymphotoxin-β receptor-independent sustenance of postnatal progenitor stemness unveils that systemic immune surveillance in the splenic white pulp is governed through subset specification of reticular cells from a multipotent periarterial progenitor cell. In sum, the finding that discrete signaling events in perivascular niches determine the differentiation trajectories of reticular cell networks explains the development of distinct microenvironmental niches in secondary and tertiary lymphoid tissues that are crucial for the induction and regulation of innate and adaptive immune processes.

Date: 2019
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DOI: 10.1038/s41467-019-09728-3

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