Postnatal expansion of mesenteric lymph node stromal cells towards reticular and CD34+ stromal cell subsets

Joern Pezoldt, Carolin Wiechers, Mangge Zou, Maria Litovchenko, Marjan Biocanin, Michael Beckstette, Katarzyna Sitnik, Martina Palatella, Guido Mierlo, Wanze Chen, Vincent Gardeux, Stefan Floess, Maria Ebel, Julie Russeil, Panagiota Arampatzi, Ehsan Vafardanejad, Antoine-Emmanuel Saliba, Bart Deplancke and Jochen Huehn ()
Additional contact information
Joern Pezoldt: Helmholtz Centre for Infection Research
Carolin Wiechers: Helmholtz Centre for Infection Research
Mangge Zou: Helmholtz Centre for Infection Research
Maria Litovchenko: École Polytechnique Fédérale de Lausanne
Marjan Biocanin: École Polytechnique Fédérale de Lausanne
Michael Beckstette: Helmholtz Centre for Infection Research
Katarzyna Sitnik: University of Veterinary Medicine Vienna
Martina Palatella: Helmholtz Centre for Infection Research
Guido Mierlo: École Polytechnique Fédérale de Lausanne
Wanze Chen: École Polytechnique Fédérale de Lausanne
Vincent Gardeux: École Polytechnique Fédérale de Lausanne
Stefan Floess: Helmholtz Centre for Infection Research
Maria Ebel: Helmholtz Centre for Infection Research
Julie Russeil: École Polytechnique Fédérale de Lausanne
Panagiota Arampatzi: University of Wuerzburg
Ehsan Vafardanejad: Helmholtz Center for Infection Research (HZI)
Antoine-Emmanuel Saliba: Helmholtz Center for Infection Research (HZI)
Bart Deplancke: École Polytechnique Fédérale de Lausanne
Jochen Huehn: Helmholtz Centre for Infection Research

Nature Communications, 2022, vol. 13, issue 1, 1-19

Abstract: Abstract Gut-draining mesenteric lymph nodes (LN) provide the framework to shape intestinal adaptive immune responses. Based on the transcriptional signatures established by our previous work, the composition and immunomodulatory function of LN stromal cells (SC) vary according to location. Here, we describe the single-cell composition and development of the SC compartment within mesenteric LNs derived from postnatal to aged mice. We identify CD34+ SC and fibroblastic reticular stromal cell (FRC) progenitors as putative progenitors, both supplying the typical rapid postnatal mesenteric LN expansion. We further establish the location-specific chromatin accessibility and DNA methylation landscape of non-endothelial SCs and identify a microbiota-independent core epigenomic signature, showing characteristic differences between SCs from mesenteric and skin-draining peripheral LNs. The epigenomic landscape of SCs points to dynamic expression of Irf3 along the differentiation trajectories of FRCs. Accordingly, a mesenchymal stem cell line acquires a Cxcl9+ FRC molecular phenotype upon lentiviral overexpression of Irf3, and the relevance of Irf3 for SC biology is further underscored by the diminished proportion of Ccl19+ and Cxcl9+ FRCs in LNs of Irf3-/- mice. Together, our data constitute a comprehensive transcriptional and epigenomic map of mesenteric LNSC development in early life and dissect location-specific, microbiota-independent properties of non-endothelial SCs.

Date: 2022
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DOI: 10.1038/s41467-022-34868-4

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