Specification of CNS macrophage subsets occurs postnatally in defined niches

Takahiro Masuda (), Lukas Amann, Gianni Monaco, Roman Sankowski, Ori Staszewski, Martin Krueger, Francesca Gaudio, Liqun He, Neil Paterson, Elisa Nent, Francisco Fernández-Klett, Ayato Yamasaki, Maximilian Frosch, Maximilian Fliegauf, Lance Fredrick Pahutan Bosch, Hatice Ulupinar, Nora Hagemeyer, Dietmar Schreiner, Cayce Dorrier, Makoto Tsuda, Claudia Grothe, Anne Joutel, Richard Daneman, Christer Betsholtz, Urban Lendahl, Klaus-Peter Knobeloch, Tim Lämmermann, Josef Priller, Katrin Kierdorf and Marco Prinz ()
Additional contact information
Takahiro Masuda: University of Freiburg
Lukas Amann: University of Freiburg
Gianni Monaco: University of Freiburg
Roman Sankowski: University of Freiburg
Ori Staszewski: University of Freiburg
Martin Krueger: University of Leipzig
Francesca Gaudio: Karolinska Institute
Liqun He: Rudbeck Laboratory, Uppsala University
Neil Paterson: Max Planck Institute of Immunobiology and Epigenetics
Elisa Nent: Max Planck Institute of Immunobiology and Epigenetics
Francisco Fernández-Klett: Charité − Universitätsmedizin Berlin, and DZNE
Ayato Yamasaki: Kyushu University
Maximilian Frosch: University of Freiburg
Maximilian Fliegauf: University of Freiburg
Lance Fredrick Pahutan Bosch: University of Freiburg
Hatice Ulupinar: University of Freiburg
Nora Hagemeyer: University of Freiburg
Dietmar Schreiner: Hannover Medical School
Cayce Dorrier: University of California San Diego
Makoto Tsuda: Kyushu University
Claudia Grothe: Hannover Medical School
Anne Joutel: University of Paris
Richard Daneman: University of California San Diego
Christer Betsholtz: Rudbeck Laboratory, Uppsala University
Urban Lendahl: Karolinska Institute
Klaus-Peter Knobeloch: University of Freiburg
Tim Lämmermann: Max Planck Institute of Immunobiology and Epigenetics
Josef Priller: Charité − Universitätsmedizin Berlin, and DZNE
Katrin Kierdorf: University of Freiburg
Marco Prinz: University of Freiburg

Nature, 2022, vol. 604, issue 7907, 740-748

Abstract: Abstract All tissue-resident macrophages of the central nervous system (CNS)—including parenchymal microglia, as well as CNS-associated macrophages (CAMs1) such as meningeal and perivascular macrophages2–7—are part of the CNS endogenous innate immune system that acts as the first line of defence during infections or trauma2,8–10. It has been suggested that microglia and all subsets of CAMs are derived from prenatal cellular sources in the yolk sac that were defined as early erythromyeloid progenitors11–15. However, the precise ontogenetic relationships, the underlying transcriptional programs and the molecular signals that drive the development of distinct CAM subsets in situ are poorly understood. Here we show, using fate-mapping systems, single-cell profiling and cell-specific mutants, that only meningeal macrophages and microglia share a common prenatal progenitor. By contrast, perivascular macrophages originate from perinatal meningeal macrophages only after birth in an integrin-dependent manner. The establishment of perivascular macrophages critically requires the presence of arterial vascular smooth muscle cells. Together, our data reveal a precisely timed process in distinct anatomical niches for the establishment of macrophage subsets in the CNS.

Date: 2022
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DOI: 10.1038/s41586-022-04596-2

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