Nasopharyngeal lymphatic plexus is a hub for cerebrospinal fluid drainage

Jin-Hui Yoon, Hokyung Jin, Hae Jin Kim, Seon Pyo Hong, Myung Jin Yang, Ji Hoon Ahn, Young-Chan Kim, Jincheol Seo, Yongjeon Lee, Donald M. McDonald, Michael J. Davis () and Gou Young Koh ()
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Jin-Hui Yoon: Institute for Basic Science
Hokyung Jin: Institute for Basic Science
Hae Jin Kim: University of Missouri
Seon Pyo Hong: Institute for Basic Science
Myung Jin Yang: Institute for Basic Science
Ji Hoon Ahn: Institute for Basic Science
Young-Chan Kim: Institute for Basic Science
Jincheol Seo: Korea Research Institute of Bioscience and Biotechnology
Yongjeon Lee: Korea Research Institute of Bioscience and Biotechnology
Donald M. McDonald: University of California, San Francisco
Michael J. Davis: University of Missouri
Gou Young Koh: Institute for Basic Science

Nature, 2024, vol. 625, issue 7996, 768-777

Abstract: Abstract Cerebrospinal fluid (CSF) in the subarachnoid space around the brain has long been known to drain through the lymphatics to cervical lymph nodes1–17, but the connections and regulation have been challenging to identify. Here, using fluorescent CSF tracers in Prox1-GFP lymphatic reporter mice18, we found that the nasopharyngeal lymphatic plexus is a major hub for CSF outflow to deep cervical lymph nodes. This plexus had unusual valves and short lymphangions but no smooth-muscle coverage, whereas downstream deep cervical lymphatics had typical semilunar valves, long lymphangions and smooth muscle coverage that transported CSF to the deep cervical lymph nodes. α-Adrenergic and nitric oxide signalling in the smooth muscle cells regulated CSF drainage through the transport properties of deep cervical lymphatics. During ageing, the nasopharyngeal lymphatic plexus atrophied, but deep cervical lymphatics were not similarly altered, and CSF outflow could still be increased by adrenergic or nitric oxide signalling. Single-cell analysis of gene expression in lymphatic endothelial cells of the nasopharyngeal plexus of aged mice revealed increased type I interferon signalling and other inflammatory cytokines. The importance of evidence for the nasopharyngeal lymphatic plexus functioning as a CSF outflow hub is highlighted by its regression during ageing. Yet, the ageing-resistant pharmacological activation of deep cervical lymphatic transport towards lymph nodes can still increase CSF outflow, offering an approach for augmenting CSF clearance in age-related neurological conditions in which greater efflux would be beneficial.

Date: 2024
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DOI: 10.1038/s41586-023-06899-4

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