Venous-plexus-associated lymphoid hubs support meningeal humoral immunity

Zachary Fitzpatrick, Nagela Ghabdan Zanluqui, Jared S. Rosenblum, Zewen Kelvin Tuong, Colin Y. C. Lee, Vikram Chandrashekhar, Maria Luciana Negro-Demontel, Andrew P. Stewart, David A. Posner, Monica Buckley, Kieren S. J. Allinson, Panagiotis Mastorakos, Prashant Chittiboina, Dragan Maric, Danielle Donahue, Adel Helmy, Tamara Tajsic, John R. Ferdinand, Anais Portet, Ana Peñalver, Eleanor Gillman, Zhengping Zhuang, Menna R. Clatworthy () and Dorian B. McGavern ()
Additional contact information
Zachary Fitzpatrick: National Institute of Health (NIH)
Nagela Ghabdan Zanluqui: National Institute of Health (NIH)
Jared S. Rosenblum: NeuroSimplicity
Zewen Kelvin Tuong: University of Cambridge
Colin Y. C. Lee: University of Cambridge
Vikram Chandrashekhar: NeuroSimplicity
Maria Luciana Negro-Demontel: National Institute of Health (NIH)
Andrew P. Stewart: University of Cambridge
David A. Posner: University of Cambridge
Monica Buckley: National Institute of Health (NIH)
Kieren S. J. Allinson: University of Cambridge
Panagiotis Mastorakos: National Institute of Health (NIH)
Prashant Chittiboina: NINDS, NIH
Dragan Maric: NINDS, NIH
Danielle Donahue: NINDS, NIH
Adel Helmy: University of Cambridge
Tamara Tajsic: University of Cambridge
John R. Ferdinand: University of Cambridge
Anais Portet: University of Cambridge
Ana Peñalver: University of Cambridge
Eleanor Gillman: University of Cambridge
Zhengping Zhuang: National Cancer Institute, NIH
Menna R. Clatworthy: University of Cambridge
Dorian B. McGavern: National Institute of Health (NIH)

Nature, 2024, vol. 628, issue 8008, 612-619

Abstract: Abstract There is increasing interest in how immune cells in the meninges—the membranes that surround the brain and spinal cord—contribute to homeostasis and disease in the central nervous system1,2. The outer layer of the meninges, the dura mater, has recently been described to contain both innate and adaptive immune cells, and functions as a site for B cell development3–6. Here we identify organized lymphoid structures that protect fenestrated vasculature in the dura mater. The most elaborate of these dural-associated lymphoid tissues (DALT) surrounded the rostral-rhinal confluence of the sinuses and included lymphatic vessels. We termed this structure, which interfaces with the skull bone marrow and a comparable venous plexus at the skull base, the rostral-rhinal venolymphatic hub. Immune aggregates were present in DALT during homeostasis and expanded with age or after challenge with systemic or nasal antigens. DALT contain germinal centre B cells and support the generation of somatically mutated, antibody-producing cells in response to a nasal pathogen challenge. Inhibition of lymphocyte entry into the rostral-rhinal hub at the time of nasal viral challenge abrogated the generation of germinal centre B cells and class-switched plasma cells, as did perturbation of B–T cell interactions. These data demonstrate a lymphoid structure around vasculature in the dura mater that can sample antigens and rapidly support humoral immune responses after local pathogen challenge.

Date: 2024
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DOI: 10.1038/s41586-024-07202-9

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