Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders

Simone Brioschi; Wei Le Wang; Vincent Peng; Meng Wang; Irina Shchukina; Zev J. Greenberg; Jennifer K. Bando; Natalia Jaeger; Rafael S. Czepielewski; Amanda Swain; Denis A. Mogilenko; Wandy L. Beatty; Peter Bayguinov; James A.J. Fitzpatrick; Laura G. Schuettpelz; Catrina C. Fronick; Igor Smirnov; Jonathan Kipnis; Virginia S. Shapiro; Gregory F. Wu; Susan Gilfillan; Marina Cella; Maxim N. Artyomov; Steven H. Kleinstein; Marco Colonna

doi:10.1126/science.abf9277

Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders

Simone Brioschi, Wei Le Wang, Vincent Peng, Meng Wang, Irina Shchukina, Zev J. Greenberg, Jennifer K. Bando, Natalia Jaeger, Rafael S. Czepielewski, Amanda Swain, Denis A. Mogilenko, Wandy L. Beatty, Peter Bayguinov, James A.J. Fitzpatrick, Laura G. Schuettpelz, Catrina C. Fronick, Igor Smirnov, Jonathan Kipnis, Virginia S. Shapiro, Gregory F. WuSusan Gilfillan, Marina Cella, Maxim N. Artyomov, Steven H. Kleinstein, Marco Colonna

Research output: Contribution to journal › Article › peer-review

255 Scopus citations

Abstract

The meninges contain adaptive immune cells that provide immunosurveillance of the central nervous system (CNS). These cells are thought to derive from the systemic circulation. Through single-cell analyses, confocal imaging, bone marrow chimeras, and parabiosis experiments, we show that meningeal B cells derive locally from the calvaria, which harbors a bone marrow niche for hematopoiesis. B cells reach the meninges from the calvaria through specialized vascular connections. This calvarial–meningeal path of B cell development may provide the CNS with a constant supply of B cells educated by CNS antigens. Conversely, we show that a subset of antigen-experienced B cells that populate the meninges in aging mice are blood-borne. These results identify a private source for meningeal B cells, which may help maintain immune privilege within the CNS.

Original language	English
Article number	eabf9277
Journal	Science
Volume	373
Issue number	6553
DOIs	https://doi.org/10.1126/science.abf9277
State	Published - Jul 23 2021

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Brioschi, S., Wang, W. L., Peng, V., Wang, M., Shchukina, I., Greenberg, Z. J., Bando, J. K., Jaeger, N., Czepielewski, R. S., Swain, A., Mogilenko, D. A., Beatty, W. L., Bayguinov, P., Fitzpatrick, J. A. J., Schuettpelz, L. G., Fronick, C. C., Smirnov, I., Kipnis, J., Shapiro, V. S., ... Colonna, M. (2021). Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders. Science, 373(6553), Article eabf9277. https://doi.org/10.1126/science.abf9277

@article{54d27933b48c43b796cc7784da69f482,

title = "Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders",

abstract = "The meninges contain adaptive immune cells that provide immunosurveillance of the central nervous system (CNS). These cells are thought to derive from the systemic circulation. Through single-cell analyses, confocal imaging, bone marrow chimeras, and parabiosis experiments, we show that meningeal B cells derive locally from the calvaria, which harbors a bone marrow niche for hematopoiesis. B cells reach the meninges from the calvaria through specialized vascular connections. This calvarial–meningeal path of B cell development may provide the CNS with a constant supply of B cells educated by CNS antigens. Conversely, we show that a subset of antigen-experienced B cells that populate the meninges in aging mice are blood-borne. These results identify a private source for meningeal B cells, which may help maintain immune privilege within the CNS.",

author = "Simone Brioschi and Wang, {Wei Le} and Vincent Peng and Meng Wang and Irina Shchukina and Greenberg, {Zev J.} and Bando, {Jennifer K.} and Natalia Jaeger and Czepielewski, {Rafael S.} and Amanda Swain and Mogilenko, {Denis A.} and Beatty, {Wandy L.} and Peter Bayguinov and Fitzpatrick, {James A.J.} and Schuettpelz, {Laura G.} and Fronick, {Catrina C.} and Igor Smirnov and Jonathan Kipnis and Shapiro, {Virginia S.} and Wu, {Gregory F.} and Susan Gilfillan and Marina Cella and Artyomov, {Maxim N.} and Kleinstein, {Steven H.} and Marco Colonna",

year = "2021",

month = jul,

day = "23",

doi = "10.1126/science.abf9277",

language = "English",

volume = "373",

journal = "Science",

issn = "0036-8075",

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Brioschi, S, Wang, WL, Peng, V, Wang, M, Shchukina, I, Greenberg, ZJ, Bando, JK, Jaeger, N, Czepielewski, RS, Swain, A, Mogilenko, DA, Beatty, WL , Bayguinov, P, Fitzpatrick, JAJ, Schuettpelz, LG, Fronick, CC, Smirnov, I , Kipnis, J, Shapiro, VS, Wu, GF , Gilfillan, S , Cella, M, Artyomov, MN, Kleinstein, SH & Colonna, M 2021, 'Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders', Science, vol. 373, no. 6553, eabf9277. https://doi.org/10.1126/science.abf9277

TY - JOUR

T1 - Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders

AU - Brioschi, Simone

AU - Wang, Wei Le

AU - Peng, Vincent

AU - Wang, Meng

AU - Shchukina, Irina

AU - Greenberg, Zev J.

AU - Bando, Jennifer K.

AU - Jaeger, Natalia

AU - Czepielewski, Rafael S.

AU - Swain, Amanda

AU - Mogilenko, Denis A.

AU - Beatty, Wandy L.

AU - Bayguinov, Peter

AU - Fitzpatrick, James A.J.

AU - Schuettpelz, Laura G.

AU - Fronick, Catrina C.

AU - Smirnov, Igor

AU - Kipnis, Jonathan

AU - Shapiro, Virginia S.

AU - Wu, Gregory F.

AU - Gilfillan, Susan

AU - Cella, Marina

AU - Artyomov, Maxim N.

AU - Kleinstein, Steven H.

AU - Colonna, Marco

PY - 2021/7/23

Y1 - 2021/7/23

N2 - The meninges contain adaptive immune cells that provide immunosurveillance of the central nervous system (CNS). These cells are thought to derive from the systemic circulation. Through single-cell analyses, confocal imaging, bone marrow chimeras, and parabiosis experiments, we show that meningeal B cells derive locally from the calvaria, which harbors a bone marrow niche for hematopoiesis. B cells reach the meninges from the calvaria through specialized vascular connections. This calvarial–meningeal path of B cell development may provide the CNS with a constant supply of B cells educated by CNS antigens. Conversely, we show that a subset of antigen-experienced B cells that populate the meninges in aging mice are blood-borne. These results identify a private source for meningeal B cells, which may help maintain immune privilege within the CNS.

AB - The meninges contain adaptive immune cells that provide immunosurveillance of the central nervous system (CNS). These cells are thought to derive from the systemic circulation. Through single-cell analyses, confocal imaging, bone marrow chimeras, and parabiosis experiments, we show that meningeal B cells derive locally from the calvaria, which harbors a bone marrow niche for hematopoiesis. B cells reach the meninges from the calvaria through specialized vascular connections. This calvarial–meningeal path of B cell development may provide the CNS with a constant supply of B cells educated by CNS antigens. Conversely, we show that a subset of antigen-experienced B cells that populate the meninges in aging mice are blood-borne. These results identify a private source for meningeal B cells, which may help maintain immune privilege within the CNS.

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U2 - 10.1126/science.abf9277

DO - 10.1126/science.abf9277

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C2 - 34083450

AN - SCOPUS:85109758013

SN - 0036-8075

VL - 373

JO - Science

JF - Science

IS - 6553

M1 - eabf9277

ER -

Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders

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