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The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS

The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS
The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS

Meninges that surround the CNS consist of an outer fibrous sheet of dura mater (pachymeninx) that is also the inner periosteum of the skull. Underlying the dura are the arachnoid and pia mater (leptomeninges) that form the boundaries of the subarachnoid space. In this review we (1) examine the development of leptomeninges and their role as barriers and facilitators in the foetal CNS. There are two separate CSF systems during early foetal life, inner CSF in the ventricles and outer CSF in the subarachnoid space. As the foramina of Magendi and Luschka develop, one continuous CSF system evolves. Due to the lack of arachnoid granulations during foetal life, it is most likely that CSF is eliminated by lymphatic drainage pathways passing through the cribriform plate and nasal submucosa. (2) We then review the fine structure of the adult human and rodent leptomeninges to establish their roles as barriers and facilitators for the movement of fluid, cells and pathogens. Leptomeningeal cells line CSF spaces, including arachnoid granulations and lymphatic drainage pathways, and separate elements of extracellular matrix from the CSF. The leptomeningeal lining facilitates the traffic of inflammatory cells within CSF but also allows attachment of bacteria such as Neisseria meningitidis and of tumour cells as CSF metastases. Single layers of leptomeningeal cells extend into the brain closely associated with the walls of arteries so that there are no perivascular spaces around arteries in the cerebral cortex. Perivascular spaces surrounding arteries in the white matter and basal ganglia relate to their two encompassing layers of leptomeninges. (3) Finally we examine the roles of ligands expressed by leptomeningeal cells for the attachment of inflammatory cells, bacteria and tumour cells as understanding these roles may aid the design of therapeutic strategies to manage developmental, autoimmune, infectious and neoplastic diseases relating to the CSF, the leptomeninges and the associated CNS.

Attachment of Neisseria meningitidis, inflammatory cells and tumour cells to leptomeninges, Barriers and facilitators, CSF, Developing human and rat brain, Leptomeninges, Lymphatic drainage of the CNS, Perivascular compartments and spaces
0001-6322
363-385
Weller, Roy O
4a501831-e38a-4d39-a125-d7141d6c667b
Sharp, Matthew M
ec57c53a-a10a-4b8a-94fe-03eca85ab7c3
Christodoulides, Myron
eba99148-620c-452a-a334-c1a52ba94078
Carare, Roxana O
0478c197-b0c1-4206-acae-54e88c8f21fa
Møllgård, Kjeld
6ad4aac0-21da-4d16-89bd-b9d6380dc32a
Weller, Roy O
4a501831-e38a-4d39-a125-d7141d6c667b
Sharp, Matthew M
ec57c53a-a10a-4b8a-94fe-03eca85ab7c3
Christodoulides, Myron
eba99148-620c-452a-a334-c1a52ba94078
Carare, Roxana O
0478c197-b0c1-4206-acae-54e88c8f21fa
Møllgård, Kjeld
6ad4aac0-21da-4d16-89bd-b9d6380dc32a

Weller, Roy O, Sharp, Matthew M, Christodoulides, Myron, Carare, Roxana O and Møllgård, Kjeld (2018) The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathologica, 135 (3), 363-385. (doi:10.1007/s00401-018-1809-z).

Record type: Review

Abstract

Meninges that surround the CNS consist of an outer fibrous sheet of dura mater (pachymeninx) that is also the inner periosteum of the skull. Underlying the dura are the arachnoid and pia mater (leptomeninges) that form the boundaries of the subarachnoid space. In this review we (1) examine the development of leptomeninges and their role as barriers and facilitators in the foetal CNS. There are two separate CSF systems during early foetal life, inner CSF in the ventricles and outer CSF in the subarachnoid space. As the foramina of Magendi and Luschka develop, one continuous CSF system evolves. Due to the lack of arachnoid granulations during foetal life, it is most likely that CSF is eliminated by lymphatic drainage pathways passing through the cribriform plate and nasal submucosa. (2) We then review the fine structure of the adult human and rodent leptomeninges to establish their roles as barriers and facilitators for the movement of fluid, cells and pathogens. Leptomeningeal cells line CSF spaces, including arachnoid granulations and lymphatic drainage pathways, and separate elements of extracellular matrix from the CSF. The leptomeningeal lining facilitates the traffic of inflammatory cells within CSF but also allows attachment of bacteria such as Neisseria meningitidis and of tumour cells as CSF metastases. Single layers of leptomeningeal cells extend into the brain closely associated with the walls of arteries so that there are no perivascular spaces around arteries in the cerebral cortex. Perivascular spaces surrounding arteries in the white matter and basal ganglia relate to their two encompassing layers of leptomeninges. (3) Finally we examine the roles of ligands expressed by leptomeningeal cells for the attachment of inflammatory cells, bacteria and tumour cells as understanding these roles may aid the design of therapeutic strategies to manage developmental, autoimmune, infectious and neoplastic diseases relating to the CSF, the leptomeninges and the associated CNS.

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More information

e-pub ahead of print date: 24 January 2018
Published date: March 2018
Keywords: Attachment of Neisseria meningitidis, inflammatory cells and tumour cells to leptomeninges, Barriers and facilitators, CSF, Developing human and rat brain, Leptomeninges, Lymphatic drainage of the CNS, Perivascular compartments and spaces

Identifiers

Local EPrints ID: 417605
URI: http://eprints.soton.ac.uk/id/eprint/417605
ISSN: 0001-6322
PURE UUID: e6c6fac5-4715-472e-9a03-4d21c0764218
ORCID for Matthew M Sharp: ORCID iD orcid.org/0000-0002-6623-5078
ORCID for Myron Christodoulides: ORCID iD orcid.org/0000-0002-9663-4731
ORCID for Roxana O Carare: ORCID iD orcid.org/0000-0001-6458-3776

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Date deposited: 07 Feb 2018 17:30
Last modified: 16 Mar 2024 04:03

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Contributors

Author: Roy O Weller
Author: Matthew M Sharp ORCID iD
Author: Roxana O Carare ORCID iD
Author: Kjeld Møllgård

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