Large-scale morphometry of the subarachnoid space of the optic nerve.
Arachnoid
Cerebrospinal fluid
Meningothelial cells
Normal tension glaucoma
Optic nerve
Optic nerve compartment syndrome
Papilledema
Pia mater
Subarachnoid space
Journal
Fluids and barriers of the CNS
ISSN: 2045-8118
Titre abrégé: Fluids Barriers CNS
Pays: England
ID NLM: 101553157
Informations de publication
Date de publication:
21 Mar 2023
21 Mar 2023
Historique:
received:
24
11
2022
accepted:
10
03
2023
entrez:
22
3
2023
pubmed:
23
3
2023
medline:
24
3
2023
Statut:
epublish
Résumé
The meninges, formed by dura, arachnoid and pia mater, cover the central nervous system and provide important barrier functions. Located between arachnoid and pia mater, the cerebrospinal fluid (CSF)-filled subarachnoid space (SAS) features a variety of trabeculae, septae and pillars. Like the arachnoid and the pia mater, these structures are covered with leptomeningeal or meningothelial cells (MECs) that form a barrier between CSF and the parenchyma of the optic nerve (ON). MECs contribute to the CSF proteome through extensive protein secretion. In vitro, they were shown to phagocytose potentially toxic proteins, such as α-synuclein and amyloid beta, as well as apoptotic cell bodies. They therefore may contribute to CSF homeostasis in the SAS as a functional exchange surface. Determining the total area of the SAS covered by these cells that are in direct contact with CSF is thus important for estimating their potential contribution to CSF homeostasis. Using synchrotron radiation-based micro-computed tomography (SRµCT), two 0.75 mm-thick sections of a human optic nerve were acquired at a resolution of 0.325 µm/pixel, producing images of multiple terabytes capturing the geometrical details of the CSF space. Special-purpose supercomputing techniques were employed to obtain a pixel-accurate morphometric description of the trabeculae and estimate internal volume and surface area of the ON SAS. In the bulbar segment, the ON SAS microstructure is shown to amplify the MECs surface area up to 4.85-fold compared to an "empty" ON SAS, while just occupying 35% of the volume. In the intraorbital segment, the microstructure occupies 35% of the volume and amplifies the ON SAS area 3.24-fold. We provided for the first time an estimation of the interface area between CSF and MECs. This area is of importance for estimating a potential contribution of MECs on CSF homeostasis.
Sections du résumé
BACKGROUND
BACKGROUND
The meninges, formed by dura, arachnoid and pia mater, cover the central nervous system and provide important barrier functions. Located between arachnoid and pia mater, the cerebrospinal fluid (CSF)-filled subarachnoid space (SAS) features a variety of trabeculae, septae and pillars. Like the arachnoid and the pia mater, these structures are covered with leptomeningeal or meningothelial cells (MECs) that form a barrier between CSF and the parenchyma of the optic nerve (ON). MECs contribute to the CSF proteome through extensive protein secretion. In vitro, they were shown to phagocytose potentially toxic proteins, such as α-synuclein and amyloid beta, as well as apoptotic cell bodies. They therefore may contribute to CSF homeostasis in the SAS as a functional exchange surface. Determining the total area of the SAS covered by these cells that are in direct contact with CSF is thus important for estimating their potential contribution to CSF homeostasis.
METHODS
METHODS
Using synchrotron radiation-based micro-computed tomography (SRµCT), two 0.75 mm-thick sections of a human optic nerve were acquired at a resolution of 0.325 µm/pixel, producing images of multiple terabytes capturing the geometrical details of the CSF space. Special-purpose supercomputing techniques were employed to obtain a pixel-accurate morphometric description of the trabeculae and estimate internal volume and surface area of the ON SAS.
RESULTS
RESULTS
In the bulbar segment, the ON SAS microstructure is shown to amplify the MECs surface area up to 4.85-fold compared to an "empty" ON SAS, while just occupying 35% of the volume. In the intraorbital segment, the microstructure occupies 35% of the volume and amplifies the ON SAS area 3.24-fold.
CONCLUSIONS
CONCLUSIONS
We provided for the first time an estimation of the interface area between CSF and MECs. This area is of importance for estimating a potential contribution of MECs on CSF homeostasis.
Identifiants
pubmed: 36944985
doi: 10.1186/s12987-023-00423-6
pii: 10.1186/s12987-023-00423-6
pmc: PMC10029327
doi:
Substances chimiques
SNCA protein, human
0
Amyloid beta-Peptides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21Subventions
Organisme : SNF Grant
ID : 320030 196877
Organisme : Kanton Hospital Aarau research Council
ID : 1410.000.111
Informations de copyright
© 2023. The Author(s).
Références
Brain Commun. 2022 Sep 26;4(5):fcac240
pubmed: 36262370
J Glaucoma. 2013 Jun-Jul;22 Suppl 5:S19-20
pubmed: 23733118
Fluids Barriers CNS. 2014 Dec 02;11(1):26
pubmed: 25678956
Clin Anat. 2021 Jan;34(1):40-50
pubmed: 32519396
Neuroophthalmology. 2020 Sep 3;45(1):29-35
pubmed: 33762785
Science. 2023 Jan 6;379(6627):84-88
pubmed: 36603070
Ann Biomed Eng. 2019 Sep;47(9):1982-1992
pubmed: 30673954
Exp Cell Res. 2020 Nov 15;396(2):112322
pubmed: 33068559
J Neuroimmunol. 2012 Mar;244(1-2):45-50
pubmed: 22261544
J Comp Neurol. 2000 Dec 4;428(1):62-78
pubmed: 11058225
Clin Exp Ophthalmol. 2020 Mar;48(2):212-219
pubmed: 31648390
Br J Ophthalmol. 1999 Feb;83(2):231-5
pubmed: 10396204
J Mol Neurosci. 2009 Nov;39(3):366-71
pubmed: 19598000
PLoS One. 2011;6(5):e20142
pubmed: 21611150
Surv Ophthalmol. 2020 Jan - Feb;65(1):48-66
pubmed: 31449832
Ophthalmologica. 2006;220(6):393-6
pubmed: 17095886
Clin Exp Ophthalmol. 2008 May;36(4):308-11
pubmed: 18700915
Br J Ophthalmol. 2003 Jun;87(6):777-81
pubmed: 12770980
Brain. 2006 Apr;129(Pt 4):1027-30
pubmed: 16504971
Anat Res Int. 2015;2015:279814
pubmed: 26090230
Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9070-4
pubmed: 8415655
Surg Radiol Anat. 2022 May;44(5):759-766
pubmed: 35507023
Am J Ophthalmol. 2017 Jul;179:25-31
pubmed: 28455115
J Neurosci. 2002 Jun 15;22(12):4885-96
pubmed: 12077186
Prog Brain Res. 2020;256(1):209-220
pubmed: 32958213
Fluids Barriers CNS. 2022 Aug 30;19(1):67
pubmed: 36042452
J Bone Miner Res. 2010 Jul;25(7):1468-86
pubmed: 20533309
Sci Am. 1979 Jan;240(1):108-17
pubmed: 451521
Cell Mol Life Sci. 2021 Mar;78(6):2429-2457
pubmed: 33427948
Fluids Barriers CNS. 2014 May 01;11:10
pubmed: 24817998
J Histochem Cytochem. 2008 Dec;56(12):1087-92
pubmed: 18765840
J Biomech Eng. 2009 Feb;131(2):021010
pubmed: 19102569
Ophthalmology. 2011 Oct;118(10):2058-69
pubmed: 21849212
Brain. 2007 Feb;130(Pt 2):514-20
pubmed: 17114796