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

Weller, Roy O.; Sharp, Matthew M.; Christodoulides, Myron; Carare, Roxana O.; Møllgård, Kjeld

doi:10.1007/s00401-018-1809-z

Cited by 225Cerebrospinal fluid and hydrocephalusBarrier Structure and Function StudiesBacterial Infections and Vaccines

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

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Weller, Roy O., Sharp, Matthew M., Christodoulides, Myron, Carare, Roxana O., Møllgård, Kjeld·2018·Acta Neuropathologica

DOI 10.1007/s00401-018-1809-z

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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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Single-cell profiling suggested that CAMs share functions with microglia and astrocytes in maintaining CNS homeostasis and regulating barrier functions.
“Single-cell profiling suggested functions shared with microglia and astrocytes in maintaining CNS homeostasis [372] and regulating barrier functions [367,378,379,380].”
From Revisiting the Pathogenesis of X-Linked Adrenoleukodystrophy (2025) · cites this paper as [380]
The cited reference is attached to the sentence’s barrier-functions clause. In “Leptomeninges as barriers and facilitators in the CNS” (page unavailable), the review describes barrier functions of leptomeningeal cells, but it does not attribute those functions to CAMs or establish shared functions through single-cell profiling. The homeostasis clause carries a different citation. (LLM, conf=0.84)
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All major meningitis causing bacteria can adhere strongly to meningeal fibroblasts and arachnoid barrier-like cells, and Group B Streptococcus bacteria cross the blood brain barrier by binding to vimentin on endothelial cells, which is also highly expressed by arachnoid barrier cells.
“All major meningitis causing bacteria can adhere strongly to meningeal fibroblasts and arachnoid barrier-like cells”
From Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease (2021) · cites this paper as Weller et al., 2018

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The biological significance of brain barrier mechanisms: help or hindrance in drug delivery to the central nervous system?
Saunders, N. R., Habgood, M. D., Møllgård, K., & Dziegielewska, K. M. (2016) · F1000Research · doi:10.12688/f1000research.7378.1 · Cited by 143 · cited 1× · see citing works
“An additional sixth interface, (f) the interface between the CSF and the embryonic brain is present only in the foetus [62, 83].”
Self-citation
Meninges: from protective membrane to stem cell niche.
Decimo, I., Fumagalli, G. F., Berton, V., Krampera, M., & Bifari, F. (2012) · Europe PMC (PubMed Central) · Cited by 135 · see citing works
Interaction ofNeisseria meningitidiswith the Components of the Blood‐Brain Barrier Correlates with an Increased Expression of PilC
Pron, B., Taha, M., Rambaud, C., Fournet, J., Pattey, N., Monnet, J., Musílek, M., Béretti, J., & Nassif, X. (1997) · The Journal of Infectious Diseases · doi:10.1086/514124 · Cited by 128 · cited 1× · see citing works
“1 3 inside choroidal epithelial cells or penetrating the tight junctions [76].”
Background
Drug transporters on arachnoid barrier cells contribute to the blood-cerebrospinal fluid barrier
Yasuda, K., Cline, C., Vogel, P., Onciu, M., Fatima, S., Sorrentino, B. P., Thirumaran, R. K., Ekins, S., Urade, Y., Fujimori, K., et al. (2013) · Drug Metabolism and Disposition · doi:10.1124/dmd.112.050344 · Cited by 128 · cited 2× · see citing works
“However in light of recent findings of drug transporters and drug-metabolising enzymes in the arachnoid blood–CSF barrier [108] and taking into account that the arachnoid barrier cell layer constitutes a much larger fraction of the brain surface area during early development, it is clear that the arachnoid blood–CSF b…”
Background
The inner CSF–brain barrier: developmentally controlled access to the brain via intercellular junctions
Whish, S. C., Dzięgielewska, K. M., MÃ¸llgÃ¥rd, K., Noor, N. M., Liddelow, S. A., Habgood, M. D., Richardson, S. J., & Saunders, N. R. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00016 · Cited by 118 · see citing works
Vacuolar transcellular channels as a drainage pathway for cerebrospinal fluid
Tripathi, B. J., & Tripathi, R. C. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010563 · Cited by 116 · cited 1× · see citing works
“CSF then appears to pass by macrovacuolar bulk flow through the venous endothelium into the blood [97].”
Background
Binding of the Complement Inhibitor C4bp to Serogroup B Neisseria meningitidis
Jarva, H., Ram, S., Vogel, U. F., Blom, A. M., & Meri, S. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.10.6299 · Cited by 110 · see citing works
Outer brain barriers in rat and human development
Brøchner, C. B., Holst, C. B., & Møllgård, K. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00075 · Cited by 104 · cited 9× · see citing works
“More recently it has been demonstrated that the early rat brain (E10–E14) shows no signs of claudin-11 immunoreactivity, but that at E15, weak staining is present in the loosely packed arachnoid barrier cells at the base of the brain and extending into the future tentorium cerebelli [14].”
Influential
Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin
Scarselli, M., Serruto, D., Montanari, P., Capecchi, B., Adu‐Bobie, J., Veggi, D., Rappuoli, R., Pizza, M., & Aricò, B. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05261.x · Cited by 101 · cited 2× · see citing works
“Laminin receptor 1 (LamR; also known as RPSA)–galectin 3 (GAL3) complex) Binds PorA and PilQ [73] and NhhA (Neisseria hia/hsf homologue; Msf, meningococcal surface fibril) [84]”
Background
Development of Arachnoid Villi and Granulations in Man
Gomez, D. G., DiBenedetto, A. T., Pavese, A. M., Firpo, A., Hershan, D. B., & Potts, D. G. (1981) · Cells Tissues Organs · doi:10.1159/000145473 · Cited by 99 · cited 1× · see citing works
“However, during foetal life, CSF is not likely to drain through arachnoid granulations as they are not present prior to 39 weeks gestation [36].”
Background
Classification and Pathogenesis of Meningococcal Infections
Brandtzaeg, P., & van Deuren, M. (2012) · Methods in Molecular Biology · doi:10.1007/978-1-61779-346-2_2 · Cited by 99 · cited 1× · see citing works
“LOS is the major component of meningococci that induces leptomeningitis [12], via binding to CD14-Toll-like receptor Fig.”
Background
In vitro resistance mechanisms of N eisseria meningitidis against neutrophil extracellular traps
Lappann, M., Danhof, S., Guenther, F., Olivares‐Florez, S., Mordhorst, I. L., & Vogel, U. F. (2013) · Molecular Microbiology · doi:10.1111/mmi.12288 · Cited by 93 · cited 1× · see citing works
“Phosphoethanolamine modification of LOS can increase adherence to human cells and also protects meningococci from neutrophil extracellular trap (NET)-bound cathepsin G [58].”
Background
A light and electron microscopic and immunohistochemical study of human arachnoid villi
Kida, S., Yamashima, T., Kubota, T., Ito, H., & Yamamoto, S. (1988) · Journal of neurosurgery · doi:10.3171/jns.1988.69.3.0429 · Cited by 93 · cited 2× · see citing works
“Leptomeningeal cells also surround collagen bundles in the stroma of the choroid plexus [3] and in the cores of arachnoid granulations [56, 98].”
Background
White Matter Perivascular Spaces on Magnetic Resonance Imaging
Charidimou, A., Hong, Y. T., Jäger, H. R., Fox, Z. V., Aigbirhio, F. I., Fryer, T. D., Menon, D. K., Warburton, E. A., Werring, D. J., & Baron, J. (2015) · Stroke · doi:10.1161/strokeaha.115.009090 · Cited by 93 · cited 3× · see citing works
“Dilated perivascular spaces around arteries in the human cerebral white matter can be detected by MRI and by histology and have been associated with CAA and consequent failure of drainage of interstitial fluid [19, 79, 104].”
Interactions of <i>Neisseria meningitidis</i> with cells of the human meninges
Hardy, S. J., Christodoulides, M., Weller, R. O., & Heckels, J. E. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01923.x · Cited by 78 · cited 5× · see citing works
“7c) [5, 9, 34, 39], although the nature of the bacterial ligands and meningeal cell receptors has not been explored extensively.”
BackgroundInfluential
Neisseria meningitidis factor H-binding protein fHbp: a key virulence factor and vaccine antigen
Seib, K. L., Scarselli, M., Comanducci, M., Toneatto, D., & Masignani, V. (2015) · Expert Review of Vaccines · doi:10.1586/14760584.2015.1016915 · Cited by 71 · cited 1× · see citing works
“Meningococci also avoid complement killing through expression of Porin A that binds the complement inhibitor C4 bp protein [47], and of fHbp (factor H binding protein), NspA (Neisserial surface protein A) and PorinB3, which all bind human factor H [35, 88].”
Background
Dilated Perivascular Spaces in the Basal Ganglia Are a Biomarker of Small-Vessel Disease in a Very Elderly Population with Dementia
Hansen, T., Cain, J. R., Thomas, O., & Jackson, A. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4237 · Cited by 68 · cited 2× · see citing works
“Dilatation of perivascular spaces in the basal ganglia is related to age and small vessel disease and can be detected by MRI [38] and by histology [75].”
Background
Immune responses at brain barriers and implications for brain development and neurological function in later life
Stolp, H. B., Liddelow, S. A., Sá-Pereira, I., Dzięgielewska, K. M., & Saunders, N. R. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00061 · Cited by 67 · cited 1× · see citing works
“The outer barriers of the brain function as morphogenetic signalling centres [27, 89], dynamic transport systems [108], a stem cell niche [27] and regulators of immune cell entry into the CNS [93] as summarised by Brøchner et al.”
Background
Topographical and Cytological Evolution of the Glial Phase During Prenatal Development of the Human Brain: Histochemical and Electron Microscopic Study
Kadhim, H. J., Gadisseux, J., & Evrard, P. (1988) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198803000-00009 · Cited by 66 · cited 1× · see citing works
“…by O’Rahilly and Müller [71] and from mammals to human according to the work of Clancy et al. [22] E14 etc. embryonic day Schmechel and Rakic [86]; Voigt [101] 25th–28th Transition from subpial end feet layer to glia limitans Human Kadhim et al. [50] choroid plexus as this has not yet developed.”
Brain barriers and functional interfaces with sequential appearance of ABC efflux transporters during human development
Møllgård, K., Dzięgielewska, K. M., Holst, C. B., Habgood, M. D., & Saunders, N. R. (2017) · Scientific Reports · doi:10.1038/s41598-017-11596-0 · Cited by 66 · cited 5× · see citing works
“1 3 a very dense leptomeningeal vascular plexus, the vascular distribution system, in the SAS [62].”
BackgroundInfluential
Dual Pili Post-translational Modifications Synergize to Mediate Meningococcal Adherence to Platelet Activating Factor Receptor on Human Airway Cells
Jen, F. E. ‐., Warren, M. J., Schulz, B. L., Power, P. M., Swords, W. E., Weiser, J. N., Apicella, M. A., Edwards, J. L., & Jennings, M. P. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003377 · Cited by 59 · cited 1× · see citing works
“Other Tfp-associated proteins that may be involved in cell interactions include the tip-associated PilC1/C2 and a phosphorylcholine modification of Tfp that interacts with Platelet Activating Factor receptor [48].”
Background
Comparison of cerebrospinal fluid transport in fetal and adult sheep
Mollanji, R., Papaiconomou, C., Boulton, M., Midha, R., & Johnston, M. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.4.r1215 · Cited by 57 · cited 2× · see citing works
“They appear in greater number as children age and are clearly visible by 2 years and then increase further in size and number with increasing age [61].”
Background
Barrier functions of the leptomeninges: a study of normal meninges and meningiomas in tissue culture
FEURER, D. J., & Weller, R. O. (1991) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1991.tb00739.x · Cited by 56 · cited 1× · see citing works
“Meningioma cells share many structural features with normal leptomeningeal cells [32]; they are characterised by the presence of desmosomes, and, except in certain sites in the leptomeninges, tight junctions are absent.”
Background
The Adhesin Complex Protein (ACP) of Neisseria meningitidis Is a New Adhesin with Vaccine Potential
Hung, M.-C., Heckels, J. E., & Christodoulides, M. (2013) · mBio · doi:10.1128/mbio.00041-13 · Cited by 56 · cited 1× · see citing works
“Only one other protein, the Adhesin Complex Protein, has been reported to bind directly to cell surfaces and mediate adherence of capsulated meningococci to meningeal cells [44].”
Integrins mediate adhesion of medulloblastoma cells to tenascin and activate pathways associated with survival and proliferation
Fiorilli, P. N., Partridge, D. D., Staniszewska, I., Wang, J. Y., Grabacka, M., So, K., Marcinkiewicz, C., Krzysztof Reiss, F., Khalili, K., & Croul, S. E. (2008) · Laboratory Investigation · doi:10.1038/labinvest.2008.89 · Cited by 55 · cited 2× · see citing works
“In vitro and in vivo data suggest that expression of α9 and β1 integrins, in combination with tenascin in the extracellular matrix, mediate the adhesion of medulloblastoma cells to the leptomeninges [33].”
Background
CALCIFICATION IN THE HUMAN CHOROID PLEXUS, MENINGIOMAS AND PINEAL GLAND
Alcolado, J. C., Moore, I. E., & Weller, R. O. (1986) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1986.tb00137.x · Cited by 55 · see citing works
The development of the human cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle.
Brocklehurst, G. (1969) · PubMed · Cited by 54 · see citing works
Neisseria meningitidis Adhesin NadA Targets β1 Integrins
Nägele, V., Heesemann, J., Schielke, S., Soto, L. F. J., Kurzai, O., & Ackermann, N. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.188326 · Cited by 51 · see citing works
Activation of human meningeal cells is modulated by lipopolysaccharide (LPS) and non-LPS components of Neisseria meningitidis and is independent of Toll-like receptor (TLR)4 and TLR2 signalling
Humphries, H. E., Triantafilou, M., Makepeace, B. L., Heckels, J. E., Triantafilou, K., & Christodoulides, M. (2005) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00471.x · Cited by 45 · cited 1× · see citing works
“By contrast, cytokine release by meningeal cells can occur independently of LOS-CD14/TLR4/MD2 interactions or the involvement of other host accessory proteins such as HSP70, HSP90α, CXCR4 or GDF5 [43].”
Background
Morphogenesis of rat cranial meninges
Angelov, D. N., & Vasilev, V. (1989) · Cell and Tissue Research · doi:10.1007/bf00221652 · Cited by 43 · see citing works
Different meningitis-causing bacteria induce distinct inflammatory responses on interaction with cells of the human meninges
Fowler, M. I., Weller, R. O., Heckels, J. E., & Christodoulides, M. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00382.x · Cited by 42 · cited 1× · see citing works
“7c) [5, 9, 34, 39], although the nature of the bacterial ligands and meningeal cell receptors has not been explored extensively.”
Background
Neisserial Heparin Binding Antigen (NHBA) Contributes to the Adhesion of Neisseria meningitidis to Human Epithelial Cells
Vacca, I., Tordello, E. D., Gasperini, G., Pezzicoli, A., Fede, M. D., Paccani, S. R., Marchi, S., Mubaiwa, T. D., Hartley‐Tassell, L. E., Jennings, M. P., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162878 · Cited by 41 · cited 1× · see citing works
“Heparan sulphate proteoglycans (HSPG) Binds NhhA [84], NHBA (Neisseria Heparin Binding Antigen) [99], Opa and Opc proteins [42]”
Background
SR-A, MARCO and TLRs Differentially Recognise Selected Surface Proteins from Neisseria meningitidis: an Example of Fine Specificity in Microbial Ligand Recognition by Innate Immune Receptors
Plüddemann, A., Mukhopadhyay, S., Sankala, M., Savino, S., Pizza, M., Rappuoli, R., Tryggvason, K., & Gordon, S. (2008) · Journal of Innate Immunity · doi:10.1159/000155227 · Cited by 40 · cited 1× · see citing works
“Binds to various meningococcal proteins (NMB0278, DsbA; NMB0346, NMB0667, NMB1513, hypothetical; NMB1220, Stomatin/Mec-2 family protein; NMB1567, Macrophage infectivity potentiator) [74]”
Background
Neisseria gonorrhoeaebreaches the apical junction of polarized epithelial cells for transmigration by activating EGFR
Edwards, V. L., Wang, L., Dawson, V., Stein, D. C., & Song, W. (2012) · Cellular Microbiology · doi:10.1111/cmi.12099 · Cited by 39 · cited 1× · see citing works
“gonorrhoeae across polarised epithelial cells [29].”
Binding of Complement Factor H to PorB3 and NspA Enhances Resistance of Neisseria meningitidis to Anti-Factor H Binding Protein Bactericidal Activity
Giuntini, S., Pajón, R., Ram, S., & Granoff, D. M. (2015) · Infection and Immunity · doi:10.1128/iai.02984-14 · Cited by 38 · cited 1× · see citing works
“Meningococci also avoid complement killing through expression of Porin A that binds the complement inhibitor C4 bp protein [47], and of fHbp (factor H binding protein), NspA (Neisserial surface protein A) and PorinB3, which all bind human factor H [35, 88].”
Background
The mouse cortical meninges are the site of immune responses to many different pathogens, and are accessible to intravital imaging
Coles, J. A., Stewart-Hutchinson, P. J., Myburgh, E., & Brewer, J. M. (2017) · Methods · doi:10.1016/j.ymeth.2017.03.020 · Cited by 38 · cited 2× · see citing works
“The SAS is shallower and much less extensive in rodents than in humans [23, 54].”
Role of Epidermal Growth Factor Receptor Signaling in the Interaction of Neisseria meningitidis with Endothelial Cells
Slanina, H., Mündlein, S., Hebling, S., & Schubert‐Unkmeir, A. (2013) · Infection and Immunity · doi:10.1128/iai.01346-13 · Cited by 37 · cited 1× · see citing works
“In endothelial cells, EGFR, Erb2 and Erb4 are activated in response to meningococcal infection and involved in the internalisation of bacteria [90].”
T-cell stimulating protein A (TspA) of Neisseria meningitidis is required for optimal adhesion to human cells
Oldfield, N. J., Bland, S. J., Taraktsoglou, M., Ramos, F. J. D., Robinson, K., Wooldridge, K. G., & Ala’Aldeen, D. A. A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00803.x · Cited by 34 · cited 1× · see citing works
“Expression of TspA (T cell-stimulating protein A) has been reported to contribute to the adhesion of meningococci to meningioma cells [72].”
Background
The Polysialic Acid Units of the Neural Cell Adhesion Molecule N-CAM Form Filament Bundle Networks
Toikka, J., Aalto, J., Häyrinen, J., Pelliniemi, L. J., & Finne, J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.28557 · Cited by 33 · cited 2× · see citing works
“For example, the α(2-8) N -acetyl-neuraminic acid linked homopolymer of serogroup B CPS is structurally identical to a modification of mammalian neural cell adhesion molecule (N-CAM) [95].”
Group B Streptococcus Interactions with Human Meningeal Cells and Astrocytes In Vitro
Alkuwaity, K. K., Taylor, A., Heckels, J. E., Doran, K. S., & Christodoulides, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042660 · Cited by 33 · cited 1× · see citing works
“7c) [5, 9, 34, 39], although the nature of the bacterial ligands and meningeal cell receptors has not been explored extensively.”
Background
Nuclear trafficking, histone cleavage and induction of apoptosis by the meningococcal App and MspA autotransporters
Khairalla, A. S., Omer, S. A., Mahdavi, J., Aslam, A., Dufailu, O. A., Self, T. J., Jonsson, A., Geörg, M., Sjölinder, H., Royer, P., et al. (2015) · Cellular Microbiology · doi:10.1111/cmi.12417 · Cited by 32 · cited 1× · see citing works
“Histones Intracellular proteins that can associate with App (Adhesion and penetration autotransporter protein) and MspA/Aus1 (meningococcal serine protease A/autotransporter serine protease 1) [53]”
Background
Medulloblastoma: experimental models and reality
Neumann, J. E., Swartling, F. J., & Schüller, U. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1753-3 · Cited by 31 · cited 1× · see citing works
“It is predicted that molecular characterisation will lead to more targeted therapies for leptomeningeal metastases of medulloblastoma [67].”
Background
Ontogenetic development of diffusional restriction to protein at the pial surface of the rat brain: an electron microscopical study
Balslev, Y., Saunders, N. R., & Møllgård, K. (1997) · Journal of Neurocytology · doi:10.1023/a:1018527928760 · Cited by 30 · cited 1× · see citing works
“Complex barriers at the surface of the brain, particularly during development, are poorly defined [10], but by mid-gestation subarachnoid interfaces are almost fully developed.”
Background
Normal pio-dural arterial connections
Bhogal, P., Makalanda, L., Brouwer, P. A., Gontu, V. K., Rodesch, G., Mercier, P., & Söderman, M. (2015) · Interventional Neuroradiology · doi:10.1177/1591019915609137 · Cited by 29 · cited 1× · see citing works
“The only regions of adherence are where cortical veins join venous sinuses in the dura and where a small number of vascular bundles containing arteries and veins cross the subarachnoid and subdural spaces from the surface of the brain to the dura [11].”
Background
Cerebrospinal fluid abnormalities in meningeosis neoplastica: a retrospective 12-year analysis
Djukic, M., Trimmel, R., Nagel, I., Spreer, A., Lange, P., Stadelmann, C., & Nau, R. (2017) · Fluids and Barriers of the CNS · doi:10.1186/s12987-017-0057-2 · Cited by 26 · cited 1× · see citing works
“Three major categories of tumours cause Meningeosis neoplastica : namely carcinomas, lymphomas and primary tumours of the CNS, particularly medulloblastomas [28, 77].”
Pathogenic Neisseria Hitchhike on the Uropod of Human Neutrophils
Söderholm, N., Vielfort, K., Hultenby, K. R., & Aro, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024353 · Cited by 24 · cited 1× · see citing works
“Interestingly, Tfp-mediated adherence of Neisseriae to the uropod of polarised PMNL suggests a hypothesis that the bacteria can hitchhike on PMNL both to hide from their phagocytic activity and to enable dissemination through cell barriers [92].”
Background
Interactions of Streptococcus suis serotype 2 with human meningeal cells and astrocytes
Auger, J.-P., Christodoulides, M., Segura, M., Xu, J., & Gottschalk, M. G. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1581-2 · Cited by 23 · cited 1× · see citing works
“7c) [5, 9, 34, 39], although the nature of the bacterial ligands and meningeal cell receptors has not been explored extensively.”
Background
Compromise of Brain Tissue Caused by Cortical Venous Reflux of Intracranial Dural Arteriovenous Fistulas
Sato, K., Shimizu, H., Fujimura, M., Inoue, T., Matsumoto, Y., & Tominaga, T. (2011) · Stroke · doi:10.1161/strokeaha.110.597203 · Cited by 23 · cited 1× · see citing works
“Arteriovenous malformations in the dura have a significant effect on the vasculature of the brain through these connections and may be associated with cerebral venous thrombosis or intracranial haemorrhage [82].”
Background
BASEMENT MEMBRANE SURFACES AND PERIVASCULAR COMPARTMENTS IN NORMAL HUMAN BRAIN AND GLIAL TUMOURS. A SCANNING ELECTRON MICROSCOPE STUDY
SAPSFORD, I., BUONTEMPO, J. M., & Weller, R. O. (1983) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1983.tb00106.x · Cited by 19 · cited 1× · see citing works
“Much of the confusion has arisen first from artefact in histological and electron microscope preparations due to swelling of perivascular astrocytes thus forming an artefactual space around cortical arteries [81].”
Background
Leukodiapedesis and leukocyte migration in the leptomeninges and in the subarachnoid space
Krahn, V. (1981) · Journal of Neurology · doi:10.1007/bf00313317 · Cited by 13 · cited 1× · see citing works
“The leptomeningeal cells of the pia offer little resistance to the passage of inflammatory cells [45, 57] (Fig.”
Background
Neisseriae internalization by epithelial cells is enhanced by TLR2 stimulation
Toussi, D. N., Wetzler, L. M., Liu, X., & Massari, P. (2016) · Microbes and Infection · doi:10.1016/j.micinf.2016.06.001 · Cited by 13 · cited 1× · see citing works
“TLR2 Toll-like receptor 2: pathogen recognition receptor (PRR) for Grampositive lipoteichoic acid and other lipoproteins and meningococcal PorB [96]”
Background
Morphological Basis for Fluid Transport Through and Around Ependymal, Arachnoidal, and Glial Cells
Kida, S., & Weller, R. O. (1993) · Principles of pediatric neurosurgery · doi:10.1007/978-1-4615-7281-7_3 · Cited by 11 · see citing works
The structure of the perivascular compartment in the old canine brain: a case study
Criswell, T. P., Sharp, M. M., Dobson, H., Finucane, C. M., Weller, R. O., Verma, A., & Carare, R. O. (2017) · Clinical Science · doi:10.1042/cs20171278 · Cited by 11 · cited 4× · see citing works
“There is one layer of leptomeningeal cells around arteries in the cerebral cortex but there tends to be two layers of leptomeninges surrounding arteries in the white matter and basal ganglia [26, 75, 109].”
BackgroundMethodInfluential
Comment on the topology of mammalian blood–cerebrospinal fluid barrier
Wolburg, H., & Mack, A. F. (2014) · Neurology Psychiatry and Brain Research · doi:10.1016/j.npbr.2014.10.004 · Cited by 8 · cited 1× · see citing works
“These findings are important in discussions about the continuity of the SAS and pial tissues with the stroma of the choroid plexus [107] and the so-called functional leak at the tela choroidea between ependyma and choroid plexus epithelium [13].”
Background
Editorial: Clearance Pathways for Amyloid-β. Significance for Alzheimer's Disease and Its Therapy
Carare, R. O. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00339 · Cited by 7 · cited 1× · see citing works
“…out of the brain along basement membranes in the walls of capillaries and along basement membranes surrounding smooth muscle cells in the tunica media of cerebral arterioles and arteries [7, 16–18] [the Intramural Peri-Arterial Drainage (IPAD) pathway]; IPAD is impaired with age in mice [40].”
Meningitis: cellular and molecular basis
Christodoulides, M. (2013) · CABI eBooks · doi:10.1079/9781780641621.0000 · Cited by 5 · see citing works
A history of bacterial meningitis from antiquity to modern times.
Christodoulides, M. (2013) · CABI eBooks · doi:10.1079/9781780641621.0001 · Cited by 4 · cited 1× · see citing works
“Leptomeningitis is an acute, compartmentalised intracranial inflammatory response centred on the leptomeninges and can be caused by a plethora of different bacteria that can gain access to the SAS [20].”
Inflammation in the subarachnoid space.
Christodoulides, M. (2013) · CABI eBooks · doi:10.1079/9781780641621.0242 · Cited by 2 · cited 2× · see citing works
“Leptomeningitis is an ‘inflammatory soup’ of host response molecules [21] to invading menin-gococci and infection is characterised by the rapid infiltration of PMNLs. Neutrophils with intracellular bacteria have been observed in the CSF of patients, suggesting that this organism can survive and…”

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Weller RO (1999) Reaction of intrathecal and epidural spaces to infection and inflammation. In: Yaksh TL (ed) Spinal drug delivery. Elsevier, Amsterdam, pp 297-315 103.
Whish S, Dziegielewska KM, Møllgård K, Noor NM, Liddelow SA, Habgood MD, Richardson SJ, Saunders NR (2015) The inner CSF-brain barrier: developmentally controlled access to the brain. Front Neurosci 9:16 106.

Sorted by citations

Revisiting the neurovascular unit
Schaeffer, S. M., & Iadecola, C. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00904-7 · Cited by 654 · see citing works
Fluid transport in the brain
Rasmussen, M. K., Mestre, H., & Nedergaard, M. (2021) · Physiological Reviews · doi:10.1152/physrev.00031.2020 · Cited by 622 · see citing works
Cerebrospinal fluid outflow: a review of the historical and contemporary evidence for arachnoid villi, perineural routes, and dural lymphatics
Proulx, S. T. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03706-5 · Cited by 400 · see citing works
“Anatomical support for this pathway is found from developmental studies in rats that have indicated that the arachnoid barrier layer of the meninges is not present above the cribriform plate [146] and thus would not accompany the olfactory nerves outside of the skull.”
Background
Gastrointestinal and brain barriers: unlocking gates of communication across the microbiota–gut–brain axis
Aburto, M. R., & Cryan, J. F. (2024) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00890-0 · Cited by 391 · see citing works
Cerebrovascular Smooth Muscle Cells as the Drivers of Intramural Periarterial Drainage of the Brain
Aldea, R., Weller, R. O., Wilcock, D. M., Carare, R. O., & Richardson, G. W. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00001 · Cited by 335 · see citing works
Convective influx/glymphatic system: tracers injected into the CSF enter and leave the brain along separate periarterial basement membrane pathways
Albargothy, N. J., Johnston, D. A., MacGregor-Sharp, M., Weller, R. O., Verma, A., Hawkes, C. A., & Carare, R. O. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1862-7 · Cited by 311 · see citing works
“Electron microscope studies have shown that there are no perivascular spaces around arteries in the cerebral cortex [23, 37, 40] although dilated perivascular spaces do develop in other parts of the brain such as cerebral white matter and the basal ganglia [32].”
BackgroundSelf-citation
Cytokines in CAR T Cell–Associated Neurotoxicity
Gust, J., Ponce, R. A., Liles, W. C., Garden, G. A., & Turtle, C. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.577027 · Cited by 268 · see citing works
“An explanation of this finding may be an opening of the meningeal blood-CSF barrier, with meningeal vessels becoming more permeable (55).”
Background
Single-cell transcriptomic analyses of the developing meninges reveal meningeal fibroblast diversity and function.
DeSisto, J., O’Rourke, R., Jones, H. E., Pawlikowski, B., Malek, A. D., Bonney, S., Guimiot, F., Jones, K. L., & Siegenthaler, J. A. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.06.009 · Cited by 241 · see citing works
The glymphatic hypothesis: the theory and the evidence
Hladky, S. B., & Barrand, M. A. (2022) · Fluids and Barriers of the CNS · doi:10.1186/s12987-021-00282-z · Cited by 271 · see citing works
“• Weller, Carare, Morris, Abernathy and coworkers have put forward an opposing view that there are no such spaces, neither intramural nor extramural, and that within the parenchyma both periarterial influx and efflux occur via basement membranes [8, 10, 100, 129, 130, 145].”
Background
A Historical Review of Brain Drug Delivery
Pardridge, W. M. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14061283 · Cited by 219 · see citing works
Neuroinflammation-induced lymphangiogenesis near the cribriform plate contributes to drainage of CNS-derived antigens and immune cells
Hsu, M., Rayasam, A., Kijak, J. A., Choi, Y. H., Harding, J. S., Marcus, S. A., Karpus, W. J., Sándor, M., & Fábry, Z. (2019) · Nature Communications · doi:10.1038/s41467-018-08163-0 · Cited by 208 · see citing works
Elimination of substances from the brain parenchyma: efflux via perivascular pathways and via the blood–brain barrier
Hladky, S. B., & Barrand, M. A. (2018) · Fluids and Barriers of the CNS · doi:10.1186/s12987-018-0113-6 · Cited by 206 · see citing works
Emerging roles for CNS fibroblasts in health, injury and disease
Dorrier, C., Jones, H. E., Pintarić, L., Siegenthaler, J. A., & Daneman, R. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00525-w · Cited by 194 · see citing works
Perivascular spaces and brain waste clearance systems: relevance for neurodegenerative and cerebrovascular pathology
Gouveia-Freitas, K., & de Bastos-Leite, A. J. (2021) · Neuroradiology · doi:10.1007/s00234-021-02718-7 · Cited by 161 · see citing works
“Finally, a major criticism of the “glymphatic” system includes the reported absence of PVS around cortical arteries [15, 16].”
Background
Structure and Junctional Complexes of Endothelial, Epithelial and Glial Brain Barriers
Dias, M. C., Mapunda, J. A., Vladymyrov, M., & Engelhardt, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215372 · Cited by 152 · see citing works
“Recent studies have shown positive immunostaining for claudin-11 in arachnoid barrier cells in the brains of both humans and rodents [8,189], suggesting that the arachnoid BCSFB establishes TJs similar to those at the ChP BCSFB.”
BackgroundInfluential
Anatomical basis and physiological role of cerebrospinal fluid transport through the murine cribriform plate
Norwood, J. N., Zhang, Q., Card, D., Craine, A., Ryan, T. M., & Drew, P. J. (2019) · eLife · doi:10.7554/elife.44278 · Cited by 144 · see citing works
Living on the Edge of the CNS: Meninges Cell Diversity in Health and Disease
Derk, J., Jones, H. E., Como, C., Pawlikowski, B., & Siegenthaler, J. A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.703944 · Cited by 120 · see citing works
Current understanding of meningeal and cerebral vascular function underlying migraine headache
Levy, D., Labastida‐Ramírez, A., & MaassenVanDenBrink, A. (2018) · Cephalalgia · doi:10.1177/0333102418771350 · Cited by 129 · see citing works
“is maintained for a short distance and separates between the vessel wall and the glia limitans (9,10).”
Background
ABC Transporters at the Blood–Brain Interfaces, Their Study Models, and Drug Delivery Implications in Gliomas
Gomez‐Zepeda, D., Taghi, M., Scherrmann, J., Declèves, X., & Menet, M. (2019) · Pharmaceutics · doi:10.3390/pharmaceutics12010020 · Cited by 124 · see citing works
“The meninges are composed of three layers; starting with the outermost pachymeninx composed of a fibrous sheet of dura mater; then, the two innermost layers form the leptomeninges, including the arachnoid mater followed by the pia mater lining the brain, both enclosing CSF in the subarachnoid space [32] (Figure 1D).”
Background
Post-capillary venules are the key locus for transcytosis-mediated brain delivery of therapeutic nanoparticles
Kucharz, K., Kristensen, K., Johnsen, K. B., Lund, M. A., Lønstrup, M., Moos, T., Andresen, T. L., & Lauritzen, M. J. (2021) · Nature Communications · doi:10.1038/s41467-021-24323-1 · Cited by 123 · see citing works
Ischemia–reperfusion injury in stroke: impact of the brain barriers and brain immune privilege on neutrophil function
Enzmann, G., Kargaran, S., & Engelhardt, B. (2018) · Therapeutic Advances in Neurological Disorders · doi:10.1177/1756286418794184 · Cited by 119 · see citing works
Open pathways for cerebrospinal fluid outflow at the cribriform plate along the olfactory nerves
Spera, I., Cousin, N., Ries, M., Kedracka, A., Castillo, A., Aleandri, S., Vladymyrov, M., Mapunda, J. A., Engelhardt, B., Luciani, P., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104558 · Cited by 117 · see citing works
Meningeal macrophages protect against viral neuroinfection
Rebejac, J., Eme‐Scolan, E., Arnaud, L., Kharbouche, S., Teleman, M., Spinelli, L., Gallo, E., Roussel‐Queval, A., Zarubica, A., Sansoni, A., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.10.005 · Cited by 115 · see citing works
Meningeal Lymphatics: From Anatomy to Central Nervous System Immune Surveillance
Papadopoulos, Z., Herz, J., & Kipnis, J. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1900838 · Cited by 108 · see citing works
Arachnoid granulations are lymphatic conduits that communicate with bone marrow and dura-arachnoid stroma
Shah, T., Leurgans, S. E., Mehta, R. I., Yang, J., Galloway, C. A., Bentley, K. L. D. M., Schneider, J. A., & Mehta, R. I. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20220618 · Cited by 108 · see citing works
“Type I consisted of intrasinus AG that have been previously described (Kida et al., 1988; Weller et al., 2018).”
Method
Physiology and Clinical Relevance of Enlarged Perivascular Spaces in the Aging Brain
Bown, C. W., Carare, R. O., Schrag, M., & Jefferson, A. L. (2021) · Neurology · doi:10.1212/wnl.0000000000013077 · Cited by 106 · see citing works
Cerebral Vessels: An Overview of Anatomy, Physiology, and Role in the Drainage of Fluids and Solutes
Agarwal, N., & Carare, R. O. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2020.611485 · Cited by 104 · see citing works
“However, the contemporary presence of the meninx primitiva and the lack of arachnoid granulations in the fetus suggests that there must be alternative routes for its absorption (37, 39).”
Background
Ultraflexible Neural Electrodes for Long-Lasting Intracortical Recording
He, F., Lycke, R., Ganji, M., Xie, C., & Luan, L. (2020) · iScience · doi:10.1016/j.isci.2020.101387 · Cited by 98 · see citing works
Meningeal inflammation as a driver of cortical grey matter pathology and clinical progression in multiple sclerosis
Magliozzi, R., Howell, O., Calabrese, M., & Reynolds, R. (2023) · Nature Reviews Neurology · doi:10.1038/s41582-023-00838-7 · Cited by 82 · see citing works
Trigeminal ganglion neurons are directly activated by influx of CSF solutes in a migraine model
Rasmussen, M. K., Møllgård, K., Bork, P. A. R., Weikop, P., Esmail, T., Drici, L., Albrechtsen, N. J. W., Carlsen, J. F., Huynh, N. P. T., Ghitani, N., et al. (2024) · Science · doi:10.1126/science.adl0544 · Cited by 95 · see citing works
Redefining CNS immune privilege
Smyth, L. C. D., & Kipnis, J. (2025) · Nature Reviews Immunology · doi:10.1038/s41577-025-01175-0 · Cited by 80 · see citing works
“The arachnoid barrier has gaps where bridging veins pass across it, termed arachnoid cuff exit (ACE) points, as well as a gap where cranial nerves exit beneath the olfactory bulbs 30–33 .”
Dispersion in porous media in oscillatory flow between flat plates: applications to intrathecal, periarterial and paraarterial solute transport in the central nervous system
Sharp, M. K., Carare, R. O., & Martin, B. A. (2019) · Fluids and Barriers of the CNS · doi:10.1186/s12987-019-0132-y · Cited by 85 · see citing works
Neuroinflammation creates an immune regulatory niche at the meningeal lymphatic vasculature near the cribriform plate
Hsu, M., Laaker, C. J., Madrid, A., Herbáth, M., Choi, Y. H., Sándor, M., & Fábry, Z. (2022) · Nature Immunology · doi:10.1038/s41590-022-01158-6 · Cited by 91 · see citing works
Advances and controversies in meningeal biology
Betsholtz, C., Engelhardt, B., Koh, G. Y., McDonald, D. M., Proulx, S. T., & Siegenthaler, J. A. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01701-8 · Cited by 85 · see citing works
“The pia is a monolayer of cells (Box 1c) but is thicker in humans than in mice 51 .”
Influential
Functional analysis of the human perivascular subarachnoid space
Eide, P. K., & Ringstad, G. A. (2024) · Nature Communications · doi:10.1038/s41467-024-46329-1 · Cited by 82 · see citing works
Hierarchical imaging and computational analysis of three-dimensional vascular network architecture in the entire postnatal and adult mouse brain
Wälchli, T., Bisschop, J., Miettinen, A., Ulmann‐Schuler, A., Hintermüller, C., Meyer, E. P., Krucker, T., Waelchli, R., Monnier, P. P., Carmeliet, P., et al. (2021) · Nature Protocols · doi:10.1038/s41596-021-00587-1 · Cited by 77 · see citing works
Central nervous system zoning: How brain barriers establish subdivisions for CNS immune privilege and immune surveillance
Proulx, S. T., & Engelhardt, B. (2022) · Journal of Internal Medicine · doi:10.1111/joim.13469 · Cited by 83 · see citing works
The role of T cells in the pathogenesis of Parkinson’s disease
Chen, Z., Chen, S., & Liu, J. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.08.002 · Cited by 78 · see citing works
Border-associated macrophages as gatekeepers of brain homeostasis and immunity
Vara‐Pérez, M., & Movahedi, K. (2025) · Immunity · doi:10.1016/j.immuni.2025.04.005 · Cited by 81 · see citing works
Pulsatile flow drivers in brain parenchyma and perivascular spaces: a resistance network model study
Rey, J. A., & Sarntinoranont, M. (2018) · Fluids and Barriers of the CNS · doi:10.1186/s12987-018-0105-6 · Cited by 74 · see citing works
Current views on meningeal lymphatics and immunity in aging and Alzheimer’s disease
Rego, S., Sánchez, G., & Mesquita, S. D. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00645-0 · Cited by 74 · see citing works
“…encompassing the brain and the spinal cord, and are composed of three distinct layers: the innermost layer, known as the pia mater, the arach-noid (mostly acellular and linked to the pia via trabeculae), and the outermost layer, the dura mater, which is in direct contact with the skull [6–8].”
Background
VE-cadherin in arachnoid and pia mater cells serves as a suitable landmark for in vivo imaging of CNS immune surveillance and inflammation
Mapunda, J. A., Pareja, J. R., Vladymyrov, M., Bouillet, E., Hélie, P., Pleskač, P., Barcos, S., Andræ, J., Vestweber, D., McDonald, D. M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-41580-4 · Cited by 70 · see citing works
Functional hyperemia drives fluid exchange in the paravascular space
Kedarasetti, R. T., Turner, K. L., Echagarruga, C., Gluckman, B. J., Drew, P. J., & Costanzo, F. (2020) · Fluids and Barriers of the CNS · doi:10.1186/s12987-020-00214-3 · Cited by 70 · see citing works
Retention of Gadolinium in Brain Parenchyma: Pathways for Speciation, Access, and Distribution. A Critical Review
Rasschaert, M., Weller, R. O., Schroeder, J. A., Brochhausen, C., & Idée, J. (2020) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.27124 · Cited by 64 · see citing works
Inflammatory Regulation of CNS Barriers After Traumatic Brain Injury: A Tale Directed by Interleukin-1
Garnett, C. N., Watson, J. B., Higgins, E. K., Quan, N., & Bachstetter, A. D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.688254 · Cited by 60 · see citing works
Small Vessel Disease-Related Dementia: An Invalid Neurovascular Coupling?
Moretti, R., & Caruso, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031095 · Cited by 58 · see citing works
Molecular Mechanisms of Neuroimmune Crosstalk in the Pathogenesis of Stroke
Choi, Y. H., Laaker, C. J., Hsu, M., Cismaru, P., Sándor, M., & Fábry, Z. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179486 · Cited by 57 · see citing works
Induced Pluripotent Stem Cell-Derived Brain Endothelial Cells as a Cellular Model to Study Neisseria meningitidis Infection
Gomes, S. F. M., Westermann, A. J., Sauerwein, T., Hertlein, T., Förstner, K. U., Ohlsen, K., Metzger, M., Shusta, E. V., Kim, B. J., Appelt‐Menzel, A., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01181 · Cited by 55 · see citing works
A microfabricated, 3D-sharpened silicon shuttle for insertion of flexible electrode arrays through dura mater into brain
Joo, H. R., Fan, J. L., Chen, S., Pebbles, J. A., Liang, H., Chung, J. E., Yorita, A. M., Tooker, A., Tolosa, V. M., Geaghan-Breiner, C., et al. (2019) · Journal of Neural Engineering · doi:10.1088/1741-2552/ab2b2e · Cited by 53 · see citing works
“…rat pia for chronic recording include temporarily stiffening the array during insertion by associating it with biodissolvable coatings of silk (Wu et al., 2015), maltose (Xiang et al., 2014), or polyethylene glycol (PEG; Patel et al., 2015, Khilwani et al., 2016, Kozai et al., 2014, Lo et…”
Background
Dwellers and Trespassers: Mononuclear Phagocytes at the Borders of the Central Nervous System
Ivan, D. C., Walthert, S., Berve, K., Steudler, J., & Locatelli, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.609921 · Cited by 53 · see citing works
“However, the permeability of the pia mater to immune cell trafficking remains debated, and the required interaction molecules are unknown (104, 107, 260).”
BackgroundInfluential
Quantifying cerebrospinal fluid dynamics: A review of human neuroimaging contributions to CSF physiology and neurodegenerative disease
Mehta, N. H., Suss, R. A., Dyke, J. P., Theise, N. D., Chiang, G. C.-Y., Strauß, S., Saint-Louis, L. A., Li, Y., Pahlajani, S. S., Babaria, V., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105776 · Cited by 51 · see citing works
“Trabeculae divide the subarachnoid space into compartments and suspend arteries and veins within the subarachnoid space (Weller et al., 2018).”
Background
Physiological and Pathological Factors Affecting Drug Delivery to the Brain by Nanoparticles
Islam, Y., Leach, A. G., Smith, J. A., Pluchino, S., Coxon, C. R., Sivakumaran, M., Downing, J. R., Fatokun, A. A., Teixidò, M., & Ehtezazi, T. (2021) · Advanced Science · doi:10.1002/advs.202002085 · Cited by 51 · see citing works
Mechanisms of myeloid cell entry to the healthy and diseased central nervous system
Amann, L., Masuda, T., & Prinz, M. (2023) · Nature Immunology · doi:10.1038/s41590-022-01415-8 · Cited by 50 · see citing works
Blockade of VEGFR3 signaling leads to functional impairment of dural lymphatic vessels without affecting autoimmune neuroinflammation
Li, Z., Antila, S., Nurmi, H. J., Chilov, D., Korhonen, E. A., Fang, S., Karaman, S., Engelhardt, B., & Alitalo, K. K. (2023) · Science Immunology · doi:10.1126/sciimmunol.abq0375 · Cited by 51 · see citing works
“In contrast, the arachnoid mater is avascular and composed of several layers of closely packed leptomeningeal cells, with the outermost layer composed of arachnoid barrier cells interconnected with tight junctions (1, 4, 42, 43).”
Background
Fluid outflow in the rat spinal cord: the role of perivascular and paravascular pathways
Liu, S., Lam, M. A., Sial, A. W., Hemley, S. J., Bilston, L. E., & Stoodley, M. A. (2018) · Fluids and Barriers of the CNS · doi:10.1186/s12987-018-0098-1 · Cited by 50 · see citing works
Paravascular spaces: entry to or exit from the brain?
Bakker, E. N. T. P., Naessens, D. M. P., & VanBavel, E. (2018) · Experimental Physiology · doi:10.1113/ep087424 · Cited by 49 · see citing works
Designing and optimizing AAV-mediated gene therapy for neurodegenerative diseases: from bench to bedside
Xu, L., Yao, S., Ding, Y. E., Xie, M., Feng, D., Sha, P., Tan, L., Bei, F., & Yao, Y. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05661-2 · Cited by 48 · see citing works
“The CSF system envelops the CNS system, while separated by pia mater and ependyma in the subarachnoid space and brain ventricular zones respectively to form the CSF-brain barrier [84].”
Background
Novel Therapeutic Potentials of Taxifolin for Amyloid-β-associated Neurodegenerative Diseases and Other Diseases: Recent Advances and Future Perspectives
Tanaka, M., Saitô, S., Inoue, T., Satoh‐Asahara, N., & Ihara, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092139 · Cited by 47 · see citing works
“Aβ distribution in CAA as well as vaccinated AD cases closely corresponds to the intramural periarterial drainage (IPAD) route, which is one of the major systems related to Aβ elimination [21].”
Background
Is CAA a perivascular brain clearance disease? A discussion of the evidence to date and outlook for future studies
van Veluw, S. J., Benveniste, H., Bakker, E. N. T. P., Carare, R. O., Greenberg, S. M., Iliff, J. J., Lorthois, S., Nostrand, W. E. V., Petzold, G. C., Shih, A. Y., et al. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05277-1 · Cited by 50 · see citing works
“In parallel, post-mortem high resolution anatomical data in the human brain show pial sheets at this location [68].”
Background
Meningiomas from a developmental perspective: exploring the crossroads between meningeal embryology and tumorigenesis
Boetto, J., Peyre, M., & Kalamarides, M. (2020) · Acta Neurochirurgica · doi:10.1007/s00701-020-04650-w · Cited by 49 · see citing works
“In addition to this structural role, leptomeninges have complex functions as barriers and facilitators for the movement of fluid, solutes, and cell at the surface and within the CNS, playing a fundamental role in nutrition [74].”
Background
Postmortem changes in brain cell structure: a reviewPreprint
Krassner, M. M., Kauffman, J., Sowa, A., Cialowicz, K. I., Walsh, S., Farrell, K. W., Crary, J. F., & McKenzie, A. T. (2023) · Free Neuropathology · doi:10.17879/freeneuropathology-2023-4790 · Cited by 64 · see citing works
Cerebrospinal fluid flow extends to peripheral nerves further unifying the nervous system
Ligocki, A. P., Vinson, A. V., Yachnis, A. T., Dunn, W. A., Smith, D. E., Scott, E. A., Alvarez-Castanon, J. V., Montalvo, D. E. B., Frisone, O. G., Brown, G. A. J., et al. (2024) · Science Advances · doi:10.1126/sciadv.adn3259 · Cited by 45 · see citing works
“CSF provides physical cushioning while delivering nutrients and remov ing waste for CNS tissues ( 12 ).”
Virulence Factors of Meningitis-Causing Bacteria: Enabling Brain Entry across the Blood–Brain Barrier
Herold, R., Schroten, H., & Schwerk, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20215393 · Cited by 48 · see citing works
“Another major barrier protecting the brain is the BCSFB, which can be separated into a barrier to the inner CSF in the ventricles at the choroid plexus (CP) and barriers to the outer CSF located at the arachnoidea and blood vessels present in the subarachnoidal space [15].”
Background
Epidural and Intrathecal Drug Delivery in Rats and Mice for Experimental Research: Fundamental Concepts, Techniques, Precaution, and Application
Rahman, M. M., Lee, J., Kim, Y. H., & Park, C. (2023) · Biomedicines · doi:10.3390/biomedicines11051413 · Cited by 43 · see citing works
“Similarly, as compared to humans, rodents have a lower relative amount of CSF and slower rates of CSF circulation, but they have similar systems for production and circulation [1,31,33,81].”
Background
The blood–CSF–brain route of neurological disease: The indirect pathway into the brain
Cousins, O., Hodges, A., Schubert, J. J., Veronese, M., Turkheimer, F., Miyan, J. A., Engelhardt, B., & Roncaroli, F. (2021) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12789 · Cited by 44 · see citing works
“Human postmortem studies have questioned the existence of VRS at the brain cortex suggesting that VRS are restricted to the basal ganglia and white matter [33].”
Background
Deficient Leptin Cellular Signaling Plays a Key Role in Brain Ultrastructural Remodeling in Obesity and Type 2 Diabetes Mellitus
Hayden, M. R., & Banks, W. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115427 · Cited by 40 · see citing works
A control mechanism for intra-mural peri-arterial drainage via astrocytes: How neuronal activity could improve waste clearance from the brain
Diem, A. K., Carare, R. O., Weller, R. O., & Bressloff, N. W. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205276 · Cited by 40 · see citing works
Meningeal immunity: Structure, function and a potential therapeutic target of neurodegenerative diseases
Ma, T., Wang, F., Xu, S., & Huang, J. H. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.01.028 · Cited by 37 · see citing works
Subpial Hemorrhage in Neonates: What Radiologists Need to Know
Barreto, A. R. F., Carrasco, M., Dabrowski, A. K., Sun, L. R., & Tekes, A. (2021) · American Journal of Roentgenology · doi:10.2214/ajr.20.22999 · Cited by 40 · see citing works
The lymphatic system: a therapeutic target for central nervous system disorders
Lü, H., Cao, Y., Hu, J., Xu, J., Liu, Q., Huang, S., & Duan, C. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.355741 · Cited by 39 · see citing works
“In the traditional routes, the molecular contents of the CSF are cleared via arachnoid granulations into the dural venous sinus, through the cribriform plate into the nasal mucosa, and via transporters and receptors present on the apical side of the choroid plexus epithelium (Weller et al., 2018).”
Background
A mosquito mouthpart-like bionic neural probe
Zhou, Y., Yang, H., Wang, X., Yang, H., Sun, K., Zhou, Z., Sun, L., Zhao, J., Tao, T. H., & Wei, X. (2023) · Microsystems & Nanoengineering · doi:10.1038/s41378-023-00565-5 · Cited by 37 · see citing works
The anatomic basis of leptomeningeal metastasis
Freret, M. E., & Boire, A. A. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20212121 · Cited by 38 · see citing works
“The meninges that surround the brain and spinal cord comprise three layers (reviewed in Weller et al., 2018).”
Background
Breaching Brain Barriers: B Cell Migration in Multiple Sclerosis
Rodriguez-Mogeda, C., Rodríguez‐Lorenzo, S., Attia, J. V. D., van Horssen, J., Witte, M. E., & de Vries, H. E. (2022) · Biomolecules · doi:10.3390/biom12060800 · Cited by 35 · see citing works
“Directly attached to the meningeal dural mater layer is the arachnoid mater, a translucent multilayer of dense leptomeningeal cells [62].”
BackgroundInfluential
Central Nervous System Fibroblast-Like Cells in Stroke and Other Neurological Disorders
Xu, L., & Yao, Y. (2021) · Stroke · doi:10.1161/strokeaha.120.033431 · Cited by 34 · see citing works
Use of supercritical CO2 in soft tissue decellularization
Topuz, B., Günal, G., Guler, S., & Aydın, H. M. (2019) · Methods in cell biology · doi:10.1016/bs.mcb.2019.10.012 · Cited by 33 · see citing works
VEGFR2 signaling drives meningeal vascular regeneration upon head injury
Koh, B. I., Lee, H. J., Kwak, P. A., Yang, M. J., Kim, J., Kim, H.-S., Koh, G. Y., & Kim, I. (2020) · Nature Communications · doi:10.1038/s41467-020-17545-2 · Cited by 30 · see citing works
Tracking down the White Plague. Chapter two: The role of endocranial abnormal blood vessel impressions and periosteal appositions in the paleopathological diagnosis of tuberculous meningitis
Spekker, O., Schultz, M., Paja, L., Váradi, O. A., Molnár, E., Pálfi, G., & Hunt, D. R. (2020) · PLoS ONE · doi:10.1371/journal.pone.0238444 · Cited by 32 · see citing works
The Underlying Biology and Therapeutic Vulnerabilities of Leptomeningeal Metastases in Adult Solid Cancers
Dankner, M., Lam, S., Degenhard, T., Garzia, L., Guiot, M., Petrecca, K., & Siegel, P. M. (2021) · Cancers · doi:10.3390/cancers13040732 · Cited by 32 · see citing works
“The brain and spinal cord are surrounded by tissues called meninges (Figure 1) [26].”
BackgroundInfluential
Idiopathic Neonatal Subpial Hemorrhage with Underlying Cerebral Infarct: Imaging Features and Clinical Outcome
Assis, Z., Kirton, A., Pauranik, A., Sherriff, M., & Wei, X. (2020) · American Journal of Neuroradiology · doi:10.3174/ajnr.a6872 · Cited by 30 · see citing works
“However, the veins coursing through the subpial space may or may not be invested by the pia mater.(12) Hence, it could be speculated that cortical veins, unlike cortical arteries, which have little-or-no leptomeningeal investment around them, can bleed directly into the subpial space.”
Background
Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time
Kanwal, J. K., Coddington, E. J., Frazer, R., Limbania, D., Turner, G., Davila, K. J., Givens, M. A., Williams, V. M., Datta, S. R., & Wasserman, S. M. (2021) · Integrative and Comparative Biology · doi:10.1093/icb/icab101 · Cited by 28 · see citing works
“These structures at the interface include but are not limited to the lymphatic system, glymphatic system, meninges, blood vasculature, choroid plexus, glial cells, and the skin (Paus et al. 2006; Chen and Lyga 2014; Jessen et al. 2015; Weller et al. 2018; Wilton et al. 2019; Decimo et al. 2020; Kaplan et al. 2020; Tho…”
Background
A Microfluidic Model of AQP4 Polarization Dynamics and Fluid Transport in the Healthy and Inflamed Human Brain: The First Step Towards Glymphatics‐on‐a‐Chip
Soden, P. A., Henderson, A. R., & Lee, E. (2022) · Advanced Biology · doi:10.1002/adbi.202200027 · Cited by 32 · see citing works
The nasal lymphatic route of CSF outflow: implications for neurodegenerative disease diagnosis and monitoring
Chae, J., Choi, M., Choi, J., & Yoo, S. (2024) · Animal Cells and Systems · doi:10.1080/19768354.2024.2307559 · Cited by 29 · see citing works
“Cerebrospinal ﬂ uid (CSF) is a ﬂ uid that ﬂ ows within the central nervous system (CNS), and most is found in the cranial or spinal subarachnoid space (SAS).”
BackgroundInfluential
Development of a Multicomponent Intervention to Prevent Alzheimer's Disease
Saitô, S., Yamamoto, Y., & Ihara, M. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00490 · Cited by 30 · see citing works
“Interestingly, IPAD was impaired in the aging mouse brain and in the presence of CAA (106).”
BackgroundInfluential
Targeting the Choroid Plexuses for Protein Drug Delivery
Bryniarski, M. A., Ren, T., Rizvi, A. R., Snyder, A. M., & Morris, M. E. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12100963 · Cited by 26 · see citing works
Bacterial meningitis in the early postnatal mouse studied at single-cell resolution
Wang, J., Rattner, A., & Nathans, J. (2023) · eLife · doi:10.7554/elife.86130 · Cited by 25 · see citing works
“The brain and spinal cord are protected, both physically and immunologically, by the meninges, a multi-layered tissue that occupies the space between the CNS parenchyma and the surrounding bone (Figure 1A; Coles et al., 2017a ; Weller et al., 2018 ).”
Background
Widespread distribution of lymphatic vessels in human dura mater remote from sinus veins
Quesada, C. L. V., Rao, S. B., Torp, R., & Eide, P. K. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1228344 · Cited by 25 · see citing works
“These MLVs were found to carry substances and waste from the cerebrospinal ﬂ uid (CSF), and impairing their function reduced ef ﬂ ux of toxic waste substances from CSF (Zou et al., 2019; Da Mesquita et al., 2021; Ding et al., 2021).”
Influential
Brain Barriers and Multiple Sclerosis: Novel Treatment Approaches from a Brain Barriers Perspective
Nishihara, H., & Engelhardt, B. (2020) · Handbook of experimental pharmacology · doi:10.1007/164_2020_407 · Cited by 27 · see citing works
Ultrastructural Remodeling of the Neurovascular Unit in the Female Diabetic db/db Model—Part I: Astrocyte
Hayden, M. R., Grant, D. G., Aroor, A. R., & DeMarco, V. G. (2018) · Neuroglia · doi:10.3390/neuroglia1010015 · Cited by 23 · see citing works
“Concurrent with the above findings, other groups identified lymphatic channels in the meninges, and suggested that the drainage was accomplished via a “perivascular channel” that moves within the basal lamina regions of the outer arteriole smooth muscle cells and adventitia [54].”
Result
The contribution of the meningeal immune interface to neuroinflammation in traumatic brain injury
Mokbel, A. Y., Burns, M. P., & Main, B. S. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03122-7 · Cited by 23 · see citing works
“In addition, the dura contains fenestrated blood vessels and lymphatics that form a connection with the periphery [171–176].”
Background
A route for cerebrospinal fluid flow through leptomeningeal arterial–venous overlaps enables macromolecule and fluid shunting
Plog, B. A., Kim, K., Verhaege, D., Kim, M. W., Papadopoulos, Z., Dikranian, K. T., Dykstra, T., Cao, J., Perrin, R. J., Schwetye, K. E., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01977-4 · Cited by 22 · see citing works
“This suggests that the pia–arachnoid membrane forming the periarterial space of the MCA allows an exchange of molecules, but not beads, between the periarterial and subarachnoid spaces 26,27 .”
Development of a multicellular in vitro model of the meningeal blood-CSF barrier to study Neisseria meningitidis infection
Endres, L. M., Jungblut, M., Divyapicigil, M., Sauer, M., Stigloher, C., Christodoulides, M., Kim, B. J., & Schubert‐Unkmeir, A. (2022) · Fluids and Barriers of the CNS · doi:10.1186/s12987-022-00379-z · Cited by 22 · see citing works
Subdural Lesions Linking Additional Intracranial Spaces and Chronic Subdural Hematomas: A Narrative Review with Mutual Correlation and Possible Mechanisms behind High Recurrence
Lin, M.-S. (2023) · Diagnostics · doi:10.3390/diagnostics13020235 · Cited by 21 · see citing works
“The second layer of the meninges, the arachnoid mater, which lies beneath the dura, constitutes the following two layers: the arachnoid barrier cell layer and the arachnoid trabeculae [16].”
Background
Aquaporin-4 expression in the human choroid plexus
Deffner, F., Gleiser, C., Mattheus, U., Wagner, A., Neckel, P. H., Fallier‐Becker, P., Hirt, B., & Mack, A. F. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04136-1 · Cited by 20 · see citing works
Evaluation of AQP4/TRPV4 Channel Co-expression, Microvessel Density, and its Association with Peritumoral Brain Edema in Intracranial Meningiomas
Faropoulos, K., Polia, A., Tsakona, C., Pitaraki, E., Moutafidi, A., Gatzounis, G. D., & Assimakopoulou, M. (2021) · Journal of Molecular Neuroscience · doi:10.1007/s12031-021-01801-1 · Cited by 19 · see citing works
Neuroinflammation-Driven Lymphangiogenesis in CNS Diseases
Hsu, M., Laaker, C. J., Sándor, M., & Fábry, Z. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.683676 · Cited by 20 · see citing works
“Anatomical studies in developing rats revealed the lack of an arachnoid barrier near the cribriform plate (Weller et al., 2018), suggesting that meningeal lymphatics near the cribriform plate may have direct, unrestricted access to the subarachnoid space where prolymphangiogenic factors such as VEGFC may be present du…”
Background
Chronic social defeat alters brain vascular-associated cell gene expression patterns leading to vascular dysfunction and immune system activation
Samuels, J. D., Lotstein, M. L., Lehmann, M. L., ELKAHLOUN, A. G., Banerjee, S., & Herkenham, M. A. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02827-5 · Cited by 17 · see citing works
“In addition to the BBB, the blood-cerebrospinal fluid barrier separates blood from the cerebrospinal fluid (CSF) [1], and the arachnoid blood-cerebrospinal fluid barrier separates dural fenestrated blood vessels from the CSF in the subarachnoid space [2].”
Background
Subarachnoid space trabeculae architecture
Saboori, P. (2020) · Clinical Anatomy · doi:10.1002/ca.23635 · Cited by 18 · see citing works
“This is evident when the studies of Yamashima and Friede (1984) and Pasquesi (2016) are considered together.”
Method
The Balance between the Safety of Mother, Fetus, and Newborn Undergoing Cystic Fibrosis Transmembrane Conductance Regulator Treatments during Pregnancy
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Niche-specific therapeutic targeting of myeloid cells in the central nervous system
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Mechanical allodynia in mice with tenascin-X deficiency associated with Ehlers-Danlos syndrome
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Microscopic morphology and histology of the human meninges
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Anatomy and Physiology of the Leptomeninges and CSF Space
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LEUKOCYTE AND LYMPHATIC INTERACTIONS AT THE CRIBRIFORM PLATE DURING NEUROINFLAMMATION
Laaker, C. J., Baenen, C. M., Hubacek, A. J., Sándor, M., & Fábry, Z. (2023) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2023.08.489
Structural Validation of the Intermediate Leptomeningeal Layer in the Human Central Nervous SystemPreprint
Kumar, A., Paikra, S. K., Kumar, R., Narayan, R. K., Jha, R. K., Yadav, S. S., Kumar, P., Ganapathy, A., Anant, M., Bharti, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.14.664673 · Cited by 2 · see citing works
Advances and controversies in meningeal biology.
Betsholtz, C., Engelhardt, B., Koh, G. Y., McDonald, D. M., Proulx, S. T., & Siegenthaler, J. A. (2024) · Open Access CRIS of the University of Bern · doi:10.48620/75978

Authors: Weller, R. O., Sharp, M. M., Christodoulides, M., Carare, R. O., & Møllgård, K.
Affiliations: Southampton General Hospital (GB)
University of Copenhagen (DK)
Corresponding author: Weller, Roy O.
ORCID: Weller, Roy O.
Sharp, Matthew M.
Christodoulides, Myron
Carare, Roxana O.
Møllgård, Kjeld
Venue: Acta Neuropathologica
Publisher: Springer Science and Business Media LLC
Published: 2018-01-24
Volume: 135
Issue: 3
Pages: 363-385
ISSN: 0001-6322 (ISSN-L)
1432-0533
DOI: 10.1007/s00401-018-1809-z
OpenAlex: W2786295633
Cited by: 222
References: 109
Citations by year: 2026: 24 · 2025: 25 · 2024: 28 · 2023: 35 · 2022: 22 · 2021: 27 · 2020: 28 · 2019: 22 · 2018: 11
FWCI: 2.85
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
Locations: Acta Neuropathologica (publishedVersion, cc-by)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
ePrints Soton (University of Southampton) (submittedVersion)
Funders: Professor Ajay Verma and Biogen
Vera and Carl Johan Michaelsen Foundation (34077)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
Keywords: meninges, leptomeninges, dura mater, arachnoid granulations, cerebrospinal fluid drainage, lymphatic drainage, cribriform plate, meningeal cells, extracellular matrix, Neisseria meningitidis, perivascular spaces, ligand expression
MeSH terms: Animals, Humans, Meninges, Rodentia

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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.

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