دورية أكاديمية

Identification of direct connections between the dura and the brain.

التفاصيل البيبلوغرافية
العنوان: Identification of direct connections between the dura and the brain.
المؤلفون: Smyth LCD; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA. l.c.smyth@wustl.edu.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA. l.c.smyth@wustl.edu., Xu D; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Okar SV; Translational Neuroradiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA., Dykstra T; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Rustenhoven J; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Department of Pharmacology and Clinical Pharmacology, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand.; Centre for Brain Research, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand., Papadopoulos Z; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Neuroscience Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Bhasiin K; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Kim MW; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Immunology Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Drieu A; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Mamuladze T; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Immunology Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Blackburn S; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Gu X; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Gaitán MI; Translational Neuroradiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA., Nair G; Quantitative MRI Core Facility, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA., Storck SE; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Du S; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Immunology Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA., White MA; Department of Genetics, Washington University School of Medicine, Washington University in St Louis, St Louis, MO, USA., Bayguinov P; Washington University Center for Cellular Imaging, Washington University School of Medicine, Washington University in St Louis, St Louis, MO, USA.; Department of Neuroscience, Washington University School of Medicine, Washington University in St Louis, St Louis, MO, USA., Smirnov I; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA., Dikranian K; Department of Neuroscience, Washington University School of Medicine, Washington University in St Louis, St Louis, MO, USA., Reich DS; Translational Neuroradiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA., Kipnis J; Brain Immunology and Glia (BIG) Center, Washington University in St Louis, St Louis, MO, USA. kipnis@wustl.edu.; Department of Pathology and Immunology, School of Medicine, Washington University in St Louis, St Louis, MO, USA. kipnis@wustl.edu.; Neuroscience Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA. kipnis@wustl.edu.; Immunology Graduate Program, School of Medicine, Washington University in St Louis, St Louis, MO, USA. kipnis@wustl.edu.
المصدر: Nature [Nature] 2024 Mar; Vol. 627 (8002), pp. 165-173. Date of Electronic Publication: 2024 Feb 07.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE
أسماء مطبوعة: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
مواضيع طبية MeSH: Arachnoid*/anatomy & histology , Arachnoid*/blood supply , Arachnoid*/immunology , Arachnoid*/metabolism , Brain*/anatomy & histology , Brain*/blood supply , Brain*/immunology , Brain*/metabolism , Dura Mater*/anatomy & histology , Dura Mater*/blood supply , Dura Mater*/immunology , Dura Mater*/metabolism, Animals ; Humans ; Mice ; Biological Transport ; Encephalomyelitis, Autoimmune, Experimental/immunology ; Encephalomyelitis, Autoimmune, Experimental/metabolism ; Gene Expression Profiling ; Magnetic Resonance Imaging ; Mice, Transgenic ; Subarachnoid Space/anatomy & histology ; Subarachnoid Space/blood supply ; Subarachnoid Space/immunology ; Subarachnoid Space/metabolism ; Cerebrospinal Fluid/metabolism ; Veins/metabolism
مستخلص: The arachnoid barrier delineates the border between the central nervous system and dura mater. Although the arachnoid barrier creates a partition, communication between the central nervous system and the dura mater is crucial for waste clearance and immune surveillance 1,2 . How the arachnoid barrier balances separation and communication is poorly understood. Here, using transcriptomic data, we developed transgenic mice to examine specific anatomical structures that function as routes across the arachnoid barrier. Bridging veins create discontinuities where they cross the arachnoid barrier, forming structures that we termed arachnoid cuff exit (ACE) points. The openings that ACE points create allow the exchange of fluids and molecules between the subarachnoid space and the dura, enabling the drainage of cerebrospinal fluid and limited entry of molecules from the dura to the subarachnoid space. In healthy human volunteers, magnetic resonance imaging tracers transit along bridging veins in a similar manner to access the subarachnoid space. Notably, in neuroinflammatory conditions such as experimental autoimmune encephalomyelitis, ACE points also enable cellular trafficking, representing a route for immune cells to directly enter the subarachnoid space from the dura mater. Collectively, our results indicate that ACE points are a critical part of the anatomy of neuroimmune communication in both mice and humans that link the central nervous system with the dura and its immunological diversity and waste clearance systems.
(© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)
References: Louveau, A. et al. Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337–341 (2015). (PMID: 26030524450623410.1038/nature14432)
Rustenhoven, J. et al. Functional characterization of the dural sinuses as a neuroimmune interface. Cell 184, 1000–1016 (2021). (PMID: 33508229848765410.1016/j.cell.2020.12.040)
Mastorakos, P. & McGavern, D. The anatomy and immunology of vasculature in the central nervous system. Sci. Immunol. 4, eaav0492 (2019). (PMID: 31300479681646810.1126/sciimmunol.aav0492)
Iliff, J. J. et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med. 4, 147ra111 (2012). (PMID: 22896675355127510.1126/scitranslmed.3003748)
Shah, T. et al. Arachnoid granulations are lymphatic conduits that communicate with bone marrow and dura-arachnoid stroma. J. Exp. Med. 220, e20220618 (2022). (PMID: 36469302972813610.1084/jem.20220618)
Ringstad, G. & Eide, P. K. Cerebrospinal fluid tracer efflux to parasagittal dura in humans. Nat. Commun. 11, 354 (2020). (PMID: 31953399696904010.1038/s41467-019-14195-x)
Eide, P. K., Vatnehol, S. A. S., Emblem, K. E. & Ringstad, G. Magnetic resonance imaging provides evidence of glymphatic drainage from human brain to cervical lymph nodes. Sci. Rep. 8, 7194 (2018). (PMID: 29740121594079310.1038/s41598-018-25666-4)
Jacob, L. et al. Conserved meningeal lymphatic drainage circuits in mice and humans. J. Exp. Med. 219, e20220035 (2022). (PMID: 35776089925362110.1084/jem.20220035)
Spera, I. et al. Open pathways for cerebrospinal fluid outflow at the cribriform plate along the olfactory nerves. eBioMedicine 91, 104558 (2023). (PMID: 370438711011971310.1016/j.ebiom.2023.104558)
Ma, Q., Ineichen, B. V., Detmar, M. & Proulx, S. T. Outflow of cerebrospinal fluid is predominantly through lymphatic vessels and is reduced in aged mice. Nat. Commun. 8, 1434 (2017). (PMID: 29127332568155810.1038/s41467-017-01484-6)
Ahn, J. H. et al. Meningeal lymphatic vessels at the skull base drain cerebrospinal fluid. Nature 572, 62–66 (2019). (PMID: 3134127810.1038/s41586-019-1419-5)
Hsu, M. et al. Neuroinflammation creates an immune regulatory niche at the meningeal lymphatic vasculature near the cribriform plate. Nat. Immunol. 23, 581–593 (2022). (PMID: 35347285898965610.1038/s41590-022-01158-6)
Absinta, M. et al. Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. eLife 6, e29738 (2017). (PMID: 28971799562648210.7554/eLife.29738)
Louveau, A. et al. CNS lymphatic drainage and neuroinflammation are regulated by meningeal lymphatic vasculature. Nat. Neurosci. 21, 1380–1391 (2018). (PMID: 30224810621461910.1038/s41593-018-0227-9)
Mazzitelli, J. A. et al. Cerebrospinal fluid regulates skull bone marrow niches via direct access through dural channels. Nat. Neurosci. 25, 555–560 (2022). (PMID: 35301477908115810.1038/s41593-022-01029-1)
Wang, Y. et al. Early developing B cells undergo negative selection by central nervous system-specific antigens in the meninges. Immunity 54, 2784–2794 (2021). (PMID: 3462654810.1016/j.immuni.2021.09.016)
Alves de Lima, K. et al. Meningeal γδ T cells regulate anxiety-like behavior via IL-17a signaling in neurons. Nat. Immunol. 21, 1421–1429 (2020). (PMID: 3292927310.1038/s41590-020-0776-4)
Santisteban, M. M. et al. Meningeal interleukin-17-producing T cells mediate cognitive impairment in a mouse model of salt-sensitive hypertension. Nat. Neurosci. https://doi.org/10.1038/s41593-023-01497-z (2023).
Choi, B.-R., Johnson, K. R., Maric, D. & McGavern, D. B. Monocyte-derived IL-6 programs microglia to rebuild damaged brain vasculature. Nat. Immunol. 24, 1110–1123 (2023). (PMID: 3724842010.1038/s41590-023-01521-1)
Roth, T. L. et al. Transcranial amelioration of inflammation and cell death after brain injury. Nature 505, 223–228 (2014). (PMID: 2431769310.1038/nature12808)
Magliozzi, R. et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 130, 1089–1104 (2007). (PMID: 1743802010.1093/brain/awm038)
Chi, Y. et al. Cancer cells deploy lipocalin-2 to collect limiting iron in leptomeningeal metastasis. Science 369, 276–282 (2020). (PMID: 32675368781619910.1126/science.aaz2193)
Yao, H. et al. Leukaemia hijacks a neural mechanism to invade the central nervous system. Nature 560, 55–60 (2018). (PMID: 300221661025714210.1038/s41586-018-0342-5)
Remsik, J. et al. Leptomeningeal anti-tumor immunity follows unique signaling principles. Preprint at bioRxiv https://doi.org/10.1101/2023.03.17.533041 (2023).
De Vlaminck, K. et al. Differential plasticity and fate of brain-resident and recruited macrophages during the onset and resolution of neuroinflammation. Immunity 55, 2085–2102 (2022). (PMID: 3622861510.1016/j.immuni.2022.09.005)
Rebejac, J. et al. Meningeal macrophages protect against viral neuroinfection. Immunity 55, 2103–2117 (2022). (PMID: 3632331110.1016/j.immuni.2022.10.005)
Wang, J., Rattner, A. & Nathans, J. Bacterial meningitis in the early postnatal mouse studied at single-cell resolution. eLife 12, e86130 (2023). (PMID: 373189811027068710.7554/eLife.86130)
Kim, Y.-C. et al. Immaturity of immune cells around the dural venous sinuses contributes to viral meningoencephalitis in neonates. Sci. Immunol. 8, eadg6155 (2023). (PMID: 3780151710.1126/sciimmunol.adg6155)
Pinho-Ribeiro, F. A. et al. Bacteria hijack a meningeal neuroimmune axis to facilitate brain invasion. Nature 615, 472–481 (2023). (PMID: 368595441059311310.1038/s41586-023-05753-x)
Hasel, P. et al. Defining the molecular identity and morphology of glia limitans superficialis astrocytes in mouse and human. Preprint at bioRxiv https://doi.org/10.1101/2023.04.06.535893 (2023).
DeSisto, J. et al. Single-cell transcriptomic analyses of the developing meninges reveal meningeal fibroblast diversity and function. Dev. Cell 54, 43–59 (2020). (PMID: 32634398776905010.1016/j.devcel.2020.06.009)
Pietilä, R. et al. Molecular anatomy of adult mouse leptomeninges. Neuron 111, 3745–3764 (2023).
Drieu, A. et al. Parenchymal border macrophages regulate the flow dynamics of the cerebrospinal fluid. Nature 611, 585–593 (2022). (PMID: 36352225989982710.1038/s41586-022-05397-3)
Park, L. et al. Brain perivascular macrophages initiate the neurovascular dysfunction of Alzheimer Aβ peptides. Circ. Res. 121, 258–269 (2017). (PMID: 28515043552236010.1161/CIRCRESAHA.117.311054)
Møllgård, K. et al. A mesothelium divides the subarachnoid space into functional compartments. Science 379, 84–88 (2023). (PMID: 3660307010.1126/science.adc8810)
Mapunda, J. A. et al. VE-cadherin in arachnoid and pia mater cells serves as a suitable landmark for in vivo imaging of CNS immune surveillance and inflammation. Nat. Commun. 14, 5837 (2023). (PMID: 377307441051163210.1038/s41467-023-41580-4)
Chen, X. et al. Cerebral amyloid angiopathy is associated with glymphatic transport reduction and time-delayed solute drainage along the neck arteries. Nat. Aging 2, 214–223 (2022). (PMID: 36199752953184110.1038/s43587-022-00181-4)
Naganawa, S., Nakane, T., Kawai, H. & Taoka, T. Age dependence of gadolinium leakage from the cortical veins into the cerebrospinal fluid assessed with whole brain 3D-real inversion recovery MR imaging. Magn. Reson. Med. Sci. 18, 163–169 (2019). (PMID: 3039327510.2463/mrms.mp.2018-0053)
Okar, S. V. et al. Highly sensitive 3-Tesla real inversion recovery MRI detects leptomeningeal contrast enhancement in chronic active multiple sclerosis. Invest. Radiol. https://doi.org/10.1097/RLI.0000000000001011 (2023).
Montagne, A. et al. Blood-brain barrier breakdown in the aging human hippocampus. Neuron 85, 296–302 (2015). (PMID: 25611508435077310.1016/j.neuron.2014.12.032)
Da Mesquita, S. et al. Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease. Nature 560, 185–191 (2018). (PMID: 30046111608514610.1038/s41586-018-0368-8)
Wu, J. Y. et al. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 410, 948–952 (2001). (PMID: 11309622207286210.1038/35073616)
Derk, J. et al. Formation and function of the meningeal arachnoid barrier around the developing mouse brain. Dev. Cell 58, 635–644 (2023). (PMID: 3699681610.1016/j.devcel.2023.03.005)
Schaff, M. et al. Integrin α6β1 is the main receptor for vascular laminins and plays a role in platelet adhesion, activation, and arterial thrombosis. Circulation https://doi.org/10.1161/CIRCULATIONAHA.112.000799 (2013).
Kearns, N. A. et al. Dissecting the human leptomeninges at single-cell resolution. Nat. Commun. 14, 7036 (2023). (PMID: 379237211062490010.1038/s41467-023-42825-y)
Chen, J. et al. Meningeal lymphatics clear erythrocytes that arise from subarachnoid hemorrhage. Nat. Commun. 11, 3159 (2020). (PMID: 32572022730841210.1038/s41467-020-16851-z)
Upton, M. L. & Weller, R. O. The morphology of cerebrospinal fluid drainage pathways in human arachnoid granulations. J. Neurosurg. 63, 867–875 (1985). (PMID: 405690110.3171/jns.1985.63.6.0867)
Gailloud, P. et al. Anatomic relationship between arachnoid granulations in the transverse sinus and the termination of the vein of Labbé: an angiographic study. Neuroradiology 43, 139–143 (2001). (PMID: 1132655910.1007/s002340000468)
Balin, B. J., Broadwell, R. D., Salcman, M. & El-Kalliny, M. Avenues for entry of peripherally administered protein to the central nervous system in mouse, rat, and squirrel monkey. J. Comp. Neurol. 251, 260–280 (1986). (PMID: 378250110.1002/cne.902510209)
Holstein-Rønsbo, S. et al. Glymphatic influx and clearance are accelerated by neurovascular coupling. Nat. Neurosci. 26, 1042–1053 (2023). (PMID: 372641581050015910.1038/s41593-023-01327-2)
Mestre, H. et al. Flow of cerebrospinal fluid is driven by arterial pulsations and is reduced in hypertension. Nat. Commun. 9, 4878 (2018). (PMID: 30451853624298210.1038/s41467-018-07318-3)
Bojarskaite, L. et al. Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport. Nat. Commun. 14, 953 (2023). (PMID: 36806170994149710.1038/s41467-023-36643-5)
Fitzpatrick, Z. et al. Gut-educated IgA plasma cells defend the meningeal venous sinuses. Nature 587, 472–476 (2020). (PMID: 33149302774838310.1038/s41586-020-2886-4)
Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483–486 (2010). (PMID: 2044553710.1038/nature09002)
Ben-Zvi, A. et al. Mfsd2a is critical for the formation and function of the blood–brain barrier. Nature 509, 507–511 (2014). (PMID: 24828040413487110.1038/nature13324)
Schachenmayr, W. & Friede, R. L. The origin of subdural neomembranes. I. Fine structure of the dura-arachnoid interface in man. Am. J. Pathol. 92, 53–68 (1978). (PMID: 6861482018597)
Nabeshima, S., Reese, T. S., Landis, D. M. D. & Brightman, M. W. Junctions in the meninges and marginal glia. J. Comp. Neurol. 164, 127–169 (1975). (PMID: 81049710.1002/cne.901640202)
Vandenabeele, F., Creemers, J. & Lambrichts, I. Ultrastructure of the human spinal arachnoid mater and dura mater. J. Anat. 189, 417–430 (1996). (PMID: 88869631167758)
Mestre, H. et al. Periarteriolar spaces modulate cerebrospinal fluid transport into brain and demonstrate altered morphology in aging and Alzheimer’s disease. Nat. Commun. 13, 3897 (2022). (PMID: 35794106925966910.1038/s41467-022-31257-9)
Murray, H. C. et al. Lamina-specific immunohistochemical signatures in the olfactory bulb of healthy, Alzheimer’s and Parkinson’s disease patients. Commun. Biol. 5, 88 (2022). (PMID: 35075270878693410.1038/s42003-022-03032-5)
Maric, D. et al. Whole-brain tissue mapping toolkit using large-scale highly multiplexed immunofluorescence imaging and deep neural networks. Nat. Commun. 12, 1550 (2021). (PMID: 33692351794693310.1038/s41467-021-21735-x)
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018). (PMID: 29608179670074410.1038/nbt.4096)
Lun, A. T. L., McCarthy, D. J. & Marioni, J. C. A step-by-step workflow for low-level analysis of single-cell RNA-seq data with Bioconductor. F1000Res. https://doi.org/10.12688/f1000research.9501.2 (2016).
McCarthy, D. J., Campbell, K. R., Lun, A. T. L. & Wills, Q. F. Scater: pre-processing, quality control, normalization and visualization of single-cell RNA-seq data in R. Bioinformatics 33, 1179–1186 (2017). (PMID: 28088763540884510.1093/bioinformatics/btw777)
Hong, G., Zhang, W., Li, H., Shen, X. & Guo, Z. Separate enrichment analysis of pathways for up- and downregulated genes. J. R. Soc. Interface 11, 20130950 (2014). (PMID: 24352673389986310.1098/rsif.2013.0950)
Yu, G., Wang, L.-G., Han, Y. & He, Q.-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS J. Integr. Biol. 16, 284–287 (2012). (PMID: 10.1089/omi.2011.0118)
Baccin, C. et al. Combined single-cell and spatial transcriptomics reveal the molecular, cellular and spatial bone marrow niche organization. Nat. Cell Biol. 22, 38–48 (2020). (PMID: 3187132110.1038/s41556-019-0439-6)
Yushkevich, P. A. et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. NeuroImage 31, 1116–1128 (2006). (PMID: 1654596510.1016/j.neuroimage.2006.01.015)
معلومات مُعتمدة: P01 AG078106 United States AG NIA NIH HHS; R01 AG034113 United States AG NIA NIH HHS; R37 AG034113 United States AG NIA NIH HHS; ZIA NS003119 United States ImNIH Intramural NIH HHS
تواريخ الأحداث: Date Created: 20240207 Date Completed: 20240308 Latest Revision: 20240723
رمز التحديث: 20240725
مُعرف محوري في PubMed: PMC11254388
DOI: 10.1038/s41586-023-06993-7
PMID: 38326613
قاعدة البيانات: MEDLINE
الوصف
تدمد:1476-4687
DOI:10.1038/s41586-023-06993-7