Advances in Meningeal Immunity
Open accessAbstract
The central nervous system (CNS) is an immunologically specialized tissue protected by a blood-brain barrier. The CNS parenchyma is enveloped by a series of overlapping membranes that are collectively referred to as the meninges. The meninges provide an additional CNS barrier, harbor a diverse array of resident immune cells, and serve as a crucial interface with the periphery. Recent studies have significantly advanced our understanding of meningeal immunity, demonstrating how a complex immune landscape influences CNS functions under steady-state and inflammatory conditions. The location and activation state of meningeal immune cells can profoundly influence CNS homeostasis and contribute to neurological disorders, but these cells are also well equipped to protect the CNS from pathogens. In this review, we discuss advances in our understanding of the meningeal immune repertoire and provide insights into how this CNS barrier operates immunologically under conditions ranging from neurocognition to inflammatory diseases.
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The dura mater resembles the periphery with its permeable vasculature, lymphatic drainage, and diverse assortment of resident immune cells.
“The dura mater resembles the periphery with its permeable vasculature, lymphatic drainage, and diverse assortment of resident immune cells (such as macrophages, DCs, mast cells, innate lymphoid cells, B cells, and T cells) (92).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [92]
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Mizgerd, J. P., Kubo, H., Kutkoski, G. J., Bhagwan, S. D., Scharffetter-Kochanek, K., Beaudet, A. L., & Doerschuk, C. M. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.8.1357 · Cited by 7,332 · see citing works
Iliff, J. J., Wang, M., Liao, Y., Plogg, B. A., Peng, W., Gundersen, G. A., Benveniste, H., Vates, G. E., Deane, R., Goldman, S. A., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003748 · Cited by 5,824 · see citing works
Structural and functional features of central nervous system lymphatic vessels
Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J., Peske, J. D., Derecki, N. C., Castle, D., Mandell, J. W., Lee, K. S., et al. (2015) · Nature · doi:10.1038/nature14432 · Cited by 4,413 · see citing works
Azevedo, R. S. S., de Sousa, J. R., Araujo, M. T. F., Martins Filho, A. J., de Alcantara, B. N., Araujo, F. M. C., Queiroz, M. G. L., Cruz, A. C. R., Vasconcelos, B. H. B., Chiang, J. O., et al. (2018) · Scientific Reports · doi:10.1038/s41598-017-17765-5 · Cited by 3,478 · see citing works
A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules
Aspelund, A., Antila, S., Proulx, S. T., Karlsen, T. V., Karaman, S., Detmar, M., Wiig, H., & Alitalo, K. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20142290 · Cited by 2,198 · see citing works
Magliozzi, R., Howell, O. W., Vora, A., Serafini, B., Nicholas, R. S., Puopolo, M., Reynolds, R., & Aloisi, F. (2006) · Brain · doi:10.1093/brain/awm038 · Cited by 1,444 · see citing works
Intravascular Danger Signals Guide Neutrophils to Sites of Sterile Inflammation
McDonald, B., Pittman, K., Menezes, G. B., Hirota, S. A., Slaba, I., Waterhouse, C. C. M., Beck, P. L., Muruve, D. A., & Kubes, P. (2010) · Science · doi:10.1126/science.1195491 · Cited by 1,210 · see citing works
Origin, fate and dynamics of macrophages at central nervous system interfaces
Goldmann, T., Wieghofer, P., Jordão, M. J. C., Prutek, F., Hagemeyer, N., Frenzel, K., Amann, L., Staszewski, O., Kierdorf, K., Krueger, M., et al. (2016) · Nature Immunology · doi:10.1038/ni.3423 · Cited by 1,209 · see citing works
Codarri, L., Gyülvészi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., Suter, T., & Becher, B. (2011) · Nature Immunology · doi:10.1038/ni.2027 · Cited by 1,191 · see citing works
Microglia development and function
Nayak, D., Roth, T. L., & McGavern, D. B. (2014) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032713-120240 · Cited by 1,154 · see citing works
Self-citationCommensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells
Benakis, C., Brea, D., Caballero, S., Faraco, G., Moore, J., Murphy, M., Sita, G., Racchumi, G., Ling, L., Pamer, E. G., et al. (2016) · Nature Medicine · doi:10.1038/nm.4068 · Cited by 1,114 · see citing works
Temporal and Spatial Dynamics of Cerebral Immune Cell Accumulation in Stroke
Gelderblom, M., Leypoldt, F., Steinbach, K., Behrens, D., Choe, C.-U., Siler, D. A., Arumugam, T. V., Orthey, E., Gerloff, C., Tolosa, E., et al. (2009) · Stroke · doi:10.1161/strokeaha.108.534503 · Cited by 1,066 · see citing works
Three or more routes for leukocyte migration into the central nervous system
Ransohoff, R. M., Kivisäkk, P., & Kidd, G. (2003) · Nature Reviews Immunology · doi:10.1038/nri1130 · Cited by 1,052 · see citing works
Mrdjen, D., Pavlovic, A., Hartmann, F. J., Schreiner, B., Utz, S. G., Leung, B. P., Lelios, I., Heppner, F. L., Kipnis, J., Merkler, D., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.01.011 · Cited by 1,010 · see citing works
Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis
Greter, M., Heppner, F. L., Lemos, M. P., Odermatt, B. M., Goebels, N., Laufer, T., Noelle, R. J., & Becher, B. (2005) · Nature Medicine · doi:10.1038/nm1197 · Cited by 862 · see citing works
Inflammation and neuroprotection in traumatic brain injury.
Corps, K. N., Roth, T. L., & McGavern, D. B. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2014.3558 · Cited by 853 · see citing works
Self-citationShichita, T., Sugiyama, Y., Ooboshi, H., Sugimori, H., Nakagawa, R., Takada, I., Iwaki, T., Okada, Y., Iida, M., Cua, D. J., et al. (2009) · Nature Medicine · doi:10.1038/nm.1999 · Cited by 842 · see citing works
Regulation of learning and memory by meningeal immunity: a key role for IL-4
Derecki, N. C., Cardani, A. N., Yang, C. H., Quinnies, K. M., Crihfield, A., Lynch, K. R., & Kipnis, J. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20091419 · Cited by 800 · see citing works
What is immune privilege (not)?
Galea, I., Bechmann, I., & Perry, V. H. (2007) · Trends in Immunology · doi:10.1016/j.it.2006.11.004 · Cited by 768 · see citing works
Sensitization of meningeal sensory neurons and the origin of headaches
Strassman, A. M., Raymond, S. A., & Burstein, R. (1996) · Nature · doi:10.1038/384560a0 · Cited by 704 · see citing works
Unexpected role of interferon-γ in regulating neuronal connectivity and social behaviour
Filiano, A. J., Xu, Y., Tustison, N. J., Marsh, R. L., Baker, W., Smirnov, I., Overall, C. C., Gadani, S. P., Turner, S. D., Weng, Z., et al. (2016) · Nature · doi:10.1038/nature18626 · Cited by 697 · see citing works
Ma, Q., Ineichen, B. V., Detmar, M., & Proulx, S. T. (2017) · Nature Communications · doi:10.1038/s41467-017-01484-6 · Cited by 690 · see citing works
Capture, crawl, cross: the T cell code to breach the blood–brain barriers
Engelhardt, B., & Ransohoff, R. M. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.07.004 · Cited by 686 · see citing works
Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions.
Bartholomäus, I., Kawakami, N., Odoardi, F., Schläger, C., Miljkovic, D., Ellwart, J. W., Klinkert, W. E. F., Flügel-Koch, C., Issekutz, T. B., Wekerle, H., et al. (2009) · Nature · doi:10.1038/nature08478 · Cited by 685 · see citing works
Shechter, R., Miller, O., Yovel, G., Rosenzweig, N., London, A., Ruckh, J., Kim, K.-W., Klein, E., Kalchenko, V., Bendel, P., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.02.012 · Cited by 683 · see citing works
Migraine Headache Triggered Specifically by Sunlight: Report of 16 Cases
Tekataş, A., & Mungen, B. (2013) · European Neurology · doi:10.1159/000354165 · Cited by 665 · see citing works
Targeting Neutrophils in Ischemic Stroke: Translational Insights from Experimental Studies
Jickling, G. C., Liu, D., Ander, B. P., Stamova, B., Zhan, X., & Sharp, F. R. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.45 · Cited by 644 · see citing works
Absinta, M., Ha, S.-K., Nair, G., Sati, P., Luciano, N. J., Palisoc, M., Louveau, A., Zaghloul, K. A., Pittaluga, S., Kipnis, J., et al. (2017) · eLife · doi:10.7554/elife.29738 · Cited by 643 · see citing works
Transcranial amelioration of inflammation and cell death after brain injury.
Roth, T. L., Nayak, D., Atanasijevic, T., Koretsky, A. P., Latour, L. L., & McGavern, D. B. (2014) · Nature · doi:10.1038/nature12808 · Cited by 574 · cited 9× · see citing works
“Sterile Injury Triggers Meningeal Inflammation Traumatic brain injury (TBI) affects more than 2 million people in the United States every year, and there are currently no highly effective treatments available [105].”
InfluentialKivisäkk, P., Mahad, D., Callahan, M. K., Trebst, C., Tucky, B. H., Wei, T., Wu, L., Bækkevold, E. S., Lassmann, H., Staugaitis, S. M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1433000100 · Cited by 546 · see citing works
Kipnis, J., Cohen, H., Cardon, M., Ziv, Y., & Schwartz, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402268101 · Cited by 510 · see citing works
Neutralization of the IL-17 axis diminishes neutrophil invasion and protects from ischemic stroke
Gelderblom, M., Weymar, A., Bernreuther, C., Velden, J., Arunachalam, P., Steinbach, K., Orthey, E., Arumugam, T. V., Leypoldt, F., Simova, O., et al. (2012) · Blood · doi:10.1182/blood-2012-02-412726 · Cited by 457 · see citing works
A balanced view of the cerebrospinal fluid composition and functions: Focus on adult humans
Spector, R., Snodgrass, S. R., & Johanson, C. E. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.07.027 · Cited by 445 · see citing works
Markowitz, S., Saito, K., & Moskowitz, M. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-04129.1987 · Cited by 441 · see citing works
High-dimensional, single-cell characterization of the brain's immune compartment
Korin, B., Ben-Shaanan, T. L., Schiller, M., Dubovik, T., Azulay‐Debby, H., Boshnak, N., Koren, T., & Rolls, A. (2017) · Nature Neuroscience · doi:10.1038/nn.4610 · Cited by 423 · see citing works
Nakae, S., Suto, H., Iikura, M., Kakurai, M., Sedgwick, J. D., Tsai, M. M., & Galli, S. J. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.4.2238 · Cited by 412 · see citing works
Zhang, X., Levy, D., Noseda, R., Kainz, V., Jakubowski, M., & Burstein, R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0511-10.2010 · Cited by 408 · see citing works
Ontogeny and homeostasis of CNS myeloid cells
Prinz, M., Erny, D., & Hagemeyer, N. (2017) · Nature Immunology · doi:10.1038/ni.3703 · Cited by 391 · see citing works
Animal models of multiple sclerosis: the good, the bad and the bottom line
Ransohoff, R. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3168 · Cited by 379 · see citing works
Effector T-cell trafficking between the leptomeninges and the cerebrospinal fluid
Schläger, C., Körner, H., Krueger, M., Vidoli, S., Haberl, M., Mielke, D., Brylla, E., Issekutz, T., Cabañas, C., Nelson, P. J., et al. (2016) · Nature · doi:10.1038/nature16939 · Cited by 372 · see citing works
Mast cell degranulation activates a pain pathway underlying migraine headache
Levy, D., Burstein, R., Kainz, V., et al. (2007) · Pain · doi:10.1016/j.pain.2007.03.012 · Cited by 371 · see citing works
Smith, A. J., Yao, X., Dix, J. A., Jin, B.-J., & Verkman, A. S. (2017) · eLife · doi:10.7554/elife.27679 · Cited by 362 · see citing works
Balin, B. J., Broadwell, R. D., Salcman, M., & El‐Kalliny, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510209 · Cited by 358 · see citing works
Simon, M. J., & Iliff, J. J. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.014 · Cited by 339 · see citing works
Wolf, S. A., Steiner, B., Akpinarli, A., Kammertoens, T., Nassenstein, C., Braun, A., Blankenstein, T., & Kempermann, G. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0801218 · Cited by 329 · see citing works
Takeshita, Y., & Ransohoff, R. M. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01127.x · Cited by 327 · see citing works
Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis
Kim, J. V., Kang, S. S., Dustin, M. L., & McGavern, D. B. (2009) · Nature · doi:10.1038/nature07591 · Cited by 326 · see citing works
Self-citationBlocking CGRP in migraine patients – a review of pros and cons
Deen, M., Correnti, E., Kamm, K., Kelderman, T., Papetti, L., Rubio‐Beltrán, E., Vigneri, S., Edvinsson, L. I., & MaassenVanDenBrink, A. (2017) · The Journal of Headache and Pain · doi:10.1186/s10194-017-0807-1 · Cited by 301 · see citing works
Nerve fibres and their terminals of the dura mater encephali of the rat
Andres, K. H., D�ring, M., Muszynski, K., & Schmidt, R. F. (1987) · Anatomy and Embryology · doi:10.1007/bf00309843 · Cited by 289 · see citing works
Kivisäkk, P., Imitola, J., Rasmussen, S. O., Elyaman, W., Zhu, B., Ransohoff, R. M., & Khoury, S. J. (2008) · Annals of Neurology · doi:10.1002/ana.21379 · Cited by 287 · see citing works
Reperfusion therapy in acute ischemic stroke: dawn of a new era?
Bhaskar, S. M. M., Stanwell, P., Cordato, D. J., Attia, J., & Levi, C. R. (2018) · BMC Neurology · doi:10.1186/s12883-017-1007-y · Cited by 251 · see citing works
Comparative anatomy and histology : a mouse and human atlas
Treuting, P. M., & Dintzis, S. M. (2012) · doi:10.1016/c2009-0-61166-1 · Cited by 241 · see citing works
Stirling, D. P., Liu, S., Kubes, P., & Yong, V. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4918-08.2009 · Cited by 234 · see citing works
Pikor, N. B., Astarita, J. L., Summers-Deluca, L., Galicia, G., Qu, J., Ward, L. A., Armstrong, S., Dominguez, C. X., Malhotra, D., Heiden, B., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.010 · Cited by 229 · see citing works
Enzmann, G., Mysiorek, C., Gorina, R., Cheng, Y.-J., Ghavampour, S., Hannocks, M.-J., Prinz, V., Dirnagl, U., Endres, M., Prinz, M., et al. (2013) · Acta Neuropathologica · doi:10.1007/s00401-012-1076-3 · Cited by 225 · see citing works
Adaptive immunity affects learning behavior in mice
Brynskikh, A., Warren, T., Zhu, J., & Kipnis, J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.12.008 · Cited by 221 · see citing works
Mrdjen, D., Pavlovic, A., Hartmann, F. J., Schreiner, B., Utz, S. G., Leung, B. P., Lelios, I., Heppner, F. L., Kipnis, J., Merkler, D., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.014 · Cited by 220 · cited 3× · see citing works
“It was also recently discovered using mass cytometry that T cells are enriched in the CNS of mice upon aging [37].”
Interactions of innate and adaptive immunity in brain development and function
Filiano, A. J., Gadani, S. P., & Kipnis, J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.07.050 · Cited by 217 · see citing works
MHCII-independent CD4+ T cells protect injured CNS neurons via IL-4.
Walsh, J. T., Hendrix, S., Boato, F., Smirnov, I., Zheng, J., Lukens, J. R., Gadani, S. P., Hechler, D., Gölz, G., Rosenberger, K., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci76210 · Cited by 208 · see citing works
Brain perivascular macrophages: characterization and functional roles in health and disease
Faraco, G., Park, L., Anrather, J., & Iadecola, C. (2017) · Journal of Molecular Medicine · doi:10.1007/s00109-017-1573-x · Cited by 206 · see citing works
Sensory innervation of the calvarial bones of the mouse
Kosaras, B., Jakubowski, M., Kainz, V., et al. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22049 · Cited by 205 · see citing works
Molecular characterization of perivascular drainage pathways in the murine brain
Hannocks, M.-J., Pizzo, M. E., Huppert, J., Deshpande, T., Abbott, N. J., Thorne, R. G., & Sorokin, L. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17749689 · Cited by 201 · see citing works
Brown, D. A., & Sawchenko, P. E. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21307 · Cited by 200 · see citing works
How and why do T cells and their derived cytokines affect the injured and healthy brain?
Filiano, A. J., Gadani, S. P., & Kipnis, J. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.39 · Cited by 199 · see citing works
Migraine pain, meningeal inflammation, and mast cells
Levy, D. (2009) · Current Pain and Headache Reports · doi:10.1007/s11916-009-0040-y · Cited by 191 · see citing works
Peptidergic and serotoninergic innervation of the rat dura mater
Keller, J. T., & Marfurt, C. F. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903090408 · Cited by 184 · see citing works
Galea, I., Palin, K., Newman, T. A., van Rooijen, N., Perry, V. H., & Boche, D. (2004) · Glia · doi:10.1002/glia.20124 · Cited by 183 · see citing works
Neurovascular contributions to migraine: Moving beyond vasodilation
Jacobs, B. A., & Dussor, G. O. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.06.012 · Cited by 182 · see citing works
Blank, T., Detje, C. N., Spieß, A., Hagemeyer, N., Brendecke, S. M., Wolfart, J., Staszewski, O., Zöller, T., Papageorgiou, I. E., Schneider, J., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.04.005 · Cited by 179 · see citing works
The spectrum of neuropathological changes associated with congenital Zika virus infection
Chimelli, L. M. C., Melo, A., Portari, E. A., Wiley, C. A., Camacho, A. H. S., Lopes, V. S., Machado, H. N., de Andrade, C. V., Dock, D. C. D. A., Moreira, M. E. L., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1699-5 · Cited by 168 · see citing works
Wilson, E. H., Harris, T. H., Mrass, P., John, B., Wojno, E. D. T., Wu, G. F., Pepper, M., Wherry, E. J., Dzierzinski, F., Roos, D. S., et al. (2009) · Immunity · doi:10.1016/j.immuni.2008.12.013 · Cited by 167 · see citing works
Pattern of intracranial and extracranial projections of trigeminal ganglion cells
O'Connor, T., & van der Kooy, D. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-08-02200.1986 · Cited by 166 · see citing works
Christy, A. L., Walker, M. E., Hessner, M. J., & Brown, M. A. (2012) · Journal of Autoimmunity · doi:10.1016/j.jaut.2012.11.003 · Cited by 165 · see citing works
Sayed, B. A., Christy, A. L., Walker, M. E., & Brown, M. A. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000126 · Cited by 163 · see citing works
Cerebrospinal Fluid in Clinical Practice
Jellinger, K. A. (2009) · European Journal of Neurology · doi:10.1111/j.1468-1331.2009.02601.x · Cited by 161 · see citing works
Nakae, S., Suto, H., Berry, G. J., & Galli, S. J. (2006) · Blood · doi:10.1182/blood-2006-09-046128 · Cited by 160 · see citing works
THE MEMBRANOUS COVERINGS OF NEURAL TISSUES: AN ELECTORN MICROSCOPY STUDY
WAGGENER, J. D., & BEGGS, J. (1967) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-196707000-00005 · Cited by 154 · see citing works
Inducible MHC Class II Expression by Mast Cells Supports Effector and Regulatory T Cell Activation
Kambayashi, T., Allenspach, E. J., Chang, J. T., Zou, T., Shoag, J. E., Reiner, S. L., Caton, A. J., & Koretzky, G. A. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803180 · Cited by 153 · see citing works
Central memory CD4+ T cells dominate the normal cerebrospinal fluid
de Graaf, M. T., Smitt, P. A. E. S., Luitwieler, R. L., et al. (2010) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20542 · Cited by 149 · see citing works
Gardner, C., Magliozzi, R., Durrenberger, P. F., Howell, O. W., Rundle, J., & Reynolds, R. (2013) · Brain · doi:10.1093/brain/awt279 · Cited by 148 · see citing works
Characterization of meningeal type 2 innate lymphocytes and their response to CNS injury
Gadani, S. P., Smirnov, I., Wiltbank, A. T., Overall, C. C., & Kipnis, J. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20161982 · Cited by 148 · see citing works
Lodygin, D., Odoardi, F., Schläger, C., Körner, H., Kitz, A., Nosov, M., van den Brandt, J., Reichardt, H. M., Haberl, M., & Flügel, A. (2013) · Nature Medicine · doi:10.1038/nm.3182 · Cited by 144 · see citing works
Radjavi, A., Smirnov, I., & Kipnis, J. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.08.013 · Cited by 135 · see citing works
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 · see citing works
Activation of Meningeal 5‐HT2B Receptors: An Early Step in the Generation of Migraine Headache?
Schmuck, K., Ullmer, C., Kalkman, H. O., et al. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01583.x · Cited by 127 · see citing works
The collagenic architecture of human dura mater
Protasoni, M., Sangiorgi, S., Cividini, A., Culuvaris, G. T., Tomei, G., Dell’Orbo, C., Raspanti, M., Balbi, S., & Reguzzoni, M. (2011) · Journal of neurosurgery · doi:10.3171/2010.12.jns101732 · Cited by 126 · see citing works
Coles, J. A., Myburgh, E., Brewer, J. M., & McMenamin, P. G. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.002 · Cited by 123 · see citing works
T-bet-dependent NKp46+ innate lymphoid cells regulate the onset of TH17-induced neuroinflammation
Kwong, B., Rua, R., Gao, Y., Flickinger, J. C., Wang, Y., Kruhlak, M. J., Zhu, J., Vivier, É., McGavern, D. B., & Lazarevic, V. (2017) · Nature Immunology · doi:10.1038/ni.3816 · Cited by 114 · see citing works
Self-citationRadjavi, A., Smirnov, I., Derecki, N., & Kipnis, J. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.79 · Cited by 112 · see citing works
In vivo dynamics of innate immune sentinels in the CNS
Nayak, D., Zinselmeyer, B. H., Corps, K. N., & McGavern, D. B. (2012) · IntraVital · doi:10.4161/intv.22823 · Cited by 109 · see citing works
Self-citationActivation of pial and dural macrophages and dendritic cells by cortical spreading depression
Schain, A. J., Melo‐Carrillo, A., Borsook, D., Grutzendler, J., Strassman, A. M., & Burstein, R. (2018) · Annals of Neurology · doi:10.1002/ana.25169 · Cited by 105 · see citing works
Dural and pial pain-sensitive structures in humans: new inputs from awake craniotomies
Fontaine, D., Almairac, F., Santucci, S., et al. (2018) · Brain · doi:10.1093/brain/awy005 · Cited by 105 · see citing works
Primary Afferent Neurons Innervating Guinea Pig Dura
Bove, G. M., & Moskowitz, M. A. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.1.299 · Cited by 103 · see citing works
Clearance from the mouse brain by convection of interstitial fluid towards the ventricular system
Bedussi, B., van Lier, M. G. J. T. B., Bartstra, J. W., de Vos, J., Siebes, M., VanBavel, E., & Bakker, E. N. T. P. (2015) · Fluids and Barriers of the CNS · doi:10.1186/s12987-015-0019-5 · Cited by 102 · see citing works
Afferent and efferent immunological pathways of the brain. Anatomy, Function and Failure
Carare, R. O., Hawkes, C. A., & Weller, R. O. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.10.012 · Cited by 100 · see citing works
Alternatively activated myeloid (M2) cells enhance cognitive function in immune compromised mice
Derecki, N. C., Quinnies, K. M., & Kipnis, J. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.11.009 · Cited by 97 · see citing works
Vasorum lymphaticorum corporis humani historia et ichnographia
Mascagni, P. (1983) · Readex Microprint eBooks · Cited by 89 · see citing works
The meninges: new therapeutic targets for multiple sclerosis
Russi, A. E., & Brown, M. A. (2014) · Translational research · doi:10.1016/j.trsl.2014.08.005 · Cited by 89 · see citing works
Lymphocytic choriomeningitis infection of the central nervous system
Silvia, S. K. (2008) · Frontiers in bioscience · doi:10.2741/3021 · Cited by 87 · see citing works
Kemp, W. J., Tubbs, R. S., & Cohen‐Gadol, A. (2011) · World Neurosurgery · doi:10.1016/j.wneu.2011.10.045 · Cited by 86 · see citing works
Lamers, S. L., Gray, R. R., Salemi, M., et al. (2010) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2010.10.016 · Cited by 85 · see citing works
Hatfield, J. K., & Brown, M. A. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.06.006 · Cited by 77 · see citing works
Referral of pain from dural stimulation in man
Wirth, F. P., & Buren, J. M. V. (1971) · Journal of neurosurgery · doi:10.3171/jns.1971.34.5.0630 · Cited by 76 · see citing works
Evidence that Meningeal mast cells can worsen stroke pathology in mice.
Arac, A., Grimbaldeston, M. A., Nepomuceno, A. R. B., Olayiwola, O., Pereira, M. P., Nishiyama, Y., Tsykin, A., Goodall, G. J., Schlecht, U., Vogel, H., et al. (2014) · The American Journal of Pathology · doi:10.1016/j.ajpath.2014.06.003 · Cited by 74 · see citing works
Poltera, A. A., Hochmann, A., Rudin, W., et al. (1980) · PubMed · Cited by 67 · see citing works
Postmortem Findings for 7 Neonates with Congenital Zika Virus Infection
Sousa, A. D. Q., Cavalcante, D. I. M., Franco, L. M., Araújo, F. M. D. C., de Sousa, E. T., Valença, J. T., Rolim, D. B., de Melo, M. E. L., Filho, P. D. T. S., de Araújo, M. T. F., et al. (2017) · Emerging infectious diseases · doi:10.3201/eid2307.162019 · Cited by 59 · see citing works
Rods and cones project to the inner plexiform layer during development
Johnson, P. T., Williams, R. R., Cusato, K., & Reese, B. E. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991108)414:1 · Cited by 56 · see citing works
African trypanosomes and brain infection – the unsolved question
Mogk, S., Boßelmann, C. M., Mudogo, C. N., Stein, J., Wolburg, H., & Duszenko, M. (2016) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12301 · Cited by 56 · see citing works
Zarif, H., Nicolas, S., Guyot, M., Hosseiny, S., Lazzari, A., Canali, M. M., Cazareth, J., Brau, F., Golzné, V., Dourneau, E., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.11.016 · Cited by 56 · see citing works
Late Stage Infection in Sleeping Sickness
Wolburg, H., Mogk, S., Acker, S., Frey, C., Meinert, M., Schönfeld, C., Lazarus, M., Urade, Y., Kubata, B. K., & Duszenko, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034304 · Cited by 55 · see citing works
Meningeal mast cell-T cell crosstalk regulates T cell encephalitogenicity
Russi, A. E., Caulfield, M. E., Guo, Y. X., Lucchinetti, C. F., & Brown, M. A. (2016) · Journal of Autoimmunity · doi:10.1016/j.jaut.2016.06.015 · Cited by 54 · see citing works
Neurobehavioral Changes Resulting from Recombinase Activation Gene 1 Deletion
Cushman, J. D., Lo, J., Huang, Z. L., Wasserfall, C. H., & Petitto, J. M. (2003) · Clinical and Vaccine Immunology · doi:10.1128/cdli.10.1.13-18.2003 · Cited by 51 · see citing works
The pathogenesis of trypanosomiasis of the CNS
Schmidt, H. (1983) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/bf00612951 · Cited by 50 · see citing works
Kang, S. S., Herz, J., Kim, J. V., Nayak, D., Stewart-Hutchinson, P. J., Dustin, M. L., & McGavern, D. B. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101295 · Cited by 47 · see citing works
Self-citationPathophysiology of Blood–Brain Barrier Breakdown
Nag, S. (2003) · Humana Press eBooks · doi:10.1385/1-59259-419-0:97 · Cited by 45 · see citing works
Microbial Induction of Vascular Pathology in the CNS
Kang, S. S., & McGavern, D. B. (2010) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-010-9208-9 · Cited by 44 · see citing works
Self-citationStokely, M. E., & Orr, E. L. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2007.0397 · Cited by 42 · see citing works
The role of histamine in dural vessel dilation
Akerman, S., Williamson, D. J., Kaube, H., & Goadsby, P. J. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03485-6 · Cited by 41 · see citing works
Meningeal Afferent Signaling and the Pathophysiology of Migraine
Burgos-Vega, C., Moy, J. K., & Dussor, G. O. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.01.001 · Cited by 39 · see citing works
The fine structure of subarachnoid macrophages in the rat
Morse, D. E., & Low, F. N. (1972) · The Anatomical Record · doi:10.1002/ar.1091740406 · Cited by 39 · see citing works
Coles, J. A., Myburgh, E., Ritchie, R., Hamilton, A., Rodgers, J., Mottram, J. C., Barrett, M. P., & Brewer, J. M. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003714 · Cited by 39 · see citing works
Fricke, B., von Düring, M., & Andres, K. H. (1996) · Cell and Tissue Research · doi:10.1007/s004410050728 · Cited by 38 · see citing works
5-HT7 receptor-mediated dilatation in the middle meningeal artery of anesthetized rats
Terrón, J. A., & Martínez-García, E. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.01.019 · Cited by 36 · see citing works
Cassella, J. P., Lawrenson, J. G., & Firth, J. A. (1997) · Journal of Neurocytology · doi:10.1023/a:1015438624949 · Cited by 34 · see citing works
5-HT7 Receptors Are Involved in Neurogenic Dural Vasodilatation in an Experimental Model of Migraine
Wang, X., Fang, Y., Liang, J., Yan, M., Hu, R., & Pan, X. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0268-9 · Cited by 28 · see citing works
Contribution of mast cells to injury mechanisms in a mouse model of pediatric traumatic brain injury
Moretti, R., Chhor, V., Bettati, D., Banino, E., Lucia, S. D., Charpentier, T. L., Lebon, S., Schwendimann, L., Pansiot, J., Rasika, S., et al. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23911 · Cited by 28 · see citing works
Jeon, S. G., Kim, K. A., Chung, H., Choi, J., Song, E. J., Han, S. Y., Oh, M. S., Park, J. H., Kim, J.-I., & Moon, M. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.0072 · Cited by 23 · see citing works
Grände, G., Labruijere, S., Haanes, K. A., et al. (2014) · The Journal of Headache and Pain · doi:10.1186/1129-2377-15-22 · Cited by 22 · see citing works
The Involvement of Pial Microvessels in Leukocyte Invasion after Mild Traumatic Brain Injury
Szmydynger-Chodobska, J., Shan, R., Thomasian, N. M., & Chodobski, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167677 · Cited by 22 · see citing works
Differential Gene Expression Associated with Meningeal Injury in Acute Mild Traumatic Brain Injury
Livingston, W. S., Gill, J., Cota, M. R., Olivera, A., O'Keefe, J., Martin, C. G., & Latour, L. L. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2016.4479 · Cited by 18 · see citing works
Watanabe, R., Kakizaki, M., Ikehara, Y., & Togayachi, A. (2016) · Neuropathology · doi:10.1111/neup.12302 · Cited by 17 · see citing works
Normal Anatomy of the Cerebrospinal Fluid Compartment
Hartman, A. L. (2009) · Elsevier eBooks · doi:10.1016/b978-141602908-3.50005-4 · Cited by 14 · see citing works
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Research works printed but not linked: 1
- [16]Cipolla M.J. Anatomy and ultrastructure (Chapter 2) The Cerebral Circulation 2009 Morgan & Claypool Life Sciences 3 11 21452434
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Sorted by citations
Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders
Brioschi, S., Wang, W.-L., Peng, V., Wang, M., Shchukina, I., Greenberg, Z. J., Bando, J. K., Jaeger, N., Czepielewski, R. S., Swain, A., et al. (2021) · Science · doi:10.1126/science.abf9277 · Cited by 472 · see citing works
Alves de Lima, K., Rustenhoven, J., & Kipnis, J. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-102319-103410 · Cited by 348 · see citing works
The anatomy and immunology of vasculature in the central nervous system
Mastorakos, P., & McGavern, D. (2019) · Science Immunology · doi:10.1126/sciimmunol.aav0492 · Cited by 333 · see citing works
Self-citationA Binary Cre Transgenic Approach Dissects Microglia and CNS Border-Associated Macrophages
Kim, J.-S., Kolesnikov, M., Peled-Hajaj, S., Scheyltjens, I., Xia, Y., Trzebanski, S., Haimon, Z., Shemer, A., Lubart, A., Van Hove, H., et al. (2021) · Immunity · doi:10.1016/j.immuni.2020.11.007 · Cited by 176 · see citing works
Microbiota–neuroepithelial signalling across the gut–brain axis
Ohara, T. E., & Hsiao, E. Y. (2025) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01136-9 · Cited by 147 · see citing works
Brain macrophage development, diversity and dysregulation in health and disease
Silvin, A., Qian, J., & Ginhoux, F. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-01053-6 · Cited by 137 · see citing works
Kaushik, D. K., Bhattacharya, A., Mirzaei, R., Rawji, K. S., Ahn, Y., Rho, J. M., & Yong, V. W. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124012 · Cited by 136 · 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
Infection drives meningeal engraftment by inflammatory monocytes that impairs CNS immunity
Rua, R., Lee, J. Y., Silva, A. B., Swafford, I. S., Maric, D., Johnson, K. R., & McGavern, D. B. (2019) · Nature Immunology · doi:10.1038/s41590-019-0344-y · Cited by 123 · see citing works
Self-citationMcMenamin, P. G., Saban, D. R., & Dando, S. J. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.12.002 · Cited by 115 · see citing works
(2020) · International Review of Neurobiology · doi:10.1016/bs.irn.2020.02.006 · Cited by 87 · see citing works
Basal lamina changes in neurodegenerative disorders
Nguyen, B., Bix, G., & Yao, Y. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00502-y · Cited by 75 · see citing works
Immunological defense of CNS barriers against infections
Ampie, L., & McGavern, D. B. (2022) · Immunity · doi:10.1016/j.immuni.2022.04.012 · Cited by 63 · see citing works
Self-citationMeningeal mast cells as key effectors of stroke pathology.
Arac, A., Grimbaldeston, M. A., Galli, S. J., Bliss, T. M., & Steinberg, G. K. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00126 · Cited by 37 · see citing works
Impact of aging on meningeal gene expression
Neutzner, M., Kohler, C., Frank, S., Killer, H. E., & Neutzner, A. (2023) · Fluids and Barriers of the CNS · doi:10.1186/s12987-023-00412-9 · Cited by 17 · see citing works
- Authors
- Rua, R., & McGavern, D. B.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- McGavern, Dorian B.
- ORCID
- McGavern, Dorian B.
- Venue
- Trends in Molecular Medicine
- Publisher
- Elsevier BV
- Published
- 2018-06
- Volume
- 24
- Issue
- 6
- Pages
- 542-559
- ISSN
- 1471-4914 (ISSN-L)
- PMC
- PMC6044730
- OpenAlex
- W2800974699
- Cited by
- 326
- References
- 132
- Citations by year
- 2026: 38 · 2025: 42 · 2024: 52 · 2023: 46 · 2022: 49 · 2021: 38 · 2020: 34 · 2019: 24 · 2018: 2
- FWCI
- 2.32
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Trends in Molecular Medicine (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (ZIANS003112)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Migraine and Headache Studies
- Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
- Keywords
- meningeal immunity, meninges, blood-brain barrier, meningeal immune cells, CNS homeostasis, neuroinflammation, neurological disorders, neurocognitive function
- MeSH terms
- Animals, Central Nervous System, Disease Susceptibility, Homeostasis, Humans, Immune System, Immunity, Meninges, Meningitis
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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