Three or more routes for leukocyte migration into the central nervous system
Abstract
Leukocyte migration into and through tissues is fundamental to normal physiology, immunopathology and host defence. Leukocyte entry into the central nervous system (CNS) is restricted, in part, because of the blood-brain barrier (BBB). During the past decade, crucial components that are involved in the process of leukocyte migration have been identified and progress has been made in understanding the mechanisms of neuroinflammatory reactions. In this review, present knowledge of the trafficking determinants that guide the migration of leukocytes is superimposed onto the vascular and compartmental anatomy of the CNS. We discuss three distinct routes for leukocytes to enter the CNS and consider how different populations of leukocytes use trafficking signals to gain entry.
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Leukocyte recruitment to the CNS is a multistep process regulated through expression of adherent surface molecules on leukocytes and endothelial cells.
“Leukocyte recruitment to the CNS is a multistep process that is regulated through expression of adherent surface molecules on leukocytes and endothelial cells (Ransohoff et al, 2003).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Ransohoff et al, 2003
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Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm
Springer, T. A. (1994) · Cell · doi:10.1016/0092-8674(94)90337-9 · Cited by 7,009 · see citing works
Prevention of experimental autoimmune encephalomyelitis by antibodies against α4βl integrin
Yednock, T. A., Cannon, C., Fritz, L. C., Sánchez‐Madrid, F., Steinman, L., & Karin, N. (1992) · Nature · doi:10.1038/356063a0 · Cited by 1,737 · see citing works
Integrins: Emerging Paradigms of Signal Transduction
Schwartz, M. A., Schaller, M. D., & Ginsberg, M. H. (1995) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cb.11.110195.003001 · Cited by 1,596 · see citing works
Flexible Programs of Chemokine Receptor Expression on Human Polarized T Helper 1 and 2 Lymphocytes
Sallusto, F., Lenig, D., Mackay, C. R., & Lanzavecchia, A. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.6.875 · Cited by 1,535 · see citing works
Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo
Hickey, W. F., & Kimura, H. (1988) · Science · doi:10.1126/science.3276004 · Cited by 1,466 · see citing works
Jaeschke, H. (2002) · Toxicological Sciences · doi:10.1093/toxsci/65.2.166 · Cited by 1,308 · see citing works
A controlled trial of natalizumab for relapsing multiple sclerosis.
Miller, D. H., Khan, O., Sheremata, W., Blumhardt, L., Rice, G., Libonati, M., Willmer-Hulme, A., Dalton, C., Miszkiel, K., & O'Connor, P. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa020696 · Cited by 1,265 · see citing works
α4 integrins mediate lymphocyte attachment and rolling under physiologic flow
Berlin, C., Bargatze, R. F., Campbell, J. J., von Andrian, U. H., Szabo, M. C., Hasslen, S. R., Nelson, R. D., Berg, E. L., Erlandsen, S. L., & Butcher, E. C. (1995) · Cell · doi:10.1016/0092-8674(95)90491-3 · Cited by 1,002 · see citing works
Babbe, H., Roers, A., Waisman, A., Lassmann, H., Goebels, N., Hohlfeld, R., Friese, M., Schröder, R., Deckert, M., Schmidt, S., et al. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.3.393 · Cited by 951 · see citing works
Baron, J. L., Madri, J. A., Ruddle, N. H., Hashim, G. A., & Janeway, C. A. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.177.1.57 · Cited by 834 · see citing works
Molecular physiology and pathophysiology of tight junctions in the blood–brain barrier
Huber, J. D., Egleton, R. D., & Davis, T. P. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)02004-x · Cited by 790 · see citing works
Chemokines as regulators of T cell differentiation
Luther, S. A., & Cyster, J. G. (2001) · Nature Immunology · doi:10.1038/84205 · Cited by 736 · see citing works
A Pathogenic Role for Myelin-Specific Cd8+ T Cells in a Model for Multiple Sclerosis
Huseby, E. S., Liggitt, D., Brabb, T., Schnabel, B., Öhlén, C., & Goverman, J. M. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.5.669 · Cited by 660 · see citing works
Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view
Cserr, H. F., & Knopf, P. M. (1992) · Immunology Today · doi:10.1016/0167-5699(92)90027-5 · Cited by 648 · see citing works
Chemokines in tissue-specific and microenvironment-specific lymphocyte homing
Campbell, J. J., & Butcher, E. C. (2000) · Current Opinion in Immunology · doi:10.1016/s0952-7915(00)00096-0 · Cited by 625 · see citing works
Izikson, L., Klein, R. S., Charo, I. F., Weiner, H. L., & Luster, A. D. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.7.1075 · Cited by 584 · see citing works
Huang, D., Wang, J., Kivisäkk, P., Rollins, B. J., & Ransohoff, R. M. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.6.713 · Cited by 576 · see citing works
Self-citationKivisäkk, 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
Self-citationCXCL13 Is Required for B1 Cell Homing, Natural Antibody Production, and Body Cavity Immunity
Ansel, K. M., Harris, R. B. S., & Cyster, J. G. (2002) · Immunity · doi:10.1016/s1074-7613(01)00257-6 · Cited by 543 · see citing works
Multistep Navigation and the Combinatorial Control of Leukocyte Chemotaxis
Foxman, E. F., Campbell, J. J., & Butcher, E. C. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.5.1349 · Cited by 534 · see citing works
Campbell, J. J., Qin, S., Unutmaz, D., Soler, D. F., Murphy, K. E., Hodge, M. R., Wu, L., & Butcher, E. C. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.11.6477 · Cited by 514 · see citing works
Cc Chemokine Receptor 2 Is Critical for Induction of Experimental Autoimmune Encephalomyelitis
Fife, B. T., Huffnagle, G. B., Kuziel, W. A., & Karpus, W. J. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.6.899 · Cited by 511 · see citing works
Huitinga, I., van Rooijen, N., de Groot, C. J., Uitdehaag, B. M., & Dijkstra, C. D. (1990) · The Journal of experimental medicine · doi:10.1084/jem.172.4.1025 · Cited by 506 · see citing works
Karpus, W. J., Lukacs, N. W., McRae, B. L., Strieter, R. M., Kunkel, S. L., & Miller, S. D. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.10.5003 · Cited by 482 · see citing works
Cytotoxic T lymphocytes in autoimmune and degenerative CNS diseases
Neumann, H. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02154-9 · Cited by 480 · see citing works
Hughes, P. E., & Pfaff, M. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(98)01339-7 · Cited by 436 · see citing works
Flügel, A., Berkowicz, T., Ritter, T., Labeur, M. S., Jenne, D. E., Li, Z., Ellwart, J. W., Willem, M., Lassmann, H., & Wekerle, H. (2001) · Immunity · doi:10.1016/s1074-7613(01)00143-1 · Cited by 431 · see citing works
Neuroinflammation in Alzheimer's disease and prion disease
Eikelenboom, P., Bate, C., van Gool, W. A., Hoozemans, J. J. M., Rozemüller, A. J. M., Veerhuis, R., & Williams, A. (2002) · Glia · doi:10.1002/glia.10146 · Cited by 402 · see citing works
Microglia and inflammatory mechanisms in the clearance of amyloid β peptide
Rogers, J., Strohmeyer, R., Kovelowski, C. J., & Li, R. (2002) · Glia · doi:10.1002/glia.10153 · Cited by 381 · see citing works
A central role for microvillous receptor presentation in leukocyte adhesion under flow
von Andrian, U. H., Hasslen, S. R., Nelson, R. D., Erlandsen, S. L., & Butcher, E. C. (1995) · Cell · doi:10.1016/0092-8674(95)90278-3 · Cited by 370 · see citing works
Hickey, W. F. (1991) · Brain Pathology · doi:10.1111/j.1750-3639.1991.tb00646.x · Cited by 357 · see citing works
Vajkoczy, P., Laschinger, M., & Engelhardt, B. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12440 · Cited by 357 · see citing works
Bone marrow derived elements and resident microglia in brain inflammation
Lassmann, H., Schmied, M. C., Vass, K., & Hickey, W. F. (1993) · Glia · doi:10.1002/glia.440070106 · Cited by 349 · see citing works
Leukocyte traffic in the central nervous system: the participants and their roles
Hickey, W. F. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0168 · Cited by 345 · see citing works
A Functional Role of HLA-G Expression in Human Gliomas: An Alternative Strategy of Immune Escape
Wiendl, H., Mitsdoerffer, M., Hofmeister, V., Wischhusen, J., Bornemann, A., Meyermann, R., Weiss, E. H., Melms, A., & Weller, M. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.9.4772 · Cited by 325 · see citing works
The effect of anti-α4 integrin antibody on brain lesion activity in MS
Tubridy, N. J., Behan, P. O., Capildeo, R., Chaudhuri, A., Forbes, R. B., Hawkins, C. P., Hughes, R. A., Palace, J. A., Sharrack, B., Swingler, R. J., et al. (1999) · Neurology · doi:10.1212/wnl.53.3.466 · Cited by 315 · see citing works
Choroid Plexus in the Central Nervous System: Biology and Physiopathology
Strazielle, N., & Ghersi-Egea, J.-F. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.7.561 · Cited by 307 · see citing works
Echchannaoui, H., Frei, K., Schnell, C., Leib, S. L., Zimmerli, W., & Landmann, R. M. (2002) · The Journal of Infectious Diseases · doi:10.1086/342845 · Cited by 303 · see citing works
Kuchroo, V. K., Martin, C., Greer, J. M., Ju, S.-T., Sobel, R., & Dorf, M. (1993) · Journal of Immunology · doi:10.4049/jimmunol.151.8.4371 · Cited by 300 · see citing works
Graesser, D., Solowiej, A., Bruckner, M., Osterweil, E. K., Juedes, A. E., Davis, S., Ruddle, N. H., Engelhardt, B., & Madri, J. A. (2002) · Journal of Clinical Investigation · doi:10.1172/jci13595 · Cited by 290 · see citing works
Brocke, S., Piercy, C., Steinman, L., Weissman, I. L., & Veromaa, T. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.12.6896 · Cited by 281 · see citing works
Weller, R. O., Kida, S., & Zhang, E. (1992) · Brain Pathology · doi:10.1111/j.1750-3639.1992.tb00704.x · Cited by 279 · see citing works
Transfer of Central Nervous System Autoantigens and Presentation in Secondary Lymphoid Organs
de Vos, A. F., van Meurs, M., Brok, H., Boven, L. A., Hintzen, R. Q., van der Valk, P., Ravid, R., Rensing, S., Boon, L., Hart, B. A. ‘., et al. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.10.5415 · Cited by 278 · see citing works
Graesser, D., Solowiej, A., Bruckner, M., et al. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0213595 · Cited by 275 · see citing works
Huo, Y., Weber, C., Forlow, S. B., Sperandio, M., Thatte, J., Mack, M., Jung, S., Littman, D. R., & Ley, K. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12877 · Cited by 266 · see citing works
Bö, L., Mørk, S. J., Kong, P. A., Nyland, H., Pardo, C. A., & Trapp, B. D. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90075-2 · Cited by 256 · see citing works
Fife, B. T., Kennedy, K. J., Paniagua, M. C., Lukacs, N. W., Kunkel, S. L., Luster, A. D., & Karpus, W. J. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.12.7617 · Cited by 255 · see citing works
Serafini, B., Cabezas, S. C., Rosa, F. D., & Aloisi, F. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64838-9 · Cited by 246 · see citing works
Piccio, L., Rossi, B., Scarpini, E., Laudanna, C., Giagulli, C., Issekutz, A. C., Vestweber, D., Butcher, E. C., & Constantin, G. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.4.1940 · Cited by 245 · see citing works
Two subsets of dendritic cells are present in human cerebrospinal fluid
Pashenkov, M. V., Huang, Y.-M., Kostulas, V., Haglund, M., Söderström, M. B., & Link, H. (2001) · Brain · doi:10.1093/brain/124.3.480 · Cited by 238 · see citing works
Tavares, J. C., Hickey, M. J., Hutchison, J. S., Michaud, J., Sutcliffe, I. T., & Kubes, P. (2000) · Circulation Research · doi:10.1161/01.res.87.12.1141 · Cited by 236 · see citing works
Matyszak, M. K., & Perry, V. H. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00160-1 · Cited by 234 · see citing works
Inflammation in the nervous system
Perry, V. H., Bell, M. D., Brown, H. C., & Matyszak, M. K. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80069-7 · Cited by 229 · see citing works
Weller, R. O. (1998) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199810000-00001 · Cited by 224 · see citing works
Brosnan, C. F., Bornstein, M. B., & Bloom, B. R. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.126.2.614 · Cited by 220 · see citing works
Differential adhesion molecule requirements for immune surveillance and inflammatory recruitment
Carrithers, M. D., Visintin, I., Kang, S. J., & Janeway, C. A. (2000) · Brain · doi:10.1093/brain/123.6.1092 · Cited by 220 · see citing works
Steffen, B. J., Butcher, E. C., & Engelhardt, B. (1994) · PubMed Central · Cited by 215 · see citing works
Weller, R. O., Engelhardt, B., & Phillips, M. J. (1996) · Brain Pathology · doi:10.1111/j.1750-3639.1996.tb00855.x · Cited by 213 · see citing works
Acute experimental autoimmune encephalomyelitis in mice
Linthicum, D. S., Munoz, J. J., & Blaskett, A. (1982) · Cellular Immunology · doi:10.1016/0008-8749(82)90457-9 · Cited by 210 · see citing works
Kerfoot, S. M., & Kubes, P. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.2.1000 · Cited by 210 · see citing works
Kielian, T., Barry, B. J., & Hickey, W. F. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.7.4634 · Cited by 208 · see citing works
Microglia in human immunodeficiency virus‐associated neurodegeneration
Garden, G. A. (2002) · Glia · doi:10.1002/glia.10155 · Cited by 206 · see citing works
Hyduk, S. J., Karlik, S. J., Cannon, C., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00165-k · Cited by 203 · see citing works
Engelhardt, B., Laschinger, M., Schulz, M., Samulowitz, U., Vestweber, D., & Hoch, G. (1998) · Journal of Clinical Investigation · doi:10.1172/jci4271 · Cited by 203 · see citing works
Knopf, P. M., Harling‐Berg, C. J., Cserr, H. F., Basu, D., Sirulnick, E. J., Nolan, S. C., Park, J. T., Keir, G., Thompson, E. J., & Hickey, W. F. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.2.692 · Cited by 193 · see citing works
Yoneyama, H., Narumi, S., Zhang, Y., Murai, M., Baggiolini, M., Lanzavecchia, A., Ichida, T., Asakura, H., & Matsushima, K. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011983 · Cited by 192 · see citing works
Martínez‐Lorenzo, M. J., Álava, M. A., Gamen, S., Kim, K. J., Chuntharapai, A., Piñeiro, A., Naval, J., & Anel, A. (1998) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199809)28:09 · Cited by 182 · see citing works
Archelos, J. J., Jung, S., Mäurer, M., Schmied, M. C., Lassmann, H., Tamatani, T., Miyasaka, M., Toyka, K. V., & Hartung, H. (1993) · Annals of Neurology · doi:10.1002/ana.410340209 · Cited by 180 · see citing works
Engelhardt, B., Vestweber, D., Hallmann, R., & Schulz, M. (1997) · Blood · doi:10.1182/blood.v90.11.4459 · Cited by 175 · see citing works
Fischer, H., Bonifas, U., & Reichmann, G. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.9.4826 · Cited by 162 · see citing works
Anthony, D. C., Dempster, R., Fearn, S., Clements, J. M., Wells, G., Perry, V. H., & Walker, K. M. (1998) · Current Biology · doi:10.1016/s0960-9822(07)00373-9 · Cited by 161 · see citing works
Rickert, C. H., & Paulus, W. (2000) · Microscopy Research and Technique · doi:10.1002/1097-0029(20010101)52:1 · Cited by 160 · see citing works
In Situ Tolerance within the Central Nervous System as a Mechanism for Preventing Autoimmunity
Brabb, T., von Dassow, P., Ordonez, N., Schnabel, B., Duke, B., & Goverman, J. M. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.6.871 · Cited by 159 · see citing works
Tani, M., Fuentes, M. E., Peterson, J. W., Trapp, B. D., Durham, S. K., Loy, J. K., Bravo, R., Ransohoff, R. M., & Lira, S. A. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118821 · Cited by 157 · see citing works
Self-citationLee, S. C., Moore, G. R. W., Golenwsky, G., & Raine, C. S. (1990) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199003000-00005 · Cited by 149 · see citing works
Kivisäkk, P., Trebst, C., Liu, Z., Tucky, B. H., Sørensen, T. L., Rudick, R. A., Mack, M., & Ransohoff, R. M. (2002) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2002.01947.x · Cited by 142 · see citing works
Self-citationBoulton, M., Flessner, M. F., Armstrong, D. W., Mohamed, R., Hay, J. B., & Johnston, M. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.3.r818 · Cited by 140 · see citing works
Dendritic cells at the host-pathogen interface
Kelsall, B. L., Biron, C. A., Sharma, O. K., & Kaye, P. M. (2002) · Nature Immunology · doi:10.1038/ni0802-699 · Cited by 138 · see citing works
Cytokine-induced meningitis is dramatically attenuated in mice deficient in endothelial selectins.
Tang, T., Frenette, P. S., Hynes, R. O., Wagner, D. D., & Mayadas, T. N. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118695 · Cited by 135 · see citing works
Richards, D. F., Fernandez, M., Caulfield, J., & Hawrylowicz, C. M. (2000) · European Journal of Immunology · doi:10.1002/1521-4141(2000)30:8 · Cited by 133 · see citing works
Lymphocyte phenotype and subset distribution in normal cerebrospinal fluid
Svenningsson, A., Andersen, O., Edsbagge, M., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(95)00126-3 · Cited by 125 · see citing works
Stein, J. V., Cheng, G., Stockton, B. M., Fors, B. P., Butcher, E. C., & von Andrian, U. H. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.1.37 · Cited by 121 · see citing works
Ma, M., Wei, T., Boring, L. F., Charo, I. F., Ransohoff, R. M., & Jakeman, L. B. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10269 · Cited by 118 · see citing works
Self-citationGordon, E. J., Myers, K. J., Dougherty, J. P., Rosen, H., & Ron, Y. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(95)00120-2 · Cited by 116 · see citing works
Svenningsson, A., Hansson, G. K., Andersen, O., et al. (1993) · Annals of Neurology · doi:10.1002/ana.410340210 · Cited by 115 · see citing works
Theien, B. E., Vanderlugt, C. L., Eagar, T. N., Nickerson‐Nutter, C. L., Nazareno, R., Kuchroo, V. K., & Miller, S. D. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11717 · Cited by 112 · see citing works
Dendritic cells and dendritic-like microglia in focal cortical ischemia of the mouse brain
Reichmann, G., Schroeter, M., Jander, S., & Fischer, H. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00184-4 · Cited by 110 · see citing works
Anti-adhesion molecule therapy in experimental autoimmune encephalomyelitis
Cannella, B., Cross, A. H., & Raine, C. S. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90232-n · Cited by 104 · see citing works
Functional capacity of solid tissue transplants in the brain: evidence for immunological privilege
Head, J. R., & Griffin, W. S. T. (1985) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1985.0039 · Cited by 102 · see citing works
Recruitment of dendritic cells to the cerebrospinal fluid in bacterial neuroinfections
Pashenkov, M. V., Teleshova, N., Kouwenhoven, M. C. M., Смирнова, Т. А., Jin, Y.-P., Kostulas, V., Huang, Y.-M., Pinegin, B. V., Boiko, A. N., & Link, H. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(01)00451-9 · Cited by 95 · see citing works
Very late antigen 4 (VLA4) antagonists as anti-inflammatory agents
Lin, K., & Castro, A. C. (1998) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(98)80120-8 · Cited by 94 · see citing works
Blurton-Jones, M. M., Roberts, J. A., & Tuszynski, M. H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990322)405:4 · Cited by 94 · see citing works
Zeine, R. R., & Owens, T. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90213-5 · Cited by 92 · see citing works
Widner, H., Möller, G., & JOHANSSON, B. B. (1988) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.1988.tb01488.x · Cited by 91 · see citing works
β7 integrins contribute to demyelinating disease of the central nervous system
Kanwar, J. R., Harrison, J. E. B., Wang, D., Leung, E. Y., Müller, W., Wagner, N., & Krissansen, G. W. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00245-3 · Cited by 91 · see citing works
Cardona, A. E., Restrepo, B. I., Jaramillo, J. M., & Teale, J. M. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.2.995 · Cited by 89 · see citing works
Cardona, A. E., Restrepo, B. I., Jaramillo, J. M., & Teale, J. M. (1999) · PubMed · Cited by 86 · see citing works
Dopp, J. M., Breneman, S. M., & Olschowka, J. A. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90239-9 · Cited by 84 · see citing works
The inflammatory response in the CNS
Perry, V. H., & Andersson, P.-B. (1992) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1992.tb00811.x · Cited by 84 · see citing works
Rajan, A. J., Asensio, V. C., Campbell, I. L., & Brosnan, C. F. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.4.2120 · Cited by 83 · see citing works
Kielian, T., & Hickey, W. F. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64575-0 · Cited by 82 · see citing works
Role of genetic background in P selectin-dependent immune surveillance of the central nervous system
Carrithers, M. D., Visintin, I., Viret, C., & Janeway, C. A. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00172-8 · Cited by 80 · see citing works
Grewal, I. S., Foellmer, H. G., Grewal, K. D., Wang, H., Lee, W. P., Tumas, D. B., Janeway, C. A., & Flavell, R. A. (2001) · Immunity · doi:10.1016/s1074-7613(01)00110-8 · Cited by 76 · see citing works
Brennan, F. R., O'Neill, J. K., Allen, S. J., Butter, C., Nuki, G., & Baker, D. (1999) · Immunology · doi:10.1046/j.1365-2567.1999.00894.x · Cited by 75 · see citing works
Welsh, C. T., ROSE, J. W., Hill, K. E., et al. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90087-f · Cited by 72 · see citing works
Willenborg, D. O., Simmons, R. D., Tamatani, T., et al. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90175-x · Cited by 72 · see citing works
Kanwar, J. R., Kanwar, R. K., Wang, D., et al. (2000) · Immunology and Cell Biology · doi:10.1046/j.1440-1711.2000.00947.x · Cited by 63 · see citing works
Keszthelyi, E., Karlik, S. J., Hyduk, S. J., et al. (1996) · Neurology · doi:10.1212/wnl.47.4.1053 · Cited by 60 · see citing works
Skundric, D. S., Kim, C., Tse, H. Y., et al. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90240-y · Cited by 57 · see citing works
Kobayashi, Y., Kawai, K., Honda, H., et al. (1995) · Cellular Immunology · doi:10.1006/cimm.1995.1173 · Cited by 55 · see citing works
Bell, M. D., Taub, D. D., Kunkel, S. L., Strieter, R. M., Foley, R., Gauldie, J., & Perry, V. H. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01324.x · Cited by 51 · see citing works
Qing, Z., Sándor, M., Radvány, Z., et al. (2001) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/60.8.798 · Cited by 49 · see citing works
Cardona, A. E., & Teale, J. M. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.6.3163 · Cited by 46 · see citing works
Experimental Autoimmune Encephalomyelitis in Intercellular Adhesion Molecule-1-Deficient Mice
Samoilova, E. B., Horton, J. L., & Chen, Y. (1998) · Cellular Immunology · doi:10.1006/cimm.1998.1395 · Cited by 35 · see citing works
Chemokines and atherosclerosis: what Adam Smith has to say about vascular disease
Rollins, B. J. (2001) · Journal of Clinical Investigation · doi:10.1172/jci14273 · Cited by 30 · see citing works
Gao, Y., Rajan, A. J., Raine, C. S., & Brosnan, C. F. (2001) · Journal of Autoimmunity · doi:10.1006/jaut.2001.0547 · Cited by 30 · see citing works
Stat6 activation and Th2 cell proliferation driven by CD28 signals
Oki, S., Otsuki, N., Kohsaka, T., & Azuma, M. (2000) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(200005)30:5 · Cited by 25 · see citing works
Analysis of CD27 surface expression on T cell subsets in MS patients and control individuals
Hintzen, R. Q., Fiszer, U., Fredrikson, S., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00137-d · Cited by 25 · see citing works
Massacesi, L. (2002) · Clinical Neurology and Neurosurgery · doi:10.1016/s0303-8467(02)00035-5 · Cited by 19 · see citing works
Uncoupling of virus-induced inflammation and anti-viral immunity in the brain parenchyma
Stevenson, P. G., Austyn, J. M., & Hawke, S. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-7-1735 · Cited by 13 · see citing works
T cell approach to demyelinating diseases
Wekerle, H., & Fierz, W. (1985) · Springer Seminars in Immunopathology · doi:10.1007/bf00197249 · Cited by 11 · see citing works
Short peptides sensitize target cells to CTL specific for the MHC class Ib molecule, H2-M3
Dabhi, V. M., & Fischer Lindahl, K. (1998) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199811)28:11
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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
“Both lymphocytes and antigen-presenting cells in the subarachnoid CSF (49) may detect interstitial antigens delivered to the CSF by paravenous bulk outflow.”
BackgroundThe Blood-Brain Barrier in Health and Chronic Neurodegenerative Disorders
Zlokovic, B. V. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.003 · Cited by 3,280 · see citing works
The many roles of chemokines and chemokine receptors in inflammation
Charo, I. F., & Ransohoff, R. M. (2006) · New England Journal of Medicine · doi:10.1056/nejmra052723 · Cited by 2,523 · see citing works
Self-citationThe role of inflammation in epilepsy
Vezzani, A., French, J., Bartfai, T., & Baram, T. Z. (2011) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.178 · Cited by 1,876 · see citing works
Serafini, B., Rosicarelli, B., Magliozzi, R., Stigliano, E., & Aloisi, F. (2004) · Brain Pathology · doi:10.1111/j.1750-3639.2004.tb00049.x · Cited by 1,208 · see citing works
Reboldi, A., Coisne, C., Baumjohann, D., Benvenuto, F., Bottinelli, D., Lira, S., Uccelli, A., Lanzavecchia, A., Engelhardt, B., & Sallusto, F. (2009) · Nature Immunology · doi:10.1038/ni.1716 · Cited by 1,206 · 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
The blood-brain barrier in Alzheimer’s disease
Zenaro, E., Piacentino, G., & Constantin, G. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.07.007 · Cited by 767 · see citing works
Revisiting the Mechanisms of CNS Immune Privilege
Louveau, A., Harris, T. H., & Kipnis, J. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.08.006 · Cited by 682 · see citing works
The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective
Shaftel, S. S., Griffin, W. S. T., & O'Banion, M. K. (2008) · Journal of Neuroinflammation · doi:10.1186/1742-2094-5-7 · Cited by 565 · see citing works
The immune response in autism: a new frontier for autism research
Ashwood, P., Wills, S., & Van de Water, J. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.1205707 · Cited by 528 · see citing works
Brain endothelial cells and the glio-vascular complex
Wolburg, H., Noell, S., Mack, A., Wolburg-Buchholz, K., & Fallier-Becker, P. (2009) · Cell and Tissue Research · doi:10.1007/s00441-008-0658-9 · Cited by 438 · see citing works
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Larochelle, C., Alvarez, J. I., & Prat, A. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.04.066 · Cited by 405 · see citing works
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Rustenhoven, J., Jansson, D., Smyth, L. C., & Dragunow, M. (2017) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.12.001 · Cited by 371 · see citing works
Schwartz, M., & Baruch, K. (2014) · The EMBO Journal · doi:10.1002/embj.201386609 · Cited by 349 · 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
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Emerging roles of innate and adaptive immunity in Alzheimer’s disease
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Dickens, A. M., Tovar-y-Romo, L. B., Yoo, S.-W., Trout, A. L., Bae, M., Kanmogne, M., Megra, B., Williams, D. W., Witwer, K. W., Gacias, M., et al. (2017) · Science Signaling · doi:10.1126/scisignal.aai7696 · Cited by 285 · see citing works
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Weber, M. D., Godbout, J. P., & Sheridan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.102 · Cited by 283 · see citing works
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Michaud, J.-P., Bellavance, M.-A., Préfontaine, P., & Rivest, S. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.10.010 · Cited by 257 · see citing works
Perivascular spaces—MRI marker of inflammatory activity in the brain?
Wuerfel, J., Haertle, M., Waiczies, H., Tysiak, E., Bechmann, I., Wernecke, K. D., Zipp, F., & Paul, F. (2008) · Brain · doi:10.1093/brain/awn171 · Cited by 244 · see citing works
The blood-brain barrier, chemokines and multiple sclerosis
Holman, D. W., Klein, R. S., & Ransohoff, R. M. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.07.019 · Cited by 247 · see citing works
Self-citationShaftel, S. S., Carlson, T. J., Olschowka, J. A., Kyrkanides, S., Matousek, S. B., & O'Banion, M. K. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1418-07.2007 · Cited by 243 · see citing works
Systemic inflammatory cells fight off neurodegenerative disease
Schwartz, M., & Shechter, R. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.71 · Cited by 240 · see citing works
Cazareth, J., Guyon, A., Heurteaux, C., Chabry, J., & Petit-Paitel, A. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-132 · Cited by 206 · see citing works
Jin, X., Ishii, H., Bai, Z., Itokazu, T., & Yamashita, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041892 · Cited by 211 · see citing works
McCandless, E. E., Piccio, L., Woerner, B. M., Schmidt, R. E., Rubin, J. B., Cross, A. H., & Klein, R. S. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.070918 · Cited by 206 · see citing works
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Kaur, C., Rathnasamy, G., & Ling, E.-A. (2016) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlv030 · Cited by 176 · see citing works
Zhou, H., Andonegui, G., Wong, C. H. Y., & Kubes, P. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901309 · Cited by 174 · see citing works
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Woelfer, M., Kasties, V., Kahlfuss, S., & Walter, M. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.034 · Cited by 171 · see citing works
Waclawiková, B., & El Aidy, S. (2018) · Pharmaceuticals · doi:10.3390/ph11030063 · Cited by 172 · see citing works
Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity
Klein, R. S., & Rubin, J. B. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.04.002 · Cited by 132 · 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
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Lewitus, G. M., Cohen, H., & Schwartz, M. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.05.002 · Cited by 123 · see citing works
Regulation of astrocyte glutamine synthetase in epilepsy
Eid, T., Tu, N., Lee, T.-S. W., & Lai, J. C. K. (2013) · Neurochemistry International · doi:10.1016/j.neuint.2013.06.008 · Cited by 109 · see citing works
The Association and Linkage of the HLA-A2 Class I Allele with Autism
Torres, A. R., Sweeten, T. L., Cutler, A., Bedke, B. J., Fillmore, M., Stubbs, E. G., & Odell, D. (2006) · Human Immunology · doi:10.1016/j.humimm.2006.01.001 · Cited by 104 · see citing works
Microglia in Alzheimer's Disease: It's All About Context
Weitz, T. M., & Town, T. (2012) · International Journal of Alzheimer's Disease · doi:10.1155/2012/314185 · Cited by 95 · see citing works
Brambilla, P., Bellani, M., Isola, M., Bergami, A., Marinelli, V, Dusi, N., Rambaldelli, G., Tansella, M., Maria Finardi, A., Martino, G., et al. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.46 · Cited by 86 · see citing works
Tabor-Godwin, J. M., Ruller, C. M., Bagalso, N., An, N., Pagarigan, R. R., Harkins, S., Gilbert, P. E., Kiosses, W. B., Gude, N. A., Cornell, C. T., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1860-10.2010 · Cited by 84 · see citing works
Keller, C. W., Sina, C., Kotur, M. B., Ramelli, G., Mundt, S., Quast, I., Ligeon, L.-A., Weber, P., Becher, B., Münz, C., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713664114 · Cited by 81 · see citing works
Narayan, N., Mandhair, H., Smyth, E., Dakin, S. G., Kiriakidis, S., Wells, L., Owen, D., Sabokbar, A., & Taylor, P. (2017) · PLOS ONE · doi:10.1371/journal.pone.0185767 · Cited by 79 · see citing works
Sun, N., Hu, H., Wang, F., Li, L., Zhu, W., Shen, Y., Xiu, J., & Xu, Q. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.11.032 · Cited by 75 · see citing works
Baker, S. K., Chen, Z.-L., Norris, E. H., Revenko, A. S., MacLeod, A. R., & Strickland, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1811172115 · Cited by 68 · 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
Engler, H., Doenlen, R., Riether, C., Engler, A., Niemi, M.-B., Besedovsky, H. O., Rey, A. D., Pacheco-López, G., Feldon, J., & Schedlowski, M. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2009.01.018 · Cited by 59 · see citing works
Yang, Y.-M., Shang, D.-S., Zhao, W.-D., Fang, W.-G., & Chen, Y.-H. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1138-5 · Cited by 57 · 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
Neurons under viral attack: Victims or warriors?
Chakraborty, S., Nazmi, A., Dutta, K., & Basu, A. (2010) · Neurochemistry International · doi:10.1016/j.neuint.2010.02.016 · Cited by 42 · see citing works
Puccini, J. M., Ruller, C. M., Robinson, S. M., Knopp, K. A., Buchmeier, M. J., Doran, K. S., & Feuer, R. (2014) · Laboratory Investigation · doi:10.1038/labinvest.2013.138 · Cited by 24 · see citing works
Virus infection as a cause of inflammation in psychiatric disorders
Bechter, K. (2013) · Modern trends in psychiatry · doi:10.1159/000343967 · Cited by 16 · see citing works
- Authors
- Ransohoff, R. M., Kivisäkk, P., & Kidd, G.
- Affiliations
- Cleveland Clinic (US)
- Corresponding author
- Ransohoff, Richard M.
- Venue
- Nature Reviews Immunology
- Published
- 2003-07
- Volume
- 3
- Issue
- 7
- Pages
- 569-581
- ISSN
- 1474-1733 (ISSN-L)
- 1474-1741
- OpenAlex
- W1977899668
- Cited by
- 1,052
- References
- 123
- Citations by year
- 2026: 12 · 2025: 26 · 2024: 33 · 2023: 36 · 2022: 36 · 2021: 45 · 2020: 36 · 2019: 32 · 2018: 43 · 2017: 55 · 2016: 47 · 2015: 46 · 2014: 73 · 2013: 64 · 2012: 60
- FWCI
- 5.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature reviews. Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- leukocyte migration, central nervous system, blood-brain barrier, neuroinflammation, chemokines, immune privilege
- MeSH terms
- Animals, Cell Movement, Central Nervous System, Cerebrospinal Fluid, Encephalomyelitis, Autoimmune, Experimental, Humans, Immunologic Surveillance, Killer Cells, Natural, Lymphocytes, Neutrophils, Phagocytes, Spinal Cord, Receptors, Antigen, T-Cell, gamma-delta, CD8-Positive T-Lymphocytes
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