Potential role of MCP-1 in endothelial cell tight junction `opening': signaling via Rho and Rho kinase
Abstract
The expression of the monocyte chemoattractant protein-1 (MCP-1) receptor CCR2 by brain endothelial cells suggests that MCP-1 may have other functions than purely driving leukocyte migration into brain parenchyma during inflammation. This study examines one of these potential novel roles of MCP-1 regulation of endothelial permeability using primary cultures of mouse brain endothelial cells. MCP-1 induces reorganization of actin cytoskeleton (stress fiber formation) and redistribution of tight junction proteins, ZO-1, ZO-2 occludin and claudin-5, from the Triton X-100-soluble to the Triton X-100-insoluble fractions. These morphological changes are associated with a decrease in transendothelial electrical membrane resistance and an increase in [14C]inulin permeability. MCP-1 did not induce these events in brain endothelial cells prepared from mice genotype CCR2-/-. The Rho kinase inhibitor Y27632 and inhibition of Rho (C3 exoenzyme, and dominant negative mutant of Rho, RhoT19N) prevented MCP-1-induced stress fiber assembly, reorganization of tight junction proteins and alterations in endothelial permeability. In all, this suggests that a small GTPase Rho and Rho kinase have a pivotal role in MCP-1-induced junction disarrangement. These data are the first to strongly suggest that MCP-1, via CCR2 present on brain endothelial cells, contributes to increased brain endothelial permeability.
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Etienne‐Manneville, S., & Hall, A. (2002) · Nature · doi:10.1038/nature01148 · Cited by 4,796 · see citing works
Regulation of Myosin Phosphatase by Rho and Rho-Associated Kinase (Rho-Kinase)
Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., et al. (1996) · Science · doi:10.1126/science.273.5272.245 · Cited by 2,889 · see citing works
Phosphorylation and Activation of Myosin by Rho-associated Kinase (Rho-kinase)
Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., & Kaibuchi, K. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.34.20246 · Cited by 2,009 · see citing works
Rollins, B. J. (1997) · Blood · doi:10.1182/blood.v90.3.909 · Cited by 1,983 · see citing works
Boring, L., Gosling, J., Cleary, M., & Charo, I. F. (1998) · Nature · doi:10.1038/29788 · Cited by 1,965 · see citing works
Martín-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A., et al. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.1.117 · Cited by 1,387 · see citing works
The Molecular Biology of Leukocyte Chemoattractant Receptors
Murphy, P. M. (1994) · Annual Review of Immunology · doi:10.1146/annurev.iy.12.040194.003113 · Cited by 1,197 · see citing works
THE CELL BIOLOGY OF THE BLOOD-BRAIN BARRIER
Rubin, L. L., & Staddon, J. M. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.11 · Cited by 1,005 · see citing works
Signalling to and from tight junctions
Matter, K., & Balda, M. S. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1055 · Cited by 887 · see citing works
Rosenberg, G. A., Estrada, E. Y., & Dencoff, J. E. (1998) · Stroke · doi:10.1161/01.str.29.10.2189 · Cited by 861 · see citing works
Salcedo, R., Ponce, M. L., Young, H. A., Wasserman, K., Ward, J. M., Kleinman, H. K., Oppenheim, J. J., & Murphy, W. J. (2000) · Blood · doi:10.1182/blood.v96.1.34 · Cited by 860 · see citing works
Oxidant stress and endothelial cell dysfunction
Lum, H., & Roebuck, K. A. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.280.4.c719 · Cited by 832 · see citing works
Inflammatory Mediators and Modulation of Blood–Brain Barrier Permeability
Abbott, N. J. (2000) · Cellular and Molecular Neurobiology · doi:10.1023/a:1007074420772 · Cited by 803 · 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
Rho family proteins: coordinating cell responses
Ridley, A. J. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02153-5 · Cited by 767 · 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
MOLECULAR ARCHITECTURE OF TIGHT JUNCTIONS
Mitic, L. L., & Anderson, J. M. (1998) · Annual Review of Physiology · doi:10.1146/annurev.physiol.60.1.121 · Cited by 721 · see citing works
The chemokine system: redundancy for robust outputs
Mantovani, A. (1999) · Immunology Today · doi:10.1016/s0167-5699(99)01469-3 · Cited by 703 · see citing works
Possible Involvement of Phosphorylation of Occludin in Tight Junction Formation
Sakakibara, A., Furuse, M., Saitou, M., Ando‐Akatsuka, Y., & Tsukita, S. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.6.1393 · Cited by 590 · see citing works
Phosphorylation of Myosin-Binding Subunit (Mbs) of Myosin Phosphatase by Rho-Kinase in Vivo
Kawano, Y., Fukata, Y., Oshiro, N., Amano, M., Nakamura, T., Ito, M., Matsumura, F., Inagaki, M., & Kaibuchi, K. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.5.1023 · Cited by 570 · see citing works
Huot, J., Houle, F., Marceau, F., & Landry, J. (1997) · Circulation Research · doi:10.1161/01.res.80.3.383 · Cited by 567 · see citing works
Fey, E. G., Wan, K. M., & Penman, S. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.6.1973 · Cited by 542 · see citing works
Ransohoff, R. M., Hamilton, T. A., Tani, M., Stoler, M. H., Shick, H. E., Major, J. A., Estes, M. L., Thomas, D. M., & Tuohy, V. K. (1993) · The FASEB Journal · doi:10.1096/fasebj.7.6.8472896 · Cited by 496 · see citing works
Regulation of vascular endothelial barrier function
Lum, H., & Malik, A. B. (1994) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1994.267.3.l223 · Cited by 471 · see citing works
Activation of RhoA by Thrombin in Endothelial Hyperpermeability
Amerongen, G. P. V. N., van Delft, S., Vermeer, M. A., Collard, J. G., & van Hinsbergh, V. W. M. (2000) · Circulation Research · doi:10.1161/01.res.87.4.335 · Cited by 410 · see citing works
Molecular structure and assembly of the tight junction
Denker, B. M., & Nigám, S. K. (1998) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.1998.274.1.f1 · Cited by 405 · see citing works
Proteolytic Cascade Enzymes Increase in Focal Cerebral Ischemia in Rat
Rosenberg, G. A., Navratil, M., Barone, F. C., & Feuerstein, G. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199605000-00002 · Cited by 403 · see citing works
Expression of chemokine receptors by subsets of neurons in the central nervous system
Horuk, R., Martin, A. W., Wang, Z., Schweitzer, L., Gerassimides, A., Guo, H.-D., Lu, Z., Hesselgesser, J., Perez, H. D., Kim, J., et al. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.6.2882 · Cited by 385 · see citing works
Uguccioni, M., D’Apuzzo, M., Loetscher, M., Dewald, B., & Baggiolini, M. (1995) · European Journal of Immunology · doi:10.1002/eji.1830250113 · Cited by 346 · see citing works
Youakim, A., & Ahdieh, M. (1999) · American Journal of Physiology - Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1999.276.5.g1279 · Cited by 340 · see citing works
Fujimura, M., Gasche, Y., Morita‐Fujimura, Y., Massengale, J. L., 川瀬, 誠., & Chan, P. H. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01843-0 · Cited by 339 · see citing works
Rho/Rho-kinase mediated signaling in physiology and pathophysiology
Wettschureck, N., & Offermanns, S. (2002) · Journal of Molecular Medicine · doi:10.1007/s00109-002-0370-2 · Cited by 335 · see citing works
Rho-Kinase–Mediated Contraction of Isolated Stress Fibers
Katoh, K., Kano, Y., Amano, M., Onishi, H., Kaibuchi, K., & Fujiwara, K. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.153.3.569 · Cited by 331 · see citing works
Monocyte Chemoattractant Protein-1
Gu, L., Tseng, S., & Rollins, B. J. (1999) · KARGER eBooks · doi:10.1159/000058723 · Cited by 326 · see citing works
Calcium Modulation of Adherens and Tight Junction Function
Brown, R. C., & Davis, T. P. (2002) · Stroke · doi:10.1161/01.str.0000016405.06729.83 · Cited by 320 · see citing works
Hirase, T., Kawashima, S., Wong, E. Y. M., Ueyama, T., Rikitake, Y., Tsukita, S., Yokoyama, M., & Staddon, J. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007136200 · Cited by 312 · see citing works
Glabinski, A. R., Balasingam, V., Tani, M., Kunkel, S. L., Strieter, R. M., Yong, V. W., & Ransohoff, R. M. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.11.4363 · Cited by 309 · see citing works
Rotrosen, D., & Gallin, J. I. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.6.2379 · Cited by 297 · see citing works
Regulation of Airway Tight Junctions by Proinflammatory Cytokines
Coyne, C. B., Vanhook, M. K., Gambling, T. M., Carson, J. L., Boucher, R. C., & Johnson, L. G. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-03-0134 · Cited by 292 · see citing works
Wang, W., Dentler, W. L., & Borchardt, R. T. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.1.h434 · Cited by 288 · see citing works
Expression of CCR2 by Endothelial Cells
Weber, K. S. C., Nelson, P. J., Gröne, H., & Weber, C. (1999) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.19.9.2085 · Cited by 280 · see citing works
IL-8 activates endothelial cell CXCR1 and CXCR2 through Rho and Rac signaling pathways
Schraufstätter, I. U., Chung, J., & Burger, M. (2001) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2001.280.6.l1094 · Cited by 278 · see citing works
Chemokines and chemokine receptors in the CNS: a possible role in neuroinflammation and patterning
Mennicken, F., Maki, R. A., Souza, E. B. D., & Quirion, R. (1999) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(99)01308-5 · Cited by 276 · see citing works
Increased endothelial albumin permeability mediated by protein kinase C activation.
Lynch, J. J., Ferro, T. J., Blumenstock, F. A., Brockenauer, A. M., & Malik, A. B. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114663 · Cited by 266 · see citing works
Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression
Huber, J. D., Witt, K. A., Hom, S., Egleton, R. D., Mark, K. S., & Davis, T. P. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.3.h1241 · Cited by 266 · see citing works
Regulated assembly of tight junctions by protein kinase C.
Stuart, R. O., & Nigám, S. K. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.13.6072 · Cited by 265 · see citing works
Transient and Prolonged Increase in Endothelial Permeability Induced by Histamine and Thrombin
Amerongen, G. P. V. N., Draijer, R., Vermeer, M. A., & van Hinsbergh, V. W. M. (1998) · Circulation Research · doi:10.1161/01.res.83.11.1115 · Cited by 265 · see citing works
ICAM-1 Signaling Pathways Associated with Rho Activation in Microvascular Brain Endothelial Cells
Etienne‐Manneville, S., Adamson, P., Greenwood, J., Strosberg, A. D., Cazaubon, S. M., & Couraud, P. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.10.5755 · Cited by 248 · see citing works
Blamire, A. M., Anthony, D. C., Rajagopalan, B., Sibson, N. R., Perry, V. H., & Styles, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08153.2000 · Cited by 245 · see citing works
Molecular and cellular permeability control at the blood-brain barrier
Gloor, S. M., Wachtel, M., Bolliger, M. F., Ishihara, H., Landmann, R., & Frei, K. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00102-3 · Cited by 244 · see citing works
Vouret‐Craviari, V., Boquet, P., Pouysségur, J., & Obberghen‐Schilling, E. V. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.9.2639 · Cited by 241 · see citing works
H 2 O 2 -mediated permeability: role of MAPK and occludin
Kevil, C. G., Oshima, T., Alexander, B., Coe, L. L., & Alexander, J. S. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.1.c21 · Cited by 222 · see citing works
Hulkower, K. I., Brosnan, C. F., Aquino, D. A., Cammer, W., Kulshrestha, S., Guida, M. P., Rapoport, D. A., & Berman, J. W. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.150.6.2525 · Cited by 215 · see citing works
Moy, A. B., Engelenhoven, J. V., Bodmer, J. E., Kamath, J., Keese, C. R., Giæver, I., Shasby, S. S., & Shasby, D. M. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118493 · Cited by 204 · see citing works
Benais-Pont, G., Punn, A., Flores-Maldonado, C., Eckert, J. J., Raposo, G., Fleming, T. P., Cereijido, M., Balda, M. S., & Matter, K. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200211047 · Cited by 202 · see citing works
Novel lymphocyte-specific CC chemokines and their receptors
Yoshie, O., Imai, T., & Nomiyama, H. (1997) · Journal of Leukocyte Biology · doi:10.1002/jlb.62.5.634 · Cited by 199 · see citing works
Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins
Tsukamoto, T., & Nigám, S. K. (1999) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.1999.276.5.f737 · Cited by 198 · see citing works
Tsukamoto, T., & Nigám, S. K. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.26.16133 · Cited by 191 · see citing works
Oshima, T., Laroux, F. S., Coe, L. L., Morise, Z., Kawachi, S., Bauer, P. R., Grisham, M. B., Specian, R. D., Carter, P., Jennings, S. R., et al. (2001) · Microvascular Research · doi:10.1006/mvre.2000.2288 · Cited by 190 · see citing works
Ahdieh, M., VandenBos, T., & Youakim, A. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.281.6.c2029 · Cited by 183 · see citing works
Bell, M. D., Taub, D. D., & Perry, V. H. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00083-8 · Cited by 178 · see citing works
Banisadr, G., Quéraud-LeSaux, F., Boutterin, M., Pélaprat, D., Zalc, B., Rostène, W. H., Haour, F., & Parsadaniantz, S. M. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00809.x · Cited by 177 · see citing works
Histamine increases venular permeability via a phospholipase C-NO synthase-guanylate cyclase cascade
Yuan, Y., Granger, H. J., Zawieja, D. C., DeFily, D. V., & Chilian, W. M. (1993) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1993.264.5.h1734 · Cited by 173 · see citing works
Farshori, P. (1999) · The Journal of Membrane Biology · doi:10.1007/s002329900544 · Cited by 167 · see citing works
Regulation of endothelial cell gap formation and paracellular permeability.
Garcia, J., & Schaphorst, K. L. (1995) · PubMed · Cited by 162 · see citing works
Stasek, J. E., Patterson, C. E., & Garcia, J. G. N. (1992) · Journal of Cellular Physiology · doi:10.1002/jcp.1041530110 · Cited by 161 · see citing works
Vascular endothelial adhesion molecules and tissue inflammation.
Malik, A. B., & Lo, S. K. (1996) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)06941-8 · Cited by 160 · see citing works
Chemokines and chemotaxis of leukocytes in infectious meningitis
Lahrtz, F., Piali, L., Spanaus, K. S., Seebach, J. D., & Fontana, A. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00267-1 · Cited by 155 · see citing works
Matsumoto, T., Ikeda, K., Mukaida, N., Harada, A., Matsumoto, Y., Yamashita, J., & Matsushima, K. (1997) · PubMed · Cited by 154 · see citing works
Levine, J. B., Kong, J., Nadler, M., & Xu, Z. (1999) · Glia · doi:10.1002/(sici)1098-1136(199912)28:3 · Cited by 141 · see citing works
Endothelial Permeability for Macromolecules
van Hinsbergh, V. W. M. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.6.1018 · Cited by 138 · see citing works
AIDS and the brain: is there a chemokine connection?
Miller, R. J., & Meucci, O. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01408-3 · Cited by 134 · see citing works
Pedram, A., Razandi, M., & Levin, E. R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202391200 · Cited by 129 · see citing works
Intracellular signalling involved in modulating human endothelial barrier function*
van Hinsbergh, V. W. M., & Amerongen, G. P. V. N. (2002) · Journal of Anatomy · doi:10.1046/j.1469-7580.2002.00060.x · Cited by 128 · see citing works
Adamson, R. H., CURRY, F. E., Adamson, G. N., Liu, B., Jiang, Y., Aktories, K., Barth, H., Daigeler, A., Golenhofen, N., Ness, W., et al. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013117 · Cited by 128 · see citing works
Tanaka, K., Abé, M., & Sato, Y. (1999) · Japanese Journal of Cancer Research · doi:10.1111/j.1349-7006.1999.tb00796.x · Cited by 125 · see citing works
RhoA inactivation enhances endothelial barrier function
Carbajal, J. M., & Schaeffer, R. C. (1999) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1999.277.5.c955 · Cited by 124 · see citing works
Eriksson, A., Cao, R., Roy, J., Tritsaris, K., Wahlestedt, C., Dissing, S., Thyberg, J., & Cao, Y. (2003) · Circulation · doi:10.1161/01.cir.0000055324.34758.32 · Cited by 121 · see citing works
Cultured rat microglia express functional β-chemokine receptors
Boddeke, E., Meigel, I., Frentzel, S., Gourmala, N. G., Harrison, J. K., Buttini, M., Spleiss, O., & Gebicke‐Haerter, P. J. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00096-x · Cited by 120 · see citing works
Rezaie, P., Trillo‐Pazos, G., Everall, I., & Male, D. K. (2001) · Glia · doi:10.1002/glia.1128 · Cited by 120 · see citing works
Paracrine angiogenic loop between head-and-neck squamous-cell carcinomas and macrophages
Liss, C., Fekete, M. J., Hasina, R., Lam, C. D., & Lingen, M. W. (2001) · International Journal of Cancer · doi:10.1002/ijc.1407 · Cited by 114 · see citing works
Interaction of PKC and NOS in signal transduction of microvascular hyperpermeability
Huang, Q., & Yuan, Y. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.273.5.h2442 · Cited by 113 · see citing works
Stuart, R. O., Sun, A. M., Bush, K. T., & Nigám, S. K. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.23.13636 · Cited by 109 · see citing works
Tight junction proteins1This review is dedicated to the memory of Thomas Kreis.1
Citi, S., & Cordenonsi, M. (1998) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(98)00125-6 · Cited by 95 · see citing works
Dzenko, K. A., Andjelkovic, A. V., Kuziel, W. A., & Pachter, J. S. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09214.2001 · Cited by 89 · see citing works
Coghlan, M. P., Chou, M. M., & Carpenter, C. L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.8.2880-2889.2000 · Cited by 84 · see citing works
Visualization of Chemokine Binding Sites on Human Brain Microvessels
Andjelkovic, A. V., Spencer, D. D., & Pachter, J. S. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.145.2.403 · Cited by 83 · see citing works
Zhang, W., Smith, C. D., Shapiro, A., Monette, R., Hutchison, J. S., & Stanimirovic, D. B. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00137-x · Cited by 80 · see citing works
The Role of p38 MAP Kinase in Hydrogen Peroxide Mediated Endothelial Solute Permeability
Kevil, C. G., Oshima, T., & Alexander, J. S. (2001) · Endothelium · doi:10.3109/10623320109165320 · Cited by 77 · see citing works
Pal, S., Datta, K., Khosravi‐Far, R., & Mukhopadhyay, D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007818200 · Cited by 76 · see citing works
Interaction of Protein Kinase C Isozymes with Rho GTPases
Slater, S. J., Seiz, J. L., Stagliano, B. A., & Stubbs, C. D. (2001) · Biochemistry · doi:10.1021/bi001654n · Cited by 73 · see citing works
Regulation of endothelial cell barrier function by calcium/calmodulin-dependent protein kinase II
Borbiev, T., Verin, A. D., Shi, S., Liu, F., & Garcia, J. G. N. (2001) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2001.280.5.l983 · Cited by 71 · see citing works
Rimbach, G. H., Valacchi, G., Canali, R., & Virgili, F. (2000) · Molecular Cell Biology Research Communications · doi:10.1006/mcbr.2000.0219 · Cited by 71 · see citing works
Characterization of Binding Sites for Chemokines MCP‐1 and MIP‐1α on Human Brain Microvessels
Andjelkovic, A. V., & Pachter, J. S. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0751898.x · Cited by 69 · see citing works
Functional expression of CCR2 by human fetal astrocytes
Andjelkovic, A. V., Song, L., Dzenko, K. A., Cong, H., & Pachter, J. S. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10372 · Cited by 68 · see citing works
Chemokines and cardiovascular diseases
Sasayama, S. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(99)00381-8 · Cited by 68 · see citing works
Association of IL-8 and MCP-1 with the development of reexpansion pulmonary edema in rabbits
Sakao, Y., Kajikawa, O., Martin, T. R., Nakahara, Y., Hadden, W. A., Harmon, C. L., & Miller, E. J. (2001) · The Annals of Thoracic Surgery · doi:10.1016/s0003-4975(01)02489-4 · Cited by 63 · see citing works
Interleukin-8 Increases Endothelial Permeability Independent of Neutrophils
Biffl, W. L., Moore, E. E., Moore, F. A., Carl, V. S., Franciose, R. J., & Banerjee, A. M. (1995) · doi:10.1097/00005373-199507000-00013 · Cited by 59 · see citing works
Schmitz, H., Lorberg, A., & Heinisch, J. J. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02925.x · Cited by 55 · see citing works
Boven, L. A., Middel, J., Breij, E. C. W., Schotte, D., Verhoef, J., Soderland, C., & Nottet, H. S. L. M. (2000) · Journal of NeuroVirology · doi:10.3109/13550280009018302 · Cited by 51 · see citing works
Wachtel, M., Frei, K., Ehler, E., Bauer, C., Gassmann, M., & Gloor, S. M. (2002) · Biochemical Journal · doi:10.1042/bj20020746 · Cited by 49 · see citing works
Anin vitro model for endothelial permeability: Assessment of monolayer integrity
Kazakoff, P. W., McGuire, T. R., Hoie, E. B., Cano, M., & Iversen, P. L. (1995) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/bf02634568 · Cited by 49 · see citing works
Chemokines. Introduction and overview.
Mantovani, A. (1999) · PubMed · Cited by 47 · see citing works
Functional expression of chemokine receptor 2 by normal human eosinophils
Dunzendorfer, S., Kaneider, N. C., Kaser, A., Woell, E., Rodrı́guez-Frade, J. M., Mellado, M., Martínez-Alonso, C., & Wiedermann, C. J. (2001) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2001.118518 · Cited by 46 · see citing works
Niwa, K., Inanami, O., Ohta, T., Ito, S., Karino, T., & Kuwabara, M. (2001) · Free Radical Research · doi:10.1080/10715760100301531 · Cited by 45 · see citing works
Bogatcheva, N. V., Verin, A. D., Wang, P., Birukova, A. A., Birukov, K. G., Mirzopoyazova, T., Adyshev, D. M., Chiang, E. T., Crow, M. T., & Garcia, J. G. N. (2003) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00364.2001 · Cited by 41 · see citing works
Mantovani, A. (1999) · KARGER eBooks · doi:10.1159/000058734 · Cited by 39 · see citing works
Molecular decipherment of Rho effector pathways regulating tight-junction permeability
Fujita, H., Katoh, H., Hasegawa, H., Yasui, H., Aoki, J., Yamaguchi, Y., & Negishi, M. (2000) · Biochemical Journal · doi:10.1042/bj3460617 · Cited by 37 · see citing works
Ross, D., & Joyner, W. L. (1997) · Endothelium · doi:10.3109/10623329709052596 · Cited by 34 · see citing works
Blood-CSF barrier integrity in multiple sclerosis
Liebsch, R., Kornhuber, M. E., Dietl, D., Einsiedel, H. G., & Conrad, B. (1996) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1996.tb00052.x · Cited by 31 · see citing works
Platelet-activating factor modulates microvascular transport by stimulation of protein kinase C
Kobayashi, I., Kim, D., Hobson, R. W., & Durán, W. N. (1994) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1994.266.3.h1214 · Cited by 31 · see citing works
Vascular endothelial growth factor, a multifunctional polypeptide.
STEPHAN, C. C., & Brock, T. A. (1996) · PubMed · Cited by 31 · see citing works
Klockmann, M. T. U., Jahn, H., Hippenstiel, S., Krämer, H., & Suttorp, N. (1998) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199806)175:3 · Cited by 19 · see citing works
Signalling by Rho family proteins
Ridley, A. J. (1997) · Biochemical Society Transactions · doi:10.1042/bst0251005 · Cited by 19 · see citing works
Horwitz, M. A., & Silverstein, S. C. (1980) · Cited by 18 · see citing works
Pathophysiology of ischaemia-reperfusion injury
Carden, D. L., & Granger, D. N. (2000) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(200002)190:3 · Cited by 5 · see citing works
Collins (1998) · doi:10.1002/(sici)1097-4652(199807)176:1
Flagged first, then by citations
2 of the 119 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Neutrophils, from marrow to microbes.
Borregaard, N. (2010) · Immunity · doi:10.1016/j.immuni.2010.11.011 · Cited by 1,550 · see citing works
Mesenchymal Stem Cell Homing: The Devil Is in the Details
Karp, J. M., & Leng Teo, G. S. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.02.001 · Cited by 1,445 · see citing works
Dengue Virus Pathogenesis: an Integrated View
Martina, B. E. E., Koraka, P., & Osterhaus, A. D. M. E. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00035-09 · Cited by 1,057 · see citing works
Blood–brain Barrier: Structural Components and Function Under Physiologic and Pathologic Conditions
Persidsky, Y., Ramirez, S. H., Haorah, J., & Kanmogne, G. D. (2006) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-006-9025-3 · Cited by 922 · see citing works
Helms, H. C., Abbott, N. J., Burek, M., Cecchelli, R., Couraud, P.-O., Deli, M. A., Förster, C., Galla, H. J., Romero, I. A., Shusta, E. V., et al. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16630991 · Cited by 843 · see citing works
Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease
Argaw, A. T., Asp, L., Zhang, J., Navrazhina, K., Pham, T., Mariani, J. N., Mahase, S., Dutta, D. J., Seto, J., Kramer, E. G., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60842 · Cited by 733 · see citing works
Statin therapy and autoimmune disease: from protein prenylation to immunomodulation
Greenwood, J., Steinman, L., & Zamvil, S. S. (2006) · Nature reviews. Immunology · doi:10.1038/nri1839 · Cited by 685 · see citing works
Para-Inflammation in the Aging Retina
Xu, H., Chen, M., & Forrester, J. V. (2009) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2009.06.001 · Cited by 659 · see citing works
Luissint, A.-C., Artus, C., Glacial, F., Ganeshamoorthy, K., & Couraud, P.-O. (2012) · Fluids and Barriers of the CNS · doi:10.1186/2045-8118-9-23 · Cited by 654 · see citing works
Blood–Brain Barrier Pathophysiology in Traumatic Brain Injury
Chodobski, A., Zink, B. J., & Szmydynger‐Chodobska, J. (2011) · Translational Stroke Research · doi:10.1007/s12975-011-0125-x · Cited by 655 · see citing works
The impact of microglial activation on blood-brain barrier in brain diseases
da Fonseca, A. C. C., Matias, D., Garcia, C., Amaral, R., Geraldo, L. H., Freitas, C., & Lima, F. R. S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00362 · Cited by 572 · see citing works
The complexity of neurobiological processes in acute ischemic stroke
Brouns, R., & Deyn, P. P. D. (2009) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2009.04.001 · Cited by 527 · see citing works
Increased MCP-1 and microglia in various regions of the human alcoholic brain
He, J., & Crews, F. T. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.11.017 · Cited by 516 · see citing works
Brain Endothelial Cell-Cell Junctions: How to “Open” the Blood Brain Barrier
Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2008) · Current Neuropharmacology · doi:10.2174/157015908785777210 · Cited by 516 · see citing works
MCP-1: Chemoattractant with a role beyond immunity: A review
Yadav, A., Saini, V., & Arora, S. (2010) · Clinica Chimica Acta · doi:10.1016/j.cca.2010.07.006 · Cited by 488 · see citing works
Pathophysiology and treatment of cerebral edema in traumatic brain injury
Jha, R. M., Kochanek, P. M., & Simard, J. M. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.004 · Cited by 483 · see citing works
Role of Chemokines in CNS Health and Pathology: A Focus on the CCL2/CCR2 and CXCL8/CXCR2 Networks
Semple, B. D., Kossmann, T., & Morganti-Kossmann, M. C. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.240 · Cited by 457 · see citing works
Recent advances in chitosan-based nanoparticles for oral delivery of macromolecules
Chen, M., Mi, F., Liao, Z., Hsiao, C., Sonaje, K., Chung, M., Hsu, L., & Sung, H. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.10.010 · Cited by 453 · see citing works
Zhang, J., Shi, X., Echeverry, S., Mogil, J. S., Koninck, Y. D., & Rivest, S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3016-07.2007 · Cited by 421 · see citing works
Monocyte Chemoattractant Protein-1 Regulation of Blood–Brain Barrier Permeability
Stamatovic, S. M., Shakui, P., Keep, R. F., Moore, B. B., Kunkel, S. L., van Rooijen, N., & Andjelkovic, A. V. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600055 · Cited by 415 · see citing works
Hutchinson, M. R., Shavit, Y., Grace, P. M., Rice, K. C., Maier, S. F., & Watkins, L. R. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.004135 · Cited by 397 · see citing works
Turksen, K., & Troy, T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01235 · Cited by 397 · see citing works
Progress towards biocompatible intracortical microelectrodes for neural interfacing applications
Jorfi, M., Skousen, J. L., Weder, C., & Capadona, J. R. (2015) · Journal of Neural Engineering · doi:10.1088/1741-2560/12/1/011001 · Cited by 384 · see citing works
Mechanism and consequence of chitosan-mediated reversible epithelial tight junction opening
Yeh, T.-H., Hsu, L.-W., Tseng, M. T., Lee, P., Sonjae, K., Ho, Y., & Sung, H. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.03.056 · Cited by 381 · see citing works
Dikalova, A., Pandey, A. K., Xiao, L., Arslanbaeva, L. R., Sidorova, T. N., Lopez, M. G., Billings, F. T., Verdin, E. M., Auwerx, J. H., Harrison, D. G., et al. (2019) · Circulation Research · doi:10.1161/circresaha.119.315767 · Cited by 374 · see citing works
Zhang, J., & Koninck, Y. D. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03746.x · Cited by 345 · see citing works
Pathogenesis of acute stroke and the role of inflammasomes
Fann, D. Y., Lee, S.-Y., Manzanero, S., Chunduri, P., Sobey, C. G., & Arumugam, T. V. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.09.004 · Cited by 334 · 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
Cong, X., & Kong, W. (2019) · Cellular Signalling · doi:10.1016/j.cellsig.2019.109485 · Cited by 303 · see citing works
Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium
Vestweber, D. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2007.00533.x · Cited by 295 · see citing works
Li, F., Wang, Y., Lan, Y., Cao, S., Wang, K., Yuan, J., Wang, C., Wang, K., Cui, M., & Fu, Z. F. (2015) · Journal of Virology · doi:10.1128/jvi.00143-15 · Cited by 277 · see citing works
Chemokines and pain mechanisms
Abbadie, C., Bhangoo, S. K., Koninck, Y. D., Malcangio, M., Parsadaniantz, S. M., & White, F. A. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.12.002 · Cited by 278 · see citing works
Skelly, D., Hennessy, E., Dansereau, M., & Cunningham, C. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069123 · Cited by 278 · see citing works
Baumgart, D. C., & Dignass, A. U. (2002) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200211000-00012 · Cited by 275 · see citing works
Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis
Nakazawa, T., Hisatomi, T., Nakazawa, C., Noda, K., Maruyama, K., She, H., Matsubara, A., Miyahara, S., Nakao, S., Yin, Y., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608167104 · Cited by 272 · see citing works
Polymeric nanoparticle drug delivery technologies for oral delivery applications
Pridgen, E. M., Alexis, F., & Farokhzad, O. C. (2015) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2015.1018175 · Cited by 270 · see citing works
Cytokines and Chemokines in Cerebral Malaria Pathogenesis
Dunst, J., Kamena, F., & Matuschewski, K. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00324 · Cited by 264 · see citing works
Statins and the vascular endothelial inflammatory response
Greenwood, J., & Mason, J. C. (2007) · Trends in Immunology · doi:10.1016/j.it.2006.12.003 · Cited by 263 · see citing works
Rajesh, M., Mukhopadhyay, P., Bátkai, S., Haskó, G., Liaudet, L., Huffman, J. W., Csiszár, A., Ungvari, Z. I., Mackie, K., Chatterjee, S. B., et al. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00688.2007 · Cited by 262 · see citing works
Effects of the Chemokine CCL2 on Blood–Brain Barrier Permeability during Ischemia–Reperfusion Injury
Dimitrijevic, O. B., Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600229 · Cited by 252 · see citing works
Self-citationESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability
Wegmann, F., Petri, B., Khandoga, A. G., Moser, C., Khandoga, A., Volkery, S., Li, H., Nasdala, I., Brandau, O., Fässler, R., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060565 · Cited by 249 · 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
Current status of chemokines in the adult CNS
Goazigo, A. R.-L., Steenwinckel, J. V., Rostène, W. H., & Parsadaniantz, S. M. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.02.001 · Cited by 237 · see citing works
Molecular perspective on tight-junction assembly and epithelial polarity
Miyoshi, J., & Takai, Y. (2005) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2005.01.008 · Cited by 231 · see citing works
Vascular disruption and blood–brain barrier dysfunction in intracerebral hemorrhage
Keep, R. F., Zhou, N., Xiang, J., Andjelkovic, A. V., Hua, Y., & Xi, G. (2014) · Fluids and Barriers of the CNS · doi:10.1186/2045-8118-11-18 · Cited by 220 · see citing works
Self-citationViral disruption of the blood–brain barrier
Spindler, K. R., & Hsu, T.-H. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.03.009 · Cited by 219 · see citing works
Protein Kinase Cα-RhoA Cross-talk in CCL2-induced Alterations in Brain Endothelial Permeability
Stamatovic, S. M., Dimitrijevic, O. B., Keep, R. F., & Andjelkovic, A. V. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513122200 · Cited by 208 · see citing works
de Pablos, R. M., Herrera, A. J., Espinosa-Oliva, A. M., Sarmiento, M., Muñoz, M. F., Machado, A., & Venero, J. L. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-34 · Cited by 201 · see citing works
Stamatovic, S. M., Keep, R. F., Wang, M. M., Janković, I., & Andjelkovic, A. V. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.000521 · Cited by 198 · see citing works
Persidsky, Y., Heilman, D., Haorah, J., Zelivyanskaya, M., Persidsky, R., Weber, G. A., Shimokawa, H., Kaibuchi, K., & Ikezu, T. (2006) · Blood · doi:10.1182/blood-2005-11-4721 · Cited by 200 · see citing works
Lee, Y., Liu, M.-T., Lei, H.-Y., Liu, C., Wu, J.-M., Tung, Y.-C., Lin, Y.-S., Yeh, T., Chen, S., & Liu, H. (2006) · Journal of General Virology · doi:10.1099/vir.0.82093-0 · Cited by 192 · see citing works
Keep, R. F., Andjelkovic, A. V., Xiang, J., Stamatovic, S. M., Antonetti, D. A., Hua, Y., & Xi, G. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18774666 · Cited by 183 · see citing works
Monocyte chemoattractant protein-1 and the blood–brain barrier
Yao, Y., & Tsirka, S. E. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1459-1 · Cited by 175 · see citing works
CCL2 Regulates Angiogenesis via Activation of Ets-1 Transcription Factor
Stamatovic, S. M., Keep, R. F., Mostarica‐Stojković, M., & Andjelkovic, A. V. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2651 · Cited by 177 · see citing works
Thurgur, H., & Pinteaux, E. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.06.046 · Cited by 181 · see citing works
Chai, Q., He, W., Zhou, M., Lu, H., & Fu, Z. F. (2014) · Journal of Virology · doi:10.1128/jvi.03149-13 · Cited by 175 · see citing works
Haorah, J., Heilman, D., Knipe, B., Chrastil, J., Leibhart, J., Ghorpade, A., Miller, D. W., & Persidsky, Y. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000166944.79914.0a · Cited by 169 · see citing works
Cell‐specific blood–brain barrier regulation in health and disease: a focus on hypoxia
Engelhardt, S., Patkar, S., & Ogunshola, O. O. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12489 · Cited by 165 · see citing works
Glial influences on BBB functions and molecular players in immune cell trafficking
Lécuyer, M., Kébir, H., & Prat, A. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.004 · Cited by 163 · see citing works
Acute Minocycline Treatment Mitigates the Symptoms of Mild Blast-Induced Traumatic Brain Injury
Kövesdi, E., Kamnaksh, A., Wingo, D., Ahmed, F. A. K. M., Grunberg, N. E., Long, J. B., Kasper, C. E., & Agoston, D. V. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00111 · Cited by 160 · see citing works
Yin, J., Tu, C., Zhao, J., Ou, D., Chen, G., Liu, Y., & Xiao, X. (2012) · Brain Research · doi:10.1016/j.brainres.2012.10.046 · Cited by 160 · see citing works
CCL2-CCR2 Signaling in Disease Pathogenesis
O’Connor, T., Borsig, L., & Heikenwälder, M. F. (2015) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530315666150316120920 · Cited by 160 · see citing works
Dysfunction of Cerebrovascular Endothelial Cells: Prelude to Vascular Dementia
Wang, F., Cao, Y., Ma, L., Pei, H., Rausch, W., & Li, H. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00376 · Cited by 160 · see citing works
Stamatovic, S. M., Martínez-Revollar, G., Hu, A., Choi, J. H. K., Keep, R. F., & Andjelkovic, A. V. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.09.006 · Cited by 149 · see citing works
Li, B., Zhao, W., Tan, Z., Fang, W., Zhu, L. X., & Chen, Y. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.06.056 · Cited by 144 · see citing works
Matrix-specific p21-activated kinase activation regulates vascular permeability in atherogenesis
Orr, A. W., Stockton, R. A., Simmers, M. B., Sanders, J. M., Sarembock, I. J., Blackman, B. R., & Schwartz, M. A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609008 · Cited by 141 · see citing works
New experimental models of the blood-brain barrier for CNS drug discovery
Kaisar, M. A., Sajja, R. K., Prasad, S., Abhyankar, V. V., Liles, T., & Cucullo, L. (2016) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2017.1253676 · Cited by 134 · see citing works
Inflammation of the Embryonic Choroid Plexus Barrier following Maternal Immune Activation
Cui, J., Shipley, F. B., Shannon, M. L., Alturkistani, O., Dani, N., Webb, M. D., Sugden, A. U., Andermann, M. L., & Lehtinen, M. K. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.09.020 · Cited by 128 · see citing works
The role of actin-binding proteins in the control of endothelial barrier integrity
García‐Ponce, A., Citalán‐Madrid, A. F., Velázquez-Avila, M., Vargas‐Robles, H., & Michael Schnoor, A. (2014) · Thrombosis and Haemostasis · doi:10.1160/th14-04-0298 · Cited by 130 · see citing works
Inflammation and brain edema: new insights into the role of chemokines and their receptors
Stamatovic, S. M., Dimitrijevic, O. B., Keep, R. F., & Andjelkovic, A. V. (2006) · Springer eBooks · doi:10.1007/3-211-30714-1_91 · Cited by 125 · see citing works
Microglia at the blood brain barrier in health and disease
Mayer, M. G., & Fischer, T. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1360195 · Cited by 128 · see citing works
Man, S., Ma, Y., Shang, D., Zhao, W., Li, B., Guo, D., Fang, W., Zhu, L., & Chen, Y. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.02.013 · Cited by 122 · see citing works
Systemic immune system alterations in early stages of Alzheimer's disease
Zhang, R., Miller, R. G., Madison, C. A., Jin, X., Honrada, R., Harris, W., Katz, J., Forshew, D. A., & McGrath, M. S. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.01.002 · Cited by 121 · see citing works
Tarabra, E., Giunti, S., Barutta, F., Salvidio, G., Burt, D. J., Deferrari, G., Gambino, R., Vergola, D., Pinach, S., Perin, P. C., et al. (2009) · Diabetes · doi:10.2337/db08-0895 · Cited by 121 · see citing works
Blood–Brain Barrier in Cerebral Malaria: Pathogenesis and Therapeutic Intervention
Nishanth, G., & Schlüter, D. (2019) · Trends in Parasitology · doi:10.1016/j.pt.2019.04.010 · Cited by 117 · see citing works
CCL2 disrupts the adherens junction: implications for neuroinflammation
Roberts, T. K., Eugenin, E. A., Lopez, L., Romero, I. A., Weksler, B. B., Couraud, P.-O., & Berman, J. W. (2012) · Laboratory Investigation · doi:10.1038/labinvest.2012.80 · Cited by 115 · see citing works
Acquired immunodeficiency syndrome and the blood-brain barrier
Ivey, N., MacLean, A. G., & Lackner, A. A. (2009) · Journal of NeuroVirology · doi:10.1080/13550280902769764 · Cited by 115 · see citing works
Cytokines and Pathogenesis of Central Retinal Vein Occlusion
Noma, H., Yasuda, K., & Shimura, M. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9113457 · Cited by 112 · see citing works
Involvement of Cytokines in the Pathogenesis of Diabetic Macular Edema
Noma, H., Yasuda, K., & Shimura, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073427 · Cited by 111 · see citing works
Subileau, E. A., Rezaie, P., Davies, H. A., Colyer, F. M., Greenwood, J., Male, D. K., & Romero, I. A. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e318197eca7 · Cited by 111 · see citing works
Liu, L., Xue, Y., Liu, Y., & Wang, Y. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21558 · Cited by 111 · see citing works
C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins
Vogelsgesang, M., Pautsch, A., & Aktories, K. (2006) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-006-0113-y · Cited by 108 · see citing works
Niego, B., & Medcalf, R. L. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.99 · Cited by 102 · see citing works
Sagar, D., Lamontagne, A., Foss, C. A., Khan, Z. K., Pomper, M. G., & Jain, P. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-245 · Cited by 106 · see citing works
Ramirez, S. H., Heilman, D., Morsey, B., Potula, R., Haorah, J., & Persidsky, Y. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.3.1854 · Cited by 105 · see citing works
Foresti, M. L., Arisi, G. M., Katki, K. A., Montañez, A., Sanchez, R. M., & Shapiro, L. A. (2009) · Journal of Neuroinflammation · doi:10.1186/1742-2094-6-40 · Cited by 105 · see citing works
Control of Chemokine Gradients by the Retinal Pigment Epithelium
Shi, G., Maminishkis, A., Banzon, T., Jalickee, S., Li, R., Hammer, J., & Miller, S. S. (2008) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.08-1816 · Cited by 102 · see citing works
The role of CCL2/CCR2 axis in cancer and inflammation: The next frontier in nanomedicine
Pozzi, S., & Satchi‐Fainaro, R. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115318 · Cited by 103 · see citing works
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Berghoff, S. A., Düking, T., Spieth, L., Winchenbach, J., Stumpf, S. K., Gerndt, N., Kusch, K., Ruhwedel, T., Möbius, W., & Saher, G. (2017) · Acta Neuropathologica Communications · doi:10.1186/s40478-017-0497-6 · Cited by 100 · see citing works
Wu, T.-S., & Tang, M. (2018) · Nanomedicine · doi:10.2217/nnm-2017-0270 · Cited by 90 · see citing works
Influence of silver and titanium dioxide nanoparticles on in vitro blood-brain barrier permeability
Chen, I.-C., Hsiao, I., Lin, H.-C., Wu, C., Chuang, C., & Huang, Y.-J. (2016) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2016.09.009 · Cited by 99 · see citing works
Dengue virus infection: current concepts in immune mechanisms and lessons from murine models
Guabiraba, R., & Ryffel, B. (2013) · Immunology · doi:10.1111/imm.12188 · Cited by 98 · see citing works
Brain Cytokines and Chemokines: Roles in Ischemic Injury and Pain
Minami, M., Katayama, T., & Satoh, M. (2006) · Journal of Pharmacological Sciences · doi:10.1254/jphs.crj06005x · Cited by 99 · see citing works
Gorska, M. M., Liang, Q., Stafford, S. J., Goplen, N., Dharajiya, N. G., Guo, L., Sur, S. A., Gaestel, M., & Alam, R. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062621 · Cited by 97 · see citing works
Zhu, H., Wang, Z., Xing, Y., Gao, Y., Ma, T., Lou, L., Lou, J., Gao, Y., Wang, S., & Wang, Y. (2011) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2011.08.063 · Cited by 94 · see citing works
McCaffrey, G., Staatz, W. D., Quigley, C. A., Nametz, N., Seelbach, M. J., Campos, C. R., Brooks, T. A., Egleton, R. D., & Davis, T. P. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04943.x · Cited by 93 · see citing works
Haydinger, C. D., Ferreira, L. B., Williams, K. A., & Smith, J. R. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1128811 · Cited by 92 · see citing works
The CCL2‐CCR2 system affects the progression and clearance of intracerebral hemorrhage
Yao, Y., & Tsirka, S. E. (2012) · Glia · doi:10.1002/glia.22323 · Cited by 90 · see citing works
Cytokines and junction restructuring during spermatogenesis—a lesson to learn from the testis
Xia, W., Mruk, D. D., Lee, W. M., & Cheng, C. Y. (2005) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2005.05.007 · Cited by 90 · see citing works
Guo, F., Xu, D., Lin, Y., Wang, G., Wang, F., Gao, Q., Wei, Q., & Lei, S. (2019) · The FASEB Journal · doi:10.1096/fj.201902203rr · Cited by 88 · see citing works
- Authors
- Stamatovic, S. M., Keep, R. F., Kunkel, S. L., & Andjelkovic, A. V.
- Affiliations
- University of Michigan (US)
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2003-11-15
- Volume
- 116
- Issue
- 22
- Pages
- 4615-4628
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W1968099474
- Cited by
- 381
- References
- 119
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 14 · 2023: 20 · 2022: 15 · 2021: 19 · 2020: 20 · 2019: 21 · 2018: 19 · 2017: 17 · 2016: 19 · 2015: 20 · 2014: 16 · 2013: 20 · 2012: 21
- FWCI
- 6.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Keywords
- MCP-1, CCR2, brain endothelial cells, endothelial permeability, tight junctions, Rho kinase, Rho GTPases, actin cytoskeleton remodeling, stress fibers, ZO-1, occludin, claudin-5, transendothelial electrical resistance, leukocyte migration
- MeSH terms
- Acute-Phase Proteins, Animals, Brain, Cells, Cultured, Inulin, Membrane Proteins, Microscopy, Fluorescence, Mutation, Permeability, Electric Impedance, Protein Serine-Threonine Kinases, Octoxynol, Mice, Knockout, Chemokine CCL2, Tight Junctions, Receptors, Chemokine, Oligonucleotide Array Sequence Analysis, Stress Fibers, Endothelial Cells, Intracellular Signaling Peptides and Proteins, Mice, Receptors, CCR2, rho-Associated Kinases, Claudin-5, Occludin, Zonula Occludens-2 Protein
About these checks
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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