Truncation of monocyte chemoattractant protein 1 by plasmin promotes blood-brain barrier disruption

Journal of Cell Science

Volumn 124, Issue 9, 2011, Pages 1486-1495

  Yao, Yao ^a   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Blood brain barrier; Endothelia cells; Monocyte chemoattractant protein 1 (CCL2); Plasmin; Tight junction

Indexed keywords

ALPHA 2 ANTIPLASMIN; MONOCYTE CHEMOTACTIC PROTEIN 1; OCCLUDIN; PLASMIN; PROTEIN ZO1; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; CELLS, CULTURED; CHEMOKINE CCL2; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; FIBRINOLYSIN; HUMANS; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICE; OCTOXYNOL; PHOSPHOPROTEINS; PLASMINOGEN; PROTEIN BINDING; TIGHT JUNCTIONS; TISSUE PLASMINOGEN ACTIVATOR; TRANSCRIPTION FACTORS;

MUS;

EID: 79955531506     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.082834     Document Type: Article

References (70)

1. Ahdieh, M., Vandenbos, T. and Youakim, A. (2001). Lung epithelial barrier function and wound healing are decreased by IL-4 and IL-13 and enhanced by IFN-gamma. Am. J. Physiol. Cell Physiol. 281, C2029-C2038.
2. Alter, A., Duddy, M., Hebert, S., Biernacki, K., Prat, A., Antel, J. P., Yong, V. W., Nuttall, R. K., Pennington, C. J., Edwards, D. R. et al. (2003). Determinants of human B cell migration across brain endothelial cells. J. Immunol. 170, 4497-4505.
3. Blamire, A., Anthony, D., Rajagopalan, B., Sibson, N., Perry, V. and Styles, P. (2000). Interleukin-1beta-induced changes in blood-brain barrier permeability, apparent diffusion coefficient, and cerebral blood volume in the rat brain: a magnetic resonance study. J. Neurosci. 20, 8153-8159.
4. Bretscher, A., Gary, R. and Berryman, M. (1995). Soluble ezrin purified from placenta exists as stable monomers and elongated dimers with masked C-terminal ezrin-radixin-moesin association domains. Biochemistry 34, 16830-16837.
5. Calabria, A. R., Weidenfeller, C., Jones, A. R., de Vries, H. E. and Shusta, E. V. (2006). Puromycin-purified rat brain microvascular endothelial cell cultures exhibit improved barrier properties in response to glucocorticoid induction. J. Neurochem. 97, 922-933.
6. Capoccia, B. J., Gregory, A. D. and Link, D. C. (2008). Recruitment of the inflammatory subset of monocytes to sites of ischemia induces angiogenesis in a monocyte chemoattractant protein-1-dependent fashion. J. Leukoc. Biol. 84, 760-768.
7. Citi, S. and Cordenonsi, M. (1998). Tight junction proteins. Biochim. Biophys. Acta 1448, 1-11.
8. Clarke, H., Marano, C. W., Peralta Soler, A. and Mullin, J. M. (2000). Modification of tight junction function by protein kinase C isoforms. Adv. Drug Deliv. Rev. 41, 283-301.
9. Coyne, C., Vanhook, M., Gambling, T., Carson, J., Boucher, R. and Johnson, L. (2002). Regulation of airway tight junctions by proinflammatory cytokines. Mol. Biol. Cell 13, 3218-3234.
10. Deli, M. A., Abraham, C. S., Niwa, M. and Falus, A. (2003). N,N-diethyl-2-[4-(phenylmethyl)phenoxy]ethanamine increases the permeability of primary mouse cerebral endothelial cell monolayers. Inflamm. Res. 52 Suppl. 1, S39-S40.
11. Dimitrijevic, O. B., Stamatovic, S. M., Keep, R. F. and Andjelkovic, A. V. (2006). Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury. J. Cereb. Blood Flow Metab. 26, 797-810.
12. Eugenin, E. A., Osiecki, K., Lopez, L., Goldstein, H., Calderon, T. M. and Berman, J. W. (2006). CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: a potential mechanism of HIV-CNS invasion and NeuroAIDS. J. Neurosci. 26, 1098-1106.
13. Farshori, P. and Kachar, B. (1999). Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. J. Membr. Biol. 170, 147-156.
14. Fey, E. G., Wan, K. M. and Penman, S. (1984). Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition. J. Cell Biol. 98, 1973-1984.
15. Förster, C. (2008). Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 130, 55-70.
16. Frangogiannis, N. G., Dewald, O., Xia, Y., Ren, G., Haudek, S., Leucker, T., Kraemer, D., Taffet, G., Rollins, B. J. and Entman, M. L. (2007). Critical role of monocyte chemoattractant protein-1/CC chemokine ligand 2 in the pathogenesis of ischemic cardiomyopathy. Circulation 115, 584-592.
17. Glabinski, A. R., Balasingam, V., Tani, M., Kunkel, S. L., Strieter, R. M., Yong, V. W. and Ransohoff, R. M. (1996). Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J. Immunol. 156, 4363-4368.
18. Glynn, S. L. and Yazdanian, M. (1998). In vitro blood-brain barrier permeability of nevirapine compared to other HIV antiretroviral agents. J. Pharm. Sci. 87, 306-310.
19. Guillemin, G. J. and Brew, B. J. (2004). Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J. Leukoc. Biol. 75, 388-397.
20. Hanisch, U. K. (2002). Microglia as a source and target of cytokines. Glia 40, 140-155.
21. Hart, M. N., VanDyk, L. F., Moore, S. A., Shasby, D. M. and Cancilla, P. A. (1987). Differential opening of the brain endothelial barrier following neutralization of the endothelial luminal anionic charge in vitro. J. Neuropathol. Exp. Neurol. 46, 141-153.
22. Hayashi, K., Nakao, S., Nakaoke, R., Nakagawa, S., Kitagawa, N. and Niwa, M. (2004). Effects of hypoxia on endothelial/pericytic co-culture model of the blood-brain barrier. Regul. Pept. 123, 77-83.
23. Helander, T. S., Carpen, O., Turunen, O., Kovanen, P. E., Vaheri, A. and Timonen, T. (1996). ICAM-2 redistributed by ezrin as a target for killer cells. Nature 382, 265-268.
24. Hicks, K., O'Neil, R. G., Dubinsky, W. S. and Brown, R. C. (2010). TRPC-mediated actin-myosin contraction is critical for BBB disruption following hypoxic stress. Am. J. Physiol. Cell Physiol. 298, C1583-C1593.
25. Hirase, T., Kawashima, S., Wong, E. Y., Ueyama, T., Rikitake, Y., Tsukita, S., Yokoyama, M. and Staddon, J. M. (2001). Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J. Biol. Chem. 276, 10423-10431.
26. Huber, J. D., Egleton, R. D. and Davis, T. P. (2001). Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci. 24, 719-725.
27. Hulkower, K., Brosnan, C. F., Aquino, D. A., Cammer, W., Kulshrestha, S., Guida, M. P., Rapoport, D. A. and Berman, J. W. (1993). Expression of CSF-1, c-fms, and MCP-1 in the central nervous system of rats with experimental allergic encephalomyelitis. J. Immunol. 150, 2525-2533.
28. Jung, H., Bhangoo, S., Banisadr, G., Freitag, C., Ren, D., White, F. A. and Miller, R. J. (2009). Visualization of chemokine receptor activation in transgenic mice reveals peripheral activation of CCR2 receptors in states of neuropathic pain. J. Neurosci. 29, 8051-8062.
29. Kacem, K., Lacombe, P., Seylaz, J. and Bonvento, G. (1998). Structural organization of the perivascular astrocyte endfeet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia 23, 1-10.
30. Kataoka, K., Asai, T., Taneda, M., Ueshima, S., Matsuo, O., Kuroda, R., Kawabata, A. and Carmeliet, P. (2000). Roles of urokinase type plasminogen activator in a brain stab wound. Brain Res. 887, 187-190.
31. Kawedia, J. D., Nieman, M. L., Boivin, G. P., Melvin, J. E., Kikuchi, K., Hand, A. R., Lorenz, J. N. and Menon, A. G. (2007). Interaction between transcellular and paracellular water transport pathways through Aquaporin 5 and the tight junction complex. Proc. Natl. Acad. Sci. USA 104, 3621-3626.
32. Kim, G. H., Kellner, C. P., Hahn, D. K., Desantis, B. M., Musabbir, M., Starke, R. M., Rynkowski, M., Komotar, R. J., Otten, M. L., Sciacca, R. et al. (2008). Monocyte chemoattractant protein-1 predicts outcome and vasospasm following aneurysmal subarachnoid hemorrhage. J. Neurosurg. 109, 38-43.
33. Lahrtz, F., Piali, L., Spanaus, K. S., Seebach, J. and Fontana, A. (1998). Chemokines and chemotaxis of leukocytes in infectious meningitis. J. Neuroimmunol. 85, 33-43.
34. Louvet-Vallee, S. (2000). ERM proteins: from cellular architecture to cell signaling. Biol. Cell 92, 305-316.
35. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K. and Tsukita, S. (1998). Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657.
36. Michel, C. and Curry, F. (1999). Microvascular permeability. Physiol. Rev. 79 703-761.
37. Miller, R. J. and Meucci, O. (1999). AIDS and the brain: is there a chemokine connection? Trends Neurosci. 22, 471-479.
38. Mitic, L. L. and Anderson, J. M. (1998). Molecular architecture of tight junctions. Annu. Rev. Physiol. 60, 121-142.
39. Morimoto, H., Hirose, M., Takahashi, M., Kawaguchi, M., Ise, H., Kolattukudy, P. E., Yamada, M. and Ikeda, U. (2008). MCP-1 induces cardioprotection against ischaemia/reperfusion injury: role of reactive oxygen species. Cardiovasc. Res. 78, 554-562.
40. Nakamura, F., Amieva, M. R. and Furthmayr, H. (1995). Phosphorylation of threonine 558 in the carboxyl-terminal actin-binding domain of moesin by thrombin activation of human platelets. J. Biol. Chem. 270, 31377-31385.
41. Neuhaus, W., Plattner, V. E., Wirth, M., Germann, B., Lachmann, B., Gabor, F. and Noe, C. R. (2008). Validation of in vitro cell culture models of the blood-brain barrier: tightness characterization of two promising cell lines. J. Pharm. Sci. 97, 5158-5175.
42. Ohno, K., Chiueh, C. C., Burns, E. M., Pettigrew, K. D. and Rapoport, S. I. (1980). Cerebrovascular integrity in protein-deprived rats. Brain Res. Bull. 5, 251-255.
43. Parathath, S., Parathath, S. and Tsirka, S. (2006). Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice. J. Cell Sci. 119, 339-349.
44. Paul, R., Koedel, U., Winkler, F., Kieseier, B., Fontana, A., Kopf, M., Hartung, H. and Pfister, H. (2003). Lack of IL-6 augments inflammatory response but decreases vascular permeability in bacterial meningitis. Brain 126, 1873-1882.
45. Pearson, M. A., Reczek, D., Bretscher, A. and Karplus, P. A. (2000). Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101, 259-270.
46. Pestonjamasp, K., Amieva, M. R., Strassel, C. P., Nauseef, W. M., Furthmayr, H. and Luna, E. J. (1995). Moesin, ezrin, and p205 are actin-binding proteins associated with neutrophil plasma membranes. Mol. Biol. Cell 6, 247-259.
47. Reijerkerk, A., Kooij, G., van der Pol, S. M., Leyen, T., van Het Hof, B., Couraud, P. O., Vivien, D., Dijkstra, C. D. and de Vries, H. E. (2008). Tissue-type plasminogen activator is a regulator of monocyte diapedesis through the brain endothelial barrier. J. Immunol. 181, 3567-3574.
48. Ross, D. and Joyner, W. (1997). Resting distribution and stimulated translocation of protein kinase C isoforms alpha, epsilon and zeta in response to bradykinin and TNF in human endothelial cells. Endothelium 5, 321-332.
49. Serrador, J. M., Alonso-Lebrero, J. L., del Pozo, M. A., Furthmayr, H., Schwartz-Albiez, R., Calvo, J., Lozano, F. and Sanchez-Madrid, F. (1997). Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization. J. Cell Biol. 138, 1409-1423.
50. Sheehan, J. J., Zhou, C., Gravanis, I., Rogove, A. D., Wu, Y. P., Bogenhagen, D. F. and Tsirka, S. E. (2007). Proteolytic activation of monocyte chemoattractant protein-1 by plasmin underlies excitotoxic neurodegeneration in mice. J. Neurosci. 27, 1738-1745.
51. Simard, M., Arcuino, G., Takano, T., Liu, Q. S. and Nedergaard, M. (2003). Signaling at the gliovascular interface. J. Neurosci. 23, 9254-9262.
52. Stamatovic, S. M., Keep, R. F., Kunkel, S. L. and Andjelkovic, A. V. (2003). Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase. J. Cell Sci. 116, 4615-4628.
53. Stamatovic, S. M., Shakui, P., Keep, R. F., Moore, B. B., Kunkel, S. L., Van Rooijen, N. and Andjelkovic, A. V. (2005). Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J. Cereb. Blood Flow Metab. 25, 593-606.
54. Stamatovic, S. M., Dimitrijevic, O. B., Keep, R. F. and Andjelkovic, A. V. (2006). Protein kinase Calpha-RhoA cross-talk in CCL2-induced alterations in brain endothelial permeability. J. Biol. Chem. 281, 8379-8388.
55. Stephan, C. C. and Brock, T. A. (1996). Vascular endothelial growth factor, a multifunctional polypeptide. P. R. Health Sci. J. 15, 169-178.
56. Sugimoto, M., Inoko, A., Shiromizu, T., Nakayama, M., Zou, P., Yonemura, S., Hayashi, Y., Izawa, I., Sasoh, M., Uji, Y. et al. (2008). The keratin-binding protein Albatross regulates polarization of epithelial cells. J. Cell Biol. 183, 19-28.
57. Tsukamoto, T. and Nigam, S. (1997). Tight junction proteins form large complexes and associate with the cytoskeleton in an ATP depletion model for reversible junction assembly. J. Biol. Chem. 272, 16133-16139.
58. Tsukamoto, T. and Nigam, S. (1999). Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am. J. Physiol. 276, F737-F750.
59. Tsukita, S., Oishi, K., Sato, N., Sagara, J. and Kawai, A. (1994). ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126, 391-401.
60. Turunen, O., Wahlstrom, T. and Vaheri, A. (1994). Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126, 1445-1453.
61. van Nieuw Amerongen, G. P., van Delft, S., Vermeer, M. A., Collard, J. G. and van Hinsbergh, V. W. (2000). Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ. Res. 87, 335-340.
62. Ward, P. D., Klein, R. R., Troutman, M. D., Desai, S. and Thakker, D. R. (2002). Phospholipase C-gamma modulates epithelial tight junction permeability through hyperphosphorylation of tight junction proteins. J. Biol. Chem. 277, 35760-35765.
63. Wojciak-Stothard, B., Entwistle, A., Garg, R. and Ridley, A. (1998). Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell-cell junction by Rho, Rac and Cdc42 in human endothelial cells. J. Cell Physiol. 176, 150-165.
64. Wu, M. and Tsirka, S. (2009). Endothelial NOS-deficient mice reveal dual roles for nitric oxide during experimental autoimmune encephalomyelitis. Glia 57, 1204-1215.
65. Yan, Y. P., Sailor, K. A., Lang, B. T., Park, S. W., Vemuganti, R. and Dempsey, R. J. (2007). Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 27, 1213-1224.
66. Yang, G., Gong, C., Qin, Z., Liu, X. and Betz, L. (1999). Tumor necrosis factor alpha expression produces increased blood-brain barrier permeability following temporary focal cerebral ischemia in mice. Brain Res. Mol. Brain Res. 69, 135-143.
67. Yao, Y. and Tsirka, S. E. (2010). The C terminus of mouse monocyte chemoattractant protein 1 (MCP1) mediates MCP1 dimerization while blocking its chemotactic potency. J. Biol. Chem. 285, 31509-31516.
68. Yepes, M., Sandkvist, M., Moore, E., Bugge, T., Strickland, D. and Lawrence, D. (2003). Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 112, 1533-1540.
69. Yonemura, S., Nagafuchi, A., Sato, N. and Tsukita, S. (1993). Concentration of an integral membrane protein, CD43 (leukosialin, sialophorin), in the cleavage furrow through the interaction of its cytoplasmic domain with actin-based cytoskeletons. J. Cell Biol. 120, 437-449.
70. Youakim, A. and Ahdieh, M. (1999). Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am. J. Physiol. 276, G1279-G1288.