Plasminogen activator inhibitor type 1 regulates microglial motility and phagocytic activity

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Jeon, Hyejin ^a   Kim, Jong Heon ^a   Kim, Jae Hong ^a   Lee, Won Ha ^b   Lee, Myung Shik ^c   Suk, Kyoungho ^a  

^a Kyungpook National University School of Medicine   (South Korea)

^b Kyungpook National University   (South Korea)

^c Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; GAMMA INTERFERON; JANUS KINASE; LIPOPOLYSACCHARIDE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEINASE; STAT1 PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; VITRONECTIN; ZYMOSAN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOCRINE EFFECT; CELL MIGRATION; CELL MOTILITY; CELL PHAGOCYTOSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MICROGLIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; STAB WOUND; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; WOUND HEALING;

EID: 84862989708     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-149     Document Type: Article

References (107)

1. Popovich PG, Longbrake EE. Can the immune system be harnessed to repair the CNS?. Nat Rev Neurosci 2008, 9:481-493. 10.1038/nrn2398, 18490917.
2. Streit WJ, Mrak RE, Griffin WS. Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 2004, 1:14. 10.1186/1742-2094-1-14, 509427, 15285801.
3. Lafon-Cazal M, Adjali O, Galeotti N, Poncet J, Jouin P, Homburger V, Bockaert J, Marin P. Proteomic analysis of astrocytic secretion in the mouse. Comparison with the cerebrospinal fluid proteome. J Biol Chem 2003, 278:24438-24448. 10.1074/jbc.M211980200, 12709418.
4. Keene SD, Greco TM, Parastatidis I, Lee SH, Hughes EG, Balice-Gordon RJ, Speicher DW, Ischiropoulos H. Mass spectrometric and computational analysis of cytokine-induced alterations in the astrocyte secretome. Proteomics 2009, 9:768-782. 10.1002/pmic.200800385, 2667946, 19132682.
5. Moore NH, Costa LG, Shaffer SA, Goodlett DR, Guizzetti M. Shotgun proteomics implicates extracellular matrix proteins and protease systems in neuronal development induced by astrocyte cholinergic stimulation. J Neurochem 2009, 108:891-908. 10.1111/j.1471-4159.2008.05836.x, 2754805, 19077055.
6. Kim S, Ock J, Kim AK, Lee HW, Cho JY, Kim DR, Park JY, Suk K. Neurotoxicity of microglial cathepsin D revealed by secretome analysis. J Neurochem 2007, 103:2640-2650.
7. Liu J, Hong Z, Ding J, Liu J, Zhang J, Chen S. Predominant release of lysosomal enzymes by newborn rat microglia after LPS treatment revealed by proteomic studies. J Proteome Res 2008, 7:2033-2049. 10.1021/pr7007779, 18380473.
8. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007, 8:57-69. 10.1038/nrn2038, 17180163.
9. Garden GA, Moller T. Microglia biology in health and disease. J Neuroimmune Pharmacol 2006, 1:127-137. 10.1007/s11481-006-9015-5, 18040779.
10. Graeber MB, Streit WJ. Microglia: biology and pathology. Acta Neuropathol 2010, 119:89-105. 10.1007/s00401-009-0622-0, 20012873.
11. Mallat M, Marin-Teva JL, Cheret C. Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 2005, 15:101-107. 10.1016/j.conb.2005.01.006, 15721751.
12. Woo MS, Park JS, Choi IY, Kim WK, Kim HS. Inhibition of MMP-3 or -9 suppresses lipopolysaccharide-induced expression of proinflammatory cytokines and iNOS in microglia. J Neurochem 2008, 106:770-780. 10.1111/j.1471-4159.2008.05430.x, 18419763.
13. Magnus T, Chan A, Savill J, Toyka KV, Gold R. Phagocytotic removal of apoptotic, inflammatory lymphocytes in the central nervous system by microglia and its functional implications. J Neuroimmunol 2002, 130:1-9. 10.1016/S0165-5728(02)00212-6, 12225883.
14. Orr CF, Rowe DB, Halliday GM. An inflammatory review of Parkinson's disease. Prog Neurobiol 2002, 68:325-340. 10.1016/S0301-0082(02)00127-2, 12531233.
15. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010, 6:193-201. 10.1038/nrneurol.2010.17, 20234358.
16. Wersinger C, Sidhu A. An inflammatory pathomechanism for Parkinson's disease?. Curr Med Chem 2006, 13:591-602. 10.2174/092986706776055760, 16515523.
17. Eikelenboom P, Bate C, Van Gool WA, Hoozemans JJ, Rozemuller JM, Veerhuis R, Williams A. Neuroinflammation in Alzheimer's disease and prion disease. Glia 2002, 40:232-239. 10.1002/glia.10146, 12379910.
18. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934. 10.1016/j.cell.2010.02.016, 2873093, 20303880.
19. McGeer PL, McGeer EG. Glial reactions in Parkinson's disease. Mov Disord 2008, 23:474-483. 10.1002/mds.21751, 18044695.
20. Stence N, Waite M, Dailey ME. Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 2001, 33:256-266. 10.1002/1098-1136(200103)33:3<256::AID-GLIA1024>3.0.CO;2-J, 11241743.
21. Ha H, Oh EY, Lee HB. The role of plasminogen activator inhibitor 1 in renal and cardiovascular diseases. Nat Rev Nephrol 2009, 5:203-211. 10.1038/nrneph.2009.15, 19322185.
22. Gabriel C, Ali C, Lesne S, Fernandez-Monreal M, Docagne F, Plawinski L, MacKenzie ET, Buisson A, Vivien D. Transforming growth factor alpha-induced expression of type 1 plasminogen activator inhibitor in astrocytes rescues neurons from excitotoxicity. FASEB J 2003, 17:277-279.
23. Hultman K, Blomstrand F, Nilsson M, Wilhelmsson U, Malmgren K, Pekny M, Kousted T, Jern C, Tjarnlund-Wolf A. Expression of plasminogen activator inhibitor-1 and protease nexin-1 in human astrocytes: Response to injury-related factors. J Neurosci Res 2010, 88:2441-2449.
24. Myohanen H, Vaheri A. Regulation and interactions in the activation of cell-associated plasminogen. Cell Mol Life Sci 2004, 61:2840-2858. 10.1007/s00018-004-4230-9, 15558213.
25. Pepper MS, Rosnoblet C, Di Sanza C, Kruithof EK. Synergistic induction of t-PA by vascular endothelial growth factor and basic fibroblast growth factor and localization of t-PA to Weibel-Palade bodies in bovine microvascular endothelial cells. Thromb Haemost 2001, 86:702-709.
26. Czekay RP, Aertgeerts K, Curriden SA, Loskutoff DJ. Plasminogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating integrins. J Cell Biol 2003, 160:781-791. 10.1083/jcb.200208117, 2173358, 12615913.
27. Park YJ, Liu G, Lorne EF, Zhao X, Wang J, Tsuruta Y, Zmijewski J, Abraham E. PAI-1 inhibits neutrophil efferocytosis. Proc Natl Acad Sci U S A 2008, 105:11784-11789. 10.1073/pnas.0801394105, 2575264, 18689689.
28. Stefansson S, Lawrence DA. The serpin PAI-1 inhibits cell migration by blocking integrin alpha V beta 3 binding to vitronectin. Nature 1996, 383:441-443. 10.1038/383441a0, 8837777.
29. Deng G, Curriden SA, Wang S, Rosenberg S, Loskutoff DJ. Is plasminogen activator inhibitor-1 the molecular switch that governs urokinase receptor-mediated cell adhesion and release?. J Cell Biol 1996, 134:1563-1571. 10.1083/jcb.134.6.1563, 2120994, 8830783.
30. Kjoller L, Kanse SM, Kirkegaard T, Rodenburg KW, Ronne E, Goodman SL, Preissner KT, Ossowski L, Andreasen PA. Plasminogen activator inhibitor-1 represses integrin- and vitronectin-mediated cell migration independently of its function as an inhibitor of plasminogen activation. Exp Cell Res 1997, 232:420-429. 10.1006/excr.1997.3540, 9168821.
31. Kirchheimer JC, Binder BR, Remold HG. Matrix-bound plasminogen activator inhibitor type 1 inhibits the invasion of human monocytes into interstitial tissue. J Immunol 1990, 145:1518-1522.
32. Zhou A, Huntington JA, Pannu NS, Carrell RW, Read RJ. How vitronectin binds PAI-1 to modulate fibrinolysis and cell migration. Nat Struct Biol 2003, 10:541-544. 10.1038/nsb943, 12808446.
33. Kamikubo Y, Neels JG, Degryse B. Vitronectin inhibits plasminogen activator inhibitor-1-induced signalling and chemotaxis by blocking plasminogen activator inhibitor-1 binding to the low-density lipoprotein receptor-related protein. Int J Biochem Cell Biol 2009, 41:578-585. 10.1016/j.biocel.2008.07.006, 18703159.
34. Degryse B, Sier CF, Resnati M, Conese M, Blasi F. PAI-1 inhibits urokinase-induced chemotaxis by internalizing the urokinase receptor. FEBS Lett 2001, 505:249-254. 10.1016/S0014-5793(01)02797-1, 11566185.
35. Degryse B, Neels JG, Czekay RP, Aertgeerts K, Kamikubo Y, Loskutoff DJ. The low density lipoprotein receptor-related protein is a motogenic receptor for plasminogen activator inhibitor-1. J Biol Chem 2004, 279:22595-22604. 10.1074/jbc.M313004200, 15001579.
36. Harrison BH. Intercellular junctions in the developing mammalian thymus. Anat Histol Embryol 1977, 6:325-331. 10.1111/j.1439-0264.1977.tb00442.x, 146444.
37. Cao C, Lawrence DA, Li Y, Von Arnim CA, Herz J, Su EJ, Makarova A, Hyman BT, Strickland DK, Zhang L. Endocytic receptor LRP together with tPA and PAI-1 coordinates Mac-1-dependent macrophage migration. EMBO J 2006, 25:1860-1870. 10.1038/sj.emboj.7601082, 1456942, 16601674.
38. Gveric D, Herrera B, Petzold A, Lawrence DA, Cuzner ML. Impaired fibrinolysis in multiple sclerosis: a role for tissue plasminogen activator inhibitors. Brain 2003, 126:1590-1598. 10.1093/brain/awg167, 12805124.
39. Jacobsen JS, Comery TA, Martone RL, Elokdah H, Crandall DL, Oganesian A, Aschmies S, Kirksey Y, Gonzales C, Xu J, Zhou H, Atchison K, Wagner E, Zaleska MM, Das I, Arias RL, Bard J, Riddell D, Gardell SJ, Abou-Gharbia M, Robichaud A, Magolda R, Vlasuk GP, Bjornsson T, Reinhart PH, Pangalos MN. Enhanced clearance of Abeta in brain by sustaining the plasmin proteolysis cascade. Proc Natl Acad Sci U S A 2008, 105:8754-8759. 10.1073/pnas.0710823105, 2438386, 18559859.
40. Muracciole X, Romain S, Dufour H, Palmari J, Chinot O, Ouafik L, Grisoli F, Branger DF, Martin PM. PAI-1 and EGFR expression in adult glioma tumors: toward a molecular prognostic classification. Int J Radiat Oncol Biol Phys 2002, 52:592-598. 10.1016/S0360-3016(01)02699-2, 11849778.
41. Nagai N, Suzuki Y, Van Hoef B, Lijnen HR, Collen D. Effects of plasminogen activator inhibitor-1 on ischemic brain injury in permanent and thrombotic middle cerebral artery occlusion models in mice. J Thromb Haemost 2005, 3:1379-1384. 10.1111/j.1538-7836.2005.01466.x, 15978095.
42. Yang D, Nemkul N, Shereen A, Jone A, Dunn RS, Lawrence DA, Lindquist D, Kuan CY. Therapeutic administration of plasminogen activator inhibitor-1 prevents hypoxic-ischemic brain injury in newborns. J Neurosci 2009, 29:8669-8674. 10.1523/JNEUROSCI.1117-09.2009, 19587273.
43. Docagne F, Nicole O, Gabriel C, Fernandez-Monreal M, Lesne S, Ali C, Plawinski L, Carmeliet P, MacKenzie ET, Buisson A, Vivien D. Smad3-dependent induction of plasminogen activator inhibitor-1 in astrocytes mediates neuroprotective activity of transforming growth factor-beta 1 against NMDA-induced necrosis. Mol Cell Neurosci 2002, 21:634-644. 10.1006/mcne.2002.1206, 12504596.
44. Simon D, Martin-Bermejo MJ, Gallego-Hernandez MT, Pastrana E, Garcia-Escudero V, Garcia-Gomez A, Lim F, Diaz-Nido J, Avila J, Moreno-Flores MT. Expression of plasminogen activator inhibitor-1 by olfactory ensheathing glia promotes axonal regeneration. Glia 2011, 59:1458-1471. 10.1002/glia.21189, 21626571.
45. Xu Z, Balsara RD, Gorlatova NV, Lawrence DA, Castellino FJ, Ploplis VA. Conservation of critical functional domains in murine plasminogen activator inhibitor-1. J Biol Chem 2004, 279:17914-17920. 10.1074/jbc.M314197200, 14963029.
46. Lawrence DA, Berkenpas MB, Palaniappan S, Ginsburg D. Localization of vitronectin binding domain in plasminogen activator inhibitor-1. J Biol Chem 1994, 269:15223-15228.
47. Lee HJ, Im H. Purification of recombinant plasminogen activator inhibitor-1 in the active conformation by refolding from inclusion bodies. Protein Expr Purif 2003, 31:99-107. 10.1016/S1046-5928(03)00160-8, 12963346.
48. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 1990, 27:229-237. 10.1016/0165-5728(90)90073-V, 2110186.
49. Bocchini V, Mazzolla R, Barluzzi R, Blasi E, Sick P, Kettenmann H. An immortalized cell line expresses properties of activated microglial cells. J Neurosci Res 1992, 31:616-621. 10.1002/jnr.490310405, 1578513.
50. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980, 85:890-902. 10.1083/jcb.85.3.890, 2111442, 6248568.
51. Jeon H, Lee S, Lee WH, Suk K. Analysis of glial secretome: the long pentraxin PTX3 modulates phagocytic activity of microglia. J Neuroimmunol 2010, 229:63-72. 10.1016/j.jneuroim.2010.07.001, 20674043.
52. Saura J, Tusell JM, Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia 2003, 44:183-189. 10.1002/glia.10274, 14603460.
53. Ock J, Kim S, Yi KY, Kim NJ, Han HS, Cho JY, Suk K. A novel anti-neuroinflammatory pyridylimidazole compound KR-31360. Biochem Pharmacol 2009, 87:2578-2590.
54. Yin GN, Lee HW, Cho JY, Suk K. Neuronal pentraxin receptor in cerebrospinal fluid as a potential biomarker for neurodegenerative diseases. Brain Res 2009, 1265:158-170.
55. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007, 2:329-333.
56. Bassi R, Giussani P, Anelli V, Colleoni T, Pedrazzi M, Patrone M, Viani P, Sparatore B, Melloni E, Riboni L. HMGB1 as an autocrine stimulus in human T98G glioblastoma cells: role in cell growth and migration. J Neurooncol 2008, 87:23-33. 10.1007/s11060-007-9488-y, 17975708.
57. Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS. Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 2007, 21:108-116.
58. Ryu JK, Cho T, Choi HB, Wang YT, McLarnon JG. Microglial VEGF receptor response is an integral chemotactic component in Alzheimer's disease pathology. J Neurosci 2009, 29:3-13. 10.1523/JNEUROSCI.2888-08.2009, 19129379.
59. Wada M, Yoshimi K, Higo N, Ren YR, Mochizuki H, Mizuno Y, Kitazawa S. Statistical parametric mapping of immunopositive cell density. Neurosci Res 2006, 56:96-102. 10.1016/j.neures.2006.05.013, 16846658.
60. Kagan JC, Roy CR. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 2002, 4:945-954. 10.1038/ncb883, 12447391.
61. Park D, Han CZ, Elliott MR, Kinchen JM, Trampont PC, Das S, Collins S, Lysiak JJ, Hoehn KL, Ravichandran KS. Continued clearance of apoptotic cells critically depends on the phagocyte Ucp2 protein. Nature 2011, 477:220-224. 10.1038/nature10340, 21857682.
62. Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ, Bose N, Chan AS, Magee AS, Danielson ME, Weiss A, Vasilakos JP, Underhill DM. Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature 2011, 472:471-475. 10.1038/nature10071, 3084546, 21525931.
63. Greenbaum D, Luscombe NM, Jansen R, Qian J, Gerstein M. Interrelating different types of genomic data, from proteome to secretome: 'oming in on function. Genome Res 2001, 11:1463-1468. 10.1101/gr.207401, 11544189.
64. Grimmond SM, Miranda KC, Yuan Z, Davis MJ, Hume DA, Yagi K, Tominaga N, Bono H, Hayashizaki Y, Okazaki Y, Teasdale RD. The mouse secretome: functional classification of the proteins secreted into the extracellular environment. Genome Res 2003, 13:1350-1359. 10.1101/gr.983703, 403661, 12819133.
65. Dowell JA, Johnson JA, Li L. Identification of astrocyte secreted proteins with a combination of shotgun proteomics and bioinformatics. J Proteome Res 2009, 8:4135-4143. 10.1021/pr900248y, 2866504, 19469553.
66. Delcourt N, Jouin P, Poncet J, Demey E, Mauger E, Bockaert J, Marin P, Galeotti N. Difference in mass analysis using labeled lysines (DIMAL-K): a new, efficient proteomic quantification method applied to the analysis of astrocytic secretomes. Mol Cell Proteomics 2005, 4:1085-1094. 10.1074/mcp.M500040-MCP200, 15905179.
67. Suk K. Combined analysis of the glia secretome and the CSF proteome: neuroinflammation and novel biomarkers. Expert Rev Proteomics 2010, 7:263-274. 10.1586/epr.10.6, 20377392.
68. Liu RM. Oxidative stress, plasminogen activator inhibitor 1, and lung fibrosis. Antioxid Redox Signal 2008, 10:303-319. 10.1089/ars.2007.1903, 17979497.
69. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev 2008, 88:887-918. 10.1152/physrev.00033.2007, 2744109, 18626063.
70. Binder BR, Christ G, Gruber F, Grubic N, Hufnagl P, Krebs M, Mihaly J, Prager GW. Plasminogen activator inhibitor 1: physiological and pathophysiological roles. News Physiol Sci 2002, 17:56-61.
71. Aaronson DS, Horvath CM. A road map for those who don't know JAK-STAT. Science 2002, 296:1653-1655. 10.1126/science.1071545, 12040185.
72. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci 2004, 117:1281-1283. 10.1242/jcs.00963, 15020666.
73. Kovarik P, Stoiber D, Novy M, Decker T. Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J 1998, 17:3660-3668. 10.1093/emboj/17.13.3660, 1170702, 9649436.
74. Huang Y, Border WA, Yu L, Zhang J, Lawrence DA, Noble NA. A PAI-1 mutant, PAI-1R, slows progression of diabetic nephropathy. J Am Soc Nephrol 2008, 19:329-338. 10.1681/ASN.2007040510, 2396741, 18216319.
75. Cunningham O, Campion S, Perry VH, Murray C, Sidenius N, Docagne F, Cunningham C. Microglia and the urokinase plasminogen activator receptor/uPA system in innate brain inflammation. Glia 2009, 57:1802-1814. 10.1002/glia.20892, 2816357, 19459212.
76. Kim JW, Lee SH, Ko HM, Kwon KJ, Cho KS, Choi CS, Park JH, Kim HY, Lee J, Han SH, Ignarro LJ, Cheong JH, Kim WK, Shin CY. Biphasic regulation of tissue plasminogen activator activity in ischemic rat brain and in cultured neural cells: essential role of astrocyte-derived plasminogen activator inhibitor-1. Neurochem Int 2011, 58:423-433. 10.1016/j.neuint.2010.12.020, 21193004.
77. Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 1999, 17:593-623. 10.1146/annurev.immunol.17.1.593, 10358769.
78. Chan GC, Chan WK, Sze DM. The effects of beta-glucan on human immune and cancer cells. J Hematol Oncol 2009, 2:25. 10.1186/1756-8722-2-25, 2704234, 19515245.
79. Brown GD, Gordon S. Immune recognition. A new receptor for beta-glucans. Nature 2001, 413:36-37.
80. Scibelli A, Roperto S, Manna L, Pavone LM, Tafuri S, Della Morte R, Staiano N. Engagement of integrins as a cellular route of invasion by bacterial pathogens. Vet J 2007, 173:482-491. 10.1016/j.tvjl.2006.01.010, 16546423.
81. Schleef RR, Loskutoff DJ. Fibrinolytic system of vascular endothelial cells. Role of plasminogen activator inhibitors. Haemostasis 1988, 18:328-341.
82. Brown NJ. Therapeutic potential of plasminogen activator inhibitor-1 inhibitors. Ther Adv Cardiovasc Dis 2010, 4:315-324. 10.1177/1753944710379126, 20660535.
83. Vial D, McKeown-Longo PJ. PAI1 stimulates assembly of the fibronectin matrix in osteosarcoma cells through crosstalk between the alphavbeta5 and alpha5beta1 integrins. J Cell Sci 2008, 121:1661-1670. 10.1242/jcs.020149, 2535923, 18445685.
84. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318. 10.1016/0166-2236(96)10049-7, 8843599.
85. Lehnardt S, Lehmann S, Kaul D, Tschimmel K, Hoffmann O, Cho S, Krueger C, Nitsch R, Meisel A, Weber JR. Toll-like receptor 2 mediates CNS injury in focal cerebral ischemia. J Neuroimmunol 2007, 190:28-33. 10.1016/j.jneuroim.2007.07.023, 17854911.
86. Dellas C, Loskutoff DJ. Historical analysis of PAI-1 from its discovery to its potential role in cell motility and disease. Thromb Haemost 2005, 93:631-640.
87. Garg N, Goyal N, Strawn TL, Wu J, Mann KM, Lawrence DA, Fay WP. Plasminogen activator inhibitor-1 and vitronectin expression level and stoichiometry regulate vascular smooth muscle cell migration through physiological collagen matrices. J Thromb Haemost 2010, 8:1847-1854. 10.1111/j.1538-7836.2010.03907.x, 2941703, 20492459.
88. Stahl A, Mueller BM. Melanoma cell migration on vitronectin: regulation by components of the plasminogen activation system. Int J Cancer 1997, 71:116-122. 10.1002/(SICI)1097-0215(19970328)71:1<116::AID-IJC19>3.0.CO;2-G, 9096674.
89. Bajou K, Noel A, Gerard RD, Masson V, Brunner N, Holst-Hansen C, Skobe M, Fusenig NE, Carmeliet P, Collen D, Foidart JM. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat Med 1998, 4:923-928. 10.1038/nm0898-923, 9701244.
90. Bajou K, Maillard C, Jost M, Lijnen RH, Gils A, Declerck P, Carmeliet P, Foidart JM, Noel A. Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoral angiogenesis and growth. Oncogene 2004, 23:6986-6990. 10.1038/sj.onc.1207859, 15286708.
91. Marshall LJ, Ramdin LS, Brooks T, DPhil PC, Shute JK. Plasminogen activator inhibitor-1 supports IL-8-mediated neutrophil transendothelial migration by inhibition of the constitutive shedding of endothelial IL-8/heparan sulfate/syndecan-1 complexes. J Immunol 2003, 171:2057-2065.
92. Arndt PG, Young SK, Worthen GS. Regulation of lipopolysaccharide-induced lung inflammation by plasminogen activator Inhibitor-1 through a JNK-mediated pathway. J Immunol 2005, 175:4049-4059.
93. Osterholzer JJ, Christensen PJ, Lama V, Horowitz JC, Hattori N, Subbotina N, Cunningham A, Lin Y, Murdock BJ, Morey RE, Olszewski MA, Lawrence DA, Simon RH, Sisson TH. EPAI-1 promotes the accumulation of exudate macrophages and worsens pulmonary fibrosis following type II alveolar epithelial cell injury. J Pathol 2012,
94. Sanes JR. Extracellular matrix molecules that influence neural development. Annu Rev Neurosci 1989, 12:491-516. 10.1146/annurev.ne.12.030189.002423, 2648958.
95. Sobel RA. The extracellular matrix in multiple sclerosis lesions. J Neuropathol Exp Neurol 1998, 57:205-217. 10.1097/00005072-199803000-00001, 9600212.
96. Lo EH, Wang X, Cuzner ML. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J Neurosci Res 2002, 69:1-9. 10.1002/jnr.10270, 12111810.
97. Zmijewski JW, Bae HB, Deshane JS, Peterson CB, Chaplin DD, Abraham E. Inhibition of neutrophil apoptosis by PAI-1. Am J Physiol Lung Cell Mol Physiol 2011, 301:L247-L254. 10.1152/ajplung.00075.2011, 3154633, 21622848.
98. Gerold G, Ajaj KA, Bienert M, Laws HJ, Zychlinsky A, de Diego JL. A Toll-like receptor 2-integrin beta3 complex senses bacterial lipopeptides via vitronectin. Nat Immunol 2008, 9:761-768. 10.1038/ni.1618, 18516040.
99. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci U S A 2000, 97:13766-13771. 10.1073/pnas.250476497, 17650, 11095740.
100. Frasnelli ME, Tarussio D, Chobaz-Peclat V, Busso N, So A. TLR2 modulates inflammation in zymosan-induced arthritis in mice. Arthritis Res Ther 2005, 7:R370-R379. 10.1186/ar1494, 1065330, 15743485.
101. Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, Bassetti M, Aderem A. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 1999, 401:811-815. 10.1038/44605, 10548109.
102. Letiembre M, Echchannaoui H, Bachmann P, Ferracin F, Nieto C, Espinosa M, Landmann R. Toll-like receptor 2 deficiency delays pneumococcal phagocytosis and impairs oxidative killing by granulocytes. Infect Immun 2005, 73:8397-8401. 10.1128/IAI.73.12.8397-8401.2005, 1307087, 16299338.
103. De Taeye B, Smith LH, Vaughan DE. Plasminogen activator inhibitor-1: a common denominator in obesity, diabetes and cardiovascular disease. Curr Opin Pharmacol 2005, 5:149-154. 10.1016/j.coph.2005.01.007, 15780823.
104. Skurk T, Hauner H. Obesity and impaired fibrinolysis: role of adipose production of plasminogen activator inhibitor-1. Int J Obes Relat Metab Disord 2004, 28:1357-1364. 10.1038/sj.ijo.0802778, 15356668.
105. Schneider DJ. Abnormalities of coagulation, platelet function, and fibrinolysis associated with syndromes of insulin resistance. Coron Artery Dis 2005, 16:473-476. 10.1097/00019501-200512000-00003, 16319656.
106. Esposito K, Giugliano D. The metabolic syndrome and inflammation: association or causation?. Nutr Metab Cardiovasc Dis 2004, 14:228-232. 10.1016/S0939-4753(04)80048-6, 15673055.
107. Monteiro R, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediators Inflamm 2010, 2010:289645. 2913796, 20706689.