Chronic relapsing experimental allergic encephalomyelitis (CREAE) in plasminogen activator inhibitor-1 knockout mice: The effect of fibrinolysis during neuroinflammation

Neuropathology and Applied Neurobiology

Volumn 34, Issue 2, 2008, Pages 216-230

  East, E ^a   Gveric D ^a   Baker, D ^a   Pryce, G ^a   Lijnen, H R ^b   Cuzner, M L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Experimental allergic encephalomyelitis; Fibrinolysis; Multiple sclerosis; Plasminogen; Plasminogen activator inhibitor 1

Indexed keywords

FIBRIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; TISSUE PLASMINOGEN ACTIVATOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CLINICAL EXAMINATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE SEVERITY; ENCEPHALITIS; FIBRINOLYSIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INCIDENCE; KNOCKOUT MOUSE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; WILD TYPE;

ANIMALS; AXONS; BLOTTING, WESTERN; CHRONIC DISEASE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBRINOLYSIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICE; MICE, KNOCKOUT; PLASMINOGEN ACTIVATOR INHIBITOR 1; SPINAL CORD; TISSUE PLASMINOGEN ACTIVATOR;

EID: 40149098058     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2007.00889.x     Document Type: Article

References (54)

1. East E, Baker D, Pryce G, Lijnen HR, Cuzner ML, Gveric D. A role for the plasminogen activator system in inflammation and neurodegeneration in the central nervous system during experimental allergic encephalomyelitis. Am J Pathol 2005 167 : 545 54
2. Gveric D, Hanemaaijer R, Newcombe J, van Lent NA, Sier CF, Cuzner ML. Plasminogen activators in multiple sclerosis lesions: implications for the inflammatory response and axonal damage. Brain 2001 124 : 1978 88
3. 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
4. Teesalu T, Hinkkanen AE, Vaheri A. Coordinated induction of extracellular proteolysis systems during experimental autoimmune encephalomyelitis in mice. Am J Pathol 2001 159 : 2227 37
5. Gveric D, Herrera BM, Cuzner ML. Impaired fibrinolysis in multiple sclerosis: a role for tissue plasminogen activator inhibitors. Brain 2003 126 : 1590 8
6. Akenami FO, Koskiniemi M, Farkkila M, Vaheri A. Cerebrospinal fluid plasminogen activator inhibitor-1 in patients with neurological disease. J Clin Pathol 1997 50 : 157 60
7. Akassoglou K, Kombrinck KW, Degen JL, Strickland S. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol 2000 149 : 1157 66
8. Paterson PY. Experimental allergic encephalomyelitis: a role of fibrin deposition in immunopathogenesis of inflammation in rats. Fed Proc 1976 35 : 2428 35
9. Koh CS, Gausas J, Paterson PY. Neurovascular permeability and fibrin deposition in the central neuraxis of Lewis rats with cell-transferred experimental allergic encephalomyelitis in relationship to clinical and histopathological features of the disease. J Neuroimmunol 1993 47 : 141 5
10. 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
11. Carmeliet P, Bouche A, De Clercq C, Janssen S, Pollefeyt S, Wyns S, Mulligan RC, Collen D. Biological effects of disruption of the tissue-type plasminogen activator, urokinase-type plasminogen activator, and plasminogen activator inhibitor-1 genes in mice. Ann N Y Acad Sci 1995 17 : 367 81
12. Carmeliet P, Kieckens L, Schoonjans L, Ream B, van Nuffelen A, Prendergast G, Cole M, Bronson R, Collen D, Mulligan RC. Plasminogen activator inhibitor-1 gene-deficient mice. I. Generation by homologous recombination and characterisation. J Clin Invest 1993 92 : 2746 55
13. Baker D, O'Neill JK, Gschmeissner SE, Wilcox CE, Butter C, Turk JL. Induction of chronic relapsing experimental allergic encephalomyelitis in Biozzi mice. J Neuroimmunol 1990 28 : 261 70
14. Levine S, Sowinski R. Experimental allergic encephalomyelitis in inbred and outbred mice. J Immunol 1973 110 : 139 43
15. Allen SJ, Baker D, O'Neill JK, Davison AN, Turk JL. Isolation and characterization of cells infiltrating the spinal cord during the course of chronic relapsing experimental allergic encephalomyelitis in the Biozzi AB/H mouse. Cell Immunol 1993 146 : 335 50
16. Gveric D, Cuzner ML, Newcombe J. Insulin-like growth factors and binding proteins in multiple sclerosis plaques. Neuropathol Appl Neurobiol 1999 25 : 215 25
17. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951 193 : 265 75
18. Declerck PJ, Verstreken M, Collen D. Immunoassay of murine t-PA, u-PA and PAI-1 using monoclonal antibodies raised in gene-inactivated mice. Thromb Haemost 1995 74 : 1305 9
19. Urano T, Takada Y, Ihara H, Takada A. Re-examination of the extent of the activation of Lys(78) plasminogen by tissue plasminogen activator in the presence of polymerised fibrin. Haemostasis 1996 26 : 220 7
20. Pryce G, Ahmed Z, Hankey DJ, Jackson SJ, Croxford JL, Pocock JM, Lendent C, Petzold A, Thompson AJ, Giovannoni G, Cuzner ML, Baker D. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003 126 : 2191 202
21. Butter C, Baker D, O'Neill JK, Turk JL. Mononuclear cell trafficking and plasma protein extravasation into the CNS during chronic relapsing experimental allergic encephalomyelitis in Biozzi AB/H mice. J Neurol Sci 1991 104 : 9 12
22. Johnson GV, Jope RS. The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res 1992 33 : 505 12
23. Matesic DF, Lin RCS. Microtubule-associated protein as an early indicator of ischemia-induced neurodegeneration in the gerbil forebrain. J Neurochem 1994 63 : 1012 20
24. Zhu B, Luo L, Moore GRW, Paty DW, Cynader MS. Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis. Am J Pathol 2003 162 : 1639 50
25. Kerschensteiner M, Bareyre FM, Buddeberg BS, Merkler D, Stadelmann C, Brück W, Misgeld T, Schwab ME. Remodelling of axonal connections contributes to recovery in an animal model of multiple sclerosis. J Exp Med 2004 200 : 1027 38
26. Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 2006 67 : 960 7
27. Claudio L, Raine CS, Brosnan CF. Evidence of persistent blood-brain barrier abnormalities in chronic progressive multiple sclerosis. Acta Neuropathol 1995 30 : 228 38
28. 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 40
29. Loskutoff DJ, Curriden SA, Hu G, Deng G. Regulation of cell adhesion by PAI-1. APMIS 1999 107 : 54 61
30. Hertig A, Rondeau E. Plasminogen activator inhibitor type 1: two faces of the same coin. Curr Opin Nephr Hyper 2004 13 : 39 44
31. 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 71
32. Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 1997 20 : 84 91
33. Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM. Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 2006 67 : 960 7
34. Bogdanovic N, Davidsson P, Volkmann I, Winblad B, Blennow K. Growth-associated protein GAP-43 in the front cortex and in the hippocampus in Alzheimer's disease: an immunohistochemical and quantitative study. J Neural Transm 2000 107 : 463 78
35. Thompson SN, Gibson TR, Thompson BM, Deng Y, Hall ED. Relationship of calpain-mediated proteolysis to the expression of axonal and synaptic plasticity markers following traumatic brain injury in mice. Exp Neurol 2006 201 : 253 65
36. Akassoglou K, Wei-Ming Y, Akpinar P, Strickland S. Fibrin inhibits peripheral nerve remyelination by regulating schwann cell differentiation. Neuron 2002 33 : 861 75
37. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K. Fibrinogen inhibits neurite outgrowth via beta3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci 2007 104 : 11814 19
38. Huber K. Plasminogen activator inhibitor type-1 (part one): basic mechanisms, regulation and role for thromboembolic disease. J Thromb Thrombolysis 2001 11 : 183 93
39. Kasza A, Kowanetz M, Poslednik K, Witek B, Kordula T, Koj A. Epidermal growth factor and pro-inflammatory cytokines regulate the expression of components of the plasminogen activator system in U373-MG astrocytoma cells. Cytokine 2001 16 : 187 90
40. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001 167 : 2887 94
41. Flick MJ, Du X, Witte DP, Jirouskova M, Soloview DA, Busuttil SJ, Plow EF, Degen JL. Leukocyte engagement of fibrin(ogen) via the integrin receptor αMβ2/Mac-1 is critical for host inflammatory response in vitro. J Clin Invest 2004 113 : 1596 606
42. Adams RA, Passino M, Sachs BD, Nuriel T, Akassoglou K. Fibrin mechanisms and functions in nervous system pathology. Mol Interv 2004 4 : 163 76
43. Cruz-Topete D, Iwaki T, Ploplis V, Castellino F. Delayed inflammatory responses to endotoxin in fibrinogen-deficient mice. J Pathol 2006 210 : 325 33
44. Languino LR, Duperray A, Joganic KJ, Fornaro M, Thornton GB, Altieri DC. Regulation of leukocyte-endothelium interaction and leukocyte transendothelial migration by intracellular adhesion molecule 1-fibrinogen recognition. Proc Natl Acad Sci USA 1995 92 : 1505 9
45. Akassoglou K, Adams RA, Bauer J, Mercado P, Tseveleki V, Lassmann H, Probert L, Strickland S. Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumour necrosis factor transgenic mouse model for multiple sclerosis. Proc Natl Acad Sci USA 2004 101 : 6698 703
46. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, Akassoglou K. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 2007 204 : 571 82
47. Strickland DK, Ranganathan S. Diverse role of LDL receptor-related protein in the clearance of proteases and in signaling. J Thromb Haemost 2003 1 : 1663 70
48. Rogove AD, Siao C, Keyt B, Strickland S, Tsirka SE. Activation of microglia reveals a non-proteolytic cytokine function for tissue plasminogen activator in the central nervous system. J Cell Sci 1999 112 (Pt 22 4007 16
49. Dobrovolsky AB, Titaeva EV. The fibrinolysis system: regulation of activity and physiologic functions of its main components. Biochemistry (Mosc) 2002 67 : 99 108
50. Irigoyen JP, Muñoz-Cánoves P, Montero L, Koziczak M, Nagamine Y. The plasminogen activator system: biology and regulation. Cell Mol Life Sci 1999 56 : 104 32
51. Hastings GA, Coleman TA, Haudenschild CC, Stefansson S, Smith EP, Barthlow R, Cherry S, Sandkvist M, Lawrence DA. Neuroserpin, a brain-associated inhibitor of tissue plasminogen activator is localised primarily in neurons. J Biol Chem 1997 272 : 33062 7
52. Teesalu T, Kulla A, Simisker A, Siren V, Lawrence DA, Asser T, Vaheri A. Tissue plasminogen activator and neuroserpin are widely expressed in the human central nervous system. Thromb Haemost 2004 92 : 358 68
53. Leik CE, Su EJ, Nambi P, Crandall DL, Lawrence DA. Effect of pharmacologic PAI-1 inhibition on cell motility and tumor angiogenesis. J Thromb Haemost 2006 4 : 2710 5
54. Gorlatova NV, Cale JM, Elokdah H, Li D, Fan K, Warnock M, Crandall DL, Lawrence DA. Mechanism of inactivation of plasminogen activator inhibitor-1 by a small molecule inhibitor. J Biol Chem 2007 282 : 9288 96