Contributions of multiple proteases to neurotoxicity in a mouse model of intracerebral haemorrhage

Brain

Volumn 132, Issue 1, 2009, Pages 26-36

  Xue, Mengzhou ^a,b   Fan, Yan ^a,b   Liu, Shuhong ^a,b   Zygun, David A ^b   Demchuk, Andrew ^a,b   Yong, V Wee ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Metalloproteinases; MMPs; Neuronal death; Stroke; Thrombin

Indexed keywords

GELATINASE B; HIRUDIN; STROMELYSIN; THROMBIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD AUTOTRANSFUSION; BRAIN DAMAGE; BRAIN HEMORRHAGE; CELL KILLING; CONTROLLED STUDY; CORPUS STRIATUM; DRUG TARGETING; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO CULTURE; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; BRAIN; CELL DEATH; CELLS, CULTURED; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; GENOTYPE; HUMANS; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MICE; MICE, KNOCKOUT; NEURONS; THROMBIN;

EID: 58849121775     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn215     Document Type: Article

References (41)

1. Abilleira S, Montaner J, Molina CA, Monasterio J, Castillo J, Alvarez-Sabin J. Matrix metalloproteinase-9 concentration after spontaneous intracerebral hemorrhage. J Neurosurg 2003; 99: 65-70.
2. Agrawal SM, Lau L, Yong VW. MMPs in the central nervous system: where the good guys go bad. Semin Cell Dev Biol 2008; 19: 42-51.
3. Alvarez-Sabin J, Delgado P, Abilleira S, Molina CA, Arenillas J, Ribo M, et al. Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: relationship to clinical and radiological outcome. Stroke 2004; 35: 1316-22.
4. Broderick JP, Diringer MN, Hill MD, Brun NC, Mayer SA, Steiner T, et al. Determinants of intracerebral hemorrhage growth: an exploratory analysis. Stroke 2007; 38: 1072-5.
5. Castellanos M, Leira R, Serena J, Pumar JM, Lizasoain I, Castillo J, et al. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 2003; 34: 40-6.
6. Chen ZL, Strickland S. Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 1997; 91: 917-25.
7. Duhamel-Clerin E, Orvain C, Lanza F, Cazenave JP, Klein-Soyer C. Thrombin receptor-mediated increase of two matrix metalloproteinases, MMP-1 and MMP-3, in human endothelial cells. Arterioscler Thromb Vasc Biol 1997; 17: 1931-8.
8. Falo MC, Fillmore HL, Reeves TM, Phillips LL. Matrix metalloproteinase-3 expression profile differentiates adaptive and maladaptive synaptic plasticity induced by traumatic brain injury. J Neurosci Res 2006; 84: 768-81.
9. Fenton JW 2nd, Villanueva GB, Ofosu FA, Maraganore JM. Thrombin inhibition by hirudin: how hirudin inhibits thrombin. Haemostasis 1991; 21 (Suppl 1): 27-31.
10. Geurts N, Martens E, Van Aelst I, Proost P, Opdenakker G, Van den Steen PE. Beta-hematin interaction with the hemopexin domain of gelatinase B/MMP-9 provokes autocatalytic processing of the propeptide, thereby priming activation by MMP-3. Biochemistry 2008; 47: 2689-99.
11. Grossetete M, Rosenberg GA. Matrix metalloproteinase inhibition facilitates cell death in intracerebral hemorrhage in mouse. J Cereb Blood Flow Metab 2008; 28: 752-63.
12. Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, Strongin A, et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 2002; 297: 1186-90.
13. Gurney KJ, Estrada EY, Rosenberg GA. Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol Dis 2006; 23: 87-96.
14. Hu J, Van den Steen PE, Sang QX, Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 2007; 6: 480-98.
15. Hua Y, Keep RF, Hoff JT, Xi G. Brain injury after intracerebral hemorrhage: the role of thrombin and iron. Stroke 2007; 38: 759-62.
16. Jourquin J, Tremblay E, Decanis N, Charton G, Hanessian S, Chollet AM, et al. Neuronal activity-dependent increase of net matrix metalloproteinase activity is associated with MMP-9 neurotoxicity after kainate. Eur J Neurosci 2003; 18: 1507-17.
17. Kim YS, Choi DH, Block ML, Lorenzl S, Yang L, Kim YJ, et al. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J 2007; 21: 179-87.
18. Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH, et al. Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 2005; 25: 3701-11.
19. Mayer SA, Brun NC, Broderick J, Davis S, Diringer MN, Skolnick BE, et al. Safety and feasibility of recombinant factor VIIa for acute intracerebral hemorrhage. Stroke 2005; 36: 74-9.
20. Mudgett JS, Hutchinson NI, Chartrain NA, Forsyth AJ, McDonnell J, Singer II, et al. Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis Rheum 1998; 41: 110-21.
21. Newman TA, Woolley ST, Hughes PM, Sibson NR, Anthony DC, Perry VH. T-cell- and macrophage-mediated axon damage in the absence of a CNS-specific immune response: involvement of metalloproteinases. Brain 2001; 124: 2203-14.
22. Ogata Y, Enghild JJ, Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor for the human matrix metalloproteinase 9. J Biol Chem 1992; 267: 3581-4.
23. Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8: 221-33.
24. Powell WC, Fingleton B, Wilson CL, Boothby M, Matrisian LM. The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis. Curr Biol 1999; 9: 1441-7.
25. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, et al. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol 2003; 53: 731-42.
26. Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernandez-Cadenas I, Ribo M, Molina CA, et al. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 2006; 37: 1399-406.
27. Rosenberg GA, Cunningham LA, Wallace J, Alexander S, Estrada EY, Grossetete M, et al. Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res 2001; 893: 104-12.
28. Rosenberg GA, Navratil M. Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat. Neurology 1997; 48: 921-6.
29. Si-Tayeb K, Monvoisin A, Mazzocco C, Lepreux S, Decossas M, Cubel G, et al. Matrix metalloproteinase 3 is present in the cell nucleus and is involved in apoptosis. Am J Pathol 2006; 169: 1390-401.
30. Suzuki Y, Nagai N, Umemura K, Collen D, Lijnen HR. Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice. J Thromb Haemost 2007; 5: 1732-9.
31. Vecil GG, Larsen PH, Corley SM, Herx LM, Besson A, Goodyer CG, et al. Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J Neurosci Res 2000; 61: 212-24.
32. Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998; 93: 411-22.
33. Wang J, Dore S. Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab 2007; 27: 894-908.
34. Wang J, Tsirka SE. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 2005; 128: 1622-33.
35. Wells JE, Biernaskie J, Szymanska A, Larsen PH, Yong VW, Corbett D. Matrix metalloproteinase (MMP)-12 expression has a negative impact on sensorimotor function following intracerebral haemorrhage in mice. Eur J Neurosci 2005; 21: 187-96.
36. Wetzel M, Rosenberg GA, Cunningham LA. Tissue inhibitor of metalloproteinases-3 and matrix metalloproteinase-3 regulate neuronal sensitivity to doxorubicin-induced apoptosis. Eur J Neurosci 2003; 18: 1050-60.
37. Xue M, Del Bigio MR. Injections of blood, thrombin and plasminogen more severely damage neonatal mouse brain than mature mouse brain. Brain Pathol 2005; 15: 273-80.
38. Xue M, Hollenberg MD, Yong VW. Combination of thrombin and matrix metalloproteinase-9 exacerbates neurotoxicity in cell culture and intracerebral hemorrhage in mice. J Neurosci 2006; 26: 10281-91.
39. Yong VW. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 2005; 6: 931-44.
40. Yong VW, Power C, Forsyth P, Edwards DR. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001; 2: 502-11.
41. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, et al. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 2006; 12: 441-5.