Neuroserpin protects neurons from ischemia-induced plasmin-mediated cell death independently of tissue-type plasminogen activator inhibition

American Journal of Pathology

Volumn 177, Issue 5, 2010, Pages 2576-2584

  Wu, Jialing ^a,b   Echeverry, Ramiro ^a   Guzman, Johanna ^a   Yepes, Manuel ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIZOCILPINE; EXCITOTOXIN; KAINIC ACID; NEUROSERPIN; PLASMIN; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN ISCHEMIA; CONTROLLED STUDY; GENE OVEREXPRESSION; HIPPOCAMPUS; IN VITRO STUDY; INHIBITION KINETICS; ISCHEMIC PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 78149324499     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100466     Document Type: Article

References (34)

1. Bugge TH, Kombrinck KW, Flick MJ, Daugherty CC, Danton MJ, Degen JL: Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 1996, 87:709-719
2. Polavarapu R, Gongora MC, Yi H, Ranganthan S, Lawrence DA, Strickland D, Yepes M: Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood 2007, 109:3270-3278
3. Qian Z, Gilbert ME, Colicos MA, Kandel ER, Kuhl D: Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 1993, 361:453-457
4. Seeds NW, Williams BL, Bickford PC: Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 1995, 270:1992-1994
5. Yepes M, Sandkvist M, Coleman TA, Moore E, Wu JY, Mitola D, Bugge TH, Lawrence DA: Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. J Clin Invest 2002, 109:1571-1578
6. Mataga N, Nagai N, Hensch TK: Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA 2002, 99:7717-7721
7. Tsirka SE, Gualandris A, Amaral DG, Strickland S: Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 1995, 377:340-344
8. Yepes M, Sandkvist M, Wong MK, Coleman TA, Smith E, Cohan SL, Lawrence DA: Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 2000, 96:569-576
9. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, Sonderegger P: Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 1996, 15:2944-2953
10. 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 localized primarily in neurons: implications for the regulation of motor learning and neuronal survival. J Biol Chem 1997, 272:33062-33067
11. Lloyd-Jones D, Adams R, Carnethon M, De SG, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, O'Donnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y: Heart disease and stroke statistics- 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009, 119:480-486
12. Berger P, Kozlov SV, Cinelli P, Kruger SR, Vogt L, Sonderegger P: Neuronal depolarization enhances the transcription of the neuronal serine protease inhibitor neuroserpin. Mol Cell Neurosci 1999, 14:455-467
13. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, Lipton SA: Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 1998, 4:228-231
14. Cinelli P, Madani R, Tsuzuki N, Vallet P, Arras M, Zhao CN, Osterwalder T, Rulicke T, Sonderegger P: Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol Cell Neurosci 2001, 18:443-457
15. Kitagawa K, Matsumoto M, Kuwabara K, Tagaya M, Ohtsuki T, Hata R, Ueda H, Handa N, Kimura K, Kamada T: "Ischemic tolerance" phenomenon detected in various brain regions. Brain Res 1991, 561:203-211
16. Echeverry R, Wu J, Haile WB, Guzman J, Yepes M: Tissue-type plasminogen activator is a neuroprotectant in the mouse hippocampus. J Clin Invest 2010, 120:2194-2205
17. Zhang X, Polavarapu R, She H, Mao Z, Yepes M: Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappaB pathway activation. Am J Pathol 2007, 171:1281-1290
18. Belayev L, Busto R, Zhao W, Fernandez G, Ginsberg MD: Middle cerebral artery occlusion in the mouse by intraluminal suture coated with poly-L-lysine: neurological and histological validation. Brain Res 1999, 833:181-190
19. Stagliano NE, Perez-Pinzon MA, Moskowitz MA, Huang PL: Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 1999, 19:757-761
20. Paxinos G, Franklin KBJ: The Mouse Brain in Stereotaxic Coordinates. San Diego, Academic Press Inc., 2001, pp 1-93
21. Zhang X, Winkles JA, Gongora MC, Polavarapu R, Michaelson JS, Hahm K, Burkly L, Friedman M, Li XJ, Yepes M: TWEAK-Fn14 pathway inhibition protects the integrity of the neurovascular unit during cerebral ischemia. J Cereb Blood Flow Metab 2007, 27:534-544
22. Greene JG, Borges K, Dingledine R: Quantitative transcriptional neuroanatomy of the rat hippocampus: evidence for wide-ranging, pathway-specific heterogeneity among three principal cell layers. Hippocampus 2009, 19:253-264
23. 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, 92:358-368
24. Osterwalder T, Cinelli P, Baici A, Pennella A, Krueger SR, Schrimpf SP, Meins M, Sonderegger P: The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators, and plasmin but not thrombin. J Biol Chem 1998, 273:2312-2321
25. Mannaioni G, Orr AG, Hamill CE, Yuan H, Pedone KH, McCoy KL, Palmini RB, Junge CE, Lee CJ, Yepes M, Hepler JR, Traynelis SF: Plasmin potentiates synaptic N-methyl-D-aspartate receptor function in hippocampal neurons through activation of protease-activated receptor-1. J Biol Chem 2008, 283:20600-20611
26. Yuan H, Vance KM, Junge CE, Geballe MT, Snyder JP, Hepler JR, Yepes M, Low CM, Traynelis SF: The serine protease plasmin cleaves the amino-terminal domain of the NR2A subunit to relieve zinc inhibition of the N-methyl-D-aspartate receptors. J Biol Chem 2009, 284:12862-12873
27. Tsirka SE, Bugge TH, Degen JL, Strickland S: Neuronal death in the central nervous system demonstrates a non-fibrin substrate for plasmin. Proc Natl Acad Sci USA 1997, 94:9779-9781
28. Seeds NW, Basham ME, Ferguson JE: Absence of tissue plasminogen activator gene or activity impairs mouse cerebellar motor learning. J Neurosci 2003, 23:7368-7375
29. Baranes D, Lederfein D, Huang YY, Chen M, Bailey CH, Kandel ER: Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 1998, 21:813-825
30. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA: Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 2003, 112:1533-1540
31. Yepes M, Lawrence DA: Neuroserpin: a selective inhibitor of tissue-type plasminogen activator in the central nervous system. Thromb Haemost 2004, 91:457-464 (Pubitemid 38396867)
32. Madani R, Kozlov S, Akhmedov A, Cinelli P, Kinter J, Lipp HP, Sonderegger P, Wolfer DP: Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol Cell Neurosci 2003, 23:473-494
33. Lee TW, Coates LC, Birch NP: Neuroserpin regulates N-cadherin-mediated cell adhesion independently of its activity as an inhibitor of tissue plasminogen activator. J Neurosci Res 2008, 86:1243-1253
34. Yamada M, Takahashi K, Ukai W, Hashimoto E, Saito T, Yamada M: Neuroserpin is expressed in early stage of neurogenesis in adult rat hippocampus. Neuroreport 2010, 21:138-142