Deficiency in Serine Protease Inhibitor Neuroserpin Exacerbates Ischemic Brain Injury by Increased Postischemic Inflammation

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Gelderblom, Mathias ^a   Neumann, Melanie ^a   Ludewig, Peter ^a   Bernreuther, Christian ^a   Krasemann, Susanne ^a   Arunachalam, Priyadharshini ^a   Gerloff, Christian ^a   Glatzel, Markus ^a   Magnus, Tim ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROSERPIN; TISSUE PLASMINOGEN ACTIVATOR; NEUROPEPTIDE; SERINE PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL ACTIVATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE EXACERBATION; FIBRINOLYSIS; INFLAMMATION; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN DEFICIENCY; PROTEIN FUNCTION; ANIMAL; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; SECRETION (PROCESS);

ANIMALIA; MUS;

ANIMALS; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; INFLAMMATION; MICE; MICE, KNOCKOUT; MICROGLIA; NEUROPEPTIDES; NEUTROPHIL INFILTRATION; SERPINS; STROKE; TISSUE PLASMINOGEN ACTIVATOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877053029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063118     Document Type: Article

References (32)

1. Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, et al. (2011) Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol 10: 471-480.
2. Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, et al. (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 359: 1317-1329.
3. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, et al. (1998) Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 4: 228-231.
4. Nagai N, De Mol M, Lijnen HR, Carmeliet P, Collen D, (1999) Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation 99: 2440-2444.
5. Yepes M, Sandkvist M, Wong MK, Coleman TA, Smith E, et al. (2000) Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 96: 569-576.
6. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, Sonderegger P, (1996) Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 15: 2944-2953.
7. Osterwalder T, Cinelli P, Baici A, Pennella A, Krueger SR, et al. (1998) The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J Biol Chem 273: 2312-2321.
8. Cinelli P, Madani R, Tsuzuki N, Vallet P, Arras M, et al. (2001) Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol Cell Neurosci 18: 443-457.
9. Cole JW, Naj AC, O'Connell JR, Stine OC, Sorkin JD, et al. (2007) Neuroserpin polymorphisms and stroke risk in a biracial population: the stroke prevention in young women study. BMC Neurol 7: 37.
10. Rodriguez-Gonzalez R, Sobrino T, Rodriguez-Yanez M, Millan M, Brea D, et al. (2011) Association between neuroserpin and molecular markers of brain damage in patients with acute ischemic stroke. J Transl Med 9: 58.
11. Tjarnlund-Wolf A, Olsson S, Jood K, Blomstrand C, Jern C, (2011) No evidence for an association between genetic variation at the SERPINI1 locus and ischemic stroke. J Neurol 258: 1885-1887.
12. Dirnagl U, (2006) Bench to bedside: the quest for quality in experimental stroke research. J Cereb Blood Flow Metab 26: 1465-1478.
13. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, et al. (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 112: 1533-1540.
14. Galliciotti G, Glatzel M, Kinter J, Kozlov SV, Cinelli P, et al. (2007) Accumulation of mutant neuroserpin precedes development of clinical symptoms in familial encephalopathy with neuroserpin inclusion bodies. Am J Pathol 170: 1305-1313.
15. Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, et al. (2009) Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 40: 1849-1857.
16. Siao CJ, Tsirka SE, (2002) Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 22: 3352-3358.
17. Iadecola C, Anrather J, (2011) The immunology of stroke: from mechanisms to translation. Nat Med 17: 796-808.
18. Hastings GA, Coleman TA, Haudenschild CC, Stefansson S, Smith EP, et al. (1997) 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 272: 33062-33067.
19. Siao CJ, Fernandez SR, Tsirka SE, (2003) Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J Neurosci 23: 3234-3242.
20. Yepes M, Roussel BD, Ali C, Vivien D, (2009) Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci 32: 48-55.
21. Zhang C, An J, Haile WB, Echeverry R, Strickland DK, et al. (2009) Microglial low-density lipoprotein receptor-related protein 1 mediates the effect of tissue-type plasminogen activator on matrix metalloproteinase-9 activity in the ischemic brain. J Cereb Blood Flow Metab 29: 1946-1954.
22. Chen H, Song YS, Chan PH, (2009) Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. J Cereb Blood Flow Metab 29: 1262-1272.
23. Iadecola C, Zhang F, Xu X, (1995) Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am J Physiol 268: R286-292.
24. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, et al. (2006) Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281: 21362-21368.
25. del Zoppo GJ, Milner R, Mabuchi T, Hung S, Wang X, et al. (2007) Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke 38: 646-651.
26. Shohami E, Ginis I, Hallenbeck JM, (1999) Dual role of tumor necrosis factor alpha in brain injury. Cytokine Growth Factor Rev 10: 119-130.
27. Zhang C, An J, Strickland DK, Yepes M, (2009) The low-density lipoprotein receptor-related protein 1 mediates tissue-type plasminogen activator-induced microglial activation in the ischemic brain. Am J Pathol 174: 586-594.
28. Yenari MA, Kauppinen TM, Swanson RA, (2010) Microglial activation in stroke: therapeutic targets. Neurotherapeutics 7: 378-391.
29. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J, (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27: 2596-2605.
30. Neumann J, Sauerzweig S, Ronicke R, Gunzer F, Dinkel K, et al. (2008) Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J Neurosci 28: 5965-5975.
31. Lees KR, Bluhmki E, von Kummer R, Brott TG, Toni D, et al. (2010) Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet 375: 1695-1703.
32. Copin JC, Bengualid DJ, Da Silva RF, Kargiotis O, Schaller K, et al. (2011) Recombinant tissue plasminogen activator induces blood-brain barrier breakdown by a matrix metalloproteinase-9-independent pathway after transient focal cerebral ischemia in mouse. Eur J Neurosci 34: 1085-1092.