Recombinant tissue plasminogen activator enhances microglial cell recruitment after stroke in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 5, 2014, Pages 802-812

  Lenglet, Sébastien ^a   Montecucco, Fabrizio ^a,b   Denes, Adam ^c   Coutts, Graham ^c   Pinteaux, Emmanuel ^c   Mach, François ^a   Schaller, Karl ^a,d   Gasche, Yvan ^a,d   Copin, Jean Christophe ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

animal model; brain ischemia; CCL3; innate immunity; tPA

Indexed keywords

ALTEPLASE; CELL ADHESION MOLECULE; CXCL1 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FRACTALKINE; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BRAIN INFARCTION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; ENDOTHELIUM CELL; HEMISPHERE; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BRAIN; CHEMOKINE CCL3; GENE EXPRESSION REGULATION; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MICE; MICROGLIA; RECOMBINANT PROTEINS; RNA, MESSENGER; TISSUE PLASMINOGEN ACTIVATOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84899971257     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.9     Document Type: Article

References (43)

1. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 2010; 87: 779-789.
2. Eltzschig HK, Eckle T. Ischemia and reperfusion-from mechanism to translation. Nat Med 2011; 17: 1391-1401.
3. Gloire G, Legrand-Poels S, Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol 2006; 72: 1493-1505.
4. Rossi B, Angiari S, Zenaro E, Budui SL, Constantin G. Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyteendothelial interactions. J Leukoc Biol 2010; 89: 539-556.
5. Mirabelli-Badenier M, Braunersreuther V, Viviani GL, Dallegri F, Quercioli A, Veneselli E et al. CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke. Thromb Haemost 2011; 105: 409-420.
6. Takami S, Minami M, Nagata I, Namura S, Satoh M. Chemokine receptor antagonist peptide, viral MIP-II, protects the brain against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2001; 21: 1430-1435.
7. Zhang L, Zhang ZG, Zhang RL, Lu M, Krams M, Chopp M. Effects of a selective CD11b/CD18 antagonist and recombinant human tissue plasminogen activator treatment alone and in combination in a rat embolic model of stroke. Stroke 2003; 34: 1790-1795.
8. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM. The promise of minocycline in neurology. Lancet Neurol 2004; 3: 744-751.
9. Lees KR, Bluhmki E, von Kummer R, Brott TG, Toni D, Grotta JC et al. Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet 2010; 375: 1695-1703.
10. Vivien D, Gauberti M, Montagne A, Defer G, Touze E. Impact of tissue plasminogen activator on the neurovascular unit: from clinical data to experimental evidence. J Cereb Blood Flow Metab 2011; 31: 2119-2134.
11. 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.
12. Siao CJ, Fernandez SR, Tsirka SE. Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J Neurosci 2003; 23: 3234-3242.
13. Reijerkerk A, Kooij G, van der Pol SM, Leyen T, van Het Hof B, Couraud PO et al. Tissue-type plasminogen activator is a regulator of monocyte diapedesis through the brain endothelial barrier. J Immunol 2008; 181: 3567-3574.
14. Miyazaki T, Kimura Y, Ohata H, Hashimoto T, Shibata K, Hasumi K et al. Distinct effects of tissue-type plasminogen activator and SMTP-7 on cerebrovascular inflammation following thrombolytic reperfusion. Stroke 2011; 42: 1097-1104.
15. Copin JC, Bengualid DJ, Da Silva RF, Kargiotis O, Schaller K, Gasche Y. 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 2011; 34: 1085-1092.
16. Korninger C, Collen D. Studies on the specific fibrinolytic effect of human extrinsic (tissue-type) plasminogen activator in human blood and in various animal species in vitro. Thromb Haemost 1981; 46: 561-565.
17. Copin JC, da Silva RF, Fraga-Silva RA, Capettini L, Quintao S, Lenglet S et al. Treatment with Evasin-3 reduces atherosclerotic vulnerability for ischemic stroke, but not brain injury in mice. J Cereb Blood Flow Metab 2013; 33: 490-498.
18. Badaut J, Copin JC, Fukuda AM, Gasche Y, Schaller K, da Silva RF. Increase of arginase activity in old apolipoprotein-E deficient mice under Western diet associated with changes in neurovascular unit. J Neuroinflammation 2012; 9: 132.
19. Zhang XH, Polavarapu R, She H, Mao ZX, Yepes M. Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappa B pathway activation. Am J Pathol 2007; 171: 1281-1290.
20. Nicole O, Docagne F, Ali C, Margaill I, Carmeliet P, MacKenzie ET et al. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 2001; 7: 59-64.
21. Pineda D, Ampurdanes C, Medina MG, Serratosa J, Tusell JM, Saura J et al. Tissue plasminogen activator induces microglial inflammation via a noncatalytic molecular mechanism involving activation of mitogen-activated protein kinases and Akt signaling pathways and AnnexinA2 and Galectin-1 receptors. Glia 2012; 60: 526-540.
22. An J, Zhang C, Polavarapu R, Zhang X, Yepes M. Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein induce Akt phosphorylation in the ischemic brain. Blood 2008; 112: 2787-2794.
23. Nagai N, De Mol M, Lijnen HR, Carmeliet P, Collen D. Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation 1999; 99: 2440-2444.
24. Patel AR, Ritzel R, McCullough LD, Liu F. Microglia and ischemic stroke: a doubleedged sword. Int J Physiol Pathophysiol Pharmacol 2013; 5: 73-90.
25. Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG. Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 2006; 37: 1087-1093.
26. Fan X, Lo EH, Wang X. Effects of minocycline plus tissue plasminogen activator combination therapy after focal embolic stroke in type 1 diabetic rats. Stroke 2013; 44: 745-752.
27. Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S et al. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012; 43: 3063-3070.
28. Gelderblom M, Leypoldt F, Steinbach K, Behrens D, Choe CU, Siler DA et al. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009; 40: 1849-1857.
29. Maurer M, von Stebut E. Macrophage inflammatory protein-1. Int J Biochem Cell Biol 2004; 36: 1882-1886.
30. Skuljec J, Sun H, Pul R, Benardais K, Ragancokova D, Moharregh-Khiabani D et al. CCL5 induces a pro-inflammatory profile in microglia in vitro. Cell Immunol 2011; 270: 164-171.
31. Wang HK, Park UJ, Kim SY, Lee JH, Kim SU, Gwag BJ et al. Free radical production in CA1 neurons induces MIP-1alpha expression, microglia recruitment, and delayed neuronal death after transient forebrain ischemia. J Neurosci 2008; 28: 1721-1727.
32. Nishi T, Maier CM, Hayashi T, Saito A, Chan PH. Superoxide dismutase 1 overexpression reduces MCP-1 and MIP-1 alpha expression after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2005; 25: 1312-1324.
33. Gourmala NG, Limonta S, Bochelen D, Sauter A, Boddeke HW. Localization of macrophage inflammatory protein: macrophage inflammatory protein-1 expression in rat brain after peripheral administration of lipopolysaccharide and focal cerebral ischemia. Neuroscience 1999; 88: 1255-1266.
34. Zaremba J, Ilkowski J, Losy J. Serial measurements of levels of the chemokines CCL2, CCL3 and CCL5 in serum of patients with acute ischaemic stroke. Folia Neuropathol 2006; 44: 282-289.
35. Lu W, Bhasin M, Tsirka SE. Involvement of tissue plasminogen activator in onset and effector phases of experimental allergic encephalomyelitis. J Neurosci 2002; 22: 10781-10789.
36. Lee SR, Guo SZ, Scannevin RH, Magliaro BC, Rhodes KJ, Wang X et al. Induction of matrix metalloproteinase, cytokines and chemokines in rat cortical astrocytes exposed to plasminogen activators. Neurosci Lett 2007; 417: 1-5.
37. Cartier L, Hartley O, Dubois-Dauphin M, Krause KH. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 2005; 48: 16-42.
38. Gamo K, Kiryu-Seo S, Konishi H, Aoki S, Matsushima K, Wada K et al. G-proteincoupled receptor screen reveals a role for chemokine receptor CCR5 in suppressing microglial neurotoxicity. J Neurosci 2008; 28: 11980-11988.
39. Lambertsen KL, Biber K, Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab 2012; 32: 1677-1698.
40. Schroeter M, Kury P, Jander S. Inflammatory gene expression in focal cortical brain ischemia: differences between rats and mice. Brain Res Mol Brain Res 2003; 117: 1-7.
41. Yoshida T, Waeber C, Huang Z, Moskowitz MA. Induction of nitric oxide synthase activity in rodent brain following middle cerebral artery occlusion. Neurosci Lett 1995; 194: 214-218.
42. Copin JC, Merlani P, Sugawara T, Chan PH, Gasche Y. Delayed matrix metalloproteinase inhibition reduces intracerebral hemorrhage after embolic stroke in rats. Exp Neurol 2008; 213: 196-201.
43. Kahles T, Foerch C, Sitzer M, Schroeter M, Steinmetz H, Rami A et al. Tissue plasminogen activator mediated blood-brain barrier damage in transient focal cerebral ischemia in rats: relevance of interactions between thrombotic material and thrombolytic agent. Vascul Pharmacol 2005; 43: 254-259.