HMGB-1 promotes fibrinolysis and reduces neurotoxicity mediated by tissue plasminogen activator

Journal of Cell Science

Volumn 124, Issue 12, 2011, Pages 2070-2076

  Roussel, Benoit D ^a,d   Mysiorek, Caroline ^b   Rouhiainen, Ari ^c   Jullienne, Amandine ^a   Parcq, Jerome ^a   Hommet, Yannick ^a   Culot, Maxime ^b   Berezowski, Vincent ^b   Cecchelli, Romeo ^b   Rauvala, Heikki ^c   Vivien, Denis ^a   Ali, Carine ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ D'ARTOIS   (France)

^c UNIVERSITY OF HELSINKI   (Finland)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Excitotoxicity; High mobility group box 1 protein; Stroke; Tissue plasminogen activator

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BLOOD CLOT LYSIS; CALCIUM TRANSPORT; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; DRUG RECEPTOR BINDING; FETUS; FIBRINOLYSIS; HUMAN; ISCHEMIA; MOUSE; NEUROTOXICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 79958150851     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.084392     Document Type: Article

References (43)

1. Abraham, E., Arcaroli, J., Carmody, A., Wang, H. and Tracey, K. J. (2000). HMG-1 as a mediator of acute lung inflammation. J. Immunol. 165, 2950-2954.
2. Agnello, D., Wang, H., Yang, H., Tracey, K. J. and Ghezzi, P. (2002). HMGB-1, a DNAbinding protein with cytokine activity, induces brain TNF and IL-6 production, and mediates anorexia and taste aversion. Cytokine 18, 231-236.
3. Benchenane, K., Berezowski, V., Ali, C., Fernandez-Monreal, M., Lopez-Atalaya, J. P., Brillault, J., Chuquet, J., Nouvelot, A., MacKenzie, E. T., Bu, G. et al. (2005a). Tissuetype plasminogen activator crosses the intact blood-brain barrier by low-density lipoprotein receptor-related protein-mediated transcytosis. Circulation 111, 2241-2249.
4. Benchenane, K., Berezowski, V., Fernandez-Monreal, M., Brillault, J., Valable, S., Dehouck, M. P., Cecchelli, R., Vivien, D., Touzani, O. and Ali, C. (2005b). Oxygen glucose deprivation switches the transport of tPA across the blood-brain barrier from an LRP-dependent to an increased LRP-independent process. Stroke 36, 1065-1070.
5. Benchenane, K., Castel, H., Boulouard, M., Bluthe, R., Fernandez-Monreal, M., Roussel, B. D., Lopez-Atalaya, J. P., Butt-Gueulle, S., Agin, V., Maubert, E. et al. (2007). Anti-GluN1 N-terminal-domain vaccination unmasks the crucial action of tPA on NMDAreceptor-mediated toxicity and spatial memory. J. Cell Sci. 120, 578-585.
6. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A. and Bianchi, M. E. (2003). Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551-5560.
7. Brillault, J., Berezowski, V., Cecchelli, R. and Dehouck, M. P. (2002). Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J. Neurochem. 83, 807-817.
8. Bustin, M. (1999). Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246.
9. Culot, M., Mysiorek, C., Renftel, M., Roussel, B. D., Hommet, Y., Vivien, D., Cecchelli, R., Fenart, L., Berezowski, V., Dehouck, M. P. et al. (2009). Cerebrovascular protection as a possible mechanism for the protective effects of NXY-059 in preclinical models: an in vitro study. Brain Res. 1294, 144-152.
10. Dehouck, M. P., Meresse, S., Delorme, P., Fruchart, J. C. and Cecchelli, R. (1990). An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. J. Neurochem. 54, 1798-1801.
11. Dehouck, M. P., Jolliet-Riant, P., Bree, F., Fruchart, J. C., Cecchelli, R. and Tillement, J. P. (1992). Drug transfer across the blood-brain barrier: correlation between in vitro and in vivo models. J. Neurochem. 58, 1790-1797.
12. Dirnagl, U., Iadecola, C. and Moskowitz, M. A. (1999). Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397.
13. Faraco, G., Fossati, S., Bianchi, M. E., Patrone, M., Pedrazzi, M., Sparatore, B., Moroni, F. and Chiarugi, A. (2007). High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo. J. Neurochem. 103, 590-603.
14. Fernandez-Monreal, M., Lopez-Atalaya, J. P., Benchenane, K., Cacquevel, M., Dulin, F., Le Caer, J. P., Rossier, J., Jarrige, A. C., Mackenzie, E. T., Colloc'h, N. et al. (2004). Arginine 260 of the amino-terminal domain of GluN1 subunit is critical for tissue-type plasminogen activator-mediated enhancement of N-methyl-D-aspartate receptor signaling. J. Biol. Chem. 279, 50850-50856.
15. Hacke, W., Kaste, M., Bluhmki, E., Brozman, M., Davalos, A., Guidetti, D., Larrue, V., Lees, K. R., Medeghri, Z., Machnig, T. et al. (2008). Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med. 359, 1317-1329.
16. Hayakawa, K., Mishima, K., Nozako, M., Hazekawa, M., Mishima, S., Fujioka, M., Orito, K., Egashira, N., Iwasaki, K. and Fujiwara, M. (2008). Delayed treatment with minocycline ameliorates neurologic impairment through activated microglia expressing a high-mobility group box1-inhibiting mechanism. Stroke 39, 951-958.
17. Hayakawa, K., Arai, K. and Lo, E. H. (2010a). Role of ERK map kinase and CRM1 in IL-1beta-stimulated release of HMGB1 from cortical astrocytes. Glia 58, 1007-1015.
18. Hayakawa, K., Qiu, J. and Lo, E. H. (2010b). Biphasic actions of HMGB1 signaling in inflammation and recovery after stroke. Ann. N. Y. Acad. Sci. 1207, 50-57.
19. Kim, J. B., Sig Choi, J., Yu, Y. M., Nam, K., Piao, C. S., Kim, S. W., Lee, M. H., Han, P. L., Park, J. S. and Lee, J. K. (2006). HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J. Neurosci. 26, 6413-6421.
20. Kvajo, M., Albrecht, H., Meins, M., Hengst, U., Troncoso, E., Lefort, S., Kiss, J. Z., Petersen, C. C. and Monard, D. (2004). Regulation of brain proteolytic activity is necessary for the in vivo function of NMDA receptors. J. Neurosci. 24, 9734-9743.
21. Landsman, D. and Bustin, M. (1993). A signature for the HMG-1 box DNA-binding proteins. BioEssays 15, 539-546.
22. Liu, K., Mori, S., Takahashi, H. K., Tomono, Y., Wake, H., Kanke, T., Sato, Y., Hiraga, N., Adachi, N., Yoshino, T. et al. (2007). Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J. 21, 3904-3916.
23. Lopez-Atalaya, J. P., Roussel, B. D., Ali, C., Maubert, E., Petersen, K. U., Berezowski, V., Cecchelli, R., Orset, C. and Vivien, D. (2007). Recombinant Desmodus rotundus salivary plasminogen activator crosses the blood-brain barrier through a low-density lipoprotein receptor-related protein-dependent mechanism without exerting neurotoxic effects. Stroke 38, 1036-1043.
24. Lopez-Atalaya, J. P., Roussel, B. D., Levrat, D., Parcq, J., Nicole, O., Hommet, Y., Benchenane, K., Castel, H., Leprince, J., To Van, D. et al. (2008). Toward safer thrombolytic agents in stroke: molecular requirements for NMDA receptor-mediated neurotoxicity. J. Cereb. Blood Flow Metab. 28, 1212-1221.
25. Muhammad, S., Barakat, W., Stoyanov, S., Murikinati, S., Yang, H., Tracey, K. J., Bendszus, M., Rossetti, G., Nawroth, P. P., Bierhaus, A. et al. (2008). The HMGB1 receptor RAGE mediates ischemic brain damage. J. Neurosci. 28, 12023-12031.
26. Mysiorek, C., Culot, M., Dehouck, L., Derudas, B., Staels, B., Bordet, R., Cecchelli, R., Fenart, L. and Berezowski, V. (2009). Peroxisome-proliferator-activated receptor-alpha activation protects brain capillary endothelial cells from oxygen-glucose deprivationinduced hyperpermeability in the blood-brain barrier. Curr. Neurovasc. Res. 6, 181-193.
27. Nicole, O., Docagne, F., Ali, C., Margaill, I., Carmeliet, P., MacKenzie, E. T., Vivien, D. and Buisson, A. (2001). The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 7, 59-64.
28. Parkkinen, J. and Rauvala, H. (1991). Interactions of plasminogen and tissue plasminogen activator (t-PA) with amphoterin. Enhancement of t-PA-catalyzed plasminogen activation by amphoterin. J. Biol. Chem. 266, 16730-16735.
29. Qiu, J., Nishimura, M., Wang, Y., Sims, J. R., Qiu, S., Savitz, S. I., Salomone, S. and Moskowitz, M. A. (2008). Early release of HMGB-1 from neurons after the onset of brain ischemia. J. Cereb. Blood Flow Metab. 28, 927-938.
30. Qiu, J., Xu, J., Zheng, Y., Wei, Y., Zhu, X., Lo, E. H., Moskowitz, M. A. and Sims, J. R. (2010). High-mobility group box 1 promotes metalloproteinase-9 upregulation through toll-like receptor 4 after cerebral ischemia. Stroke 41, 2077-2082.
31. Rouhiainen, A., Tumova, S., Valmu, L., Kalkkinen, N. and Rauvala, H. (2007). Pivotal advance: analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin). J. Leukoc. Biol. 81, 49-58.
32. Samson, A. L. and Medcalf, R. L. (2006). Tissue-type plasminogen activator: a multifaceted modulator of neurotransmission and synaptic plasticity. Neuron 50, 673-678.
33. Samson, A. L., Nevin, S. T., Croucher, D., Niego, B., Daniel, P. B., Weiss, T. W., Moreno, E., Monard, D., Lawrence, D. A. and Medcalf, R. L. (2008). Tissue-type plasminogen activator requires a co-receptor to enhance NMDA receptor function. J. Neurochem. 107, 1091-1101.
34. Saqqur, M., Tsivgoulis, G., Molina, C. A., Demchuk, A. M., Siddiqui, M., Alvarez-Sabin, J., Uchino, K., Calleja, S. and Alexandrov, A. V. (2008). Symptomatic intracerebral hemorrhage and recanalization after IV rt-PA: a multicenter study. Neurology 71, 1304-1312.
35. Sha, Y., Zmijewski, J., Xu, Z. and Abraham, E. (2008). HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J. Immunol. 180, 2531-2537.
36. Tanswell, P., Seifried, E., Su, P. C., Feuerer, W. and Rijken, D. C. (1989). Pharmacokinetics and systemic effects of tissue-type plasminogen activator in normal subjects. Clin. Pharmacol. Ther. 46, 155-162.
37. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group (1995). Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. 333, 1581-1587.
38. Tian, J., Avalos, A. M., Mao, S. Y., Chen, B., Senthil, K., Wu, H., Parroche, P., Drabic, S., Golenbock, D., Sirois, C. et al. (2007). Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 8, 487-496.
39. Tsirka, S. E., Gualandris, A., Amaral, D. G. and Strickland, S. (1995). Excitotoxininduced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377, 340-344.
40. Vassalli, J. D., Sappino, A. P. and Belin, D. (1991). The plasminogen activator/plasmin system. J. Clin. Invest. 88, 1067-1072.
41. Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., Frazier, A., Yang, H., Ivanova, S., Borovikova, L. et al. (1999). HMG-1 as a late mediator of endotoxin lethality in mice. Science 285, 248-251.
42. Wang, X., Rosell, A. and Lo, E. H. (2008). Targeting extracellular matrix proteolysis for hemorrhagic complications of tPA stroke therapy. CNS Neurol. Disord. Drug Targets 7, 235-242.
43. Yepes, M., Roussel, B. D., Ali, C. and Vivien, D. (2009). Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci. 32, 48-55.