Increased brain plasmin levels following experimental ischemic stroke in male mice.
experimental stroke model
fibrinolytic system
mouse
tPA
thrombolysis
Journal
Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
12
02
2020
revised:
29
10
2020
accepted:
15
11
2020
pubmed:
10
12
2020
medline:
24
11
2021
entrez:
9
12
2020
Statut:
ppublish
Résumé
Many coagulation factor proteases are increased in the brain during ischemic stroke. One of these proteases is plasmin. In this study we established a novel method for direct quantitative measurement of plasmin activity in male mouse brain slices using a sensitive fluorescent substrate in the presence of specific protease inhibitors. In both the ischemic and contralateral hemispheres, plasmin activity increased 3, 6, and 24 hr following stroke in comparison to healthy mice (F(3, 72) = 39.5, p < 0.0001, repeated measures ANOVA) after the induction of permanent middle cerebral artery occlusion (PMCAo). Plasmin activity was higher in the ischemic hemisphere (F(1,36) = 9.1, p = 0.005) and there was a significant interaction between time and ischemic hemisphere (F(3,36) = 4.4, p = 0.009). Plasmin activity was correlated with infarct volume (R
Substances chimiques
Tissue Plasminogen Activator
EC 3.4.21.68
Fibrinolysin
EC 3.4.21.7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
966-976Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Bardehle, S., Rafalski, V. A., & Akassoglou, K. (2015). Breaking boundaries-coagulation and fibrinolysis at the neurovascular interface. Frontiers in Cellular Neuroscience, 9(September), 354. https://doi.org/10.3389/fncel.2015.00354
Basham, M. E., & Seeds, N. W. (2001). Plasminogen expression in the neonatal and adult mouse brain. Journal of Neurochemistry, 77(1), 318-325. https://doi.org/10.1046/j.1471-4159.2001.00239.x
Bushi, D., Ben Shimon, M., Shavit Stein, E., Chapman, J., Maggio, N., & Tanne, D. (2015). Increased thrombin activity following reperfusion after ischemic stroke alters synaptic transmission in the hippocampus. Journal of Neurochemistry, 135(6), 1140-1148. https://doi.org/10.1111/jnc.13372
Bushi, D., Chapman, J., Katzav, A., Shavit-Stein, E., Molshatzki, N., Maggio, N., & Tanne, D. (2013). Quantitative detection of thrombin activity in an ischemic stroke model. Journal of Molecular Neuroscience, 51(3), 844-850. https://doi.org/10.1007/s12031-013-0072-y
Bushi, D., Chapman, J., Wohl, A., Stein, E. S., Feingold, E., & Tanne, D. (2018). Apixaban decreases brain thrombin activity in a male mouse model of acute ischemic stroke. Journal of Neuroscience Research, 96(8), 1406-1411. https://doi.org/10.1002/jnr.24253
Bushi, D., Stein, E. S., Golderman, V., Feingold, E., Gera, O., Chapman, J., & Tanne, D. (2017). A linear temporal increase in thrombin activity and loss of its receptor in mouse brain following ischemic stroke. Frontiers in Neurology, 8(April), 138. https://doi.org/10.3389/fneur.2017.00138
Capone, C., Anrather, J., Milner, T. A., & Iadecola, C. (2009). Estrous cycle-dependent neurovascular dysfunction induced by angiotensin II in the mouse neocortex. Hypertension, 54(2), 302-307. https://doi.org/10.1161/HYPERTENSIONAHA.109.133249
Chen, Y., Zhu, W., Zhang, W., Libal, N., Murphy, S. J., Offner, H., & Alkayed, N. J. (2015). A novel mouse model of thromboembolic stroke. Journal of Neuroscience Methods, 256, 203-211. Elsevier B.V. https://doi.org/10.1016/j.jneumeth.2015.09.013
Chen, Z. L., & Strickland, S. (1997). Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell, 91(7), 917-925. https://doi.org/10.1016/S0092-8674(00)80483-3
Cinelli, P., Madani, R., Tsuzuki, N., Vallet, P., Arras, M., Zhao, C. N., Osterwalder, T., Ru, T., & Sonderegger, P. (2001). Neuroserpin, a neuroprotective factor in focal ischemic. Stroke, 457, 443-457. https://doi.org/10.1006/mcne.2001.1028
Draxler, D. F., Lee, F., Ho, H., Keragala, C. B., Medcalf, R. L., & Niego, B. (2019). T-PA suppresses the immune response and aggravates neurological deficit in a murine model of ischemic stroke. Frontiers in Immunology, 10(March), 591. https://doi.org/10.3389/fimmu.2019.00591
Draxler, D. F., & Medcalf, R. L. (2015). The fibrinolytic system-more than fibrinolysis? Transfusion Medicine Reviews, 29(2), 102-109. W.B. Saunders. https://doi.org/10.1016/j.tmrv.2014.09.006
Feigin, V. L., Roth, G. A., Naghavi, M., Parmar, P., Krishnamurthi, R., Chugh, S., Mensah, G. A., Norrving, B., Shiue, I., Ng, M., Estep, K., Cercy, K., Murray, C. J. L., & Forouzanfar, M. H. (2016). Global burden of stroke and risk factors in 188 countries, during 1990-2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet Neurology, 15(9), 913-924. https://doi.org/10.1016/S1474-4422(16)30073-4
Gerzanich, V., Kwon, M. S., Woo, S. K., Ivanov, A., & Marc Simard, J. (2018). SUR1-TRPM4 channel activation and phasic secretion of MMP-9 induced by tPA in brain endothelial cells. PLoS One, 13(4), e0195526. https://doi.org/10.1371/journal.pone.0195526
Gur-Wahnon, D., Mizrachi, T., Wald-Altman, S., Al-Roof Higazi, A., & Brenner, T. (2014). Tissue plasminogen activator involvement in experimental autoimmune myasthenia gravis: Aggravation and therapeutic potential. Journal of Autoimmunity, 52, 36-43. https://doi.org/10.1016/j.jaut.2013.12.017
Hajjar, K. A., & Ruan, J. (2015). Chapter 135: Fibrinolysis and thrombolysis. In Kenneth Kaushansky, Marshall A. Lichtman, Josef T. Prchal, Marcel Levi, Oliver W. Press, Linda J. Burns, & Michael A. Caligiuri (eds.), Williams hematology (Vol. 12, 9th ed.). McGraw-Hill Education.
Iwanaga, S., Wallén, P., Gröndahl, N. J., Henschen, A., & Blombäck, B. (1969). On the primary structure of human fibrinogen: Isolation and characterization of N-terminal fragments from plasmic digests. European Journal of Biochemistry, 8(2), 189-199. https://doi.org/10.1111/j.1432-1033.1969.tb00514.x
Johnson, C. O., Nguyen, M., Roth, G. A., Nichols, E., Alam, T., Abate, D., Abd-Allah, F., Abdelalim, A., Abraha, H. N., Abu-Rmeileh, N. M. E., Adebayo, O. M., Adeoye, A. M., Agarwal, G., Agrawal, S., Aichour, A. N., Aichour, I., Aichour, M. T. E., Alahdab, F., Ali, R., … Murray, C. J. L. (2019). Global, regional, and national burden of stroke, 1990-2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurology, 18(5), 439-458. https://doi.org/10.1016/S1474-4422(19)30034-1
Kato, H., Adachi, N., Ohno, Y., Iwanaga, S., Takada, K., & Sakakibara, S. (1980). New fluorogenic peptide substrates for plasmin. Journal of Biochemistry, 88(1), 183-190. https://doi.org/10.1093/oxfordjournals.jbchem.a132947
Kolev, K., Komorowicz, E., Owen, W. G., & Machovich, R. (1996). Quantitative comparison of fibrin degradation with plasmin, miniplasmin, neurophil leukocyte elastase and cathepsin G. Thrombosis and Haemostasis, 75(1), 140-146. https://doi.org/10.1055/s-0038-1650234
Longa, E. Z., Weinstein, P. R., Carlson, S., & Cummins, R. (1989). Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke, 20(1), 84-91. https://doi.org/10.1161/01.str.20.1.84
Mandl-Weber, S., Haslinger, B., & Sitter, T. (1999). Thrombin upregulates production of plasminogen activator inhibitor type 1 in human peritoneal mesothelial cells. Peritoneal Dialysis International: Journal of the International Society for Peritoneal Dialysis, 19(4), 319-324. http://www.ncbi.nlm.nih.gov/pubmed/10507812
Medcalf, R. L. (2017). Fibrinolysis: From blood to the brain. Journal of Thrombosis and Haemostasis, 15(11), 2089-2098. https://doi.org/10.1111/jth.13849
Mizrachi, T., Gur-Wahnon, D., Al-Roof Higazi, A., & Brenner, T. (2020). Role of tissue plasminogen activator in clinical aggravation of experimental autoimmune encephalomyelitis and its therapeutic potential. Cellular Immunology, 348, 104040. https://doi.org/10.1016/j.cellimm.2020.104040
Moldthan, H. L., Hirko, A. C., Thinschmidt, J. S., Grant, M., Li, Z., Peris, J., Lu, Y., Elshikha, A., King, M. A., Hughes, J. A., & Song, S. (2014). Alpha 1-antitrypsin therapy mitigated ischemic stroke damage in rats. Journal of Stroke and Cerebrovascular Diseases, 23(5), 355-363. https://doi.org/10.1016/j.jstrokecerebrovasdis.2013.12.029.Alpha
Nebendahl, K. (2000). Routes of administration. Laboratory Rat, 16(7-8), 463-483. https://doi.org/10.1016/B978-012426400-7.50063-7
Niego, B., Freeman, R., Puschmann, T. B., Turnley, A. M., & Medcalf, R. L. (2012). t-PA-specific modulation of a human blood-brain barrier model involves plasmin-mediated activation of the Rho kinase pathway in astrocytes. Blood, 119(20), 4752-4761. https://doi.org/10.1182/blood-2011-07-369512
Niego, B., & Medcalf, R. L. (2014). Plasmin-dependent modulation of the blood-brain barrier: A major consideration during tPA-induced thrombolysis? Journal of Cerebral Blood Flow and Metabolism, 34(8), 1283-1296. https://doi.org/10.1038/jcbfm.2014.99
Paul, C. L., Ryan, A., Rose, S., Attia, J. R., Kerr, E., Koller, C., & Levi, C. R. (2016). How can we improve stroke thrombolysis rates? A review of health system factors and approaches associated with thrombolysis administration rates in acute stroke care. Implementation Science, 11, 51. https://doi.org/10.1186/s13012-016-0414-6
Sheehan, J. J., Zhou, C., Gravanis, I., Rogove, A. D., Wu, Y.-P., Bogenhagen, D. F., & Tsirka, S. E. (2007). Proteolytic activation of monocyte chemoattractant protein-1 by plasmin underlies excitotoxic neurodegeneration in mice. Journal of Neuroscience, 27(7), 1738-1745. https://doi.org/10.1523/JNEUROSCI.4987-06.2007
Siao, C.-J., & Tsirka, S. E. (2002). Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. Journal of Neuroscience, 22(9), 3352-3358. https://doi.org/10.1523/JNEUROSCI.22-09-03352.2002
Stein, E. S., Itsekson-Hayosh, Z., Aronovich, A., Reisner, Y., Bushi, D., Pick, C. G., Tanne, D., Chapman, J., Vlachos, A., & Maggio, N. (2015). Thrombin induces ischemic LTP (iLTP): Implications for synaptic plasticity in the acute phase of ischemic stroke. Scientific Reports, 5, 7912. https://doi.org/10.1038/srep07912
Wallen, P., Iwanaga, S., Wallén, P., & Iwanaga, S. (1968). Differences between plasmic and tryptic digests of human S-sulfo-fibrinogen. Biochimica et Biophysica Acta, 154(2), 414-417. https://doi.org/10.1016/0005-2795(68)90114-1
Wang, Y., Luo, W., & Reiser, G. (2008). Trypsin and trypsin-like proteases in the brain: Proteolysis and cellular functions. Cellular and Molecular Life Sciences, 65(2), 237-252. https://doi.org/10.1007/s00018-007-7288-3
Wang, Y. F., Tsirka, S. E., Strickland, S., Stieg, P. E., Soriano, S. G., & Lipton, S. A. (1998). Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nature Medicine, 4(2), 228-231. https://doi.org/10.1038/nm0298-228
Wu, L., Xu, L., Xu, X., Fan, X., Xie, Y., Yang, L., Lan, W., Zhu, J., Xu, G., Dai, J., Jiang, Y., & Liu, X. (2014). Keep warm and get success: The role of postischemic temperature in the mouse middle cerebral artery occlusion model. Brain Research Bulletin, 101, 12-17. https://doi.org/10.1016/j.brainresbull.2013.12.003
Zhang, F., & Chen, J. (2012). Infarct measurement in focal cerebral ischemia: TTC staining. Animal Models of Acute Neurological Injuries II, 9(December), 93-98. https://doi.org/10.1007/978-1-61779-782-8_9
Zhao, X. J., Larkin, T. M., Lauver, M. A., Ahmad, S., & Ducruet, A. F. (2017). Tissue plasminogen activator mediates deleterious complement cascade activation in stroke. PLoS One, 12(7), e0180822. https://doi.org/10.1371/journal.pone.0180822