|Generate QR code
Open Access
Subscription Access
The role of matrix metalloproteinases in the pathogenetic mechanisms of ischemic stroke
https://doi.org/10.30629/2658-7947-2024-29-3-5-15
Abstract
Modern understanding of the mechanisms of the pathogenesis of ischemic stroke has expanded due to the study of neuroinfl ammation processes, in which matrix metalloproteinases (MMPs) play an important role. This literature review describes the main types of MMPs and provides current data on the pathophysiological role of this group of proteases in acute cerebral ischemia, which have multidirectional eff ects depending on the stage of the disease. Clinical studies assessing the role of MMPs in ischemic stroke are in most cases based on experimental models, and their results are ambiguous, which is determined by the versatility of their actions. MMPs are an important regulator of infl ammatory processes, the permeability of the blood-brain barrier and, as a consequence, cerebral edema. However, the positive eff ect of MMPs in the processes of angiogenesis, neurogenesis and neuroplasticity has been proven. Thus, further study of MMPs is relevant from the point of view of their role in functional recovery after ischemic stroke.
Keywords
ischemic stroke,
matrix metalloproteinases,
neuroinfl ammation,
hemorrhagic transformation,
angiogenesis,
neuroregeneration
Supporting agencies: The study had no sponsorship
About the Authors
K. S. Kucherova
Siberian State Medical University
Russian Federation
Russian Federation
Tomsk
E. S. Koroleva
Siberian State Medical University
Russian Federation
Russian Federation
Tomsk
V. M. Alifirova
Siberian State Medical University
Russian Federation
Russian Federation
Tomsk
References
1. Feigin V.L, Brainin M, Norrving B, Martins S, Sacco R.L, Hacke W, et al. World Stroke Organization (WSO): Global Stroke Fact Sheet 2022. International journal of stroke. 2022;17(1):18–29. doi: 10.1177/17474930211065917
2. GBD 2019 Stroke Collaborators. Global, regional, and national burden of stroke and its risk factors, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Neurol. 2021;20(10):795–820. doi: 10.1016/S1474-4422(21)00252-0
3. Suslina Z.A., Varakin Y.Y. Epidemiological aspects of the study of stroke. Time to take stock. Annals of Clinical and Experimental Neurology. 2007;1(2):22–28. (In Russ.). URL: https://cyberleninka.ru/article/n/epidemiologicheskie-aspekty-izucheniya-insulta-vremya-podvodit-itogi?ysclid=lyy6xdxhjt361794254
4. Skvortsova V.I., Stakhovskaya L.V., Ayriyan N.Y. Epidemiology of stroke in the Russian Federation. Systemic Hypertension. 2005;2(1):10–12. (In Russ.). doi: 10.26442/SG28725
5. Jayaraj R.L., Azimullah S., Beiram R., Jalal F.Y., Rosenberg G.A. Neuroinfl ammation: friend and foe for ischemic stroke. J Neuro-inflammation. 2019;16(1):142. doi: 10.1186/s12974-019-1516-2
6. Candelario-Jalil E., Dijkhuizen R.M., Magnus T. Neuroinfl ammation, Stroke, Blood-Brain Barrier Dysfunction, and Imaging Modalities. Stroke. 2022;53(5):1473–1486. doi: 10.1161/STROKEAHA.122.036946
7. Qin C., Yang S., Chu Y.H., Zhang H., Pang X.W., Chen L. et al. Signaling pathways involved in ischemic stroke: molecular mechanisms and therapeutic interventions. Signal Transduct Target Ther. 2022;7(1):215. doi: 10.1038/s41392-022-01064-1
8. Ji Y., Gao Q., Ma Y., Wang F., Tan X., Song D. et al. An MMP-9 exclusive neutralizing antibody attenuates blood-brain barrier breakdown in mice with stroke and reduces stroke patient-derived MMP-9 activity. Pharmacol. Res. 2023;190:106720. doi: 10.1016/j.phrs.2023.106720
9. Tirandi A., Sgura C., Carbone F., Montecucco F., Liberale L. Inflammatory biomarkers of ischemic stroke. Intern Emerg Med. 2023;18(3):723–732. doi: 10.1007/s11739-023-03201-2
10. Montellano F.A., Ungethüm K., Ramiro L., Nacu A., Hellwig S., Fluri F. et al. Role of Blood-Based Biomarkers in Ischemic Stroke Prognosis: A Systematic Review. Stroke. 2021;52(2):543–551. doi: 10.1161/STROKEAHA.120.029232
11. Bai M., Sun R., Cao B., Feng J., Wang J. Monocyte-related cytokines/chemokines in cerebral ischemic stroke. CNS Neurosci Ther. 2023;29(12):3693–3712. doi: 10.1111/cns.14368
12. Yang Y., Rosenberg G.A. Matrix metalloproteinases as therapeutic targets for stroke. Brain Res. 2015;1623:30–8. doi: 10.1016/j.brainres.2015.04.024
13. Kimura-Ohba S., Yang Y. Oxidative DNA Damage Mediated by Intranuclear MMP Activity Is Associated with Neuronal Apoptosis in Ischemic Stroke. Oxid Med Cell Longev. 2016;2016:6927328. doi: 10.1155/2016/6927328
14. Schönbeck U., Mach F., Libby P. Generation of biologically active IL-1β by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1β processing. Journal of Immunology. 1998;161(7):3340–3346. doi: 10.4049/jimmunol.161.7.3340
15. Berta T., Liu T., Liu Y.C., Xu Z.Z., Ji R.R. Acute morphine activates satellite glial cells and up-regulates IL-1β in dorsal root ganglia in mice via matrix metalloprotease-9. Molecular Pain. 2012;8, article 18. doi: 10.1186/1744-8069-8-18
16. Costru-Tasnic E., Gavriliuc M., Manole E. The importance of matrix metalloproteinases in the prognosis of acute ischemic stroke patients. Mold Med J. 2021;62(3):44–49. doi: 10.52418/moldovan-med-j.64-3.21.09
17. Chang J.J., Stanfi ll A., Pourmotabbed T. The Role of Matrix Metalloproteinase Polymorphisms in Ischemic Stroke. Int J Mol Sci. 2016;17(8):1323. doi: 10.3390/ijms17081323
18. Adibhatla R.M., Hatcher J.F. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol Disord Drug Targets. 2008;7(3):243–53. doi: 10.2174/187152708784936608
19. Cui N., Hu M., Khalil R.A. Biochemical and biological attributes of matrix metalloproteinases. Prog Mol Biol Transl Sci. 2017;147(617):1–73. doi: 10.1016/bs.pmbts.2017.02.005
20. Ågren M.S., Auf dem Keller U. Matrix Metalloproteinases: How Much Can They Do? Int J Mol Sci. 2020;21(8):2678. doi: 10.3390/ijms21082678
21. Romi F., Helgeland G., Gilhus N.E. Serum levels of matrix metalloproteinases: implications in clinical neurology. Eur Neurol. 2012;67(2):121–8. doi: 10.1159/000334862
22. Almutairi S., Kalloush H.M., Manoon N.A., Bardaweel S.K. Matrix Metalloproteinases Inhibitors in Cancer Treatment: An Updated Review (2013–2023). Molecules. 2023;28(14):5567. doi: 10.3390/molecules28145567
23. Boziki M., Grigoriadis N. An Update on the Role of Matrix Metalloproteinases in the Pathogenesis of Multiple Sclerosis. Med Chem. 2018;14(2):155–169. doi: 10.2174/1573406413666170906122803
24. Sánchez-Torres J.L., Yescas-Gómez P., Torres-Romero J., Espinosa O.R., Canovas L.L., Tecalco-Cruz Á.C., et al. Matrix metalloproteinases deregulation in amyotrophic lateral sclerosis. J Neurol Sci. 2020;419:117175. doi: 10.1016/j.jns.2020.117175
25. Zipfel P., Rochais C., Baranger K., Rivera S., Dallemagne P. Matrix Metalloproteinases as New Targets in Alzheimer’s Disease: Opportunities and Challenges. J Med Chem. 2020;63(19):10705–10725. doi: 10.1021/acs.jmedchem.0c00352
26. Montaner J., Ramiro L., Simats A., Hernández-Guillamon M., Delgado P., Bustamante A., Rosell A. Matrix metalloproteinases and ADAMs in stroke. Cellular and Molecular Life Sciences. 2019;76(16):3117–3140. doi: 10.1007/s00018-019-03175-5
27. Planas A.M., Solé S., Justicia C. Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol Dis. 2001;8(5):834–46. doi: 10.1006/nbdi.2001.0435
28. Cuadrado E., Rosell A., Borrell-Pagès M., García-Bonilla L., Hernández-Guillamon M., Ortega-Aznar A., Montaner J. Matrix metalloproteinase-13 is activated and is found in the nucleus of neural cells after cerebral ischemia. J Cereb Blood Flow Metab. 2009;29(2):398–410. doi: 10.1038/jcbfm.2008.130
29. Chelluboina B., Klopfenstein J.D., Pinson D.M., Wang D.Z., Vemuganti R., Veeravalli K.K. Matrix Metalloproteinase-12 Induces Blood-Brain Barrier Damage After Focal Cerebral Ischemia. Stroke. 2015;46(12):3523–31. doi: 10.1161/STROKEAHA.115.011031
30. Cuadrado E., Ortega L., Hernández-Guillamon M., Penalba A., Fernández-Cadenas I., Rosell A., Montaner J. Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release. J Leukoc Biol. 2008;84(1):207–14. doi: 10.1189/jlb.0907606
31. Turner R.J., Sharp F.R. Implications of MMP-9 for blood-brain barrier disruption and hemorrhagic transformation following ischemic stroke. Front Cell Neurosci. 2016;10:1–13. doi: 10.3389/fncel.2016.00056
32. Thomsen M.S., Routhe L.J., Moos T. The vascular basement membrane in the healthy and pathological brain. J Cereb Blood Flow Metab. 2017;37(10):3300–17. doi: 10.1177/0271678X17722436
33. Maestrini I., Ducroquet A., Moulin S., Leys D., Cordonnier C., Bordet R. Blood biomarkers in the early stage of cerebral ischemia. Rev Neurol (Paris). 2016;172(3):198–219. doi: 10.1016/j.neurol.2016.02.003
34. Yang C., Hawkins K.E., Doré S., Candelario-Jalil E. Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am J Physiol Cell Physiol. 2019;316(2):135–153. doi: 10.1152/ajpcell.00136.2018
35. Liu J., Jin X., Liu K.J., Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J Neurosci. 2012;32:3044–3057. doi: 10.1523/JNEUROSCI.6409-11.2012
36. Park K.P., Rosell A., Foerch C., Xing C., Kim W.J., Lee S. et al. Plasma and brain matrix metalloproteinase-9 after acute focal cerebral ischemia in rats. Stroke. 2009;40:2836–2842. doi: 10.1161/STROKEAHA.109.554824
37. Asahi M., Sumii T., Fini M.E., Itohara S., Lo E.H. Matrix metalloproteinase 2 gene knockout has no eff ect on acute brain injury after focal ischemia. Neuroreport. 2001;12:3003–3007. doi: 10.1097/00001756-200109170-00050
38. Lu A., Suofu Y., Guan F., Broderick J.P., Wagner K.R., Clark J.F. Matrix metalloproteinase-2 deletions protect against hemorrhagic transformation after 1 h of cerebral ischemia and 23 h of reperfusion. Neuroscience. 2013;253:361–367. doi: 10.1016/j.neuroscience.2013.08.068
39. Sarvari S., Moakedi F., Hone E., Simpkins J.W., Ren X. Mechanisms in blood-brain barrier opening and metabolism-challenged cerebrovascular ischemia with emphasis on ischemic stroke. Metab Brain Dis. 2020;35(6):851–68. doi: 10.1007/s11011-020-00573-8
40. Lakhan S.E., Kirchgessner A., Tepper D., Leonard A. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol. 2013;4:1–15. doi: 10.3389/fneur.2013.00032
41. Suzuki Y., Nagai N., Umemura K., Collen D., Lijnen H.R. Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice. J Thromb Haemost. 2007;5:1732–1739. doi: 10.1111/j.1538-7836.2007.02628.x
42. Chelluboina B., Klopfenstein J.D., Pinson D.M., Wang D.Z., Vemuganti R., Veeravalli K.K. Matrix metalloproteinase-12 induces blood-brain barrier damage after focal cerebral ischemia. Stroke. 2015;46:3523–3531. doi: 10.1161/STROKEAHA.115.011031
43. Zhao B.Q., Wang S., Kim H.Y., Storrie H., Rosen B.R., Mooney D.J., et al. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med. 2006;12(4):441–5. doi: 10.1038/nm1387
44. Sood R.R., Taheri S., Candelario-Jalil E., Estrada E.Y., Rosenberg G.A. Early benefi cial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J Cereb Blood Flow Metab. 2008;28(2):431–8. doi: 10.1038/sj.jcbfm.9600534
45. Wójcik-Stanaszek L., Sypecka J., Szymczak P., Ziemka-Nalecz M., Khrestchatisky M., Rivera S., Zalewska T. The potential role of metalloproteinases in neurogenesis in the gerbil hippocampus following global forebrain ischemia. PLoS One. 2011;6(7):e22465. doi: 10.1371/journal.pone.0022465
46. Wang L., Zhang Z.G., Zhang R.L., Gregg S.R., Hozeska-Solgot A., LeTourneau Y., Wang Y. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. Journal of Neuroscience. 2006;26(22):5996–6003. doi: 10.1523/JNEUROSCI.5380-05.2006
47. Ma F., Martínez-San Segundo P., Barceló V., Morancho A., Gabriel-Salazar M., Giralt D. et al. Matrix metalloproteinase-13 participates in neuroprotection and neurorepair after cerebral ischemia in mice. Neurobiol Dis. 2016;91:236–46. doi: 10.1016/j.nbd.2016.03.016
48. Ould-Yahoui A., Sbai O., Baranger K., Bernard A., Gueye Y., Charrat E. et al. Role of matrix metalloproteinases in migration and neurotrophic properties of nasal olfactory stem and ensheathing cells. Cell Transplant. 2013;22(6):993–1010. doi: 10.3727/096368912X657468
49. Esquiva G., Grayston A., Rosell A. Revascularization and endothelial progenitor cells in stroke. Am J Physiol Cell Physiol. 2018;315(5):664–674. doi: 10.1152/ajpcell.00200.2018
50. Huang P.H., Chen Y.H., Wang C.H., Chen J.S., Tsai H.Y., Lin F.Y. et al. Matrix metalloproteinase-9 is essential for ischemia-induced neovascularization by modulating bone marrow-derived endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2009;29(8):1179–84. doi: 10.1161/ATVBAHA.109.189175
51. Morancho A., Hernández-Guillamon M., Boada C., Barceló V., Giralt D., Ortega L. et al. Cerebral ischaemia and matrix metalloproteinase-9 modulate the angiogenic function of early and late outgrowth endothelial progenitor cells. J Cell Mol Med. 2013;17(12):1543–53. doi: 10.1111/jcmm.12116
52. Liu C., Xie J., Sun S., Li H., Li T., Jiang C. et al. Hemorrhagic Transformation After Tissue Plasminogen Activator Treatment in Acute Ischemic Stroke. Cell Mol Neurobiol. 2022;42(3):621–646. doi: 10.1007/s10571-020-00985-1
53. Wang L., Wei C., Deng L., Wang Z., Song M., Xiong Y. The accuracy of serum matrix metalloproteinase-9 for predicting hemorrhagic transformation after acute ischemic stroke : a systematic review and metaanalysis. J Stroke Cerebrovasc Dis. 2018;27(6):1653–65. doi: 10.1016/j.jstrokecerebrovasdis.2018.01.023
54. Miao Y., Liao J.K. Potential serum biomarkers in the pathophysiological processes of stroke. Expert Rev Neurother. 2014;14(2):173–85. doi: 10.1586/14737175.2014.875471.
55. Sumii T., Lo E.H. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke. 2002;33(3):831–6. doi: 10.1161/hs0302.104542
56. Mishiro K., Ishiguro M., Suzuki Y., Tsuruma K., Shimazawa M., Hara H. A broad-spectrum matrix metalloproteinase inhibitor prevents hemorrhagic complications induced by tissue plasminogen activator in mice. Neuroscience. 2012;205:39–48. doi: 10.1016/j.neuroscience.2011.12.042
57. Fagan S.C., Waller J.L., Nichols F.T., Edwards D.J., Pettigrew L.C., Clark W.M. et al. Minocycline to improve neurologic outcome in stroke (MINOS): a dose-finding study. Stroke. 2010;41(10):2283–7. doi: 10.1161/STROKEAHA.110.582601
58. Switzer J.A., Hess D.C., Ergul A., Waller J.L., Machado L.S., Portik-Dobos V. et al. Matrix metalloproteinase-9 in an exploratory trial of intravenous minocycline for acute ischemic stroke. Stroke. 2011;42(9):2633–5. doi: 10.1161/STROKEAHA.111.618215
59. Ramos-Fernandez M., Bellolio M.F., Stead L.G. Matrix metalloproteinase-9 as a marker for acute ischemic stroke : a systematic review. J Stroke Cerebrovasc Dis. 2011;20(1):47–54. doi: 10.1016/j.jstrokecerebrovasdis.2009.10.008
60. Castellanos M., Sobrino T., Millán M., García M., Arenillas J., Nombela F. Serum cellular fibronectin and matrix metalloproteinase-9 as screening biomarkers for the prediction of parenchymal hematoma after thrombolytic therapy in acute ischemic stroke: a multicenter confirmatory study. Stroke. 2007;38(6):1855–9. doi: 10.1161/STROKEAHA.106.481556
61. Tejima E., Guo S., Murata Y., Arai K., Lok J., van Leyen K. et al. Neuroprotective effects of overexpressing tissue inhibitor of metalloproteinase TIMP-1. J Neurotrauma. 2009;26(11):1935–41. doi: 10.1089/neu.2009.0959
62. Jiang X., Namura S., Nagata I. Matrix metalloproteinase inhibitor KB-R7785 attenuates brain damage resulting from permanent focal cerebral ischemia in mice. Neurosci Lett. 2001;305(1):41–4. doi: 10.1016/s0304-3940(01)01800-6
63. Romanic A.M., White R.F., Arleth A.J., Ohlstein E.H., Barone F.C. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke. 1998;29(5):1020–30. doi: 10.1161/01.str.29.5.1020.
64. Manso H., Krug T., Sobral J. Variants of the Matrix Metalloproteinase-2 but not the Matrix Metalloproteinase-9 genes significantly infl uence functional outcome after stroke. BMC Med Genet. 2010;11(40). doi: 10.1186/1471-2350-11-40
65. Cui J., Chen S., Zhang C., Meng F., Wu W., Hu R. et al. Inhibition of MMP-9 by a selective gelatinase inhibitor protects neurovasculature from embolic focal cerebral ischemia. Mol Neurodegener. 2012;7:21. doi: 10.1186/1750-1326-7-21
66. Ranasinghe H.S., Scheepens A., Sirimanne E., Mitchell M.D., Williams C.E., Fraser M. Inhibition of MMP-9 activity following hypoxic ischemia in the developing brain using a highly specific inhibitor. Dev Neurosci. 2012;34(5):417–27. doi: 10.1159/000343257
67. Machado L.S., Sazonova I.Y., Kozak A., Wiley D.C., El-Remessy A.B., Ergul A. et al. Minocycline and tissue-type plasminogen activator for stroke: assessment of interaction potential. Stroke. 2009;40(9):3028–33. doi: 10.1161/STROKEAHA.109.556852
68. Machado L.S., Kozak A., Ergul A., Hess D.C., Borlongan C.V., Fagan S.C. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 2006;7:56. doi: 10.1186/1471-2202-7-56
69. Zhang L., Chopp M., Jia L., Cui Y., Lu M., Zhang Z.G. Atorvastatin extends the therapeutic window for tPA to 6 h after the onset of embolic stroke in rats. J Cereb Blood Flow Metab. 2009;29(11):1816–24. doi: 10.1038/jcbfm.2009.105
70. Jang J.W., Lee J.K., Lee M.C., Piao M.S., Kim S.H., Kim H.S. Melatonin reduced the elevated matrix metalloproteinase-9 level in a rat photothrombotic stroke model. J Neurol Sci. 2012;323(1–2):221–7. doi: 10.1016/j.jns.2012.09.021
71. Tanaka H., Takai S., Jin D., Furubayashi K., Inoue N., Kajimoto Y. et al. Inhibition of matrix metalloproteinase-9 activity by trandolapril after middle cerebral artery occlusion in rats. Hypertens Res. 2007;30(5):469–75. doi: 10.1291/hypres.30.469
72. Candelario-Jalil E., Taheri S., Yang Y., Sood R., Grossetete M., Estrada E.Y. et al. Cyclooxygenase inhibition limits blood-brain barrier disruption following intracerebral injection of tumor necrosis factor-alpha in the rat. J Pharmacol Exp Ther. 2007;323(2):488–98. doi: 10.1124/jpet.107.127035
73. Hamann G.F., Burggraf D., Martens H.K., Liebetrau M., Jäger G., Wunderlich N. et al. Mild to moderate hypothermia prevents microvascular basal lamina antigen loss in experimental focal cerebral ischemia. Stroke. 2004;35(3):764–9. doi: 10.1161/01.STR.0000116866.60794.21
74. Rodríguez J.A., Sobrino T., Orbe J., Purroy A., Martínez-Vila E., Castillo J., Páramo J.A. proMetalloproteinase-10 is associated with brain damage and clinical outcome in acute ischemic stroke. J Thromb Haemost. 2013;11(8):1464–73. doi: 10.1111/jth.12312
75. Horstmann S., Kalb P., Koziol J., Gardner H., Wagner S. Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke. 2003;34(9):2165–70. doi: 10.1161/01.STR.0000088062.86084.F2
76. Worthmann H., Tryc A.B., Goldbecker A., Ma Y.T., Tountopoulou A., Hahn A., et al. The temporal profile of inflammatory markers and mediators in blood after acute ischemic stroke differs depending on stroke outcome. Cerebrovasc Dis. 2010;30(1):85–92. doi: 10.1159/000314624
77. Tayebjee M.H., Nadar S., Blann A.D., Gareth Beevers D., Mac-Fadyen R.J., Lip G.Y. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in hypertension and their relationship to cardiovascular risk and treatment: a substudy of the Anglo-Scandinavian Cardiac Outcomes Trial (ASCOT). Am J Hypertens. 2004;17(9):764–9. doi: 10.1016/j.amjhyper.2004.05.019
78. Eldrup N., Grønholdt M.L., Sillesen H., Nordestgaard B.G. Elevated matrix metalloproteinase-9 associated with stroke or cardiovascular death in patients with carotid stenosis. Circulation. 2006;114(17):1847–54. doi: 10.1161/CIRCULATIONAHA.105.593483
79. Zielinska-Turek J., Dorobek M., Turek G., Barcikowska-Kotowicz M. MMP-9 and/or TIMP as predictors of ischaemic stroke in patients with symptomatic and asymptomatic atherosclerotic stenosis of carotid artery treated by stenting or endarterectomy — A review. Neurol Neurochir Pol. 2018;52(5):555–561. doi: 10.1016/j.pjnns.2018.05.005
80. Peeters W., Moll F.L., Vink A., van der Spek P.J., de Kleijn D.P., de Vries J.P. et al. Collagenase matrix metalloproteinase-8 expressed in atherosclerotic carotid plaques is associated with systemic cardiovascular outcome. Eur Heart J. 2011;32(18):2314–25. doi: 10.1093/eurheartj/ehq517
81. Tsioufi s C., Konstantinidis D., Nikolakopoulos I., Vemmou E., Kalos T., Georgiopoulos G. et al. Biomarkers of Atrial Fibrillation in Hypertension. Curr Med Chem. 2019;26(5):888–897. doi: 10.2174/0929867324666171006155516
82. Hijazi Z., Wallentin L., Lindbäck J., Alexander J.H., Connolly S.J., Eikelboom J.W. Screening of multiple biomarkers associated with ischemic stroke in atrial fi brillation. J Am Heart Assoc. 2020;9(24):e018984. doi: 10.1161/JAHA.120.018984
83. Zhong C., Yang J., Xu T., Xu T., Peng Y., Wang A. et al. Serum matrix metalloproteinase-9 levels and prognosis of acute ischemic stroke. Neurology. 2017;89(8):805–812. doi: 10.1212/WNL.0000000000004257
Review
For citations:
Kucherova K.S., Koroleva E.S., Alifirova V.M. The role of matrix metalloproteinases in the pathogenetic mechanisms of ischemic stroke. Russian neurological journal. 2024;29(3):5-15. (In Russ.) https://doi.org/10.30629/2658-7947-2024-29-3-5-15
Views:
408
Email this article 