Matrix Metalloprotease 3 Exacerbates Hemorrhagic Transformation and Worsens Functional Outcomes in Hyperglycemic Stroke

Stroke

Volumn 47, Issue 3, 2016, Pages 843-851

  Hafez, Sherif ^a   Abdelsaid, Mohammed ^a   El Shafey, Sally ^a   Johnson, Maribeth H ^a   Fagan, Susan C ^a   Ergul, Adviye ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

blood glucose; brain ischemia; hyperglycemia; intracranial hemorrhages; stroke

Indexed keywords

GLUCOSE; HEMOGLOBIN; SHORT HAIRPIN RNA; STROMELYSIN; MATRIX METALLOPROTEINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN HOMOGENATE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PERICYTE; CEREBROVASCULAR ACCIDENT; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DISEASE EXACERBATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; FUNCTIONAL STATUS; GLUCOSE BLOOD LEVEL; GRIP STRENGTH; HEMISPHERE; HEMOGLOBIN BLOOD LEVEL; HEMORRHAGIC TRANSFORMATION; HYPERGLYCEMIA; HYPERGLYCEMIC STROKE; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION; ANIMAL; BIOSYNTHESIS; CONVALESCENCE; DRUG EFFECTS; ENZYMOLOGY; GENE SILENCING; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; CEREBRAL HEMORRHAGE; GENE KNOCKDOWN TECHNIQUES; HYPERGLYCEMIA; MALE; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE INHIBITORS; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; STROKE; TREATMENT OUTCOME;

EID: 84959563821     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.115.011258     Document Type: Article

References (28)

1. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation. 2012;125:e2-e220. doi: 10.1161/CIR.0b013e31823ac046.
2. Bruno A, Biller J, Adams HP Jr, Clarke WR, Woolson RF, et al. Acute blood glucose level and outcome from ischemic stroke. Trial of org 10172 in acute stroke treatment (TOAST) investigators. Neurology. 1999;52:280-284.
3. Bruno A, Levine SR, Frankel MR, Brott TG, Lin Y, Tilley BC, et al. Admission glucose level and clinical outcomes in the NINDS rt-PA stroke trial. Neurology. 2002;59:669-674.
4. Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC. Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke. 2001;32:2426-2432.
5. Hafez S, Coucha M, Bruno A, Fagan SC, Ergul A. Hyperglycemia, acute ischemic stroke, and thrombolytic therapy. Transl StrokeRes. 2014;5:442-453. doi: 10.1007/s12975-014-0336-z.
6. Kruyt ND, Biessels GJ, Devries JH, Roos YB. Hyperglycemia in acute ischemic stroke: pathophysiology and clinical management. Nat Rev Neurol. 2010;6:145-155. doi: 10.1038/nrneurol.2009.231.
7. Elgebaly MM, Ogbi S, Li W, Mezzetti EM, Prakash R, Johnson MH, et al. Neurovascular injury in acute hyperglycemia and diabetes: a comparative analysis in experimental stroke. Transl StrokeRes. 2011;2:391-398. doi: 10.1007/s12975-011-0083-3.
8. Hafez S, Hoda MN, Guo X, Johnson MH, Fagan SC, Ergul A. Comparative analysis of different methods of ischemia/reperfusion in hyperglycemic stroke outcomes: interaction with tPA. Transl StrokeRes. 2015;6:171-180. doi: 10.1007/s12975-015-0391-0.
9. Jin R, Yang G, Li G. Molecular insights and therapeutic targets for bloodbrain barrier disruption in ischemic stroke: critical role of matrix metalloproteinases and tissue-type plasminogen activator. Neurobiol Dis. 2010;38:376-385. doi: 10.1016/j.nbd.2010.03.008.
10. Lakhan SE, Kirchgessner A, Tepper D, Leonard A. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol. 2013;4:32. doi: 10.3389/fneur.2013.00032.
11. Kim EM, Hwang O. Role of matrix metalloproteinase-3 in neurodegeneration. J Neurochem. 2011;116:22-32. doi: 10.1111/j.1471-4159.2010.07082.x.
12. Solé S, Petegnief V, Gorina R, Chamorro A, Planas AM. Activation of matrix metalloproteinase-3 and agrin cleavage in cerebral ischemia/reperfusion. J Neuropathol Exp Neurol. 2004;63:338-349.
13. Suzuki Y, Nagai N, Umemura K, Collen D, Lijnen HR. 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.
14. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI, et al; STAIR Group. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009;40:2244-2250. doi: 10.1161/STROKEAHA.108.541128.
15. Lapchak PA, Zhang JH, Noble-Haeusslein LJ. RIGOR guidelines: escalating STAIR and STEPS for effective translational research. Transl StrokeRes. 2013;4:279-285. doi: 10.1007/s12975-012-0209-2.
16. Ergul A, Elgebaly MM, Middlemore ML, Li W, Elewa H, Switzer JA, et al. Increased hemorrhagic transformation and altered infarct size and localization after experimental stroke in a rat model type 2 diabetes. BMC Neurol. 2007;7:33. doi: 10.1186/1471-2377-7-33.
17. Candelario-Jalil E, Thompson J, Taheri S, Grossetete M, Adair JC, Edmonds E, et al. Matrix metalloproteinases are associated with increased blood-brain barrier opening in vascular cognitive impairment. Stroke. 2011;42:1345-1350. doi: 10.1161/STROKEAHA.110.600825.
18. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, et al. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med. 2006;12:441-445. doi: 10.1038/nm1387.
19. Yang Y, Thompson JF, Taheri S, Salayandia VM, McAvoy TA, Hill JW, et al. Early inhibition of MMP activity in ischemic rat brain promotes expression of tight junction proteins and angiogenesis during recovery. J Cereb Blood Flow Metab. 2013;33:1104-1114. doi: 10.1038/jcbfm.2013.56.
20. Suzuki Y, Nagai N, Yamakawa K, Kawakami J, Lijnen HR, Umemura K. Tissue-type plasminogen activator (t-PA) induces stromelysin-1 (MMP-3) in endothelial cells through activation of lipoprotein receptor-related protein. Blood. 2009;114:3352-3358. doi: 10.1182/blood-2009-02-203919.
21. Castellanos M, Leira R, Serena J, Pumar JM, Lizasoain I, Castillo J, et al. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke. 2003;34:40-46.
22. Demir R, Ulvi H, Özel L, Özdemir G, Güzelcik M, Aygül R. Relationship between plasma metalloproteinase-9 levels and volume and severity of infarct in patients with acute ischemic stroke. Acta Neurol Belg. 2012;112:351-356. doi: 10.1007/s13760-012-0067-4.
23. Ramos-Fernandez M, Bellolio MF, Stead LG. Matrix metalloproteinase-9 as a marker for acute ischemic stroke: a systematic review. J StrokeCerebrovasc Dis. 2011;20:47-54. doi: 10.1016/j. jstrokecerebrovasdis.2009.10.008.
24. Pfefferkorn T, Rosenberg GA. Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke. 2003;34:2025-2030. doi: 10.1161/01.STR.0000083051.93319.28.
25. 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. doi: 10.1161/STROKEAHA.111.000309.
26. Kelly-Cobbs AI, Prakash R, Li W, Pillai B, Hafez S, Coucha M, et al. Targets of vascular protection in acute ischemic stroke differ in type 2 diabetes. Am J Physiol Heart Circ Physiol. 2013;304:H806-H815. doi: 10.1152/ajpheart.00720.2012.
27. Fagan SC, Waller JL, Nichols FT, Edwards DJ, Pettigrew LC, Clark WM, et al. Minocycline to improve neurologic outcome in stroke (MINOS): a dose-finding study. Stroke. 2010;41:2283-2287. doi: 10.1161/STROKEAHA.110.582601.
28. Switzer JA, Hess DC, Ergul A, Waller JL, Machado LS, Portik-Dobos V, et al. Matrix metalloproteinase-9 in an exploratory trial of intravenous minocycline for acute ischemic stroke. Stroke. 2011;42:2633-2635. doi: 10.1161/STROKEAHA.111.618215.