Ischemic Postconditioning Decreases Cerebral Edema and Brain Blood Barrier Disruption Caused by Relief of Carotid Stenosis in a Rat Model of Cerebral Hypoperfusion

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Yang, Fuwei ^a   Zhang, Xiaojie ^b   Sun, Ying ^c   Wang, Boyu ^a   Zhou, Chuibing ^b   Luo, Yinan ^a   Ge, Pengfei ^a  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b Changchun Childrens Hospital   (China)

^c HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; EVANS BLUE; FLUORESCEIN SODIUM; GELATINASE B; OCCLUDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN PERFUSION; BRAIN WATER; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; ISCHEMIC POSTCONDITIONING; MALE; MEMBRANE PERMEABILITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; UPREGULATION; ZYMOGRAPHY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN EDEMA; CAROTID STENOSIS; CEREBROVASCULAR CIRCULATION; CLAUDIN-5; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; ISCHEMIC POSTCONDITIONING; MALE; MATRIX METALLOPROTEINASE 9; OCCLUDIN; PERMEABILITY; RATS; RATS, WISTAR;

EID: 84874566825     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057869     Document Type: Article

References (52)

1. Taussky P, Hanel RA, Meyer FB, (2011) Clinical considerations in the management of asymptomatic carotid artery stenosis. Neurosurg Focus 31: E7.
2. Young KC, Jain A, Jain M, Replogle RE, Benesch CG, et al. (2011) Evidence-based treatment of carotid artery stenosis. Neurosurg Focus 30: E2.
3. Landgraff NC, Whitney SL, Rubinstein EN, Yonas H, (2010) Cognitive and physical performance in patients with asymptomatic carotid artery disease. J Neurol 257: 982-991.
4. Zhou Z, Zhang Y, Zhu C, Sui J, Wu G, et al. (2012) Cognitive functions of carotid artery stenosis in the aged rat. Neuroscience 219: 137-144.
5. Liu H, Zhang J, Yang Y, Zhang L, Zeng X, (2012) Decreased cerebral perfusion and oxidative stress result in acute and delayed cognitive impairment. Curr Neurovasc Res 9: 152-158.
6. Wu TY, Anderson NE, Barber PA, (2012) Neurological complications of carotid revascularization. J Neurol Neurosurg Psychiatry 83: 543-550.
7. Marnane M, Ni CD, Callaly E, Sheehan OC, Merwick A, (2011) Stroke recurrence within the time window recommended for carotid endarterectomy. Neurology 77: 738-743.
8. Annambhotla S, Park MS, Keldahl ML, Morasch MD, Rodriguez HE, (2012) Early vs delayed carotid endarterectomy in symptomatic patients. J Vasc Surg 56: 1296-1302.
9. Chen YH, Lin MS, Lee JK, Chao CL, Tang SC, (2012) Carotid stenting improves cognitive function in asymptomatic cerebral ischemia. Int J Cardiol 157: 104-107.
10. Duan W, Chun-Qing Z, Zheng J, Gui L, Huang HQ, (2011) Relief of carotid stenosis improves impaired cognition in a rat model of chronic cerebral hypoperfusion. Acta Neurobiol Exp (Wars) 71: 233-243.
11. Moulakakis KG, Mylonas SN, Sfyroeras GS, Andrikopoulos V, (2009) Hyperperfusion syndrome after carotid revascularization. J Vasc Surg 49: 1060-1068.
12. Cho AH, Suh DC, Kim GE, Kim JS, Lee DH, et al. (2009) MRI evidence of reperfusion injury associated with neurological deficits after carotid revascularization procedures. Eur J Neurol 16: 1066-1069.
13. Karapanayiotides T, Meuli R, Devuyst G, Piechowski-Jozwiak B, Dewarrat A, et al. (2005) Post Carotid Endarterectomy Hyerperfusion or Reperfusion Syndrome. Stroke 36: 21-26.
14. Ivens S, Gabriel S, Greenberg G, Friedman A, Shelef I, (2010) Blood-brain barrier breakdown as a novel mechanism underlying cerebral hyperperfusion syndrome. J Neurol 257: 615-620.
15. Kokuzawa J, Kaku Y, Watarai T, Tanaka T, Hatsuda N, et al. (2010) Pure vasogenic edema caused by cerebral hyperperfusion after superficial temporal artery to middle cerebral artery anastomosis--case report. Neurol Med Chir (Tokyo) 50: 250-253.
16. Wang J, Tsirka SE, (2005) Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 128Pt 7): 1622-1633.
17. Lok J, Zhao S, Leung W, Seo JH, Navaratna D, et al. (2012) Neuregulin-1 effects on endothelial and blood-brain-barrier permeability after experimental injury. Transl Stroke Res 3(S1): S119-S124.
18. Chen F, Ohashi N, Li W, Eckman C, Nguyen JH, (2009) Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology 50: 1914-1923.
19. Lee H, Park JW, Kim SP, Lo EH, Lee SR, (2009) Doxycycline inhibits matrix metalloproteinase-9 and laminin degradation after transient global cerebral ischemia. Neurobiol Dis 34: 189-198.
20. Switzer JA, Hess DC, Ergul A, Waller JL, Machado LS, et al. (2011) Matrix Metalloproteinase-9 in an Exploratory Trial of Intravenous Minocycline for Acute Ischemic Stroke. Stroke 42: 2633-2635.
21. Gu Z, Cui J, Brown S, Fridman R, Mobashery S, et al. (2005) A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 25: 6401-6408.
22. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA, (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27: 697-709.
23. Panickar KS, Anderson RA, (2011) Effect of polyphenols on oxidative stress and mitochondrial dysfunction in neuronal death and brain edema in cerebral ischemia. Int J Mol Sci 12: 8181-8207.
24. Penna C, Mancardi D, Rastaldo R, Pagliaro P, (2009) Cardioprotection: a radical view Free radicals in pre and postconditioning. Biochim Biophys Acta 1787: 781-793.
25. Guo JY, Yang T, Sun XG, Zhou NY, Li FS, et al. (2011) Ischemic postconditioning attenuates liver warm ischemia-reperfusion injury through Akt-eNOS-NO-HIF pathway. J Biomed Sci18: 79.
26. Liu KX, Li YS, Huang WQ, Li C, Liu JX, et al. (2009) Immediate postconditioning during reperfusion attenuates intestinal injury. Intensive. Care Med 35: 933-942.
27. Liu X, Chen H, Zhan B, Xing B, Zhou J, et al. (2007) Attenuation of reperfusion injury by renal ischemic postconditioning: the role of NO. Biochem Biophys Res Commun. 359: 628-634.
28. Loukogeorgakis SP, Panagiotidou AT, Yellon DM, Deanfield JE, MacAllister RJ, (2006) Postconditioning protects against endothelial ischemia-reperfusion injury in the human forearm. Circulation 113: 1015-1019.
29. Ma XJ, Zhang XH, Li CM, Luo M, (2006) Effect of postconditioning on coronary blood flow velocity and endothelial function in patients with acute myocardial infarction. Scand Cardiovasc J 40: 327-333.
30. Xu B, Gao X, Xu J, Lei S, Xia ZY, Xu Y, Xia Z, (2011) Ischemic postconditioning attenuates lung reperfusion injury and reduces systemic proinflammatory cytokine release via heme oxygenase 1. J Surg Res 166 (2) (): e157-64.
31. Zhao H, Sapolsky RM, Steinberg GK, (2006) Interrupting reperfusion as a stroke therapy: ischemic postconditioning reduces infarct size after focal ischemia in rats. J Cereb Blood Flow Metab 26: 1114-1121.
32. Thuny F, Lairez O, Roubille F, Mewton N, Rioufol G, et al. (2012) Post-conditioning reduces infarct size and edema in patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 59: 2175-2181.
33. Liu XR, Luo M, Yan F, Zhang CC, Li SJ, et al. (2012) Ischemic postconditioning diminishes matrix metalloproteinase 9 expression and attenuates loss of the extracellular matrix proteins in rats following middle cerebral artery occlusion and reperfusion. CNS Neurosci Ther 18: 855-863.
34. Feng CF, Luo TF, Qi L, Wang BY, Luo YN, et al. (2012) Ischemic postconditioning alleviates neuronal injury caused by relief of carotid stenosis in a rat model of cerebral hypoperfusion. Int J Mol Sci 13: 13338-13351.
35. Dong X, Song YN, Liu WG, Guo XL, (2009) Mmp-9, a potential target for cerebral ischemic treatment. Curr Neuropharmacol 7: 269-275.
36. Wang JY, Shen J, Gao Q, Ye ZG, Yang SY, et al. (2008) Ischemic postconditioning protects against global cerebral ischemia/reperfusion-induced injury in rats. Stroke 39: 983-90.
37. Roach DM, Fitridge RA, Laws PE, Millard SH, Varelias A, et al. (2002) Up-regulation of MMP-2 and MMP-9 leads to degradation of type IV collagen during skeletal muscle reperfusion injury; protection by the MMP inhibitor, doxycycline. Eur J Vasc Endovasc Surg 23: 260-269.
38. Yan J, Li L, Khatibi NH, Yang L, Wang K, et al. (2011) Blood-brain barrier disruption following subarchnoid hemorrhage may be faciliated through PUMA induction of endothelial cell apoptosis from the endoplasmic reticulum. Exp Neurol 230: 240-247.
39. Lee CZ, Xu B, Hashimoto T, McCulloch CE, Yang GY, Young WL, (2004) Doxycycline suppresses cerebral matrix metalloproteinase-9 and angiogenesis induced by focal hyperstimulation of vascular endothelial growth factor in a mouse model. Stroke 35: 1715-9.
40. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, et al. (2004) Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 113: 1447-1455.
41. Yang CM, Lin CC, Lee IT, Lin YH, Yang CM, et al. (2012) Japanese encephalitis virus induces matrix metalloproteinase-9 expression via a ROS/c-Src/PDGFR/PI3K/Akt/MAPKs-dependent AP-1 pathway in rat brain astrocytes. J Neuroinflammation 9: 12.
42. Zhou C, Tu J, Zhang Q, Zhu Y, Zhang W, et al. (2011) Delayed ischemic postconditioning protects hippocampal CA1 neurons by preserving mitochondrial integrity via Akt/GSK3β signaling. Neurochem Int 59: 749-758.
43. Li ZY, Liu B, Yu J, Yang FW, Luo YN, et al. (2012) Ischemic Postconditioning Rescues Brain Injury Caused by Focal Ischemia Reperfusion via Attenuating Proteins Oxidization. Journal of International Medical Research 40: 954-966.
44. Wang Q, Zhang X, Ding Q, Hu B, Xie Y, et al. (2011) Limb remote postconditioning alleviates cerebral reperfusion injury through reactive oxygen species-mediated inhibition of delta protein kinase C in rats. Anesth Analg 113: 1180-1187.
45. Zhang W, Miao Y, Zhou S, Jiang J, Luo Q, et al. (2011) Neuroprotective effects of ischemic postconditioning on global brain ischemia in rats through upregulation of hippocampal glutamine synthetase. J Clin Neurosci 18: 685-689.
46. Yuan Y, Guo Q, Ye Z, Pingping X, Wang N, et al. (2011) Ischemic postconditioning protects brain from ischemia/reperfusion injury by attenuating endoplasmic reticulum stress-induced apoptosis through PI3K-Akt pathway. Brain Res 1367: 85-93.
47. Rehni AK, Singh TG, (2012) Involvement of CCR-2 chemokine receptor activation in ischemic preconditioning and postconditioning of brain in mice. Cytokine 60: 83-89.
48. Liu KJ, Rosenberg GA, (2005) Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med 39: 71-80.
49. Lukic-Panin V, Deguchi K, Yamashita T, Shang J, Zhang X, et al. (2010) Free radical scavenger edaravone administration protects against tissue plasminogen activator induced oxidative stress and blood brain barrier damage. Curr Neurovasc Res 7: 319-329.
50. Meng F, Liu R, Gao M, Wang Y, Yu X, et al. (2011) Pinocembrin attenuates blood-brain barrier injury induced by global cerebral ischemia-reperfusion in rats. Brain Res 1391: 93-101.
51. Lee SR, Tsuji K, Lee SR, Lo EH, (2004) Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J Neurosci 24: 671-678.
52. Jiao H, Wang Z, Liu Y, Wang P, Xue Y, (2011) Specific role of tight junction proteins claudin-5, occludin, and ZO-1 of the blood-brain barrier in a focal cerebral ischemic insult. J Mol Neurosci 44: 130-139.