Protection of Vascular Endothelial Growth Factor to Brain Edema Following Intracerebral Hemorrhage and Its Involved Mechanisms: Effect of Aquaporin-4

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Chu, Heling ^a   Tang, Yuping ^a   Dong, Qiang ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; MITOGEN ACTIVATED PROTEIN KINASE; RECOMBINANT VASCULOTROPIN; STRESS ACTIVATED PROTEIN KINASE; VASCULOTROPIN; RECOMBINANT PROTEIN; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN HEMORRHAGE; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME PHOSPHORYLATION; KNOCKOUT MOUSE; MALE; MEMBRANE PERMEABILITY; MOUSE; NEUROPROTECTION; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN CORTEX; CELL CULTURE; COMPLICATION; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

MUS;

ANIMALS; AQUAPORIN 4; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN EDEMA; CELLS, CULTURED; CEREBRAL CORTEX; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84879258004     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066051     Document Type: Article

References (53)

1. De Almodovar CR, Lambrechts D, Mazzone M, Carmellet P, (2009) Role and therapeutic potential of VEGF in the nervous system. Physiol Rev 89: 607-648.
2. Feng YZ, Rhodes PG, Bhatt AJ, (2010) Hypoxic preconditioning provides neuroprotection and increases vascular endothelial growth factor A, preserves the phosphorylation of Akt-Ser-473 and diminishes the increase in caspase-3 activity in neonatal rat hypoxic-ischemic model. Brain Res 1325: 1-9.
3. Sutherland BA, Rahman RMA, Clarkson AN, Shaw OM, Nair SM, et al. (2009) Cerebral heme oxygenase 1 and 2 spatial distribution is modulated following injury from hypoxia-ischemia and middle cerebral artery occlusion in rats. Neurosci Res 65: 326-334.
4. Wang YQ, Guo X, Qiu MH, Feng XY, Sun FY, (2007) VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion. J Neurosci Res 85: 73-82.
5. Yang JP, Liu HJ, Liu XF, (2010) VEGF promotes angiogenesis and functional recovery in stroke rats. J Invest Surg 23: 149-155.
6. Tang T, Liu XJ, Zhan ZQ, Zhou HJ, Luo JK, et al. (2007) Cerebral angiogenesis after collagenase-induced intracerebral hemorrhage in rats. Brain Res 175: 134-142.
7. Lee HJ, Kim KS, Park IH, Kim SU, (2007) Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. Plos One 156: 1-14.
8. Bates DO, (2010) Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 87: 262-271.
9. Miki Y, Nonoguchi N, Ikeda N, Coffin RS, Kuroiwa T, et al. (2007) Vascular endothelial growth factor gene-transferred bone marrow stromal cells engineered with a herpes simplex virus type 1 vector can improve neurological deficits and reduce infarction volume in rat brain ischemia. Neurosurgry 61: 586-594.
10. Harrigan MR, Ennis RS, Sullivan SE, Keep RF, (2003) Effects of Intraventricular infusion of vascular endothelial growth factor on cerebral blood flow, edema, and infarct volume. Acta Neurochir 145: 49-53.
11. Verkman AS, (2009) Knock-Out Models Reveal New Aquaporin Functions. Handb Exp Pharmacol 190: 359-381.
12. Zador Z, Stiver S, Wang V, Manley GT, (2009) Role of aquaporin-4 in cerebral edema and stroke. Handb Exp Pharmacol 190: 159-170.
13. Tang Y, Wu P, Su J, Xiang J, Cai D, et al. (2010) Effects of Aquaporin-4 on edema formation following intracerebral hemorrhage. Exp Neurol 223: 485-495.
14. Kaur C, Sivakumar V, Zhang Y, Ling EA, (2006) Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia 54: 826-839.
15. Rite I, Machado A, Cano J, Venero JL, (2008) Intracerebral VEGF injection highly upregulates AQP4 mRNA and protein in the perivascular space and glia limitans externa. Neurochem Int 52: 897-903.
16. Kilic E, Kilic U, Wang Y, Bassetti CL, Marti HH, et al. (2006) The phosphatidylinositol-3 kinase/Akt pathway mediates VEGF's neuroprotective activity and induces blood brain barrier permeability after focal cerebral ischemia. FASEB J 20: 1185-1187.
17. Greenberg DA, Jin KL, (2005) From angiogenesis to neuropathology. Nature 438: 954-959.
18. Rao KVR, Jayakumar AR, Reddy PVB, Tong XY, Curtis KM, et al. (2010) Aquaporin-4 in manganese-treated cultured astrocytes. Glia 58: 1490-1499.
19. Qi LL, Fang SH, Shi WZ, Huang XQ, Zhang XY, et al. (2011) CysLT2 receptor-mediated AQP4 up-regulation is involved in ischemic-like injury through activation of ERK and p38 MAPK in rat astrocytes. Life Sci 88: 50-56.
20. Sun Y, Jin K, Xie L, Childs J, Mao XO, et al. (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111: 1843-1851.
21. Yang CS, Tzou BC, Liu YP, Tsai MJ, Shyue SK, et al. (2008) Inhibition of cadmium-induced oxidative injury in rat primary astrocytes by the addition of antioxidants and the reduction of intracellular calcium. J Cell Biochem 183: 213-221.
22. Sanchez A, Wadhwani S, Grammas P, (2010) Multiple neurotrophic effects of VEGF on cultured neurons. Neuropeptides 44: 323-331.
23. Kawasaki T, Kitao T, Nakagawa K, Fujisaki H, Takegawa Y, et al. (2007) Nitric Oxide-Induced Apoptosis in Cultured Rat Astrocytes: Protection by Edaravone, a Radical Scavenger. Glia 55: 1325-1333.
24. Sinke AP, Jayakumar AR, Panickar KS, Moriyama M, Reddy VB, et al. (2008) NFkB in the mechanism of ammonia-induced astrocyte swelling in culture. J Neurochem 106: 2302-2311.
25. Habas A, Kharebava G, Szatmari E, Hetman M, (2006) NMDA neuroprotection against a phosphatidylinositol-3 kinase inhibitor, LY294002 by NR2B-mediated suppression of glycogen synthase kinase-3b-induced apoptosis. J Neurochem 96: 335-348.
26. Belayev L, Saul I, Curbelo K, Busto R, Belayev A, et al. (2003) Experimental intracerebral hemorrhage in the mouse histological, behavioral, and hemodynamic characterization of a double-injection model. Stroke 34: 2221-2227.
27. Agrawal HC, Davis JM, Himwich WA, (1968) Development changes in mouse brain: weight, water content and free amino acides. J Neurochem 15: 917-923.
28. Pettersson CA, Sharma HS, Olsson Y, (1990) Vascular permeability of spinal nerve roots. A study in the rat with Evans blue and lanthanum as tracers. Acta Neuropathol 81: 148-154.
29. Vajda Z, Pedersen M, Fuchtbauer EM, Wertz K, Stødkilde-Jørgensen H, et al. (2002) Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc Natl Acad Sci USA 99: 13131-13136.
30. Wang P, Ni RY, Chen MN, Mou KJ, Mao Q, et al. (2011) Expression of aquaporin-4 in human supratentorial meningiomas with peritumoral brain edema and correlation of VEGF with edema formation. Genet Mol Res10: 2165-2171.
31. Cao Y, Wang YF, Fan ZK, Yu DS, Zhang YQ, et al. (2011) 2-Methoxyestradiol inhibits the up-regulation of AQP4 and AQP1 expression after spinal cord injury. Brain Res 1370: 220-226.
32. Zhang ZG, Zhang L, Jiang Q, Zhang RL, Davies K, et al. (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106: 829-838.
33. Wang Y, Galvan V, Gorostiza O, Ataie M, Jin K, et al. (2006) Vascular endothelial growth factor improves recovery of sensorimotor and cognitive deficits after focal cerebral ischemia in the rat. Brain Res 1115: 186-193.
34. Reggio E, Loretol C, (2010) Aquaporin and Vascular Diseases. Curr Neuropharmacol 8: 105-111.
35. Xi GH, Keep RF, Hoff JT, (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5: 53-63.
36. Dobrogowska DH, Lossinsky AS, Tarnawski M, Vorbrodt AW, (1998) Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 27: 163-173.
37. Rite I, Machado A, Cano J, Venero JL, (2007) Blood-brain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons. J Neurochem 101: 1567-1582.
38. Nag S, Kapadia A, Stewart DJ, (2011) Molecular pathogenesis of blood-brain barrier breakdown in acute brain injury. Neuropath Appl Neuro 37: 3-23.
39. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR, (2009) VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA 106: 1977-1982.
40. Kaya D, Gursoy-Ozdemir Y, Yemisci M, Tuncer N, Aktan S, et al. (2005) VEGF protects brain against focal ischemia without increasing blood-brain permeability when administered intracerebroventricularly. J Cereb Blood Flow Metab 25: 1111-1118.
41. Abumiya T, Yokota C, Kuge Y, Minematsu K, (2005) Aggravation of hemorrhagic transformation by early intraarterial infusion of low-dose vascular endothelial growth factor after transient focal cerebral ischemia in rats. Brain Res 1049: 95-103.
42. Lee HT, Chang YC, Tu YF, Huang CC, (2010) CREB activation mediates VEGF-A's protection of neurons and cerebral vascular endothelial cells. J Neurochem 113: 79-91.
43. Nico B, Frigeri A, Nicchia GP, Quondamatteo F, Herken R (2001) Role of aquaporin-4 water channel in the development and integrity of the blood-brain barrier. J. Cell Sci. 114, 1297-1307.
44. Zhou JP, Kong H, Hua XD, Xiao M, Ding J, et al. (2008) Altered blood-brain barrier integrity in adult aquaporin-4 knockout mice. Neuroreport 19: 1-5.
45. Zachary I, (2005) Neuroprotective role of vascular endothelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14: 207-221.
46. Li Z, Gao L, Liu Q, Cao C, Sun XL, et al. (2006) Aquaporin-4 knockout regulated cocaine-induced behavior and neurochemical changes in mice. Neurosci Lett 403: 294-298.
47. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, et al. (2007) Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 34: 34-39.
48. Thau-Zuchman O, Shohami E, Alexandrovich AG, Leker RR, (2010) Vascular endothelial growth factor increases neurogenesis after traumatic brain injury. J Cereb Blood Flow Metab 30: 1008-1016.
49. Emerich DF, Silva E, Ali O, Mooney D, Bell W, et al. (2010) Injectable VEGF hydrogels produce near complete neurological and anatomical protection following cerebral ischemia in rats. Cell Transplant 19: 1063-1071.
50. Sobrino T, Arias S, Gonzalez RR, Brea D, Silva Y, et al. (2009) High serum levels of growth factors are associated with good outcome in intracerebral hemorrhage. J Cereb Blood Flow Metab 29: 1968-1974.
51. Wu GF, Luo JC, Rana JS, Laham R, Sellke FW, et al. (2006) Involvement of COX-2 in VEGF-induced angiogenesis via P38 and JNK pathways in vascular endothelial cells. Cardiovasc Res 69: 512-519.
52. Nakagawa T, Kaneko S, (2010) Spinal astrocytes as therapeutic targets for pathological pain. J Pharmacol Sci 114: 347-353.
53. David L, Mallet C, Vailhe B, Lamouille S, Feige JJ, et al. (2007) Activin receptor-like kinase 1 inhibits human microvascular endothelial cell migration: Potential roles for JNK and ERK kinase. J Cell Physiol 213: 484-489.