Src kinase inhibition improves acute outcomes after experimental intracerebral hemorrhage

Stroke

Volumn 38, Issue 5, 2007, Pages 1621-1625

  Ardizzone, Timothy D ^a   Zhan, Xinhua ^a   Ander, Brad P ^a   Sharp, Frank R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Behavior; Intracerebral hemorrhage; Src kinase; Striatum

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; APOMORPHINE; GLUCOSE; MATRIX METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN TYROSINE KINASE; PROTEINASE ACTIVATED RECEPTOR; THROMBIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD AUTOTRANSFUSION; BRAIN HEMORRHAGE; BRAIN INJURY; CELL COUNT; CELL DEATH; CONTROLLED STUDY; CORPUS STRIATUM; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOSE METABOLISM; HYPERMETABOLISM; MALE; NICK END LABELING; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SPRAGUE DAWLEY RAT; STAINING;

ANIMALS; CEREBRAL HEMORRHAGE; ENZYME INHIBITORS; MALE; PYRAZOLES; PYRIMIDINES; RATS; SRC-FAMILY KINASES; TREATMENT OUTCOME;

EID: 34247624074     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/STROKEAHA.106.478966     Document Type: Article

References (64)

1. Tang Y, Lu A, Aronow BJ, Wagner KR, Sharp FR. Genomic responses of the brain to ischemic stroke, intracerebral haemorrhage, kainate seizures, hypoglycemia, and hypoxia. Eur J Neurosci. 2002;15:1937-1952.
2. Lu A, Tang Y, Ran R, Ardizzone TL, Wagner KR, Sharp FR. Brain genomics of intracerebral hemorrhage. J Cereb Blood Flow Metab. 2006;26:230-252.
3. Manzerra P, Behrens MM, Canzoniero LM, Wang XQ, Heidinger V, Ichinose T, Yu SP, Choi DW. Zinc induces a src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc Natl Acad Sci U S A. 2001;98:11055-11061.
4. Thomas SM, Brugge JS. Cellular functions regulated by src family kinases. Annu Rev Cell Dev Biol. 1997;13:513-609.
5. Paul R, Zhang ZG, Eliceiri BP, Jiang Q, Boccia AD, Zhang RL, Chopp M, Cheresh DA, Schwartzberg PL, Hood JD, Leng J. Src deficiency or blockade of src activity in mice provides cerebral protection following stroke selective requirement for src kinases during VEGF-induced angiogenesis and vascular permeability. Nat Med. 2001;7:222-227.
6. Sato H, Kita M, Seiki M. V-Src activates the expression of 92-kda type iv collagenase gene through the ap-1 site and the gt box homologous to retinoblastoma control elements: a mechanism regulating gene expression independent of that by inflammatory cytokines. J Biol Chem. 1993;268:23460-23468.
7. Onodera S, Nishihira J, Iwabuchi K, Koyama Y, Yoshida K, Tanaka S, Minami A. Macrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblasts: relevance to intracellular signaling pathways. J Biol Chem. 2002;277:7865-7874.
8. Zhang Q, Thomas SM, Xi S, Smithgall TE, Siegfried JM, Kamens J, Gooding WE, Grandis JR. Src family kinases mediate epidermal growth factor receptor ligand cleavage, proliferation, and invasion of head and neck cancer cells. Cancer Res. 2004;64:6166-6173.
9. Shin EY, Ma EK, Kim CK, Kwak SJ, Kim EG. Src/erk but not phospholipase d is involved in keratinocyte growth factor-stimulated secretion of matrix metalloprotease-9 and urokinase-type plasminogen activator in snu-16 human stomach cancer cell. J Cancer Res Clin Oncol. 2002;128:596-602.
10. Ernst M, Inglese M, Scholz GM, Harder KW, Clay FJ, Bozinovski S, Waring P, Darwiche R, Kay T, Sly P, Collins R, Turner D, Hibbs ML, Anderson GP, Dunn AR. Constitutive activation of the Src family kinase Hck results in spontaneous pulmonary inflammation and an enhanced innate immune response. J Exp Med. 2002;196:589-604.
11. Guerrero J, Santibanez JF, Gonzalez A, Martinez J. EGF receptor transactivation by urokinase receptor stimulus through a mechanism involving src and matrix metalloproteinases. Exp Cell Res. 2004;292:201-208.
12. Kale G, Naren AP, Sheth P, Rao RK, Basuroy S, Kuppuswamy D, Balasubramanian S, Ray RM. Tyrosine phosphorylation of occludin attenuates its interactions with zo-1, zo-2, and zo-3 expression of kinase-inactive c-src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the caco-2 cell monolayer. Biochem Biophys Res Commun. 2003;302:324-329.
13. Liu Y, Zhang G, Gao C, Hou X. NMDA receptor activation results in tyrosine phosphorylation of nmda receptor subunit 2a(nr2a) and interaction of pyk2 and Src with nr2a after transient cerebral ischemia and reperfusion. Brain Res. 2001;909:51-58.
14. Pedram A, Razandi M, Levin ER. Deciphering vascular endothelial cell growth factor/vascular permeability factor signaling to vascular permeability: inhibition by atrial natriuretic peptide. J Biol Chem. 2002;277:44385-44398.
15. Meyer TN, Schwesinger C, Ye J, Denker BM, Nigam SK. Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity. J Biol Chem. 2001;276:22048-22055.
16. Gomez S, del Mont Llosas M, Verdu J, Roura S, Lloreta J, Fabre M, Garcia de Herreros A. Independent regulation of adherens and tight junctions by tyrosine phosphorylation in caco-2 cells. Biochim Biophys Acta. 1999;1452:121-132.
17. Lee SW, Kim WJ, Choi YK, Song HS, Son MJ, Gelman IH, Kim YJ, Kim KW, Achen MG, Clauss M, Schnurch H, Risau W. SSECKS regulates angiogenesis and tight junction formation in blood-brain barrier the nonreceptor tyrosine kinase Lyn is localised in the developing murine blood-brain barrier. Nat Med. 2003;9:900-906.
18. Xi G, Wagner KR, Keep RF, Hua Y, de Courten-Myers GM, Broderick JP, Brott TG, Hoff JT, Muizelaar JP. Role of blood clot formation on early edema development after experimental intracerebral hemorrhage. Stroke. 1998;29:2580-2586.
19. Matsushita K, Meng W, Wang X, Asahi M, Asahi K, Moskowitz MA, Lo EH. Evidence for apoptosis after intercerebral hemorrhage in rat striatum. J Cereb Blood Flow Metab. 2000;20:396-404.
20. Xi G, Keep RF, Hua Y, Xiang J, Hoff JT. Attenuation of thrombin-induced brain edema by cerebral thrombin preconditioning. Stroke. 1999;30:1247-1255.
21. Ferrell JE Jr, Martin GS. Platelet tyrosine-specific protein phosphorylation is regulated by thrombin. Mol Cell Biol. 1988;8:3603-3610.
22. Sharp FR, Bernaudin M. HIF1 and oxygen sensing in the brain. Nat Rev Neurosci. 2004;5:437-448.
23. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for src kinases during vegf-induced angiogenesis and vascular permeability. Mol Cell. 1999;4:915-924.
24. Liu Y, Cox SR, Morita T, Kourembanas S, Kern FG, McLeskey SW, Zhang L, Kurebayashi J, Ding IY, Kharbanda S, Chen D, Miller D, Cullen K. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells: identification of a 5′ enhancer transfected mcf-7 cells as a model for breast-cancer progression. Circ Res. 1995;77:638-643.
25. Jiang Y, Wu J, Keep RF, Hua Y, Hoff JT, Xi G. Hypoxia-inducible factor-1alpha accumulation in the brain after experimental intracerebral hemorrhage. J Cereb Blood Flow Metab. 2002;22:689-696.
26. Jiang BH, Agani F, Passaniti A, Semenza GL. V-Src induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-1 in tumor progression. Cancer Res. 1997;57:5328-5335.
27. Karni R, Dor Y, Keshet E, Meyuhas O, Levitzki A. Activated pp60c-src leads to elevated hypoxia-inducible factor (HIF)-1alpha expression under normoxia. J Biol Chem. 2002;277:42919-42925.
28. Vincenti MP, Coon CI, White LA, Barchowsky A, Brinckerhoff CE. Src-related tyrosine kinases regulate transcriptional activation of the interstitial collagenase gene, MMP-1, in interleukin-1-stimulated synovial fibroblasts. Arthritis Rheum. 1996;39:574-582.
29. Rosenberg GA, Estrada EY, Dencoff JE. Matrix metalloproteinases and timps are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke. 1998;29:2189-2195.
30. Ardizzone TD, Lu A, Wagner KR, Tang Y, Ran R, Sharp FR. Glutamate receptor blockade attenuates glucose hypermetabolism in perihematomal brain after experimental intracerebral hemorrhage in rat. Stroke. 2004;35:2587-2591.
31. Nakashima K, Yamashita K, Uesugi S, Ito H. Temporal and spatial profile of apoptotic cell death in transient intracerebral mass lesion of the rat. J Neurotr. 1999;16:143-151.
32. Qureshi AI, Suri MF, Ostrow PT, Kim SH, Ali Z, Shatla AA, Guterman LR, Hopkins LN. Apoptosis as a form of cell death in intracerebral hemorrhage. Neurosurgery. 2003;52:1041-1048.
33. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, Yong VW, Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol. 2003;53:731-742.
34. Deinsberger W, Vogel J, Fuchs C, Auer LM, Kuschinsky W, Boker DK. Fibrinolysis and aspiration of experimental intracerebral hematoma reduces the volume of ischemic brain in rats. Neurol Res. 1999;21:517-523.
35. Del Bigio MR, Yan HJ, Buist R, Peeling J. Experimental intracerebral hemorrhage in rats: magnetic resonance imaging and histopathological correlates. Stroke. 1996;27:2312-2319; discussion 2319-2320.
36. Hoff JT, Xi G. Brain edema from intracerebral hemorrhage. Acta Neurochir Suppl. 2003;86:11-15.
37. Xi G, Keep RF, Hoff JT. Pathophysiology of brain edema formation. Neurosurg Clin North Am. 2002;13:371-383.
38. Andaluz N, Zuccarello M, Wagner KR. Experimental animal models of intracerebral hemorrhage. Neurosurg Clin North Am. 2002;13:385-393.
39. Honkaniemi J, Massa SM, Breckinridge M, Sharp FR. Global ischemia induces apoptosis-associated genes in hippocampus. Brain Res Mol Brain Res. 1996;42:79-88.
40. Lu A, Ran R, Parmentier-Batteur S, Nee A, Sharp FR. Geldanamycin induces heat shock proteins in brain and protects against focal cerebral ischemia. J Neurochem. 2002;81:355-364.
41. Gong C, Boulis N, Qian J, Turner DE, Hoff JT, Keep RF. Intracerebral hemorrhage-induced neuronal death. Neurosurgery. 2001;48:875- 882.
42. Hickenbottom SL, Grotta JC, Strong R, Denner LA, Aronowski J. Nuclear factor-kappab and cell death after experimental intracerebral hemorrhage in rats. Stroke. 1999;30:2477-2478.
43. Xue M, Del Bigio MR. Acute tissue damage after injections of thrombin and plasmin into rat striatum. Stroke. 2001;32:2164-2169.
44. Xi G, Reiser G, Keep RF. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury:Deleterious or protective? J Neurochem. 2003;84:3-9.
45. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407:258-264.
46. Lennmyr F, Ericsson A, Gerwins P, Akterin S, Ahlstrom H, Terent A. Src family kinase-inhibitor PP2 reduces focal ischemic brain injury. Acta Neurol Scand. 2004;110:175-179.
47. Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2004;24:916-925.
48. Gingrich JR, Pelkey KA, Fam SR, Huang Y, Petralia RS, Wenthold RJ, Salter MW. Unique domain anchoring of src to synaptic nmda receptors via the mitochondrial protein NADH dehydrogenase subunit 2. Proc Natl Acad Sci U S A. 2004;101:6237-6242.
49. Kalia LV, Salter MW. Interactions between Src family protein tyrosine kinases and PSD-95. Neuropharmacology. 2003;45:720-728.
50. Qureshi AI, Ling GS, Khan J, Suri MF, Miskolczi L, Guterman LR, Hopkins LN. Quantitative analysis of injured, necrotic, and apoptotic cells in a new experimental model of intracerebral hemorrhage. Crit Care Med. 2001;29:152-157.
51. Karwacki Z, Kowianski P, Dziewatkowski J, Domaradzka-Pytel B, Ludkiewcz B, Wojcik S, Narkiewicz O, Morys J. Apoptosis in the course of experimetal intracerebral haemorrhage in the rat. Folia Morphol (Warsz). 2005;64:248-252.
52. Xue M, Del Bigio MR. Injections of blood, thrombin, and plasminogen more severely damage neonatal mouse brain than mature mouse brain. Brain Pathol. 2005;15:273-280.
53. Wagner KR, Dean C, Beiler S, Bryan DW, Packard BA, Smulian AG, Linke MJ, de Courten-Myers GM. Plasma infusions into porcine cerebral white matter induce early edema, oxidative stress, pro-inflammatory cytokine gene expression and DNA fragmentation: implications for white matter injury with increased blood-brain-barrier permeability. Curr Neurovasc Res. 2005;2:149-155.
54. Zhao X, Zhang Y, Strong R, Grotta JC, Aronowski J. 15d-prostaglandin J2 activates peroxisome proliferator-activated receptor-gamma, promotes expression of catalase, and reduces inflammation, behavioral dysfunction, and neuronal loss after intracerebral hemorrhage in rats. J Cereb Blood Flow Metab. 2006;26:811-820.
55. Matz PG, Fujimura M, Chan PH. Subarachnoid hemolysate produces DNA fragmentation in a pattern similar to apoptosis in mouse brain. Brain Res. 2000;858:312-319.
56. Lee ST, Chu K, Jung KH, Kim J, Kim EH, Kim SJ, Sinn DI, Ko SY, Kim M, Roh JK. Memantine reduces hematoma expansion in experimental intracerebral hemorrhage, resulting in functional improvement. J Cereb Blood Flow Metab. 2006;26:536-544.
57. Peeling J, Yan HJ, Corbett D, Xue M, Del Bigio MR. Effect of fk-506 on inflammation and behavioral outcome following intracerebral hemorrhage in rat. Exp Neurol. 2001;167:341-347.
58. Mayne M, Ni W, Yan HJ, Xue M, Johnston JB, Del Bigio MR, Peeling J, Power C. Antisense oligodeoxynucleotide inhibition of tumor necrosis factor-alpha expression is neuroprotective after intracerebral hemorrhage. Stroke. 2001;32:240-248.
59. Mayne M, Fotheringham J, Yan HJ, Power C, Del Bigio MR, Peeling J, Geiger JD. Adenosine a2a receptor activation reduces proinflammatory events and decreases cell death following intracerebral hemorrhage. Ann Neurol. 2001;49:727-735.
60. Rodrigues CM, Sola S, Nan Z, Castro RE, Ribeiro PS, Low WC, Steer CJ. Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc Natl Acad Sci U S A. 2003;100:6087-6092.
61. Lee ST, Chu K, Sinn DI, Jung KH, Kim EH, Kim SJ, Kim JM, Ko SY, Kim M, Roh JK. Erythropoietin reduces perihematomal inflammation and cell death with enos and stat3 activations in experimental intracerebral hemorrhage. J Neurochem. 2006;96:1728-1739.
62. Wang SJ. A role for src kinase in the regulation of glutamate release from rat cerebrocortical nerve terminals. Neuroreport. 2003;14:1519-1522.
63. Chesney JA, Kondoh T, Conrad JA, Low WC. Collagenase-induced intrastriatal hemorrhage in rats results in long-term locomotor deficits. Stroke. 1995;26:317.
64. Imamura N, Hida H, Aihara N, Ishida K, Kanda Y, Nishino H, Yamada K. Neurodeg. Neurodegeneration of substantia nigra accompanied with macrophage/microglia infiltration after intrastriatal hemorrhage. Neurosci Res. 2003;46:289-298.