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01-07-2012 | Review Article

Excitatory and Mitogenic Signaling in Cell Death, Blood–brain Barrier Breakdown, and BBB Repair after Intracerebral Hemorrhage

Authors: Da-Zhi Liu, Frank R. Sharp

Published in: Translational Stroke Research | Special Issue 1/2012

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Abstract

Intracerebral hemorrhage (ICH) results in the release of a large number of endogenous molecules, including glutamate, Ca2+, ROS, thrombin, heme, iron, TNF-α, and others. These molecules participate in excitatory and mitogenic signaling transduction in which N-methyl-d-aspartate (NMDA) receptors and Src family kinases (SFKs) are implicated. Mitogenic signaling initiates the cell cycle for normal cell division of microglia and neural progenitor cells, whereas aberrant mitogenic signaling causes toxicity, killing neurons, astrocytes, and brain microvascular endothelial cells in neurological diseases including ICH. In this review, we summarize (1) how SFKs modulate NMDA receptors to kill neurons following ICH and (2) how SFKs modulate mitogenic signaling transduction to kill neurons and play a role in disrupting the blood–brain barrier (BBB) immediately following ICH and in repairing the BBB during the recovery phases weeks following ICH.
Literature
1.
go back to reference Thiex R, Tsirka SE. Brain edema after intracerebral hemorrhage: mechanisms, treatment options, management strategies, and operative indications. Neurosurg Focus. 2007;22(5):E6.PubMedCrossRef Thiex R, Tsirka SE. Brain edema after intracerebral hemorrhage: mechanisms, treatment options, management strategies, and operative indications. Neurosurg Focus. 2007;22(5):E6.PubMedCrossRef
2.
go back to reference Thiex R, Weis J, Krings T, Barreiro S, Yakisikli-Alemi F, Gilsbach JM, et al. Addition of intravenous N-methyl-D-aspartate receptor antagonists to local fibrinolytic therapy for the optimal treatment of experimental intracerebral hemorrhages. J Neurosurg. 2007;106(2):314–20.PubMedCrossRef Thiex R, Weis J, Krings T, Barreiro S, Yakisikli-Alemi F, Gilsbach JM, et al. Addition of intravenous N-methyl-D-aspartate receptor antagonists to local fibrinolytic therapy for the optimal treatment of experimental intracerebral hemorrhages. J Neurosurg. 2007;106(2):314–20.PubMedCrossRef
3.
go back to reference Hossain MI, Kamaruddin MA, Cheng HC. Aberrant regulation and function of Src-family tyrosine kinases—their potential contributions to glutamate-induced neurotoxicity. Clin Exp Pharmacol Physiol. 2012. doi:10.1111/j.1440-1681.2011.05621.x. Hossain MI, Kamaruddin MA, Cheng HC. Aberrant regulation and function of Src-family tyrosine kinases—their potential contributions to glutamate-induced neurotoxicity. Clin Exp Pharmacol Physiol. 2012. doi:10.​1111/​j.​1440-1681.​2011.​05621.​x.
4.
go back to reference Liu DZ, Cheng XY, Ander BP, Xu H, Davis RR, Gregg JP, et al. Src kinase inhibition decreases thrombin-induced injury and cell cycle re-entry in striatal neurons. Neurobiol Dis. 2008;30(2):201–11.PubMedCrossRef Liu DZ, Cheng XY, Ander BP, Xu H, Davis RR, Gregg JP, et al. Src kinase inhibition decreases thrombin-induced injury and cell cycle re-entry in striatal neurons. Neurobiol Dis. 2008;30(2):201–11.PubMedCrossRef
5.
go back to reference Liu DZ, Ander BP, Sharp FR. Cell cycle inhibition without disruption of neurogenesis is a strategy for treatment of central nervous system diseases. Neurobiol Dis. 2010;37:549–57.PubMedCrossRef Liu DZ, Ander BP, Sharp FR. Cell cycle inhibition without disruption of neurogenesis is a strategy for treatment of central nervous system diseases. Neurobiol Dis. 2010;37:549–57.PubMedCrossRef
6.
go back to reference Liu DZ, Ander BP. Cell cycle inhibition without disruption of neurogenesis is a strategy for treatment of aberrant cell cycle diseases: an update. Sci World J, 2012, (in press). Liu DZ, Ander BP. Cell cycle inhibition without disruption of neurogenesis is a strategy for treatment of aberrant cell cycle diseases: an update. Sci World J, 2012, (in press).
7.
go back to reference Liu DZ, Ander BP. Cell cycle phase transitions: signposts for aberrant cell cycle reentry in dying mature neurons. J Cytol Histol. 2011;2:5. Liu DZ, Ander BP. Cell cycle phase transitions: signposts for aberrant cell cycle reentry in dying mature neurons. J Cytol Histol. 2011;2:5.
8.
go back to reference 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(11):2587–91.PubMedCrossRef 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(11):2587–91.PubMedCrossRef
9.
go back to reference Groveman BR, Feng S, Fang XQ, Pflueger M, Lin SX, Bienkiewicz EA, et al. The regulation of N-methyl-D-aspartate receptors by Src kinase. FEBS J. 2012;279(1):20–8.PubMedCrossRef Groveman BR, Feng S, Fang XQ, Pflueger M, Lin SX, Bienkiewicz EA, et al. The regulation of N-methyl-D-aspartate receptors by Src kinase. FEBS J. 2012;279(1):20–8.PubMedCrossRef
10.
go back to reference Ardizzone TD, Zhan X, Ander BP, Sharp FR. SRC kinase inhibition improves acute outcomes after experimental intracerebral hemorrhage. Stroke. 2007;38(5):1621–5.PubMedCrossRef Ardizzone TD, Zhan X, Ander BP, Sharp FR. SRC kinase inhibition improves acute outcomes after experimental intracerebral hemorrhage. Stroke. 2007;38(5):1621–5.PubMedCrossRef
11.
go back to reference Sharp F, Liu DZ, Zhan X, Ander BP. Intracerebral hemorrhage injury mechanisms: glutamate neurotoxicity, thrombin, and Src. Acta Neurochir Suppl. 2008;105:43–6.PubMedCrossRef Sharp F, Liu DZ, Zhan X, Ander BP. Intracerebral hemorrhage injury mechanisms: glutamate neurotoxicity, thrombin, and Src. Acta Neurochir Suppl. 2008;105:43–6.PubMedCrossRef
12.
go back to reference Oda H, Kumar S, Howley PM. Regulation of the Src family tyrosine kinase Blk through E6AP-mediated ubiquitination. Proc Natl Acad Sci USA. 1999;96(17):9557–62.PubMedCrossRef Oda H, Kumar S, Howley PM. Regulation of the Src family tyrosine kinase Blk through E6AP-mediated ubiquitination. Proc Natl Acad Sci USA. 1999;96(17):9557–62.PubMedCrossRef
13.
go back to reference Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ. Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res. 2000;2(3):203–10.PubMedCrossRef Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ. Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res. 2000;2(3):203–10.PubMedCrossRef
14.
go back to reference Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB, et al. Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell. 2007;128(2):269–80.PubMedCrossRef Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB, et al. Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell. 2007;128(2):269–80.PubMedCrossRef
15.
go back to reference Kasahara K, Nakayama Y, Nakazato Y, Ikeda K, Kuga T, Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem. 2007;282(8):5327–39.PubMedCrossRef Kasahara K, Nakayama Y, Nakazato Y, Ikeda K, Kuga T, Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem. 2007;282(8):5327–39.PubMedCrossRef
16.
go back to reference Liu Z, Falola J, Zhu X, Gu Y, Kim LT, Sarosi GA, et al. Antiproliferative effects of Src inhibition on medullary thyroid cancer. J Clin Endocrinol Metab. 2004;89(7):3503–9.PubMedCrossRef Liu Z, Falola J, Zhu X, Gu Y, Kim LT, Sarosi GA, et al. Antiproliferative effects of Src inhibition on medullary thyroid cancer. J Clin Endocrinol Metab. 2004;89(7):3503–9.PubMedCrossRef
17.
go back to reference Mishra R, Wang Y, Simonson MS. Cell cycle signaling by endothelin-1 requires Src nonreceptor protein tyrosine kinase. Mol Pharmacol. 2005;67(6):2049–56.PubMedCrossRef Mishra R, Wang Y, Simonson MS. Cell cycle signaling by endothelin-1 requires Src nonreceptor protein tyrosine kinase. Mol Pharmacol. 2005;67(6):2049–56.PubMedCrossRef
18.
19.
go back to reference Liu DZ, Ander BP, Xu H, Shen Y, Kaur P, Deng W, et al. Blood–brain barrier breakdown and repair by Src after thrombin-induced injury. Ann Neurol. 2010;67(4):526–33.PubMedCrossRef Liu DZ, Ander BP, Xu H, Shen Y, Kaur P, Deng W, et al. Blood–brain barrier breakdown and repair by Src after thrombin-induced injury. Ann Neurol. 2010;67(4):526–33.PubMedCrossRef
20.
go back to reference Liu DZ, Sharp FR. The dual role of SRC kinases in intracerebral hemorrhage. Acta Neurochir Suppl. 2011;111:77–81.PubMedCrossRef Liu DZ, Sharp FR. The dual role of SRC kinases in intracerebral hemorrhage. Acta Neurochir Suppl. 2011;111:77–81.PubMedCrossRef
21.
go back to reference Copani A, Condorelli F, Caruso A, Vancheri C, Sala A, Giuffrida Stella AM, et al. Mitotic signaling by beta-amyloid causes neuronal death. FASEB J. 1999;13(15):2225–34.PubMed Copani A, Condorelli F, Caruso A, Vancheri C, Sala A, Giuffrida Stella AM, et al. Mitotic signaling by beta-amyloid causes neuronal death. FASEB J. 1999;13(15):2225–34.PubMed
22.
go back to reference Varvel NH, Bhaskar K, Patil AR, Pimplikar SW, Herrup K, Lamb BT. Abeta oligomers induce neuronal cell cycle events in Alzheimer's disease. J Neurosci. 2008;28(43):10786–93.PubMedCrossRef Varvel NH, Bhaskar K, Patil AR, Pimplikar SW, Herrup K, Lamb BT. Abeta oligomers induce neuronal cell cycle events in Alzheimer's disease. J Neurosci. 2008;28(43):10786–93.PubMedCrossRef
23.
go back to reference Williamson R, Scales T, Clark BR, Gibb G, Reynolds CH, Kellie S, et al. Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-beta peptide exposure: involvement of Src family protein kinases. J Neurosci. 2002;22(1):10–20.PubMed Williamson R, Scales T, Clark BR, Gibb G, Reynolds CH, Kellie S, et al. Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-beta peptide exposure: involvement of Src family protein kinases. J Neurosci. 2002;22(1):10–20.PubMed
24.
go back to reference Wang H, Reiser G. Thrombin signaling in the brain: the role of protease-activated receptors. Biol Chem. 2003;384(2):193–202.PubMedCrossRef Wang H, Reiser G. Thrombin signaling in the brain: the role of protease-activated receptors. Biol Chem. 2003;384(2):193–202.PubMedCrossRef
25.
go back to reference Ohnishi M, Katsuki H, Fujimoto S, Takagi M, Kume T, Akaike A. Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury. Exp Neurol. 2007;206(1):43–52.PubMedCrossRef Ohnishi M, Katsuki H, Fujimoto S, Takagi M, Kume T, Akaike A. Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury. Exp Neurol. 2007;206(1):43–52.PubMedCrossRef
26.
go back to reference Guan J, Luo Y, Denker BM. Purkinje cell protein-2 (Pcp2) stimulates differentiation in PC12 cells by Gbetagamma-mediated activation of Ras and p38 MAPK. Biochem J. 2005;392(Pt 2):389–97.PubMed Guan J, Luo Y, Denker BM. Purkinje cell protein-2 (Pcp2) stimulates differentiation in PC12 cells by Gbetagamma-mediated activation of Ras and p38 MAPK. Biochem J. 2005;392(Pt 2):389–97.PubMed
27.
go back to reference Segarra J, Balenci L, Drenth T, Maina F, Lamballe F. Combined signaling through ERK, PI3K/AKT, and RAC1/p38 is required for met-triggered cortical neuron migration. J Biol Chem. 2006;281(8):4771–8.PubMedCrossRef Segarra J, Balenci L, Drenth T, Maina F, Lamballe F. Combined signaling through ERK, PI3K/AKT, and RAC1/p38 is required for met-triggered cortical neuron migration. J Biol Chem. 2006;281(8):4771–8.PubMedCrossRef
28.
go back to reference Lopez-Bergami P, Ronai Z. Requirements for PKC-augmented JNK activation by MKK4/7. Int J Biochem Cell Biol. 2008;40(5):1055–64.PubMedCrossRef Lopez-Bergami P, Ronai Z. Requirements for PKC-augmented JNK activation by MKK4/7. Int J Biochem Cell Biol. 2008;40(5):1055–64.PubMedCrossRef
29.
go back to reference Dwivedi Y, Pandey GN. Effects of treatment with haloperidol, chlorpromazine, and clozapine on protein kinase C (PKC) and phosphoinositide-specific phospholipase C (PI-PLC) activity and on mRNA and protein expression of PKC and PLC isozymes in rat brain. J Pharmacol Exp Ther. 1999;291(2):688–704.PubMed Dwivedi Y, Pandey GN. Effects of treatment with haloperidol, chlorpromazine, and clozapine on protein kinase C (PKC) and phosphoinositide-specific phospholipase C (PI-PLC) activity and on mRNA and protein expression of PKC and PLC isozymes in rat brain. J Pharmacol Exp Ther. 1999;291(2):688–704.PubMed
30.
go back to reference Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA. Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol. 2000;59(10):880–8.PubMed Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA. Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol. 2000;59(10):880–8.PubMed
31.
go back to reference Khurana V, Lu Y, Steinhilb ML, Oldham S, Shulman JM, Feany MB. TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr Biol. 2006;16(3):230–41.PubMedCrossRef Khurana V, Lu Y, Steinhilb ML, Oldham S, Shulman JM, Feany MB. TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr Biol. 2006;16(3):230–41.PubMedCrossRef
32.
go back to reference Xing B, Xin T, Hunter RL, Bing G. Pioglitazone inhibition of lipopolysaccharide-induced nitric oxide synthase is associated with altered activity of p38 MAP kinase and PI3K/Akt. J Neuroinflammation. 2008;5:4.PubMedCrossRef Xing B, Xin T, Hunter RL, Bing G. Pioglitazone inhibition of lipopolysaccharide-induced nitric oxide synthase is associated with altered activity of p38 MAP kinase and PI3K/Akt. J Neuroinflammation. 2008;5:4.PubMedCrossRef
33.
go back to reference Goody RJ, Beckham JD, Rubtsova K, Tyler KL. JAK-STAT signaling pathways are activated in the brain following reovirus infection. J Neurovirol. 2007;13(4):373–83.PubMedCrossRef Goody RJ, Beckham JD, Rubtsova K, Tyler KL. JAK-STAT signaling pathways are activated in the brain following reovirus infection. J Neurovirol. 2007;13(4):373–83.PubMedCrossRef
34.
go back to reference Li N, Wang C, Wu Y, Liu X, Cao X. Ca2+/calmodulin-dependent protein kinase II promotes cell cycle progression by directly activating MEK1 and subsequently modulating p27 phosphorylation. J Biol Chem. 2009;284(5):3021–7.PubMedCrossRef Li N, Wang C, Wu Y, Liu X, Cao X. Ca2+/calmodulin-dependent protein kinase II promotes cell cycle progression by directly activating MEK1 and subsequently modulating p27 phosphorylation. J Biol Chem. 2009;284(5):3021–7.PubMedCrossRef
35.
go back to reference Mao LM, Tang QS, Wang JQ. Regulation of extracellular signal-regulated kinase phosphorylation in cultured rat striatal neurons. Brain Res Bull. 2009;78(6):328–34.PubMedCrossRef Mao LM, Tang QS, Wang JQ. Regulation of extracellular signal-regulated kinase phosphorylation in cultured rat striatal neurons. Brain Res Bull. 2009;78(6):328–34.PubMedCrossRef
36.
go back to reference de Bernardo S, Canals S, Casarejos MJ, Solano RM, Menendez J, Mena MA. Role of extracellular signal-regulated protein kinase in neuronal cell death induced by glutathione depletion in neuron/glia mesencephalic cultures. J Neurochem. 2004;91(3):667–82.PubMedCrossRef de Bernardo S, Canals S, Casarejos MJ, Solano RM, Menendez J, Mena MA. Role of extracellular signal-regulated protein kinase in neuronal cell death induced by glutathione depletion in neuron/glia mesencephalic cultures. J Neurochem. 2004;91(3):667–82.PubMedCrossRef
37.
go back to reference Copani A, Nicoletti F. Cell-cycle mechanisms and neuronal cell death. New York: Kluwer Academic; 2005.CrossRef Copani A, Nicoletti F. Cell-cycle mechanisms and neuronal cell death. New York: Kluwer Academic; 2005.CrossRef
38.
go back to reference Qian JY, Leung A, Harding P, LaPointe MC. PGE2 stimulates human brain natriuretic peptide expression via EP4 and p42/44 MAPK. Am J Physiol Heart Circ Physiol. 2006;290(5):H1740–6.PubMedCrossRef Qian JY, Leung A, Harding P, LaPointe MC. PGE2 stimulates human brain natriuretic peptide expression via EP4 and p42/44 MAPK. Am J Physiol Heart Circ Physiol. 2006;290(5):H1740–6.PubMedCrossRef
39.
go back to reference Fiebich BL, Schleicher S, Spleiss O, Czygan M, Hull M. Mechanisms of prostaglandin E2-induced interleukin-6 release in astrocytes: possible involvement of EP4-like receptors, p38 mitogen-activated protein kinase and protein kinase C. J Neurochem. 2001;79(5):950–8.PubMedCrossRef Fiebich BL, Schleicher S, Spleiss O, Czygan M, Hull M. Mechanisms of prostaglandin E2-induced interleukin-6 release in astrocytes: possible involvement of EP4-like receptors, p38 mitogen-activated protein kinase and protein kinase C. J Neurochem. 2001;79(5):950–8.PubMedCrossRef
40.
go back to reference Meissirel C, Ruiz de Almodovar C, Knevels E, Coulon C, Chounlamountri N, Segura I, et al. VEGF modulates NMDA receptors activity in cerebellar granule cells through Src-family kinases before synapse formation. Proc Natl Acad Sci USA. 2011;108(33):13782–7.PubMedCrossRef Meissirel C, Ruiz de Almodovar C, Knevels E, Coulon C, Chounlamountri N, Segura I, et al. VEGF modulates NMDA receptors activity in cerebellar granule cells through Src-family kinases before synapse formation. Proc Natl Acad Sci USA. 2011;108(33):13782–7.PubMedCrossRef
41.
go back to reference Rosenberg GA. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 2009;8(2):205–16.PubMedCrossRef Rosenberg GA. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 2009;8(2):205–16.PubMedCrossRef
42.
go back to reference Xiao L, Hu C, Feng C, Chen Y. Switching of N-methyl-D-aspartate (NMDA) receptor-favorite intracellular signal pathways from ERK1/2 protein to p38 mitogen-activated protein kinase leads to developmental changes in NMDA neurotoxicity. J Biol Chem. 2011;286(23):20175–93.PubMedCrossRef Xiao L, Hu C, Feng C, Chen Y. Switching of N-methyl-D-aspartate (NMDA) receptor-favorite intracellular signal pathways from ERK1/2 protein to p38 mitogen-activated protein kinase leads to developmental changes in NMDA neurotoxicity. J Biol Chem. 2011;286(23):20175–93.PubMedCrossRef
43.
go back to reference Centeno C, Repici M, Chatton JY, Riederer BM, Bonny C, Nicod P, et al. Role of the JNK pathway in NMDA-mediated excitotoxicity of cortical neurons. Cell Death Differ. 2007;14(2):240–53.PubMedCrossRef Centeno C, Repici M, Chatton JY, Riederer BM, Bonny C, Nicod P, et al. Role of the JNK pathway in NMDA-mediated excitotoxicity of cortical neurons. Cell Death Differ. 2007;14(2):240–53.PubMedCrossRef
44.
go back to reference Jantas D, Szymanska M, Budziszewska B, Lason W. An involvement of BDNF and PI3-K/Akt in the anti-apoptotic effect of memantine on staurosporine-evoked cell death in primary cortical neurons. Apoptosis. 2009;14(7):900–12.PubMedCrossRef Jantas D, Szymanska M, Budziszewska B, Lason W. An involvement of BDNF and PI3-K/Akt in the anti-apoptotic effect of memantine on staurosporine-evoked cell death in primary cortical neurons. Apoptosis. 2009;14(7):900–12.PubMedCrossRef
45.
go back to reference Yu XM, Askalan R, Keil 2nd GJ, Salter MW. NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science. 1997;275(5300):674–8.PubMedCrossRef Yu XM, Askalan R, Keil 2nd GJ, Salter MW. NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science. 1997;275(5300):674–8.PubMedCrossRef
46.
go back to reference Salter MW, Kalia LV. Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci. 2004;5(4):317–28.PubMedCrossRef Salter MW, Kalia LV. Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci. 2004;5(4):317–28.PubMedCrossRef
47.
go back to reference Trepanier CH, Jackson MF, MacDonald JF. Regulation of NMDA receptors by the tyrosine kinase Fyn. FEBS J. 2012;279(1):12–9.PubMedCrossRef Trepanier CH, Jackson MF, MacDonald JF. Regulation of NMDA receptors by the tyrosine kinase Fyn. FEBS J. 2012;279(1):12–9.PubMedCrossRef
48.
go back to reference Choi UB, Xiao S, Wollmuth LP, Bowen ME. Effect of Src kinase phosphorylation on disordered C-terminal domain of N-methyl-D-aspartic acid (NMDA) receptor subunit GluN2B protein. J Biol Chem. 2011;286(34):29904–12.PubMedCrossRef Choi UB, Xiao S, Wollmuth LP, Bowen ME. Effect of Src kinase phosphorylation on disordered C-terminal domain of N-methyl-D-aspartic acid (NMDA) receptor subunit GluN2B protein. J Biol Chem. 2011;286(34):29904–12.PubMedCrossRef
49.
go back to reference Heidinger V, Manzerra P, Wang XQ, Strasser U, Yu SP, Choi DW, et al. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J Neurosci. 2002;22(13):5452–61.PubMed Heidinger V, Manzerra P, Wang XQ, Strasser U, Yu SP, Choi DW, et al. Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J Neurosci. 2002;22(13):5452–61.PubMed
50.
go back to reference Bernabeu R, Sharp FR. NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab. 2000;20(12):1669–80.PubMedCrossRef Bernabeu R, Sharp FR. NMDA and AMPA/kainate glutamate receptors modulate dentate neurogenesis and CA3 synapsin-I in normal and ischemic hippocampus. J Cereb Blood Flow Metab. 2000;20(12):1669–80.PubMedCrossRef
51.
go back to reference Liu J, Solway K, Messing RO, Sharp FR. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci. 1998;18(19):7768–78.PubMed Liu J, Solway K, Messing RO, Sharp FR. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci. 1998;18(19):7768–78.PubMed
52.
go back to reference Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood–brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol. 2006;1(3):223–36.PubMedCrossRef Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood–brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol. 2006;1(3):223–36.PubMedCrossRef
53.
go back to reference Banerjee S, Bhat MA. Neuron-glial interactions in blood–brain barrier formation. Annu Rev Neurosci. 2007;30:235–58.PubMedCrossRef Banerjee S, Bhat MA. Neuron-glial interactions in blood–brain barrier formation. Annu Rev Neurosci. 2007;30:235–58.PubMedCrossRef
54.
go back to reference Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci. 2006;26(50):13007–16.PubMedCrossRef Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci. 2006;26(50):13007–16.PubMedCrossRef
55.
go back to reference Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 2000;425(4):479–94.PubMedCrossRef Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 2000;425(4):479–94.PubMedCrossRef
Metadata
Title
Excitatory and Mitogenic Signaling in Cell Death, Blood–brain Barrier Breakdown, and BBB Repair after Intracerebral Hemorrhage
Authors
Da-Zhi Liu
Frank R. Sharp
Publication date
01-07-2012
Publisher
Springer-Verlag
Published in
Translational Stroke Research / Issue Special Issue 1/2012
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-012-0147-z