Skip to main content
Top
Published in: Metabolic Brain Disease 2/2015

01-04-2015 | Research Article

Intracerebral hemorrhage in mouse models: therapeutic interventions and functional recovery

Authors: Balachandar Kathirvelu, S. Thomas Carmichael

Published in: Metabolic Brain Disease | Issue 2/2015

Login to get access

Abstract

There has been strong pre-clinical research on mechanisms of initial cell death and tissue injury in intracerebral hemorrhage (ICH). This data has led to the evaluation of several therapeutics for neuroprotection or the mitigation of early tissue damage. Most of these studies have been done in the rat. Also, there has been little study of the mechanisms of tissue repair and recovery. This review examines the testing of candidate therapeutics in mouse models of ICH for their effect on tissue protection and repair. This review will help the readers compare it to the extensively researched rat model of ICH and thus enhance work that are pending in mouse model.
Literature
go back to reference Belayev L, Saul I, Curbelo K, Busto R, Belayev A, Zhang Y, Riyamongkol P, Zhao W, Ginsberg MD (2003) Experimental intracerebral hemorrhage in the mouse: histological, behavioral, and hemodynamic characterization of a double-injection model. Stroke 34(9):2221–2227. doi:10.1161/01.STR.0000088061.06656.1E CrossRefPubMed Belayev L, Saul I, Curbelo K, Busto R, Belayev A, Zhang Y, Riyamongkol P, Zhao W, Ginsberg MD (2003) Experimental intracerebral hemorrhage in the mouse: histological, behavioral, and hemodynamic characterization of a double-injection model. Stroke 34(9):2221–2227. doi:10.​1161/​01.​STR.​0000088061.​06656.​1E CrossRefPubMed
go back to reference Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M (1999) Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 30(4):905–915CrossRefPubMed Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M (1999) Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 30(4):905–915CrossRefPubMed
go back to reference Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, Krieger D, Mayberg M, Morgenstern L, Ogilvy CS, Vespa P, Zuccarello M, American Heart Association/American Stroke Association Stroke C, American Heart Association/American Stroke Association High Blood Pressure Research C, Quality of C, Outcomes in Research Interdisciplinary Working G (2007) Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation 116(16):e391–e413. doi:10.1161/CIRCULATIONAHA.107.183689 CrossRefPubMed Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, Krieger D, Mayberg M, Morgenstern L, Ogilvy CS, Vespa P, Zuccarello M, American Heart Association/American Stroke Association Stroke C, American Heart Association/American Stroke Association High Blood Pressure Research C, Quality of C, Outcomes in Research Interdisciplinary Working G (2007) Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation 116(16):e391–e413. doi:10.​1161/​CIRCULATIONAHA.​107.​183689 CrossRefPubMed
go back to reference Bullock R, Mendelow AD, Teasdale GM, Graham DI (1984) Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol Res 6(4):184–188PubMed Bullock R, Mendelow AD, Teasdale GM, Graham DI (1984) Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol Res 6(4):184–188PubMed
go back to reference Caplan LR (2009) Basic Pathology, anatomy, and pathophysiology of stroke. In: Caplan’s Stroke: A clinical Approach. 4th edn. Saunders Elsevier, Philadelphia, p 22 Caplan LR (2009) Basic Pathology, anatomy, and pathophysiology of stroke. In: Caplan’s Stroke: A clinical Approach. 4th edn. Saunders Elsevier, Philadelphia, p 22
go back to reference Centers for Disease C, Prevention (2009) Prevalence and most common causes of disability among adults—United States, 2005. MMWR Morbidity and mortality weekly report 58 (16):421–426 Centers for Disease C, Prevention (2009) Prevalence and most common causes of disability among adults—United States, 2005. MMWR Morbidity and mortality weekly report 58 (16):421–426
go back to reference Centers for Disease C, Prevention (2013) Vital signs: avoidable deaths from heart disease, stroke, and hypertensive disease—United States, 2001–2010. MMWR Morbidity and mortality weekly report 62 (35):721–727 Centers for Disease C, Prevention (2013) Vital signs: avoidable deaths from heart disease, stroke, and hypertensive disease—United States, 2001–2010. MMWR Morbidity and mortality weekly report 62 (35):721–727
go back to reference Chen SJ, Tsai JC, Lin TY, Chang CK, Tseng TH, Chien CL (2012b) Brain-derived neurotrophic factor-transfected and non transfected 3T3 fibroblasts enhance migratory neuroblasts and functional restoration in mice with intracerebral hemorrhage. J Neuropathol Exp Neurol 71(12):1123–1136. doi:10.1097/NEN.0b013e3182779e96 CrossRefPubMed Chen SJ, Tsai JC, Lin TY, Chang CK, Tseng TH, Chien CL (2012b) Brain-derived neurotrophic factor-transfected and non transfected 3T3 fibroblasts enhance migratory neuroblasts and functional restoration in mice with intracerebral hemorrhage. J Neuropathol Exp Neurol 71(12):1123–1136. doi:10.​1097/​NEN.​0b013e3182779e96​ CrossRefPubMed
go back to reference Chesney JA, Kondoh T, Conrad JA, Low WC (1995) Collagenase-induced Intrastriatal hemorrhage in rats results in long-term locomotor deficits. Stroke 26(2):312–316, discussion 317CrossRefPubMed Chesney JA, Kondoh T, Conrad JA, Low WC (1995) Collagenase-induced Intrastriatal hemorrhage in rats results in long-term locomotor deficits. Stroke 26(2):312–316, discussion 317CrossRefPubMed
go back to reference Counsell C, Boonyakarnkul S, Dennis M, Sandercock P, Bamford J, Burn J, Warlow C (1995) Primary intracerebral haemorrhage in the Oxford shire community stroke project. Cerebrovasc Dis 5(1):26–34CrossRef Counsell C, Boonyakarnkul S, Dennis M, Sandercock P, Bamford J, Burn J, Warlow C (1995) Primary intracerebral haemorrhage in the Oxford shire community stroke project. Cerebrovasc Dis 5(1):26–34CrossRef
go back to reference Dierksen GA, Skehan ME, Khan MA, Jeng J, Nandigam RN, Becker JA, Kumar A, Neal KL, Betensky RA, Frosch MP, Rosand J, Johnson KA, Viswanathan A, Salat DH, Greenberg SM (2010) Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 68(4):545–548. doi:10.1002/ana.22099 CrossRefPubMedCentralPubMed Dierksen GA, Skehan ME, Khan MA, Jeng J, Nandigam RN, Becker JA, Kumar A, Neal KL, Betensky RA, Frosch MP, Rosand J, Johnson KA, Viswanathan A, Salat DH, Greenberg SM (2010) Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 68(4):545–548. doi:10.​1002/​ana.​22099 CrossRefPubMedCentralPubMed
go back to reference Ewen T, Qiuting L, Chaogang T, Tao T, Jun W, Liming T, Guanghong X (2013) Neuroprotective effect of atorvastatin involves suppression of TNF-alpha and up regulation of IL-10 in a rat model of intracerebral hemorrhage. Cell Biochem Biophys 66(2):337–346. doi:10.1007/s12013-012-9453-z CrossRefPubMed Ewen T, Qiuting L, Chaogang T, Tao T, Jun W, Liming T, Guanghong X (2013) Neuroprotective effect of atorvastatin involves suppression of TNF-alpha and up regulation of IL-10 in a rat model of intracerebral hemorrhage. Cell Biochem Biophys 66(2):337–346. doi:10.​1007/​s12013-012-9453-z CrossRefPubMed
go back to reference Gillespie CD, Hurvitz KA, Centers for Disease C, Prevention (2013) Prevalence of hypertension and controlled hypertension—United States, 2007–2010. Morbidity and mortality weekly report Surveillance summaries 62 Suppl 3:144–148 Gillespie CD, Hurvitz KA, Centers for Disease C, Prevention (2013) Prevalence of hypertension and controlled hypertension—United States, 2007–2010. Morbidity and mortality weekly report Surveillance summaries 62 Suppl 3:144–148
go back to reference Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2013a) Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation. doi:10.1161/01.cir.0000441139.02102.80 Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2013a) Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation. doi:10.​1161/​01.​cir.​0000441139.​02102.​80
go back to reference Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2013b) Executive summary: heart disease and stroke statistics—2013 update: a report from the American Heart Association. Circulation 127(1):143–152CrossRefPubMed Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2013b) Executive summary: heart disease and stroke statistics—2013 update: a report from the American Heart Association. Circulation 127(1):143–152CrossRefPubMed
go back to reference Indraswari F, Wang H, Lei B, James ML, Kernagis D, Warner DS, Dawson HN, Laskowitz DT (2012) Statins improve outcome in murine models of intracranial hemorrhage and traumatic brain injury: a translational approach. J Neurotrauma 29(7):1388–1400. doi:10.1089/neu.2011.2117 CrossRefPubMed Indraswari F, Wang H, Lei B, James ML, Kernagis D, Warner DS, Dawson HN, Laskowitz DT (2012) Statins improve outcome in murine models of intracranial hemorrhage and traumatic brain injury: a translational approach. J Neurotrauma 29(7):1388–1400. doi:10.​1089/​neu.​2011.​2117 CrossRefPubMed
go back to reference James ML, Wang H, Cantillana V, Lei B, Kernagis DN, Dawson HN, Klaman LD, Laskowitz DT (2012) TT-301 inhibits microglial activation and improves outcome after central nervous system injury in adult mice. Anesthesiology 116(6):1299–1311. doi:10.1097/ALN.0b013e318253a02a CrossRefPubMed James ML, Wang H, Cantillana V, Lei B, Kernagis DN, Dawson HN, Klaman LD, Laskowitz DT (2012) TT-301 inhibits microglial activation and improves outcome after central nervous system injury in adult mice. Anesthesiology 116(6):1299–1311. doi:10.​1097/​ALN.​0b013e318253a02a​ CrossRefPubMed
go back to reference Katsuki H, Kurimoto E, Takemori S, Kurauchi Y, Hisatsune A, Isohama Y, Izumi Y, Kume T, Shudo K, Akaike A (2009) Retinoic acid receptor stimulation protects midbrain dopaminergic neurons from inflammatory degeneration via BDNF-mediated signaling. J Neurochem 110(2):707–718. doi:10.1111/j.1471-4159.2009.06171.x CrossRefPubMed Katsuki H, Kurimoto E, Takemori S, Kurauchi Y, Hisatsune A, Isohama Y, Izumi Y, Kume T, Shudo K, Akaike A (2009) Retinoic acid receptor stimulation protects midbrain dopaminergic neurons from inflammatory degeneration via BDNF-mediated signaling. J Neurochem 110(2):707–718. doi:10.​1111/​j.​1471-4159.​2009.​06171.​x CrossRefPubMed
go back to reference Kurauchi Y, Hisatsune A, Isohama Y, Sawa T, Akaike T, Shudo K, Katsuki H (2011) Midbrain dopaminergic neurons utilize nitric oxide/cyclic GMP signaling to recruit ERK that links retinoic acid receptor stimulation to up-regulation of BDNF. J Neurochem 116(3):323–333. doi:10.1111/j.1471-4159.2010.06916.x CrossRefPubMed Kurauchi Y, Hisatsune A, Isohama Y, Sawa T, Akaike T, Shudo K, Katsuki H (2011) Midbrain dopaminergic neurons utilize nitric oxide/cyclic GMP signaling to recruit ERK that links retinoic acid receptor stimulation to up-regulation of BDNF. J Neurochem 116(3):323–333. doi:10.​1111/​j.​1471-4159.​2010.​06916.​x CrossRefPubMed
go back to reference Laskowitz DT, McKenna SE, Song P, Wang H, Durham L, Yeung N, Christensen D, Vitek MP (2007) COG1410, a novel apolipoprotein E-based peptide, improves functional recovery in a murine model of traumatic brain injury. J Neurotrauma 24(7):1093–1107. doi:10.1089/neu.2006.0192 CrossRefPubMed Laskowitz DT, McKenna SE, Song P, Wang H, Durham L, Yeung N, Christensen D, Vitek MP (2007) COG1410, a novel apolipoprotein E-based peptide, improves functional recovery in a murine model of traumatic brain injury. J Neurotrauma 24(7):1093–1107. doi:10.​1089/​neu.​2006.​0192 CrossRefPubMed
go back to reference Laskowitz DT, Lei B, Dawson HN, Wang H, Bellows ST, Christensen DJ, Vitek MP, James ML (2012) The apoE-mimetic peptide, COG1410, improves functional recovery in a murine model of intracerebral hemorrhage. Neurocrit Care 16(2):316–326. doi:10.1007/s12028-011-9641-5 CrossRefPubMed Laskowitz DT, Lei B, Dawson HN, Wang H, Bellows ST, Christensen DJ, Vitek MP, James ML (2012) The apoE-mimetic peptide, COG1410, improves functional recovery in a murine model of intracerebral hemorrhage. Neurocrit Care 16(2):316–326. doi:10.​1007/​s12028-011-9641-5 CrossRefPubMed
go back to reference Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU (2007a) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25(5):1204–1212. doi:10.1634/stemcells.2006-0409 CrossRefPubMed Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU (2007a) Brain transplantation of immortalized human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25(5):1204–1212. doi:10.​1634/​stemcells.​2006-0409 CrossRefPubMed
go back to reference Lee HJ, Lim IJ, Lee MC, Kim SU (2010) Human neural stem cells genetically modified to overexpress brain-derived Neurotrophic factor promote functional recovery and neuroprotection in a mouse stroke model. J Neurosci Res 88(15):3282–3294. doi:10.1002/jnr.22474 CrossRefPubMed Lee HJ, Lim IJ, Lee MC, Kim SU (2010) Human neural stem cells genetically modified to overexpress brain-derived Neurotrophic factor promote functional recovery and neuroprotection in a mouse stroke model. J Neurosci Res 88(15):3282–3294. doi:10.​1002/​jnr.​22474 CrossRefPubMed
go back to reference MacLellan C, Shuaib A, Colbourne F (2002) Failure of delayed and prolonged hypothermia to favorably affect hemorrhagic stroke in rats. Brain Res 958(1):192–200CrossRefPubMed MacLellan C, Shuaib A, Colbourne F (2002) Failure of delayed and prolonged hypothermia to favorably affect hemorrhagic stroke in rats. Brain Res 958(1):192–200CrossRefPubMed
go back to reference Matsushita H, Hijioka M, Hisatsune A, Isohama Y, Shudo K, Katsuki H (2011) A retinoic acid receptor agonist Am80 rescues neurons, attenuates inflammatory reactions, and improves behavioral recovery after intracerebral hemorrhage in mice. J Cereb Blood Flow Metab 31(1):222–234. doi:10.1038/jcbfm.2010.80 CrossRefPubMedCentralPubMed Matsushita H, Hijioka M, Hisatsune A, Isohama Y, Shudo K, Katsuki H (2011) A retinoic acid receptor agonist Am80 rescues neurons, attenuates inflammatory reactions, and improves behavioral recovery after intracerebral hemorrhage in mice. J Cereb Blood Flow Metab 31(1):222–234. doi:10.​1038/​jcbfm.​2010.​80 CrossRefPubMedCentralPubMed
go back to reference Mey J (2001) Retinoic acid as a regulator of cytokine signaling after nerve injury. Zeitschrift fur Naturforschung C. J Biosci 56(3–4):163–176 Mey J (2001) Retinoic acid as a regulator of cytokine signaling after nerve injury. Zeitschrift fur Naturforschung C. J Biosci 56(3–4):163–176
go back to reference Minino AM, Murphy SL, Xu J, Kochanek KD (2011) Deaths: final data for 2008. National vital statistics reports: from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System 59 (10):1–126 Minino AM, Murphy SL, Xu J, Kochanek KD (2011) Deaths: final data for 2008. National vital statistics reports: from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System 59 (10):1–126
go back to reference Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2003) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. Neurosurg Focus 15(4):ECP4CrossRefPubMed Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2003) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. Neurosurg Focus 15(4):ECP4CrossRefPubMed
go back to reference Penner M, Silasi G, Wowk S, Warkentin L, Colbourne F (2011) Brief hyperthermia does not worsen outcome after Striatal hemorrhage in rats. Curr Neurovasc Res 8(1):35–43CrossRefPubMed Penner M, Silasi G, Wowk S, Warkentin L, Colbourne F (2011) Brief hyperthermia does not worsen outcome after Striatal hemorrhage in rats. Curr Neurovasc Res 8(1):35–43CrossRefPubMed
go back to reference Pontes-Neto OM, Auriel E, Greenberg SM (2012) Advances in our understanding of the pathophysiology, detection and management of cerebral amyloid angiopathy. Eur Neurol Rev 7(2):134–139PubMedCentralPubMed Pontes-Neto OM, Auriel E, Greenberg SM (2012) Advances in our understanding of the pathophysiology, detection and management of cerebral amyloid angiopathy. Eur Neurol Rev 7(2):134–139PubMedCentralPubMed
go back to reference Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M (1990) Collagenase-induced intracerebral hemorrhage in rats. Stroke 21(5):801–807CrossRefPubMed Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M (1990) Collagenase-induced intracerebral hemorrhage in rats. Stroke 21(5):801–807CrossRefPubMed
go back to reference Rynkowski MA, Kim GH, Komotar RJ, Otten ML, Ducruet AF, Zacharia BE, Kellner CP, Hahn DK, Merkow MB, Garrett MC, Starke RM, Cho BM, Sosunov SA, Connolly ES (2008) A mouse model of intracerebral hemorrhage using autologous blood infusion. Nat Protoc 3(1):122–128. doi:10.1038/nprot.2007.513 CrossRefPubMed Rynkowski MA, Kim GH, Komotar RJ, Otten ML, Ducruet AF, Zacharia BE, Kellner CP, Hahn DK, Merkow MB, Garrett MC, Starke RM, Cho BM, Sosunov SA, Connolly ES (2008) A mouse model of intracerebral hemorrhage using autologous blood infusion. Nat Protoc 3(1):122–128. doi:10.​1038/​nprot.​2007.​513 CrossRefPubMed
go back to reference Sheng SP, Lei B, James ML, Lascola CD, Venkatraman TN, Jung JY, Maze M, Franks NP, Pearlstein RD, Sheng H, Warner DS (2012) Xenon neuroprotection in experimental stroke: interactions with hypothermia and intracerebral hemorrhage. Anesthesiology 117(6):1262–1275. doi:10.1097/ALN.0b013e3182746b81 CrossRefPubMed Sheng SP, Lei B, James ML, Lascola CD, Venkatraman TN, Jung JY, Maze M, Franks NP, Pearlstein RD, Sheng H, Warner DS (2012) Xenon neuroprotection in experimental stroke: interactions with hypothermia and intracerebral hemorrhage. Anesthesiology 117(6):1262–1275. doi:10.​1097/​ALN.​0b013e3182746b81​ CrossRefPubMed
go back to reference Suzuki T, Hide I, Matsubara A, Hama C, Harada K, Miyano K, Andra M, Matsubayashi H, Sakai N, Kohsaka S, Inoue K, Nakata Y (2006) Microglial alpha7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J Neurosci Res 83(8):1461–1470. doi:10.1002/jnr.20850 CrossRefPubMed Suzuki T, Hide I, Matsubara A, Hama C, Harada K, Miyano K, Andra M, Matsubayashi H, Sakai N, Kohsaka S, Inoue K, Nakata Y (2006) Microglial alpha7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J Neurosci Res 83(8):1461–1470. doi:10.​1002/​jnr.​20850 CrossRefPubMed
go back to reference Tamakoshi K, Ishida A, Takamatsu Y, Hamakawa M, Nakashima H, Shimada H, Ishida K (2014) Motor skills training promotes motor functional recovery and induces synaptogenesis in the motor cortex and striatum after intracerebral hemorrhage in rats. Behav Brain Res 260:34–43. doi:10.1016/j.bbr.2013.11.034 CrossRefPubMed Tamakoshi K, Ishida A, Takamatsu Y, Hamakawa M, Nakashima H, Shimada H, Ishida K (2014) Motor skills training promotes motor functional recovery and induces synaptogenesis in the motor cortex and striatum after intracerebral hemorrhage in rats. Behav Brain Res 260:34–43. doi:10.​1016/​j.​bbr.​2013.​11.​034 CrossRefPubMed
go back to reference Tang YJ, Wang S, Zhu MW, Sun YL, Zhao JZ (2013) Severe pathological manifestation of cerebral amyloid angiopathy correlates with poor outcome from cerebral amyloid angiopathy related intracranial hemorrhage. Chin Med J 126(4):603–608PubMed Tang YJ, Wang S, Zhu MW, Sun YL, Zhao JZ (2013) Severe pathological manifestation of cerebral amyloid angiopathy correlates with poor outcome from cerebral amyloid angiopathy related intracranial hemorrhage. Chin Med J 126(4):603–608PubMed
go back to reference Thiyagarajan M, Sharma SS (2004) Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci 74(8):969–985CrossRefPubMed Thiyagarajan M, Sharma SS (2004) Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci 74(8):969–985CrossRefPubMed
go back to reference Wan S, Hua Y, Keep RF, Hoff JT, Xi G (2006) Deferoxamine reduces CSF free iron levels following intracerebral hemorrhage. Acta Neurochir Suppl 96:199–202CrossRefPubMed Wan S, Hua Y, Keep RF, Hoff JT, Xi G (2006) Deferoxamine reduces CSF free iron levels following intracerebral hemorrhage. Acta Neurochir Suppl 96:199–202CrossRefPubMed
go back to reference Zhao X, Sun G, Zhang J, Strong R, Song W, Gonzales N, Grotta JC, Aronowski J (2007) Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann Neurol 61(4):352–362. doi:10.1002/ana.21097 CrossRefPubMed Zhao X, Sun G, Zhang J, Strong R, Song W, Gonzales N, Grotta JC, Aronowski J (2007) Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann Neurol 61(4):352–362. doi:10.​1002/​ana.​21097 CrossRefPubMed
Metadata
Title
Intracerebral hemorrhage in mouse models: therapeutic interventions and functional recovery
Authors
Balachandar Kathirvelu
S. Thomas Carmichael
Publication date
01-04-2015
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 2/2015
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-014-9559-7

Other articles of this Issue 2/2015

Metabolic Brain Disease 2/2015 Go to the issue