Skip to main content
SpringerLink
Log in

Experimental Global Ischemia and White Matter Injury

  • Chapter
  • First Online:
White Matter Injury in Stroke and CNS Disease

Part of the book series: Springer Series in Translational Stroke Research ((SSTSR,volume 4))

  • 1419 Accesses

Abstract

White matter injury has been increasingly recognized as an important part of several CNS diseases including brain ischemia. However, compared to mechanisms of neuronal cell death in gray matter, white matter pathophysiology remains relatively understudied and poorly understood. This is especially true in the research field of global ischemia. In both experimental animals and humans, transient global cerebral ischemia leads to delayed cell death in selectively vulnerable brain areas, such as hippocampus, striatum, and the layers 3, 5, and 6 in cortex. Thus far, most efforts in this field have focused on understanding the mechanisms of neuronal cell death, especially in hippocampal CA1 region. However, studies using whole-animal and cell culture models of global ischemia have shown key mechanisms of white matter damage after the injury. In this chapter, we overview those rodent models of global ischemia and, then, try to summarize the current knowledge about the white matter pathophysiology. Similar to stroke or head injury, white matter damage by global cerebral ischemia, such as cardiac arrest, remains a major cause of permanent disability. Hence, a deeper understanding of pathophysiology of white matter injury after global cerebral ischemia may eventually lead us to new therapeutic targets for patients suffering from a wide range of white matter-related diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Alberdi E, Sanchez-Gomez MV, Torre I, Domercq M, Perez-Samartin A, Perez-Cerda F, Matute C (2006) Activation of kainate receptors sensitizes oligodendrocytes to complement attack. J Neurosci 26:3220–3228

    PubMed  CAS  Google Scholar 

  • Alvarez-Sabin J, Delgado P, Abilleira S, Molina CA, Arenillas J, Ribo M, Santamarina E, Quintana M, Monasterio J, Montaner J (2004) Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: relationship to clinical and radiological outcome. Stroke 35:1316–1322

    PubMed  CAS  Google Scholar 

  • Anthony DC, Ferguson B, Matyzak MK, Miller KM, Esiri MM, Perry VH (1997) Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol Appl Neurobiol 23:406–415

    PubMed  CAS  Google Scholar 

  • Arai K, Lo EH (2009) Experimental models for analysis of oligodendrocyte pathophysiology in stroke. Exp Transl Stroke Med 1:6

    PubMed  Google Scholar 

  • Arai K, Lee SR, Lo EH (2003) Essential role for ERK mitogen-activated protein kinase in matrix metalloproteinase-9 regulation in rat cortical astrocytes. Glia 43:254–264

    PubMed  Google Scholar 

  • Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 18:6241–6253

    PubMed  CAS  Google Scholar 

  • Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455–463

    PubMed  CAS  Google Scholar 

  • Bakiri Y, Hamilton NB, Karadottir R, Attwell D (2008) Testing NMDA receptor block as a therapeutic strategy for reducing ischaemic damage to CNS white matter. Glia 56:233–240

    PubMed  Google Scholar 

  • Bakiri Y, Burzomato V, Frugier G, Hamilton NB, Karadottir R, Attwell D (2009) Glutamatergic signaling in the brain's white matter. Neuroscience 158:266–274

    PubMed  CAS  Google Scholar 

  • Baltan S (2009) Ischemic injury to white matter: an age-dependent process. Neuroscientist 15: 126–133

    PubMed  CAS  Google Scholar 

  • Baltan S, Besancon EF, Mbow B, Ye Z, Hamner MA, Ransom BR (2008) White matter vulnerability to ischemic injury increases with age because of enhanced excitotoxicity. J Neurosci 28: 1479–1489

    PubMed  CAS  Google Scholar 

  • Bendel O, Alkass K, Bueters T, von Euler M, von Euler G (2005a) Reproducible loss of CA1 neurons following carotid artery occlusion combined with halothane-induced hypotension. Brain Res 1033:135–142

    PubMed  CAS  Google Scholar 

  • Bendel O, Bueters T, von Euler M, Ove Ogren S, Sandin J, von Euler G (2005b) Reappearance of hippocampal CA1 neurons after ischemia is associated with recovery of learning and memory. J Cereb Blood Flow Metab 25:1586–1595

    PubMed  CAS  Google Scholar 

  • Benveniste H, Jorgensen MB, Sandberg M, Christensen T, Hagberg H, Diemer NH (1989) Ischemic damage in hippocampal CA1 is dependent on glutamate release and intact innervation from CA3. J Cereb Blood Flow Metab 9:629–639

    PubMed  CAS  Google Scholar 

  • Bottiger BW, Teschendorf P, Krumnikl JJ, Vogel P, Galmbacher R, Schmitz B, Motsch J, Martin E, Gass P (1999) Global cerebral ischemia due to cardiocirculatory arrest in mice causes neuronal degeneration and early induction of transcription factor genes in the hippocampus. Brain Res Mol Brain Res 65:135–142

    PubMed  CAS  Google Scholar 

  • Bueters T, von Euler M, Bendel O, von Euler G (2008) Degeneration of newly formed CA1 neurons following global ischemia in the rat. Exp Neurol 209:114–124

    PubMed  CAS  Google Scholar 

  • Buntinx M, Gielen E, Van Hummelen P, Raus J, Ameloot M, Steels P, Stinissen P (2004) Cytokine-induced cell death in human oligodendroglial cell lines. II: alterations in gene expression induced by interferon-gamma and tumor necrosis factor-alpha. J Neurosci Res 76:846–861

    PubMed  CAS  Google Scholar 

  • Cai Z, Lin S, Fan LW, Pang Y, Rhodes PG (2006) Minocycline alleviates hypoxic-ischemic injury to developing oligodendrocytes in the neonatal rat brain. Neuroscience 137:425–435

    PubMed  CAS  Google Scholar 

  • Carty ML, Wixey JA, Colditz PB, Buller KM (2008) Post-insult minocycline treatment attenuates hypoxia-ischemia-induced neuroinflammation and white matter injury in the neonatal rat: a comparison of two different dose regimens. Int J Dev Neurosci 26:477–485

    PubMed  CAS  Google Scholar 

  • Chandler MJ, DeLeo J, Carney JM (1985) An unanesthetized-gerbil model of cerebral ischemia-induced behavioral changes. J Pharmacol Methods 14:137–146

    PubMed  CAS  Google Scholar 

  • Chandler S, Coates R, Gearing A, Lury J, Wells G, Bone E (1995) Matrix metalloproteinases degrade myelin basic protein. Neurosci Lett 201:223–226

    PubMed  CAS  Google Scholar 

  • Dewar D, Underhill SM, Goldberg MP (2003) Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 23:263–274

    PubMed  Google Scholar 

  • Dirnagl U, Becker K, Meisel A (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8:398–412

    PubMed  CAS  Google Scholar 

  • D'Souza CA, Moscarello MA (2006) Differences in susceptibility of MBP charge isomers to digestion by stromelysin-1 (MMP-3) and release of an immunodominant epitope. Neurochem Res 31:1045–1054

    PubMed  Google Scholar 

  • Fagan SC, Waller JL, Nichols FT, Edwards DJ, Pettigrew LC, Clark WM, Hall CE, Switzer JA, Ergul A, Hess DC (2010) Minocycline to improve neurologic outcome in stroke (MINOS): a dose-finding study. Stroke 41:2283–2287

    PubMed  CAS  Google Scholar 

  • Fan LW, Lin S, Pang Y, Lei M, Zhang F, Rhodes PG, Cai Z (2005) Hypoxia-ischemia induced neurological dysfunction and brain injury in the neonatal rat. Behav Brain Res 165:80–90

    PubMed  CAS  Google Scholar 

  • Feuerstein GZ, Wang X, Barone FC (1998) The role of cytokines in the neuropathology of stroke and neurotrauma. Neuroimmunomodulation 5:143–159

    PubMed  CAS  Google Scholar 

  • Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE (2004) Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 24:4412–4420

    PubMed  CAS  Google Scholar 

  • Gallo V, Patneau DK, Mayer ML, Vaccarino FM (1994) Excitatory amino acid receptors in glial progenitor cells: molecular and functional properties. Glia 11:94–101

    PubMed  CAS  Google Scholar 

  • Genc K, Genc S, Baskin H, Semin I (2006) Erythropoietin decreases cytotoxicity and nitric oxide formation induced by inflammatory stimuli in rat oligodendrocytes. Physiol Res 55:33–38

    PubMed  CAS  Google Scholar 

  • Genersch E, Hayess K, Neuenfeld Y, Haller H (2000) Sustained ERK phosphorylation is necessary but not sufficient for MMP-9 regulation in endothelial cells: involvement of ras-dependent and -independent pathways. J Cell Sci 113(Pt 23):4319–4330

    PubMed  CAS  Google Scholar 

  • Gidday JM (2006) Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 7:437–448

    PubMed  CAS  Google Scholar 

  • Gijbels K, Proost P, Masure S, Carton H, Billiau A, Opdenakker G (1993) Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein. J Neurosci Res 36:432–440

    PubMed  CAS  Google Scholar 

  • Gordon PH, Moore DH, Miller RG, Florence JM, Verheijde JL, Doorish C, Hilton JF, Spitalny GM, MacArthur RB, Mitsumoto H, Neville HE, Boylan K, Mozaffar T, Belsh JM, Ravits J, Bedlack RS, Graves MC, McCluskey LF, Barohn RJ, Tandan R (2007) Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol 6:1045–1053

    PubMed  CAS  Google Scholar 

  • Grewer C, Gameiro A, Zhang Z, Tao Z, Braams S, Rauen T (2008) Glutamate forward and reverse transport: from molecular mechanism to transporter-mediated release after ischemia. IUBMB Life 60:609–619

    PubMed  CAS  Google Scholar 

  • Hara K, Yasuhara T, Matsukawa N, Maki M, Masuda T, Yu G, Xu L, Tambrallo L, Rodriguez NA, Stern DM, Kawase T, Yamashima T, Buccafusco JJ, Hess DC, Borlongan CV (2007) Hippocampal CA1 cell loss in a non-human primate model of transient global ischemia: a pilot study. Brain Res Bull 74:164–171

    PubMed  CAS  Google Scholar 

  • Hatakeyama T, Matsumoto M, Brengman JM, Yanagihara T (1988) Immunohistochemical investigation of ischemic and postischemic damage after bilateral carotid occlusion in gerbils. Stroke 19:1526–1534

    PubMed  CAS  Google Scholar 

  • Hewlett KA, Corbett D (2006) Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 141:27–33

    PubMed  CAS  Google Scholar 

  • Hirano A, Zimmerman HM (1971) Some new pathological findings in the central myelinated axon. J Neuropathol Exp Neurol 30:325–336

    PubMed  CAS  Google Scholar 

  • Horn M, Schlote W (1992) Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol 85:79–87

    PubMed  CAS  Google Scholar 

  • Horstmann S, Kalb P, Koziol J, Gardner H, Wagner S (2003) Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke 34: 2165–2170

    PubMed  Google Scholar 

  • Husain J, Juurlink BH (1995) Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species. Brain Res 698:86–94

    PubMed  CAS  Google Scholar 

  • Iadecola C, Anrather J (2011) The immunology of stroke: from mechanisms to translation. Nat Med 17:796–808

    PubMed  CAS  Google Scholar 

  • Imai H, Masayasu H, Dewar D, Graham DI, Macrae IM (2001) Ebselen protects both gray and white matter in a rodent model of focal cerebral ischemia. Stroke 32:2149–2154

    PubMed  CAS  Google Scholar 

  • Irving EA, Yatsushiro K, McCulloch J, Dewar D (1997) Rapid alteration of tau in oligodendrocytes after focal ischemic injury in the rat: involvement of free radicals. J Cereb Blood Flow Metab 17:612–622

    PubMed  CAS  Google Scholar 

  • Iwai M, Stetler RA, Xing J, Hu X, Gao Y, Zhang W, Chen J, Cao G (2010) Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 41:1032–1037

    PubMed  CAS  Google Scholar 

  • James G, Butt AM (2001) P2X and P2Y purinoreceptors mediate ATP-evoked calcium signalling in optic nerve glia in situ. Cell Calcium 30:251–259

    PubMed  CAS  Google Scholar 

  • Jean WC, Spellman SR, Nussbaum ES, Low WC (1998) Reperfusion injury after focal cerebral ischemia: the role of inflammation and the therapeutic horizon. Neurosurgery 43:1382–1396, discussion 1396–1387

    PubMed  CAS  Google Scholar 

  • Kalaria RN (2012) Cerebrovascular disease and mechanisms of cognitive impairment: evidence from clinicopathological studies in humans. Stroke 43:2526–2534

    PubMed  Google Scholar 

  • Karadottir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–1166

    PubMed  CAS  Google Scholar 

  • Kawahara N, Ruetzler CA, Klatzo I (1995) Protective effect of spreading depression against neuronal damage following cardiac arrest cerebral ischaemia. Neurol Res 17:9–16

    PubMed  CAS  Google Scholar 

  • Kim YS, Kim SU (1991) Oligodendroglial cell death induced by oxygen radicals and its protection by catalase. J Neurosci Res 29:100–106

    PubMed  CAS  Google Scholar 

  • Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57–69

    PubMed  CAS  Google Scholar 

  • Kirino T, Sano K (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol 62:201–208

    PubMed  CAS  Google Scholar 

  • Kirino T, Tamura A, Sano K (1986) A reversible type of neuronal injury following ischemia in the gerbil hippocampus. Stroke 17:455–459

    PubMed  CAS  Google Scholar 

  • Kiryk A, Pluta R, Figiel I, Mikosz M, Ulamek M, Niewiadomska G, Jablonski M, Kaczmarek L (2011) Transient brain ischemia due to cardiac arrest causes irreversible long-lasting cognitive injury. Behav Brain Res 219:1–7

    PubMed  Google Scholar 

  • Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, Handa N, Fukunaga R, Kimura K, Mikoshiba K et al (1990) “Ischemic tolerance” phenomenon found in the brain. Brain Res 528:21–24

    PubMed  CAS  Google Scholar 

  • Kitagawa K, Matsumoto M, Yang G, Mabuchi T, Yagita Y, Hori M, Yanagihara T (1998) Cerebral ischemia after bilateral carotid artery occlusion and intraluminal suture occlusion in mice: evaluation of the patency of the posterior communicating artery. J Cereb Blood Flow Metab 18:570–579

    PubMed  CAS  Google Scholar 

  • Kofler J, Hattori K, Sawada M, DeVries AC, Martin LJ, Hurn PD, Traystman RJ (2004) Histopathological and behavioral characterization of a novel model of cardiac arrest and cardiopulmonary resuscitation in mice. J Neurosci Methods 136:33–44

    PubMed  Google Scholar 

  • Kubo K, Nakao S, Jomura S, Sakamoto S, Miyamoto E, Xu Y, Tomimoto H, Inada T, Shingu K (2009) Edaravone, a free radical scavenger, mitigates both gray and white matter damages after global cerebral ischemia in rats. Brain Res 1279:139–146

    PubMed  CAS  Google Scholar 

  • Langdon KD, Granter-Button S, Corbett D (2008) Persistent behavioral impairments and neuroinflammation following global ischemia in the rat. Eur J Neurosci 28:2310–2318

    PubMed  Google Scholar 

  • Le Feuvre RA, Brough D, Touzani O, Rothwell NJ (2003) Role of P2X7 receptors in ischemic and excitotoxic brain injury in vivo. J Cereb Blood Flow Metab 23:381–384

    PubMed  Google Scholar 

  • Lee SR, Tsuji K, Lo EH (2004) Role of matrix metalloproteinases in delayed neuronal damage after transient global cerebral ischemia. J Neurosci 24:671–678

    PubMed  CAS  Google Scholar 

  • Lee SR, Kim HY, Rogowska J, Zhao BQ, Bhide P, Parent JM, Lo EH (2006) Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26:3491–3495

    PubMed  CAS  Google Scholar 

  • Levene MI, Sands C, Grindulis H, Moore JR (1986) Comparison of two methods of predicting outcome in perinatal asphyxia. Lancet 1:67–69

    PubMed  CAS  Google Scholar 

  • Levine S, Payan H (1966) Effects of ischemia and other procedures on the brain and retina of the gerbil (Meriones unguiculatus). Exp Neurol 16:255–262

    PubMed  CAS  Google Scholar 

  • Lin S, Rhodes PG, Lei M, Zhang F, Cai Z (2004) alpha-Phenyl-n-tert-butyl-nitrone attenuates hypoxic-ischemic white matter injury in the neonatal rat brain. Brain Res 1007:132–141

    PubMed  CAS  Google Scholar 

  • Lin S, Cox HJ, Rhodes PG, Cai Z (2006) Neuroprotection of alpha-phenyl-n-tert-butyl-nitrone on the neonatal white matter is associated with anti-inflammation. Neurosci Lett 405:52–56

    PubMed  CAS  Google Scholar 

  • Lipton SA (2006) NMDA receptors, glial cells, and clinical medicine. Neuron 50:9–11

    PubMed  CAS  Google Scholar 

  • Lo EH (2008) A new penumbra: transitioning from injury into repair after stroke. Nat Med 14: 497–500

    PubMed  CAS  Google Scholar 

  • Macdonald H, Kelly RG, Allen ES, Noble JF, Kanegis LA (1973) Pharmacokinetic studies on minocycline in man. Clin Pharmacol Ther 14:852–861

    PubMed  CAS  Google Scholar 

  • Manning SM, Talos DM, Zhou C, Selip DB, Park HK, Park CJ, Volpe JJ, Jensen FE (2008) NMDA receptor blockade with memantine attenuates white matter injury in a rat model of periventricular leukomalacia. J Neurosci 28:6670–6678

    PubMed  CAS  Google Scholar 

  • Matute C (2011) Glutamate and ATP signalling in white matter pathology. J Anat 219:53–64

    PubMed  CAS  Google Scholar 

  • Matute C, Alberdi E, Domercq M, Sanchez-Gomez MV, Perez-Samartin A, Rodriguez-Antiguedad A, Perez-Cerda F (2007) Excitotoxic damage to white matter. J Anat 210:693–702

    PubMed  CAS  Google Scholar 

  • Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK (2006) NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988–992

    PubMed  CAS  Google Scholar 

  • Mishima K, Ikeda T, Aoo N, Takai N, Takahashi S, Egashira N, Ikenoue T, Iwasaki K, Fujiwara M (2005) Hypoxia-ischemic insult in neonatal rats induced slowly progressive brain damage related to memory impairment. Neurosci Lett 376:194–199

    PubMed  CAS  Google Scholar 

  • Montaner J, Alvarez-Sabin J, Molina C, Angles A, Abilleira S, Arenillas J, Gonzalez MA, Monasterio J (2001) Matrix metalloproteinase expression after human cardioembolic stroke: temporal profile and relation to neurological impairment. Stroke 32:1759–1766

    PubMed  CAS  Google Scholar 

  • Nakayama M, Uchimura K, Zhu RL, Nagayama T, Rose ME, Stetler RA, Isakson PC, Chen J, Graham SH (1998) Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc Natl Acad Sci U S A 95:10954–10959

    PubMed  CAS  Google Scholar 

  • North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067

    PubMed  CAS  Google Scholar 

  • O’Neill M, Canney M, Earley B, Junien JL, Leonard BE (1996) The novel sigma ligand JO 1994 protects against ischaemia-induced behavioural changes, cell death and receptor dysfunction in the gerbil. Neurochem Int 28:193–207

    PubMed  Google Scholar 

  • Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ (1993) Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 13:1441–1453

    PubMed  CAS  Google Scholar 

  • Onken M, Berger S, Kristian T (2012) Simple model of forebrain ischemia in mouse. J Neurosci Methods 204:254–261

    PubMed  Google Scholar 

  • Othman T, Yan H, Rivkees SA (2003) Oligodendrocytes express functional A1 adenosine receptors that stimulate cellular migration. Glia 44:166–172

    PubMed  Google Scholar 

  • Panahian N, Yoshida T, Huang PL, Hedley-Whyte ET, Dalkara T, Fishman MC, Moskowitz MA (1996) Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience 72:343–354

    PubMed  CAS  Google Scholar 

  • Petito CK, Olarte JP, Roberts B, Nowak TS Jr, Pulsinelli WA (1998) Selective glial vulnerability following transient global ischemia in rat brain. J Neuropathol Exp Neurol 57:231–238

    PubMed  CAS  Google Scholar 

  • Proctor PH, Tamborello LP (2007) SAINT-I worked, but the neuroprotectant is not NXY-059. Stroke 38:e109, author reply e110

    PubMed  Google Scholar 

  • Pulsinelli WA, Brierley JB (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10:267–272

    PubMed  CAS  Google Scholar 

  • Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491–498

    PubMed  CAS  Google Scholar 

  • Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492

    PubMed  CAS  Google Scholar 

  • Recker R, Adami A, Tone B, Tian HR, Lalas S, Hartman RE, Obenaus A, Ashwal S (2009) Rodent neonatal bilateral carotid artery occlusion with hypoxia mimics human hypoxic-ischemic injury. J Cereb Blood Flow Metab 29:1305–1316

    PubMed  Google Scholar 

  • Rennie JM, Hagmann CF, Robertson NJ (2007) Outcome after intrapartum hypoxic ischaemia at term. Semin Fetal Neonatal Med 12:398–407

    PubMed  Google Scholar 

  • Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J (2005) A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke 36:1415–1420

    PubMed  CAS  Google Scholar 

  • Sairanen TR, Lindsberg PJ, Brenner M, Siren AL (1997) Global forebrain ischemia results in differential cellular expression of interleukin-1beta (IL-1beta) and its receptor at mRNA and protein level. J Cereb Blood Flow Metab 17:1107–1120

    PubMed  CAS  Google Scholar 

  • Saivin S, Houin G (1988) Clinical pharmacokinetics of doxycycline and minocycline. Clin Pharmacokinet 15:355–366

    PubMed  CAS  Google Scholar 

  • Salter MG, Fern R (2005) NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167–1171

    PubMed  CAS  Google Scholar 

  • Sanchez-Gomez MV, Matute C (1999) AMPA and kainate receptors each mediate excitotoxicity in oligodendroglial cultures. Neurobiol Dis 6:475–485

    PubMed  CAS  Google Scholar 

  • Sanchez-Gomez MV, Alberdi E, Ibarretxe G, Torre I, Matute C (2003) Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 23:9519–9528

    PubMed  CAS  Google Scholar 

  • Schwedenberg TH (1959) Leukoencephalopathy following carbon monoxide asphyxia. J Neuropathol Exp Neurol 18:597–608

    PubMed  CAS  Google Scholar 

  • Sekeljic V, Bataveljic D, Stamenkovic S, Ulamek M, Jablonski M, Radenovic L, Pluta R, Andjus PR (2012) Cellular markers of neuroinflammation and neurogenesis after ischemic brain injury in the long-term survival rat model. Brain Struct Funct 217:411–420

    PubMed  CAS  Google Scholar 

  • Sharma HS, Miclescu A, Wiklund L (2011) Cardiac arrest-induced regional blood–brain barrier breakdown, edema formation and brain pathology: a light and electron microscopic study on a new model for neurodegeneration and neuroprotection in porcine brain. J Neural Transm 118:87–114

    PubMed  Google Scholar 

  • Sheng H, Laskowitz DT, Pearlstein RD, Warner DS (1999) Characterization of a recovery global cerebral ischemia model in the mouse. J Neurosci Methods 88:103–109

    PubMed  CAS  Google Scholar 

  • Shimada N, Graf R, Rosner G, Heiss WD (1993) Ischemia-induced accumulation of extracellular amino acids in cerebral cortex, white matter, and cerebrospinal fluid. J Neurochem 60:66–71

    PubMed  CAS  Google Scholar 

  • Small DL, Buchan AM (2000) Animal models. Br Med Bull 56:307–317

    PubMed  CAS  Google Scholar 

  • Stevens B, Porta S, Haak LL, Gallo V, Fields RD (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36:855–868

    PubMed  CAS  Google Scholar 

  • Stolp HB, Ek CJ, Johansson PA, Dziegielewska KM, Potter AM, Habgood MD, Saunders NR (2007) Effect of minocycline on inflammation-induced damage to the blood–brain barrier and white matter during development. Eur J Neurosci 26:3465–3474

    PubMed  CAS  Google Scholar 

  • Sugawa M, Sakurai Y, Ishikawa-Ieda Y, Suzuki H, Asou H (2002) Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci Res 44:391–403

    PubMed  CAS  Google Scholar 

  • Takahashi JL, Giuliani F, Power C, Imai Y, Yong VW (2003) Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann Neurol 53:588–595

    PubMed  CAS  Google Scholar 

  • Talos DM, Follett PL, Folkerth RD, Fishman RE, Trachtenberg FL, Volpe JJ, Jensen FE (2006a) Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 497:61–77

    PubMed  CAS  Google Scholar 

  • Talos DM, Fishman RE, Park H, Folkerth RD, Follett PL, Volpe JJ, Jensen FE (2006b) Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J Comp Neurol 497:42–60

    PubMed  CAS  Google Scholar 

  • Thorburne SK, Juurlink BH (1996) Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J Neurochem 67:1014–1022

    PubMed  CAS  Google Scholar 

  • Triulzi F, Parazzini C, Righini A (2006) Patterns of damage in the mature neonatal brain. Pediatr Radiol 36:608–620

    PubMed  Google Scholar 

  • van der Kooij MA, Groenendaal F, Kavelaars A, Heijnen CJ, van Bel F (2008) Neuroprotective properties and mechanisms of erythropoietin in in vitro and in vivo experimental models for hypoxia/ischemia. Brain Res Rev 59:22–33

    PubMed  Google Scholar 

  • von Euler M, Bendel O, Bueters T, Sandin J, von Euler G (2006) Profound but transient deficits in learning and memory after global ischemia using a novel water maze test. Behav Brain Res 166:204–210

    Google Scholar 

  • Walker EJ, Rosenberg GA (2009) TIMP-3 and MMP-3 contribute to delayed inflammation and hippocampal neuronal death following global ischemia. Exp Neurol 216:122–131

    PubMed  CAS  Google Scholar 

  • Walker EJ, Rosenberg GA (2010) Divergent role for MMP-2 in myelin breakdown and oligodendrocyte death following transient global ischemia. J Neurosci Res 88:764–773

    PubMed  CAS  Google Scholar 

  • Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med 10:821–827

    PubMed  CAS  Google Scholar 

  • Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184:53–68

    PubMed  CAS  Google Scholar 

  • Wang J, Jin H, Hua Y, Keep RF, Xi G (2012) Role of protease-activated receptor-1 in brain injury after experimental global cerebral ischemia. Stroke 43:2476–2482

    PubMed  CAS  Google Scholar 

  • Wellons JC 3rd, Sheng H, Laskowitz DT, Burkhard Mackensen G, Pearlstein RD, Warner DS (2000) A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Res 868:14–21

    PubMed  CAS  Google Scholar 

  • Wojcik-Stanaszek L, Sypecka J, Szymczak P, Ziemka-Nalecz M, Khrestchatisky M, Rivera S, Zalewska T (2011) The potential role of metalloproteinases in neurogenesis in the gerbil hippocampus following global forebrain ischemia. PloS one 6:e22465

    PubMed  CAS  Google Scholar 

  • Wu CY, Hsieh HL, Jou MJ, Yang CM (2004) Involvement of p42/p44 MAPK, p38 MAPK, JNK and nuclear factor-kappa B in interleukin-1beta-induced matrix metalloproteinase-9 expression in rat brain astrocytes. J Neurochem 90:1477–1488

    PubMed  CAS  Google Scholar 

  • Wu O, Sorensen AG, Benner T, Singhal AB, Furie KL, Greer DM (2009) Comatose patients with cardiac arrest: predicting clinical outcome with diffusion-weighted MR imaging. Radiology 252:173–181

    PubMed  Google Scholar 

  • Yamashima T, Tonchev AB, Tsukada T, Saido TC, Imajoh-Ohmi S, Momoi T, Kominami E (2003) Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 13:791–800

    PubMed  CAS  Google Scholar 

  • Yonekura I, Kawahara N, Nakatomi H, Furuya K, Kirino T (2004) A model of global cerebral ischemia in C57 BL/6 mice. J Cereb Blood Flow Metab 24:151–158

    PubMed  Google Scholar 

  • Yoshioka H, Niizuma K, Katsu M, Sakata H, Okami N, Chan PH (2011) Consistent injury to medium spiny neurons and white matter in the mouse striatum after prolonged transient global cerebral ischemia. J Neurotrauma 28:649–660

    PubMed  Google Scholar 

  • Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 95:15769–15774

    PubMed  CAS  Google Scholar 

  • Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A 96:13496–13500

    PubMed  CAS  Google Scholar 

  • Zhang K, Sejnowski TJ (2000) A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci U S A 97:5621–5626

    PubMed  CAS  Google Scholar 

  • Zhang W, Wang B, Zhou S, Qiu Y (2012) The effect of ischemic post-conditioning on hippocampal cell apoptosis following global brain ischemia in rats. J Clin Neurosci 19:570–573

    PubMed  Google Scholar 

  • Zhao H (2009) Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29:873–885

    PubMed  CAS  Google Scholar 

  • Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, Wang X, Lo EH (2006) Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med 12:441–445

    PubMed  CAS  Google Scholar 

  • Zola-Morgan S, Squire LR, Rempel NL, Clower RP, Amaral DG (1992) Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci 12:2582–2596

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

  Supported in part by the National Institutes of Health, the American Heart Association, and the Deane Institute. Materials in this chapter have been extensively drawn from previously published reviews from the authors including Arai and Lo, Biol Pharm Bull 2009, and Arai and Lo, Exp Transl Stroke Med 2009.

Author information

Authors and Affiliations

  1. Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital/Harvard Medical School, 149 Thirteenth Street, MGH-CNY149, Room 2401, Charlestown, MA, 02129, USA

    Ji Hae Seo, Kazuhide Hayakawa, Nobukazu Miyamoto, Takakuni Maki, Loc-Duyen D. Pham, Eng H. Lo & Ken Arai Ph.D.

Authors
  1. Ji Hae Seo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuhide Hayakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nobukazu Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takakuni Maki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loc-Duyen D. Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eng H. Lo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ken Arai Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ken Arai Ph.D. .

Editor information

Editors and Affiliations

  1. Cleveland Clinic Lerner Research Institute, Cleveland, Ohio, USA

    Selva Baltan

  2. Department of Neurology, University of California, Los Angeles, Los Angeles, California, USA

    S. Thomas Carmichael

  3. Departamento de Neurociencias, Achucarro Basque Centger for Neuroscience, University del Pais Vasco (UPV/EHU), and Centro de, Investigación Biomédica en Red en Enfermedades Neurodegenerativas (CIBERNED), Leioa, Spain

    Carlos Matute

  4. University of Michigan Dept. Neurosurgery, Ann Arbor, Michigan, USA

    Guohua Xi

  5. Dept. Pharmacology Dept. Neurosurgery, Loma Linda University Dept. Physiology, Loma Linda, California, USA

    John H Zhang

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Seo, J.H. et al. (2014). Experimental Global Ischemia and White Matter Injury. In: Baltan, S., Carmichael, S., Matute, C., Xi, G., Zhang, J. (eds) White Matter Injury in Stroke and CNS Disease. Springer Series in Translational Stroke Research, vol 4. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9123-1_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-9123-1_10

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4614-9122-4

  • Online ISBN: 978-1-4614-9123-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation