Top

Published in:

01-08-2010 | Movement Disorders-Review Article

Inflammation processes in perinatal brain damage

Authors: Vincent Degos, Géraldine Favrais, Angela M. Kaindl, Stéphane Peineau, Anne Marie Guerrot, Catherine Verney, Pierre Gressens

Published in: Journal of Neural Transmission | Issue 8/2010

Abstract

Once viewed as an isolated, immune-privileged organ, the central nervous system has undergone a conceptual change. Neuroinflammation has moved into the focus of research work regarding pathomechanisms underlying perinatal brain damage. In this review, we provide an overview of current concepts regarding perinatal brain damage and the role of inflammation in the disease pathomechanism.

Adén U, Favrais G, Plaisant F, Winerdal M, Felderhoff-Mueser UJL, Lelievre V, Gressens P (2010) Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/anti-inflammatory imbalance: key role of TNF-α pathway and protection by etanercept. Brain Behav Immun (in press)

Anthony DC, Bolton SJ, Fearn S, Perry VH (1997) Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 120(Pt 3):435–444CrossRefPubMed

Anthony D, Dempster R, Fearn S, Clements J, Wells G, Perry VH, Walker K (1998) CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood-brain barrier breakdown. Curr Biol 8:923–926CrossRefPubMed

Arvin KL, Han BH, Du Y, Lin SZ, Paul SM, Holtzman DM (2002) Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 52:54–61CrossRefPubMed

Bartha AI, Foster-Barber A, Miller SP, Vigneron DB, Glidden DV, Barkovich AJ, Ferriero DM (2004) Neonatal encephalopathy: association of cytokines with MR spectroscopy and outcome. Pediatr Res 56:960–966CrossRefPubMed

Baud O, Daire JL, Dalmaz Y, Fontaine RH, Krueger RC, Sebag G, Evrard P, Gressens P, Verney C (2004) Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol 14:1–10CrossRefPubMed

Biran V, Cochois V, Karroubi A, Arrang JM, Charriaut-Marlangue C, Heron A (2008) Stroke induces histamine accumulation and mast cell degranulation in the neonatal rat brain. Brain Pathol 18:1–9CrossRefPubMed

Dammann O, Leviton A (1997) Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42:1–8CrossRefPubMed

Dammann O, Leviton A (2007) Perinatal brain damage causation. Dev Neurosci 29:280–288CrossRefPubMed

Dammann O, Kuban KC, Leviton A (2002) Perinatal infection, fetal inflammatory response, white matter damage, and cognitive limitations in children born preterm. Ment Retard Dev Disabil Res Rev 8:46–50CrossRefPubMed

Debillon T, Gras-Leguen C, Verielle V, Winer N, Caillon J, Roze JC, Gressens P (2000) Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr Res 47:736–742CrossRefPubMed

Degos V, Loron G, Mantz J, Gressens P (2008) Neuroprotective strategies for the neonatal brain. Anesth Analg 106:1670–1680CrossRefPubMed

Denker SP, Ji S, Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2007) Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 100:893–904CrossRefPubMed

Derrick M, Luo NL, Bregman JC, Jilling T, Ji X, Fisher K, Gladson CL, Beardsley DJ, Murdoch G, Back SA, Tan S (2004) Preterm fetal hypoxia–ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J Neurosci 24:24–34CrossRefPubMed

Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2006) Aminoguanidine inhibits caspase-3 and calpain activation without affecting microglial activation following neonatal transient cerebral ischemia. J Neurochem 96:1467–1479CrossRefPubMed

Dommergues MA, Patkai J, Renauld JC, Evrard P, Gressens P (2000) Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium. Ann Neurol 47:54–63CrossRefPubMed

Dommergues MA, Plaisant F, Verney C, Gressens P (2003) Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection. Neuroscience 121:619–628CrossRefPubMed

Doverhag C, Keller M, Karlsson A, Hedtjarn M, Nilsson U, Kapeller E, Sarkozy G, Klimaschewski L, Humpel C, Hagberg H, Simbruner G, Gressens P, Savman K (2008) Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiol Dis 31:133–144CrossRefPubMed

Ek CJ, Habgood MD, Dziegielewska KM, Potter A, Saunders NR (2001) Permeability and route of entry for lipid-insoluble molecules across brain barriers in developing Monodelphis domestica. J Physiol 536(Pt 3):841–853CrossRefPubMed

Ek CJ, Dziegielewska KM, Stolp H, Saunders NR (2006) Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 496(1):13–26CrossRefPubMed

Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H (2001) Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 13:1101–1106CrossRefPubMed

Eklind S, Mallard C, Arvidsson P, Hagberg H (2005) Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 58:112–116CrossRefPubMed

Engelhardt B (2003) Development of the blood-brain barrier. Cell Tissue Res 314:119–129CrossRefPubMed

Faustino J, Liu B, Lee S, Derugin N, Wendland MF, Vexler ZS (2009) Blockade of endogenous cytokine-induced neutrophil chemoattractant protein 1 exacerbates injury after neonatal stroke Stroke meeting. San Diego

Favrais G, Schwendimann L, Gressens P, Lelievre V (2007) Cyclooxygenase-2 mediates the sensitizing effects of systemic IL-1-beta on excitotoxic brain lesions in newborn mice. Neurobiol Dis 25:496–505CrossRefPubMed

Feldhaus B, Dietzel ID, Heumann R, Berger R (2004) Effects of interferon-gamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors. J Soc Gynecol Investig 11:89–96CrossRefPubMed

Follett PL, Rosenberg PA, Volpe JJ, Jensen FE (2000) NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235–9241PubMed

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 24:4412–4420CrossRefPubMed

Fontaine RH, Cases O, Lelievre V, Mesples B, Renauld JC, Loron G, Degos V, Dournaud P, Baud O, Gressens P (2008) IL-9/IL-9 receptor signaling selectively protects cortical neurons against developmental apoptosis. Cell Death Differ 15:1542–1552CrossRefPubMed

Foster-Barber A, Ferriero DM (2002) Neonatal encephalopathy in the term infant: neuroimaging and inflammatory cytokines. Ment Retard Dev Disabil Res Rev 8:20–24CrossRefPubMed

Fox C, Dingman A, Derugin N, Wendland MF, Manabat C, Ji S, Ferriero DM, Vexler ZS (2005) Minocycline confers early but transient protection in the immature brain following focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 25:1138–1149CrossRefPubMed

Galasso JM, Miller MJ, Cowell RM, Harrison JK, Warren JS, Silverstein FS (2000) Acute excitotoxic injury induces expression of monocyte chemoattractant protein-1 and its receptor, CCR2, in neonatal rat brain. Exp Neurol 165:295–305CrossRefPubMed

Ghersi-Egea JF, Strazielle N, Murat A, Jouvet A, Buénerd A, Belin MF (2006) Brain protection at the blood-cerebrospinal fluid interface involves a glutathione-dependent metabolic barrier mechanism. J Cereb Blood Flow Metab 26(9):1165–1175PubMed

Girard S, Kadhim H, Larouche A, Roy M, Gobeil F, Sebire G (2008) Pro-inflammatory disequilibrium of the IL-1 beta/IL-1ra ratio in an experimental model of perinatal brain damages induced by lipopolysaccharide and hypoxia–ischemia. Cytokine 43:54–62CrossRefPubMed

Gressens P, Marret S, Hill JM, Brenneman DE, Gozes I, Fridkin M, Evrard P (1997) Vasoactive intestinal peptide prevents excitotoxic cell death in the murine developing brain. J Clin Invest 100:390–397CrossRefPubMed

Gressens P, Rogido M, Paindaveine B, Sola A (2002) The impact of neonatal intensive care practices on the developing brain. J Pediatr 140:646–653CrossRefPubMed

Grether JK, Nelson KB (1997) Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278:207–211CrossRefPubMed

Hagberg H, Mallard C (2005) Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 18:117–123CrossRefPubMed

Hagberg H, Gilland E, Bona E, Hanson LA, Hahin-Zoric M, Blennow M, Holst M, McRae A, Soder O (1996) Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia–ischemia in neonatal rats. Pediatr Res 40:603–609CrossRefPubMed

Hagberg H, Peebles D, Mallard C (2002) Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 8:30–38CrossRefPubMed

Harding DR, Dhamrait S, Whitelaw A, Humphries SE, Marlow N, Montgomery HE (2004) Does interleukin-6 genotype influence cerebral injury or developmental progress after preterm birth? Pediatrics 114:941–947CrossRefPubMed

Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, Volpe JJ, Kinney HC (2003) Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 62:441–450PubMed

Hedtjarn M, Leverin AL, Eriksson K, Blomgren K, Mallard C, Hagberg H (2002) Interleukin-18 involvement in hypoxic-ischemic brain injury. J Neurosci 22:5910–5919PubMed

Hedtjarn M, Mallard C, Iwakura Y, Hagberg H (2005) Combined deficiency of IL-1beta18, but not IL-1alphabeta, reduces susceptibility to hypoxia–ischemia in the immature brain. Dev Neurosci 27:143–148CrossRefPubMed

Himmelmann K, Hagberg G, Beckung E, Hagberg B, Uvebrant P (2005) The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth-year period 1995–1998. Acta Paediatr 94:287–294PubMed

Inder T, Mocatta T, Darlow B, Spencer C, Volpe JJ, Winterbourn C (2002) Elevated free radical products in the cerebrospinal fluid of VLBW infants with cerebral white matter injury. Pediatr Res 52:213–218PubMed

Ivacko JA, Sun R, Silverstein FS (1996) Hypoxic-ischemic brain injury induces an acute microglial reaction in perinatal rats. Pediatr Res 39:39–47CrossRefPubMed

Jin Y, Silverman AJ, Vannucci SJ (2007) Mast cell stabilization limits hypoxic-ischemic brain damage in the immature rat. Dev Neurosci 29:373–384CrossRefPubMed

Johnson DL, Getson P, Shaer C, O’Donnell R (1987) Intraventricular hemorrhage in the newborn beagle puppy. A limited model of intraventricular hemorrhage in the premature infant. Pediatr Neurosci 13:78–83CrossRefPubMed

Kirton A, deVeber G (2009) Advances in perinatal ischemic stroke. Pediatr Neurol 40:205–214CrossRefPubMed

Kniesel U, Risau W, Wolburg H (1996) Development of blood-brain barrier tight junctions in the rat cortex. Brain Res Dev Brain Res 96:229–240CrossRefPubMed

Laudenbach V, Calo G, Guerrini R, Lamboley G, Benoist JF, Evrard P, Gressens P (2001) Nociceptin/orphanin FQ exacerbates excitotoxic white-matter lesions in the murine neonatal brain. J Clin Invest 107:457–466CrossRefPubMed

Leonardo CC, Eakin AK, Ajmo JM, Collier LA, Pennypacker KR, Strongin AY, Gottschall PE (2008) Delayed administration of a matrix metalloproteinase inhibitor limits progressive brain injury after hypoxia–ischemia in the neonatal rat. J Neuroinflammation 5:34CrossRefPubMed

Lim HB, Smith M (2007) Systemic complications after head injury: a clinical review. Anaesthesia 62:474–482CrossRefPubMed

Loeliger M, Watson CS, Reynolds JD, Penning DH, Harding R, Bocking AD, Rees SM (2003) Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep. Neuroscience 116:705–714CrossRefPubMed

Lu J, Goh SJ, Tng PY, Deng YY, Ling EA, Moochhala S (2009) Systemic inflammatory response following acute traumatic brain injury. Front Biosci 14:3795–3813CrossRefPubMed

Malaeb S, Dammann O (2009) Fetal inflammatory response and brain injury in the preterm newborn. J Child Neurol 24:1119–1126CrossRefPubMed

Mallard C, Welin AK, Peebles D, Hagberg H, Kjellmer I (2003) White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 28:215–223CrossRefPubMed

McColl BW, Allan SM, Rothwell NJ (2009) Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158:1049–1061CrossRefPubMed

McRae A, Gilland E, Bona E, Hagberg H (1995) Microglia activation after neonatal hypoxic-ischemia. Brain Res Dev Brain Res 84:245–252CrossRefPubMed

Mesples B, Plaisant F, Gressens P (2003) Effects of interleukin-10 on neonatal excitotoxic brain lesions in mice. Brain Res Dev Brain Res 141:25–32CrossRefPubMed

Mesples B, Plaisant F, Fontaine RH, Gressens P (2005) Pathophysiology of neonatal brain lesions: lessons from animal models of excitotoxicity. Acta Paediatr 94:185–190CrossRefPubMed

Miller RJ, Tran PB (2005) Chemokinetics. Neuron 47:621–623CrossRefPubMed

Monier A, Evrard P, Gressens P, Verney C (2006) Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J Comp Neurol 499:565–582CrossRefPubMed

Monier A, Adle-Biassette H, Delezoide AL, Evrard P, Gressens P, Verney C (2007) Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J Neuropathol Exp Neurol 66:372–382CrossRefPubMed

Nelson KB, Chang T (2008) Is cerebral palsy preventable? Curr Opin Neurol 21:129–135CrossRefPubMed

Nelson KB, Grether JK (1999) Causes of cerebral palsy. Curr Opin Pediatr 11:487–491CrossRefPubMed

Nelson KB, Willoughby RE (2000) Infection, inflammation and the risk of cerebral palsy. Curr Opin Neurol 13:133–139CrossRefPubMed

Nijboer CH, Kavelaars A, Vroon A, Groenendaal F, van Bel F, Heijnen CJ (2008) Low endogenous G-protein-coupled receptor kinase 2 sensitizes the immature brain to hypoxia–ischemia-induced gray and white matter damage. J Neurosci 28:3324–3332CrossRefPubMed

Normann E, Lacaze-Masmonteil T, Eaton F, Schwendimann L, Gressens P, Thebaud B (2009) A novel mouse model of ureaplasma-induced perinatal inflammation: effects on lung and brain injury. Pediatr Res 65:430–436CrossRefPubMed

Olivier P, Baud O, Evrard P, Gressens P, Verney C (2005) Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 64:998–1006CrossRefPubMed

Pang Y, Campbell L, Zheng B, Fan L, Cai Z, Rhodes P (2010) Lipopolysaccharide-activated microglia induce death of oligodendrocyte progenitor cells and impede their development. Neuroscience 166(2):464–475CrossRefPubMed

Patkai J, Mesples B, Dommergues MA, Fromont G, Thornton EM, Renauld JC, Evrard P, Gressens P (2001) Deleterious effects of IL-9-activated mast cells and neuroprotection by antihistamine drugs in the developing mouse brain. Pediatr Res 50:222–230CrossRefPubMed

Plaisant F, Dommergues MA, Spedding M, Cecchelli R, Brillault J, Kato G, Munoz C, Gressens P (2003) Neuroprotective properties of tianeptine: interactions with cytokines. Neuropharmacology 44:801–809CrossRefPubMed

Rezaie P, Male D (1999) Colonisation of the developing human brain and spinal cord by microglia: a review. Microsc Res Tech 45:359–382CrossRefPubMed

Rezaie P, Patel K, Male DK (1999) Microglia in the human fetal spinal cord—patterns of distribution, morphology and phenotype. Brain Res Dev Brain Res 115:71–81CrossRefPubMed

Robertson CM, Watt MJ, Yasui Y (2007) Changes in the prevalence of cerebral palsy for children born very prematurely within a population-based program over 30 years. JAMA 297:2733–2740CrossRefPubMed

Rousset CI, Chalon S, Cantagrel S, Bodard S, Andres C, Gressens P, Saliba E (2006) Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 59:428–433CrossRefPubMed

Strazielle N, Ghersi-Egea JF (2000) Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol 59(7):561–574PubMed

Streit WJ, Kreutzberg GW (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248–263CrossRefPubMed

Svedin P, Hagberg H, Savman K, Zhu C, Mallard C (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia–ischemia. J Neurosci 27:1511–1518CrossRefPubMed

Tahraoui SL, Marret S, Bodenant C, Leroux P, Dommergues MA, Evrard P, Gressens P (2001) Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 11:56–71CrossRefPubMed

Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580–2588PubMed

van den Tweel ER, Nijboer C, Kavelaars A, Heijnen CJ, Groenendaal F, van Bel F (2005) Expression of nitric oxide synthase isoforms and nitrotyrosine formation after hypoxia–ischemia in the neonatal rat brain. J Neuroimmunol 167:64–71CrossRefPubMed

Vela JM, Molina-Holgado E, Arevalo-Martin A, Almazan G, Guaza C (2002) Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol Cell Neurosci 20:489–502CrossRefPubMed

Vincer MJ, Allen AC, Joseph KS, Stinson DA, Scott H, Wood E (2006) Increasing prevalence of cerebral palsy among very preterm infants: a population-based study. Pediatrics 118:e1621–e1626CrossRefPubMed

Volpe JJ (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50:553–562CrossRefPubMed

Volpe JJ (2009) The encephalopathy of prematurity-brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 16:167–178CrossRefPubMed

Wilson-Costello D, Friedman H, Minich N, Fanaroff AA, Hack M (2005) Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 115:997–1003CrossRefPubMed

Wilson-Costello D, Friedman H, Minich N, Siner B, Taylor G, Schluchter M, Hack M (2007) Improved neurodevelopmental outcomes for extremely low birth weight infants in 2000–2002. Pediatrics 119:37–45CrossRefPubMed

Title: Inflammation processes in perinatal brain damage
Authors: Vincent Degos
Géraldine Favrais
Angela M. Kaindl
Stéphane Peineau
Anne Marie Guerrot
Catherine Verney
Pierre Gressens
Publication date: 01-08-2010
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue 8/2010
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-010-0411-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Inflammation processes in perinatal brain damage

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2010

Neuroinflammatory processes in Alzheimer’s disease

Macrophages in Alzheimer’s disease: the blood-borne identity

Editorial

Neuroinflammation is a key player in Parkinson’s disease and a prime target for therapy

The role of microglia in amyloid clearance from the AD brain

Inflammation in neuroviral diseases