Skip to main content
SpringerLink
Log in
Book cover

Perinatal Programming of Neurodevelopment pp 169–198Cite as

Short- and Long-Term Consequences of Perinatal Asphyxia: Looking for Neuroprotective Strategies

  • Chapter
  • First Online:

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 10))

Abstract

Perinatal asphyxia constitutes a prototype of obstetric complications occurring when pulmonary oxygenation is delayed or interrupted. A primary insult is first produced by the length of the time without oxygenation, leading to hypoxia/ischemia and death if oxygenation is not promptly established. A second insult is produced by re-oxygenation, eliciting a cascade of biochemical events for restoring function, implying, however, improper homeostasis. The effects observed long after perinatal asphyxia can be explained by over-expression of sentinel proteins, such as poly(ADP-ribose) polymerase-1 (PARP-1), competing for oxidised nicotinamide adenine dinucleotide (NAD+) during re-oxygenation. Asphyxia also induces transcriptional activation of pro-inflammatory factors, including nuclear factor κB (NFκB) and its subunit p65, whose translocation to the nucleus is significantly increased in brain tissue from asphyxia-exposed animals, in tandem with PARP-1 overactivation, leading to the idea that sentinel protein inhibition constitutes a suitable therapeutic strategy. It is proposed that PARP-1 inhibition also down-regulates the expression of pro-inflammatory cytokines.

Nicotinamide is a suitable PARP-1 inhibitor, whose effects have been studied in an experimental model of global perinatal asphyxia in rats, inducing the insult by immersing rat foetuses into a water bath for various periods of time. Following asphyxia, the pups are delivered, immediately treated, or given to surrogate dams for nursing, pending further experiments. Systemic administration of nicotinamide 1 h after the insult inhibited PARP-1 overactivity in peripheral and brain tissue, preventing several of the long-term consequences elicited by perinatal asphyxia, supporting the idea that it constitutes a lead for exploring compounds with similar or better pharmacological profiles.

This is a preview of subscription content, 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   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
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

Learn about institutional subscriptions

Abbreviations

AIF:

Apoptosis-inducing factor

ADP:

Adenosine diphosphate

ATP:

Adenosine triphosphate

ATPase:

ATP polymerase

BAD:

Bcl-2-associated death promoter

BAX:

Bcl-2-associated X protein

BBB:

Blood–brain barrier

bFGF:

Basic fibroblast growth factor

BCL-2:

B-cell lymphoma-2

CA:

Cornus Ammonis (CA1, CA2, CA3)

CAM:

Cell adhesion molecule

CNS:

Central nervous system

CS:

Caesarean-delivered saline-treated animal

COX-2:

Cyclooxygenase-2

DG:

Dentate gyrus of the hippocampus

DNA:

Deoxyribonucleic acid

EAAC1:

Excitatory amino acid carrier 1

Elk1:

ETS domain-containing protein1

ERCC2:

Excision repair cross-complementing rodent repair group 2

ERK:

Extracellular signal-regulated kinases

FGFR:

bFGF receptors

FLRT3:

Leucine-rich repeat transmembrane protein

HIF:

Hypoxia-inducible factor

IκB:

Inhibitor of kappa B protein

iNOS:

Inducible NOS

IL-1β/-6:

Interleukin-1β/-6

IFG-1:

Insulin-like growth factor 1

ICAM-1:

TNFα adhesion molecule-1

L1:

L1CAM

LPS:

Lipopolysaccharides

MAP-2:

Microtubule-associated protein-2

MAPK:

Mitogen-activated protein kinase

NAD+ :

Oxidised nicotinamide adenine dinucleotide

NADH:

Reduced nicotinamide adenine dinucleotide

NFκB:

Nuclear factor κB

Ngn2:

Neurogenin-2

NgR:

Nogo receptor

NMDA:

N-methyl-D-aspartate

NOS:

Nitric oxide synthase

nNOS:

Neuronal NOS

p65/p50:

Protein subunits of 65/50k Dalton MW

P1:

Postnatal day 1

PARP-1:

Poly(ADP-ribose) polymerase-1

PIP2:

Phosphatidylinositol-4,5-bisphosphate

PKC:

Protein kinase C

PSD95:

Postsynaptic density protein 95

RhoA:

Ras homolog gene family, member A, small GTPase protein

ROS:

Reactive oxygen species

Sef:

Similar expression fgf gene

SIRT:

Sirtuin

SEM:

Standard error of the means

Spry:

Sprouty

SRY:

Sex-determining region Y

SVZ:

Subventricular zone

TH:

Tyrosine hydroxylase

Thy-1:

Thymocyte differentiation antigen 1

TNF-α:

Tumour necrosis factor-alpha cytokine

TUNEL:

TdT-mediated dUTP nick-end labelling

VTA:

Ventral tegmental area

XRCC1:

X-ray cross-complementing factor 1

References

  • Alano CC, Kauppinen TM, Valls AV, Swanson RA (2006) Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations. Proc Natl Acad Sci U S A 103:9685–9690

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allende-Castro C, Espina-Marchant P, Bustamante D, Rojas-Mancilla E, Neira T, Gutierrez-Hernandez MA, Esmar D, Valdes JL, Morales P, Gebicke-Haerter PJ, Herrera-Marschitz M (2012) Further studies on the hypothesis of PARP-1 inhibition as a strategy for lessening the long-term effects produced by perinatal asphyxia: effects of nicotinamide and theophylline on PARP-1 activity in brain and peripheral tissue. Neurotox Res 22:79–90

    CAS  PubMed  Google Scholar 

  • Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683–686

    CAS  PubMed  Google Scholar 

  • Amé J-C, Spenlehauer C, de Murcia G (2004) The PARP superfamily. Bioessays 26:882–893

    PubMed  Google Scholar 

  • Andersson K, Bjelke B, Bolme P, Ögren SO (1992) Asphyxia-induced lesion of the rat hippocampus (CA1, CA3) and the nigro-striatal dopamine system. In: J Gross (ed) Hypoxia and ischemia. CNS, vol 41. Wissenschafliche Publikationen der Humboldt-Universität zu Berlin, B. Medizin, Berlin, pp 71–76

    Google Scholar 

  • Andersson K, Blum M, Chen Y, Eneroth P, Gross J, Herrera-Marschitz M, Bjelke B, Bolme P, Diaz R, Jamison L, Loidl F, Ungethüm U, Åström G, Ögren SO (1995) Perinatal asphyxia increases bFGF mRNA levels and DA cell body number in mesencephalon of rats. Neuroreport 6:375–378

    CAS  PubMed  Google Scholar 

  • Antonopoulos J, Dori I, Dinopoulos A, Chiotelli M, Parnavelas JG (2002) Postnatal development of the dopaminergic system of the striatum of the rat. Neuroscience 110:245–256

    CAS  PubMed  Google Scholar 

  • Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 9:963–970

    Google Scholar 

  • 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 52:54–61

    CAS  PubMed  Google Scholar 

  • Avalos AM, Labra CV, Quest AF, Leyton L (2002) Signaling triggered by Thy-1 interaction with b3 integrin on astrocytes is an essential step towards unravelling neuronal Thy-1 function. Biol Res 35:231–238

    CAS  PubMed  Google Scholar 

  • Avalos AM, Arthur WT, Schneider P, Quest A F, Burridge K, Leyton L (2004) Aggregation of integrins and RhoA activation are required for Thy-1-induced morphological changes in astrocytes. J Biol Chem 279:39139–39145

    CAS  PubMed  Google Scholar 

  • Avalos AM, Valdivia A, Tapia JC, Muñoz N, Lavandero S, Chiong M, Burridge K, Schneider P, Quest AFG, Leyton L (2009) Neuronal Thy-1 induces adhesion by aVb3 integrin and Syndecan-4-dependent activation of PKCa and RhoA. J Cell Sci 122:3462–3471

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barkovich AJ (2006) MR imagining of the neonatal. Neuroimaging Clin N Am 16:117–135

    CAS  PubMed  Google Scholar 

  • Barlow JZ, Huntley GW (2000) Developmentally regulated expression of Thy-1 in structures of the mouse sensory-motor system. J Comp Neurol 421:215–233

    CAS  PubMed  Google Scholar 

  • Bartley J, Soltau T, Wimborne H, Kim S, Martin-Sttudard A, Hess D, Hill W, Waller J, Carrol J (2005) BrdU-positive cells in the neonatal mouse hippocampus following hypoxic-ischemic brain injury. BMC Neurosci 6:15

    PubMed Central  PubMed  Google Scholar 

  • Basovich SN (2010) The role of hypoxia in mental development and in the treatment of mental disorders. Biosci Trends 4:288–296

    PubMed  Google Scholar 

  • Bédard A, Gravel C, Parent A (2006) Chemical characterization of newly generated neurons in the striatum of adult primates. Exp Brain Res 170:501–512

    PubMed  Google Scholar 

  • Berger NA (1985) Poly (ADP-ribose) in the cellular response to DNA damage. Radiat Res 1001:4–15

    Google Scholar 

  • Bjelke B, Andersson K, Ögren SO, Bolme P (1991) Asphyctic lesion: proliferation of tyrosine hydroxylase immunoreactive nerve cell bodies in the rat substantia nigra and functional changes in dopamine transmission. Brain Res 543:1–9

    CAS  PubMed  Google Scholar 

  • Boksa P, Krishnamurthy A, Brooks W (1995) Effects of a period of asphyxia during birth on spatial learning in the rat. Pediatr Res 37:489–496

    CAS  PubMed  Google Scholar 

  • Bonfocco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apotosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 92:7162–7166

    Google Scholar 

  • Bustamante D, Goiny M, Åström G, Gross J, Andersson K, Herrera-Marschitz M (2003) Nicotinamide prevents the long-term effects of perinatal asphyxia on basal ganglia monoamine systems in the rat. Exp Brain Res 148:227–232

    CAS  PubMed  Google Scholar 

  • Bustamante D, Morales P, Torres-Pereyra J, Goiny M, Herrera-Marschitz M (2007) Nicotinamide prevents the effect of perinatal asphyxia on dopamine release evaluated with in vivo microdialysis three months after birth. Exp Brain Res 177:358–369

    CAS  PubMed  Google Scholar 

  • Calabresi P, Centonze D, Bernardi G (2000) Cellular factors controlling neuronal vulnerability in the brain: a lesson from the striatum. Neurology 55:1249–1255

    CAS  PubMed  Google Scholar 

  • Cannon M, Jones PB, Murray RM (2002) Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry 159:1080–1092

    PubMed  Google Scholar 

  • Chen Y, Ögren SO, Bjelke B, Bolme P, Eneroth P, Gross J, Loidl F, Herrera-Marschitz M, Andersson K (1995) Nicotine treatment counteracts perinatal asphyxia-induced changes in the mesostriatal/limbic dopamine systems and in motor behaviour in the four-week old male rat. Neuroscience 68:531–538

    CAS  PubMed  Google Scholar 

  • Chen Y, Engidawork E, Loidl F, Dell’Anna E, Gony M, Lubec G, Andersson K, Herrera-Marschitz M (1997a) Short- and long-term effects of perinatal asphyxia on monoamine, amino acids and glycolysis product levels measured in the basal ganglia of the rat. Dev Brain Res 104: 19–30

    CAS  Google Scholar 

  • Chen Y, Herrera-Marschitz M, Bjelke B, Blum M, Gross J, Andersson K (1997b) Perinatal asphyxia-induced changes in rat brain tyrosine-hydroxylase-immunoreactive cell body number: effects of nicotine treatment. Neurosci Lett 221:77–80

    CAS  PubMed  Google Scholar 

  • Chen Y, Hillefors-Berglund M, Herrera-Marschitz M, Bjielke B, Gross J, Andersson K, von Euler G (1997c) Perinatal asphyxia induces long-term changes in dopamine D1, D2, D3 receptor binding in the rat brain. Exp Neurol 146:74–80

    CAS  PubMed  Google Scholar 

  • Cheng Y, Black IB, DiCicco-Bloom E (2002) Hippocampal granule neuron production and population size are regulated by levels of bFGF. Eur J Neurosci 15:3–12

    PubMed  Google Scholar 

  • Chen CH, Wang SM, Yang SH, Jeng CJ (2005) Role of Thy-1 in in vivo and in vitro neural development and regeneration of dorsal root ganglionic neurons. J Cell Biochem 94:684–694

    CAS  PubMed  Google Scholar 

  • Chiappe-Gutierrez M, Kitzmueller E, Labudova O, Fuerst G, Hoeger H, Hardmeier R, Nohl H, Gille L, Lubec B (1998) mRNA levels of the hypoxia inducible factor (HIF-1) and DNA repair genes in perinatal asphyxia of the rat. Life Sci 63:1157–1167

    CAS  PubMed  Google Scholar 

  • Cohen-Armon M (2008) PARP-1 activation in the ERK signalling pathway. Trends Pharmacol Sci 28:556–560

    Google Scholar 

  • Cohen-Armon M, Visochek L, Rozendal D, Kalal A, Geistrikh I, Klein R, Bendetz-Nezer S, Yao Z, Seger R (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25:297–308

    CAS  PubMed  Google Scholar 

  • Collin T, Arvidsson A, Kokaia Z, Lindvall O (2005) Quantitative analysis of the generation of different striatal neuronal subtypes in the adult brain following excitotoxic injury. Exp Neurol 195:71–80

    PubMed  Google Scholar 

  • Cowan F, Rutherford M, Groenendaal F, Eken P, Mercuri E, Bydder GM, Meiners LC, Dubowitz LMS, de Vries LS (2003) Origin and timing of brain lesions in term infants with neonatal encephalopathy. Lancet 361:736–742

    PubMed  Google Scholar 

  • Craig A, Luo NL, Beardsley DJ, Wingate-Pearse N, Walker D, Hohimer AR, Back SA (2003) Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol 181:231–240

    PubMed  Google Scholar 

  • De Angelis E, MacFarlane J, Du JS, Yeo G, Hicks R, Rathjen FG, Kenwrick S, Brummendorf T (1999) Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities. EMBO J 18:4744–4753

    CAS  PubMed Central  PubMed  Google Scholar 

  • De Hann M, Wyatt JS, Vargha-Khadem F, Gadian D, Mishki M (2006) Brain and cognitive behavioural development after asphyxia at term birth. Dev Sci 9:350–358

    Google Scholar 

  • De Louw AJA, De Vente J, Steinbusch HPJ, Gavilanes AWD, Steinbusch HWM, Blanco CE, Troost J, Vles JSH (2002) Apoptosis in the rat spinal cord during postnatal development: the effect of perinatal asphyxia on programmed cell death. Neuroscience 112:751–758

    CAS  PubMed  Google Scholar 

  • De Murcia G, Menissier de Murcia J (1994) Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem Sci 19:172–176

    CAS  PubMed  Google Scholar 

  • Dell’Anna E, Calzolari S, Milinari M, Luvone L, Calimici R (1991) Neonatal anoxia induces transitory hyperactivity, permanent spatial memory deficits and CA1 cell density reduction in the developing rats. Behav Brain Res 45:125–134

    PubMed  Google Scholar 

  • Dell’Anna E, Chen Y, Engidawork E, Andersson K, Lubec G, Luthman J, Herrera-Marschitz M (1995) Short term effects of perinatal asphyxia studied with Fos-immunocytochemistry and in vivo microdialysis in the rat. Exp Neurol 131:279–287

    PubMed  Google Scholar 

  • Dell’Anna E, Chen Y, Engidawork E, Andersson K, Lubec G, Luthman J, Herrera-Marschitz M (1997) Delayed neuronal death following perinatal asphyxia in rat. Exp Brain Res 115:105–115

    PubMed  Google Scholar 

  • Demyanenko GP, Shibata Y, Maness PF (2001) Altered distribution of dopaminergic neurons in the brain of L1 null mice. Brain Res Dev Brain Res 126:21–30

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Dreyer EB, Leifer D, Heng JE, McConnell JE, Gorla M, Levin LA, Barnstable CJ, Lipton, SA (1995) An astrocytic binding site for neuronal Thy-1 and its effects on neurite outgrowth. Proc Natl Acad Sci U S A 92:11195–11199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ducrocq S, Benjelloun N, Plotkine M, Ben-Ari Y, Charriaut-Marlangue C (2000) Poly(ADP-ribose) synthase inhibition reduces ischemic injury and inflammation in neonatal rat brain. J Neurochem 74:2504–2511

    CAS  PubMed  Google Scholar 

  • du Plessis AJ, Volpe JJ (2002) Perinatal brain injury in the preterm and term newborn. Curr Opin Neurol 15:151–157

    PubMed  Google Scholar 

  • Ellenberger T, Tomkinson AE (2008) Eukaryotic DNA ligases: structural and functional insights. Annu Rev Biochem 77:313–338

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Engidawork E, Loidl F, Chen Y, Kohlhauser C, Stoeckler S, Dell’Anna E, Lubec B, Lubec G, Goiny M, Gross J, Andersson K, Herrera-Marschitz M (2001) Comparison between hypothermia and glutamate antagonism treatments on the immediate outcome of perinatal asphyxia. Exp Brain Res 138:375–383

    CAS  PubMed  Google Scholar 

  • Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. I: behavioral data. Behav Brain Res 31:47–59

    CAS  PubMed  Google Scholar 

  • Foster GA (1998) Chemical neuroanatomy of the prenatal rat brain. Oxford University Press, New York

    Google Scholar 

  • Gagne J-P, Isabelle M, Lo KS, Bourassa S, Hendzel MJ, Dawson VL, Daeson TM, Poirier GG (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res 36:6959–6976

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ganat Y, Soni S, Chacon M, Schwartz ML, Vaccarino FM (2002) Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience 112:977–991

    CAS  PubMed  Google Scholar 

  • Geraets L, Moonen HJJ, Wouters EFM, Bast A, Hageman GJ (2006) Caffeine metabolites are inhibitors of the nuclear enzyme poly(ADP-ribose)polymerase-1 at physiological concentrations. Biochem Pharmacol 72:902–910

    CAS  PubMed  Google Scholar 

  • Gill DA, Perry MA, McGuire EP, Perez-Gomez A, Tasker RA (2012) Low-dose neonatal domoic acid causes persistent changes in behavioural and molecular indicator of stress response in rats. Behav Brain Res 230:409–417

    CAS  PubMed  Google Scholar 

  • Girard S, Kadhim H, Roy M, Lavoie K, Brochu ME, Larouche A, Sebire G (2009) Role of perinatal inflammation in cerebral palsy. Pediatr Neurol 40:168–174

    PubMed  Google Scholar 

  • Gitto E, Reiter RJ, Karbownik M, Tan D-X, Gitto P, Barberi S, Barberi I (2002) Causes of oxidative stress in the pre- and perinatal period. Biol Neonate 81:146–157

    CAS  PubMed  Google Scholar 

  • Green A, Prager A, Stoudt PM, Murray D (1992) Relationships between DNA damage and the survival of radiosensitive mutant Chinese hamster cell lines exposed to gamma-radiation. Part 1: intrinsic radiosensitivity. Int J Radiat Biol 61:465–472

    CAS  PubMed  Google Scholar 

  • Gross J, Müller I, Chen Y, Elizalde M, Leclere N, Herrera-Marschitz M, Andersson K (2000) Perinatal asphyxia induces region specific long-term changes in mRNA levels of tyrosine hydroxylase and dopamine D1 and D2 receptors in rat brain. Mol Brain Res 79:110–117

    CAS  PubMed  Google Scholar 

  • Gross J, Andersson K, Chen Y, Müller I, Andreeva N, Herrera-Marschitz M, (2005) Effect of perinatal asphyxia on tyrosine hydroxylase and D2 and D1 dopamine receptor mRNA levels expressed during early postnatal development in rat brain. Mol Brain Res 134:275–281

    CAS  PubMed  Google Scholar 

  • Haddad GG, Jiang C (1993) O2 deprivation in the central nervous system: on the mechanisms of neuronal response, differential sensitivity and injury. Prog Neurobiol 40:277–318

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Han BH, Holtzman DM (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci 20:5775–5781

    CAS  PubMed  Google Scholar 

  • Hassa PO, Hottinger MO (1999) A role of poly(ADP-ribose) polymerase in NF-κB transcriptional activation. Biol Chem 380:953–959

    CAS  PubMed  Google Scholar 

  • Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146–154 (Erratum: rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 415:144)

    Google Scholar 

  • Hermosilla T, Munoz D, Herrera-Molina R, Valdivia A, Munoz N, Nham SU, Schneider P, Burridge K, Quest AF, Leyton L (2008) Direct Thy-1/alphaVbeta3 integrin interaction mediates neuron to astrocyte communication. Biochem Biophys Acta 1783:1111–1120

    CAS  PubMed Central  PubMed  Google Scholar 

  • Herrera-Marschitz M, Loidl CF, Andersson K, Ungerstedt U (1993) Prevention of mortality induced by perinatal asphyxia: hypothermia or glutamate antagonism? Amino Acids 5:413–419

    CAS  PubMed  Google Scholar 

  • Herrera-Marschitz M, Loidl CF, You Z-B, Andersson K, Silveira R, O’Connor WT, Goiny M (1994) Neurocircuitry of the basal ganglia studied by monitoring neurotransmitter release. Effects of intracerebral and perinatal asphyctic lesions. Mol Neurobiol 9:171–182

    CAS  PubMed  Google Scholar 

  • Herrera-Marschitz M, Morales P, Leyton L, Bustamante D, Klawitter V, Espina-Marchant P, Allende C, Lisboa F, Cunich G, Jara-Caviedes A, Neira T, Gutierrez-Hernandez MA, Gonzalez-Lira V, Simola N, Schmitt A, Morelli M, Tasker RA, Gebicke-Haerter PJ (2011) Perinatal asphyxia: current status and approaches towards neuroprotective strategies, focus on sentinel proteins. Neurotox Res 19:603–627

    CAS  PubMed Central  PubMed  Google Scholar 

  • Herrera-Molina R, Frischknecht R, Maldonado H, Seidenbecher CI, Gundelfinger ED, Hetz C, Aylwin ML, Schneider P, Quest AFG, Leyton L (2012) Astrocytic ανβ3 integrin inhibits neurite outgrowth and promotes retraction of neuronal process by clustering Thy-1. PLoS ONE 7(3):e34295

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoeger H, Engelmann M, Bernet G, Seidl R, Bubna-Littitz H, Mpsgoeller W, Lubec B, Lubec G (2000) Long term neurological and behavioral effects of graded perinatal asphyxia in the rat. Life Sci 66:947–962

    CAS  PubMed  Google Scholar 

  • Hoeger H, Engidawork E, Stolzlechner D, Bubna-Littitz H, Lubec B (2006) Long-term effect of moderate and profound hyperthermia on morphology, neurological, cognitive and behavioural functions in a rat model of perinatal asphyxia. Amino Acids 31:385–396

    CAS  PubMed  Google Scholar 

  • Hökfelt T, Ljungdahl Å, Fuxe K, Johansson O (1974) Dopamine nerve terminals in the rat limbic cortex: aspects of the dopamine hypothesis of schizophrenia. Nature 184:177–179

    Google Scholar 

  • Hong SJ, Dawson TM, Dawson VL (2004) Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signalling. Trends Pharmacol Sci 25:259–264

    CAS  PubMed  Google Scholar 

  • Horowitz A, Tkachenko E, Simons M (2002) Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol 157:715–725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ingebretsen OC, Bakken AM, Segadal L, Farstad M (1982) Uric acid determinations: reversed-phase liquid chromatography with ultraviolet detection compared with kinetic and equilibrium adaptations of the uricase method. J Chromatogr 242:119–126

    CAS  PubMed  Google Scholar 

  • Iuvone L, Geloso MC, Dell’Anna E (1996) Changes in open field behavior, spatial memory, and hippocampal parvalbumin immunoreactivity following enrichment in rats exposed to neonatal anoxia. Exp Neurol 139:25–33

    CAS  PubMed  Google Scholar 

  • Iyer NV, Kotch LE, Agani F, Leung SW, Laugner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12:149–162

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jagtap P, Szabo C (2005) Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev 4:421–440

    CAS  Google Scholar 

  • Jiang B-H, Rue E, Wang GL, Roe R, Semenza GL (1996) Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 271:17771–17778

    CAS  PubMed  Google Scholar 

  • Kaufman SA, Miller SP, Ferreiro DM, Glidden DH, Barkovich AJ, Partridge JC (2003) Encephalopathy as a predictor of magnetic resonance imaging abnormalities in asphyxiated newborns. Pediatr Neurol 28:342–346

    PubMed  Google Scholar 

  • Kauppinen TM, Swanson RA (2007) The role of poly(ADP-ribose) polymerase-1 in CNS disease. Neuroscience 147:1267–1272

    Google Scholar 

  • Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases1/2. Proc Natl Acad Sci U S A 103:7136–7141

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kauppinen TM, Suh SW, Berman AE, Hamby AM, Swanson RA (2009) Inhibition of poly(ADP-ribose) polymerase suppresses inflammation and promotes recovery after ischemic injury. J Cereb Blood Flow Metab 29:820–829

    CAS  PubMed  Google Scholar 

  • Kenwrick S, Watkins A, De Angelis E (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum Mol Genet 9:879–886

    CAS  PubMed  Google Scholar 

  • Klawitter V, Morales P, Bustamante D, Gomez-Urquijo S, Hökfelt T, Herrera-Marschitz M (2007) Neuronal plasticity of basal ganglia following perinatal asphyxia: neuroprotection by nicotinamide. Exp Brain Res 180:139–152

    Google Scholar 

  • Klawitter V, Morales P, Johansson S, Bustamante D, Goiny M, Gross J, Luthman J, Herrera-Marschitz M (2005) Effect of perinatal asphyxia on cell survival, neuronal phenotype and neurite growth evaluated with organotypic triple cultures. Amino Acids 28:149–155

    CAS  PubMed  Google Scholar 

  • Klawitter V, Morales P, Bustamante D, Goiny M, Herrera-Marschitz M (2006) Plasticity of the central nervous system (CNS) following perinatal asphyxia> Does nicotinamide provide neuroprotection? Amino Acids 31:377–384

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Koh S-H, Park Y, Song CW, Kim JG, Kim K, Kim J, Kim M-H, Lee SR, Kim DW, Yu H-J, Chang D, Hwang SJ, Kim SH (2004) The effect of PARP inhibitor on ischemic cell death, its related inflammation and survival signals. Eur J Neurosci 20:1461–1472

    PubMed  Google Scholar 

  • Kohlhauser C, Kaehler S, Mosgoeller W, Singewald N, Koulevas D, Prast H, Hoeger H, Lubec B (1999a) Histological changes and neurotransmitter levels three months following perinatal asphyxia in the rat. Life Sci 64:2109–2124

    CAS  PubMed  Google Scholar 

  • Kohlhauser C, Mosgoeller W, Hoeger H, Lubec G, Lubec B (1999b) Cholinergic, monoaminergic and glutamatergic changes following perinatal asphyxia in the rat. Cell Mol Life Sci 55:1491–1501

    CAS  PubMed  Google Scholar 

  • Kohlhauser C, Mosgoeller W, Hoeger H, Lubec B (2000) Myelination deficits in brain of rats following perinatal asphyxia. Life Sci 67:2355–2368

    CAS  PubMed  Google Scholar 

  • Kurinczuk JJ, White-Koning M, Badawi N (2010) Epidemiology of neonatal encephalopathy and hypoxic-ischemic encephalopathy. Early Hum Dev 86:329–338

    PubMed  Google Scholar 

  • Labudova O, Schuller E, Yeghiazaryan K, Kitzmueller E, Hoeger H, Lubec G, Lubec B (1999) Genes involved in the pathophysiology of perinatal asphyxia. Life Sci 64:1831–1838

    CAS  PubMed  Google Scholar 

  • Lawn JE, Kerber K, Enweronu-Laryea C, Cousens S (2010) 3.6 million neonatal deaths-what is progressing and what is not? Semin Perinatol 34:371–386

    PubMed  Google Scholar 

  • Leppard JB, Dong Z, Mackey ZB, Tomkinson AE (2003) Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol Cell Biol 23:5919–5927

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leyton L, Schneider P, Labra CV, Rüegg C, Hetz CA, Quest AF, Bron C (2001) Thy-1 binds to the integrin b3 on astrocytes and triggers formation of focal contact sites. Curr Biol 11:1028–1038

    CAS  PubMed  Google Scholar 

  • Li Q, Martin JH (2000) Postdevelopmental of differential projections from the caudal and rostral motor cortex subregions. Exp Brain Res 134:187–198

    CAS  PubMed  Google Scholar 

  • Li S, Kim JE, Budel S, Hampton TG, Strittmatter SM (2005) Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol Cell Neurosci 29:26–39

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li N, Wu H, Yang S, Chen D (2007) Ischemic preconditioning induces XRCC1, DNA polymerase-beta, and DNA ligase III and correlates with enhanced base excision repair. DNA Repair (Amst) 6:1297–1306

    CAS  Google Scholar 

  • Loidl F, Gavilanes AW, Van Dijk EH, Vreuls W, Blokland A, Vies JS, Steinbusch HW, Blanco CE (2000) Effects of hypothermia and gender on survival and behaviour after perinatal asphyxia in rats. Physiol Behav 68:263–269

    CAS  PubMed  Google Scholar 

  • Loizou LA (1972) The postnatal ontogeny of monoamine-containing neurones in the central nervous system of the albino rat. Brain Res 40:395–418

    CAS  PubMed  Google Scholar 

  • Low JA (2004) Determining the contribution of asphyxia to brain damage in the neonate. J Obstet Gynaecol Res 30:276–286

    PubMed  Google Scholar 

  • Lubec B, Mark M, Herrera-Marschitz M, Labudova O, Hoeger H, Gille L, Nohl H, Mosgoeller W, Lubec G (1997a) Decrease of heart protein kinase C and cyclin-dependent kinase precedes death in perinatal asphyxia of the rat. FASEB J 11:482–492

    CAS  PubMed  Google Scholar 

  • Lubec B, Dell’Anna E, Fang-Kircher S, Mark M, Herrera-Marschitz M, Lubec G (1997b) Decrease of brain protein kinase C, protein kinase A, and cyclin-dependent kinase correlating with pH precedes neuronal death in neonatal asphyxia of the rat. J Invest Med 45:284–294

    CAS  Google Scholar 

  • Lubec B, Labudova O, Hoeger H, Kirchner L, Lubec G (2002) Expression of transcription factors in the brain of rats with perinatal asphyxia. Biol Neonate 81:266–278

    CAS  PubMed  Google Scholar 

  • Macleod MR, O’Collins T, Howells DW, Donnan GA (2004) Pooling of animal experimental data reveals influence of study design and publication bias. Stroke 35:1203–1208

    PubMed  Google Scholar 

  • Martin SS, Perez-Polo JR, Noppens KM, Grafe MR (2005) Biphasic changes in the levels of poly(ADPribose) polymerase-1 and caspase 3 in the immature brain following hypoxia-ischemia. Int J Dev Neurosci 23:673–686

    CAS  PubMed  Google Scholar 

  • Meng Z, Martin JH (2003) Postnatal development of corticospinal postsynaptic action. J Neurophysiol 90:683–692

    PubMed  Google Scholar 

  • Meng Z, Li Q, Martin JH (2004) The transition from development to motor control function in the corticospinal system. J Neurosci 24:605–614

    CAS  PubMed  Google Scholar 

  • Miller SP, Ramaswamy V, Michelson D, Barkovich J, Holshouser B, Wycliff N, Glidden DV, Deming D, Partridge JC, Wu YW, Ashwal S, Ferreiro DM (2005) Patters of brain injury in term neonatal encephalopathy. J Pediatr 146:453–460

    PubMed  Google Scholar 

  • Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250

    CAS  PubMed  Google Scholar 

  • Mishra OP, Akhter W, Ashraf QM, Delivoria-Papadopoulus M (2003) Hypoxia-induced modification of poly (ADP-Ribose) Polymerase and DNA polymerase β activity in cerebral cortical nuclei of newborn piglets: role of nitric oxide. Neuroscience 119:1023–1032

    CAS  PubMed  Google Scholar 

  • Montgomery AM, Becker JC, Siu CH, Lemmon VP, Cheresh DA, Pancook JD, Zhao X, Reisfeld RA (1996) Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin alpha v beta 3. J Cell Biol 132:475–485

    CAS  PubMed  Google Scholar 

  • Moonen HJJ, Geraets L, Vaarhorst A, Wouters EFM, Bast A, Hageman GJ (2005) Theophylline prevents NAD+ depletion via PARP-1 inhibition in human pulmonary epithelial cells. Biochem Biophys Res Commun 338:1805–1810

    CAS  PubMed  Google Scholar 

  • Morales P, Klawitter V, Johansson S, Huaiquin P, Barros VG, Avalos AM, Fiedler J, Bustamante D, Gomez-Urquijo S, Goiny M, Herrera-Marschitz M (2003) Perinatal asphyxia impairs connectivity and dopamine branching in organotypic triple culture from rat substantia nigra. Neurosci Lett 348:175–179

    CAS  PubMed  Google Scholar 

  • Morales P, Reyes P, Klawitter V, Huaiquin P, Bustamante D, Fiedler JL, Herrera-Marschitz M (2005) Effects of perinatal asphyxia on cell proliferation and neuronal phenotype evaluated with organotypic hippocampal cultures. Neuroscience 135:421–431

    CAS  PubMed  Google Scholar 

  • Morales P, Fiedler JL, Andres S, Berrios C, Huaiquin P, Bustamante D, Cardenas S, Parra E, Herrera-Marschitz M (2008) Plasticity of hippocampus following perinatal asphyxia: effects on postnatal apoptosis and neurogenesis. J Neurosci Res 86:2650–2662

    CAS  PubMed  Google Scholar 

  • Morales P, Simola N, Bustamante D, Lisboa F, Fiedler J, Gebicke-Haerter P, Morelli M, Tasker RA, Herrera-Marschitz M (2010) Nicotinamide prevents the effect of perinatal asphyxia on apoptosis, non-spatial working memory and anxiety in rats. Exp Brain Res 202:1–14

    CAS  PubMed  Google Scholar 

  • Morris RJ, Beech JN, Barber PC, Raisman G (1985) Early stages of Purkinje cell maturation demonstrated by Thy-1 immunohistochemistry on postnatal rat cerebellum. J Neurocytol 14:427–452

    CAS  PubMed  Google Scholar 

  • Morris RJ, Tiveron MC, Xue GP (1992) The relation of the expression and function of the neuronal glycoprotein Thy-1 to axonal growth. Biochem Soc Trans 20:401–405

    CAS  PubMed  Google Scholar 

  • Mosgoeller W, Kastner P, Fang-Kircher S, Kitzmueller E, Hoeger H, Sether P, Labudova O, Lubec G, Lubec B (2000) Brain RNA polymerase and nucleolar structure in perinatal asphyxia of the rat. Exp Neurol 161:174–182

    CAS  PubMed  Google Scholar 

  • Mudò G, Bonomo A, Di Liberto V, Frinchi M, Fuxe K, Belluardo N (2009) The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J Neural Transm

    Google Scholar 

  • Nagayama T, Simon RP, Chen D, Henshall DC, Pei W, Stetler RA, Chen J (2000) Activation of Poly(ADP-Ribose) polymerase in the rat hippocampus may contribute to cellular recovery following sublethal transient global ischemia. J Neurochem 74:1636–1645

    CAS  PubMed  Google Scholar 

  • Neira-Peña T, Espina-Marchant P, Rojas-Mancilla E, Esmar D, Kraus C, Munoz V, Perez B, Rivera B, Bustamante D, Valdes JL, Hermoso M, Gebicke-Haerter P, Morales P, Herrera-Marschitz M (2013) Molecular, cellular, and behavioural effects produced by perinatal asphyxia: protection by poly(ADP-ribose) polymerase 1 (PARP-1) inhibition. In: Kostrzewa RM (ed) Handbook of neurotoxicity. Springer, New York. doi:10.1007/978-1-4614-5836-4115

    Google Scholar 

  • Northington FJ, Ferreiro DM, Graham EM, Traystman RJ, Martin LJ (2001) Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 8:207–219

    CAS  PubMed  Google Scholar 

  • Odd DE, Lewis G, Whitelaw A, Gunnell D (2009) Resuscitation at birth and cognition at 8 years of age: a cohort study. Lancet 373(9675):1615–1622

    PubMed Central  PubMed  Google Scholar 

  • Olson L, Seiger Å (1972) Early prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwicklungsgesch 137:301–316

    CAS  PubMed  Google Scholar 

  • Oo TF, Burke RE (1997) The time course of the development cell death in phenotypically defined dopaminergic neurons of the substantia nigra. Dev Brain Res 98:191–196

    CAS  Google Scholar 

  • Pasternak JF, Predey TA, Mikhael MA (1991) Neonatal asphyxia: vulnerability of basal ganglia, thalamus and brain stem. Pediatr Neurol 7:147–149

    CAS  PubMed  Google Scholar 

  • Pastuzko A (1994) Metabolic responses of the dopaminergic system during hypoxia in newborn brain. Biochem Med Metab Biol 51:1–15

    Google Scholar 

  • Pétrilli V, Herced Z, Hassa PO, Patel NS, Di Paola R, Cortes U, Dugo L, Filipe HM, Thiemermann C, Hottiger MO, Cuzzocrea S, Wang ZQ (2004) Noncleavable poly(ADP-ribose) polymerase-1 regulates inflammation response in mice. J Clin Invest 114:1072–1081

    PubMed Central  PubMed  Google Scholar 

  • Plane JM, Liu R, Wang TW, Silverstein FS, Parent JM (2004) Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol Dis 16:16585–16595

    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

    CAS  PubMed  Google Scholar 

  • Qiao M, Malisza KL, Del Biio MR, Tuor UL (2001) Correlation of cerebral hypoxic-ischemic T2 changes with tissue alterations in water content and protein extravasation. Stroke 32:958–963

    CAS  PubMed  Google Scholar 

  • Ransohoff RM, Kivisakk P, Kidd G (2003) Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3:569–581

    CAS  PubMed  Google Scholar 

  • Robertson C, Perlman M (2006) Follow-up of the term infant after hypoxic-ischemic encephalopathy. Paediatr Child Health 11:278–282

    PubMed Central  PubMed  Google Scholar 

  • Robertson NJ, Tan S, Groenedaal F, van Bel F, Juul SE, Bennet L, Derrick M, Back SA, Valdez RC, Northington F, Gunn AJ, Mallard C (2012) Which neuroprotective agents are ready for bench to bedside translation in the newborn infant? J Pediatr 160:544–552

    PubMed Central  PubMed  Google Scholar 

  • Rojas-Mancilla E, Neira-Pena T, Kraus C, Rivera B, Perez R, Alvarez A, Bustamante D, Morales P, Leyton L, Herrera-Marschitz M (2013) Perinatal asphyxia decreases neuronal branching and synaptogenesis in rat hippocampus. Implication of astrocyte reactivity and HIF-1α.XXVIth international symposium on cerebral flow, metabolism and function & XIth international conference on quantification of brain function with PET. Shanghai, China, May 20–23, 2013

    Google Scholar 

  • Romijn HJ, Hofman MA, Gramsbergen A (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26:61–67

    CAS  PubMed  Google Scholar 

  • Ruppert M, Aigner S, Hubbe M, Yagita H, Altevogt P (1995) The L1 adhesion molecule is a cellular ligand for VLA-5. J Cell Biol 131:1881–1891

    CAS  PubMed  Google Scholar 

  • Sakakibara Y, Mitha AP, Ogilvy CS, Maynard KI (2000) Post-treatment with nicotinamide (vitamin B(3)) reduces the infarct volume following permanent focal cerebral ischemia in female Sprague-Dawley and Wistar rats. Neurosci Lett 281:111–114

    CAS  PubMed  Google Scholar 

  • Saldeen J, Welsh N (1998) Nicotinamide-induced apoptosis in insulin producing cells is associated with cleavage of poly(ADP-ribose)polymerase. Mol Cell Endocrinol 139:99–107

    CAS  PubMed  Google Scholar 

  • Sawaya MR, Prasad R, Wilson SH, Kraut J, Pelletier H (1997) Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36:11205–11215

    CAS  PubMed  Google Scholar 

  • Scheepens A, Wassink G, Piersma MJ, Van de Berg WDJ, Blanco CE (2003) A delayed increase in hippocampus following global asphyxia in the neonatal rat. Brain Res Dev Brain Res 142:67–76

    CAS  PubMed  Google Scholar 

  • Schmid RS, Maness PF (2008) L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr Opin Neurobiol 18(3):245–250

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schultz N, Lopez E, Saleh-Gohari N, Helleday T (2003) Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucl Acids Res 31:4959–4964

    CAS  PubMed Central  PubMed  Google Scholar 

  • Segalowitz SJ, Davies PL (2004) Charting the maturation of the frontal lobe: an electrophysiological strategy. Brain Cogn 55:116–133

    CAS  PubMed  Google Scholar 

  • Seidl R, Stoeckler-Ipsiroglu S, Rolinski B, Kohlhauser C, Herkner KR, Lubec B, Lubec G (2000) Energy metabolism in graded perinatal asphyxia of the rat. Life Sci 67:421–435

    CAS  PubMed  Google Scholar 

  • Seiger Å, Olson L (1972) Late prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwicklungsgesch 140:281–318

    Google Scholar 

  • Simola N, Bustamante D, Pinna A, Pontis S, Morales P, Morelli M, Herrera-Marschitz M (2008) Acute perinatal asphyxia impairs non-spatial memory and alters motor coordination in adult male rats. Exp Brain Res 185:595–601

    PubMed  Google Scholar 

  • Skaper SD (2003) Poly(ADP-ribosyl)ation enzyme-1 as a target for neuroprotection in acute central nervous system injury. Curr Drug Targets CNS Neurol Disord 2:279–291

    CAS  PubMed  Google Scholar 

  • Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999) In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859–861

    CAS  PubMed  Google Scholar 

  • Strackx E, Van den Hove DL, Prickaerts J, Zimmermann L, Steinbusch HW, Blanco CE, Gavilanes AW, Vles JS (2010) Fetal asphyctic preconditioning protects against perinatal asphyxia-induced behavioral consequences in adulthood. Behav Brain Res 208:343–351

    PubMed  Google Scholar 

  • Suh H, Deng W, Cage F (2009) Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 25:253–275

    CAS  PubMed  Google Scholar 

  • Sung P, Bailly V, Weber C, Thompson LH, Prakash L, Prakash S (1993) Human xeroderma pigmentosum group D gene encodes a DNA helicase. Nature 365:852–855

    CAS  PubMed  Google Scholar 

  • Takami K, Iwane M, Kiyota Y, Miyamoto M, Tsukuda R, Shiosaka S (1992) Increase of basic fibroblast growth factor immunoreactivity and its mRNA level in rat brain following transient forebrain ischemia. Exp Brain Res 90:1–10

    CAS  PubMed  Google Scholar 

  • Tiveron MC, Barboni E, Pliego Rivero FB, Gormley AM, Seeley PJ, Grosveld F, Morris RJ (1992) Selective inhibition of neurite outgrowth on mature astrocytes by Thy-1 glycoprotein. Nature 355:745–748

    CAS  PubMed  Google Scholar 

  • Trucco C, Oliver FJ, deMurcia G, Menissier de Murcia J (1998) DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucl Acids Res 26:2644–2649

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsang M, Dawid IB (2004) Promotion and attenuation of FGF signaling through the Ras-MAPK pathway. Sci STKE 228:17

    Google Scholar 

  • Tsuji L, Yamashita T, Kubo T, Madura T, Tanaka H, Hosokawa K, Tohyama M (2004) FLRT3, a cell surface molecule containing LRR repeats and a FNIII domain, promotes neurite outgrowth. Biochem Biophys Res Commun 313:1086–1091

    CAS  PubMed  Google Scholar 

  • Ullrich O, Diestel A, Evüpoglu IY, Nitsch R (2001) Regulation of microglial expression of integrins by poly(ADP-ribose) polymerase-1. Nat Cell Biol 3:1035–1042

    CAS  PubMed  Google Scholar 

  • Ungethüm U, Chen Y, Gross J, Bjelke B, Bolme P, Eneroth P, Heldt J, Loidl CF, Herrera-Marschitz M, Andersson K (1996) Effects of perinatal asphyxia on the mesostriatal/mesolimbic dopamine system of neonatal and 4-week-old male rats. Exp Brain Res 112:403–410

    PubMed  Google Scholar 

  • Van de Berg WD, Kwaijtaal M, de Louw AJ, Lissone NP, Schmitz C, Faull RL, Blokland A, Blanco CE, Steinbusch HW (2003) Impact of perinatal asphyxia on the GABAergic and locomotor system. Neuroscience 117:83–96

    CAS  PubMed  Google Scholar 

  • Van den Broek MPH, Groenendaal F, Egberts ACG, Rademaker CMA (2010) Effects of hypothermia on pharmacokinetics and pharmacodynamics. Clin Pharmacokinet 49:277–294

    CAS  PubMed  Google Scholar 

  • Van Erp TGM, Saleh PA, Rosso PA, Huttunen M, Lönnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen V-P, Standersköld-Nordenstam C-G, Cannon TD (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings and healthy unrelated volunteers. Am J Psychiatry 159:1514–1520

    PubMed  Google Scholar 

  • Vannuci S, Hagberg H (2004) Hypoxia-ischemia in the immature brain. J Exp Biol 207:3149–3154

    Google Scholar 

  • Venerosi A, Valanzano A, Cirulli F, Alleva E, Calamandrei G (2004) Acute global anoxia during C-section birth affects dopamine-mediated behavioural responses and reactivity to stress. Behav Brain Res 154:155–164

    CAS  PubMed  Google Scholar 

  • Venerosi A, Cutuli D, Chiarotti F, Calamandrei G (2006) C-section birth per se or followed by global asphyxia altered emotional behaviour in neonate and adult rats. Behav Brain Res 168:56–63

    PubMed  Google Scholar 

  • Venkatesan A, Frucht S (2006) Movement disorders after resuscitation from cardiac arrest. Neurol Clin 24:123–132

    PubMed  Google Scholar 

  • Vexler ZS, Yenari MA (2009) Does inflammation after stroke affect the developing brain differently than adult brain? Dev Neurosci 31:378–393

    CAS  PubMed Central  PubMed  Google Scholar 

  • Virag L, Szabo C (2002) The Therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54:375–429

    CAS  PubMed  Google Scholar 

  • Voorn P, Kalsbeck A, Jorritsma-Byham B, Groenewegen HJ (1988) The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25:857–887

    CAS  PubMed  Google Scholar 

  • Wan FJ, Lin HC, Kang BH, Tseng CJ, Tung CS (1999) D-amphetamine-induced depletion of energy and dopamine in the rat striatum is attenuated by nicotinamide pretreatment. Brain Res Bull 50:167–171

    CAS  PubMed  Google Scholar 

  • Wang H, Yao Y, Jiang X, Chen D, Xiong Y, Mu D (2006) Expression of Nogo-A and NgR in the developing rat brain after hypoxia-ischemia. Brain Res 1114:212–220

    CAS  PubMed  Google Scholar 

  • Wiessner C, Bareyre FM, Allegrini PR, Mir AK, Frentzel S, Zurini M, Schnell L, Oertle T, Schwab ME (2003) Anti-Nogo-A antibody infusion 24 hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J Cereb Blood Flow Metab 23:154–165

    CAS  PubMed  Google Scholar 

  • Wilson SH (1998) Mammalian base excision repair and DNA polymerase β. Mutation Res 407:203–215

    CAS  PubMed  Google Scholar 

  • Wyss JM, Van Groen T (1992) Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review. Hippocampus 2:1–11

    CAS  PubMed  Google Scholar 

  • Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B (2011) In vivo evidence for lactate as a neuronal energy source. J Neurosci 31:7477–7485

    CAS  PubMed  Google Scholar 

  • Yan Q, Briehl M, Crowley CL, Payne CM, Bernstein H, Bernstein C (1999) The NAD+ precursors, nicotinic acid and nicotinamide upregulate glyceraldehyde-3-phosphate dehydrogenase and glucose-6-phosphate dehydrogenase mRNA in Jurkat cells. Biochem Biophys Res Commun 255:133–136

    CAS  PubMed  Google Scholar 

  • Yu SW, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GC, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1 dependent cell death by apoptosis-inducing factor. Science 297:250–263

    Google Scholar 

  • Zhang J, Pieper A, Snyder SH (1995) Poly(ADP-ribose) synthase activation: an early indicator of neurotoxic DNA damage. J Neurochem 65:1411–1414

    CAS  PubMed  Google Scholar 

  • Zhao X, Yip PM, Siu CH (1998) Identification of a homophilic binding site in immunoglobulin-like domain 2 of the cell adhesion molecule L1. J Neurochem 71:960–971

    CAS  PubMed  Google Scholar 

  • Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Contract grant sponsors: FONDECYT-Chile (contracts:1120079;1110263;1110149); Millenium Institute Initiative (BNI P09-015-F); BMBF (NGFN + TP9) and DAAD (415/alechile)-Germany. TN-P is a BNI fellow; ER-M is CONICYT (#21090557), an ICBM fellow.

Conflict of Interest

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

  1. Millenium Institute BNI-Chile, Programme of Molecular & Clinical Pharmacology, ICBM, BNI, Medical Faculty, University of Chile, Santiago 7, P. O. Box 70.000, Chile

    M. Herrera-Marschitz, T. Neira-Peña, L. Leyton, P. Gebicke-Haerter, E. Rojas-Mancilla, P. Morales & D. Bustamante

  2. Department of Psychopharmacology, Central Institute of Mental Health J5, Mannheim, Germany

    P. Gebicke-Haerter

Authors
  1. M. Herrera-Marschitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Neira-Peña
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Leyton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Gebicke-Haerter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Rojas-Mancilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. D. Bustamante
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Herrera-Marschitz .

Editor information

Editors and Affiliations

  1. Facultad de Medicina Inst de Biologia Celular y Neurociecias, Universidad de Buenos Aires, Buenos Aires, Argentina

    Marta C. Antonelli

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Herrera-Marschitz, M. et al. (2015). Short- and Long-Term Consequences of Perinatal Asphyxia: Looking for Neuroprotective Strategies. In: Antonelli, M. (eds) Perinatal Programming of Neurodevelopment. Advances in Neurobiology, vol 10. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1372-5_9

Download citation

Publish with us

Policies and ethics

Search

Navigation