Persistently Altered Metabolic Phenotype following Perinatal Excitotoxic Brain Injury

Developmental Neuroscience

Volumn 39, Issue 1-4, 2017, Pages 182-191

  Blaise, Benjamin J ^a,b   Schwendimann, Leslie ^c,d   Chhor, Vibol ^c,d,e   Degos, Vincent ^c,d,f   Hodson, Mark P ^g   Dallmann, Guido ^h   Keller, Matthias ^i,j   Gressens, Pierre ^c,d,k   Fleiss, Bobbi ^c,d,k  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HOSPICES CIVILS DE LYON   (France)

^c HÔPITAL ROBERT DEBRÉ   (France)

^d PremUP   (France)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h BIOCRATES LIFE SCIENCES AG   (Austria)

ⁱ Passau Hospital   (Germany)

^j TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^k ST THOMAS HOSPITAL   (United Kingdom)

more..

Author keywords

Diffuse white matter injury; Hypoxic ischemic encephalopathy; Ibotenate; Mass spectrometry; Metabolomics; Metabonomics; Neonatal encephalopathy; Stroke

Indexed keywords

ARGININE; CHOLESTEROL; GLUTAMINE; GLYCEROPHOSPHOLIPID; IBOTENIC ACID; PHENYLALANINE; PROLINE; SERINE; SPHINGOMYELIN; THREONINE; TRYPTOPHAN; VALINE; AMINO ACID RECEPTOR STIMULATING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ASTROCYTE; BRAIN INJURY; BRAIN MATURATION; CONFERENCE PAPER; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; EXCITOTOXICITY; FEMALE; FLOW INJECTION ANALYSIS; LIMIT OF DETECTION; MALE; MASS SPECTROMETRY; MICROGLIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; VALIDATION PROCESS; ANIMAL; BRAIN DISEASE; METABOLISM; NEWBORN;

ANIMALS; ANIMALS, NEWBORN; BRAIN DISEASES; EXCITATORY AMINO ACID AGONISTS; FEMALE; IBOTENIC ACID; MALE; MICE; PHENOTYPE;

EID: 85018670392     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000464131     Document Type: Conference Paper

References (53)

1. Mesples B, et al: Pathophysiology of neonatal brain lesions: lessons from animal models of excitotoxicity. Acta Paediatr 2005; 94: 185-190.
2. Marret S, et al: Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions. J Neuropathol Exp Neurol 1995; 54: 358-370.
3. Lee JM, Zipfel GJ, Choi DW: The changing landscape of ischaemic brain injury mechanisms. Nature 1999; 399(suppl 6738):A7-A14.
4. Wahlestedt C, et al: Antisense oligodeoxynucleotides to NMDA-R1 receptor channel protect cortical neurons from excitotoxicity and reduce focal ischaemic infarctions. Nature 1993; 363: 260-263.
5. Burd I, et al: Excitotoxicity as a common mechanism for fetal neuronal injury with hypoxia and intrauterine inflammation. Adv Pharmacol 2016; 76: 85-101.
6. Johnston MV: Excitotoxicity in perinatal brain injury. Brain Pathol 2005; 15: 234-240.
7. Palmer AM, et al: Traumatic brain injury-induced excitotoxicity assessed in a controlled cortical impact model. J Neurochem 1993; 61: 2015-2024.
8. Costeloe KL, et al: Short term outcomes after extreme preterm birth in England: comparison of two birth cohorts in 1995 and 2006 (the EPICure studies). BMJ 2012; 345:e7976.
9. Ewing-Cobbs L, et al: Late intellectual and academic outcomes following traumatic brain injury sustained during early childhood. J Neurosurg 2006; 105(4 suppl):287-296.
10. Lee J, et al: Predictors of outcome in perinatal arterial stroke: a population-based study. Ann Neurol 2005; 58: 303-308.
11. Choi DW: Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988; 1: 623-634.
12. Coyle JT, Puttfarcken P: Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993; 262: 689-695.
13. Lipton SA, Rosenberg PA: Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 1994; 330: 613-622.
14. Olney JW, et al: NMDA antagonist neurotoxicity: mechanism and prevention. Science 1991; 254: 1515-1518.
15. Olney JW, Labruyere J, Price MT: Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science 1989; 244: 1360-1362.
16. Jevtovic-Todorovic V, et al: Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci 2003; 23: 876-882.
17. Ikonomidou C, et al: Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999; 283: 70-74.
18. Fleiss B, Gressens P: Tertiary mechanisms of brain damage: a new hope for treatment of cerebral palsy? Lancet Neurol 2012; 11: 556-566.
19. Silverstein F, Johnston MV: Effects of hypoxia-ischemia on monoamine metabolism in the immature brain. Ann Neurol 1984; 15: 342-347.
20. Binienda Z, et al: Acute effects of perinatal hypoxic insult on concentrations of dopamine, serotonin, and metabolites in fetal monkey brain. Int J Dev Neurosci 1994; 12: 127-131.
21. Yavin E, et al: Ischemia stress and arachidonic acid metabolites in the fetal brain. Ann NY Acad Sci 1989; 559: 248-258.
22. Palomba L, Cerioni L, Cantoni O: Arachidonic acid inhibits neuronal nitric oxide synthase elicited by proinflammatory stimuli and promotes astrocyte survival with both exogenous and endogenous peroxynitrite via different mechanisms. J Neurosci Res 2010; 88: 2459-2468.
23. Landucci E, et al: Involvement of endocannabinoid signaling in the neuroprotective effects of subtype 1 metabotropic glutamate receptor antagonists in models of cerebral ischemia. Int Rev Neurobiol 2009; 85: 337-350.
24. Shouman B, et al: Endocannabinoids potently protect the newborn brain against AMPAkainate receptor-mediated excitotoxic damage. Br J Pharmacol 2006; 148: 442-451.
25. Fattuoni C, et al: Perinatal asphyxia: a review from a metabolomics perspective. Molecules 2015; 20: 7000-7016.
26. Walsh BH, et al: The metabolomic profile of umbilical cord blood in neonatal hypoxic ischaemic encephalopathy. PLoS One 2012; 7:e50520.
27. Kaddurah-Daouk R, Kristal BS, Weinshilboum RM: Metabolomics: a global biochemical approach to drug response and disease. Annu Rev Pharmacol Toxicol 2008; 48: 653-683.
28. Tahraoui SL, et al: Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001; 11: 56-71.
29. Husson I, et al: Melatoninergic neuroprotection of the murine periventricular white matter against neonatal excitotoxic challenge. Ann Neurol 2002; 51: 82-92.
30. Haldipur P, et al: HIP/PAP prevents excitotoxic neuronal death and promotes plasticity. Ann Clin Transl Neurol 2014; 1: 739-754.
31. Carlsson Y, et al: Genetic inhibition of caspase-2 reduces hypoxic-ischemic and excitotoxic neonatal brain injury. Ann Neurol 2011; 70: 781-789.
32. Degos V, et al: Neuroprotective effects of dexmedetomidine against glutamate agonist-induced neuronal cell death are related to increased astrocyte brain-derived neurotrophic factor expression. Anesthesiology 2013; 118: 1123-1132.
33. Bouslama M, et al: Melatonin prevents learning disorders in brain-lesioned newborn mice. Neuroscience 2007; 150: 712-719.
34. Husson I, et al: BDNF-induced white matter neuroprotection and stage-dependent neuronal survival following a neonatal excitotoxic challenge. Cereb Cortex 2005; 15: 250-261.
35. Laudenbach V, et al: Nociceptin/orphanin FQ exacerbates excitotoxic white-matter lesions in the murine neonatal brain. J Clin Invest 2001; 107: 457-466.
36. Urban M, et al: Complexity and pitfalls of mass spectrometry-based targeted metabolomics in brain research. Anal Biochem 2010; 406: 124-131.
37. FDA: Nonclinical Safety Evaluation of Pediatric Drug Products, 2006. http://www.fda. gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/ Guidances/ ucm079247.pdf.
38. Trygg J: O2-PLS for qualitative and quantitative analysis in multivariate calibration. J Chemometrics 2002; 16: 283-293.
39. Trygg J, Wold S: Orthogonal projections to latent structures (O-PLS). J Chemometrics 2002; 16: 119-128.
40. Keun HC, et al: Geometric trajectory analysis of metabolic responses to toxicity can define treatment specific profiles. Chem Res Toxicol 2004; 17: 579-587.
41. Galindo-Prieto B, Eriksson L, Trygg J: Variable influence on projection (VIP) for orthogonal projections to latent structures (OPLS). J Chemometrics 2014; 28: 623-632.
42. Ong WY, et al: Changes in brain cholesterol metabolome after excitotoxicity. Mol Neurobiol 2010; 41: 299-313.
43. Dommergues MA, et al: Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection. Neuroscience 2003; 121: 619-628.
44. Bell-Temin H, et al: Novel molecular insights into classical and alternative activation states of microglia as revealed by stable isotope labeling by amino acids in cell culture (SILAC)-based proteomics. Mol Cell Proteomics 2015; 14: 3173-3184.
45. De Simone R, et al: Branched-chain amino acids influence the immune properties of microglial cells and their responsiveness to proinflammatory signals. Biochim Biophys Acta 2013; 1832: 650-659.
46. Amaral AI, et al: A comprehensive metabolic profile of cultured astrocytes using isotopic transient metabolic flux analysis and C-labeled glucose. Front Neuroenergetics 2011; 3: 5.
47. Xu D, et al: Increased arachidonic acid-containing phosphatidylcholine is associated with reactive microglia and astrocytes in the spinal cord after peripheral nerve injury. Sci Rep 2016; 6: 26427.
48. He X, et al: Expression, activity, and role of serine palmitoyltransferase in the rat hippocampus after kainate injury. J Neurosci Res 2007; 85: 423-432.
49. Volpe JJ: The encephalopathy of prematurity-brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 2009; 16: 167-178.
50. Beckstrom AC, et al: Application of comprehensive two-dimensional gas chromatography with time-of-flight mass spectrometry method to identify potential biomarkers of perinatal asphyxia in a non-human primate model. J Chromatogr A 2011; 1218: 1899-1906.
51. Dudzik D, et al: LC-MS-based metabolomics identification of novel biomarkers of chorioamnionitis and its associated perinatal neurological damage. J Proteome Res 2015; 14: 1432-1444.
52. Chun PT, et al: Serial plasma metabolites following hypoxic-ischemic encephalopathy in a nonhuman primate model. Dev Neurosci 2015; 37: 161-171.
53. Keller M, et al: Inflammatory-induced hibernation in the fetus: priming of fetal sheep metabolism correlates with developmental brain injury. PLoS One 2011; 6:e29503.