13C nmr metabolomic evaluation of immediate and delayed mild hypothermia in cerebrocortical slices after oxygen-glucose deprivation

Anesthesiology

Volumn 119, Issue 5, 2013, Pages 1120-1136

  Liu, Jia ^a   Segal, Mark R ^b   Kelly, Mark J S ^c   Pelton, Jeffrey G ^d   Kim, Myungwon ^a   James, Thomas L ^c   Litt, Lawrence ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department of Epidemiology and Biostatistics ^*  (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLUTAMINE; OXYGEN; PYRUVATE CARBOXYLASE; ACETIC ACID DERIVATIVE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BIOLOGICAL MARKER; CREATINE PHOSPHATE; TRICARBOXYLIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN TEMPERATURE; CARBON NUCLEAR MAGNETIC RESONANCE; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE SEVERITY; DISEASE SIMULATION; FEMALE; GLIA; HYPOTHERMIA; IMMUNOREACTIVITY; MALE; METABOLITE; NEUROPROTECTION; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPERATURE MEASUREMENT; ANIMAL; BODY TEMPERATURE; BRAIN HYPOXIA; BRAIN LEVEL; IN VITRO STUDY; INDUCED HYPOTHERMIA; METABOLISM; METABOLOMICS; NERVE CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; REGRESSION ANALYSIS; SPRAGUE DAWLEY RAT; BRAIN CHEMISTRY; DEFICIENCY; HYPOXIA, BRAIN;

ACETATES; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL MARKERS; BODY TEMPERATURE; BRAIN CHEMISTRY; CEREBRAL CORTEX; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; HYPOTHERMIA, INDUCED; HYPOXIA, BRAIN; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; NEUROGLIA; NEURONS; PHOSPHOCREATINE; RATS; RATS, SPRAGUE-DAWLEY; REGRESSION ANALYSIS; TRICARBOXYLIC ACIDS; IN VITRO TECHNIQUES;

EID: 84888286724     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e31829c2d90     Document Type: Article

References (39)

1. Roka A, Azzopardi D: Therapeutic hypothermia for neonatal hypoxic ischaemic encephalopathy. Early Hum Dev 2010; 86:361-7
2. Wilkinson DJ, Thayyil S, Robertson NJ: Ethical and practical issues relating to the global use of therapeutic hypothermia for perinatal asphyxial encephalopathy. Arch Dis Child Fetal Neonatal Ed 2011; 96:F75-8
3. Liu J, Litt L, Segal MR, Kelly MJ, Yoshihara HA, James TL: Outcome-related metabolomic patterns from 1H/31P NMR after mild hypothermia treatments of oxygen-glucose deprivation in a neonatal brain slice model of asphyxia. J Cereb Blood Flow Metab 2011; 31:547-59
4. Vannucci RC, Connor JR, Mauger DT, Palmer C, Smith MB, Towfighi J, Vannucci SJ: Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res 1999; 55:158-63
5. Vannucci RC, Brucklacher RM, Vannucci SJ: Glycolysis and perinatal hypoxic-ischemic brain damage. Dev Neurosci 2005; 27:185-90
6. Vannucci RC, Vannucci SJ: Perinatal hypoxic-ischemic brain damage: Evolution of an animal model. Dev Neurosci 2005; 27:81-6
7. Taylor A, McLean M, Morris P, Bachelard H: Approaches to studies on neuronal/glial relationships by 13C-MRS analysis. Dev Neurosci 1996; 18:434-42
8. Håberg A, Qu H, Bakken IJ, Sande LM, White LR, Haraldseth O, Unsgård G, Aasly J, Sonnewald U: In vitro and ex vivo 13C-NMR spectroscopy studies of pyruvate recycling in brain. Dev Neurosci 1998; 20:389-98
9. Håberg A, Qu H, Haraldseth O, Unsgård G, Sonnewald U: In vivo injection of [1-13C]glucose and [1,2-13C]acetate combined with ex vivo 13C nuclear magnetic resonance spectroscopy: A novel approach to the study of middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 1998; 18:1223-32
10. Melø TM, Nehlig A, Sonnewald U: Metabolism is normal in astrocytes in chronically epileptic rats: A 13C NMR study of neuronal-glial interactions in a model of temporal lobe epilepsy. J Cereb Blood Flow Metab 2005; 25:1254-64
11. Melø T, Bigini P, Sonnewald U, Balosso S, Cagnotto A, Barbera S, Uboldi S, Vezzani A, Mennini T: Neuronal hyperexcitability and seizures are associated with changes in glialneuronal interactions in the hippocampus of a mouse model of epilepsy with mental retardation. J Neurochem 2010; 115:1445-54
12. Müller B, Qu H, Gårseth M, White LR, Aasly J, Sonnewald U: Amino acid neurotransmitter metabolism in neurones and glia following kainate injection in rats. Neurosci Lett 2000; 279:169-72
13. Patel AB, de Graaf RA, Mason GF, Rothman DL, Shulman RG, Behar KL: The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc Natl Acad Sci U S A 2005; 102:5588-93
14. Van den Berg CJ: A model of compartmentation in mouse brain based on glucose and acetate metabolism, Metabolic Compartmentation in the Brain. Edited by Balázs R, Cremer JE. London, Macmillan, 1973, pp 137-66
15. Sonnewald U, Westergaard N, Krane J, Unsgård G, Petersen SB, Schousboe A: First direct demonstration of preferential release of citrate from astrocytes using [13C]NMR spectroscopy of cultured neurons and astrocytes. Neurosci Lett 1991; 128:235-9
16. Hassel B, Bachelard H, Jones P, Fonnum F, Sonnewald U: Trafficking of amino acids between neurons and glia in vivo. Effects of inhibition of glial metabolism by fluoroacetate. J Cereb Blood Flow Metab 1997; 17:1230-8
17. Espanol MT, Litt L, Yang GY, Chang LH, Chan PH, James TL, Weinstein PR: Tolerance of low intracellular pH during hypercapnia by rat cortical brain slices: A 31P/1H NMR study. J Neurochem 1992; 59:1820-8
18. Liu J, Hirai K, Litt L: Fructose-1,6-bisphosphate does not preserve ATP in hypoxic-ischemic neonatal cerebrocortical slices. Brain Res 2008; 1238:230-8
19. Liu J, Segal M, Yoo S, Yang GY, Kelly M, James TL, Litt L: Antioxidant effect of ethyl pyruvate in respiring neonatal cerebrocortical slices after H2O2 stress. Neurochem Int 2009; 54:106-10
20. McKenna MC, Dienel GA, Sonnewald U, Waagepetersen HS, Schousboe A: Energy metabolism of the brain, Basic Neurochemistry, 8th edition. Edited by Brady S, Siegel G, Albers RW, Price DL. New York, Elsevier, 2012, pp 221
21. Mason GF, Rothman DL, Behar KL, Shulman RG: NMR determination of the TCA cycle rate and alpha-ketoglutarate/glutamate exchange rate in rat brain. J Cereb Blood Flow Metab 1992; 12:434-47
22. Berkich DA, Xu Y, LaNoue KF, Gruetter R, Hutson SM: Evaluation of brain mitochondrial glutamate and alpha-ketoglutarate transport under physiologic conditions. J Neurosci Res 2005; 79:106-13
23. Westerhuis JA, Hoefsloot HCJ, Smit S, Vis DJ, Smilde AK, van Velzen EJJ, van Duijnhoven JPM, van Dorsten FA: Assessment of PLSDA cross validation. Metabolomics 2008; 4:81-9
24. Efron B, Hastie T, Johnstone I, Tibshirani R: Least angle regression. Ann Stat 2004; 32:407-99
25. Tibshirani R: Regression shrinkage and selection via the lasso. J R Stat Soc Series B Stat Methodol 1996; 58:267-88
26. Friedman J, Hastie T, Tibshirani R: Regularization paths for generalized linear models via coordinate descent. J Stat Softw 2010; 33:1-22
27. R, Development, Core, Team: R: A Language and Environment for Statistical Computing, Reference Index Version 2.2.1 edition. Vienna, Austria, R Foundation for Statistical Computing, 2005
28. Govindaraju V, Young K, Maudsley AA: Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 2000; 13:129-53
29. Håberg A, Qu H, Sonnewald U: Glutamate and GABA metabolism in transient and permanent middle cerebral artery occlusion in rat: Importance of astrocytes for neuronal survival. Neurochem Int 2006; 48:531-40
30. Eroglu C, Barres BA: Regulation of synaptic connectivity by glia. Nature 2010; 468:223-31
31. Rossi DJ, Brady JD, Mohr C: Astrocyte metabolism and signaling during brain ischemia. Nat Neurosci 2007; 10:1377-86
32. Thrane AS, Rangroo Thrane V, Zeppenfeld D, Lou N, Xu Q, Nagelhus EA, Nedergaard M: General anesthesia selectively disrupts astrocyte calcium signaling in the awake mouse cortex. Proc Natl Acad Sci U S A 2012; 109:18974-9
33. Franke H, Verkhratsky A, Burnstock G, Illes P: Pathophysiology of astroglial purinergic signalling. Purinergic Signal 2012; 8:629-57
34. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA: Glial and neuronal control of brain blood flow. Nature 2010; 468:232-43
35. Pekny M, Eliasson C, Siushansian R, Ding M, Dixon SJ, Pekna M, Wilson JX, Hamberger A: The impact of genetic removal of GFAP and/or vimentin on glutamine levels and transport of glucose and ascorbate in astrocytes. Neurochem Res 1999; 24:1357-62
36. Burtrum D, Silverstein FS: Hypoxic-ischemic brain injury stimulates glial fibrillary acidic protein mRNA and protein expression in neonatal rats. Exp Neurol 1994; 126:112-8
37. Zagami CJ, Beart PM, Wallis N, Nagley P, O'Shea RD: Oxidative and excitotoxic insults exert differential effects on spinal motoneurons and astrocytic glutamate transporters: Implications for the role of astrogliosis in amyotrophic lateral sclerosis. Glia 2009; 57:119-35
38. Vannucci RC, Towfighi J, Vannucci SJ: Secondary energy failure after cerebral hypoxia-ischemia in the immature rat. J Cereb Blood Flow Metab 2004; 24:1090-7
39. Ezquer ME, Valdez SR, Seltzer AM: Inflammatory responses of the substantia nigra after acute hypoxia in neonatal rats. Exp Neurol 2006; 197:391-8