Glucose metabolism and astrocyte-neuron interactions in the neonatal brain

Neurochemistry International

Volumn 82, Issue , 2015, Pages 33-41

  Brekke, Eva ^a,b   Morken, Tora Sund ^a,c   Sonnewald, Ursula ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORDLAND HOSPITAL   (Norway)

^c TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

Glutamate; Glycolysis; Neonatal; Pentose phosphate pathway; Pyruvate carboxylation; Rat

Indexed keywords

GLUCOSE; GLUCOSE 6 PHOSPHATE; GLUCOSE TRANSPORTER; GLUTAMATE TRANSPORTER; GLUTAMINE; KETONE BODY; MONOCARBOXYLATE TRANSPORTER; PYRUVATE CARBOXYLASE; PYRUVATE DEHYDROGENASE; PYRUVIC ACID; SUCCINIC SEMIALDEHYDE; GLUTAMIC ACID; PYRUVATE DEHYDROGENASE COMPLEX;

ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN METABOLISM; CARBOXYLATION; CELL INTERACTION; CITRIC ACID CYCLE; GLUCOSE INTAKE; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; GLYCOLYSIS; NERVE CELL; NEWBORN; NONHUMAN; PENTOSE PHOSPHATE CYCLE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REVIEW; ADULT; ANIMAL; BIOSYNTHESIS; BRAIN; CHEMISTRY; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MILK; PHYSIOLOGY; RAT;

RATTUS;

ADULT; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CITRIC ACID CYCLE; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; GLYCOLYSIS; HUMANS; INFANT, NEWBORN; KETONE BODIES; MILK; NEURONS; PENTOSE PHOSPHATE PATHWAY; PYRUVATE DEHYDROGENASE COMPLEX; RATS;

EID: 84923873562     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.02.002     Document Type: Review

References (61)

1. Bandeira F., Lent R., and Herculano-Houzel S. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat Proc. Natl. Acad. Sci. U.S.A. 106 2009 14108 14113
2. Baquer N.Z., Hothersall J.S., McLean P., and Greenbaum A.L. Aspects of carbohydrate metabolism in developing brain Dev. Med. Child Neurol 19 1977 81 104
3. Bartnik B.L., Sutton R.L., Fukushima M., Harris N.G., Hovda D.A., and Lee S.M. Upregulation of pentose phosphate pathway and preservation of tricarboxylic acid cycle flux after experimental brain injury J. Neurotrauma 22 2005 1052 1065
4. Ben-Yoseph O., Boxer P.A., and Ross B.D. Noninvasive assessment of the relative roles of cerebral antioxidant enzymes by quantitation of pentose phosphate pathway activity Neurochem. Res 21 1996 1005 1012
5. 2] glucose and microdialysis J. Neurochem 64 1995 1336 1342
6. Booth R.F., Patel T.B., and Clark J.B. The development of enzymes of energy metabolism in the brain of a precocial (guinea pig) and non-precocial (rat) species J. Neurochem 34 1980 17 25
7. Boulland J.-L., Rafiki A., Levy L.M., Storm-Mathisen J., and Chaudhry F.A. Highly differential expression of SN1, a bidirectional glutamine transporter, in astroglia and endothelium in the developing rat brain Glia 41 2003 260 275
8. Brekke E.M., Morken T.S., Wideroe M., Haberg A.K., Brubakk A.M., and Sonnewald U. The pentose phosphate pathway and pyruvate carboxylation after neonatal hypoxic-ischemic brain injury J. Cereb. Blood Flow Metab 34 2014 724 734
9. Chowdhury G.M., Patel A.B., Mason G.F., Rothman D.L., and Behar K.L. Glutamatergic and GABAergic neurotransmitter cycling and energy metabolism in rat cerebral cortex during postnatal development J. Cereb. Blood Flow Metab 27 2007 1895 1907
10. Cremer J.E. Substrate utilization and brain development J. Cereb. Blood Flow Metab 2 1982 394 407
11. Danbolt N.C. Glutamate uptake Prog. Neurobiol 65 2001 1 105
12. Danbolt N.C., Storm-Mathisen J., and Kanner B.I. An [Na++K+]coupled L-glutamate transporter purified from rat brain is located in glial cell processes Neuroscience 51 1992 295 310
13. Dombrowski G.J. Jr., Swiatek K.R., and Chao K.L. Lactate, 3-hydroxybutyrate, and glucose as substrates for the early postnatal rat brain Neurochem. Res 14 1989 667 675
14. Duffy T.E., Kohle S.J., and Vannucci R.C. Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia J. Neurochem 24 1975 271 276
15. 2]glucose labeling study in humans J. Cereb. Blood Flow Metab 27 2007 1593 1602
16. Gaitonde M.K., Evison E., and Evans G.M. The rate of utilization of glucose via hexosemonophosphate shunt in brain J. Neurochem 41 1983 1253 1260
17. Hagberg H., Mallard C., Rousset C.I., and Thornton C. Mitochondria: hub of injury responses in the developing brain Lancet Neurol 13 2014 217 232
18. 13C NMR spectroscopic study J. Neurochem 64 1995 2773 2782
19. Hawkins R.A., Williamson D.H., and Krebs H.A. Ketone-body utilization by adult and suckling rat brain in vivo Biochem. J. 122 1971 13 18
20. Hogstad S., Svenneby G., Torgner I.A., Kvamme E., Hertz L., and Schousboe A. Glutaminase in neurons and astrocytes cultured from mouse brain: kinetic properties and effects of phosphate, glutamate, and ammonia Neurochem. Res 13 1988 383 388
21. Hostetler K.Y., and Landau B.R. Estimation of the pentose cycle contribution to glucose metabolism in tissue in vivo Biochemistry 6 1967 2961 2964
22. 13C] glucose with or without ammonium acetate Brain Res 841 1999 11 19
23. Kreis R., Hofmann L., Kuhlmann B., Boesch C., Bossi E., and Huppi P.S. Brain metabolite composition during early human brain development as measured by quantitative in vivo 1H magnetic resonance spectroscopy Magn. Reson. Med 48 2002 949 958
24. Larsson O.M., Drejer J., Kvamme E., Svenneby G., Hertz L., and Schousboe A. Ontogenetic development of glutamate and GABA metabolizing enzymes in cultured cerebral cortex interneurons and in cerebral cortex in vivo Int. J. Dev. Neurosci 3 1985 177 185
25. Leino R.L., Gerhart D.Z., and Drewes L.R. Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: a quantitative electron microscopic immunogold study Brain Res. Dev. Brain Res 113 1999 47 54
26. Lowry O.H., Passonneau J.V., Hasselberger F.X., and Schulz D.W. Effect of ischemia on known substrates and cofactors of the glycolytic pathway in brain J. Biol. Chem 239 1964 18 30
27. McCormick D.A., and Prince D.A. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones J. Physiol 393 1987 743 762
28. McKenna M.C., Dienel G.A., Sonnewald U., Waagepetersen H.S., and Schousboe A. Energy metabolism of the brain Brady S.G.J. Siegel G. Albers R.W. Price D.L. Basic Neurochemistry: Principles of Molecular, Cellular, and Medical Neurobiology eighth ed. 2012 Elsevier Academic Press Oxford, UK 200 231
29. McKenna M.C., Sonnewald U., Huang X., Stevenson J., and Zielke H.R. Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes J. Neurochem 66 1996 386 393
30. 13C NMR study of neuronal-glial interactions in a model of temporal lobe epilepsy J. Cereb. Blood Flow Metab 25 2005 1254 1264
31. Melø T.M., Nehlig A., and Sonnewald U. Neuronal-glial interactions in rats fed a ketogenic diet Neurochem. Int 48 2006 498 507
32. 14C)succinate, after intracerebral administration J. Neurochem 23 1974 1281 1289
33. Morken T.S., Brekke E., Haberg A., Wideroe M., Brubakk A.M., and Sonnewald U. Neuron-astrocyte interactions, pyruvate carboxylation and the pentose phosphate pathway in the neonatal rat brain Neurochem. Res 39 3 2013 556 569
34. Morken T.S., Brekke E., Haberg A., Wideroe M., Brubakk A.M., and Sonnewald U. Altered astrocyte-neuronal interactions after hypoxia-ischemia in the neonatal brain in female and male rats Stroke 45 2014 2777 2785
35. Movassat J., Saulnier C., and Portha B. Insulin administration enhances growth of the beta-cell mass in streptozotocin-treated newborn rats Diabetes 46 9 1997 1445 1452
36. Nedergaard M., Ransom B., and Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain Trends Neurosci 26 2003 523 530
37. Nehlig A. Brain uptake and metabolism of ketone bodies in animal models Prostaglandins Leukot. Essent. Fatty Acids 70 2004 265 275
38. Norenberg M.D., and Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain Brain Res 161 1979 303 310
39. 2-fixing enzymes in the metabolism of rat brain J. Neurochem 22 1974 717 724
40. Patel T.B., and Clark J.B. Comparison of the development of the fatty acid content and composition of the brain of a precocial species (guinea pig) and a non-precocial species (rat) J. Neurochem 35 1980 149 154
41. Paulson O.B. Blood-brain barrier, brain metabolism and cerebral blood flow Eur. Neuropsychopharmacol 12 2002 495 501
42. 13C MR spectroscopy study of lactate as substrate for rat brain Dev. Neurosci 22 2000 429 436
43. Rae C., Fekete A.D., Kashem M.A., Nasrallah F.A., and Broer S. Metabolism, compartmentation, transport and production of acetate in the cortical brain tissue slice Neurochem. Res 37 2012 2541 2553
44. Rice J.E. 3rd, Vannucci R.C., and Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat Ann. Neurol 9 1981 131 141
45. Snead O.C. 3rd, and Stephens H.I. Ontogeny of cortical and subcortical electroencephalographic events in unrestrained neonatal and infant rats Exp. Neurol 82 1983 249 269
46. Sonnewald U. Glutamate synthesis has to be matched by its degradation - where do all the carbons go? J. Neurochem 131 2014 399 406
47. 13C NMR spectroscopy NMR Biomed 16 2003 424 429
48. 13C MRS Neurochem. Res 35 2010 1916 1921
49. Storm-Mathisen J., Leknes A.K., Bore A.T., Vaaland J.L., Edminson P., and Haug F.M. First visualization of glutamate and GABA in neurones by immunocytochemistry Nature 301 1983 517 520
50. Takahashi T., Shirane R., Sato S., and Yoshimoto T. Developmental changes of cerebral blood flow and oxygen metabolism in children AJNR Am. J. Neuroradiol 20 1999 917 922
51. Thayyil S., Chandrasekaran M., Taylor A., Bainbridge A., Cady E.B., and Chong W.K. Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis Pediatrics 125 2010 e382 e395
52. Thurston J.H., and McDougal D.B. Jr. Effect of ischemia on metabolism of the brain of the newborn mouse Am. J. Physiol 216 1969 348 352
53. Vannucci R.C., Yager J.Y., and Vannucci S.J. Cerebral glucose and energy utilization during the evolution of hypoxic-ischemic brain damage in the immature rat J. Cereb. Blood Flow Metab 14 1994 279 288
54. Vannucci S.J. Developmental expression of GLUT1 and GLUT3 glucose transporters in rat brain J. Neurochem 62 1994 240 246
55. Vannucci S.J., and Simpson I.A. Developmental switch in brain nutrient transporter expression in the rat Am. J. Physiol. Endocrinol. Metab 285 2003 E1127 E1134
56. Vannucci S.J., and Vannucci R.C. Glycogen metabolism in neonatal rat brain during anoxia and recovery J. Neurochem 34 1980 1100 1105
57. Vannucci S.J., Seaman L.B., Brucklacher R.M., and Vannucci R.C. Glucose transport in developing rat brain: glucose transporter proteins, rate constants and cerebral glucose utilization Mol. Cell. Biochem 140 1994 177 184
58. Varoqui H., Zhu H., Yao D., Ming H., and Erickson J.D. Cloning and functional identification of a neuronal glutamine transporter J. Biol. Chem 275 2000 4049 4054
59. Wang D.D., and Kriegstein A.R. Defining the role of GABA in cortical development J. Physiol 587 2009 1873 1879
60. Weiss M.D., Derazi S., Rossignol C., Varoqui H., Erickson J.D., and Kilberg M.S. Ontogeny of the neutral amino acid transporter SAT1/ATA1 in rat brain Brain Res. Dev. Brain Res 143 2003 151 159
61. Wilbur D.O., and Patel M.S. Development of mitochondrial pyruvate metabolism in rat brain J. Neurochem 22 1974 709 715