Phosphorylation status of pyruvate dehydrogenase distinguishes metabolic phenotypes of cultured rat brain astrocytes and neurons

GLIA

Volumn 58, Issue 10, 2010, Pages 1168-1176

  Halim, Nader D ^a   Mcfate, Thomas ^a   Mohyeldin, Ahmed ^a   Okagaki, Peter ^a   Korotchkina, Lioubov G ^b   Patel, Mulchand S ^b   Jeoung, Nam Ho ^c,d   Harris, Robert A ^c   Schell, Michael J ^a   Verma, Ajay ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Catholic University of Daegu   (South Korea)

Author keywords

Dichloroacetate; Glycolysis; Lactate; Oxidation

Indexed keywords

LACTIC ACID; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE COMPLEX;

ALPHA CHAIN; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; ASTROCYTE; CELL TYPE; CITRIC ACID CYCLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME METABOLISM; FEMALE; GLUCOSE METABOLISM; IN VITRO STUDY; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; COCULTURE TECHNIQUES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; L-LACTATE DEHYDROGENASE; LACTIC ACID; NEURONS; PHOSPHORYLATION; PYRUVATE DEHYDROGENASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77954354634     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20996     Document Type: Article

References (53)

1. Armstrong RC. 1998. Isolation and characterization of immature oligodendrocyte lineage cells. Methods 16:282-292.
2. Bittar PG, Charnay Y, Pellerin L, Bouras C, Magistretti PJ. 1996. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J Cereb Blood Flow Metab 16:1079-1089. (Pubitemid 26365358)
3. Bluml S, Moreno-Torres A, Shic F, Nguy CH, Ross BD. 2002. Tricarboxylic acid cycle of glia in the in vivo human brain. NMR Biomed 15:1-5.
4. Bouzier-Sore AK, Voisin P, Bouchaud V, Bezancon E, Franconi JM, Pellerin L. 2006. Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: A comparative NMR study. Eur J Neurosci 24:1687-1694.
5. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM. 1998. Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 329 (Pt 1):191-196. (Pubitemid 28022308)
6. Broer S, Rahman B, Pellegri G, Pellerin L, Martin JL, Verleysdonk S, Hamprecht B, Magistretti PJ. 1997. Comparison of lactate transport in astroglial cells and monocarboxylate transporter 1 (MCT 1) expressing Xenopus laevis oocytes. Expression of two different monocarboxylate transporters in astroglial cells and neurons. J Biol Chem 272:30096-30102.
7. Cerdan S, Rodrigues TB, Sierra A, Benito M, Fonseca LL, Fonseca CP, Garcia-Martin ML. 2006. The redox switch/redox coupling hypothesis. Neurochem Int 48:523-530.
8. Clark JB, Nicklas WJ. 1970. The metabolism of rat brain mitochondria. Preparation and characterization. J Biol Chem 245:4724-4731.
9. 13C NMR studies of metabolic compartmentation in the adult mammalian brain. NMR Biomed 12:451-462.
10. Escartin C, Pierre K, Colin A, Brouillet E, Delzescaux T, Guillermier M, Dhenain M, Deglon N, Hantraye P, Pellerin L, Bonvento G. 2007. Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J Neurosci 27:7094-7104. (Pubitemid 47037552)
11. Fiacco TA, McCarthy KD. 2006. Astrocyte calcium elevations: Properties, propagation, and effects on brain signaling. Glia 54:676-690.
12. 2+ entry in glial cells. J Neurosci 23:4737-4745.
13. Gruetter R, Seaquist ER, Ugurbil K. 2001. A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am J Physiol Endocrinol Metab 281:E100-E112.
14. Halestrap AP, Meredith D. 2004. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 447:619-628.
15. Harris RA, Huang B, Wu P. 2001. Control of pyruvate dehydrogenase kinase gene expression. Adv Enzyme Regul 41:269-288.
16. Hassoun EA, Ray S. 2003. The induction of oxidative stress and cellular death by the drinking water disinfection by-products, dichloroacetate and trichloroacetate in J774.A1 cells. Comp Biochem Physiol C Toxicol Pharmacol 135:119-128.
17. Hertz L, Dienel GA. 2005. Lactate transport and transporters: General principles and functional roles in brain cells. J Neurosci Res 79:11-18. (Pubitemid 40116412)
18. Hertz L, Peng L, Dienel GA. 2007. Energy metabolism in astrocytes: High rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27:219-249.
19. Hopper RK, Carroll S, Aponte AM, Johnson DT, French S, Shen RF, Witzmann FA, Harris RA, Balaban RS. 2006. Mitochondrial matrix phosphoproteome: Effect of extra mitochondrial calcium. Biochemistry 45:2524-2536.
20. Huang B, Wu P, Popov KM, Harris RA. 2003. Starvation and diabetes reduce the amount of pyruvate dehydrogenase phosphatase in rat heart and kidney. Diabetes 52:1371-1376.
21. Hyder F, Patel AB, Gjedde A, Rothman DL, Behar KL, Shulman RG. 2006. Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J Cereb Blood Flow Metab 26:865-877.
22. Itoh Y, Esaki T, Shimoji K, Cook M, Law MJ, Kaufman E, Sokoloff L. 2003. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc Natl Acad Sci USA 100:4879-4884.
23. Jeoung NH, Sanghani PC, Zhai L, Harris RA. 2006a. Assay of the pyruvate dehydrogenase complex by coupling with recombinant chicken liver arylamine N-acetyltransferase. Anal Biochem 356:44-50.
24. Jeoung NH, Wu P, Joshi MA, Jaskiewicz J, Bock CB, Depaoli-Roach AA, Harris RA. 2006b. Role of pyruvate dehydrogenase kinase isoenzyme 4 (PDHK4) in glucose homoeostasis during starvation. Biochem J 397:417-425.
25. Karpova T, Danchuk S, Kolobova E, Popov KM. 2003. Characterization of the isozymes of pyruvate dehydrogenase phosphatase: Implications for the regulation of pyruvate dehydrogenase activity. Biochim Biophys Acta 1652:126-135.
26. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW. 2004. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103.
27. 13C nuclear magnetic resonance spectroscopy: Elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J Neurosci 22:1523-1531.
28. Lovatt D, Sonnewald U, Waagepetersen HS, Schousboe A, He W, Lin JH, Han X, Takano T, Wang S, Sim FJ, Goldman SA, Nedergaard M. 2007. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-12266.
29. Lydell CP, Chan A, Wambolt RB, Sambandam N, Parsons H, Bondy GP, Rodrigues B, Popov KM, Harris RA, Brownsey RW, Allard MF. 2002. Pyruvate dehydrogenase and the regulation of glucose oxidation in hypertrophied rat hearts. Cardiovasc Res 53:841-851.
30. Lynch G, Kessler M, Halpain S, Baudry M. 1983. Biochemical effects of high-frequency synaptic activity studied with in vitro slices. Fed Proc 42:2886-2890. (Pubitemid 13007098)
31. Magistretti PJ. 2006. Neuron-glia metabolic coupling and plasticity. J Exp Biol 209(Pt 12):2304-2311.
32. Muir D, Berl S, Clarke DD. 1986. Acetate and fluoroacetate as possible markers for glial metabolism in vivo. Brain Res 380:336-340.
33. 2 fixation increases with brain activity. J Neurosci 24:11273-11279.
34. Patel MS, Korotchkina LG. 2006. Regulation of the pyruvate dehydrogenase complex. Biochem Soc Trans 34(Pt 2):217-222.
35. Pellerin L, Magistretti PJ. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625-10629.
36. Pellerin L, Magistretti PJ. 2004. Neuroscience. Let there be (NADH) light. Science 305:50-52.
37. Pierre K, Pellerin L. 2005. Monocarboxylate transporters in the central nervous system: Distribution, regulation and function. J Neurochem 94:1-14.
38. Pysh JJ, Khan T. 1972. Variations in mitochondrial structure and content of neurons and neuroglia in rat brain: An electron microscopic study. Brain Res 36:1-18.
39. 2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res Dev Brain Res 143:33-46.
40. Schell MJ, Erneux C, Irvine RF. 2001. Inositol 1,4,5-trisphosphate 3-kinase A associates with F-actin and dendritic spines via its N terminus. J Biol Chem 276:37537-37546.
41. Serres S, Raffard G, Franconi JM, Merle M. 2008. Close coupling between astrocytic and neuronal metabolisms to fulfill anaplerotic and energy needs in the rat brain. J Cereb Blood Flow Metab 28:712-724. (Pubitemid 351432784)
42. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG. 1998. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 95:316-321.
43. Stacpoole PW, Greene YJ. 1992. Dichloroacetate. Diabetes Care 15:785-791.
44. Sugden MC, Holness MJ. 2003. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 284:E855-E862.
45. Suh SW, Aoyama K, Matsumori Y, Liu J, Swanson RA. 2005. Pyruvate administered after severe hypoglycemia reduces neuronal death and cognitive impairment. Diabetes 54:1452-1458. (Pubitemid 40586677)
46. Takahashi S, Driscoll BF, Law MJ, Sokoloff L. 1995. Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. Proc Natl Acad Sci USA 92:4616-4620.
47. Taskinalp O, Aktas RG, Cigali B, Kutlu AK. 2000. Immunohistochemical demonstration of cytochrome oxidase in different parts of the central nervous system: A comparative experimental study. Anat Histol Embryol 29:345-349.
48. Tekkok SB, Brown AM, Westenbroek R, Pellerin L, Ransom BR. 2005. Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J Neurosci Res 81:644-652.
49. Tovar-Mendez A, Miernyk JA, Randall DD. 2003. Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 270:1043-1049.
50. Tsacopoulos M, Magistretti PJ. 1996. Metabolic coupling between glia and neurons. J Neurosci 16:877-885.
51. Vega C, Poitry-Yamate CL, Jirounek P, Tsacopoulos M, Coles JA. 1998. Lactate is released and taken up by isolated rabbit vagus nerve during aerobic metabolism. J Neurochem 71:330-337. (Pubitemid 28292566)
52. Walz W, Mukerji S. 1988. Lactate release from cultured astrocytes and neurons: A comparison. Glia 1:366-370.
53. Zielke HR, Zielke CL, Baab PJ, Tildon JT. 2007. Effect of fluorocitrate on cerebral oxidation of lactate and glucose in freely moving rats. J Neurochem 101:9-16.