Mitochondrial lactate metabolism is involved in antioxidative defense in human astrocytoma cells

Journal of Neuroscience Research

Volumn 92, Issue 4, 2014, Pages 464-475

  Lemire, Joseph ^a,b   Auger, Christopher ^a   Mailloux, Ryan ^a,c   Appanna, Vasu D ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Astrocytes; Lactate dehydrogenase; Metabolism; Pyruvate; Reactive oxygen species

Indexed keywords

ASTROCYTES; LACTATE DEHYDROGENASE; METABOLISM; PYRUVATE; REACTIVE OXYGEN SPECIES;

ALUMINUM; ANALYSIS OF VARIANCE; ANTIOXIDANTS; ASTROCYTES; CELL LINE, TRANSFORMED; CHELATING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT COMPLEX IV; HUMANS; HYDROGEN PEROXIDE; ISOENZYMES; L-LACTATE DEHYDROGENASE; LACTATES; MITOCHONDRIA; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PYRUVIC ACID; REACTIVE OXYGEN SPECIES; TIME FACTORS;

EID: 84895069893     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23338     Document Type: Article

References (55)

1. Alekseenko AV, Lemeshchenko VV, Pekun TG, Waseem TV, Fedorovich SV. 2012. Glutamate-induced free radical formation in rat brain synaptosomes is not dependent on intrasynaptosomal mitochondria membrane potential. Neurosci Lett 513:238-242.
2. Bélanger M, Magistretti PJ. 2009. The role of astroglia in neuroprotection. Dialogues Clin Neurosci 11:281-295.
3. Bergersen LH, Gjedde A. 2012. Is lactate a volume transmitter of metabolic states of the brain? Front Neuroenergetics 4:5.
4. Bezzi P, Volterra A. 2011. Astrocytes: powering memory. Cell 144:644-645.
5. Bittar BG, Charnay Y, Pellerin L, Bouras C, Magistretti PJ. 1996. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J Cereb Blow Flow Metab 16:1079-1089.
6. Bonuccelli G, Tsirigos A, Whitaker-Menezes D, Pavlides S, Pestell RG, Chiavarina B, et al. 2010. Ketones and lactate "fuel" tumor growth and metastasis: evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle 9:3506-3514.
7. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Brooks GA. 2007. Lactate: link between glycolytic and oxidative metabolism. Sports Med 37:341-343.
9. Brooks GA. 2009. Cell-cell and intracellular lactate shuttles. J Physiol 587:5591-5600.
10. Cruz RS, de Aguiar RA, Turnes T, Penteado Dos Santos R, de Oliveira MF, Caputo F. 2012. Intracellular shuttle: the lactate aerobic metabolism. Sci World J 2012:420984.
11. De Bari L, Chieppa G, Marra E, Passarella S. 2010. L-lactate metabolism can occur in normal and cancer prostate cells via the novel mitochondrial L-lactate dehydrogenase. Int J Oncol 37:1607-1620.
12. Deelchand DK, Shestov AA, Koski DM, Uǧurbil K, Henry P-G. 2009. Acetate transport and utilization in the rat brain. J Neurochem 109:46-54.
13. Desagher S, Glowinski J, Premont J. 1997. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J Neurosci 17:9060-9067.
14. Exley C. 2004. The pro-oxidant activity of aluminum. Free Radic Biol Med 36:380-387.
15. Exley C. 2009. Darwin, natural selection and the biological essentiality of aluminium and silicon. Trends Biochem Sci 34:589-593.
16. Feron O. 2009. Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol 92:329-333.
17. Giri S, Khan M, Nath N, Singh I, Singh AK. 2008. The role of AMPK in psychosine mediated effects on oligodendrocytes and astrocytes: implication for Krabbe disease. J Neurochem 105:1820-1833.
18. Gohil K, Brooks GA. 2012. Exercise tames the wild-side of the Myc-network: a hypothesis. Am J Physiol Endocrinol Metab 303:18-30.
19. Harris AD, Roberton VH, Huckle DL, Saxena N, Evans CJ, Murphy K, et al. 2013. Temporal dynamics of lactate concentration in the human brain during acute inspiratory hypoxia. J Magn Reson Imaging 37:739-745.
20. Hashimoto T, Hussien R, Brooks GA. 2006. Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am J Physiol Endocrinol Metab 290:1237-1244.
21. Hashimoto T, Hussien R, Cho HS, Kaufer D, Brooks GA. 2008. Evidence for the mitochondrial lactate oxidation complex in rat neurons: demonstration of an essential component of brain lactate shuttles. PloS One 3:e2915.
22. Henderson NS, Nijtmans LG, Lindsay JG, Lamantea E, Zeviani M, Holt IJ. 2000. Separation of intact pyruvate dehydrogenase complex using blue native agarose gel electrophoresis. Electrophoresis 21:2925-2931.
23. Holmes RS, Goldberg E. 2009. Computational analyses of mammalian lactate dehydrogenases: human, mouse, opossum and platypus LDHs. Comput Biol Chem 33:379-385.
24. Ju KD, Shin EK, Cho EJ, Yoon HB, Kim HS, Kim H, et al. 2012. Ethyl pyruvate ameliorates albuminuria and glomerular injury in the animal model of diabetic nephropathy. Am J Physiol Renal Physiol 302:606-613.
25. Kaizer RR, Correa MC, Gris LR, da Rosa CS, Bohrer D, Morsch VM, et al. 2008. Effect of long-term exposure to aluminum on the acetylcholinesterase activity in the central nervous system and erythrocytes. Neurochem Res 33:2294-2301.
26. Knott EM, Sun J, Lei Y, Ryou MG, Olivencia-Yurvati AH, Mallet RT. 2006. Pyruvate mitigates oxidative stress during reperfusion of cardioplegia-arrested myocardium. Ann Thorac Surg 81:928-934.
27. Künnecke B. 2012. Cerebral acetate metabolism: toward its in vivo assessment. Choi I-Y, Gruetter R, eds. New York: Springer. p 763-791.
28. Latham T, Mackay L, Sproul D, Karim M, Culley J, Harrison DJ, et al. 2012. Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Res 40:4794-4803.
29. Lemire J, Mailloux RJ, Appanna VD. 2008. Mitochondrial lactate dehydrogenase is involved in oxidative-energy metabolism in human astrocytoma cells (CCF-STTG1). PloS One 3:e1550.
30. Lemire J, Mailloux R, Puiseux-Dao S, Appanna VD. 2009. Aluminum-induced defective mitochondrial metabolism perturbs cytoskeletal dynamics in human astrocytoma cells. J Neurosci Res 87:1474-1483.
31. Lemire J, Mailloux R, Darwich R, Auger C, Appanna VD. 2011. The disruption of L-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells. Toxicol Lett 203:219-226.
32. Mailloux RJ, Appanna VD. 2007. Aluminum toxicity triggers the nuclear translocation of HIF-1alpha and promotes anaerobiosis in hepatocytes. Toxicol In Vitro 21:16-24.
33. Mailloux RJ, Beriault R, Lemire J, Singh R, Chenier DR, Hamel RD, et al. 2007a. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PloS One 2:e690.
34. Mailloux R, Lemire J, Appanna V. 2007b. Aluminum-induced mitochondrial dysfunction leads to lipid accumulation in human hepatocytes: a link to obesity. Cell Physiol Biochem 20:627-638.
35. Mallet RT, Sun J. 2003. Antioxidant properties of myocardial fuels. Mol Cell Biochem 253:103-111.
36. Mallet RT, Squires JE, Bhatia S, Sun J. 2002. Pyruvate restores contractile function and antioxidant defenses of hydrogen peroxide-challenged myocardium. J Mol Cell Cardiol 34:1173-1184.
37. Mallet RT, Sun J, Knott EM, Sharma AB, Olivencia-Yurvati AH. 2005. Metabolic cardioprotection by pyruvate: recent progress. Exp Biol Med 230:435-443.
38. Malthankar-Phatak GH, Patel AB, Xia Y, Hong S, Chowdhury GM, Behar KL, et al. 2008. Effects of continuous hypoxia on energy metabolism in cultured cerebro-cortical neurons. Brain Res 1229:147-154.
39. Mazzio EA, Soliman KF. 2003. Cytoprotection of pyruvic acid and reduced beta-nicotinamide adenine dinucleotide against hydrogen peroxide toxicity in neuroblastoma cells. Neurochem Res 28:733-741.
40. Mentz S, de Lacalle S, Baerga-Ortiz A, Knauer MF, Knauer DJ, Komives EA. 1999. Mechanism of thrombin clearance by human astrocytoma cells. J Neurochem 72:980-987.
41. Newinton JT, Harris RA, Cumming RC. 2013. Reevaluating metabolism in Alzheimer's disease from the perspective of the astrocyte-neuron lactate shuttle model. J Neurol Des 234572.
42. Overgaard M, Rasmussen P, Bohm AM, Seifert T, Brassard P, Zaar M, et al. 2012. Hypoxia and exercise provoke both lactate release and lactate oxidation by the human brain. FASEB J 26:3012-3020.
43. Passarella S, de Bari L, Valenti D, Pizzuto R, Paventi G, Atlante A. 2008. Mitochondria and L-lactate metabolism. FEBS Lett 582:3569-3576.
44. Pellerin L, Magistretti PJ. 1994. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625-10629.
45. Rinholm JE, Bergersen LH. 2012. Neuroscience: the wrap that feeds neurons. Nature 487:435-436.
46. Schagger H, von Jagow G. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223-231.
47. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, et al. 2003. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 23:3394-3406.
48. Simonovic AD, Gaddameedhi S, Anderson MD. 2004. In-gel precipitation of enzymatically released phosphate. Anal Biochem 334:312-317.
49. Stewart VC, Stone R, Gegg ME, Sharpe MA, Hurst RD, Clark JB, et al. 2002. Preservation of extracellular glutathione by an astrocyte derived factor with properties comparable to extracellular superoxide dismutase. J Neurochem 83:984-981.
50. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, et al. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810-823.
51. Szutowicz A, Bielarczyk H, Jankowska-Kulawy A, Pawelczyk T, Ronowska A. 2013. Acetyl-CoA the key factor for survival or death of cholinergic neurons in course of neurodegenerative diseases. Neurochem Res 38:1523-1542.
52. Tretter L, Adam-Vizi V. 2005. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos Trans R Soc Lond B Biol Sci 360:2335-2345.
53. van Hall G, Stromstad M, Rasmussen P, Jans O, Zaar M, Gam C, et al. 2009. Blood lactate is an important energy source for the human brain. J Cereb Blood Flow Metab 29:1121-1129.
54. Wellen KE, Thompson CB. 2012. A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol 13:270-276.
55. Wyss MT, Magistretti PJ, Buck A, Weber B. 2011. Labeled acetate as a marker of astrocytic metabolism. J Cereb Blood Flow Metab 31:1668-1674.