Prevention of acute/severe hypoglycemia-induced neuron death by lactate administration

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 6, 2012, Pages 1086-1096

  Won, Seok Joon ^a   Jang, Bong Geom ^b   Yoo, Byung Hoon ^a,c   Sohn, Min ^d   Lee, Min Woo ^b   Choi, Bo Young ^b   Kim, Jin Hee ^b   Song, Hong Ki ^b   Suh, Sang Won ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Hallym University   (South Korea)

^c Inje University College of Medicine   (South Korea)

^d Inha University   (South Korea)

Author keywords

hypoglycemia; lactate; microglial activation; neuron death; superoxide

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; LACTATE SODIUM; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SUPEROXIDE;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PH; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; ELECTROENCEPHALOGRAM; GLYCOLYSIS; HIPPOCAMPUS; HYPOGLYCEMIA; LACTATE BLOOD LEVEL; MALE; MICROGLIA; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; RAT;

ACUTE DISEASE; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL DEATH; DIABETIC NEUROPATHIES; ELECTROCARDIOGRAPHY; GLYCOLYSIS; HIPPOCAMPUS; HYDROGEN-ION CONCENTRATION; HYPOGLYCEMIA; LACTIC ACID; MALE; NAD; NEURONS; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84862789325     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.30     Document Type: Article

References (49)

1. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA (2010) NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30:2967-78
2. Alano CC, Tran A, Tao R, Ying W, Karliner JS, Swanson RA (2007) Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes. J Neurosci Res 85:3378-85 (Pubitemid 350058526)
3. Alano CC, Ying W, Swanson RA (2004) Poly(ADP-ribose) polymerase-1- mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J Biol Chem 279:18895-902 (Pubitemid 38623317)
4. Auer RN, Hall P, Ingvar M, Siesjo BK (1986) Hypotension as a complication of hypoglycemia leads to enhanced energy failure but no increase in neuronal necrosis. Stroke 17:442-9 (Pubitemid 16085686)
5. Auer RN, Olsson Y, Siesjo BK (1984) Hypoglycemic brain injury in the rat. Correlation of density of brain damage with the EEG isoelectric time: a quantitative study. Diabetes 33:1090-8 (Pubitemid 15204588)
6. Berthet C, Lei H, Thevenet J, Gruetter R, Magistretti PJ, Hirt L (2009) Neuroprotective role of lactate after cerebral ischemia. J Cereb Blood Flow Metab 29:1780-9
7. Boumezbeur F, Petersen KF, Cline GW, Mason GF, Behar KL, Shulman GI, Rothman DL (2011) The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J Neurosci 30:13983-91
8. Budd SL, Castilho RF, Nicholls DG (1997) Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett 415:21-4 (Pubitemid 27402041)
9. Cater HL, Chandratheva A, Benham CD, Morrison III B, Sundstrom LE (2003) Lactate and glucose as energy substrates during, and after, oxygen deprivation in rat hippocampal acute and cultured slices. J Neurochem 87:1381-90 (Pubitemid 38020572)
10. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, Epstein CJ (1998) Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18:8292-9 (Pubitemid 28465005)
11. Davis EA, Jones TW (1998) Hypoglycemia in children with diabetes: incidence, counterregulation and cognitive dysfunction. J Pediatr Endocrinol Metab 11(Suppl 1):177-82
12. Dienel GA, Cruz NF (2004) Nutrition during brain activation: does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought? Neurochem Int 45:321-51 (Pubitemid 38625624)
13. Engelsen B, Westerberg E, Fonnum F, Wieloch T (1986) Effect of insulin-induced hypoglycemia on the concentrations of glutamate and related amino acids and energy metabolites in the intact and decorticated rat neostriatum. J Neurochem 47:1634-41 (Pubitemid 17174687)
14. Heinemann U, Buchheim K, Gabriel S, Kann O, Kovacs R, Schuchmann S (2002) Cell death and metabolic activity during epileptiform discharges and status epilepticus in the hippocampus. Prog Brain Res 135:197-210 (Pubitemid 35461018)
15. Ichai C, Armando G, Orban JC, Berthier F, Rami L, Samat-Long C, Grimaud D, Leverve X (2009) Sodium lactate versus mannitol in the treatment of intracranial hypertensive episodes in severe traumatic brain-injured patients. Intensive Care Med 35:471-9
16. Kauppinen TM, Higashi Y, Suh SW, Escartin C, Nagasawa K, Swanson RA (2008) Zinc triggers microglial activation. J Neurosci 28:5827-35
17. Kauppinen TM, Swanson RA (2005) Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. J Immunol 174:2288-96 (Pubitemid 40223977)
18. Kirsch M, De Groot H (2001) NAD(P)H, a directly operating antioxidant? FASEB J 15:1569-74 (Pubitemid 32673387)
19. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-8
20. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283:496-7
21. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, Chan PH (1998) Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18:205-13 (Pubitemid 28046782)
22. Nagayama T, Simon RP, Chen D, Henshall DC, Pei W, Stetler RA, Chen J (2000) Activation of poly(ADP-ribose) polymerase in the rat hippocampus may contribute to cellular recovery following sublethal transient global ischemia. J Neurochem 74:1636-45
23. Pellerin L, Bergersen LH, Halestrap AP, Pierre K (2005) Cellular and subcellular distribution of monocarboxylate transporters in cultured brain cells and in the adult brain. J Neurosci Res 79:55-64 (Pubitemid 40116418)
24. 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 91:10625-9 (Pubitemid 24329051)
25. Pignataro G, Simon RP, Xiong ZG (2007) Prolonged activation of ASIC1a and the time window for neuroprotection in cerebral ischaemia. Brain 130:151-8 (Pubitemid 46026231)
26. Rinholm JE, Hamilton NB, Kessaris N, Richardson WD, Bergersen LH, Attwell D (2011) Regulation of oligodendrocyte development and myelination by glucose and lactate. J Neurosci 31:538-48
27. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-30
28. Schurr A (2006) Lactate: the ultimate cerebral oxidative energy substrate? J Cereb Blood Flow Metab 26:142-52
29. Schurr A, Payne RS, Miller JJ, Rigor BM (1997a) Glia are the main source of lactate utilized by neurons for recovery of function posthypoxia. Brain Res 774:221-4 (Pubitemid 28007904)
30. Schurr A, Payne RS, Miller JJ, Rigor BM (1997b) Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res 744:105-11 (Pubitemid 27033584)
31. Schurr A, Payne RS, Miller JJ, Rigor BM (1997c) Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: further in vitro validation. J Neurochem 69:423-6 (Pubitemid 27274200)
32. Schurr A, Payne RS, Miller JJ, Tseng MT (2001a) Preischemic hyperglycemia-aggravated damage: evidence that lactate utilization is beneficial and glucose-induced corticosterone release is detrimental. J Neurosci Res 66:782-9
33. Schurr A, Payne RS, Miller JJ, Tseng MT, Rigor BM (2001b) Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischemia. Brain Res 895:268-72 (Pubitemid 32231167)
34. Seltzer HS (1989) Drug-induced hypoglycemia. A review of 1418 cases. Endocrinol Metab Clin North Am 18:163-83
35. Suh SW, Aoyama K, Chen Y, Garnier P, Matsumori Y, Gum E, Liu J, Swanson RA (2003) Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J Neurosci 23:10681-90 (Pubitemid 37485282)
36. Suh SW, Aoyama K, Matsumori Y, Liu J, Swanson RA (2005) Pyruvate administered after severe hypoglycemia reduces neuronal death and cognitive impairment. Diabetes 54:1452-8 (Pubitemid 40586677)
37. Suh SW, Garnier P, Aoyama K, Chen Y, Swanson RA (2004) Zinc release contributes to hypoglycemia-induced neuronal death. Neurobiol Dis 16:538-45 (Pubitemid 38942986)
38. Suh SW, Gum ET, Hamby AM, Chan PH, Swanson RA (2007) Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest 117:910-8 (Pubitemid 46556747)
39. Suh SW, Hamby AM, Gum ET, Shin BS, Won SJ, Sheline CT, Chan PH, Swanson RA (2008a) Sequential release of nitric oxide, zinc, and superoxide in hypoglycemic neuronal death. J Cereb Blood Flow Metab 28: 1697-706
40. Suh SW, Shin BS, Ma H, Van Hoecke M, Brennan AM, Yenari MA, Swanson RA (2008b) Glucose and NADPH oxidase drive neuronal superoxide formation in stroke. Ann Neurol 64:654-63
41. van Hall G, Stromstad M, Rasmussen P, Jans O, Zaar M, Gam C, Quistorff B, Secher NH, Nielsen HB (2009) Blood lactate is an important energy source for the human brain. J Cereb Blood Flow Metab 29:1121-9
42. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR (2000) Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 20:6804-10
43. Wieloch T (1985) Hypoglycemia-induced neuronal damage prevented by an N-methyl-D- aspartate antagonist. Science 230:681-3
44. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, Wemmie JA, Price MP, Welsh MJ, Simon RP (2004) Neuroprotection in ischemia: blocking calciumpermeable acid-sensing ion channels. Cell 118:687-98 (Pubitemid 39221729)
45. Ying W, Alano CC, Garnier P, Swanson RA (2005) NAD+ as a metabolic link between DNA damage and cell death. J Neurosci Res 79:216-23 (Pubitemid 40116438)
46. Ying W, Chen Y, Alano CC, Swanson RA (2002) Tricarboxylic acid cycle substrates prevent PARP-mediated death of neurons and astrocytes. J Cereb Blood Flow Metab 22:774-9 (Pubitemid 34747594)
47. Ying W, Garnier P, Swanson RA (2003) NAD+ repletion prevents PARP-1-induced glycolytic blockade and cell death in cultured mouse astrocytes. Biochem Biophys Res Commun 308:809-13 (Pubitemid 36980637)
48. Zhao H, Kalivendi S, Zhang H, Joseph J, Nithipatikom K, Vasquez-Vivar J, Kalyanaraman B (2003) Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 34:1359-1368 (Pubitemid 36570409)
49. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 18:1272-82 (Pubitemid 38720595)