Can lactate serve as an energy substrate for axons in good times and in bad, in sickness and in health?

Metabolic Brain Disease

Volumn 30, Issue 1, 2015, Pages 25-30

  Baltan, Selva ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Axon; D lactate; End feet; Oligodendrocytes; White matter

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GLUCOSE; GLYCOGEN; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER;

ANIMAL; ASTROCYTE; AXON; BIOLOGICAL MODEL; BRAIN ISCHEMIA; CELL COMMUNICATION; ENERGY METABOLISM; HOMEOSTASIS; HUMAN; METABOLISM; MOUSE; OLIGODENDROGLIA; OPTIC NERVE; TRANSPORT AT THE CELLULAR LEVEL; WHITE MATTER;

ANIMALS; ASTROCYTES; AXONS; BIOLOGICAL TRANSPORT; BRAIN ISCHEMIA; CELL COMMUNICATION; ENERGY METABOLISM; GLUCOSE; GLYCOGEN; HOMEOSTASIS; HUMANS; LACTIC ACID; MICE; MODELS, NEUROLOGICAL; MONOCARBOXYLIC ACID TRANSPORTERS; OLIGODENDROGLIA; OPTIC NERVE; SODIUM-POTASSIUM-EXCHANGING ATPASE; WHITE MATTER;

EID: 84939886924     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-014-9595-3     Document Type: Article

References (47)

1. Alessandri B, Landolt H, Langemann H, Gregorin J, Hall J, Gratzl O (1996) Application of glutamate in the cortex of rats: a microdialysis study. Acta Neurochir Suppl 67:6–12
2. Amaral AI, Meisingset TW, Kotter MR, Sonnewald U (2013) Metabolic aspects of neuron-oligodendrocyte-astrocyte interactions. Front Endocrinol (Lausanne) 4:54
3. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145
4. Auer RN (1986) Progress review: hypoglycemic brain damage. Stroke 17:699–708
5. 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
6. Black JA, Waxman SG (1988) The perinodal astrocyte. Glia 1:169–183
7. 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
8. Brown AM, Baltan Tekkök S, Ransom BR (2003) Glycogen regulation and functional role in mouse white matter. J Physiol 549(2):501–512
9. Butt AM, Duncan A, Berry M (1994) Astrocyte associations with nodes of Ranvier: ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve. J Neurocytol 23:486–499
10. Chih C, Lipton P, Roberts EL (2001) Do active cerebral neurons really use lactate rather than glucose? TINS 24:573–578
11. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208–214
12. Frier BM, Fisher BM (1999) Hypoglycemia in clinical diabetes. Wiley, New York
13. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Mobius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517–521
14. Hajek I, Subbarao KV, Hertz L (1996) Acute and chronic effects of potassium and noradrenaline on Na+, K+−ATPase activity in cultured mouse neurons and astrocytes. Neurochem Int 28:335–342
15. Harris JJ, Attwell D (2012) The energetics of CNS white matter. J Neurosci 32:356–371
16. Henn FA, Haljamae H, Hamberger A (1972) Glial cell function: active control of extracellular K+ concentration. Brain Res 43:437–443
17. 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
18. Honegger P, Pardo B (1999) Separate neuronal and glial Na+, K+−ATPase isoforms regulate glucose utilization in response to membrane depolarization and elevated extracellular potassium. J Cereb Blood Flow Metab 19:1051–1059
19. Kuffler SW, Nicholis JG (1964) Glial cells in the central nervous system of the Leech; Their membrane potential and potassium content. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol 248:216–222
20. Kuffler SW, Potter DD (1964) Glia in the Leech central nervous system: physiological properties and neuron-glia relationship. J Neurophysiol 27:290–320
21. Kuffler SW, Nicholls JG (1966) The physiology of neuroglial cells. Ergeb Physiol 57:1–90
22. Kuffler SW, Nicholls JG, Orkand RK (1966) Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29:768–787
23. Lee S, Leach MK, Redmond SA, Chong SY, Mellon SH, Tuck SJ, Feng ZQ, Corey JM, Chan JR (2012) A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 9:917–922
24. Magistretti PJ, Pellerin L (1996) Cellular mechanisms of brain energy metabolism. Relevance to functional brain imaging and to neurodegenerative disorders. Ann N Y Acad Sci 777:380–387
25. Magistretti PJ, Sorg O, Naichen Y, Pellerin L, De Rham S, Martin JL (1994) Regulation of astrocyte energy metabolism by neurotransmitters. Ren Physiol Biochem 17:168–171
26. Maher F, Vannucci SJ, Simpson IA (1994) Glucose transporter proteins in brain. FASEB J 8:1003–1011
27. Moody DM, Bell MA, Challa VR (1990) Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: an anatomic study. Am J Neuroradiol 11:431–439
28. Munzer JS, Daly SE, Jewell-Motz EA, Lingrel JB, Blostein R (1994) Tissue- and isoform-specific kinetic behavior of the Na, K-ATPase. J Biol Chem 269:16668–16676
29. Nave KA (2010a) Myelination and support of axonal integrity by glia. Nature 468:244–252
30. Nave KA (2010b) Myelination and the trophic support of long axons. Nat Rev Neurosci 11:275–283
31. Nave KA, Ehrenreich H (2014) Myelination and oligodendrocyte functions in psychiatric diseases. JAMA Psychiatry 71:582–584
32. Pellegri G, Rossier C, Magistretti PJ, Martin JL (1996) Cloning, localization and induction of mouse brain glycogen synthase. Brain Res Mol Brain Res 38:191–199
33. Pellerin L, Bonvento G, Chatton JY, Pierre K, Magistretti PJ (2002) Role of neuron-glia interaction in the regulation of brain glucose utilization. Diabetes Nutr Metab 15:268–273, discussion 273
34. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL, Stella N, Magistretti PJ (1998) Evidence supporting the existence of an activity-dependent astrocyte- neuron lactate shuttle. Dev Neurosci 20:291–299
35. Pfeiffer-Guglielmi B, Fleckenstein B, Jung G, Hamprecht B (2003) Immunocytochemical localization of glycogen phosphorylase isozymes in rat nervous tissues by using isozyme-specific antibodies. J Neurochem 85:73–81
36. Phelps CH (1972) Barbiturate-induced glycogen accumulation in brain. An electron microscopic study. Brain Res 39:225–234
37. Poole RC, Sansom CE, Halestrap AP (1996) Studies of the membrane topology of the rat erythrocyte H+/lactate cotransporter (MCT1). Biochem J 320:817–824
38. Ransom BR, Orkand RK (1996) Glial-neuronal interactions in non-synaptic areas of the brain: studies in the optic nerve. TINS 19:352–358
39. Ros J, Pecinska N, Alessandri B, Landolt H, Fillenz M (2001) Lactate reduces glutamate-induced neurotoxicity in rat cortex. J Neurosci Res 66:790–794
40. Sanchez-Abarca LI, Tabernero A, Medina JM (2001) Oligodendrocytes use lactate as a source of energy and as a precursor of lipids. Glia 36:321–329
41. Simpson IA, Vannucci SJ, Maher F (1994) Glucose transporters in mammalian brain. Biochem Soc Trans 22:671–675
42. Swanson RA, Choi DW (1993) Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 13:162–169
43. Tekkok SB, Brown AM, Ransom BR (2003) Axon function persists during anoxia in mammalian white matter. J Cereb Blood Flow Metab 23:1340–1347
44. 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
45. Tsacopoulos M, Veuthey AL, Saravelos SG, Perrottet P, Tsoupras G (1994) Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci 14:1339–1351
46. Vannucci SJ, Maher F, Simpson IA (1997) Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 21:2–21
47. 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 20:6804–6810