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

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• 作者：Selva Baltan (1)
  
  1. Department of Neurosciences ; Lerner Research Institute ; NC/30 ; The Cleveland Clinic Foundation ; Cleveland ; OH ; 44195 ; USA
  
• 关键词：D ; lactate ; White matter ; Axon ; Oligodendrocytes ; End ; feet
• 刊名：Metabolic Brain Disease
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：30
• 期：1
• 页码：25-30
• 全文大小：199 KB
• 参考文献：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鈥?2
  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鈥?145 CrossRef
  4. Auer RN (1986) Progress review: hypoglycemic brain damage. Stroke 17:699鈥?08 CrossRef
  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鈥?089 CrossRef
  6. Black JA, Waxman SG (1988) The perinodal astrocyte. Glia 1:169鈥?83 CrossRef
  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鈥?0102 CrossRef
  8. Brown AM, Baltan Tekk枚k S, Ransom BR (2003) Glycogen regulation and functional role in mouse white matter. J Physiol 549(2):501鈥?12 CrossRef
  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鈥?99 CrossRef
  10. Chih C, Lipton P, Roberts EL (2001) Do active cerebral neurons really use lactate rather than glucose? TINS 24:573鈥?78
  11. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208鈥?14 CrossRef
  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鈥?21
  14. Hajek I, Subbarao KV, Hertz L (1996) Acute and chronic effects of potassium and noradrenaline on Na+, K+鈭扐TPase activity in cultured mouse neurons and astrocytes. Neurochem Int 28:335鈥?42 CrossRef
  15. Harris JJ, Attwell D (2012) The energetics of CNS white matter. J Neurosci 32:356鈥?71 CrossRef
  16. Henn FA, Haljamae H, Hamberger A (1972) Glial cell function: active control of extracellular K+ concentration. Brain Res 43:437鈥?43 CrossRef
  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鈥?49 CrossRef
  18. Honegger P, Pardo B (1999) Separate neuronal and glial Na+, K+鈭扐TPase isoforms regulate glucose utilization in response to membrane depolarization and elevated extracellular potassium. J Cereb Blood Flow Metab 19:1051鈥?059 CrossRef
  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鈥?22
  20. Kuffler SW, Potter DD (1964) Glia in the Leech central nervous system: physiological properties and neuron-glia relationship. J Neurophysiol 27:290鈥?20
  21. Kuffler SW, Nicholls JG (1966) The physiology of neuroglial cells. Ergeb Physiol 57:1鈥?0 CrossRef
  22. Kuffler SW, Nicholls JG, Orkand RK (1966) Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29:768鈥?87
  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鈥?22 CrossRef
  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鈥?87 CrossRef
  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鈥?71
  26. Maher F, Vannucci SJ, Simpson IA (1994) Glucose transporter proteins in brain. FASEB J 8:1003鈥?011
  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鈥?39
  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鈥?6676
  29. Nave KA (2010a) Myelination and support of axonal integrity by glia. Nature 468:244鈥?52 CrossRef
  30. Nave KA (2010b) Myelination and the trophic support of long axons. Nat Rev Neurosci 11:275鈥?83 CrossRef
  31. Nave KA, Ehrenreich H (2014) Myelination and oligodendrocyte functions in psychiatric diseases. JAMA Psychiatry 71:582鈥?84 CrossRef
  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鈥?99 CrossRef
  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鈥?73, 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鈥?99 CrossRef
  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鈥?1 CrossRef
  36. Phelps CH (1972) Barbiturate-induced glycogen accumulation in brain. An electron microscopic study. Brain Res 39:225鈥?34 CrossRef
  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鈥?24
  38. Ransom BR, Orkand RK (1996) Glial-neuronal interactions in non-synaptic areas of the brain: studies in the optic nerve. TINS 19:352鈥?58
  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鈥?94 CrossRef
  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鈥?29 CrossRef
  41. Simpson IA, Vannucci SJ, Maher F (1994) Glucose transporters in mammalian brain. Biochem Soc Trans 22:671鈥?75
  42. Swanson RA, Choi DW (1993) Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 13:162鈥?69 CrossRef
  43. Tekkok SB, Brown AM, Ransom BR (2003) Axon function persists during anoxia in mammalian white matter. J Cereb Blood Flow Metab 23:1340鈥?347 CrossRef
  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鈥?52 CrossRef
  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鈥?351
  46. Vannucci SJ, Maher F, Simpson IA (1997) Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 21:2鈥?1 CrossRef
  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鈥?810
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Neurology
  Biochemistry
  Oncology
  
• 出版者：Springer Netherlands
• ISSN：1573-7365

文摘

In the mammalian white matter, glycogen-derived lactate from astrocytes plays a critical role in supporting axon function using the astrocyte-neuron lactate transfer shuttle (ANLTS) system with specialized monocarboxylate transporters (MCTs). A rapid breakdown of glycogen to lactate during increased neuronal activity or low glucose conditions becomes essential to maintain axon function. Therefore astrocytes actively regulate their glycogen stores with respect to ambient glucose levels such that high ambient glucose upregulates glycogen and low levels of glucose depletes glycogen stores. Although lactate fully supports axon function in the absence of glucose and becomes a preferred energy metabolite when axons discharge at high frequency, it fails to benefit axon function during an ischemic episode in white matter. Emerging evidence implies a similar lactate transport system between oligodendrocytes and the axons they myelinate, suggesting another metabolic coupling pathway in white matter. Therefore the conditions that activate this lactate shuttle system and the signaling mechanisms that mediate activation of this system are of great interest. Future studies are expected to unravel the details of oligodendrocyte-axon lactate metabolic coupling to establish how white matter components metabolically cooperate and that lactate may be the universal metabolite to sustain CNS function.