White matter lactate - Does it matter?

Neuroscience

Volumn 276, Issue , 2014, Pages 109-116

  Rinholm, J E ^a,d   Bergersen, L H ^a,b,c  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Development; Energy; Lactate; Myelination; Volume transmitter

Indexed keywords

ACETYL COENZYME A; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOSE; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 2; MONOCARBOXYLATE TRANSPORTER 4; MYELIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROPIONYL COENZYME A;

ASTROCYTE; BRAIN CELL; BRAIN REGION; CITRIC ACID CYCLE; HUMAN; MYELIN SHEATH; MYELINATION; NERVE FIBER; NEUROPATHOLOGY; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; WHITE MATTER; ANIMAL; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; AXONS; HUMANS; LACTIC ACID; MYELIN SHEATH; OLIGODENDROGLIA; SIGNAL TRANSDUCTION; WHITE MATTER;

EID: 84906791714     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.10.002     Document Type: Review

References (91)

1. Agnati L.F., Guidolin D., Guescini M., Genedani S., Fuxe K. Understanding wiring and volume transmission. Brain Res Rev 2010, 64:137-159.
2. Ahmed K., Tunaru S., Offermanns S. GPR109A, GPR109B and GPR81, a family of hydroxy-carboxylic acid receptors. Trends Pharmacol Sci 2009, 30:557-562.
3. Amaral A.I., Meisingset T.W., Kotter M.R., Sonnewald U. Metabolic aspects of neuron-oligodendrocyte-astrocyte interactions. Front Endocrinol (Lausanne) 2013, 4:54.
4. Aubert A., Pellerin L., Magistretti P.J., Costalat R. A coherent neurobiological framework for functional neuroimaging provided by a model integrating compartmentalized energy metabolism. Proc Natl Acad Sci U S A 2007, 104:4188-4193.
5. Azim K., Butt A.M. GSK3beta negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 2011, 59:540-553.
6. Back S.A., Luo N.L., Mallinson R.A., O'Malley J.P., Wallen L.D., Frei B., Morrow J.D., Petito C.K., Roberts C.T., Murdoch G.H., Montine T.J. Selective vulnerability of preterm white matter to oxidative damage defined by F2-isoprostanes. Ann Neurol 2005, 58:108-120.
7. Baumgart E., Fahimi H.D., Stich A., Volkl A. L-Lactate dehydrogenase A4- and A3B isoforms are bona fide peroxisomal enzymes in rat liver. Evidence for involvement in intraperoxisomal NADH reoxidation. J Biol Chem 1996, 271:3846-3855.
8. Bergersen L.H., Gjedde A. Is lactate a volume transmitter of metabolic states of the brain?. Front Neuroenergetics 2012, 4:5.
9. Bergersen L., Johannsson E., Veruki M.L., Nagelhus E.A., Halestrap A., Sejersted O.M., Ottersen O.P. Cellular and subcellular expression of monocarboxylate transporters in the pigment epithelium and retina of the rat. Neuroscience 1999, 90:319-331.
10. Bergersen L., Waerhaug O., Helm J., Thomas M., Laake P., Davies A.J., Wilson M.C., Halestrap A.P., Ottersen O.P. A novel postsynaptic density protein: the monocarboxylate transporter MCT2 is co-localized with delta-glutamate receptors in postsynaptic densities of parallel fiber-Purkinje cell synapses. Exp Brain Res 2001, 136:523-534.
11. Bergersen L.H., Magistretti P.J., Pellerin L. Selective postsynaptic co-localization of MCT2 with AMPA receptor GluR2/3 subunits at excitatory synapses exhibiting AMPA receptor trafficking. Cereb Cortex 2005, 15:361-370.
12. Bohnen N.I., Albin R.L. White matter lesions in Parkinson disease. Nat Rev Neurol 2011, 7:229-236.
13. Broer S., Schneider H.P., Broer A., Rahman B., Hamprecht B., Deitmer J.W. Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH. Biochem J 1998, 333(Pt. 1):167-174.
14. Broer S., Broer A., Schneider H.P., Stegen C., Halestrap A.P., Deitmer J.W. Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem J 1999, 341(Pt. 3):529-535.
15. Brooks G.A. Current concepts in lactate exchange. Med Sci Sports Exerc 1991, 23:895-906.
16. Brown A.M., Tekkok S.B., Ransom B.R. Glycogen regulation and functional role in mouse white matter. J Physiol 2003, 549:501-512.
17. Brown A.M., Baltan T.S., Ransom B.R. Energy transfer from astrocytes to axons: the role of CNS glycogen. Neurochem Int 2004, 45:529-536.
18. Brown A.M., Sickmann H.M., Fosgerau K., Lund T.M., Schousboe A., Waagepetersen H.S., Ransom B.R. Astrocyte glycogen metabolism is required for neural activity during aglycemia or intense stimulation in mouse white matter. J Neurosci Res 2005, 79:74-80.
19. Brown A.M., Evans R.D., Black J., Ransom B.R. Schwann cell glycogen selectively supports myelinated axon function. Ann Neurol 2012, 72:406-418.
20. Cai T.Q., Ren N., Jin L., Cheng K., Kash S., Chen R., Wright S.D., Taggart A.K., Waters M.G. Role of GPR81 in lactate-mediated reduction of adipose lipolysis. Biochem Biophys Res Commun 2008, 377:987-991.
21. Cataldo A.M., Broadwell R.D. Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J Neurocytol 1986, 15:511-524.
22. Cavaliere F., Urra O., Alberdi E., Matute C. Oligodendrocyte differentiation from adult multipotent stem cells is modulated by glutamate. Cell Death Dis 2012, 3:e268.
23. Cavalieri M., Schmidt H., Schmidt R. Structural MRI in normal aging and Alzheimer's disease: white and black spots. Neurodegener Dis 2012, 10:253-256.
24. Chrast R., Saher G., Nave K.A., Verheijen M.H. Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J Lipid Res 2011, 52:419-434.
25. Cloutier M., Bolger F.B., Lowry J.P., Wellstead P. An integrative dynamic model of brain energy metabolism using in vivo neurochemical measurements. J Comput Neurosci 2009, 27:391-414.
26. Dalsgaard M.K., Quistorff B., Danielsen E.R., Selmer C., Vogelsang T., Secher N.H. A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J Physiol 2004, 554:571-578.
27. Desagher S., Glowinski J., Premont J. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J Neurosci 1997, 17:9060-9067.
28. Dienel G.A. Brain lactate metabolism: the discoveries and the controversies. J Cereb Blood Flow Metab 2012, 32:1107-1138.
29. Dienel GA (2012b) Fueling and imaging brain activation. ASN Neuro. [Epub ahead of print].
30. Dringen R., Gebhardt R., Hamprecht B. Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 1993, 623:208-214.
31. Dringen R., Wiesinger H., Hamprecht B. Uptake of L-lactate by cultured rat brain neurons. Neurosci Lett 1993, 163:5-7.
32. Fern R., Möller T. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 2000, 20:34-42.
33. Follett P.L., Rosenberg P.A., Volpe J.J., Jensen F.E. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 2000, 20:9235-9241.
34. Foster P.C., Bailey E. Changes in hepatic fatty acid degradation and blood lipid and ketone body content during development of the rat. Enzyme 1976, 21:397-407.
35. Fu Y., Sun W., Shi Y., Shi R., Cheng J.X. Glutamate excitotoxicity inflicts paranodal myelin splitting and retraction. PLoS One 2009, 4:e6705.
36. Funfschilling U., Supplie L.M., Mahad D., Boretius S., Saab A.S., Edgar J., Brinkmann B.G., Kassmann C.M., Tzvetanova I.D., Mobius W., Diaz F., Meijer D., Suter U., Hamprecht B., Sereda M.W., Moraes C.T., Frahm J., Goebbels S., Nave K.A. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
37. Garcia C.K., Li X., Luna J., Francke U. CDNA cloning of the human monocarboxylate transporter 1 and chromosomal localization of the SLC16A1 locus to 1p13.2-p12. Genomics 1994, 23:500-503.
38. Garcia C.K., Brown M.S., Pathak R.K., Goldstein J.L. CDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J Biol Chem 1995, 270:1843-1849.
39. Gilles F.H. Myelination in the neonatal brain. Hum Pathol 1976, 7:244-248.
40. Gordon G.R., Choi H.B., Rungta R.L., Ellis-Davies G.C., MacVicar B.A. Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 2008, 456:745-749.
41. Grollman E.F., Philp N.J., McPhie P., Ward R.D., Sauer B. Determination of transport kinetics of chick MCT3 monocarboxylate transporter from retinal pigment epithelium by expression in genetically modified yeast. Biochemistry 2000, 39:9351-9357.
42. Gur R.C., Turetsky B.I., Matsui M., Yan M., Bilker W., Hughett P., Gur R.E. Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. J Neurosci 1999, 19:4065-4072.
43. Halestrap A.P., Price N.T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem J 1999, 343(Pt. 2):281-299.
44. Hanson R.W. Thematic minireview series: a perspective on the biology of phosphoenolpyruvate carboxykinase 55years after its discovery. J Biol Chem 2009, 284:27021-27023.
45. Hassel B. Pyruvate carboxylation in neurons. J Neurosci Res 2001, 66:755-762.
46. Hawkins R.A., Williamson D.H., Krebs H.A. Ketone-body utilization by adult and suckling rat brain in vivo. Biochem J 1971, 122:13-18.
47. Iacobas S., Thomas N.M., Iacobas D.A. Plasticity of the myelination genomic fabric. Mol Genet Genomics 2012, 287:237-246.
48. Karadottir R., Cavelier P., Bergersen L.H., Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 2005, 438:1162-1166.
49. Kassmann C.M., Lappe-Siefke C., Baes M., Brugger B., Mildner A., Werner H.B., Natt O., Michaelis T., Prinz M., Frahm J., Nave K.A. Axonal loss and neuroinflammation caused by peroxisome-deficient oligodendrocytes. Nat Genet 2007, 39:969-976.
50. Kinney H.C., Karthigasan J., Borenshteyn N.I., Flax J.D., Kirschner D.A. Myelination in the developing human brain: biochemical correlates. Neurochem Res 1994, 19:983-996.
51. Lauritzen KH, Morland C, Puchades M, Holm-Hansen S, Hagelin EM, Lauritzen F, Attramadal H, Storm-Mathisen J, Gjedde A, Bergersen LH (2013) Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism. Cereb Cortex. [Epub ahead of print].
52. Lee Y., Morrison B.M., Li Y., Lengacher S., Farah M.H., Hoffman P.N., Liu Y., Tsingalia A., Jin L., Zhang P.W., Pellerin L., Magistretti P.J., Rothstein J.D. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487:443-448.
53. Li S., Mealing G.A., Morley P., Stys P.K. Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport. J Neurosci 1999, 19:RC16.
54. Liu C., Wu J., Zhu J., Kuei C., Yu J., Shelton J., Sutton S.W., Li X., Yun S.J., Mirzadegan T., Mazur C., Kamme F., Lovenberg T.W. Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81. J Biol Chem 2009, 284:2811-2822.
55. Magistretti P.J., Pellerin L. Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol Sci 1999, 14:177-182.
56. Malone M., Gary D., Yang I.H., Miglioretti A., Houdayer T., Thakor N., McDonald J. Neuronal activity promotes myelination via a cAMP pathway. Glia 2013, 61:843-854.
57. Mangia S., Simpson I.A., Vannucci S.J., Carruthers A. The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation. J Neurochem 2009, 109(Suppl. 1):55-62.
58. Mangia S., DiNuzzo M., Giove F., Carruthers A., Simpson I.A., Vannucci S.J. Response to 'comment on recent modeling studies of astrocyte-neuron metabolic interactions': much ado about nothing. J Cereb Blood Flow Metab 2011, 31:1346-1353.
59. Manning S.M., Talos D.M., Zhou C., Selip D.B., Park H.K., Park C.J., Volpe J.J., Jensen F.E. NMDA receptor blockade with memantine attenuates white matter injury in a rat model of periventricular leukomalacia. J Neurosci 2008, 28:6670-6678.
60. Manning Fox J.E., Meredith D., Halestrap A.P. Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J Physiol 2000, 529(Pt. 2):285-293.
61. McClelland G.B., Khanna S., Gonzalez G.F., Butz C.E., Brooks G.A. Peroxisomal membrane monocarboxylate transporters: evidence for a redox shuttle system?. Biochem Biophys Res Commun 2003, 304:130-135.
62. Micu I., Jiang Q., Coderre E., Ridsdale A., Zhang L., Woulfe J., Yin X., Trapp B.D., McRory J.E., Rehak R., Zamponi G.W., Wang W., Stys P.K. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 2006, 439:988-992.
63. Nave K.A. Myelination and the trophic support of long axons. Nat Rev Neurosci 2010, 11:275-283.
64. Nehlig A., Pereira de Vasconcelos A. Glucose and ketone body utilization by the brain of neonatal rats. Prog Neurobiol 1993, 40:163-221.
65. Ouardouz M., Coderre E., Basak A., Chen A., Zamponi G.W., Hameed S., Rehak R., Yin X., Trapp B.D., Stys P.K. Glutamate receptors on myelinated spinal cord axons: I. GluR6 kainate receptors. Ann Neurol 2009, 65:151-159.
66. Ouardouz M., Coderre E., Zamponi G.W., Hameed S., Yin X., Trapp B.D., Stys P.K. Glutamate receptors on myelinated spinal cord axons: II. AMPA and GluR5 receptors. Ann Neurol 2009, 65:160-166.
67. Pantoni L., Garcia J.H., Gutierrez J.A. Cerebral white matter is highly vulnerable to ischemia. Stroke 1996, 27:1641-1646.
68. Pasinelli P., Belford M.E., Lennon N., Bacskai B.J., Hyman B.T., Trotti D., Brown R.H. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 2004, 43:19-30.
69. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 1994, 91:10625-10629.
70. Pellerin L., Magistretti P.J. Excitatory amino acids stimulate aerobic glycolysis in astrocytes via an activation of the Na+/K+ ATPase. Dev Neurosci 1996, 18:336-342.
71. Pellerin L., Pellegri G., Bittar P.G., Charnay Y., Bouras C., Martin J.L., Stella N., Magistretti P.J. Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 1998, 20:291-299.
72. Peter A., Palay SL, Webster H (1991) The fine structure of the nervous system. 3rd ed. Oxford University Press.
73. Philp N.J., Yoon H., Lombardi L. Mouse MCT3 gene is expressed preferentially in retinal pigment and choroid plexus epithelia. Am J Physiol Cell Physiol 2001, 280:C1319-C1326.
74. Rafiki A., Boulland J.L., Halestrap A.P., Ottersen O.P., Bergersen L. Highly differential expression of the monocarboxylate transporters MCT2 and MCT4 in the developing rat brain. Neuroscience 2003, 122:677-688.
75. Rinholm J.E., Bergersen L.H. Neuroscience: the wrap that feeds neurons. Nature 2012, 487:435-436.
76. Rinholm J.E., Hamilton N.B., Kessaris N., Richardson W.D., Bergersen L.H., Attwell D. Regulation of oligodendrocyte development and myelination by glucose and lactate. J Neurosci 2011, 31:538-548.
77. Salter M.G., Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 2005, 438:1167-1171.
78. Sanchez-Abarca L.I., Tabernero A., Medina J.M. Oligodendrocytes use lactate as a source of energy and as a precursor of lipids. Glia 2001, 36:321-329.
79. Simpson I.A., Carruthers A., Vannucci S.J. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 2007, 27:1-26.
80. Snell K., Walker D.G. Glucose metabolism in the newborn rat. Temporal studies in vivo. Biochem J 1973, 132:739-752.
81. Sokoloff L. The brain as a chemical machine. Prog Brain Res 1992, 94:19-33.
82. Suzuki A., Stern S.A., Bozdagi O., Huntley G.W., Walker R.H., Magistretti P.J., Alberini C.M. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 2011, 144:810-823.
83. Tekkok S.B., Goldberg M.P. AMPA/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 2001, 21:4237-4248.
84. Tekkok S.B., Brown A.M., Westenbroek R., Pellerin L., Ransom B.R. Transfer of glycogen-derived lactate from astrocytes to axons via specific monocarboxylate transporters supports mouse optic nerve activity. J Neurosci Res 2005, 81:644-652.
85. Traynelis S.F., Cull-Candy S.G. Pharmacological properties and H+ sensitivity of excitatory amino acid receptor channels in rat cerebellar granule neurones. J Physiol 1991, 433:727-763.
86. Van den Branden C., Leeman J., Dacremont G., Collumbien R., Roels F. Experimental inhibition of peroxisomal beta-oxidation in rats: influence on brain myelination. Glia 1990, 3:458-463.
87. Wake H., Lee P.R., Fields R.D. Control of local protein synthesis and initial events in myelination by action potentials. Science 2011, 333:1647-1651.
88. Werner H.B., Kuhlmann K., Shen S., Uecker M., Schardt A., Dimova K., Orfaniotou F., Dhaunchak A., Brinkmann B.G., Mobius W., Guarente L., Casaccia-Bonnefil P., Jahn O., Nave K.A. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 2007, 27:7717-7730.
89. Wilson M.C., Jackson V.N., Heddle C., Price N.T., Pilegaard H., Juel C., Bonen A., Montgomery I., Hutter O.F., Halestrap A.P. Lactic acid efflux from white skeletal muscle is catalyzed by the monocarboxylate transporter isoform MCT3. J Biol Chem 1998, 273:15920-15926.
90. Wu M., Hernandez M., Shen S., Sabo J.K., Kelkar D., Wang J., O'Leary R., Phillips G.R., Cate H.S., Casaccia P. Differential modulation of the oligodendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. J Neurosci 2012, 32:6651-6664.
91. Yoon H., Fanelli A., Grollman E.F., Philp N.J. Identification of a unique monocarboxylate transporter (MCT3) in retinal pigment epithelium. Biochem Biophys Res Commun 1997, 234:90-94.