Cellular distribution of glucose and monocarboxylate transporters in human brain white matter and multiple sclerosis lesions

GLIA

Volumn 62, Issue 7, 2014, Pages 1125-1141

  Nijland, Philip G ^a   Michailidou, Iliana ^a   Witte, Maarten E ^a   Mizee, Mark R ^a   Van Der Pol, Susanne M A ^a   Van Het Hof, Bert ^a   Reijerkerk, Arie ^a   Pellerin, Luc ^b   van der Valk, Paul ^a   de Vries, Helga E ^a   van Horssen, Jack ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Neurodegeneration; Nutrient transporters; Proliferator activated receptor gamma co activator 1 alpha; Reactive astrocytes

Indexed keywords

GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 3; MONOCARBOXYLATE TRANSPORTER; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; GLUTAMATE TRANSPORTER; PPARGC1A PROTEIN, HUMAN; SLC16A7 PROTEIN, HUMAN; SLC2A3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; AGED; ARTICLE; ASTROCYTE; BRAIN CELL; BRAIN DAMAGE; BRAIN TISSUE; CELL INFILTRATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENERGY METABOLISM; ENERGY RESOURCE; FEMALE; GENE OVEREXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEUKOCYTE; MALE; MICROGLIA; MIDDLE AGED; MULTIPLE SCLEROSIS; NERVE FIBER; NUTRIENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; VERY ELDERLY; WHITE MATTER; WHITE MATTER LESION; BRAIN; CELL LINE; METABOLISM; PATHOLOGY; VASCULARIZATION;

ADULT; AGED; AGED, 80 AND OVER; ASTROCYTES; AXONS; BRAIN; CELL LINE; ENDOTHELIAL CELLS; FEMALE; GLUCOSE TRANSPORTER TYPE 3; GLUTAMATE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; LEUKOCYTES; MALE; MICROGLIA; MIDDLE AGED; MONOCARBOXYLIC ACID TRANSPORTERS; MULTIPLE SCLEROSIS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; TRANSCRIPTION FACTORS; WHITE MATTER;

EID: 84900815561     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22667     Document Type: Article

References (74)

1. Argaw AT, Zhang Y, Snyder BJ, Zhao ML, Kopp N, Lee SC, Raine CS, Brosnan CF, John GR. 2006. IL-1 beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J Immunol 177:5574-5584.
2. Bakirtzi K, Belfort G, Lopez-Coviella I, Kuruppu D, Cao L, Abel ED, Brownell AL, Kandror KV. 2009. Cerebellar neurons possess a vesicular compartment structurally and functionally similar to glut4-storage vesicles from peripheral insulin-sensitive tissues. J Neurosci 29:5193-5201.
3. Bélanger M, Allaman I, Magistretti PJ. 2011. Differential effects of pro- and anti-inflammatory cytokines alone or in combinations on the metabolic profile of astrocytes. J Neurochem 116:564-576.
4. Benton CR, Holloway GP, Han XX, Yoshida Y, Snook LA, Lally J, Glatz JFC, Luiken JJFP, Chabowski A, Bonen A. 2010. Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1 alpha) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats. Diabetologia 53:2008-2019.
5. Benton CR, Yoshida Y, Lally J, Han XX, Hatta H, Bonen A. 2008. PGC-1 alpha increases skeletal muscle lactate uptake by increasing the expression of MCT1 but not MCT2 or MCT4. Physiol Genomics 35:45-54.
6. Bonetti B, Stegagno C, Cannella B, Rizzuto N, Moretto G, Raine CS. 1999. Activation of NF-kB and c-jun transcription factors in multiple sclerosis lesions: Implications for oligodendrocyte pathology. Am J Pathol 155:1433-1438.
7. Bouzier-Sore AK, Merle M, Magistretti PJ, Pellerin L. 2002. Feeding active neurons: (Re)emergence of a nursing role for astrocytes. J Physiol Paris 96:273-282.
8. Bouzier-Sore AK, Voisin P, Canioni P, Magistretti PJ, Pellerin L. 2003. Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 23:1298-1306.
9. Chiry O, Fishbein WN, Merezhinskaya N, Clarke Sp, Galuske R, Magistretti PJ, Pellerin L. 2008. Distribution of the monocarboxylate transporter MCT2 in human cerebral cortex: An immunohistochemical study. Brain Res 1226:61-69.
10. Chiry O, Pellerin L, Monnet-Tschudi F, Fishbein WN, Merezhinskaya N, Magistretti PJ, Clarke Sp. 2006. Expression of the monocarboxylate transporter MCT1 in the adult human brain cortex. Brain Res 1070:65-70.
11. Cidad P, Garcia-Nogales P, Almeida A, Bolanos JP. 2001. Expression of glucose transporter GLUT3 by endotoxin in cultured rat astrocytes: The role of nitric oxide. J Neurochem 79:17-24.
12. Cowell RM, Talati P, Blake KR, Meador-Woodruff JH, Russell JW. 2009. Identification of novel targets for PGC-1alpha and histone deacetylase inhibitors in neuroblastoma cells. Biochem Biophys Res Commun 379:578-582.
13. De Groot CJ, Langeveld CH, Jongenelen CA, Montagne L, van der Valk P, Dijkstra CD. 1997. Establishment of human adult astrocyte cultures derived from postmortem multiple sclerosis and control brain and spinal cord regions: Immunophenotypical and functional characterization. J Neurosci Res 49:342-354.
14. De Groot CJ, Montagne L, Janssen I, Ravid R, van der Valk P, Veerhuis R. 2000. Isolation and characterization of adult microglial cells and oligodendrocytes derived from postmortem human brain tissue. Brain Res Brain Res Protoc 5:85-94.
15. Dinuzzo M, Mangia S, Maraviglia B, Giove F. 2010. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: Evidence from mathematical modeling. J Cereb Blood Flow Metab 30:586-602.
16. Doorn R, Nijland P, Dekker N, Witte M, Lopes-Pinheiro M, het Hof B, Kooij G, Reijerkerk A, Dijkstra C, Valk P, Horssen J, Vries H. 2012. Fingolimod attenuates ceramide-induced bloodGÇôbrain barrier dysfunction in multiple sclerosis by targeting reactive astrocytes. Acta Neuropathol 124:397-410.
17. Duelli R, Kuschinsky W. 2001. Brain glucose transporters: Relationship to local energy demand. Physiology 16:71-76.
18. El Messari Sd, Leloup C, Quignon M, Brisorgueil MJ, Penicaud L, Arluison M. 1998. Immunocytochemical localization of the insulin-responsive glucose transporter 4 (Glut4) in the rat central nervous system. J Comp Neurol 399:492-512.
19. Escartin C, Valette J, Lebon V, Bonvento G. 2006. NeuronGÇôastrocyte interactions in the regulation of brain energy metabolism: A focus on NMR spectroscopy. J Neurochem 99:393-401.
20. Frohman EM, Racke MK, Raine CS. 2006. Multiple sclerosis--the plaque and its pathogenesis. N Engl J Med 354:942-955.
21. 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.
22. Gallagher CN, Carpenter KLH, Grice P, Howe DJ, Mason A, Timofeev I, Menon DK, Kirkpatrick PJ, Pickard JD, Sutherland GR, Hutchinson PJ. 2009. The human brain utilizes lactate via the tricarboxylic acid cycle: A 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132:2839-2849.
23. Gavillet M, Allaman I, Magistretti PJ. 2008. Modulation of astrocytic metabolic phenotype by proinflammatory cytokines. Glia 56:975-989.
24. Gerhart DZ, Broderius MA, Borson ND, Drewes LR. 1992. Neurons and microvessels express the brain glucose transporter protein GLUT3. Proc Natl Acad Sci USA 89:733-737.
25. Gerhart DZ, Enerson BE, Zhdankina OY, Leino RL, Drewes LR. 1998. Expression of the monocarboxylate transporter MCT2 by rat brain glia. Glia 22:272-281.
26. Gveric D, Kaltschmidt C, Cuzner ML, Newcombe J. 1998. Transcription factor NF-kB and inhibitor kB[alpha] are localized in macrophages in active multiple sclerosis lesions. J Neuropathol Exp Neurol 57:168-178.
27. Halestrap AP. 2012. The monocarboxylate transporter family--structure and functional characterization. IUBMB Life 64:1-9.
28. Halestrap AP, Price NT. 1999. The proton-linked monocarboxylate transporter (MCT) family: Structure, function and regulation. Biochem J 343 (Pt 2):281-299.
29. Hanu R, Mckenna M, O'neill A, Resneck WG, Bloch RJ. 2000. Monocarboxylic acid transporters, MCT1 and MCT2, in cortical astrocytes in vitro and in vivo. Am J Physiol Cell Physiol 278:C921-C930.
30. Hock MB, Kralli A. 2009. Transcriptional control of mitochondrial biogenesis and function. Annu Rev Physiol 71:177-203.
31. Iwabuchi S, Kawahara K. 2011. Inducible astrocytic glucose transporter-3 contributes to the enhanced storage of intracellular glycogen during reperfusion after ischemia. Neurochem Int 59:319-325.
32. Kooi EJ, Prins M, Bajic N, Belien JA, Gerritsen WH, van HJ, Aronica E, van Dam AM, Hoozemans JJ, Francis PT, Van D, V, Geurts JJ. 2011. Cholinergic imbalance in the multiple sclerosis hippocampus. Acta Neuropathol 122:313-322.
33. Lassmann H, van Horssen J, Mahad D. 2012. Progressive multiple sclerosis: Pathology and pathogenesis. Nat Rev Neurol 8:647-656.
34. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD. 2012. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443-448.
35. Leino RL, Gerhart DZ, Drewes LR. 1999. Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: A quantitative electron microscopic immunogold study. Brain Res Dev Brain Res 113:47-54.
36. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. 2004. A syntaxin 1, galpha-o, and N-type calcium channel complex at a presynaptic nerve terminal: Analysis by quantitative immunocolocalization. J Neurosci 24:4070-4081.
37. Lucchinetti C, Bruck W, Noseworthy J. 2001. Multiple sclerosis: Recent developments in neuropathology, pathogenesis, magnetic resonance imaging studies and treatment. Curr Opin Neurol 14:259-269.
38. Mahad DJ, Ziabreva I, Campbell G, Lax N, White K, Hanson PS, Lassmann H, Turnbull DM. 2009. Mitochondrial changes within axons in multiple sclerosis. Brain 132:1161-1174.
39. Maher F. 1995. Immunolocalization of GLUT1 and GLUT3 glucose transporters in primary cultured neurons and glia. J Neurosci Res 42:459-469.
40. Maher F, Davies-Hill TM, Simpson IA. 1996. Substrate specificity and kinetic parameters of GLUT3 in rat cerebellar granule neurons. Biochem J 315( Pt 3):827-831.
41. Miura S, Kai Y, Ono M, Ezaki O. 2003. Overexpression of peroxisome proliferator-activated receptor coactivator-1alpha down-regulates GLUT4 mRNA in skeletal muscles. J Biol Chem 278:31385-31390.
42. Moll C, Mourre C, Lazdunski M, Ulrich J. 1991. Increase of sodium channels in demyelinated lesions of multiple sclerosis. Brain Res 556:311-316.
43. Moreira TJ, Pierre K, Maekawa F, Repond C, Cebere A, Liljequist S, Pellerin L. 2009. Enhanced cerebral expression of MCT1 and MCT2 in a rat ischemia model occurs in activated microglial cells. J Cereb Blood Flow Metab 29:1273-1283.
44. Morgello S, Uson RR, Schwartz EJ, Haber RS. 1995. The human blood-brain barrier glucose transporter (GLUT1) is a glucose transporter of gray matter astrocytes. Glia 14:43-54.
45. Ngarmukos C, Baur EL, Kumagai AK. 2001. Co-localization of GLUT1 and GLUT4 in the bloodGÇôbrain barrier of the rat ventromedial hypothalamus. Brain Res 900:1-8.
46. Nikolic N, Rhedin M, Rustan AC, Storlien L, Thoresen GH, Stromstedt M. 2012. Overexpression of PGC-1α increases fatty acid oxidative capacity of human skeletal muscle cells. Biochem Res Int 2012:714074.
47. Pellerin L, 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.
48. 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 91:10625-10629.
49. Pellerin L, Pellegri G, Martin JL, Magistretti PJ. 1998. Expression of monocarboxylate transporter mRNAs in mouse brain: Support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc Natl Acad Sci USA 95:3990-3995.
50. Pierre K, Pellerin L. 2005. Monocarboxylate transporters in the central nervous system: Distribution, regulation and function. J Neurochem 94:1-14.
51. Pierre K, Pellerin L, Debernardi R, Riederer BM, Magistretti PJ. 2000. Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience 100:617-627.
52. Rafiki A, Boulland JL, Halestrap AP, Ottersen OP, Bergersen L. 2003. Highly differential expression of the monocarboxylate transporters MCT2 and MCT4 in the developing rat brain. Neuroscience 122:677-688.
53. Reijerkerk A, Lopez-Ramirez MA, van het Hof B, Drexhage JAR, Kamphuis WW, Kooij G, Vos JB, van der Pouw Kraan T, van Zonneveld AJ, Horrevoets AJ, Prat A, Romero IA, de Vries HE. 2013. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: Implications for multiple sclerosis. J Neurosci 33:6857-6863.
54. 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 31:538-548.
55. Schiepers C, Van Hecke P, Vandenberghe R, Van Oostende S, Dupont P, Demaerel P, Bormans G, Carton H. 1997. Positron emission tomography, magnetic resonance imaging and proton NMR spectroscopy of white matter in multiple sclerosis. Mult Scler 3:8-17.
56. Schocke MFH, Berger T, Felber SR, Wolf C, Deisenhammer F, Kremser C, Seppi K, Aichner FT. 2003. Serial contrast-enhanced magnetic resonance imaging and spectroscopic imaging of acute multiple sclerosis lesions under high-dose methylprednisolone therapy. NeuroImage 20:1253-1263.
57. Simpson IA, Carruthers A, Vannucci SJ. 2007. Supply and demand in cerebral energy metabolism: The role of nutrient transporters. J Cereb Blood Flow Metab 27:1766-1791.
58. Simpson IA, Chundu KR, Davies-Hill T, Honer WG, Davies P. 1994. Decreased concentrations of GLUT1 and GLUT3 glucose transporters in the brains of patients with Alzheimer's disease. Ann Neurol 35:546-551.
59. Stadelmann C, Ludwin S, Tabira T, Guseo A, Lucchinetti CF, Leel-Ossy L, Ordinario AT, Bruck W, Lassmann H. 2005. Tissue preconditioning may explain concentric lesions in Balo's type of multiple sclerosis. Brain 128:979-987.
60. Suzuki, Akinobu, Stern, SaraháA, Bozdagi, Ozlem, Huntley, GeorgeáW, Walker, RutháH, Magistretti, PierreáJ, and Alberini, CristinaáM. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144 810-823.
61. Tekkök 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.
62. Trapp BD, Nave KA. 2008. Multiple sclerosis: An immune or neurodegenerative disorder? Annu Rev Neurosci 31:247-269.
63. Trapp BD, Stys PK. 2009. Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol 8:280-291.
64. 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 29:1121-1129.
65. Vega C, Sachleben R, Gozal D, Gozal E. 2006. Differential metabolic adaptation to acute and long-term hypoxia in rat primary cortical astrocytes. J Neurochem 97:872-883.
66. Walz W, Mukerji S. 1988. Lactate release from cultured astrocytes and neurons: A comparison. Glia 1:366-370.
67. Weisová P, Concannon CnG, Devocelle M, Prehn JHM, Ward MW. 2009. Regulation of glucose transporter 3 surface expression by the AMP-activated protein kinase mediates tolerance to glutamate excitation in neurons. J Neurosci 29:2997-3008.
68. Wilhelmus MMM, van der Pol SMA, Jansen Q, Witte ME, van der Valk P, Rozemuller AJM, Drukarch B, de Vries HE, van Horssen J. 2011. Association of Parkinson disease-related protein PINK1 with Alzheimer disease and multiple sclerosis brain lesions. Free Radic Biol Med 50:469-476.
69. Witte ME, Bo L, Rodenburg RJ, Belien JA, Musters R, Hazes T, Wintjes LT, Smeitink JA, Geurts JJ, De Vries HE, Van D, V, van HJ. 2009a. Enhanced number and activity of mitochondria in multiple sclerosis lesions. J Pathol 219:193-204.
70. Witte M, Nijland P, Drexhage J, Gerritsen W, Geerts D, het Hof B, Reijerkerk A, Vries H, Valk P, Horssen J. 2013. Reduced expression of PGC-1alpha partly underlies mitochondrial changes and correlates with neuronal loss in multiple sclerosis cortex. Acta Neuropathol 125:231-243.
71. Witte ME, Bol JG, Gerritsen WH, Valk Pvd, Drukarch B, Horssen Jv, Wilhelmus MM. 2009b. Parkinson's disease-associated parkin colocalizes with Alzheimer's disease and multiple sclerosis brain lesions. Neurobiol Dis 36:445-452.
72. Witte ME, Geurts JJG, de Vries HE, van der Valk P, van Horssen J. 2010. Mitochondrial dysfunction: A potential link between neuroinflammation and neurodegeneration? Mitochondrion 10:411-418.
73. Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B. 2011. In vivo evidence for lactate as a neuronal energy source. J Neurosci 31:7477-7485.
74. Yu S, Ding WG. 1998. The 45 kDa form of glucose transporter 1 (GLUT1) is localized in oligodendrocyte and astrocyte but not in microglia in the rat brain. Brain Res 797:65-72.