Immunocytochemical expression of monocarboxylate transporters in the human visual cortex at midgestation

Developmental Brain Research

Volumn 148, Issue 1, 2004, Pages 69-76

  Fayol, Laurence ^a   Baud, Olivier ^a   Monier, Anne ^a   Pellerin, Luc ^b   Magistretti, Pierre ^b   Evrard, Philippe ^a   Verney, Catherine ^a  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Astrocyte; Blood brain barrier; GLUT1; MCT; Neuron; Vessel

Indexed keywords

BIOLOGICAL MARKER; CD34 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MONOCARBOXYLATE TRANSPORTER; PEROXIDASE; PROTEIN S100B; VIMENTIN;

ARTICLE; ASTROCYTE; BLOOD VESSEL; BLOOD VESSEL WALL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FETUS; GESTATIONAL AGE; GLIA; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOPEROXIDASE STAINING; IMMUNOREACTIVITY; NERVE CELL; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION; VISUAL CORTEX;

EID: 0742324436     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devbrainres.2003.10.010     Document Type: Article

References (66)

1. Baud O., Fayol L., Evrard P., Verney C. Movements of energy substrates in the mammalian brain, with special emphasis on transporters during normal and pathological development. Neuroembryology. 1:2002;161-168.
2. Baud O., Fayol L., Gressens P., Pellerin L., Magistretti P., Evrard P., Verney C. Perinatal and early postnatal changes in the expression of monocarboxylate transporters MCT1 and MCT2 in the rat forebrain. J. Comp. Neurol. 465:2003;445-454.
3. Bergersen L., Waerhaug O., Helm J., Thomas M., Laake P., Dabvies A.J., Wilson M.C., Halestrap A.P., Otterson O.P. A novel postsynaptic density protein: The monocarboxylate transporter MCT2 is co-colocalized with delta-glutamate receptors in postsynaptic densities of parallel fiber_Purkinje cell synapses. Exp. Brain Res. 136:2001;523-534.
4. Bergersen L., Rafiki A., Otterson O.P. Immunogold cytochemistry identifies specialized membrane domains for monocarboxylate transport in the central nervous system. Neurochem. Res. 27:2002;89-96.
5. Bertossi M., Virgintino D., Errede M., Roncali L. Immunohistochemical and ultrastructural characterization of cortical plate microvasculature in the human fetus telencephalon. Microvasc. Res. 58:1999;49-61.
6. Bouzier-Sore A.K., Voisin P., Canioni P., Magistretti P.J., Pellerin L. Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J. Cereb. Blood Flow Metab. 23:2003;1298-1306.
7. Chan W.Y., Kostovic I., Takashima S., Feldhaus C., Stoltenburg-Didinger G., Verney C., Yew D., Ulfig N. Normal and abnormal development of the human cerebral cortex. Neuroembryology. 1:2002;78-90.
8. Debernardi R., Pierre K., Lengacher S., Magistretti P.J., Pellerin L. Cell-specific expression pattern of monocarboxylate transporters in astrocytes and neurons observed in different mouse brain cortical cell cultures. J. Neurosci. Res. 73:2003;141-155.
9. Deitmer J.W. Glial strategy for metabolic shuttling and neuronal function. Bioessays. 22:2000;747-752.
10. Dringen R., Gebhardt R., Hamprecht B. Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res. 623:1993;208-214.
11. Evrard P., Marret S., Gressens P. Environmental and genetic determinants of neural migration and postmigratory survival. Acta. Paediatr. Suppl. 422:1997;20-26.
12. Farell C.L., Pardridge W.M. Blood-brain barrier glucose transporter is asymmetrically distributed on brain capillary endothelial lumenal and ablumenal membranes: an electron microscopic immunogold study. Proc. Natl. Acad. Sci. U. S. A. 88:1991;5779-5783.
13. Fina L., Molgaard H.V., Robertson D., Bradley N.J., Monaghan P., Delia D., Sutherland D.R., Baker M.A., Greaves M.F. Expression of the CD34 gene in vascular endothelial cells. Blood. 75:1990;2417-2426.
14. Forsyth R., Fray A., Boutelle M., Fillenz M., Middleditch C., Burchel L.A. A role for astrocytes in glucose delivery to neurons? Dev. Neurosci. 18:1996;360-370.
15. Garcia C.K., Goldstein J.L., Pathak R.K., Anderson R.G., Brown M.S. Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates: implications for the Cori cycle. Cell. 76:1994;865-873.
16. Gerhart D.Z., Enerson B.E., Zhdankina O.Y., Leino R.L., Drewes L.R. Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am. J. Physiol. 273:1997;E207-E213.
17. Gerhart D.Z., Enerson B.E., Zhdankina O.Y., Leino R.L., Drewes L.R. Expression of the monocarboxylate transporter MCT2 by rat brain glia. Glia. 22:1998;272-281.
18. Gressens P., Richelme C., Kadhim H.J., Gadisseux J.F., Evrard P. The germinative zone produces the most cortical astrocytes after neuronal migration in the developing mammalian brain. Biol. Neonate. 61:1992;4-24.
19. Halestrap A.P., Price N.T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 343:1999;281-299.
20. Halestrap A.P., Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch. 2003;. May 9.
21. Hanu R., McKenna M., O'Neill A., Resneck W.G., Bloch R.J. Monocarboxylic acid transporters, MCT1 and MCT2, in cortical astrocytes in vitro and in vivo. Am. J. Physiol., Cell Physiol. 278:2000;C921-C930.
22. Honig L.S., Herrmann K., Shatz C.J. Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb. Cortex. 6:1996;794-806.
23. Hu Y., Wilson G.S. A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapid-response enzyme-based sensor. J. Neurochem. 69:1997;1484-1490.
24. Izumi Y., Benz A.M., Katsuki H., Zorumski C.F. Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J. Neurosci. 17:1997;9448-9457.
25. Kacem K., Lacombe P., Seylaz J., Bonvento G. Structural organization of the perivascular astrocyte end-feet and their relationship with the endothelial glucose transporter: a confocal microscopy study. Glia. 23:1998;1-10.
26. Kadhim H.J., Gadisseux J.F., Evrard P. Topographical and cytological evolution of the glial phase during prenatal development of the human brain: histochemical and electron microscopic study. J. Neuropathol. Exp. Neurol. 47:1988;166-188.
27. Kalhan S., Parimi P. Gluconeogenesis in the fetus and neonate. Semin. Perinatol. 24:2000;94-106.
28. Koehler-Stec E.M., Simpson I.A., Vannucci S.J., Landschulz K.T., Landschulz W.H. Monocarboxylate transporter expression in mouse brain. Am. J. Physiol. 275:1998;E516-E524.
29. Kostovic I., Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297:1990;441-470.
30. Larroche J.C. The fine structure of matrix capillaries in human embryos and young fetuses. The Second Special Ross Laboratory Conference on Perinatal Intracranial Haemorrhage. 1982;Laboratories Ross, Washington.
31. Leino R.L., Gerhart D.Z., Drewes L.R. Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: a quantitative electron microscopic immunogold study. Brain Res. Dev. Brain Res. 113:1999;47-54.
32. Magistretti P.J., Pellerin L., Rothman D.L., Shulman R.G. Energy on demand. Science. 283:1999;496-497.
33. Marin-Padilla M. Embryonic vascularization of the mammalian cerebral cortex. Peter E.J. Cerebral cortex. 1988;479-509 Plenum, New York.
34. Morgello S., Uson R.R., Schwartz E.J., Haber R.S. The human blood-brain barrier glucose transporter (GLUT1) is a glucose transporter of gray matter astrocytes. Glia. 14:1995;43-54.
35. Nakai A., Taniuchi Y., Asakura H., Oya A., Yokota A., Koshino T., Araki T. Developmental changes in mitochondrial activity and energy metabolism in fetal and neonatal rat brain. Brain Res. Dev. Brain Res. 121:2000;67-72.
36. Nakai Y., Hirayama A., Mizuguchi M., Takashima S. Changes of GLUT1 expression in normal and periventricular leukomalacia brains. Neuroembryology. 1:2002;141-143.
37. Nualart F., Godoy A., Reinicke K. Expression of the hexose transporters GLUT1 and GLUT2 during the early development of the human brain. Brain Res. 824:1999;97-104.
38. 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. 91:1994;10625-10629.
39. Pellerin L., Pellegri G., Martin J.L., Magistretti P.J. 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 U. S. A. 95:1998a;3990-3995.
40. Pellerin L., Pellegri G., Bittar P.G., Charnay Y., Bouras C., Stella N., Martin J.L., Magistretti P.J. Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20:1998b;291-299.
41. Pfrieger F.W., Barres B.A. New views on synapse-glia interactions. Curr. Opin. Neurobiol. 6:1996;615-621.
42. Pierre K., Pellerin L., Debernardi R., Riederer B.M., Magistretti P.J. Cell-specific localization of monocarboxylate transporters, MCT1 and MCT2, in the adult mouse brain revealed by double immunohistochemical labeling and confocal microscopy. Neuroscience. 100:2000;617-627.
43. Pierre K., Magistretti P.J., Pellerin L. MCT2 is a major neuronal monocarbocarboxylate transporter in the adult mouse brain. J. Cereb. Blood Flow. 22:2002;586-595.
44. Poitry-Yamate C.L., Poitry S., Tsacopoulos M. Lactate released by Muller glial cells is metabolized by photoreceptors from mammalian retina. J. Neurosci. 15:1995;5179-5191.
45. Prichard J., Rothman D., Novotny E., Petroff O., Kuwabara T., Avison M., Howseman A., Hanstock C., Shulman R. Lactate rise detected by 1H NMR in human visual cortex during physiologic stimulation. Proc. Natl. Acad. Sci. U. S. A. 88:1991;5829-5831.
46. Risau W., Wolburg H. Development of the blood-brain barrier. Trends Neurosci. 13:1990;174-178.
47. Rust R.S. Energy metabolism of developing brain. Curr. Opin. Neurosci. 7:1990;160-165.
48. Sato I., Konishi K., Mikami A., Sato T. Developmental changes in enzyme activities and in morphology of rat cortex mitochondria. Okajimas Folia Anat. Jpn. 6:2000;353-361.
49. Schurr A., Miller J.J., Payne R.S., Rigor B.M. An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons. J. Neurosci. 19:1999;34-39.
50. Schurr A., Payne R.S., Miller J.J., Tseng M.T., Rigor B.M. Blockade of lactate transport exacerbates delayed neuronal damage in a rat model of cerebral ischiemia. Brain Res. 895:2001;268-272.
51. Sibson N.R., Dhankhar A., Mason G.F., Rothman D.L., Behar K.L., Shulman R.G. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl. Acad. Sci. U. S. A. 95:1998;316-321.
52. Sokoloff L., Takahashi S., Gotoh J., Driscoll B.F., Law M.J. Contribution of astroglia to functionally activated energy metabolism. Dev. Neurosci. 18:1996;344-352.
53. Stagaard M., Mollgard K. The developing neuroepithelium in human embryonic and fetal brain studied with vimentin-immunocytochemistry. Anat. Embryol. (Berl.). 180:1989;17-28.
54. Sternberger L. The unlabeled antibody peroxydase-antiperoxydase (PAP) method. Immunocytochemistry. 1979;104-169 Wiley, New York.
55. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16:1996;877-885.
56. Ulfig N., Neudorfer F., Bohl J. Distribution patterns of vimentin-immunoreactive structures in the human prosencephalon during the second half of gestation. J. Anat. 195:1999;87-100.
57. Vannucci S.J., Seaman L.B., Brucklacher R.M., Vannucci R.C. Glucose transport in developing rat brain: glucose transporter proteins, rate constants and cerebral glucose utilization. Mol. Cell. Biochem. 140:1994;177-184.
58. Vannucci S.J., Maher F., Simpson I.A. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia. 21:1997;2-21.
59. Vannucci S.J., Clark R.R., Koehler-Stec E., Li K., Smith C.B., Davies P., Maher F., Simpson I.A. Glucose transporter expression in brain: relationship to cerebral glucose utilization. Dev. Neurosci. 20:1998;369-379.
60. Vannucci R.C., Vannucci S.J. Glucose metabolism in the developing brain. Semin. Perinatol. 24:2000;107-115.
61. Verney C., Alvarez C., Geffard M., Berger B. Ultrastructural double-labeling study of dopamine terminals and GABA-containing neurons in rat anteromedial cerbral cortex. Eur. J. Neurosci. 2:1990;960-972.
62. Verney C., Milosevic A., Alvarez C., Berger B. Immunocytochemical evidence of well-developed dopaminergic and noradrenergic innervations in the frontal cerebral cortex of human fetuses at midgestation. J. Comp. Neurol. 336:1993;331-344.
63. Virgintino D., Robertson D., Monaghan P., Errede M., Bertossi M., Ambrosi G., Roncali L. Glucose transporter GLUT1 in human brain microvessels revealed by ultrastructural immunocytochemistry. J. Submicrosc. Cytol. Pathol. 29:1997;365-370.
64. Virgintino D., Robertson D., Monaghan P., Errede M., Ambrosi G., Roncali L., Bertossi M. Glucose transporter GLUT1 localization in human foetus telencephalon. Neurosci. Lett. 256:1998;147-150.
65. Zerlin M., Goldman J.E. Interactions between glial progenitors and blood vessels during early postnatal corticogenesis: blood vessel contact represents an early stage of astrocyte differentiation. J. Comp. Neurol. 387:1997;537-546.
66. Zhang H., Sterberger N.H., Rubinsten L.I., Herman M.M., Binder L.I., Sterberger L.A. Abnormal processing of multiple proteins in Alzheimer disease. Proc. Natl. Acad. Sci. USA. 86:1989;8045-8049.