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PMID: 12967982 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons.

Burkhalter J, Fiumelli H, Allaman I, Chatton JY, Martin JL

Abstract

Brain-derived neurotrophic factor (BDNF) promotes the biochemical and morphological differentiation of selective populations of neurons during development. In this study we examined the energy requirements associated with the effects of BDNF on neuronal differentiation. Because glucose is the preferred energy substrate in the brain, the effect of BDNF on glucose utilization was investigated in developing cortical neurons via biochemical and imaging studies. Results revealed that BDNF increases glucose utilization and the expression of the neuronal glucose transporter GLUT3. Stimulation of glucose utilization by BDNF was shown to result from the activation of Na+/K+-ATPase via an increase in Na+ influx that is mediated, at least in part, by the stimulation of Na+-dependent amino acid transport. The increased Na+-dependent amino acid uptake by BDNF is followed by an enhancement of overall protein synthesis associated with the differentiation of cortical neurons. Together, these data demonstrate the ability of BDNF to stimulate glucose utilization in response to an enhanced energy demand resulting from increases in amino acid uptake and protein synthesis associated with the promotion of neuronal differentiation by BDNF.

MeSH Terms
Amino Acids/metabolism,pharmacokinetics Animals Biological Transport/drug effects Brain-Derived Neurotrophic Factor/pharmacology Cells, Cultured Cerebral Cortex/cytology,embryology,metabolism Deoxyglucose/pharmacokinetics Energy Metabolism/drug effects Glucose/metabolism,pharmacokinetics Glucose Transporter Type 3 Kinetics Mice Monosaccharide Transport Proteins/genetics,metabolism Nerve Tissue Proteins Neurons/cytology,drug effects,metabolism Neuropeptide Y/biosynthesis Protein Biosynthesis RNA, Messenger/metabolism Sodium/metabolism Sodium-Potassium-Exchanging ATPase/metabolism
Chemicals
Amino Acids Brain-Derived Neurotrophic Factor Glucose Transporter Type 3 Monosaccharide Transport Proteins Nerve Tissue Proteins Neuropeptide Y RNA, Messenger Slc2a3 protein, mouse Deoxyglucose Sodium Sodium-Potassium-Exchanging ATPase Glucose
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Burkhalter Julia
Institute of Physiology, Faculty of Medicine, University of Lausanne, CH-1005 Lausanne, Switzerland.
Fiumelli Hubert
Allaman Igor
Chatton Jean-Yves
Martin Jean-Luc
References (55)
55 references, click to expand
  1. Developmental regulation of genes mediating murine brain glucose uptake.
    Am J Physiol. 1999 Mar;276(3):R892-900 PMID: 10070152
  2. Neurotrophin regulation of synaptic transmission.
    Curr Opin Neurobiol. 1999 Feb;9(1):105-9 PMID: 10072368
  3. Neurotrophins and synaptic plasticity.
    Annu Rev Neurosci. 1999;22:295-318 PMID: 10202541
  4. Monocular deprivation decreases brain-derived neurotrophic factor immunoreactivity in the rat visual cortex.
    Neuroscience. 1999 May;90(2):363-8 PMID: 10215141
  5. BDNF stimulates expression, activity and release of tissue-type plasminogen activator in mouse cortical neurons.
    Eur J Neurosci. 1999 May;11(5):1639-46 PMID: 10215917
  6. Neurotrophin-evoked rapid excitation through TrkB receptors.
    Nature. 1999 Oct 28;401(6756):918-21 PMID: 10553907
  7. Opposite regulation of calbindin and calretinin expression by brain-derived neurotrophic factor in cortical neurons.
    J Neurochem. 2000 May;74(5):1870-7 PMID: 10800929
  8. A quantitative analysis of L-glutamate-regulated Na+ dynamics in mouse cortical astrocytes: implications for cellular bioenergetics.
    Eur J Neurosci. 2000 Nov;12(11):3843-53 PMID: 11069579
  9. CNS energy metabolism as related to function.
    Brain Res Brain Res Rev. 2000 Nov;34(1-2):42-68 PMID: 11086186
  10. Mismatch between BDNF mRNA and protein expression in the developing visual cortex: the role of visual experience.
    Eur J Neurosci. 2001 Feb;13(4):709-21 PMID: 11207806
  11. Recent molecular advances in mammalian glutamine transport.
    J Nutr. 2001 Sep;131(9 Suppl):2475S-85S; discussion 2486S-7S PMID: 11533296
  12. An energy budget for signaling in the grey matter of the brain.
    J Cereb Blood Flow Metab. 2001 Oct;21(10):1133-45 PMID: 11598490
  13. Immunolocalization of GLUTX1 in the testis and to specific brain areas and vasopressin-containing neurons.
    Endocrinology. 2002 Jan;143(1):276-84 PMID: 11751619
  14. Insulin promotes the cell surface recruitment of the SAT2/ATA2 system A amino acid transporter from an endosomal compartment in skeletal muscle cells.
    J Biol Chem. 2002 Apr 19;277(16):13628-34 PMID: 11834730
  15. Neurotrophin-evoked depolarization requires the sodium channel Na(V)1.9.
    Nature. 2002 Oct 17;419(6908):687-93 PMID: 12384689
  16. Glucose transporter expression in brain. cDNA sequence of mouse GLUT3, the brain facilitative glucose transporter isoform, and identification of sites of expression by in situ hybridization.
    J Biol Chem. 1992 Jan 5;267(1):467-72 PMID: 1730609
  17. Expression of two glucose transporters, GLUT1 and GLUT3, in cultured cerebellar neurons: Evidence for neuron-specific expression of GLUT3.
    Mol Cell Neurosci. 1991 Aug;2(4):351-60 PMID: 19912819
  18. Effect of nerve growth factor on glucose utilization and nucleotide content of pheochromocytoma cells (clone PC12).
    J Neurochem. 1986 Aug;47(2):375-81 PMID: 3016173
  19. Neutral amino acid transport in astrocytes: characterization of Na+-dependent and Na+-independent components of alpha-aminoisobutyric acid uptake.
    J Neurochem. 1988 Dec;51(6):1913-8 PMID: 3053994
  20. Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development.
    J Neurosci. 1988 Jul;8(7):2321-33 PMID: 3249228
  21. Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography.
    Science. 1986 Feb 21;231(4740):840-3 PMID: 3945811
  22. Oxygen and glucose consumption related to Na+-K+ transport in canine brain.
    Stroke. 1981 Nov-Dec;12(6):726-30 PMID: 7303061
  23. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8856-60 PMID: 7568031
  24. Neurotrophins regulate dendritic growth in developing visual cortex.
    Neuron. 1995 Oct;15(4):791-803 PMID: 7576629
  25. Functional interactions of neurotrophins and neurotrophin receptors.
    Annu Rev Neurosci. 1995;18:223-53 PMID: 7605062
  26. NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway.
    Brain Res Dev Brain Res. 1995 May 26;86(1-2):326-34 PMID: 7656424
  27. Coupled glucose transport and metabolism in cultured neuronal cells: determination of the rate-limiting step.
    J Cereb Blood Flow Metab. 1995 Sep;15(5):814-26 PMID: 7673374
  28. The role of neurotrophins in the developing nervous system.
    J Neurobiol. 1994 Nov;25(11):1334-48 PMID: 7852989
  29. The Trk family of neurotrophin receptors.
    J Neurobiol. 1994 Nov;25(11):1386-403 PMID: 7852993
  30. Glucose transport in developing rat brain: glucose transporter proteins, rate constants and cerebral glucose utilization.
    Mol Cell Biochem. 1994 Nov 23;140(2):177-84 PMID: 7898489
  31. Glucose transporter proteins in brain.
    FASEB J. 1994 Oct;8(13):1003-11 PMID: 7926364
  32. Molecular physiology of sodium-glucose cotransporters.
    Physiol Rev. 1994 Oct;74(4):993-1026 PMID: 7938229
  33. Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF.
    Eur J Neurosci. 1994 Aug 1;6(8):1343-53 PMID: 7981876
  34. The GLUT3 glucose transporter is the predominant isoform in primary cultured neurons: assessment by biosynthetic and photoaffinity labelling.
    Biochem J. 1994 Jul 15;301 ( Pt 2):379-84 PMID: 8042980
  35. Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor.
    J Neurochem. 1993 Feb;60(2):772-5 PMID: 8093484
  36. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development.
    Cell. 1994 Mar 25;76(6):989-99 PMID: 8137432
  37. Developmental expression of GLUT1 and GLUT3 glucose transporters in rat brain.
    J Neurochem. 1994 Jan;62(1):240-6 PMID: 8263524
  38. pH, morphology, and diffusion in lateral intercellular spaces of epithelial cell monolayers.
    Am J Physiol. 1994 Jan;266(1 Pt 1):C73-80 PMID: 8304432
  39. Arachidonic acid stimulates glucose uptake in cerebral cortical astrocytes.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4042-6 PMID: 8483920
  40. Brain-derived neurotrophic factor induces functional expression and phenotypic differentiation of cultured fetal neuropeptide Y-producing neurons.
    J Neurosci Res. 1995 Dec;42(5):638-47 PMID: 8600296
  41. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat.
    J Neurochem. 1977 May;28(5):897-916 PMID: 864466
  42. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice.
    Neuron. 1996 Jun;16(6):1137-45 PMID: 8663990
  43. BDNF increases the expression of neuropeptide Y mRNA and promotes differentiation/maturation of neuropeptide Y-positive cultured cortical neurons from embryonic and postnatal rats.
    Brain Res Mol Brain Res. 1996 Apr;37(1-2):283-9 PMID: 8738162
  44. Physiology of the neurotrophins.
    Annu Rev Neurosci. 1996;19:289-317 PMID: 8833445
  45. Intracellular signaling pathways activated by neurotrophic factors.
    Annu Rev Neurosci. 1996;19:463-89 PMID: 8833451
  46. Monocular deprivation decreases the expression of messenger RNA for brain-derived neurotrophic factor in the rat visual cortex.
    Neuroscience. 1995 Dec;69(4):1133-44 PMID: 8848102
  47. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12547-52 PMID: 8901619
  48. Brain-derived neurotrophic factor increases the stimulation-evoked release of glutamate and the levels of exocytosis-associated proteins in cultured cortical neurons from embryonic rats.
    J Neurochem. 1997 Jan;68(1):370-5 PMID: 8978748
  49. Expression of the Na+-D-glucose cotransporter SGLT1 in neurons.
    J Neurochem. 1997 Jul;69(1):84-94 PMID: 9202297
  50. Glucose transporter proteins in brain: delivery of glucose to neurons and glia.
    Glia. 1997 Sep;21(1):2-21 PMID: 9298843
  51. Neuronal extracellular proteases facilitate cell migration, axonal growth, and pathfinding.
    Cell Tissue Res. 1997 Nov;290(2):367-70 PMID: 9321699
  52. Brain-derived neurotrophic factor stimulates phosphorylation of stathmin in cortical neurons.
    Brain Res Mol Brain Res. 1997 Nov;51(1-2):220-8 PMID: 9427524
  53. 2-Deoxyglucose transport by intestinal epithelial cells isolated from the chick.
    J Membr Biol. 1976 Jun 30;27(4):363-79 PMID: 966264
  54. Glucose transporter expression in brain: relationship to cerebral glucose utilization.
    Dev Neurosci. 1998;20(4-5):369-79 PMID: 9778574
  55. Molecular biology of mammalian plasma membrane amino acid transporters.
    Physiol Rev. 1998 Oct;78(4):969-1054 PMID: 9790568
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-09-10
Pages
8212-20
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6740684
Subset
IM
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