Home LiteratureArticle Details
PMID: 17913925 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Brain-derived neurotrophic factor expression and respiratory function improve after ampakine treatment in a mouse model of Rett syndrome.

Ogier M, Wang H, Hong E, Wang Q, Greenberg ME, Katz DM

Abstract

Rett syndrome (RTT) is caused by loss-of-function mutations in the gene encoding methyl-CpG-binding protein 2 (MeCP2). Although MeCP2 is thought to act as a transcriptional repressor of brain-derived neurotrophic factor (BDNF), Mecp2 null mice, which develop an RTT-like phenotype, exhibit progressive deficits in BDNF expression. These deficits are particularly significant in the brainstem and nodose cranial sensory ganglia (NGs), structures critical for cardiorespiratory homeostasis, and may be linked to the severe respiratory abnormalities characteristic of RTT. Therefore, the present study used Mecp2 null mice to further define the role of MeCP2 in regulation of BDNF expression and neural function, focusing on NG neurons and respiratory control. We find that mutant neurons express significantly lower levels of BDNF than wild-type cells in vitro, as in vivo, under both depolarizing and nondepolarizing conditions. However, BDNF levels in mutant NG cells can be increased by chronic depolarization in vitro or by treatment of Mecp2 null mice with CX546, an ampakine drug that facilitates activation of glutamatergic AMPA receptors. Ampakine-treated Mecp2 null mice also exhibit marked functional improvement, characterized by restoration of normal breathing frequency and minute volume. These data demonstrate that BDNF expression remains plastic in Mecp2 null mice and raise the possibility that ampakine compounds could be of therapeutic value in the treatment of RTT.

MeSH Terms
Analysis of Variance Anesthetics, Local/pharmacology Animals Animals, Newborn Brain-Derived Neurotrophic Factor/genetics,metabolism Cells, Cultured Depsipeptides/drug effects Dioxoles/therapeutic use Disease Models, Animal Gene Expression Regulation/drug effects,genetics Methyl-CpG-Binding Protein 2/genetics Mice Mice, Inbred C57BL Mice, Knockout Neurons/drug effects,metabolism Nodose Ganglion/cytology Piperidines/therapeutic use Plethysmography/methods RNA, Messenger/biosynthesis Rett Syndrome/drug therapy,physiopathology Reverse Transcriptase Polymerase Chain Reaction/methods Tetrodotoxin/pharmacology
Chemicals
1-(1,4-benzodioxan-6-ylcarbonyl)piperidine Anesthetics, Local Brain-Derived Neurotrophic Factor Depsipeptides Dioxoles Mecp2 protein, mouse Methyl-CpG-Binding Protein 2 Piperidines RNA, Messenger respirantin Tetrodotoxin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ogier Michael
Department of Neurosciences, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106, USA.
Wang Hong
Hong Elizabeth
Wang Qifang
Greenberg Michael E
Katz David M
References (36)
36 references, click to expand
  1. Facilitative effects of the ampakine CX516 on short-term memory in rats: enhancement of delayed-nonmatch-to-sample performance.
    J Neurosci. 1998 Apr 1;18(7):2740-7 PMID: 9502831
  2. Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ.
    J Neurosci. 2000 Oct 1;20(19):7417-23 PMID: 11007900
  3. Neuropathology of Rett syndrome.
    Ment Retard Dev Disabil Res Rev. 2002;8(2):72-6 PMID: 12112730
  4. Breathing dysfunctions associated with impaired control of postinspiratory activity in Mecp2-/y knockout mice.
    J Physiol. 2007 Mar 15;579(Pt 3):863-76 PMID: 17204503
  5. Enhancement by an ampakine of memory encoding in humans.
    Exp Neurol. 1997 Aug;146(2):553-9 PMID: 9270067
  6. Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons.
    J Neurosci. 2000 Jan 1;20(1):8-21 PMID: 10627576
  7. Dysregulation of brain-derived neurotrophic factor expression and neurosecretory function in Mecp2 null mice.
    J Neurosci. 2006 Oct 18;26(42):10911-5 PMID: 17050729
  8. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2.
    Nat Genet. 1999 Oct;23(2):185-8 PMID: 10508514
  9. Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor.
    J Neurophysiol. 2006 Aug;96(2):677-85 PMID: 16707719
  10. Hyperventilation in the awake state: potentially treatable component of Rett syndrome.
    Arch Dis Child. 1988 Sep;63(9):1039-48 PMID: 3140736
  11. Reversal of neurological defects in a mouse model of Rett syndrome.
    Science. 2007 Feb 23;315(5815):1143-7 PMID: 17289941
  12. Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder.
    Arch Dis Child. 2001 Jul;85(1):29-37 PMID: 11420195
  13. FXYD1 is an MeCP2 target gene overexpressed in the brains of Rett syndrome patients and Mecp2-null mice.
    Hum Mol Genet. 2007 Mar 15;16(6):640-50 PMID: 17309881
  14. EEG and respiration in Rett syndrome.
    Acta Neurol Scand. 1991 Feb;83(2):123-8 PMID: 2017897
  15. Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons.
    J Neurosci. 2000 Mar 1;20(5):1904-11 PMID: 10684891
  16. Autonomic nervous system dysregulation: breathing and heart rate perturbation during wakefulness in young girls with Rett syndrome.
    Pediatr Res. 2006 Oct;60(4):443-9 PMID: 16940240
  17. Regulation of respiratory neuron development by neurotrophic and transcriptional signaling mechanisms.
    Respir Physiol Neurobiol. 2005 Nov 15;149(1-3):99-109 PMID: 16203214
  18. Experimental and modeling study of Na+ current heterogeneity in rat nodose neurons and its impact on neuronal discharge.
    J Neurophysiol. 1997 Dec;78(6):3198-209 PMID: 9405539
  19. Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice.
    J Neurosci. 2005 Dec 14;25(50):11521-30 PMID: 16354910
  20. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome.
    Proc Natl Acad Sci U S A. 2005 Aug 30;102(35):12560-5 PMID: 16116096
  21. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation.
    Science. 2003 Oct 31;302(5646):890-3 PMID: 14593184
  22. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation.
    Neuron. 2006 Oct 19;52(2):255-69 PMID: 17046689
  23. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2.
    Science. 2003 Oct 31;302(5646):885-9 PMID: 14593183
  24. A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases.
    Ann Neurol. 1983 Oct;14(4):471-9 PMID: 6638958
  25. A role for L-type calcium channels in developmental regulation of transmitter phenotype in primary sensory neurons.
    J Neurosci. 1998 Feb 1;18(3):1047-55 PMID: 9437025
  26. The ups and downs of BDNF in Rett syndrome.
    Neuron. 2006 Feb 2;49(3):321-3 PMID: 16446133
  27. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression.
    Neuron. 2006 Feb 2;49(3):341-8 PMID: 16446138
  28. Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine.
    Brain Res. 2006 Jan 5;1067(1):1-12 PMID: 16376315
  29. Chronic elevation of brain-derived neurotrophic factor by ampakines.
    J Pharmacol Exp Ther. 2003 Oct;307(1):297-305 PMID: 12893840
  30. Rett syndrome and MeCP2: linking epigenetics and neuronal function.
    Am J Hum Genet. 2002 Dec;71(6):1259-72 PMID: 12442230
  31. MECP2 is progressively expressed in post-migratory neurons and is involved in neuronal maturation rather than cell fate decisions.
    Mol Cell Neurosci. 2004 Nov;27(3):306-21 PMID: 15519245
  32. Acute effects of the ampakine farampator on memory and information processing in healthy elderly volunteers.
    Neuropsychopharmacology. 2007 Jun;32(6):1272-83 PMID: 17119538
  33. Rett syndrome: analysis of deaths in the British survey.
    Eur Child Adolesc Psychiatry. 1997;6 Suppl 1:71-4 PMID: 9452925
  34. Polysomnographic characteristics of patients with Rett syndrome.
    J Pediatr. 1994 Aug;125(2):218-24 PMID: 8040765
  35. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice.
    Nat Genet. 2001 Mar;27(3):327-31 PMID: 11242118
  36. Mechanism and impact of allosteric AMPA receptor modulation by the ampakine CX546.
    Neuropharmacology. 2001 Nov;41(6):650-63 PMID: 11640919
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2007-10-03
Pages
10912-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6672830
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com