Abstract
Antidepressants increase proliferation of neuronal progenitor cells and expression of brain-derived neurotrophic factor (BDNF) in the hippocampus. We investigated the role of BDNF signaling in antidepressant-induced neurogenesis by using transgenic mice with either reduced BDNF levels (BDNF+/-) or impaired trkB activation (trkB.T1-overexpressing mice). In both transgenic strains, chronic (21 d) imipramine treatment increased the number of bromodeoxyuridine (BrdU)-positive cells to degree similar to that seen in wild-type mice 24 h after BrdU administration, although the basal proliferation rate was increased in both transgenic strains. Three weeks after BrdU administration and the last antidepressant injection, the amount of newborn (BrdU- or TUC-4-positive) cells was significantly reduced in both BDNF+/- and trkB.T1-overexpressing mice, which suggests that normal BDNF signaling is required for the long-term survival of newborn hippocampal neurons. Moreover, the antidepressant-induced increase in the surviving BrdU-positive neurons seen in wild-type mice 3 weeks after treatment was essentially lost in mice with reduced BDNF signaling. Furthermore, we observed that chronic treatment with imipramine or fluoxetine produced a temporally similar increase in both BrdU-positive and terminal deoxynucleotidyl transferase-mediated biotinylated UTP nick end-labeled neurons in the dentate gyrus, indicating that these drugs simultaneously increase both neurogenesis and neuronal elimination. These data suggest that antidepressants increase turnover of hippocampal neurons rather than neurogenesis per se and that BDNF signaling is required for the long-term survival of newborn neurons in mouse hippocampus.
MeSH Terms
Animals
Antidepressive Agents/pharmacology
Apoptosis/drug effects
Brain-Derived Neurotrophic Factor/deficiency,genetics,physiology
Cell Division/drug effects
Dentate Gyrus/cytology,drug effects,metabolism
Female
Fluoxetine/pharmacology
Heterozygote
Imipramine/pharmacology
Male
Mice
Mice, Inbred BALB C
Mice, Inbred DBA
Mice, Knockout
Mice, Transgenic
Neurons/cytology,drug effects
Receptor, trkB/deficiency,genetics,physiology
Signal Transduction/drug effects,physiology
Chemicals
Antidepressive Agents
Brain-Derived Neurotrophic Factor
Fluoxetine
Receptor, trkB
Imipramine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sairanen Mikko
Neuroscience Center, University of Helsinki, 00014 Helsinki, Finland.
Lucas Guilherme
Ernfors Patrik
Castrén Maija
Castrén Eero
References (30)
30 references, click to expand
-
Neurotrophins and depression.
Trends Pharmacol Sci. 1999 Feb;20(2):59-61
PMID: 10101965
-
Stress and hippocampal plasticity.
Annu Rev Neurosci. 1999;22:105-22
PMID: 10202533
-
Serotonin and hippocampal neurogenesis.
Neuropsychopharmacology. 1999 Aug;21(2 Suppl):46S-51S
PMID: 10432488
-
A family of proteins implicated in axon guidance and outgrowth.
J Neurobiol. 1999 Oct;41(1):158-64
PMID: 10504203
-
Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons show increased susceptibility to cortical injury after focal cerebral ischemia.
Mol Cell Neurosci. 2000 Aug;16(2):87-96
PMID: 10924253
-
Enhancement of hippocampal neurogenesis by lithium.
J Neurochem. 2000 Oct;75(4):1729-34
PMID: 10987856
-
Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus.
Neuroscience. 2000;101(2):305-12
PMID: 11074154
-
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus.
J Neurosci. 2000 Dec 15;20(24):9104-10
PMID: 11124987
-
Neurotrophins as synaptic modulators.
Nat Rev Neurosci. 2001 Jan;2(1):24-32
PMID: 11253356
-
Neurotrophins: roles in neuronal development and function.
Annu Rev Neurosci. 2001;24:677-736
PMID: 11520916
-
Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication.
Biol Psychiatry. 2001 Aug 15;50(4):260-5
PMID: 11522260
-
Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine.
Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12796-801
PMID: 11675510
-
Functional neurogenesis in the adult hippocampus.
Nature. 2002 Feb 28;415(6875):1030-4
PMID: 11875571
-
Neurobiology of depression.
Neuron. 2002 Mar 28;34(1):13-25
PMID: 11931738
-
Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression.
J Neurosci. 2002 Apr 15;22(8):3251-61
PMID: 11943826
-
Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice.
J Neurochem. 2002 Sep;82(6):1367-75
PMID: 12354284
-
The developing synapse: construction and modulation of synaptic structures and circuits.
Science. 2002 Oct 25;298(5594):770-6
PMID: 12399577
-
Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus.
Eur J Neurosci. 2002 Nov;16(10):2008-12
PMID: 12453065
-
Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects.
J Neurosci. 2003 Jan 1;23(1):349-57
PMID: 12514234
-
Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways.
J Neurosci. 2003 Jun 15;23(12):5149-60
PMID: 12832539
-
Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants.
Science. 2003 Aug 8;301(5634):805-9
PMID: 12907793
-
Neurotrophic effects of antidepressant drugs.
Curr Opin Pharmacol. 2004 Feb;4(1):58-64
PMID: 15018840
-
Trophic factors and neuronal survival.
Neuron. 1989 Jun;2(6):1525-34
PMID: 2697237
-
The nerve growth factor: thirty-five years later.
EMBO J. 1987 May;6(5):1145-54
PMID: 3301324
-
Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments.
J Neurosci. 1995 Nov;15(11):7539-47
PMID: 7472505
-
Neurotrophins and neuronal plasticity.
Science. 1995 Oct 27;270(5236):593-8
PMID: 7570017
-
Mice lacking brain-derived neurotrophic factor develop with sensory deficits.
Nature. 1994 Mar 10;368(6467):147-50
PMID: 8139657
-
Antidepressant-like effect of brain-derived neurotrophic factor (BDNF).
Pharmacol Biochem Behav. 1997 Jan;56(1):131-7
PMID: 8981620
-
More hippocampal neurons in adult mice living in an enriched environment.
Nature. 1997 Apr 3;386(6624):493-5
PMID: 9087407
-
A molecular and cellular theory of depression.
Arch Gen Psychiatry. 1997 Jul;54(7):597-606
PMID: 9236543