Abstract
Infant maternal separation, a paradigm of early life stress in rodents, elicits long-lasting changes in gene expression that persist into adulthood. In BALB/c mice, an inbred strain with spontaneously elevated anxiety and stress reactivity, infant maternal separation led to increased depression-like behavioral responses to adult stress and robustly increased editing of serotonin 2C receptor pre-mRNA. Chronic fluoxetine treatment of adult BALB/c mice exposed to early life stress affected neither their behavioral responses to stress nor their basal 5-HT2C pre-mRNA editing phenotype. However, when fluoxetine was administered during adolescence, depression-like behavioral responses to stress were significantly diminished in these mice, and their basal and stress-induced 5-HT2C pre-mRNA editing phenotypes were significantly lower. Moreover, when BALB/c mice exposed to early life stress were raised in an enriched postweaning environment, their depression-like behavioral responses to adult stress were also significantly diminished. However, their 5-HT2C pre-mRNA editing phenotype remained unaltered. Hence, the similar behavioral effects of enrichment and fluoxetine treatment during adolescence were not accompanied by similar changes in 5-HT2C pre-mRNA editing. Enriched and nonenriched BALB/c mice exposed to early life stress also exhibited significantly increased expression of mRNA and protein encoding the G alpha q subunit of G-protein that couples to 5-HT2A/2C receptors. In contrast, G alpha q expression levels were significantly lower in fluoxetine-treated mice. These findings suggest that compensatory changes in G alpha q expression occur in mice with persistently altered 5-HT2C pre-mRNA editing and provide an explanation for the dissociation between 5-HT2C receptor editing phenotypes and behavioral stress responses.
MeSH Terms
Age Factors
Animals
Anxiety, Separation/complications,genetics,psychology
Body Weight
Depressive Disorder/drug therapy,etiology,genetics,physiopathology,psychology
Emotions
Environment
Female
Fluoxetine/pharmacology,therapeutic use
GTP-Binding Protein alpha Subunits, Gq-G11/biosynthesis,genetics
Genetic Predisposition to Disease
Helplessness, Learned
Male
Mice
Mice, Inbred BALB C/genetics,physiology,psychology
Mice, Inbred C57BL
Neocortex/metabolism
Protein Isoforms/biosynthesis,genetics,physiology
RNA Editing
RNA Precursors/genetics
Random Allocation
Receptor, Serotonin, 5-HT2C/biosynthesis,genetics,physiology
Serotonin/physiology
Serotonin Uptake Inhibitors/pharmacology,therapeutic use
Species Specificity
Swimming
Chemicals
Protein Isoforms
RNA Precursors
Receptor, Serotonin, 5-HT2C
Serotonin Uptake Inhibitors
Fluoxetine
Serotonin
GTP-Binding Protein alpha Subunits, Gq-G11
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bhansali Punita
Department of Psychiatry, Columbia University, New York, New York 10032, USA.
Dunning Jane
Singer Sarah E
David Leora
Schmauss Claudia
References (19)
19 references, click to expand
-
RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity.
J Biol Chem. 1999 Apr 2;274(14):9472-8
PMID: 10092629
-
Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors.
J Neurochem. 2000 Mar;74(3):1290-300
PMID: 10693963
-
Measuring normal and pathological anxiety-like behaviour in mice: a review.
Behav Brain Res. 2001 Nov 1;125(1-2):141-9
PMID: 11682105
-
Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims.
Neuron. 2002 Apr 25;34(3):349-56
PMID: 11988167
-
RNA editing by adenosine deaminases that act on RNA.
Annu Rev Biochem. 2002;71:817-46
PMID: 12045112
-
Home cage activity and behavioral performance in inbred and hybrid mice.
Behav Brain Res. 2002 Nov 15;136(2):555-69
PMID: 12429418
-
Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission.
J Neurosci. 2002 Dec 15;22(24):10529-32
PMID: 12486144
-
Neurobiological effects of childhood abuse: implications for the pathophysiology of depression and anxiety.
Arch Womens Ment Health. 2003 Feb;6(1):15-22
PMID: 12715261
-
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene.
Science. 2003 Jul 18;301(5631):386-9
PMID: 12869766
-
Differential responses to psychotherapy versus pharmacotherapy in patients with chronic forms of major depression and childhood trauma.
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14293-6
PMID: 14615578
-
Effects of chronic fluoxetine in animal models of anxiety and depression.
Neuropsychopharmacology. 2004 Jul;29(7):1321-30
PMID: 15085085
-
Tryptophan hydroxylase-2 controls brain serotonin synthesis.
Science. 2004 Jul 9;305(5681):217
PMID: 15247473
-
How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing.
J Neurosci. 2005 Jan 19;25(3):648-51
PMID: 15659601
-
Childhood sexual abuse, stressful life events and risk for major depression in women.
Psychol Med. 2004 Nov;34(8):1475-82
PMID: 15724878
-
Early life genetic, epigenetic and environmental factors shaping emotionality in rodents.
Neurosci Biobehav Rev. 2005;29(8):1335-46
PMID: 16095695
-
Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing.
Science. 2005 Sep 2;309(5740):1534-9
PMID: 16141067
-
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats.
Brain Res Mol Brain Res. 1993 May;18(3):195-200
PMID: 8497182
-
Regulation of serotonin-2C receptor G-protein coupling by RNA editing.
Nature. 1997 May 15;387(6630):303-8
PMID: 9153397
-
5-Hydroxytryptamine2-family receptors (5-hydroxytryptamine2A, 5-hydroxytryptamine2B, 5-hydroxytryptamine2C): where structure meets function.
Pharmacol Ther. 1998 Sep;79(3):231-57
PMID: 9776378