Key role of the 5-HT1A receptor addressing protein Yif1B in serotonin neurotransmission and SSRI treatment.
Animals
Autopsy
Behavior, Animal
/ physiology
Depressive Disorder, Major
/ metabolism
Disease Models, Animal
Female
Fluoxetine
/ pharmacology
Humans
Macaca mulatta
Male
Mice
Mice, 129 Strain
Mice, Inbred C57BL
Mice, Knockout
Prefrontal Cortex
/ drug effects
Raphe Nuclei
/ drug effects
Receptor, Serotonin, 5-HT1A
/ metabolism
Serotonergic Neurons
/ drug effects
Serotonin
/ metabolism
Serotonin 5-HT1 Receptor Agonists
/ pharmacology
Selective Serotonin Reuptake Inhibitors
/ pharmacology
Sex Characteristics
Social Behavior
Vesicular Transport Proteins
/ drug effects
Journal
Journal of psychiatry & neuroscience : JPN
ISSN: 1488-2434
Titre abrégé: J Psychiatry Neurosci
Pays: Canada
ID NLM: 9107859
Informations de publication
Date de publication:
01 09 2020
01 09 2020
Historique:
entrez:
28
5
2020
pubmed:
28
5
2020
medline:
27
10
2021
Statut:
ppublish
Résumé
Altered function of serotonin receptor 1A (5-HT1AR) has been consistently implicated in anxiety, major depressive disorder and resistance to antidepressants. Mechanisms by which the function of 5-HT1AR (expressed as an autoreceptor in serotonergic raphe neurons and as a heteroreceptor in serotonin [5-HT] projection areas) is altered include regulation of its expression, but 5-HT1AR trafficking may also be involved. We investigated the consequences of the lack of Yif1B (the 5-HT1AR trafficking protein) on 5-HT neurotransmission in mice, and whether Yif1B expression might be affected under conditions known to alter 5-HT neurotransmission, such as anxious or depressive states or following treatment with fluoxetine (a selective serotonin reuptake inhibitor) in humans, monkeys and mice. Compared with wild-type mice, Yif1B-knockout mice showed a significant decrease in the forebrain density of 5-HT projection fibres and a hypofunctionality of 5-HT1A autoreceptors expressed on raphe 5-HT neurons. In addition, social interaction was less in Yif1B-knockout mice, which did not respond to the antidepressant-like effect of acute fluoxetine injection. In wild-type mice, social defeat was associated with downregulated Yif1B mRNA in the prefrontal cortex, and chronic fluoxetine treatment increased Yif1B expression. The expression of Yif1B was also downregulated in the postmortem prefrontal cortex of people with major depressive disorder and upregulated after chronic treatment with a selective serotonin reuptake inhibitor in monkeys. We found sex differences in Yif1B expression in humans and monkeys, but not in mice under the tested conditions. These data support the concept that Yif1B plays a critical role in 5-HT1AR functioning and brain 5-HT homeostasis. The opposite changes in its expression observed in anxious or depressive states and after therapeutic fluoxetine treatment suggest that Yif1B might be involved in vulnerability to anxiety and depression, and fluoxetine efficacy.
Sections du résumé
Background
Altered function of serotonin receptor 1A (5-HT1AR) has been consistently implicated in anxiety, major depressive disorder and resistance to antidepressants. Mechanisms by which the function of 5-HT1AR (expressed as an autoreceptor in serotonergic raphe neurons and as a heteroreceptor in serotonin [5-HT] projection areas) is altered include regulation of its expression, but 5-HT1AR trafficking may also be involved.
Methods
We investigated the consequences of the lack of Yif1B (the 5-HT1AR trafficking protein) on 5-HT neurotransmission in mice, and whether Yif1B expression might be affected under conditions known to alter 5-HT neurotransmission, such as anxious or depressive states or following treatment with fluoxetine (a selective serotonin reuptake inhibitor) in humans, monkeys and mice.
Results
Compared with wild-type mice, Yif1B-knockout mice showed a significant decrease in the forebrain density of 5-HT projection fibres and a hypofunctionality of 5-HT1A autoreceptors expressed on raphe 5-HT neurons. In addition, social interaction was less in Yif1B-knockout mice, which did not respond to the antidepressant-like effect of acute fluoxetine injection. In wild-type mice, social defeat was associated with downregulated Yif1B mRNA in the prefrontal cortex, and chronic fluoxetine treatment increased Yif1B expression. The expression of Yif1B was also downregulated in the postmortem prefrontal cortex of people with major depressive disorder and upregulated after chronic treatment with a selective serotonin reuptake inhibitor in monkeys.
Limitations
We found sex differences in Yif1B expression in humans and monkeys, but not in mice under the tested conditions.
Conclusion
These data support the concept that Yif1B plays a critical role in 5-HT1AR functioning and brain 5-HT homeostasis. The opposite changes in its expression observed in anxious or depressive states and after therapeutic fluoxetine treatment suggest that Yif1B might be involved in vulnerability to anxiety and depression, and fluoxetine efficacy.
Identifiants
pubmed: 32459080
doi: 10.1503/jpn.190134
pmc: PMC7850149
doi:
Substances chimiques
Serotonin 5-HT1 Receptor Agonists
0
Serotonin Uptake Inhibitors
0
Vesicular Transport Proteins
0
YIF1B protein, human
0
Fluoxetine
01K63SUP8D
Receptor, Serotonin, 5-HT1A
112692-38-3
Serotonin
333DO1RDJY
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
344-355Subventions
Organisme : NIGMS NIH HHS
ID : P20 GM121334
Pays : United States
Organisme : NIGMS NIH HHS
ID : P30 GM103328
Pays : United States
Informations de copyright
© 2020 Joule Inc. or its licensors.
Déclaration de conflit d'intérêts
None declared.
Références
J Neurosci. 2019 Feb 20;39(8):1334-1346
pubmed: 30552180
J Neurosci. 2018 Sep 19;38(38):8200-8210
pubmed: 30093565
Psychopharmacology (Berl). 1992;106(2):261-7
pubmed: 1347954
Neuroscience. 1991;41(2-3):495-505
pubmed: 1714550
Int J Neuropsychopharmacol. 2010 Sep;13(8):1089-101
pubmed: 20392296
J Neurosci. 2005 Sep 7;25(36):8165-72
pubmed: 16148224
Neuropharmacology. 2017 Jan;112(Pt A):198-209
pubmed: 27211253
Prog Neuropsychopharmacol Biol Psychiatry. 2019 Jul 13;93:31-38
pubmed: 30876986
J Neurochem. 2014 Apr;129(2):240-8
pubmed: 24517494
J Neurosci. 2014 Apr 2;34(14):4809-21
pubmed: 24695701
Naunyn Schmiedebergs Arch Pharmacol. 1995 Aug;352(2):141-8
pubmed: 7477436
Neuroscience. 2017 Jul 25;356:78-88
pubmed: 28528967
Brain Res Dev Brain Res. 1997 Feb 20;98(2):185-90
pubmed: 9051259
J Neurosci. 2012 Oct 10;32(41):14227-41
pubmed: 23055492
Psychol Med. 1999 May;29(3):555-67
pubmed: 10405077
J Biol Chem. 2012 Feb 24;287(9):6615-27
pubmed: 22232550
Behav Brain Res. 2006 Feb 28;167(2):328-41
pubmed: 16256213
Psychopharmacology (Berl). 2012 Nov;224(2):313-25
pubmed: 22707231
Prog Neurobiol. 2009 May;88(1):17-31
pubmed: 19428959
J Neurosci. 2004 May 19;24(20):4807-17
pubmed: 15152041
Nat Protoc. 2011 Jul 21;6(8):1183-91
pubmed: 21799487
Br J Pharmacol. 2017 Aug;174(15):2471-2483
pubmed: 28493335
J Psychosom Res. 2010 Mar;68(3):235-43
pubmed: 20159208
Biol Psychiatry. 2007 May 1;61(9):1081-9
pubmed: 16979141
Int J Neuropsychopharmacol. 2009 Mar;12(2):155-68
pubmed: 18561871
Traffic. 2015 Sep;16(9):978-93
pubmed: 26077767
Neurosci Lett. 1989 Apr 24;99(1-2):101-6
pubmed: 2748003
Autism Res. 2017 Jan;10(1):66-77
pubmed: 27478061
Neurosci Biobehav Rev. 2019 Jan;96:219-231
pubmed: 30543906
Eur J Neurosci. 2010 Jul;32(1):18-26
pubmed: 20561047
Curr Protoc Neurosci. 2011 Jan;Chapter 9:Unit9.36
pubmed: 21207368
Brain Res. 1983 Dec 19;289(1-2):109-19
pubmed: 6140982
Eur J Pharmacol. 2008 Oct 10;594(1-3):117-24
pubmed: 18691569
Cereb Cortex. 2017 Jan 1;27(1):509-521
pubmed: 26494800
EMBO J. 2000 Sep 1;19(17):4485-92
pubmed: 10970842
Curr Pharm Des. 2014;20(23):3738-50
pubmed: 24180393
Neurosci Lett. 2011 Oct 3;503(2):83-6
pubmed: 21871532
Biol Psychiatry. 2010 Jan 15;67(2):117-24
pubmed: 19819426
J Clin Psychiatry. 2006;67 Suppl 12:20-6
pubmed: 17092192
Front Pharmacol. 2018 Oct 16;9:1185
pubmed: 30459605
eNeuro. 2018 Feb 6;5(1):
pubmed: 29445767
J Neurosci. 2008 Aug 6;28(32):8063-73
pubmed: 18685031
Brain Res. 2002 May 17;936(1-2):68-75
pubmed: 11988231
Neuroscience. 2016 May 3;321:210-221
pubmed: 26049143
Neuron. 2015 Aug 5;87(3):549-62
pubmed: 26247862
J Am Coll Dent. 2014 Summer;81(3):4-13
pubmed: 25951677
J Psychiatry Neurosci. 2019 Feb 26;44(3):164-176
pubmed: 30807072