Key role of the 5-HT1A receptor addressing protein Yif1B in serotonin neurotransmission and SSRI treatment.


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
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

344-355

Subventions

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.

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Auteurs

Vincent Martin (V)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Lionel Mathieu (L)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Jorge Diaz (J)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Haysam Salman (H)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Jeanine Alterio (J)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Caroline Chevarin (C)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Laurence Lanfumey (L)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Michel Hamon (M)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Mark C Austin (MC)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Michèle Darmon (M)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Craig A Stockmeier (CA)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

Justine Masson (J)

From Inserm UMR894, Centre de Psychiatrie et Neuroscience, Paris F-75014 France; Université Paris Descartes, Sorbonne Paris Cité - Paris 5, France (Martin, Mathieu, Diaz, Salman, Alterio, Chevarin, Lanfumey, Hamon, Darmon, Masson); the College of Pharmacy, Idaho State University, Pocatello, ID 83209 USA (Austin); the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, Jackson, MS, 39216 USA (Stockmeier); and Inserm UMR-S 1270, Paris, France; Sorbonne Université, Science and Engineering Faculty, Paris, France; Institut du Fer à Moulin, Paris, France (Darmon, Masson).

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