Contribution of the Opioid System to the Antidepressant Effects of Fluoxetine.

Mice Animals Fluoxetine / pharmacology Analgesics, Opioid / pharmacology Corticosterone Receptors, Opioid, delta / genetics Antidepressive Agents / pharmacology Selective Serotonin Reuptake Inhibitors / pharmacology Mice, Knockout
Dentate gyrus Depression Enkephalin Fluoxetine Opioid Selective serotonin reuptake inhibitors (SSRI)

Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
15 12 2022
Historique:
received: 16 12 2020
revised: 17 05 2022
accepted: 18 05 2022
pubmed: 18 8 2022
medline: 22 11 2022
entrez: 17 8 2022
Statut: ppublish

Résumé

Selective serotonin reuptake inhibitors such as fluoxetine have a limited treatment efficacy. The mechanism by which some patients respond to fluoxetine while others do not remains poorly understood, limiting treatment effectiveness. We have found the opioid system to be involved in the responsiveness to fluoxetine treatment in a mouse model for anxiety- and depressive-like behavior. We analyzed gene expression changes in the dentate gyrus of mice chronically treated with corticosterone and fluoxetine. After identifying a subset of genes of interest, we studied their expression patterns in relation to treatment responsiveness. We further characterized their expression through in situ hybridization and the analysis of a single-cell RNA sequencing dataset. Finally, we behaviorally tested mu and delta opioid receptor knockout mice in the novelty suppressed feeding test and the forced swim test after chronic corticosterone and fluoxetine treatment. Chronic fluoxetine treatment upregulates proenkephalin expression in the dentate gyrus, and this upregulation is associated with treatment responsiveness. The expression of several of the most significantly upregulated genes, including proenkephalin, is localized to an anatomically and transcriptionally specialized subgroup of mature granule cells in the dentate gyrus. We have also found that the delta opioid receptor contributes to some, but not all, of the behavioral effects of fluoxetine. These data indicate that the opioid system is involved in the antidepressant effects of fluoxetine, and this effect may be mediated through the upregulation of proenkephalin in a subpopulation of mature granule cells.

Sections du résumé

BACKGROUND
Selective serotonin reuptake inhibitors such as fluoxetine have a limited treatment efficacy. The mechanism by which some patients respond to fluoxetine while others do not remains poorly understood, limiting treatment effectiveness. We have found the opioid system to be involved in the responsiveness to fluoxetine treatment in a mouse model for anxiety- and depressive-like behavior.
METHODS
We analyzed gene expression changes in the dentate gyrus of mice chronically treated with corticosterone and fluoxetine. After identifying a subset of genes of interest, we studied their expression patterns in relation to treatment responsiveness. We further characterized their expression through in situ hybridization and the analysis of a single-cell RNA sequencing dataset. Finally, we behaviorally tested mu and delta opioid receptor knockout mice in the novelty suppressed feeding test and the forced swim test after chronic corticosterone and fluoxetine treatment.
RESULTS
Chronic fluoxetine treatment upregulates proenkephalin expression in the dentate gyrus, and this upregulation is associated with treatment responsiveness. The expression of several of the most significantly upregulated genes, including proenkephalin, is localized to an anatomically and transcriptionally specialized subgroup of mature granule cells in the dentate gyrus. We have also found that the delta opioid receptor contributes to some, but not all, of the behavioral effects of fluoxetine.
CONCLUSIONS
These data indicate that the opioid system is involved in the antidepressant effects of fluoxetine, and this effect may be mediated through the upregulation of proenkephalin in a subpopulation of mature granule cells.

Identifiants

DOI: 10.1016/j.biopsych.2022.05.030 PMID: 35977861 PMC: PMC10426813
pubmed: 35977861
pii: S0006-3223(22)01323-3
doi: 10.1016/j.biopsych.2022.05.030
pmc: PMC10426813
mid: NIHMS1907475
pii:
doi:

Substances chimiques

Fluoxetine 01K63SUP8D
Analgesics, Opioid 0
Corticosterone W980KJ009P
Receptors, Opioid, delta 0
Antidepressive Agents 0
Serotonin Uptake Inhibitors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

952-963

Subventions

Organisme : NIDA NIH HHS
ID : U01 DA043098
Pays : United States
Organisme : HSRD VA
ID : CDP 13-003
Pays : United States
Organisme : NHLBI NIH HHS
ID : R21 HL083862
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG043688
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS081203
Pays : United States
Organisme : NIMH NIH HHS
ID : R37 MH068542
Pays : United States
Organisme : NIMH NIH HHS
ID : R21 MH116462
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH083862
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Références

Nat Commun. 2019 May 20;10(1):2232
pubmed: 31110186
Br J Pharmacol. 1980 Dec;70(4):509-11
pubmed: 7470727
Neurobiol Dis. 2008 Aug;31(2):278-85
pubmed: 18586506
Elife. 2021 Jul 14;10:
pubmed: 34259630
Mol Psychiatry. 2019 Dec;24(12):1779-1786
pubmed: 31467392
Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Jun;4(6):554-566
pubmed: 31176387
Science. 2016 Aug 26;353(6302):925-8
pubmed: 27471252
Nature. 1977 Apr 21;266(5604):730-2
pubmed: 559941
Nat Med. 2017 Jan;23(1):28-38
pubmed: 27918562
Peptides. 2008 Jan;29(1):93-103
pubmed: 18069089
Brain Res. 1995 Nov 27;700(1-2):89-98
pubmed: 8624732
Cell Rep. 2020 Apr 28;31(4):107551
pubmed: 32348756
Psychopharmacology (Berl). 2016 Mar;233(6):1119-30
pubmed: 26728893
Behav Pharmacol. 1997 Nov;8(6-7):523-32
pubmed: 9832966
Psychopharmacology (Berl). 1996 Jan;123(1):71-8
pubmed: 8741957
Transl Psychiatry. 2019 Dec 10;9(1):337
pubmed: 31822658
Neuron. 2009 May 28;62(4):479-93
pubmed: 19477151
Psychopharmacology (Berl). 2008 Nov;200(4):557-72
pubmed: 18629477
Neuroscience. 2012 Sep 27;221:203-13
pubmed: 22750239
Pharmacol Ther. 2019 Sep;201:51-76
pubmed: 31051197
Nat Genet. 2006 May;38(5):500-1
pubmed: 16642009
Am J Psychiatry. 2018 Dec 1;175(12):1205-1215
pubmed: 30153752
Prog Brain Res. 2007;163:3-22
pubmed: 17765709
Neuroscientist. 2016 Feb;22(1):26-45
pubmed: 25488850
Neurobiol Stress. 2020 Oct 17;13:100257
pubmed: 33344712
Nat Neurosci. 2010 Feb;13(2):213-22
pubmed: 20037579
Genes Brain Behav. 2014 Jul;13(6):550-8
pubmed: 24804898
PLoS One. 2014 Jan 17;9(1):e85136
pubmed: 24465494
Neurology. 2012 Aug 21;79(8):807-14
pubmed: 22915176
ACS Chem Neurosci. 2021 May 5;12(9):1487-1497
pubmed: 33905229
J Pharmacol Sci. 2004 Jul;95(3):374-80
pubmed: 15272214
Neuropsychopharmacology. 2017 Sep;42(10):2052-2063
pubmed: 28303899
Am J Psychiatry. 2006 Jan;163(1):28-40
pubmed: 16390886
Eur J Pharmacol. 2007 Jul 2;566(1-3):132-6
pubmed: 17459369
Int J Neuropsychopharmacol. 2013 Feb;16(1):151-62
pubmed: 22217458
Transl Psychiatry. 2017 Mar 14;7(3):e1061
pubmed: 28291260
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
J Neurosci. 2007 Dec 12;27(50):13756-61
pubmed: 18077687
Nat Neurosci. 2015 Nov;18(11):1606-16
pubmed: 26389840
Transl Psychiatry. 2014 Jul 15;4:e411
pubmed: 25026323
Brain Res. 2006 Jan 19;1069(1):172-81
pubmed: 16364263
Nat Commun. 2018 Jan 19;9(1):298
pubmed: 29352183
Neurosci Biobehav Rev. 2018 Jan;84:272-288
pubmed: 28859997
Int J Methods Psychiatr Res. 2012 Sep;21(3):169-84
pubmed: 22865617
Neuropharmacology. 2011 Sep;61(3):408-13
pubmed: 21356220
Science. 2003 Aug 8;301(5634):805-9
pubmed: 12907793
Psychopharmacology (Berl). 2008 Feb;196(2):327-35
pubmed: 17906961
Neuropsychopharmacology. 2019 Oct;44(11):1876-1885
pubmed: 31132785
Mol Psychiatry. 2020 Jun;25(6):1191-1201
pubmed: 30804492
J Pharmacol Exp Ther. 2003 Apr;305(1):323-30
pubmed: 12649385

Auteurs

Elena Carazo-Arias (E)

Department of Biological Sciences, Columbia University, New York State Psychiatric Institute, New York, New York; Division of Integrative Neuroscience, New York State Psychiatric Institute, New York, New York.

Phi T Nguyen (PT)

Department of Psychiatry, Columbia University, New York State Psychiatric Institute, New York, New York; Division of Integrative Neuroscience, New York State Psychiatric Institute, New York, New York.

Marley Kass (M)

Department of Psychiatry, Columbia University, New York State Psychiatric Institute, New York, New York; Division of Integrative Neuroscience, New York State Psychiatric Institute, New York, New York.

Hyun Jung Jee (HJ)

Division of Integrative Neuroscience, New York State Psychiatric Institute, New York, New York.

Katherine M Nautiyal (KM)

Department of Psychological and Brain Sciences, Dartmouth College, Hanover, New Hampshire.

Valerie Magalong (V)

Program in Developmental Neurogenetics, The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, California.

Lilian Coie (L)

Department of Neuroscience, Columbia University, New York State Psychiatric Institute, New York, New York.

Valentine Andreu (V)

Department of Neuroscience, Columbia University, New York State Psychiatric Institute, New York, New York.

Mark M Gergues (MM)

Department of Psychology, Rutgers University, New Brunswick, New Jersey.

Huzefa Khalil (H)

Molecular and Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, Michigan; Department of Psychiatry, University of Michigan, Ann Arbor, Michigan.

Huda Akil (H)

Molecular and Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, Michigan; Department of Psychiatry, University of Michigan, Ann Arbor, Michigan.

Danusa Mar Arcego (DM)

Department of Psychiatry, Faculty of Medicine, Douglas Hospital Research Centre, McGill University, Montreal, Québec, Canada.

Michael Meaney (M)

Department of Psychiatry, Faculty of Medicine, Douglas Hospital Research Centre, McGill University, Montreal, Québec, Canada; Sackler Program for Epigenetics and Psychobiology, Douglas Hospital Research Centre, McGill University, Montreal, Québec, Canada; Singapore Institute for Clinical Sciences, Singapore.

Christoph Anacker (C)

Department of Psychiatry, Columbia University, New York State Psychiatric Institute, New York, New York.

Benjamin A Samuels (BA)

Department of Psychology, Rutgers University, New Brunswick, New Jersey.

John E Pintar (JE)

Department of Neuroscience & Cell Biology, Rutgers University, New Brunswick, New Jersey.

Irina Morozova (I)

Center for Genome Technology and Biomolecular Engineering, Columbia University, New York State Psychiatric Institute, New York, New York; Department of Chemical Engineering, Columbia University, New York State Psychiatric Institute, New York, New York.

Sergey Kalachikov (S)

Center for Genome Technology and Biomolecular Engineering, Columbia University, New York State Psychiatric Institute, New York, New York; Department of Chemical Engineering, Columbia University, New York State Psychiatric Institute, New York, New York; Data Science Institute, Columbia University, New York State Psychiatric Institute, New York, New York.

Rene Hen (R)

Department of Psychiatry, Columbia University, New York State Psychiatric Institute, New York, New York; Department of Neuroscience, Columbia University, New York State Psychiatric Institute, New York, New York; Department of Pharmacology, Columbia University, New York State Psychiatric Institute, New York, New York; Division of Integrative Neuroscience, New York State Psychiatric Institute, New York, New York. Electronic address: rh95@cumc.columbia.edu.

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Contribution of the Opioid System to the...
questionsmedicales.fr › Eucaryotes › Animaux › Contribution of the Opioid System to the...
questionsmedicales.fr › Composés chimiques organiques › Amines › Propylamines › Fluoxétine › Contribution of the Opioid System to the...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Agents du système nerveux central › Dépresseurs du système nerveux central › Stupéfiants › Analgésiques morphiniques › Contribution of the Opioid System to the...
questionsmedicales.fr › Hormones corticosurrénaliennes › Hydroxycorticostéroïdes › 11-Hydroxycorticostéroïdes › Corticostérone › Contribution of the Opioid System to the...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs peptidiques › Récepteur aux neuropeptides › Récepteurs aux opioïdes › Récepteur delta › Contribution of the Opioid System to the...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Utilisations thérapeutiques › Agents du système nerveux central › Psychoanaleptiques › Antidépresseurs › Contribution of the Opioid System to the...
questionsmedicales.fr › Actions chimiques et utilisations › Actions pharmacologiques › Effets physiologiques des médicaments › Agents neuromédiateurs › Agents sérotoninergiques › Inhibiteurs sélectifs de la recapture de la sérotonine › Contribution of the Opioid System to the...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souris transgéniques › Souris knockout › Contribution of the Opioid System to the...