Interleukin-10 enhances activity of ventral tegmental area dopamine neurons resulting in increased dopamine release.


Journal

Brain, behavior, and immunity
ISSN: 1090-2139
Titre abrégé: Brain Behav Immun
Pays: Netherlands
ID NLM: 8800478

Informations de publication

Date de publication:
10 2023
Historique:
received: 09 05 2023
revised: 06 07 2023
accepted: 09 07 2023
pmc-release: 01 10 2024
medline: 29 9 2023
pubmed: 16 7 2023
entrez: 15 7 2023
Statut: ppublish

Résumé

Dopamine transmission from the ventral tegmental area (VTA) to the nucleus accumbens (NAc) regulates important aspects of motivation and is influenced by the neuroimmune system. The neuroimmune system is a complex network of leukocytes, microglia and astrocytes that detect and remove foreign threats like bacteria or viruses and communicate with each other to regulate non-immune (e.g neuronal) cell activity through cytokine signaling. Inflammation is a key regulator of motivational states, though the effects of specific cytokines on VTA circuitry and motivation are largely unknown. Therefore, electrophysiology, neurochemical, immunohistochemical and behavioral studies were performed to determine the effects of the anti-inflammatory cytokine interleukin-10 (IL-10) on mesolimbic activity, dopamine transmission and conditioned behavior. IL-10 enhanced VTA dopamine firing and NAc dopamine levels via decreased VTA GABA currents in dopamine neurons. The IL-10 receptor was localized on VTA dopamine and non-dopamine cells. The IL-10 effects on dopamine neurons required post-synaptic phosphoinositide 3-kinase activity, and IL-10 appeared to have little-to-no efficacy on presynaptic GABA terminals. Intracranial IL-10 enhanced NAc dopamine levels in vivo and produced conditioned place aversion. Together, these studies identify the IL-10R on VTA dopamine neurons as a potential regulator of motivational states.

Identifiants

pubmed: 37453452
pii: S0889-1591(23)00180-0
doi: 10.1016/j.bbi.2023.07.007
pmc: PMC10530119
mid: NIHMS1919924
pii:
doi:

Substances chimiques

Dopamine VTD58H1Z2X
Interleukin-10 130068-27-8
Phosphatidylinositol 3-Kinases EC 2.7.1.-
gamma-Aminobutyric Acid 56-12-2

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

145-155

Subventions

Organisme : NIAAA NIH HHS
ID : R01 AA020919
Pays : United States
Organisme : NIAAA NIH HHS
ID : R01 AA030577
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA035958
Pays : United States

Informations de copyright

Copyright © 2023 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Références

Cell Rep. 2022 Apr 5;39(1):110616
pubmed: 35385745
Immunity. 1999 Jan;10(1):39-49
pubmed: 10023769
Nat Commun. 2019 Mar 29;10(1):1455
pubmed: 30926783
J Neurosci. 2013 Oct 2;33(40):15879-93
pubmed: 24089494
J Neurosci. 2017 Feb 22;37(8):2086-2096
pubmed: 28115487
Glia. 2002 Apr 1;38(1):24-35
pubmed: 11921201
J Biol Chem. 1993 Oct 5;268(28):21053-9
pubmed: 8407942
Neuropharmacology. 2016 Aug;107:181-188
pubmed: 27016017
Prog Neurobiol. 1998 Dec;56(6):613-72
pubmed: 9871940
Pharmacol Biochem Behav. 2019 Apr;179:34-42
pubmed: 30695700
J Neuroinflammation. 2020 Aug 22;17(1):246
pubmed: 32828124
J Biol Chem. 2006 May 26;281(21):14632-43
pubmed: 16567807
Immunity. 2001 Jul;15(1):35-46
pubmed: 11485736
Handb Exp Pharmacol. 2009;(192):209-33
pubmed: 19184651
Front Neurosci. 2012 Sep 25;6:137
pubmed: 23055953
Clin Pharmacol Ther. 1997 Aug;62(2):171-80
pubmed: 9284853
Curr Opin Pharmacol. 2006 Aug;6(4):379-86
pubmed: 16713356
Addict Biol. 2022 Jan;27(1):e13108
pubmed: 34713509
Exp Neurol. 2015 Nov;273:83-91
pubmed: 26263843
J Neurosci. 2011 Dec 7;31(49):17835-47
pubmed: 22159099
J Leukoc Biol. 2004 Aug;76(2):314-21
pubmed: 15123776
Neuron. 2014 Jun 18;82(6):1346-56
pubmed: 24857021
Am J Physiol Regul Integr Comp Physiol. 2003 Dec;285(6):R1514-9
pubmed: 14615407
J Comp Neurol. 2003 Dec 1;467(1):60-79
pubmed: 14574680
Sci Adv. 2020 Jul 29;6(31):eabb0806
pubmed: 32832688
Nature. 2015 Sep 10;525(7568):243-6
pubmed: 26322583
J Pharmacol Exp Ther. 2010 Oct;335(1):124-32
pubmed: 20605908
J Psychiatr Res. 2008 Dec;43(2):89-97
pubmed: 18394646
J Neurosci. 1998 Oct 1;18(19):8003-15
pubmed: 9742167
Physiol Behav. 2006 May 30;87(5):842-7
pubmed: 16616943
Int J Mol Sci. 2019 Nov 28;20(23):
pubmed: 31795299
J Neurosci. 1997 Jan 15;17(2):796-803
pubmed: 8987801
Neuroscience. 2011 Jan 13;172:94-103
pubmed: 20974231
Neuropharmacology. 2016 Feb;101:471-9
pubmed: 26525189
Pharmacol Rev. 1989 Dec;41(4):489-537
pubmed: 2700603
Biomolecules. 2020 Jul 09;10(7):
pubmed: 32659950
Psychoneuroendocrinology. 1999 Apr;24(3):301-11
pubmed: 10101735
Immunol Res. 2008;41(3):155-64
pubmed: 18512160
Psychopharmacology (Berl). 2000 Dec;153(1):31-43
pubmed: 11255927
Neuron. 2010 Dec 9;68(5):815-34
pubmed: 21144997
J Neuroinflammation. 2021 Sep 22;18(1):219
pubmed: 34551810
Ann Oncol. 1999 Apr;10(4):433-40
pubmed: 10370786
Proc Natl Acad Sci U S A. 2014 Jul 1;111(26):E2751-9
pubmed: 24979798
Brain Behav Immun. 2016 Jan;51:258-267
pubmed: 26365025
Curr Top Microbiol Immunol. 2014;380:191-212
pubmed: 25004819
Trends Pharmacol Sci. 2013 Mar;34(3):162-6
pubmed: 23384389
Trends Neurosci. 2015 Apr;38(4):217-25
pubmed: 25637939
J Neuroimmune Pharmacol. 2017 Jun;12(2):249-259
pubmed: 27640210
Brain Behav Immun. 2021 Oct;97:68-78
pubmed: 34224823
Cell Rep. 2022 Apr 5;39(1):110633
pubmed: 35385720
Prog Neurobiol. 2021 Apr;199:101952
pubmed: 33197496
Behav Brain Res. 2002 Dec 2;137(1-2):3-25
pubmed: 12445713
Eur J Neurosci. 2013 Mar;37(6):1022-31
pubmed: 23294165
J Pharmacol Exp Ther. 1999 Dec;291(3):1045-53
pubmed: 10565823
Behav Brain Res. 2019 Oct 17;372:112024
pubmed: 31195034
Annu Rev Immunol. 2001;19:683-765
pubmed: 11244051
Neurotox Res. 2008 Oct;14(2-3):169-83
pubmed: 19073424
Neuron. 1997 Jul;19(1):139-50
pubmed: 9247270
J Neuroinflammation. 2016 Nov 24;13(1):297
pubmed: 27881137
Structure. 2008 Sep 10;16(9):1333-44
pubmed: 18599299
J Neuroimmunol. 2002 Jan;122(1-2):9-19
pubmed: 11777539
Neurosci Lett. 2021 Nov 1;764:136235
pubmed: 34508846
J Cell Commun Signal. 2016 Mar;10(1):61-7
pubmed: 26253919
Neuropharmacology. 2015 Sep;96(Pt A):55-69
pubmed: 25446571
Mol Neurobiol. 2023 Jun;60(6):3113-3129
pubmed: 36802012
Brain Behav Immun. 2011 Jun;25 Suppl 1:S92-S105
pubmed: 21266194
Front Cell Neurosci. 2015 Mar 31;9:40
pubmed: 25873859
Glia. 2020 Nov;68(11):2228-2245
pubmed: 32275335
PLoS One. 2013 Nov 22;8(11):e81218
pubmed: 24278397
J Biol Chem. 1999 Jun 4;274(23):16513-21
pubmed: 10347215
J Immunol. 1995 May 15;154(10):5492-9
pubmed: 7730651
Blood. 1996 Jan 15;87(2):699-705
pubmed: 8555493
Neuroreport. 1998 Dec 1;9(17):3797-802
pubmed: 9875707
Int J Mol Sci. 2023 Jan 18;24(3):
pubmed: 36768252
Neuron. 2015 May 6;86(3):646-64
pubmed: 25950633
Neuropharmacology. 2007 Jan;52(1):146-55
pubmed: 16890252
Curr Biol. 2021 Nov 8;31(21):4748-4761.e8
pubmed: 34529938
Immunology. 2011 Apr;132(4):567-77
pubmed: 21255011
ACS Chem Neurosci. 2015 Jan 21;6(1):16-26
pubmed: 25491156

Auteurs

Joakim W Ronström (JW)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Stephanie B Williams (SB)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Andrew Payne (A)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Daniel J Obray (DJ)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Caylor Hafen (C)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Matthew Burris (M)

Brigham Young University, Department of Cellular Biology and Physiology, Provo, UT 84602, United States.

K Scott Weber (K)

Brigham Young University, Department of Microbiology and Molecular Biology, Provo, UT 84602, United States.

Scott C Steffensen (SC)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States.

Jordan T Yorgason (JT)

Brigham Young University, Department of Psychology/Neuroscience, Provo, UT 84602, United States; Brigham Young University, Department of Cellular Biology and Physiology, Provo, UT 84602, United States. Electronic address: jordanyorg@byu.edu.

Articles similaires

Perylene Dopamine Electrochemical Techniques Imides Luminescent Measurements
Humans Monocarboxylic Acid Transporters Glioblastoma Cell Movement Cell Proliferation
Animals Obesity Diet, High-Fat Swine Proto-Oncogene Proteins c-akt

Classifications MeSH