Prostaglandin-dependent modulation of dopaminergic neurotransmission elicits inflammation-induced aversion in mice

Systemic inflammation causes malaise and general feelings of discomfort. This fundamental aspect of the sickness response reduces the quality of life for people suffering from chronic inflammatory diseases and is a nuisance during mild infections like common colds or the flu. To investigate how infl...

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Published in:	The Journal of clinical investigation Vol. 126; no. 2; pp. 695 - 705
Main Authors:	Fritz, Michael, Klawonn, Anna M., Nilsson, Anna, Singh, Anand Kumar, Zajdel, Joanna, Björk Wilhelms, Daniel, Lazarus, Michael, Löfberg, Andreas, Jaarola, Maarit, Örtegren Kugelberg, Unn, Billiar, Timothy R., Hackam, David J., Sodhi, Chhinder P., Breyer, Matthew D., Jakobsson, Johan, Schwaninger, Markus, Schütz, Günther, Rodriguez Parkitna, Jan, Saper, Clifford B., Blomqvist, Anders, Engblom, David
Format:	Journal Article
Language:	English
Published:	United States American Society for Clinical Investigation 01.02.2016
Subjects:	Animals Basic Medicine Biomedical research Brain - metabolism Brain - pathology Brain Diseases - genetics Brain Diseases - metabolism Brain Diseases - pathology Brain research Cell Line Councils Cyclooxygenase 1 - genetics Cyclooxygenase 1 - metabolism Dinoprostone - genetics Dinoprostone - metabolism Dopaminergic mechanisms Dopaminergic Neurons - metabolism Dopaminergic Neurons - pathology Endothelium Endothelium, Vascular - metabolism Endothelium, Vascular - pathology Experiments Health aspects Inflammation Inflammation - genetics Inflammation - metabolism Inflammation - pathology Medical and Health Sciences Medicin och hälsovetenskap Medicinska och farmaceutiska grundvetenskaper Membrane Proteins - genetics Membrane Proteins - metabolism Mice Mice, Knockout Neural transmission Neurosciences Neurovetenskaper Physiological aspects Properties Prostaglandins Receptors, Dopamine D1 - genetics Receptors, Dopamine D1 - metabolism Rodents Social research Synaptic Transmission
ISSN:	0021-9738, 1558-8238, 1558-8238
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Abstract	Systemic inflammation causes malaise and general feelings of discomfort. This fundamental aspect of the sickness response reduces the quality of life for people suffering from chronic inflammatory diseases and is a nuisance during mild infections like common colds or the flu. To investigate how inflammation is perceived as unpleasant and causes negative affect, we used a behavioral test in which mice avoid an environment that they have learned to associate with inflammation-induced discomfort. Using a combination of cell-type–specific gene deletions, pharmacology, and chemogenetics, we found that systemic inflammation triggered aversion through MyD88-dependent activation of the brain endothelium followed by COX1-mediated cerebral prostaglandin E2 (PGE2) synthesis. Further, we showed that inflammation-induced PGE2 targeted EP1 receptors on striatal dopamine D1 receptor–expressing neurons and that this signaling sequence induced aversion through GABA-mediated inhibition of dopaminergic cells. Finally, we demonstrated that inflammation-induced aversion was not an indirect consequence of fever or anorexia but that it constituted an independent inflammatory symptom triggered by a unique molecular mechanism. Collectively, these findings demonstrate that PGE2-mediated modulation of the dopaminergic motivational circuitry is a key mechanism underlying the negative affect induced by inflammation.
AbstractList	Systemic inflammation causes malaise and general feelings of discomfort. This fundamental aspect of the sickness response reduces the quality of life for people suffering from chronic inflammatory diseases and is a nuisance during mild infections like common colds or the flu. To investigate how inflammation is perceived as unpleasant and causes negative affect, we used a behavioral test in which mice avoid an environment that they have learned to associate with inflammation-induced discomfort. Using a combination of cell-type-specific gene deletions, pharmacology, and chemogenetics, we found that systemic inflammation triggered aversion through MyD88-dependent activation of the brain endothelium followed by COX1-mediated cerebral prostaglandin [E.sub.2] ([PGE.sub.2]) synthesis. Further, we showed that inflammation- induced [PGE.sub.2] targeted EP1 receptors on striatal dopamine D1 receptor-expressing neurons and that this signaling sequence induced aversion through GABA-mediated inhibition of dopaminergic cells. Finally, we demonstrated that inflammation-induced aversion was not an indirect consequence of fever or anorexia but that it constituted an independent inflammatory symptom triggered by a unique molecular mechanism. Collectively, these findings demonstrate that [PGE.sub.2]-mediated modulation of the dopaminergic motivational circuitry is a key mechanism underlying the negative affect induced by inflammation. Systemic inflammation causes malaise and general feelings of discomfort. This fundamental aspect of the sickness response reduces the quality of life for people suffering from chronic inflammatory diseases and is a nuisance during mild infections like common colds or the flu. To investigate how inflammation is perceived as unpleasant and causes negative affect, we used a behavioral test in which mice avoid an environment that they have learned to associate with inflammation-induced discomfort. Using a combination of cell-type–specific gene deletions, pharmacology, and chemogenetics, we found that systemic inflammation triggered aversion through MyD88-dependent activation of the brain endothelium followed by COX1-mediated cerebral prostaglandin E2 (PGE2) synthesis. Further, we showed that inflammation-induced PGE2 targeted EP1 receptors on striatal dopamine D1 receptor–expressing neurons and that this signaling sequence induced aversion through GABA-mediated inhibition of dopaminergic cells. Finally, we demonstrated that inflammation-induced aversion was not an indirect consequence of fever or anorexia but that it constituted an independent inflammatory symptom triggered by a unique molecular mechanism. Collectively, these findings demonstrate that PGE2-mediated modulation of the dopaminergic motivational circuitry is a key mechanism underlying the negative affect induced by inflammation. Systemic inflammation causes malaise and general feelings of discomfort. This fundamental aspect of the sickness response reduces the quality of life for people suffering from chronic inflammatory diseases and is a nuisance during mild infections like common colds or the flu. To investigate how inflammation is perceived as unpleasant and causes negative affect, we used a behavioral test in which mice avoid an environment that they have learned to associate with inflammation-induced discomfort. Using a combination of cell-type-specific gene deletions, pharmacology, and chemogenetics, we found that systemic inflammation triggered aversion through MyD88-dependent activation of the brain endothelium followed by COX1-mediated cerebral prostaglandin E-2 (PGE(2)) synthesis. Further, we showed that inflammation-induced PGE(2) targeted EP1 receptors on striatal dopamine D1 receptor-expressing neurons and that this signaling sequence induced aversion through GABA-mediated inhibition of dopaminergic cells. Finally, we demonstrated that inflammation-induced aversion was not an indirect consequence of fever or anorexia but that it constituted an independent inflammatory symptom triggered by a unique molecular mechanism. Collectively, these findings demonstrate that PGE(2)-mediated modulation of the dopaminergic motivational circuitry is a key mechanism underlying the negative affect induced by inflammation.
Audience	Academic
Author	Engblom, David Billiar, Timothy R. Nilsson, Anna Singh, Anand Kumar Fritz, Michael Löfberg, Andreas Zajdel, Joanna Sodhi, Chhinder P. Saper, Clifford B. Örtegren Kugelberg, Unn Rodriguez Parkitna, Jan Björk Wilhelms, Daniel Jaarola, Maarit Blomqvist, Anders Klawonn, Anna M. Breyer, Matthew D. Schütz, Günther Jakobsson, Johan Hackam, David J. Schwaninger, Markus Lazarus, Michael
AuthorAffiliation	8 Institute of Experimental and Clinical Pharmacology and Toxicology, University of Lübeck, Lübeck, Germany 11 Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School Boston, Massachusetts, USA 4 Department of Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA 10 Department of Molecular Neuropharmacology, Institute of Pharmacology of the Polish Academy of Sciences, Krakow, Poland 2 Department of Emergency Medicine, Linköping University, Linköping, Sweden 1 Department of Clinical and Experimental Medicine and 7 Wallenberg Neuroscience Center and Lund Stem Cell Center, Lund University, Lund, Sweden 5 Department of Surgery, Johns Hopkins University, Baltimore, Maryland, USA 6 Biotechnology Discovery Research, Lilly Research Laboratories, Indianapolis, Indiana, USA 9 Molecular Biology of the Cell I, German Cancer Research Center, Heidelberg, Germany 3 International Institute for Integrative Sleep Medicine, University of Tsukuba, Tsukuba,
AuthorAffiliation_xml	– name: 8 Institute of Experimental and Clinical Pharmacology and Toxicology, University of Lübeck, Lübeck, Germany – name: 3 International Institute for Integrative Sleep Medicine, University of Tsukuba, Tsukuba, Japan – name: 10 Department of Molecular Neuropharmacology, Institute of Pharmacology of the Polish Academy of Sciences, Krakow, Poland – name: 1 Department of Clinical and Experimental Medicine and – name: 6 Biotechnology Discovery Research, Lilly Research Laboratories, Indianapolis, Indiana, USA – name: 4 Department of Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA – name: 5 Department of Surgery, Johns Hopkins University, Baltimore, Maryland, USA – name: 9 Molecular Biology of the Cell I, German Cancer Research Center, Heidelberg, Germany – name: 11 Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School Boston, Massachusetts, USA – name: 7 Wallenberg Neuroscience Center and Lund Stem Cell Center, Lund University, Lund, Sweden – name: 2 Department of Emergency Medicine, Linköping University, Linköping, Sweden
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26690700$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:liu:diva-126263$$DView record from Swedish Publication Index (Linköpings universitet)
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Copyright	COPYRIGHT 2016 American Society for Clinical Investigation Copyright American Society for Clinical Investigation Feb 2016 Copyright © 2016, American Society for Clinical Investigation 2016 American Society for Clinical Investigation
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Title	Prostaglandin-dependent modulation of dopaminergic neurotransmission elicits inflammation-induced aversion in mice
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