(R)-Ketamine Induces a Greater Increase in Prefrontal 5-HT Release Than (S)-Ketamine and Ketamine Metabolites via an AMPA Receptor-Independent Mechanism
Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine'...
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| Published in | The international journal of neuropsychopharmacology Vol. 22; no. 10; pp. 665 - 674 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Oxford University Press
01.10.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine's action, we investigated the effects of (R)-ketamine, (S)-ketamine, (R)-norketamine [(R)-NK], (S)-NK, (2R,6R)-hydroxynorketamine [(2R,6R)-HNK], and (2S,6S)-HNK on monoaminergic neurotransmission in the prefrontal cortex of mice.
The extracellular monoamine levels in the prefrontal cortex were measured by in vivo microdialysis.
(R)-Ketamine and (S)-ketamine acutely increased serotonin release in a dose-dependent manner, and the effect of (R)-ketamine was greater than that of (S)-ketamine. In contrast, (S)-ketamine caused a robust increase in dopamine release compared with (R)-ketamine. Both ketamine enantiomers increased noradrenaline release, but these effects did not differ. (2R,6R)-HNK caused a slight but significant increase in serotonin and noradrenaline but not dopamine release. (S)-NK increased dopamine and noradrenaline but not serotonin release. Differential effects between (R)-ketamine and (S)-ketamine were also observed in a lipopolysaccharide-induced model of depression. An α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4- tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX), attenuated (S)-ketamine-induced, but not (R)-ketamine-induced serotonin release, whereas NBQX blocked dopamine release induced by both enantiomers. Local application of (R)-ketamine into the prefrontal cortex caused a greater increase in prefrontal serotonin release than that of (S)-ketamine.
(R)-Ketamine strongly activates the prefrontal serotonergic system through an AMPA receptor-independent mechanism. (S)-Ketamine-induced serotonin and dopamine release was AMPA receptor-dependent. These findings provide a neurochemical basis for the underlying pharmacological differences between ketamine enantiomers and their metabolites. |
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| AbstractList | Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine's action, we investigated the effects of (R)-ketamine, (S)-ketamine, (R)-norketamine [(R)-NK], (S)-NK, (2R,6R)-hydroxynorketamine [(2R,6R)-HNK], and (2S,6S)-HNK on monoaminergic neurotransmission in the prefrontal cortex of mice.
The extracellular monoamine levels in the prefrontal cortex were measured by in vivo microdialysis.
(R)-Ketamine and (S)-ketamine acutely increased serotonin release in a dose-dependent manner, and the effect of (R)-ketamine was greater than that of (S)-ketamine. In contrast, (S)-ketamine caused a robust increase in dopamine release compared with (R)-ketamine. Both ketamine enantiomers increased noradrenaline release, but these effects did not differ. (2R,6R)-HNK caused a slight but significant increase in serotonin and noradrenaline but not dopamine release. (S)-NK increased dopamine and noradrenaline but not serotonin release. Differential effects between (R)-ketamine and (S)-ketamine were also observed in a lipopolysaccharide-induced model of depression. An α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4- tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX), attenuated (S)-ketamine-induced, but not (R)-ketamine-induced serotonin release, whereas NBQX blocked dopamine release induced by both enantiomers. Local application of (R)-ketamine into the prefrontal cortex caused a greater increase in prefrontal serotonin release than that of (S)-ketamine.
(R)-Ketamine strongly activates the prefrontal serotonergic system through an AMPA receptor-independent mechanism. (S)-Ketamine-induced serotonin and dopamine release was AMPA receptor-dependent. These findings provide a neurochemical basis for the underlying pharmacological differences between ketamine enantiomers and their metabolites. Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine's action, we investigated the effects of (R)-ketamine, (S)-ketamine, (R)-norketamine [(R)-NK], (S)-NK, (2R,6R)-hydroxynorketamine [(2R,6R)-HNK], and (2S,6S)-HNK on monoaminergic neurotransmission in the prefrontal cortex of mice.BACKGROUNDAlthough recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine's action, we investigated the effects of (R)-ketamine, (S)-ketamine, (R)-norketamine [(R)-NK], (S)-NK, (2R,6R)-hydroxynorketamine [(2R,6R)-HNK], and (2S,6S)-HNK on monoaminergic neurotransmission in the prefrontal cortex of mice.The extracellular monoamine levels in the prefrontal cortex were measured by in vivo microdialysis.METHODSThe extracellular monoamine levels in the prefrontal cortex were measured by in vivo microdialysis.(R)-Ketamine and (S)-ketamine acutely increased serotonin release in a dose-dependent manner, and the effect of (R)-ketamine was greater than that of (S)-ketamine. In contrast, (S)-ketamine caused a robust increase in dopamine release compared with (R)-ketamine. Both ketamine enantiomers increased noradrenaline release, but these effects did not differ. (2R,6R)-HNK caused a slight but significant increase in serotonin and noradrenaline but not dopamine release. (S)-NK increased dopamine and noradrenaline but not serotonin release. Differential effects between (R)-ketamine and (S)-ketamine were also observed in a lipopolysaccharide-induced model of depression. An α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4- tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX), attenuated (S)-ketamine-induced, but not (R)-ketamine-induced serotonin release, whereas NBQX blocked dopamine release induced by both enantiomers. Local application of (R)-ketamine into the prefrontal cortex caused a greater increase in prefrontal serotonin release than that of (S)-ketamine.RESULTS(R)-Ketamine and (S)-ketamine acutely increased serotonin release in a dose-dependent manner, and the effect of (R)-ketamine was greater than that of (S)-ketamine. In contrast, (S)-ketamine caused a robust increase in dopamine release compared with (R)-ketamine. Both ketamine enantiomers increased noradrenaline release, but these effects did not differ. (2R,6R)-HNK caused a slight but significant increase in serotonin and noradrenaline but not dopamine release. (S)-NK increased dopamine and noradrenaline but not serotonin release. Differential effects between (R)-ketamine and (S)-ketamine were also observed in a lipopolysaccharide-induced model of depression. An α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4- tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX), attenuated (S)-ketamine-induced, but not (R)-ketamine-induced serotonin release, whereas NBQX blocked dopamine release induced by both enantiomers. Local application of (R)-ketamine into the prefrontal cortex caused a greater increase in prefrontal serotonin release than that of (S)-ketamine.(R)-Ketamine strongly activates the prefrontal serotonergic system through an AMPA receptor-independent mechanism. (S)-Ketamine-induced serotonin and dopamine release was AMPA receptor-dependent. These findings provide a neurochemical basis for the underlying pharmacological differences between ketamine enantiomers and their metabolites.CONCLUSIONS(R)-Ketamine strongly activates the prefrontal serotonergic system through an AMPA receptor-independent mechanism. (S)-Ketamine-induced serotonin and dopamine release was AMPA receptor-dependent. These findings provide a neurochemical basis for the underlying pharmacological differences between ketamine enantiomers and their metabolites. Background Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and their metabolites is not fully understood. In view of the involvement of mechanisms other than the N-methyl-D-aspartate receptor in ketamine’s action, we investigated the effects of (R)-ketamine, (S)-ketamine, (R)-norketamine [(R)-NK], (S)-NK, (2R,6R)-hydroxynorketamine [(2R,6R)-HNK], and (2S,6S)-HNK on monoaminergic neurotransmission in the prefrontal cortex of mice. Methods The extracellular monoamine levels in the prefrontal cortex were measured by in vivo microdialysis. Results (R)-Ketamine and (S)-ketamine acutely increased serotonin release in a dose-dependent manner, and the effect of (R)-ketamine was greater than that of (S)-ketamine. In contrast, (S)-ketamine caused a robust increase in dopamine release compared with (R)-ketamine. Both ketamine enantiomers increased noradrenaline release, but these effects did not differ. (2R,6R)-HNK caused a slight but significant increase in serotonin and noradrenaline but not dopamine release. (S)-NK increased dopamine and noradrenaline but not serotonin release. Differential effects between (R)-ketamine and (S)-ketamine were also observed in a lipopolysaccharide-induced model of depression. An α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA) receptor antagonist, 2,3-dioxo-6-nitro-1,2,3,4- tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX), attenuated (S)-ketamine-induced, but not (R)-ketamine-induced serotonin release, whereas NBQX blocked dopamine release induced by both enantiomers. Local application of (R)-ketamine into the prefrontal cortex caused a greater increase in prefrontal serotonin release than that of (S)-ketamine. Conclusions (R)-Ketamine strongly activates the prefrontal serotonergic system through an AMPA receptor-independent mechanism. (S)-Ketamine-induced serotonin and dopamine release was AMPA receptor-dependent. These findings provide a neurochemical basis for the underlying pharmacological differences between ketamine enantiomers and their metabolites. |
| Author | Ago, Yukio Seiriki, Kaoru Yamaguchi, Takumi Tsukada, Shinji Tanaka, Tatsunori Kasai, Atsushi Igarashi, Hisato Nakazawa, Takanobu Higuchi, Momoko Hashimoto, Hitoshi Tanabe, Wataru Yokoyama, Rei Hashimoto, Kenji Nakagawa, Shinsaku |
| AuthorAffiliation | 7 Division of Bioscience, Institute for Datability Science, Osaka University , Suita, Osaka, Japan 1 Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University , Suita, Osaka, Japan 3 Interdisciplinary Program for Biomedical Sciences, Institute for Transdisciplinary Graduate Degree Programs, Osaka University , Suita, Osaka, Japan 8 Transdimensional Life Imaging Division, Institute for Open and Transdisciplinary Research Initiatives, Osaka University , Suita, Osaka, Japan 5 Division of Clinical Neuroscience, Chiba University Center for Forensic Mental Health , Chiba, Japan 6 Molecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui , Suita, Osaka, Japan 2 Laboratory of Biopharmaceutics, Graduate School of Pharmaceutical Sciences, Osaka University , Suita, Osaka, Japan 4 Department of |
| AuthorAffiliation_xml | – name: 5 Division of Clinical Neuroscience, Chiba University Center for Forensic Mental Health , Chiba, Japan – name: 6 Molecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui , Suita, Osaka, Japan – name: 3 Interdisciplinary Program for Biomedical Sciences, Institute for Transdisciplinary Graduate Degree Programs, Osaka University , Suita, Osaka, Japan – name: 4 Department of Pharmacology, Graduate School of Dentistry, Osaka University , Suita, Osaka, Japan – name: 8 Transdimensional Life Imaging Division, Institute for Open and Transdisciplinary Research Initiatives, Osaka University , Suita, Osaka, Japan – name: 1 Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University , Suita, Osaka, Japan – name: 2 Laboratory of Biopharmaceutics, Graduate School of Pharmaceutical Sciences, Osaka University , Suita, Osaka, Japan – name: 7 Division of Bioscience, Institute for Datability Science, Osaka University , Suita, Osaka, Japan |
| Author_xml | – sequence: 1 givenname: Yukio orcidid: 0000-0001-7562-4000 surname: Ago fullname: Ago, Yukio organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan, Laboratory of Biopharmaceutics, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 2 givenname: Wataru surname: Tanabe fullname: Tanabe, Wataru organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 3 givenname: Momoko surname: Higuchi fullname: Higuchi, Momoko organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 4 givenname: Shinji surname: Tsukada fullname: Tsukada, Shinji organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 5 givenname: Tatsunori surname: Tanaka fullname: Tanaka, Tatsunori organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 6 givenname: Takumi surname: Yamaguchi fullname: Yamaguchi, Takumi organization: Laboratory of Biopharmaceutics, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 7 givenname: Hisato surname: Igarashi fullname: Igarashi, Hisato organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 8 givenname: Rei surname: Yokoyama fullname: Yokoyama, Rei organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 9 givenname: Kaoru surname: Seiriki fullname: Seiriki, Kaoru organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan, Interdisciplinary Program for Biomedical Sciences, Institute for Transdisciplinary Graduate Degree Programs, Osaka University, Suita, Osaka, Japan – sequence: 10 givenname: Atsushi orcidid: 0000-0002-1612-3078 surname: Kasai fullname: Kasai, Atsushi organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 11 givenname: Takanobu orcidid: 0000-0003-4863-1277 surname: Nakazawa fullname: Nakazawa, Takanobu organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan, Department of Pharmacology, Graduate School of Dentistry, Osaka University, Suita, Osaka, Japan – sequence: 12 givenname: Shinsaku surname: Nakagawa fullname: Nakagawa, Shinsaku organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan, Laboratory of Biopharmaceutics, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 13 givenname: Kenji surname: Hashimoto fullname: Hashimoto, Kenji organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan – sequence: 14 givenname: Hitoshi orcidid: 0000-0001-6548-4016 surname: Hashimoto fullname: Hashimoto, Hitoshi organization: Laboratory of Molecular Neuropharmacology, Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka, Japan, Division of Clinical Neuroscience, Chiba University Center for Forensic Mental Health, Chiba, Japan, Molecular Research Center for Children’s Mental Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Suita, Osaka, Japan, Division of Bioscience, Institute for Datability Science, Osaka University, Suita, Osaka, Japan, Transdimensional Life Imaging Division, Institute for Open and Transdisciplinary Research Initiatives, Osaka University, Suita, Osaka, Japan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31325908$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s) 2019. Published by Oxford University Press on behalf of CINP. The Author(s) 2019. Published by Oxford University Press on behalf of CINP. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. The Author(s) 2019. Published by Oxford University Press on behalf of CINP. 2019 |
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| DOI | 10.1093/ijnp/pyz041 |
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| Issue | 10 |
| Keywords | (S)-ketamine AMPA receptors (R)-ketamine monoamine prefrontal cortex |
| Language | English |
| License | http://creativecommons.org/licenses/by-nc/4.0 The Author(s) 2019. Published by Oxford University Press on behalf of CINP. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Y.A. and W.T contributed equally to this work. |
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| Snippet | Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine enantiomers and... Background Although recent studies provide insight into the molecular mechanisms of the effects of ketamine, the antidepressant mechanism of ketamine... |
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| SubjectTerms | Animals Disease Models, Animal Dopamine Dopamine - metabolism Dose-Response Relationship, Drug Ketamine Ketamine - administration & dosage Ketamine - analogs & derivatives Ketamine - antagonists & inhibitors Ketamine - pharmacology Lipopolysaccharides Male Metabolites Mice Microdialysis Microinjections Norepinephrine - metabolism Prefrontal Cortex - metabolism Quinoxalines - pharmacology Receptors, AMPA - metabolism Regular Serotonin Serotonin - metabolism Stereoisomerism |
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| Title | (R)-Ketamine Induces a Greater Increase in Prefrontal 5-HT Release Than (S)-Ketamine and Ketamine Metabolites via an AMPA Receptor-Independent Mechanism |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/31325908 https://www.proquest.com/docview/3169885201 https://www.proquest.com/docview/2261976404 https://pubmed.ncbi.nlm.nih.gov/PMC6822138 |
| Volume | 22 |
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