Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus

Inhibitory γ-aminobutyric acid (GABA)-ergic interneurons mediate inhibition in neuronal circuitry and support normal brain function. Consequently, dysregulation of inhibition is implicated in various brain disorders. Parvalbumin (PV) and somatostatin (SST) interneurons, the two major types of GABAer...

Full description

Bibliographic Details
Main Authors: Tzu-Hsuan Huang, Yi-Sian Lin, Chiao-Wan Hsiao, Liang-Yun Wang, Musa Iyiola Ajibola, Wahab Imam Abdulmajeed, Yu-Ling Lin, Yu-Jui Li, Cho-Yi Chen, Cheng-Chang Lien, Cheng-Di Chiu, Irene Han-Juo Cheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2023.1146278/full
_version_ 1797776414582243328
author Tzu-Hsuan Huang
Yi-Sian Lin
Yi-Sian Lin
Chiao-Wan Hsiao
Chiao-Wan Hsiao
Liang-Yun Wang
Musa Iyiola Ajibola
Musa Iyiola Ajibola
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Yu-Ling Lin
Yu-Jui Li
Cho-Yi Chen
Cho-Yi Chen
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Irene Han-Juo Cheng
Irene Han-Juo Cheng
Irene Han-Juo Cheng
author_facet Tzu-Hsuan Huang
Yi-Sian Lin
Yi-Sian Lin
Chiao-Wan Hsiao
Chiao-Wan Hsiao
Liang-Yun Wang
Musa Iyiola Ajibola
Musa Iyiola Ajibola
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Yu-Ling Lin
Yu-Jui Li
Cho-Yi Chen
Cho-Yi Chen
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Irene Han-Juo Cheng
Irene Han-Juo Cheng
Irene Han-Juo Cheng
author_sort Tzu-Hsuan Huang
collection DOAJ
description Inhibitory γ-aminobutyric acid (GABA)-ergic interneurons mediate inhibition in neuronal circuitry and support normal brain function. Consequently, dysregulation of inhibition is implicated in various brain disorders. Parvalbumin (PV) and somatostatin (SST) interneurons, the two major types of GABAergic inhibitory interneurons in the hippocampus, exhibit distinct morpho-physiological properties and coordinate information processing and memory formation. However, the molecular mechanisms underlying the specialized properties of PV and SST interneurons remain unclear. This study aimed to compare the transcriptomic differences between these two classes of interneurons in the hippocampus using the ribosome tagging approach. The results revealed distinct expressions of genes such as voltage-gated ion channels and GABAA receptor subunits between PV and SST interneurons. Gabrd and Gabra6 were identified as contributors to the contrasting tonic GABAergic inhibition observed in PV and SST interneurons. Moreover, some of the differentially expressed genes were associated with schizophrenia and epilepsy. In conclusion, our results provide molecular insights into the distinct roles of PV and SST interneurons in health and disease.
first_indexed 2024-03-12T22:49:37Z
format Article
id doaj.art-f5e31084e68641afac963fc78b986bd5
institution Directory Open Access Journal
issn 1662-5102
language English
last_indexed 2024-03-12T22:49:37Z
publishDate 2023-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular Neuroscience
spelling doaj.art-f5e31084e68641afac963fc78b986bd52023-07-20T16:30:30ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-07-011710.3389/fncel.2023.11462781146278Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampusTzu-Hsuan Huang0Yi-Sian Lin1Yi-Sian Lin2Chiao-Wan Hsiao3Chiao-Wan Hsiao4Liang-Yun Wang5Musa Iyiola Ajibola6Musa Iyiola Ajibola7Wahab Imam Abdulmajeed8Wahab Imam Abdulmajeed9Wahab Imam Abdulmajeed10Yu-Ling Lin11Yu-Jui Li12Cho-Yi Chen13Cho-Yi Chen14Cheng-Chang Lien15Cheng-Chang Lien16Cheng-Chang Lien17Cheng-Chang Lien18Cheng-Di Chiu19Cheng-Di Chiu20Cheng-Di Chiu21Cheng-Di Chiu22Irene Han-Juo Cheng23Irene Han-Juo Cheng24Irene Han-Juo Cheng25Institute of Brain Science, National Yang Ming Chiao Tung University, Taipei, TaiwanInstitute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, TaiwanProgram in Genetics and Genomics, Baylor College of Medicine, Houston, TX, United StatesInstitute of Brain Science, National Yang Ming Chiao Tung University, Taipei, TaiwanProgram in Molecular Medicine, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanInstitute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, TaiwanInstitute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, College of Life Sciences, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanInstitute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, College of Life Sciences, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanDepartment of Physiology, Faculty of Basic Medical Sciences, College of Health Sciences, University of Ilorin, Ilorin, NigeriaInstitute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, TaiwanInstitute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, TaiwanInstitute of Biomedical Informatics, National Yang Ming Chiao Tung University, Taipei, TaiwanBrain Research Center, National Yang Ming Chiao Tung University, Taipei, TaiwanProgram in Molecular Medicine, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanInstitute of Neuroscience, National Yang Ming Chiao Tung University, Taipei, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, College of Life Sciences, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanBrain Research Center, National Yang Ming Chiao Tung University, Taipei, TaiwanDepartment of Neurosurgery, China Medical University Hospital, Taichung, Taiwan0Spine Center, China Medical University Hospital, Taichung, Taiwan1Graduate Institute of Biomedical Science, China Medical University, Taichung, Taiwan2School of Medicine, China Medical University, Taichung, TaiwanInstitute of Brain Science, National Yang Ming Chiao Tung University, Taipei, TaiwanProgram in Molecular Medicine, National Yang Ming Chiao Tung University and Academia Sinica, Taipei, TaiwanBrain Research Center, National Yang Ming Chiao Tung University, Taipei, TaiwanInhibitory γ-aminobutyric acid (GABA)-ergic interneurons mediate inhibition in neuronal circuitry and support normal brain function. Consequently, dysregulation of inhibition is implicated in various brain disorders. Parvalbumin (PV) and somatostatin (SST) interneurons, the two major types of GABAergic inhibitory interneurons in the hippocampus, exhibit distinct morpho-physiological properties and coordinate information processing and memory formation. However, the molecular mechanisms underlying the specialized properties of PV and SST interneurons remain unclear. This study aimed to compare the transcriptomic differences between these two classes of interneurons in the hippocampus using the ribosome tagging approach. The results revealed distinct expressions of genes such as voltage-gated ion channels and GABAA receptor subunits between PV and SST interneurons. Gabrd and Gabra6 were identified as contributors to the contrasting tonic GABAergic inhibition observed in PV and SST interneurons. Moreover, some of the differentially expressed genes were associated with schizophrenia and epilepsy. In conclusion, our results provide molecular insights into the distinct roles of PV and SST interneurons in health and disease.https://www.frontiersin.org/articles/10.3389/fncel.2023.1146278/fulltonic inhibitionsomatostatin (SST)parvalbumin (PV)RiboTagGABAA receptorGABRD
spellingShingle Tzu-Hsuan Huang
Yi-Sian Lin
Yi-Sian Lin
Chiao-Wan Hsiao
Chiao-Wan Hsiao
Liang-Yun Wang
Musa Iyiola Ajibola
Musa Iyiola Ajibola
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Wahab Imam Abdulmajeed
Yu-Ling Lin
Yu-Jui Li
Cho-Yi Chen
Cho-Yi Chen
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Chang Lien
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Cheng-Di Chiu
Irene Han-Juo Cheng
Irene Han-Juo Cheng
Irene Han-Juo Cheng
Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
Frontiers in Cellular Neuroscience
tonic inhibition
somatostatin (SST)
parvalbumin (PV)
RiboTag
GABAA receptor
GABRD
title Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
title_full Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
title_fullStr Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
title_full_unstemmed Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
title_short Differential expression of GABAA receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
title_sort differential expression of gabaa receptor subunits δ and α6 mediates tonic inhibition in parvalbumin and somatostatin interneurons in the mouse hippocampus
topic tonic inhibition
somatostatin (SST)
parvalbumin (PV)
RiboTag
GABAA receptor
GABRD
url https://www.frontiersin.org/articles/10.3389/fncel.2023.1146278/full
work_keys_str_mv AT tzuhsuanhuang differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT yisianlin differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT yisianlin differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chiaowanhsiao differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chiaowanhsiao differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT liangyunwang differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT musaiyiolaajibola differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT musaiyiolaajibola differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT wahabimamabdulmajeed differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT wahabimamabdulmajeed differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT wahabimamabdulmajeed differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT yulinglin differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT yujuili differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT choyichen differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT choyichen differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengchanglien differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengchanglien differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengchanglien differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengchanglien differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengdichiu differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengdichiu differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengdichiu differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT chengdichiu differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT irenehanjuocheng differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT irenehanjuocheng differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus
AT irenehanjuocheng differentialexpressionofgabaareceptorsubunitsdanda6mediatestonicinhibitioninparvalbuminandsomatostatininterneuronsinthemousehippocampus