Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia

Schizophrenia is a neuropsychiatric illness characterized by altered neurotransmission, in which adenosine, a modulator of glutamate and dopamine, plays a critical role that is relatively unexplored in the human brain. In the present study, postmortem human brain tissue from the anterior cingulate c...

Full description

Saved in:
Bibliographic Details
Main Authors: Smita Sahay, Emily A. Devine, Christina F.-A. Vargas, Robert E. McCullumsmith, Sinead M. O’Donovan
Format: Article
Language:English
Published: MDPI AG 2024-10-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/13/19/1657
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850283826047090688
author Smita Sahay
Emily A. Devine
Christina F.-A. Vargas
Robert E. McCullumsmith
Sinead M. O’Donovan
author_facet Smita Sahay
Emily A. Devine
Christina F.-A. Vargas
Robert E. McCullumsmith
Sinead M. O’Donovan
author_sort Smita Sahay
collection DOAJ
description Schizophrenia is a neuropsychiatric illness characterized by altered neurotransmission, in which adenosine, a modulator of glutamate and dopamine, plays a critical role that is relatively unexplored in the human brain. In the present study, postmortem human brain tissue from the anterior cingulate cortex (ACC) of individuals with schizophrenia (<i>n</i> = 20) and sex- and age-matched control subjects without psychiatric illness (<i>n</i> = 20) was obtained from the Bronx–Mount Sinai NIH Brain and Tissue Repository. Enriched populations of ACC pyramidal neurons were isolated using laser microdissection (LMD). The mRNA expression levels of six key adenosine pathway components—adenosine kinase (ADK), equilibrative nucleoside transporters 1 and 2 (ENT1 and ENT2), ectonucleoside triphosphate diphosphohydrolases 1 and 3 (ENTPD1 and ENTPD3), and ecto-5′-nucleotidase (NT5E)—were quantified using real-time PCR (qPCR) in neurons from these individuals. No significant mRNA expression differences were observed between the schizophrenia and control groups (<i>p</i> > 0.05). However, a significant sex difference was found in ADK mRNA expression, with higher levels in male compared with female subjects (Mann–Whitney U = 86; <i>p</i> < 0.05), a finding significantly driven by disease (t<sub>(17)</sub> = 3.289; <i>p <</i> 0.05). Correlation analyses also demonstrated significant associations (<i>n</i> = 12) between the expression of several adenosine pathway components (<i>p</i> < 0.05). In our dementia severity analysis, ENTPD1 mRNA expression was significantly higher in males in the “mild” clinical dementia rating (CDR) bin compared with males in the “none” CDR bin (F<sub>(2, 13)</sub> = 5.212; <i>p < 0.05</i>). Lastly, antipsychotic analysis revealed no significant impact on the expression of adenosine pathway components between medicated and non-medicated schizophrenia subjects (<i>p</i> > 0.05). The observed sex-specific variations and inter-component correlations highlight the value of investigating sex differences in disease and contribute to the molecular basis of schizophrenia’s pathology.
format Article
id doaj-art-833e0b4929eb46729b2bc3565f62e9f2
institution OA Journals
issn 2073-4409
language English
publishDate 2024-10-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj-art-833e0b4929eb46729b2bc3565f62e9f22025-08-20T01:47:42ZengMDPI AGCells2073-44092024-10-011319165710.3390/cells13191657Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in SchizophreniaSmita Sahay0Emily A. Devine1Christina F.-A. Vargas2Robert E. McCullumsmith3Sinead M. O’Donovan4Department of Neurosciences & Psychiatry, University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USADepartment of Pharmacology and Systems Physiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267, USADepartment of Neurosciences & Psychiatry, University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USADepartment of Neurosciences & Psychiatry, University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USADepartment of Neurosciences & Psychiatry, University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USASchizophrenia is a neuropsychiatric illness characterized by altered neurotransmission, in which adenosine, a modulator of glutamate and dopamine, plays a critical role that is relatively unexplored in the human brain. In the present study, postmortem human brain tissue from the anterior cingulate cortex (ACC) of individuals with schizophrenia (<i>n</i> = 20) and sex- and age-matched control subjects without psychiatric illness (<i>n</i> = 20) was obtained from the Bronx–Mount Sinai NIH Brain and Tissue Repository. Enriched populations of ACC pyramidal neurons were isolated using laser microdissection (LMD). The mRNA expression levels of six key adenosine pathway components—adenosine kinase (ADK), equilibrative nucleoside transporters 1 and 2 (ENT1 and ENT2), ectonucleoside triphosphate diphosphohydrolases 1 and 3 (ENTPD1 and ENTPD3), and ecto-5′-nucleotidase (NT5E)—were quantified using real-time PCR (qPCR) in neurons from these individuals. No significant mRNA expression differences were observed between the schizophrenia and control groups (<i>p</i> > 0.05). However, a significant sex difference was found in ADK mRNA expression, with higher levels in male compared with female subjects (Mann–Whitney U = 86; <i>p</i> < 0.05), a finding significantly driven by disease (t<sub>(17)</sub> = 3.289; <i>p <</i> 0.05). Correlation analyses also demonstrated significant associations (<i>n</i> = 12) between the expression of several adenosine pathway components (<i>p</i> < 0.05). In our dementia severity analysis, ENTPD1 mRNA expression was significantly higher in males in the “mild” clinical dementia rating (CDR) bin compared with males in the “none” CDR bin (F<sub>(2, 13)</sub> = 5.212; <i>p < 0.05</i>). Lastly, antipsychotic analysis revealed no significant impact on the expression of adenosine pathway components between medicated and non-medicated schizophrenia subjects (<i>p</i> > 0.05). The observed sex-specific variations and inter-component correlations highlight the value of investigating sex differences in disease and contribute to the molecular basis of schizophrenia’s pathology.https://www.mdpi.com/2073-4409/13/19/1657adenosine kinaseequilibrative nucleoside transportersectonucleoside triphosphate diphosphohydrolasesecto-5′-nucleotidasesneuromodulationpyramidal neurons
spellingShingle Smita Sahay
Emily A. Devine
Christina F.-A. Vargas
Robert E. McCullumsmith
Sinead M. O’Donovan
Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
Cells
adenosine kinase
equilibrative nucleoside transporters
ectonucleoside triphosphate diphosphohydrolases
ecto-5′-nucleotidases
neuromodulation
pyramidal neurons
title Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
title_full Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
title_fullStr Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
title_full_unstemmed Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
title_short Adenosine Metabolism Pathway Alterations in Frontal Cortical Neurons in Schizophrenia
title_sort adenosine metabolism pathway alterations in frontal cortical neurons in schizophrenia
topic adenosine kinase
equilibrative nucleoside transporters
ectonucleoside triphosphate diphosphohydrolases
ecto-5′-nucleotidases
neuromodulation
pyramidal neurons
url https://www.mdpi.com/2073-4409/13/19/1657
work_keys_str_mv AT smitasahay adenosinemetabolismpathwayalterationsinfrontalcorticalneuronsinschizophrenia
AT emilyadevine adenosinemetabolismpathwayalterationsinfrontalcorticalneuronsinschizophrenia
AT christinafavargas adenosinemetabolismpathwayalterationsinfrontalcorticalneuronsinschizophrenia
AT robertemccullumsmith adenosinemetabolismpathwayalterationsinfrontalcorticalneuronsinschizophrenia
AT sineadmodonovan adenosinemetabolismpathwayalterationsinfrontalcorticalneuronsinschizophrenia