Electroconvulsive shock restores the decreased coverage of brain blood vessels by astrocytic endfeet and ameliorates depressive-like behavior.


Journal

Journal of affective disorders
ISSN: 1573-2517
Titre abrégé: J Affect Disord
Pays: Netherlands
ID NLM: 7906073

Informations de publication

Date de publication:
01 10 2019
Historique:
received: 21 02 2019
revised: 30 06 2019
accepted: 03 07 2019
pubmed: 16 7 2019
medline: 25 6 2020
entrez: 15 7 2019
Statut: ppublish

Résumé

Although growing evidence indicates that ECT affects astrocytes, the exact mechanisms of the therapeutic effect of ECT are still unknown. Astrocytic endfeet express the water channel aquaporin (AQP) 4 abundantly and ensheath brain blood vessels to form gliovascular units. It has been shown that the coverage of blood vessels by AQP4-immunostained endfeet is decreased in the prefrontal cortex (PFC) of patients with major depression. This study was made to determine whether ECT restores the astrocytic coverage of blood vessels with amelioration of depressive symptoms. After electroconvulsive shock (ECS) administration to rats, the forced swimming test (FST) and Y-maze test were performed. Subsequently, immunofluorescence analysis was conducted to measure the coverage of blood vessels by astrocytic endfeet in the PFC and hippocampus by using the endothelial cell marker lectin and anti-AQP4 antibody. We also performed Western blot to examine the effects of ECS on the hippocampal expression of AQP4 and the tight junction molecule claudin-5. Gunn rats showed learned helplessness and impaired spatial working memory, compared to normal control Wistar rats. ECS significantly improved the depressive-like behavior. Gunn rats showed a decrease in astrocytic coverage of blood vessels, that was significantly increased by ECS. ECS significantly increased expression of AQP4 and claudin-5 in Gunn rats. ECS increased the reduced coverage of blood vessels by astrocytic endfeet in the mPFC and hippocampus with amelioration of depressive-like behavior. Therefore, therapeutic mechanism of ECT may involve restoration of the impaired gliovascular units by increasing the astrocytic-endfoot coverage of blood vessels.

Sections du résumé

BACKGROUND
Although growing evidence indicates that ECT affects astrocytes, the exact mechanisms of the therapeutic effect of ECT are still unknown. Astrocytic endfeet express the water channel aquaporin (AQP) 4 abundantly and ensheath brain blood vessels to form gliovascular units. It has been shown that the coverage of blood vessels by AQP4-immunostained endfeet is decreased in the prefrontal cortex (PFC) of patients with major depression. This study was made to determine whether ECT restores the astrocytic coverage of blood vessels with amelioration of depressive symptoms.
METHODS
After electroconvulsive shock (ECS) administration to rats, the forced swimming test (FST) and Y-maze test were performed. Subsequently, immunofluorescence analysis was conducted to measure the coverage of blood vessels by astrocytic endfeet in the PFC and hippocampus by using the endothelial cell marker lectin and anti-AQP4 antibody. We also performed Western blot to examine the effects of ECS on the hippocampal expression of AQP4 and the tight junction molecule claudin-5.
RESULTS
Gunn rats showed learned helplessness and impaired spatial working memory, compared to normal control Wistar rats. ECS significantly improved the depressive-like behavior. Gunn rats showed a decrease in astrocytic coverage of blood vessels, that was significantly increased by ECS. ECS significantly increased expression of AQP4 and claudin-5 in Gunn rats.
CONCLUSIONS
ECS increased the reduced coverage of blood vessels by astrocytic endfeet in the mPFC and hippocampus with amelioration of depressive-like behavior. Therefore, therapeutic mechanism of ECT may involve restoration of the impaired gliovascular units by increasing the astrocytic-endfoot coverage of blood vessels.

Identifiants

pubmed: 31302522
pii: S0165-0327(19)30467-7
doi: 10.1016/j.jad.2019.07.008
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

331-339

Informations de copyright

Copyright © 2019. Published by Elsevier B.V.

Auteurs

Ilhamuddin A Azis (IA)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan; Department of Psychiatry, Hasanuddin University, Jl. Perintis Kemerdekaan Km. 10, Makassar 90245, South Sulawesi, Indonesia; Department of Biochemistry, Hasanuddin University, Jl. Perintis Kemerdekaan Km. 10, Makassar 90245, South Sulawesi, Indonesia.

Sadayuki Hashioka (S)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: hashioka@f2.dion.ne.jp.

Keiko Tsuchie (K)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: keits@med.shimane-u.ac.jp.

Tsuyoshi Miyaoka (T)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: miyanyan@med.shimane-u.ac.jp.

Rostia A Abdullah (RA)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan.

Erlyn Limoa (E)

Department of Psychiatry, Hasanuddin University, Jl. Perintis Kemerdekaan Km. 10, Makassar 90245, South Sulawesi, Indonesia.

Ryosuke Arauchi (R)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: arauchi@med.shimane-u.ac.jp.

Ken Inoue (K)

Health Service Center, Kochi University, Akebono-cho, Kochi 780-8520, Japan. Electronic address: ke-inoue@kochi-u.ac.jp.

Shoko Miura (S)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: mo114928@med.shimane-u.ac.jp.

Muneto Izuhara (M)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan.

Misako Kanayama (M)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: misakoka@med.shimane-u.ac.jp.

Koji Otsuki (K)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: kotsuki@med.shimane-u.ac.jp.

Michiharu Nagahama (M)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: michi@med.shimane-u.ac.jp.

Kiminori Kawano (K)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: kkawano@med.shimane-u.ac.jp.

Tomoko Araki (T)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: tomokoa@med.shimane-u.ac.jp.

Maiko Hayashida (M)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: maiko-s@med.shimane-u.ac.jp.

Rei Wake (R)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: rei@med.shimane-u.ac.jp.

Arata Oh-Nishi (A)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: arata@resvo-inc.com.

Andi J Tanra (AJ)

Department of Psychiatry, Hasanuddin University, Jl. Perintis Kemerdekaan Km. 10, Makassar 90245, South Sulawesi, Indonesia.

Jun Horiguchi (J)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: jhorigu@med.shimane-u.ac.jp.

Masatoshi Inagaki (M)

Department of Psychiatry, Shimane University, 89-1 Enya-cho, Izumo 693-8501, Japan. Electronic address: minagaki@med.shimane-u.ac.jp.

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