TRPV4 activation at the physiological temperature is a critical determinant of neuronal excitability and behavior

Koji Shibasaki, Shouta Sugio, Keizo Takao, Akihiro Yamanaka, Tsuyoshi Miyakawa, Makoto Tominaga, Yasuki Ishizaki

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

For homeothermic animals, constant body temperature is an important determinant of brain function. It is well established that changes in brain temperature dynamically influence hippocampal activity. We previously reported that the thermosensor TRPV4 (activated above 34 °C) is activated at the physiological temperature in hippocampal neurons and controls neuronal excitability in vitro. Here, we examined if TRPV4 regulates neuronal excitability through its activation at the physiological temperature in vivo. We found that TRPV4-deficient (TRPV4KO) mice exhibit reduced depression-like and social behaviors compared to wild-type (WT) mice, and the number of c-fos positive cells in the dentate gyrus was significantly reduced upon the depression-like behaviors. We measured resting membrane potentials (RMPs) in the hippocampal granule cells from slice preparations at 35 °C and found that TRPV4-positive neurons significantly depolarized the RMPs through TRPV4 activation at the physiological temperature. The depolarization increased the spike numbers depending on the enhancement of TRPV4 activation. We also found that theta-frequency electroencephalogram (EEG) activities in TRPV4KO mice during wake periods were significantly reduced compared with those in WT mice. Taken together, we report for the first time that TRPV4 activation at the physiological temperature is important to regulate neuronal excitability and behaviors in mammals.

Original languageEnglish
Pages (from-to)2495-2507
Number of pages13
JournalPflugers Archiv European Journal of Physiology
Volume467
Issue number12
DOIs
Publication statusPublished - 01-12-2015

Fingerprint

Chemical activation
Temperature
Membrane Potentials
Neurons
Brain
Depression
Social Behavior
Membranes
Dentate Gyrus
Body Temperature
Mammals
Depolarization
Electroencephalography
Animals
Cells

All Science Journal Classification (ASJC) codes

  • Physiology
  • Clinical Biochemistry
  • Physiology (medical)

Cite this

Shibasaki, Koji ; Sugio, Shouta ; Takao, Keizo ; Yamanaka, Akihiro ; Miyakawa, Tsuyoshi ; Tominaga, Makoto ; Ishizaki, Yasuki. / TRPV4 activation at the physiological temperature is a critical determinant of neuronal excitability and behavior. In: Pflugers Archiv European Journal of Physiology. 2015 ; Vol. 467, No. 12. pp. 2495-2507.
@article{ee4128afb30643d0bb77f772c7f6b520,
title = "TRPV4 activation at the physiological temperature is a critical determinant of neuronal excitability and behavior",
abstract = "For homeothermic animals, constant body temperature is an important determinant of brain function. It is well established that changes in brain temperature dynamically influence hippocampal activity. We previously reported that the thermosensor TRPV4 (activated above 34 °C) is activated at the physiological temperature in hippocampal neurons and controls neuronal excitability in vitro. Here, we examined if TRPV4 regulates neuronal excitability through its activation at the physiological temperature in vivo. We found that TRPV4-deficient (TRPV4KO) mice exhibit reduced depression-like and social behaviors compared to wild-type (WT) mice, and the number of c-fos positive cells in the dentate gyrus was significantly reduced upon the depression-like behaviors. We measured resting membrane potentials (RMPs) in the hippocampal granule cells from slice preparations at 35 °C and found that TRPV4-positive neurons significantly depolarized the RMPs through TRPV4 activation at the physiological temperature. The depolarization increased the spike numbers depending on the enhancement of TRPV4 activation. We also found that theta-frequency electroencephalogram (EEG) activities in TRPV4KO mice during wake periods were significantly reduced compared with those in WT mice. Taken together, we report for the first time that TRPV4 activation at the physiological temperature is important to regulate neuronal excitability and behaviors in mammals.",
author = "Koji Shibasaki and Shouta Sugio and Keizo Takao and Akihiro Yamanaka and Tsuyoshi Miyakawa and Makoto Tominaga and Yasuki Ishizaki",
year = "2015",
month = "12",
day = "1",
doi = "10.1007/s00424-015-1726-0",
language = "English",
volume = "467",
pages = "2495--2507",
journal = "Pflugers Archiv European Journal of Physiology",
issn = "0031-6768",
publisher = "Springer Verlag",
number = "12",

}

TRPV4 activation at the physiological temperature is a critical determinant of neuronal excitability and behavior. / Shibasaki, Koji; Sugio, Shouta; Takao, Keizo; Yamanaka, Akihiro; Miyakawa, Tsuyoshi; Tominaga, Makoto; Ishizaki, Yasuki.

In: Pflugers Archiv European Journal of Physiology, Vol. 467, No. 12, 01.12.2015, p. 2495-2507.

Research output: Contribution to journalArticle

TY - JOUR

T1 - TRPV4 activation at the physiological temperature is a critical determinant of neuronal excitability and behavior

AU - Shibasaki, Koji

AU - Sugio, Shouta

AU - Takao, Keizo

AU - Yamanaka, Akihiro

AU - Miyakawa, Tsuyoshi

AU - Tominaga, Makoto

AU - Ishizaki, Yasuki

PY - 2015/12/1

Y1 - 2015/12/1

N2 - For homeothermic animals, constant body temperature is an important determinant of brain function. It is well established that changes in brain temperature dynamically influence hippocampal activity. We previously reported that the thermosensor TRPV4 (activated above 34 °C) is activated at the physiological temperature in hippocampal neurons and controls neuronal excitability in vitro. Here, we examined if TRPV4 regulates neuronal excitability through its activation at the physiological temperature in vivo. We found that TRPV4-deficient (TRPV4KO) mice exhibit reduced depression-like and social behaviors compared to wild-type (WT) mice, and the number of c-fos positive cells in the dentate gyrus was significantly reduced upon the depression-like behaviors. We measured resting membrane potentials (RMPs) in the hippocampal granule cells from slice preparations at 35 °C and found that TRPV4-positive neurons significantly depolarized the RMPs through TRPV4 activation at the physiological temperature. The depolarization increased the spike numbers depending on the enhancement of TRPV4 activation. We also found that theta-frequency electroencephalogram (EEG) activities in TRPV4KO mice during wake periods were significantly reduced compared with those in WT mice. Taken together, we report for the first time that TRPV4 activation at the physiological temperature is important to regulate neuronal excitability and behaviors in mammals.

AB - For homeothermic animals, constant body temperature is an important determinant of brain function. It is well established that changes in brain temperature dynamically influence hippocampal activity. We previously reported that the thermosensor TRPV4 (activated above 34 °C) is activated at the physiological temperature in hippocampal neurons and controls neuronal excitability in vitro. Here, we examined if TRPV4 regulates neuronal excitability through its activation at the physiological temperature in vivo. We found that TRPV4-deficient (TRPV4KO) mice exhibit reduced depression-like and social behaviors compared to wild-type (WT) mice, and the number of c-fos positive cells in the dentate gyrus was significantly reduced upon the depression-like behaviors. We measured resting membrane potentials (RMPs) in the hippocampal granule cells from slice preparations at 35 °C and found that TRPV4-positive neurons significantly depolarized the RMPs through TRPV4 activation at the physiological temperature. The depolarization increased the spike numbers depending on the enhancement of TRPV4 activation. We also found that theta-frequency electroencephalogram (EEG) activities in TRPV4KO mice during wake periods were significantly reduced compared with those in WT mice. Taken together, we report for the first time that TRPV4 activation at the physiological temperature is important to regulate neuronal excitability and behaviors in mammals.

UR - http://www.scopus.com/inward/record.url?scp=84947485276&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84947485276&partnerID=8YFLogxK

U2 - 10.1007/s00424-015-1726-0

DO - 10.1007/s00424-015-1726-0

M3 - Article

VL - 467

SP - 2495

EP - 2507

JO - Pflugers Archiv European Journal of Physiology

JF - Pflugers Archiv European Journal of Physiology

SN - 0031-6768

IS - 12

ER -