Involvement of TRPV4 in serotonin-evoked scratching

Tasuku Akiyama, Margaret Ivanov, Masaki Nagamine, Auva Davoodi, Mirela I. Carstens, Akihiko Ikoma, Ferda Cevikbas, Cordula Kempkes, Joerg Buddenkotte, Martin Steinhoff, E. Carstens

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

Several thermosensitive transient receptor potential channels (transient receptor potential vanilloid type-1,-3; transient receptor potential cation channel, subfamily A, member 1) have been implicated in itch. In contrast, the role of transient receptor potential vanilloid type-4 (TRPV4) in itch is unknown. Therefore, we investigated if TRPV4, a temperature-sensitive cation channel, plays an important role in acute itch in mice. Four different pruritogens, including serotonin (5-hydroxytryptamine [5-HT]), histamine, SLIGRL (protease-activated receptors 2/mas-related G-protein-coupled receptor C11 agonist), and chloroquine (mas-related G-protein-coupled receptor A3 agonist), were intradermally injected into mice and itch-related scratching behavior was assessed. TRPV4 knockout mice exhibited significantly fewer 5-HT-evoked scratching bouts compared with wild-type mice. Notably, no differences between TRPV4 knockout and wild-type mice were observed in the number of scratch bouts elicited by SLIGRL and histamine. Pretreatment with a TRPV4 antagonist significantly attenuated 5-HT-evoked scratching in vivo. Using calcium imaging in cultured primary murine dorsal root ganglion neurons, the response of neurons after 5-HT application, but not other pruritogens, was significantly lower in TRPV4 knockout compared with wild-type mice. A TRPV4 antagonist significantly suppressed 5-HT-evoked responses in dorsal root ganglion cells from wild-type mice. Approximately 90% of 5-HT-sensitive dorsal root ganglion neurons were immunoreactive for an antibody to TRPV4, as assessed by calcium imaging. These results indicate that 5-HT-induced itch is linked to TRPV4.

Original languageEnglish (US)
Pages (from-to)154-160
Number of pages7
JournalJournal of Investigative Dermatology
Volume136
Issue number1
DOIs
StatePublished - Jan 1 2016
Externally publishedYes

Fingerprint

TRPV Cation Channels
Serotonin
seryl-leucyl-isoleucyl-glycyl-arginyl-leucine
Spinal Ganglia
Transient Receptor Potential Channels
Neurons
G-Protein-Coupled Receptors
Knockout Mice
Histamine
PAR-2 Receptor
Calcium
Imaging techniques
Chloroquine
Cations
Temperature

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Dermatology
  • Cell Biology

Cite this

Akiyama, T., Ivanov, M., Nagamine, M., Davoodi, A., Carstens, M. I., Ikoma, A., ... Carstens, E. (2016). Involvement of TRPV4 in serotonin-evoked scratching. Journal of Investigative Dermatology, 136(1), 154-160. https://doi.org/10.1038/JID.2015.388

Involvement of TRPV4 in serotonin-evoked scratching. / Akiyama, Tasuku; Ivanov, Margaret; Nagamine, Masaki; Davoodi, Auva; Carstens, Mirela I.; Ikoma, Akihiko; Cevikbas, Ferda; Kempkes, Cordula; Buddenkotte, Joerg; Steinhoff, Martin; Carstens, E.

In: Journal of Investigative Dermatology, Vol. 136, No. 1, 01.01.2016, p. 154-160.

Research output: Contribution to journalArticle

Akiyama, T, Ivanov, M, Nagamine, M, Davoodi, A, Carstens, MI, Ikoma, A, Cevikbas, F, Kempkes, C, Buddenkotte, J, Steinhoff, M & Carstens, E 2016, 'Involvement of TRPV4 in serotonin-evoked scratching', Journal of Investigative Dermatology, vol. 136, no. 1, pp. 154-160. https://doi.org/10.1038/JID.2015.388
Akiyama T, Ivanov M, Nagamine M, Davoodi A, Carstens MI, Ikoma A et al. Involvement of TRPV4 in serotonin-evoked scratching. Journal of Investigative Dermatology. 2016 Jan 1;136(1):154-160. https://doi.org/10.1038/JID.2015.388
Akiyama, Tasuku ; Ivanov, Margaret ; Nagamine, Masaki ; Davoodi, Auva ; Carstens, Mirela I. ; Ikoma, Akihiko ; Cevikbas, Ferda ; Kempkes, Cordula ; Buddenkotte, Joerg ; Steinhoff, Martin ; Carstens, E. / Involvement of TRPV4 in serotonin-evoked scratching. In: Journal of Investigative Dermatology. 2016 ; Vol. 136, No. 1. pp. 154-160.
@article{6dd84da06aba481485a67139fb455cce,
title = "Involvement of TRPV4 in serotonin-evoked scratching",
abstract = "Several thermosensitive transient receptor potential channels (transient receptor potential vanilloid type-1,-3; transient receptor potential cation channel, subfamily A, member 1) have been implicated in itch. In contrast, the role of transient receptor potential vanilloid type-4 (TRPV4) in itch is unknown. Therefore, we investigated if TRPV4, a temperature-sensitive cation channel, plays an important role in acute itch in mice. Four different pruritogens, including serotonin (5-hydroxytryptamine [5-HT]), histamine, SLIGRL (protease-activated receptors 2/mas-related G-protein-coupled receptor C11 agonist), and chloroquine (mas-related G-protein-coupled receptor A3 agonist), were intradermally injected into mice and itch-related scratching behavior was assessed. TRPV4 knockout mice exhibited significantly fewer 5-HT-evoked scratching bouts compared with wild-type mice. Notably, no differences between TRPV4 knockout and wild-type mice were observed in the number of scratch bouts elicited by SLIGRL and histamine. Pretreatment with a TRPV4 antagonist significantly attenuated 5-HT-evoked scratching in vivo. Using calcium imaging in cultured primary murine dorsal root ganglion neurons, the response of neurons after 5-HT application, but not other pruritogens, was significantly lower in TRPV4 knockout compared with wild-type mice. A TRPV4 antagonist significantly suppressed 5-HT-evoked responses in dorsal root ganglion cells from wild-type mice. Approximately 90{\%} of 5-HT-sensitive dorsal root ganglion neurons were immunoreactive for an antibody to TRPV4, as assessed by calcium imaging. These results indicate that 5-HT-induced itch is linked to TRPV4.",
author = "Tasuku Akiyama and Margaret Ivanov and Masaki Nagamine and Auva Davoodi and Carstens, {Mirela I.} and Akihiko Ikoma and Ferda Cevikbas and Cordula Kempkes and Joerg Buddenkotte and Martin Steinhoff and E. Carstens",
year = "2016",
month = "1",
day = "1",
doi = "10.1038/JID.2015.388",
language = "English (US)",
volume = "136",
pages = "154--160",
journal = "Journal of Investigative Dermatology",
issn = "0022-202X",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - Involvement of TRPV4 in serotonin-evoked scratching

AU - Akiyama, Tasuku

AU - Ivanov, Margaret

AU - Nagamine, Masaki

AU - Davoodi, Auva

AU - Carstens, Mirela I.

AU - Ikoma, Akihiko

AU - Cevikbas, Ferda

AU - Kempkes, Cordula

AU - Buddenkotte, Joerg

AU - Steinhoff, Martin

AU - Carstens, E.

PY - 2016/1/1

Y1 - 2016/1/1

N2 - Several thermosensitive transient receptor potential channels (transient receptor potential vanilloid type-1,-3; transient receptor potential cation channel, subfamily A, member 1) have been implicated in itch. In contrast, the role of transient receptor potential vanilloid type-4 (TRPV4) in itch is unknown. Therefore, we investigated if TRPV4, a temperature-sensitive cation channel, plays an important role in acute itch in mice. Four different pruritogens, including serotonin (5-hydroxytryptamine [5-HT]), histamine, SLIGRL (protease-activated receptors 2/mas-related G-protein-coupled receptor C11 agonist), and chloroquine (mas-related G-protein-coupled receptor A3 agonist), were intradermally injected into mice and itch-related scratching behavior was assessed. TRPV4 knockout mice exhibited significantly fewer 5-HT-evoked scratching bouts compared with wild-type mice. Notably, no differences between TRPV4 knockout and wild-type mice were observed in the number of scratch bouts elicited by SLIGRL and histamine. Pretreatment with a TRPV4 antagonist significantly attenuated 5-HT-evoked scratching in vivo. Using calcium imaging in cultured primary murine dorsal root ganglion neurons, the response of neurons after 5-HT application, but not other pruritogens, was significantly lower in TRPV4 knockout compared with wild-type mice. A TRPV4 antagonist significantly suppressed 5-HT-evoked responses in dorsal root ganglion cells from wild-type mice. Approximately 90% of 5-HT-sensitive dorsal root ganglion neurons were immunoreactive for an antibody to TRPV4, as assessed by calcium imaging. These results indicate that 5-HT-induced itch is linked to TRPV4.

AB - Several thermosensitive transient receptor potential channels (transient receptor potential vanilloid type-1,-3; transient receptor potential cation channel, subfamily A, member 1) have been implicated in itch. In contrast, the role of transient receptor potential vanilloid type-4 (TRPV4) in itch is unknown. Therefore, we investigated if TRPV4, a temperature-sensitive cation channel, plays an important role in acute itch in mice. Four different pruritogens, including serotonin (5-hydroxytryptamine [5-HT]), histamine, SLIGRL (protease-activated receptors 2/mas-related G-protein-coupled receptor C11 agonist), and chloroquine (mas-related G-protein-coupled receptor A3 agonist), were intradermally injected into mice and itch-related scratching behavior was assessed. TRPV4 knockout mice exhibited significantly fewer 5-HT-evoked scratching bouts compared with wild-type mice. Notably, no differences between TRPV4 knockout and wild-type mice were observed in the number of scratch bouts elicited by SLIGRL and histamine. Pretreatment with a TRPV4 antagonist significantly attenuated 5-HT-evoked scratching in vivo. Using calcium imaging in cultured primary murine dorsal root ganglion neurons, the response of neurons after 5-HT application, but not other pruritogens, was significantly lower in TRPV4 knockout compared with wild-type mice. A TRPV4 antagonist significantly suppressed 5-HT-evoked responses in dorsal root ganglion cells from wild-type mice. Approximately 90% of 5-HT-sensitive dorsal root ganglion neurons were immunoreactive for an antibody to TRPV4, as assessed by calcium imaging. These results indicate that 5-HT-induced itch is linked to TRPV4.

UR - http://www.scopus.com/inward/record.url?scp=84959471003&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84959471003&partnerID=8YFLogxK

U2 - 10.1038/JID.2015.388

DO - 10.1038/JID.2015.388

M3 - Article

C2 - 26763435

AN - SCOPUS:84959471003

VL - 136

SP - 154

EP - 160

JO - Journal of Investigative Dermatology

JF - Journal of Investigative Dermatology

SN - 0022-202X

IS - 1

ER -