Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel

Makoto Ihara, Shin Hamamoto, Yohei Miyanoiri, Mitsuhiro Takeda, Masatsune Kainosho, Isamu Yabe, Nobuyuki Uozumi, Atsuko Yamashita

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Multimodal activation by various stimuli is a fundamental characteristic of TRP channels. We identified a fungal TRP channel, TRPGz, exhibiting activation by hyperosmolarity, temperature increase, cytosolic Ca2+ elevation, membrane potential, and H2O2 application, and thus it is expected to represent a prototypic multimodal TRP channel. TRPGz possesses a cytosolic C-terminal domain (CTD), primarily composed of intrinsically disordered regions with some regulatory modules, a putative coiled-coil region and a basic residue cluster. The CTD oligomerization mediated by the coiled-coil region is required for the hyperosmotic and temperature increase activations but not for the tetrameric channel formation or other activation modalities. In contrast, the basic cluster is responsible for general channel inhibition, by binding to phosphatidylinositol phosphates. The crystal structure of the presumed coiled-coil region revealed a tetrameric assembly in an offset spiral rather than a canonical coiled-coil. This structure underlies the observed moderate oligomerization affinity enabling the dynamic assembly and disassembly of the CTD during channel functions, which are compatible with the multimodal regulation mediated by each functional module.

Original languageEnglish
Pages (from-to)15303-15317
Number of pages15
JournalJournal of Biological Chemistry
Volume288
Issue number21
DOIs
Publication statusPublished - May 24 2013

Fingerprint

Transient Receptor Potential Channels
Chemical activation
Oligomerization
Phosphatidylinositol Phosphates
Temperature
Membrane Potentials
Crystal structure
Membranes

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel. / Ihara, Makoto; Hamamoto, Shin; Miyanoiri, Yohei; Takeda, Mitsuhiro; Kainosho, Masatsune; Yabe, Isamu; Uozumi, Nobuyuki; Yamashita, Atsuko.

In: Journal of Biological Chemistry, Vol. 288, No. 21, 24.05.2013, p. 15303-15317.

Research output: Contribution to journalArticle

Ihara, M, Hamamoto, S, Miyanoiri, Y, Takeda, M, Kainosho, M, Yabe, I, Uozumi, N & Yamashita, A 2013, 'Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel', Journal of Biological Chemistry, vol. 288, no. 21, pp. 15303-15317. https://doi.org/10.1074/jbc.M112.434795
Ihara, Makoto ; Hamamoto, Shin ; Miyanoiri, Yohei ; Takeda, Mitsuhiro ; Kainosho, Masatsune ; Yabe, Isamu ; Uozumi, Nobuyuki ; Yamashita, Atsuko. / Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel. In: Journal of Biological Chemistry. 2013 ; Vol. 288, No. 21. pp. 15303-15317.
@article{6fbc392094f64ed5814a0f17c39a89d0,
title = "Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel",
abstract = "Multimodal activation by various stimuli is a fundamental characteristic of TRP channels. We identified a fungal TRP channel, TRPGz, exhibiting activation by hyperosmolarity, temperature increase, cytosolic Ca2+ elevation, membrane potential, and H2O2 application, and thus it is expected to represent a prototypic multimodal TRP channel. TRPGz possesses a cytosolic C-terminal domain (CTD), primarily composed of intrinsically disordered regions with some regulatory modules, a putative coiled-coil region and a basic residue cluster. The CTD oligomerization mediated by the coiled-coil region is required for the hyperosmotic and temperature increase activations but not for the tetrameric channel formation or other activation modalities. In contrast, the basic cluster is responsible for general channel inhibition, by binding to phosphatidylinositol phosphates. The crystal structure of the presumed coiled-coil region revealed a tetrameric assembly in an offset spiral rather than a canonical coiled-coil. This structure underlies the observed moderate oligomerization affinity enabling the dynamic assembly and disassembly of the CTD during channel functions, which are compatible with the multimodal regulation mediated by each functional module.",
author = "Makoto Ihara and Shin Hamamoto and Yohei Miyanoiri and Mitsuhiro Takeda and Masatsune Kainosho and Isamu Yabe and Nobuyuki Uozumi and Atsuko Yamashita",
year = "2013",
month = "5",
day = "24",
doi = "10.1074/jbc.M112.434795",
language = "English",
volume = "288",
pages = "15303--15317",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "21",

}

TY - JOUR

T1 - Molecular bases of multimodal regulation of a fungal transient receptor potential (TRP) channel

AU - Ihara, Makoto

AU - Hamamoto, Shin

AU - Miyanoiri, Yohei

AU - Takeda, Mitsuhiro

AU - Kainosho, Masatsune

AU - Yabe, Isamu

AU - Uozumi, Nobuyuki

AU - Yamashita, Atsuko

PY - 2013/5/24

Y1 - 2013/5/24

N2 - Multimodal activation by various stimuli is a fundamental characteristic of TRP channels. We identified a fungal TRP channel, TRPGz, exhibiting activation by hyperosmolarity, temperature increase, cytosolic Ca2+ elevation, membrane potential, and H2O2 application, and thus it is expected to represent a prototypic multimodal TRP channel. TRPGz possesses a cytosolic C-terminal domain (CTD), primarily composed of intrinsically disordered regions with some regulatory modules, a putative coiled-coil region and a basic residue cluster. The CTD oligomerization mediated by the coiled-coil region is required for the hyperosmotic and temperature increase activations but not for the tetrameric channel formation or other activation modalities. In contrast, the basic cluster is responsible for general channel inhibition, by binding to phosphatidylinositol phosphates. The crystal structure of the presumed coiled-coil region revealed a tetrameric assembly in an offset spiral rather than a canonical coiled-coil. This structure underlies the observed moderate oligomerization affinity enabling the dynamic assembly and disassembly of the CTD during channel functions, which are compatible with the multimodal regulation mediated by each functional module.

AB - Multimodal activation by various stimuli is a fundamental characteristic of TRP channels. We identified a fungal TRP channel, TRPGz, exhibiting activation by hyperosmolarity, temperature increase, cytosolic Ca2+ elevation, membrane potential, and H2O2 application, and thus it is expected to represent a prototypic multimodal TRP channel. TRPGz possesses a cytosolic C-terminal domain (CTD), primarily composed of intrinsically disordered regions with some regulatory modules, a putative coiled-coil region and a basic residue cluster. The CTD oligomerization mediated by the coiled-coil region is required for the hyperosmotic and temperature increase activations but not for the tetrameric channel formation or other activation modalities. In contrast, the basic cluster is responsible for general channel inhibition, by binding to phosphatidylinositol phosphates. The crystal structure of the presumed coiled-coil region revealed a tetrameric assembly in an offset spiral rather than a canonical coiled-coil. This structure underlies the observed moderate oligomerization affinity enabling the dynamic assembly and disassembly of the CTD during channel functions, which are compatible with the multimodal regulation mediated by each functional module.

UR - http://www.scopus.com/inward/record.url?scp=84878230491&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84878230491&partnerID=8YFLogxK

U2 - 10.1074/jbc.M112.434795

DO - 10.1074/jbc.M112.434795

M3 - Article

VL - 288

SP - 15303

EP - 15317

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 21

ER -