Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana
Abstract
Two-pore channels (TPCs) contain two copies of a Shaker-like six-transmembrane (6-TM) domain in each subunit and are ubiquitously expressed in both animals and plants as organellar cation channels. Here we present the crystal structure of a vacuolar two-pore channel from Arabidopsis thaliana, AtTPC1, which functions as a homodimer. AtTPC1 activation requires both voltage and cytosolic Ca2+. Ca2+ binding to the cytosolic EF-hand domain triggers conformational changes coupled to the pair of pore-lining inner helices from the first 6-TM domains, whereas membrane potential only activates the second voltage-sensing domain, the conformational changes of which are coupled to the pair of inner helices from the second 6-TM domains. Luminal Ca2+ or Ba2+ can modulate voltage activation by stabilizing the second voltage-sensing domain in the resting state and shift voltage activation towards more positive potentials. Here, our Ba2+-bound AtTPC1 structure reveals a voltage sensor in the resting state, providing hitherto unseen structural insight into the general voltage-gating mechanism among voltage-gated channels.
- Authors:
-
- Univ. of Texas Southwestern Medical Center, Dallas, TX (United States)
- Univ. of Pennsylvania, Philadelphia, PA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health; National Inst. of General Medical Sciences; Howard Hughes Medical Inst.; USDOE Office of Science (SC), Basic Energy Sciences (BES); Welch Foundation
- OSTI Identifier:
- 1243102
- Grant/Contract Number:
- AC02-06CH11357; AC02-05CH11231; GM079179; NS055293; NS074257
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature (London)
- Additional Journal Information:
- Journal Name: Nature (London); Journal Volume: 531; Journal Issue: 7593; Journal ID: ISSN 0028-0836
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Guo, Jiangtao, Zeng, Weizhong, Chen, Qingfeng, Lee, Changkeun, Chen, Liping, Yang, Yi, Cang, Chunlei, Ren, Dejian, and Jiang, Youxing. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. United States: N. p., 2015.
Web. doi:10.1038/nature16446.
Guo, Jiangtao, Zeng, Weizhong, Chen, Qingfeng, Lee, Changkeun, Chen, Liping, Yang, Yi, Cang, Chunlei, Ren, Dejian, & Jiang, Youxing. Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana. United States. https://doi.org/10.1038/nature16446
Guo, Jiangtao, Zeng, Weizhong, Chen, Qingfeng, Lee, Changkeun, Chen, Liping, Yang, Yi, Cang, Chunlei, Ren, Dejian, and Jiang, Youxing. Mon .
"Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana". United States. https://doi.org/10.1038/nature16446. https://www.osti.gov/servlets/purl/1243102.
@article{osti_1243102,
title = {Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana},
author = {Guo, Jiangtao and Zeng, Weizhong and Chen, Qingfeng and Lee, Changkeun and Chen, Liping and Yang, Yi and Cang, Chunlei and Ren, Dejian and Jiang, Youxing},
abstractNote = {Two-pore channels (TPCs) contain two copies of a Shaker-like six-transmembrane (6-TM) domain in each subunit and are ubiquitously expressed in both animals and plants as organellar cation channels. Here we present the crystal structure of a vacuolar two-pore channel from Arabidopsis thaliana, AtTPC1, which functions as a homodimer. AtTPC1 activation requires both voltage and cytosolic Ca2+. Ca2+ binding to the cytosolic EF-hand domain triggers conformational changes coupled to the pair of pore-lining inner helices from the first 6-TM domains, whereas membrane potential only activates the second voltage-sensing domain, the conformational changes of which are coupled to the pair of inner helices from the second 6-TM domains. Luminal Ca2+ or Ba2+ can modulate voltage activation by stabilizing the second voltage-sensing domain in the resting state and shift voltage activation towards more positive potentials. Here, our Ba2+-bound AtTPC1 structure reveals a voltage sensor in the resting state, providing hitherto unseen structural insight into the general voltage-gating mechanism among voltage-gated channels.},
doi = {10.1038/nature16446},
journal = {Nature (London)},
number = 7593,
volume = 531,
place = {United States},
year = {Mon Dec 21 00:00:00 EST 2015},
month = {Mon Dec 21 00:00:00 EST 2015}
}
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Structural basis of α-scorpion toxin action on Na v channels
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A two-pore channel protein required for regulating mTORC1 activity on starvation
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Calcium-Mediated Abiotic Stress Signaling in Roots
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Endolysosomal Ca2+ Signalling and Cancer Hallmarks: Two-Pore Channels on the Move, TRPML1 Lags Behind!
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The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization
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Structural mechanisms of phospholipid activation of the human TPC2 channel
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Agonist-specific voltage-dependent gating of lysosomal two-pore Na+ channels
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Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana
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Calcium-Mediated Abiotic Stress Signaling in Roots
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The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization
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The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization
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Mechanisms of KCNQ1 Channel Dysfunction in Long QT Syndrome Involving Voltage Sensor Domain Mutations
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Regulation of lysosomal ion homeostasis by channels and transporters
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Mining of Ebola virus entry inhibitors identifies approved drugs as two-pore channel pore blockers
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Two-pore Channels Enter the Atomic Era: Structure of Plant TPC Revealed
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The complete structure of an activated open sodium channel
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Gating interaction maps reveal a noncanonical electromechanical coupling mode in the Shaker K+ channel
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Naringenin Impairs Two-Pore Channel 2 Activity And Inhibits VEGF-Induced Angiogenesis
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The human two-pore channel 1 is modulated by cytosolic and luminal calcium
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Voltage vs. Ligand I: Structural basis of the intrinsic flexibility of S3 segment and its significance in ion channel activation
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Structural insights into the mechanisms of CNBD channel function
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Replacing voltage sensor arginines with citrulline provides mechanistic insight into charge versus shape
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Phosphoinositides modulate the voltage dependence of two-pore channel 3
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The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization
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Identification and characterization of a core set of ROS wave‐associated transcripts involved in the systemic acquired acclimation response of Arabidopsis to excess light
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Mechanisms of KCNQ1 channel dysfunction in long QT syndrome involving voltage sensor domain mutations
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Role of auxin (IAA) in the regulation of slow vacuolar (SV) channels and the volume of red beet taproot vacuoles
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The Integration of Electrical Signals Originating in the Root of Vascular Plants
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Abiotic Stress Response to As and As+Si, Composite Reprogramming of Fruit Metabolites in Tomato Cultivars
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Roles of Chloroplast Retrograde Signals and Ion Transport in Plant Drought Tolerance
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ROS-Activated Ion Channels in Plants: Biophysical Characteristics, Physiological Functions and Molecular Nature
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Pharmacological Strategies for Manipulating Plant Ca2+ Signalling
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Structural mechanisms of phospholipid activation of the human TPC2 channel
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Agonist-specific voltage-dependent gating of lysosomal two-pore Na+ channels
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