Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana

Guo, Jiangtao; Zeng, Weizhong; Chen, Qingfeng; Lee, Changkeun; Chen, Liping; Yang, Yi; Cang, Chunlei; Ren, Dejian; Jiang, Youxing

doi:10.1038/nature16446

Title: Structure of the voltage-gated two-pore channel TPC1 from Arabidopsis thaliana

Journal Article · Mon Dec 21 00:00:00 EST 2015 · Nature (London)

DOI:https://doi.org/10.1038/nature16446· OSTI ID:1243102

Guo, Jiangtao ^[1]; Zeng, Weizhong ^[1]; Chen, Qingfeng ^[1]; Lee, Changkeun ^[1]; Chen, Liping ^[1]; Yang, Yi ^[1]; Cang, Chunlei ^[2]; Ren, Dejian ^[2]; Jiang, Youxing ^[1]

Univ. of Texas Southwestern Medical Center, Dallas, TX (United States)
Univ. of Pennsylvania, Philadelphia, PA (United States)

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: 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

Grant/Contract Number:: AC02-06CH11357; AC02-05CH11231; GM079179; NS055293; NS074257

OSTI ID:: 1243102

Journal Information:: Nature (London), Vol. 531, Issue 7593; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 166 works

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Agonist-specific voltage-dependent gating of lysosomal two-pore Na+ channels Zhang, Xiaoli; Chen, Wei; Li, Ping eLife, Vol. 8 https://doi.org/10.7554/elife.51423	journal	December 2019
Cryo-EM structure of the KvAP channel reveals a non-domain-swapped voltage sensor topology Tao, Xiao; MacKinnon, Roderick eLife, Vol. 8 https://doi.org/10.7554/elife.52164	journal	November 2019
Structural basis of dual Ca2+/pH regulation of the endolysosomal TRPML1 channel Li, Minghui; Zhang, Wei K.; Benvin, Nicole M. Nature Structural & Molecular Biology, Vol. 24, Issue 3 https://doi.org/10.1038/nsmb.3362	journal	January 2017
Structure, inhibition and regulation of two-pore channel TPC1 from Arabidopsis thaliana Kintzer, Alexander F.; Stroud, Robert M. Nature https://doi.org/10.1101/041400	posted_content	February 2016
Calcium-Mediated Abiotic Stress Signaling in Roots Wilkins, Katie; Matthus, Elsa; Swarbreck, Stephanie Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.4839	text	January 2016
The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization Dai, Gucan; Aman, Teresa K.; DiMaio, Frank Zenodo https://doi.org/10.5281/zenodo.3066429	text	January 2019
The HCN Channel Voltage Sensor Undergoes A Large Downward Motion During Hyperpolarization Dai, Gucan; Aman, Teresa K.; DiMaio, Frank Nature Structural & Molecular Biology https://doi.org/10.1101/522581	posted_content	January 2019
Mechanisms of KCNQ1 Channel Dysfunction in Long QT Syndrome Involving Voltage Sensor Domain Mutations Huang, Hui; Kuenze, Georg; Smith, Jarrod A. Science Advances https://doi.org/10.1101/231845	posted_content	December 2017
Mining of Ebola virus entry inhibitors identifies approved drugs as two-pore channel pore blockers Penny, Christopher J.; Vassileva, Kristin; Jha, Archana Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1866, Issue 7 https://doi.org/10.1016/j.bbamcr.2018.10.022	journal	July 2019
Two-pore Channels Enter the Atomic Era: Structure of Plant TPC Revealed Patel, Sandip; Penny, Christopher J.; Rahman, Taufiq Trends in Biochemical Sciences, Vol. 41, Issue 6 https://doi.org/10.1016/j.tibs.2016.04.007	journal	June 2016
Naringenin Impairs Two-Pore Channel 2 Activity And Inhibits VEGF-Induced Angiogenesis Pafumi, Irene; Festa, Margherita; Papacci, Francesca Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-04974-1	journal	July 2017
The human two-pore channel 1 is modulated by cytosolic and luminal calcium Lagostena, Laura; Festa, Margherita; Pusch, Michael Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43900	journal	March 2017
Structural insights into the mechanisms of CNBD channel function James, Zachary M.; Zagotta, William N. Journal of General Physiology, Vol. 150, Issue 2 https://doi.org/10.1085/jgp.201711898	journal	December 2017
Replacing voltage sensor arginines with citrulline provides mechanistic insight into charge versus shape Infield, Daniel T.; Lee, Elizabeth E. L.; Galpin, Jason D. Journal of General Physiology, Vol. 150, Issue 7 https://doi.org/10.1085/jgp.201812075	journal	June 2018
Role of auxin (IAA) in the regulation of slow vacuolar (SV) channels and the volume of red beet taproot vacuoles Burdach, Zbigniew; Siemieniuk, Agnieszka; Trela, Zenon BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1321-6	journal	June 2018
Isolated pores dissected from human two-pore channel 2 are functional. Penny, Christopher J.; Rahman, Taufiq; Sula, Altin Nature Publishing Group https://doi.org/10.17863/cam.25768	journalarticle	January 2016
Atomic Mechanisms of Timothy Syndrome-Associated Mutations in Calcium Channel Cav1.2 Korkosh, Vyacheslav S.; Kiselev, Artem M.; Mikhaylov, Evgeny N. Frontiers in Physiology, Vol. 10 https://doi.org/10.3389/fphys.2019.00335	journal	March 2019
The Integration of Electrical Signals Originating in the Root of Vascular Plants Canales, Javier; Henriquez-Valencia, Carlos; Brauchi, Sebastian Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02173	journal	January 2018
Abiotic Stress Response to As and As+Si, Composite Reprogramming of Fruit Metabolites in Tomato Cultivars Marmiroli, Marta; Mussi, Francesca; Imperiale, Davide Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02201	journal	December 2017

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