Swapping of transmembrane domains in the epithelial calcium channel TRPV6

Singh, Appu K.; Saotome, Kei; Sobolevsky, Alexander I.

doi:10.1038/s41598-017-10993-9

Swapping of transmembrane domains in the epithelial calcium channel TRPV6

Journal Article · Wed Sep 06 00:00:00 EDT 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-10993-9· OSTI ID:1430345

Singh, Appu K. ^[1]; Saotome, Kei ^[1]; Sobolevsky, Alexander I. ^[1]

Columbia Univ., New York, NY (United States)

Tetrameric ion channels have either swapped or non-swapped arrangements of the S1–S4 and pore domains. Here we show that mutations in the transmembrane domain of TRPV6 can result in conversion from a domain-swapped to non-swapped fold. These results reveal structural determinants of domain swapping and raise the possibility that a single ion channel subtype can fold into either arrangement in vivo, affecting its function in normal or disease states.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: NIH

OSTI ID:: 1430345

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (27)

TRP channels in calcium homeostasis: from hormonal control to structure-function relationship of TRPV5 and TRPV6 van Goor, Mark K. C.; Hoenderop, Joost G. J.; van der Wijst, Jenny Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1864, Issue 6 https://doi.org/10.1016/j.bbamcr.2016.11.027	journal	June 2017
TRPV6 and prostate cancer: cancer growth beyond the prostate correlates with increased TRPV6 Ca2+ channel expression Wissenbach, Ulrich; Niemeyer, Barbara; Himmerkus, Nina Biochemical and Biophysical Research Communications, Vol. 322, Issue 4 https://doi.org/10.1016/j.bbrc.2004.08.042	journal	October 2004
Structure of the Full-Length TRPV2 Channel by Cryo-EM Huynh, Kevin W.; Cohen, Matthew R.; Jiang, Jiansen Microscopy and Microanalysis, Vol. 22, Issue S3 https://doi.org/10.1017/s1431927616006437	journal	July 2016
Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment Long, Stephen B.; Tao, Xiao; Campbell, Ernest B. Nature, Vol. 450, Issue 7168 https://doi.org/10.1038/nature06265	journal	November 2007
Structure of the TRPV1 ion channel determined by electron cryo-microscopy Liao, Maofu; Cao, Erhu; Julius, David Nature, Vol. 504, Issue 7478 https://doi.org/10.1038/nature12822	journal	December 2013
Crystal structure of the epithelial calcium channel TRPV6 Saotome, Kei; Singh, Appu K.; Yelshanskaya, Maria V. Nature, Vol. 534, Issue 7608 https://doi.org/10.1038/nature17975	journal	June 2016
Structure of a eukaryotic cyclic-nucleotide-gated channel Li, Minghui; Zhou, Xiaoyuan; Wang, Shu Nature, Vol. 542, Issue 7639 https://doi.org/10.1038/nature20819	journal	January 2017
CaT1 and the Calcium Release-activated Calcium Channel Manifest Distinct Pore Properties Voets, Thomas; Prenen, Jean; Fleig, Andrea Journal of Biological Chemistry, Vol. 276, Issue 51 https://doi.org/10.1074/jbc.c100607200	journal	October 2001
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/s0907444906045975	journal	December 2006
The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity Doyle, D. A. Science, Vol. 280, Issue 5360 https://doi.org/10.1126/science.280.5360.69	journal	April 1998
Structure of the voltage-gated K+ channel Eag1 reveals an alternative voltage sensing mechanism Whicher, J. R.; MacKinnon, R. Science, Vol. 353, Issue 6300 https://doi.org/10.1126/science.aaf8070	journal	August 2016
TRP Channels Venkatachalam, Kartik; Montell, Craig Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.75.103004.142819	journal	June 2007
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Structures of the Human HCN1 Hyperpolarization-Activated Channel Lee, Chia-Hsueh; MacKinnon, Roderick Cell, Vol. 168, Issue 1-2 https://doi.org/10.1016/j.cell.2016.12.023	journal	January 2017
Structural Titration of Slo2.2, a Na + -Dependent K + Channel Hite, Richard K.; MacKinnon, Roderick Cell, Vol. 168, Issue 3 https://doi.org/10.1016/j.cell.2016.12.030	journal	January 2017
Structure of the TRPA1 ion channel suggests regulatory mechanisms Paulsen, Candice E.; Armache, Jean-Paul; Gao, Yuan Nature, Vol. 520, Issue 7548 https://doi.org/10.1038/nature14367	journal	April 2015
Erratum: Structure of the TRPA1 ion channel suggests regulatory mechanisms Paulsen, Candice E.; Armache, Jean-Paul; Gao, Yuan Nature, Vol. 525, Issue 7570 https://doi.org/10.1038/nature14871	journal	July 2015
Cryo-EM structure of the open high-conductance Ca2+-activated K+ channel Tao, Xiao; Hite, Richard K.; MacKinnon, Roderick Nature, Vol. 541, Issue 7635 https://doi.org/10.1038/nature20608	journal	December 2016
Structure of the full-length TRPV2 channel by cryo-EM Huynh, Kevin W.; Cohen, Matthew R.; Jiang, Jiansen Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11130	journal	March 2016
Cryo-electron microscopy structure of the TRPV2 ion channel Zubcevic, Lejla; Herzik, Mark A.; Chung, Ben C. Nature Structural & Molecular Biology, Vol. 23, Issue 2 https://doi.org/10.1038/nsmb.3159	journal	January 2016
CaT1 and the Calcium Release-activated Calcium Channel Manifest Distinct Pore Properties Voets, Thomas; Prenen, Jean; Fleig, Andrea Journal of Biological Chemistry, Vol. 276, Issue 51 https://doi.org/10.1074/jbc.C100607200	journal	October 2001
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/S0907444906045975	journal	December 2006
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Calcium Channel TRPV6 as a Potential Therapeutic Target in Estrogen Receptor-Negative Breast Cancer Peters, A. A.; Simpson, P. T.; Bassett, J. J. Molecular Cancer Therapeutics, Vol. 11, Issue 10 https://doi.org/10.1158/1535-7163.MCT-11-0965	journal	July 2012

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Structure and gating mechanism of the transient receptor potential channel TRPV3 Singh, Appu K.; McGoldrick, Luke L.; Sobolevsky, Alexander I. Nature Structural & Molecular Biology, Vol. 25, Issue 9 https://doi.org/10.1038/s41594-018-0108-7	journal	August 2018
Structural insights on TRPV5 gating by endogenous modulators Hughes, Taylor E. T.; Pumroy, Ruth A.; Yazici, Aysenur Torun https://doi.org/10.1101/338798	posted_content	July 2018
Mechanism of calmodulin inactivation of the calcium-selective TRP channel TRPV6 Singh, Appu K.; McGoldrick, Luke L.; Twomey, Edward C. Science Advances, Vol. 4, Issue 8 https://doi.org/10.1126/sciadv.aau6088	journal	August 2018
Eukaryotic Voltage-Gated Sodium Channels: On Their Origins, Asymmetries, Losses, Diversification and Adaptations Fux, Julia E.; Mehta, Amrit; Moffat, Jack Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.01406	journal	November 2018
New Structures and Gating of Voltage-Dependent Potassium (Kv) Channels and Their Relatives: A Multi-Domain and Dynamic Question Barros, Francisco; Pardo, Luis; Domínguez, Pedro International Journal of Molecular Sciences, Vol. 20, Issue 2 https://doi.org/10.3390/ijms20020248	journal	January 2019
TRPV6 as A Target for Cancer Therapy Stewart, John M. Journal of Cancer, Vol. 11, Issue 2 https://doi.org/10.7150/jca.31640	journal	January 2020
Structural Insights on TRPV5 Gating by Endogenous Modulators Hughes, Taylor; Pumroy, Ruth; Yazici, Aysenur Biophysical Journal, Vol. 116, Issue 3 https://doi.org/10.1016/j.bpj.2018.11.2873	journal	February 2019
Opening of the human epithelial calcium channel TRPV6 McGoldrick, Luke L.; Singh, Appu K.; Saotome, Kei Nature, Vol. 553, Issue 7687 https://doi.org/10.1038/nature25182	journal	December 2017
Structural insights on TRPV5 gating by endogenous modulators Hughes, Taylor E. T.; Pumroy, Ruth A.; Yazici, Aysenur Torun Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06753-6	journal	October 2018
Cryo-EM and X-ray structures of TRPV4 reveal insight into ion permeation and gating mechanisms Deng, Zengqin; Paknejad, Navid; Maksaev, Grigory Nature Structural & Molecular Biology, Vol. 25, Issue 3 https://doi.org/10.1038/s41594-018-0037-5	journal	February 2018
X-ray crystallography of TRP channels Singh, Appu K.; McGoldrick, Luke L.; Saotome, Kei Channels, Vol. 12, Issue 1 https://doi.org/10.1080/19336950.2018.1457898	journal	January 2018
Structural mechanisms of transient receptor potential ion channels Cao, Erhu Journal of General Physiology, Vol. 152, Issue 3 https://doi.org/10.1085/jgp.201811998	journal	January 2020
A hypothetical molecular mechanism for TRPV1 activation that invokes rotation of an S6 asparagine Kasimova, Marina A.; Yazici, Aysenur Torun; Yudin, Yevgen Journal of General Physiology, Vol. 150, Issue 11 https://doi.org/10.1085/jgp.201812124	journal	October 2018
Never at rest: insights into the conformational dynamics of ion channels from cryo-electron microscopy: Cryo-EM studies of ion channels Lau, Carus; Hunter, Mark J.; Stewart, Alastair The Journal of Physiology, Vol. 596, Issue 7 https://doi.org/10.1113/jp274888	journal	March 2018

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Swapping of transmembrane domains in the epithelial calcium channel TRPV6

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