Structure and selectivity in bestrophin ion channels

Yang, T.; Liu, Q.; Kloss, B.; Bruni, R.; Kalathur, R. C.; Guo, Y.; Kloppmann, E.; Rost, B.; Colecraft, H. M.; Hendrickson, W. A.

doi:10.1126/science.1259723

Title: Structure and selectivity in bestrophin ion channels

Journal Article · Thu Sep 25 00:00:00 EDT 2014 · Science

DOI:https://doi.org/10.1126/science.1259723· OSTI ID:1427843

Yang, T.; Liu, Q.; Kloss, B.; Bruni, R.; Kalathur, R. C.; Guo, Y.; Kloppmann, E.; Rost, B.; Colecraft, H. M.; Hendrickson, W. A.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1427843

Journal Information:: Science, Vol. 346, Issue 6207; ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: ENGLISH

References (44)

Bestrophin, the product of the Best vitelliform macular dystrophy gene (VMD2), localizes to the basolateral plasma membrane of the retinal pigment epithelium Marmorstein, A. D.; Marmorstein, L. Y.; Rayborn, M. Proceedings of the National Academy of Sciences, Vol. 97, Issue 23 https://doi.org/10.1073/pnas.220402097	journal	October 2000
Mutations in a novel gene, VMD2, encoding a protein of unknown properties cause juvenile-onset vitelliform macular dystrophy (Best's disease) Marquardt, A. Human Molecular Genetics, Vol. 7, Issue 9 https://doi.org/10.1093/hmg/7.9.1517	journal	September 1998
Identification of the gene responsible for Best macular dystrophy Petrukhin, Konstantin; Koisti, Markus J.; Bakall, Benjamin Nature Genetics, Vol. 19, Issue 3 https://doi.org/10.1038/915	journal	July 1998
The presence of bestrophin-1 modulates the Ca2+ recruitment from Ca2+ stores in the ER Neussert, Rudgar; Müller, Claudia; Milenkovic, Vladimir M. Pflügers Archiv - European Journal of Physiology, Vol. 460, Issue 1 https://doi.org/10.1007/s00424-010-0840-2	journal	April 2010
The spectrum of ocular phenotypes caused by mutations in the BEST1 gene Boon, Camiel J. F.; Klevering, B. Jeroen; Leroy, Bart P. Progress in Retinal and Eye Research, Vol. 28, Issue 3 https://doi.org/10.1016/j.preteyeres.2009.04.002	journal	May 2009
Missense Mutations in a Retinal Pigment Epithelium Protein, Bestrophin-1, Cause Retinitis Pigmentosa Davidson, Alice E.; Millar, Ian D.; Urquhart, Jill E. The American Journal of Human Genetics, Vol. 85, Issue 5 https://doi.org/10.1016/j.ajhg.2009.09.015	journal	November 2009
Bestrophins and retinopathies Xiao, Qinghuan; Hartzell, H. Criss; Yu, Kuai Pflügers Archiv - European Journal of Physiology, Vol. 460, Issue 2 https://doi.org/10.1007/s00424-010-0821-5	journal	March 2010
Molecular Physiology of Bestrophins: Multifunctional Membrane Proteins Linked to Best Disease and Other Retinopathies Hartzell, H. Criss; Qu, Zhiqiang; Yu, Kuai Physiological Reviews, Vol. 88, Issue 2 https://doi.org/10.1152/physrev.00022.2007	journal	April 2008
Ten novel mutations in VMD2 associated with Best macular dystrophy (BMD) : MUTATIONS IN BRIEF Krämer, Franziska; Mohr, Nicole; Kellner, Ulrich Human Mutation, Vol. 22, Issue 5 https://doi.org/10.1002/humu.9189	journal	September 2003
Mutations in the VMD2 gene are associated with juvenile-onset vitelliform macular dystrophy (Best disease) and adult vitelliform macular dystrophy but not age-related macular degeneration Krämer, Franziska; White, Karen; Pauleikhoff, Daniel European Journal of Human Genetics, Vol. 8, Issue 4 https://doi.org/10.1038/sj.ejhg.5200447	journal	April 2000
Evaluation of the Best disease gene in patients with age-related macular degeneration and other maculopathies Allikmets, R.; Seddon, Johanna M.; Bernstein, Paul S. Human Genetics, Vol. 104, Issue 6 https://doi.org/10.1007/s004390050986	journal	July 1999
The vitelliform macular dystrophy protein defines a new family of chloride channels Sun, Hui; Tsunenari, Takashi; Yau, King-Wai Proceedings of the National Academy of Sciences, Vol. 99, Issue 6 https://doi.org/10.1073/pnas.052692999	journal	March 2002
Regulation of Bestrophin Cl Channels by Calcium: Role of the C Terminus Xiao, Qinghuan; Prussia, Andrew; Yu, Kuai The Journal of General Physiology, Vol. 132, Issue 6 https://doi.org/10.1085/jgp.200810056	journal	November 2008
Chloride Channel Activity of Bestrophin Mutants Associated with Mild or Late-Onset Macular Degeneration Yu, Kuai; Qu, Zhiqiang; Cui, Yuanyuan Investigative Opthalmology & Visual Science, Vol. 48, Issue 10 https://doi.org/10.1167/iovs.07-0301	journal	October 2007
The Bestrophin Mutation A243V, Linked to Adult-Onset Vitelliform Macular Dystrophy, Impairs Its Chloride Channel Function Yu, Kuai; Cui, Yuanyuan; Hartzell, H. Criss Investigative Opthalmology & Visual Science, Vol. 47, Issue 11 https://doi.org/10.1167/iovs.06-0524	journal	November 2006
Functional roles of bestrophins in ocular epithelia Marmorstein, Alan D.; Cross, Harold E.; Peachey, Neal S. Progress in Retinal and Eye Research, Vol. 28, Issue 3 https://doi.org/10.1016/j.preteyeres.2009.04.004	journal	May 2009
Hydrodynamic properties of porcine bestrophin-1 in Triton X-100 Stanton, J. Brett; Goldberg, Andrew F. X.; Hoppe, George Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 2 https://doi.org/10.1016/j.bbamem.2006.01.024	journal	February 2006
Insertion and Topology of Normal and Mutant Bestrophin-1 in the Endoplasmic Reticulum Membrane Milenkovic, Vladimir M.; Rivera, Andrea; Horling, Franziska Journal of Biological Chemistry, Vol. 282, Issue 2 https://doi.org/10.1074/jbc.M607383200	journal	November 2006
Regulation of Bestrophins by Ca2+: A Theoretical and Experimental Study Kranjc, Agata; Grillo, Federico W.; Rievaj, Juraj PLoS ONE, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pone.0004672	journal	March 2009
TMEM16F Forms a Ca2+-Activated Cation Channel Required for Lipid Scrambling in Platelets during Blood Coagulation Yang, Huanghe; Kim, Andrew; David, Tovo Cell, Vol. 151, Issue 1 https://doi.org/10.1016/j.cell.2012.07.036	journal	September 2012
Mouse Bestrophin-2 Is a Bona fide Cl ⁻ Channel : Identification of a Residue Important in Anion Binding and Conduction Qu, Zhiqiang; Fischmeister, Rodolphe; Hartzell, Criss The Journal of General Physiology, Vol. 123, Issue 4 https://doi.org/10.1085/jgp.200409031	journal	March 2004
Determinants of Anion Permeation in the Second Transmembrane Domain of the Mouse Bestrophin-2 Chloride Channel Qu, Zhiqiang; Hartzell, Criss The Journal of General Physiology, Vol. 124, Issue 4 https://doi.org/10.1085/jgp.200409108	journal	September 2004
The Anion-Selective Pore of the Bestrophins, a Family of Chloride Channels Associated with Retinal Degeneration Qu, Z. Journal of Neuroscience, Vol. 26, Issue 20 https://doi.org/10.1523/JNEUROSCI.5500-05.2006	journal	May 2006
Ca ²⁺ -activated Cl ⁻ Current from Human Bestrophin-4 in Excised Membrane Patches Tsunenari, Takashi; Nathans, Jeremy; Yau, King-Wai The Journal of General Physiology, Vol. 127, Issue 6 https://doi.org/10.1085/jgp.200609527	journal	May 2006
Rescue of Volume-regulated Anion Current by Bestrophin Mutants with Altered Charge Selectivity Chien, Li-Ting; Hartzell, H. Criss The Journal of General Physiology, Vol. 132, Issue 5 https://doi.org/10.1085/jgp.200810065	journal	October 2008
Homologue structure of the SLAC1 anion channel for closing stomata in leaves Chen, Yu-hang; Hu, Lei; Punta, Marco Nature, Vol. 467, Issue 7319 https://doi.org/10.1038/nature09487	journal	October 2010
Expression Cloning of TMEM16A as a Calcium-Activated Chloride Channel Subunit Schroeder, Björn Christian; Cheng, Tong; Jan, Yuh Nung Cell, Vol. 134, Issue 6 https://doi.org/10.1016/j.cell.2008.09.003	journal	September 2008
TMEM16A confers receptor-activated calcium-dependent chloride conductance Yang, Young Duk; Cho, Hawon; Koo, Jae Yeon Nature, Vol. 455, Issue 7217 https://doi.org/10.1038/nature07313	journal	August 2008
Anion selectivity in biological systems Wright, E. M.; Diamond, J. M. Physiological Reviews, Vol. 57, Issue 1 https://doi.org/10.1152/physrev.1977.57.1.109	journal	January 1977
Focus on Molecules: Bestrophin (Best-1) Marmorstein, Alan D.; Kinnick, Tyson R. Experimental Eye Research, Vol. 85, Issue 4 https://doi.org/10.1016/j.exer.2006.03.021	journal	October 2007
Structural genomics target selection for the New York consortium on membrane protein structure Punta, Marco; Love, James; Handelman, Samuel Journal of Structural and Functional Genomics, Vol. 10, Issue 4 https://doi.org/10.1007/s10969-009-9071-1	journal	October 2009
Online Size-Exclusion High-Performance Liquid Chromatography Light Scattering and Differential Refractometry Methods to Determine Degree of Polymer Conjugation to Proteins and Protein–Protein or Protein–Ligand Association States Kendrick, Brent S.; Kerwin, Bruce A.; Chang, Byeong S. Analytical Biochemistry, Vol. 299, Issue 2 https://doi.org/10.1006/abio.2001.5411	journal	December 2001
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
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
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
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures Landau, M.; Mayrose, I.; Rosenberg, Y. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki370	journal	July 2005
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Tmem16F forms a Ca2+-Activated Cation Channel Required for Lipid Scrambling in Platelets during Blood Coagulation Yang, Huanghe; Kim, Andrew; David, Tovo Biophysical Journal, Vol. 104, Issue 2 https://doi.org/10.1016/j.bpj.2012.11.2033	journal	January 2013
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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Mutant Best1 Expression and Impaired Phagocytosis in an iPSC Model of Autosomal Recessive Bestrophinopathy Marmorstein, Alan D.; Johnson, Adiv A.; Bachman, Lori A. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21651-z	journal	March 2018
Investigation and Restoration of BEST1 Activity in Patient-derived RPEs with Dominant Mutations Ji, Changyi; Li, Yao; Kittredge, Alec Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-54892-7	journal	December 2019
Dual Ca2+-dependent gates in human Bestrophin1 underlie disease-causing mechanisms of gain-of-function mutations Ji, Changyi; Kittredge, Alec; Hopiavuori, Austin Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0433-3	journal	June 2019
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BEST1 gene therapy corrects a diffuse retina-wide microdetachment modulated by light exposure Guziewicz, Karina E.; Cideciyan, Artur V.; Beltran, William A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 12 https://doi.org/10.1073/pnas.1720662115	journal	March 2018
The TMEM16A channel mediates the fast polyspermy block in Xenopus laevis Wozniak, Katherine L.; Phelps, Wesley A.; Tembo, Maiwase Journal of General Physiology, Vol. 150, Issue 9 https://doi.org/10.1085/jgp.201812071	journal	July 2018
A clearer image of the structure and regulation of bestrophin Stockbridge, Randy B. Journal of General Physiology, Vol. 150, Issue 11 https://doi.org/10.1085/jgp.201812220	journal	October 2018
BEST1 protein stability and degradation pathways differ between autosomal dominant Best disease and autosomal recessive bestrophinopathy accounting for the distinct retinal phenotypes Milenkovic, Andrea; Milenkovic, Vladimir M.; Wetzel, Christian H. Human Molecular Genetics, Vol. 27, Issue 9 https://doi.org/10.1093/hmg/ddy070	journal	February 2018
A bestrophin-like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis : Involvement of AtBest in fine-tuning of photosynthesis Duan, Zhikun; Kong, Fanna; Zhang, Lin Journal of Integrative Plant Biology, Vol. 58, Issue 10 https://doi.org/10.1111/jipb.12475	journal	April 2016
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The Y227N mutation affects bestrophin-1 protein stability and impairs sperm function in a mouse model of Best vitelliform macular dystrophy Milenkovic, Andrea; Schmied, Denise; Tanimoto, Naoyuki Biology Open, Vol. 8, Issue 7 https://doi.org/10.1242/bio.041335	journal	June 2019
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