X-ray and cryo-EM structures of the mitochondrial calcium uniporter

Fan, Chao; Fan, Minrui; Orlando, Benjamin J.; Fastman, Nathan M.; Zhang, Jinru; Xu, Yan; Chambers, Melissa G.; Xu, Xiaofang; Perry, Kay; Liao, Maofu; Feng, Liang

doi:10.1038/s41586-018-0330-9

X-ray and cryo-EM structures of the mitochondrial calcium uniporter

Journal Article · 01 July 2018 · Nature (London)

DOI:https://doi.org/10.1038/s41586-018-0330-9· OSTI ID:1467708

Fan, Chao; Fan, Minrui; Orlando, Benjamin J.; Fastman, Nathan M.; Zhang, Jinru; Xu, Yan; Chambers, Melissa G.; Xu, Xiaofang; Perry, Kay; Liao, Maofu; Feng, Liang

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

Sponsoring Organization:: NSFNIH

OSTI ID:: 1467708

Journal Information:: Nature (London), Vol. 559, Issue 7715; ISSN 0028-0836

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: ENGLISH

References (72)

MICU1 Serves as a Molecular Gatekeeper to Prevent In Vivo Mitochondrial Calcium Overload Liu, Julia C.; Liu, Jie; Holmström, Kira M. Cell Reports, Vol. 16, Issue 6 https://doi.org/10.1016/j.celrep.2016.07.011	journal	August 2016
HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs Pape, Thomas; Schneider, Thomas R. Journal of Applied Crystallography, Vol. 37, Issue 5 https://doi.org/10.1107/S0021889804018047	journal	September 2004
Mitochondrial calcium uniporter regulator 1 (MCUR1) regulates the calcium threshold for the mitochondrial permeability transition Chaudhuri, Dipayan; Artiga, Daniel J.; Abiria, Sunday A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 13 https://doi.org/10.1073/pnas.1602264113	journal	March 2016
Isolating and engineering human antibodies using yeast surface display Chao, Ginger; Lau, Wai L.; Hackel, Benjamin J. Nature Protocols, Vol. 1, Issue 2 https://doi.org/10.1038/nprot.2006.94	journal	July 2006
Quantitative measurements of membrane potential in Escherichia coli Felle, H.; Porter, J. S.; Slayman, C. L. Biochemistry, Vol. 19, Issue 15 https://doi.org/10.1021/bi00556a026	journal	July 1980
Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution Yan, Zhen; Bai, Xiao-chen; Yan, Chuangye Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature14063	journal	December 2014
Ca2+ Hot Spots on the Mitochondrial Surface Are Generated by Ca2+ Mobilization from Stores, but Not by Activation of Store-Operated Ca2+ Channels Giacomello, Marta; Drago, Ilaria; Bortolozzi, Mario Molecular Cell, Vol. 38, Issue 2 https://doi.org/10.1016/j.molcel.2010.04.003	journal	April 2010
Mitochondrial Ca 2+ Uniporter Is a Mitochondrial Luminal Redox Sensor that Augments MCU Channel Activity Dong, Zhiwei; Shanmughapriya, Santhanam; Tomar, Dhanendra Molecular Cell, Vol. 65, Issue 6 https://doi.org/10.1016/j.molcel.2017.01.032	journal	March 2017
Structural basis of MsbA-mediated lipopolysaccharide transport Mi, Wei; Li, Yanyan; Yoon, Sung Hwan Nature, Vol. 549, Issue 7671 https://doi.org/10.1038/nature23649	journal	September 2017
Structure and symmetry inform gating principles of ionotropic glutamate receptors Zhu, Shujia; Gouaux, Eric Neuropharmacology, Vol. 112 https://doi.org/10.1016/j.neuropharm.2016.08.034	journal	January 2017
A genetically targeted optical sensor to monitor calcium signals in astrocyte processes Shigetomi, Eiji; Kracun, Sebastian; Sofroniew, Michael V. Nature Neuroscience, Vol. 13, Issue 6 https://doi.org/10.1038/nn.2557	journal	May 2010
Structural Insights into Mitochondrial Calcium Uniporter Regulation by Divalent Cations Lee, Samuel K.; Shanmughapriya, Santhanam; Mok, Mac C. Y. Cell Chemical Biology, Vol. 23, Issue 9 https://doi.org/10.1016/j.chembiol.2016.07.012	journal	September 2016
MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake Perocchi, Fabiana; Gohil, Vishal M.; Girgis, Hany S. Nature, Vol. 467, Issue 7313 https://doi.org/10.1038/nature09358	journal	August 2010
The mitochondrial calcium uniporter is a highly selective ion channel Kirichok, Yuriy; Krapivinsky, Grigory; Clapham, David E. Nature, Vol. 427, Issue 6972 https://doi.org/10.1038/nature02246	journal	January 2004
X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Sobolevsky, Alexander I.; Rosconi, Michael P.; Gouaux, Eric Nature, Vol. 462, Issue 7274 https://doi.org/10.1038/nature08624	journal	November 2009
Substrate Recognition at the Cytoplasmic and Extracellular Binding Site of the Lactose Transport Protein of Streptococcus thermophilus Veenhoff, Liesbeth M.; Poolman, Bert Journal of Biological Chemistry, Vol. 274, Issue 47 https://doi.org/10.1074/jbc.274.47.33244	journal	November 1999
CTFFIND4: Fast and accurate defocus estimation from electron micrographs Rohou, Alexis; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 192, Issue 2 https://doi.org/10.1016/j.jsb.2015.08.008	journal	November 2015
MCUR1 Is a Scaffold Factor for the MCU Complex Function and Promotes Mitochondrial Bioenergetics Tomar, Dhanendra; Dong, Zhiwei; Shanmughapriya, Santhanam Cell Reports, Vol. 15, Issue 8 https://doi.org/10.1016/j.celrep.2016.04.050	journal	May 2016
Structure of the voltage-gated calcium channel Cav1.1 at 3.6 Å resolution Wu, Jianping; Yan, Zhen; Li, Zhangqiang Nature, Vol. 537, Issue 7619 https://doi.org/10.1038/nature19321	journal	August 2016
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4193	journal	February 2017
Reconstitution of the mitochondrial calcium uniporter in yeast Kovacs-Bogdan, E.; Sancak, Y.; Kamer, K. J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 24 https://doi.org/10.1073/pnas.1400514111	journal	June 2014
Architecture of the mitochondrial calcium uniporter Oxenoid, Kirill; Dong, Ying; Cao, Chan Nature, Vol. 533, Issue 7602 https://doi.org/10.1038/nature17656	journal	May 2016
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
Calcium Uptake by rat Kidney Mitochondria DeLuca, H. F.; Engstrom, G. W. Proceedings of the National Academy of Sciences, Vol. 47, Issue 11 https://doi.org/10.1073/pnas.47.11.1744	journal	November 1961
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 a Eukaryotic CLC Transporter Defines an Intermediate State in the Transport Cycle Feng, Liang; Campbell, Ernest B.; Hsiung, Yichun Science, Vol. 330, Issue 6004 https://doi.org/10.1126/science.1195230	journal	September 2010
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Likelihood-based classification of cryo-EM images using FREALIGN Lyumkis, Dmitry; Brilot, Axel F.; Theobald, Douglas L. Journal of Structural Biology, Vol. 183, Issue 3 https://doi.org/10.1016/j.jsb.2013.07.005	journal	September 2013
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Quantifying the local resolution of cryo-EM density maps Kucukelbir, Alp; Sigworth, Fred J.; Tagare, Hemant D. Nature Methods, Vol. 11, Issue 1 https://doi.org/10.1038/nmeth.2727	journal	November 2013
Enjoy the Trip: Calcium in Mitochondria Back and Forth De Stefani, Diego; Rizzuto, Rosario; Pozzan, Tullio Annual Review of Biochemistry, Vol. 85, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-034216	journal	June 2016
Crystal Structure of the Calcium Release-Activated Calcium Channel Orai Hou, X.; Pedi, L.; Diver, M. M. Science, Vol. 338, Issue 6112 https://doi.org/10.1126/science.1228757	journal	November 2012
Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria Rizzuto, R.; Brini, M.; Murgia, M. Science, Vol. 262, Issue 5134 https://doi.org/10.1126/science.8235595	journal	October 1993
Mitochondria as sensors and regulators of calcium signalling Rizzuto, Rosario; De Stefani, Diego; Raffaello, Anna Nature Reviews Molecular Cell Biology, Vol. 13, Issue 9 https://doi.org/10.1038/nrm3412	journal	August 2012
Site-directed mutagenesis by overlap extension using the polymerase chain reaction Ho, Steffan N.; Hunt, Henry D.; Horton, Robert M. Gene, Vol. 77, Issue 1, p. 51-59 https://doi.org/10.1016/0378-1119(89)90358-2	journal	April 1989
Mechanisms by which mitochondria transport calcium Gunter, T. E.; Pfeiffer, D. R. American Journal of Physiology-Cell Physiology, Vol. 258, Issue 5 https://doi.org/10.1152/ajpcell.1990.258.5.C755	journal	May 1990
A putative mitochondrial calcium uniporter in A. fumigatus contributes to mitochondrial Ca2+ homeostasis and stress responses Song, Jinxing; Liu, Xiao; Zhai, Pengfei Fungal Genetics and Biology, Vol. 94 https://doi.org/10.1016/j.fgb.2016.07.001	journal	September 2016
Yeast surface display platform for rapid discovery of conformationally selective nanobodies McMahon, Conor; Baier, Alexander S.; Pascolutti, Roberta Nature Structural & Molecular Biology, Vol. 25, Issue 3 https://doi.org/10.1038/s41594-018-0028-6	journal	February 2018
Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter Baughman, Joshua M.; Perocchi, Fabiana; Girgis, Hany S. Nature, Vol. 476, Issue 7360 https://doi.org/10.1038/nature10234	journal	June 2011
Structural basis for Ca2+ selectivity of a voltage-gated calcium channel Tang, Lin; Gamal El-Din, Tamer M.; Payandeh, Jian Nature, Vol. 505, Issue 7481 https://doi.org/10.1038/nature12775	journal	November 2013
MICU1 Controls Both the Threshold and Cooperative Activation of the Mitochondrial Ca2+ Uniporter Csordás, György; Golenár, Tünde; Seifert, Erin L. Cell Metabolism, Vol. 17, Issue 6 https://doi.org/10.1016/j.cmet.2013.04.020	journal	June 2013
Gating machinery of InsP3R channels revealed by electron cryomicroscopy Fan, Guizhen; Baker, Matthew L.; Wang, Zhao Nature, Vol. 527, Issue 7578 https://doi.org/10.1038/nature15249	journal	October 2015
A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter De Stefani, Diego; Raffaello, Anna; Teardo, Enrico Nature, Vol. 476, Issue 7360 https://doi.org/10.1038/nature10230	journal	June 2011
HOLE: A program for the analysis of the pore dimensions of ion channel structural models Smart, Oliver S.; Neduvelil, Joseph G.; Wang, Xiaonan Journal of Molecular Graphics, Vol. 14, Issue 6 https://doi.org/10.1016/S0263-7855(97)00009-X	journal	December 1996
A Bayesian View on Cryo-EM Structure Determination Scheres, Sjors H. W. Journal of Molecular Biology, Vol. 415, Issue 2 https://doi.org/10.1016/j.jmb.2011.11.010	journal	January 2012
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
Structure, Activity Regulation, and Role of the Mitochondrial Calcium Uniporter in Health and Disease Mammucari, Cristina; Gherardi, Gaia; Rizzuto, Rosario Frontiers in Oncology, Vol. 7 https://doi.org/10.3389/fonc.2017.00139	journal	July 2017
Structure and function of the N‐terminal domain of the human mitochondrial calcium uniporter Lee, Youngjin; Min, Choon Kee; Kim, Tae Gyun EMBO reports, Vol. 16, Issue 10 https://doi.org/10.15252/embr.201540436	journal	August 2015
MICU1 and MICU2 Finely Tune the Mitochondrial Ca2+ Uniporter by Exerting Opposite Effects on MCU Activity Patron, Maria; Checchetto, Vanessa; Raffaello, Anna Molecular Cell, Vol. 53, Issue 5 https://doi.org/10.1016/j.molcel.2014.01.013	journal	March 2014
A general protocol for the generation of Nanobodies for structural biology Pardon, Els; Laeremans, Toon; Triest, Sarah Nature Protocols, Vol. 9, Issue 3 https://doi.org/10.1038/nprot.2014.039	journal	February 2014
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
RELION: Implementation of a Bayesian approach to cryo-EM structure determination Scheres, Sjors H. W. Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530 https://doi.org/10.1016/j.jsb.2012.09.006	journal	December 2012
Asynchronous data acquisition and on-the-fly analysis of dose fractionated cryoEM images by UCSFImage Li, Xueming; Zheng, Shawn; Agard, David A. Journal of Structural Biology, Vol. 192, Issue 2 https://doi.org/10.1016/j.jsb.2015.09.003	journal	November 2015
MCU encodes the pore conducting mitochondrial calcium currents Chaudhuri, Dipayan; Sancak, Yasemin; Mootha, Vamsi K. eLife, Vol. 2 https://doi.org/10.7554/eLife.00704	journal	June 2013
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
EMRE Is an Essential Component of the Mitochondrial Calcium Uniporter Complex Sancak, Y.; Markhard, A. L.; Kitami, T. Science, Vol. 342, Issue 6164 https://doi.org/10.1126/science.1242993	journal	November 2013
Lysine Methylation as a Routine Rescue Strategy for Protein Crystallization Walter, Thomas S.; Meier, Christoph; Assenberg, Rene Structure, Vol. 14, Issue 11 https://doi.org/10.1016/j.str.2006.09.005	journal	November 2006
Architecture and conformational switch mechanism of the ryanodine receptor Efremov, Rouslan G.; Leitner, Alexander; Aebersold, Ruedi Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13916	journal	December 2014
Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2 Tallini, Y. N.; Ohkura, M.; Choi, B. -R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 12 https://doi.org/10.1073/pnas.0509378103	journal	March 2006
MCUR1 is an essential component of mitochondrial Ca2+ uptake that regulates cellular metabolism Mallilankaraman, Karthik; Cárdenas, César; Doonan, Patrick J. Nature Cell Biology, Vol. 14, Issue 12 https://doi.org/10.1038/ncb2622	journal	November 2012
The mitochondrial calcium uniporter is a multimer that can include a dominant-negative pore-forming subunit Raffaello, Anna; De Stefani, Diego; Sabbadin, Davide The EMBO Journal, Vol. 32, Issue 17 https://doi.org/10.1038/emboj.2013.157	journal	July 2013
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
Structure of a mammalian ryanodine receptor Zalk, Ran; Clarke, Oliver B.; des Georges, Amédée Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13950	journal	December 2014
Molecular Mechanism of V(D)J Recombination from Synaptic RAG1-RAG2 Complex Structures Ru, Heng; Chambers, Melissa G.; Fu, Tian-Min Cell, Vol. 163, Issue 5 https://doi.org/10.1016/j.cell.2015.10.055	journal	November 2015
Preparation of selenomethionyl proteins for phase determination Doublié, Sylvie Methods in Enzymology https://doi.org/10.1016/S0076-6879(97)76075-0 p. 523-530	book	January 1997
Structural analysis, identification, and design of calcium-binding sites in proteins Yang, Wei; Lee, Hsiau-Wei; Hellinga, Homme Proteins: Structure, Function, and Genetics, Vol. 47, Issue 3 https://doi.org/10.1002/prot.10093	journal	April 2002
Evolutionary Diversity of the Mitochondrial Calcium Uniporter Bick, A. G.; Calvo, S. E.; Mootha, V. K. Science, Vol. 336, Issue 6083 https://doi.org/10.1126/science.1214977	journal	May 2012
Automated electron microscope tomography using robust prediction of specimen movements Mastronarde, David N. Journal of Structural Biology, Vol. 152, Issue 1 https://doi.org/10.1016/j.jsb.2005.07.007	journal	October 2005
High‐affinity cooperative Ca ²⁺ binding by MICU 1– MICU 2 serves as an on–off switch for the uniporter Kamer, Kimberli J.; Grabarek, Zenon; Mootha, Vamsi K. EMBO reports, Vol. 18, Issue 8 https://doi.org/10.15252/embr.201643748	journal	June 2017
[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
Systematic Identification of MCU Modulators by Orthogonal Interspecies Chemical Screening Arduino, Daniela M.; Wettmarshausen, Jennifer; Vais, Horia Molecular Cell, Vol. 67, Issue 4 https://doi.org/10.1016/j.molcel.2017.07.019	journal	August 2017
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007

Similar Records

The effect of mitochondrial calcium uniporter on mitochondrial fission in hippocampus cells ischemia/reperfusion injury

Journal Article · 2015 · Biochemical and Biophysical Research Communications · OSTI ID:22462072

Zhao, Lantao; Li, Shuhong; Wang, Shilei; +2 more

Mitochondrial calcium uniporter silencing potentiates caspase-independent cell death in MDA-MB-231 breast cancer cells

Journal Article · 2013 · Biochemical and Biophysical Research Communications · OSTI ID:22239591

Curry, Merril C.; Peters, Amelia A.; Kenny, Paraic A.; +1 more

Blockage of mitochondrial calcium uniporter prevents iron accumulation in a model of experimental subarachnoid hemorrhage

Journal Article · 2015 · Biochemical and Biophysical Research Communications · OSTI ID:22416904

Yan, Huiying; Hao, Shuangying; Sun, Xiaoyan; +5 more

X-ray and cryo-EM structures of the mitochondrial calcium uniporter

Citation Formats

References (72)

Similar Records

Related Subjects