Quaternary structure independent folding of voltage-gated ion channel pore domain subunits

Arrigoni, Cristina; Lolicato, Marco; Shaya, David; Rohaim, Ahmed; Findeisen, Felix; Fong, Lam-Kiu; Colleran, Claire M.; Dominik, Pawel; Kim, Sangwoo S.; Schuermann, Jonathan P.; DeGrado, William F.; Grabe , Michael; Kossiakoff, Anthony A.; Minor Jr., Daniel L.

doi:10.1038/s41594-022-00775-x

Title: Quaternary structure independent folding of voltage-gated ion channel pore domain subunits

Journal Article · 01 June 2022 · Nat. Struct. Mol. Biol.

DOI:https://doi.org/10.1038/s41594-022-00775-x· OSTI ID:1878400

Arrigoni, Cristina; Lolicato, Marco; Shaya, David; Rohaim, Ahmed; Findeisen, Felix; Fong, Lam-Kiu; Colleran, Claire M.; Dominik, Pawel; Kim, Sangwoo S.; Schuermann, Jonathan P.; DeGrado, William F.; Grabe , Michael; Kossiakoff, Anthony A.; Minor Jr., Daniel L.

Cite

Export

Save

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

Sponsoring Organization:: DOE - Office Of Science; National Institutes of Health (NIH); OTHER

OSTI ID:: 1878400

Journal Information:: Nat. Struct. Mol. Biol., Vol. 29

Country of Publication:: United States

Language:: ENGLISH

References (82)

The VGL-Chanome: A Protein Superfamily Specialized for Electrical Signaling and Ionic Homeostasis Yu, F. H.; Catterall, W. A. Science Signaling, Vol. 2004, Issue 253 https://doi.org/10.1126/stke.2532004re15	journal	September 2004
Conduits of Life’s Spark: A Perspective on Ion Channel Research since the Birth of Neuron Isacoff, Ehud Y.; Jan, Lily Y.; Minor, Daniel L. Neuron, Vol. 80, Issue 3 https://doi.org/10.1016/j.neuron.2013.10.040	journal	October 2013
Structural Pharmacology of TRP Channels Zhao, Yaxian; McVeigh, Bridget M.; Moiseenkova-Bell, Vera Y. Journal of Molecular Biology, Vol. 433, Issue 17 https://doi.org/10.1016/j.jmb.2021.166914	journal	August 2021
The chemical basis for electrical signaling Catterall, William A.; Wisedchaisri, Goragot; Zheng, Ning Nature Chemical Biology, Vol. 13, Issue 5 https://doi.org/10.1038/nchembio.2353	journal	April 2017
Targeting Two-Pore Channels: Current Progress and Future Challenges Jin, Xuhui; Zhang, Yuxuan; Alharbi, Abeer Trends in Pharmacological Sciences, Vol. 41, Issue 8 https://doi.org/10.1016/j.tips.2020.06.002	journal	August 2020
Structural Insights into the Mechanisms and Pharmacology of K2P Potassium Channels Natale, Andrew M.; Deal, Parker E.; Minor, Daniel L. Journal of Molecular Biology, Vol. 433, Issue 17 https://doi.org/10.1016/j.jmb.2021.166995	journal	August 2021
The activated state of a sodium channel voltage sensor in a membrane environment Chakrapani, S.; Sompornpisut, P.; Intharathep, P. Proceedings of the National Academy of Sciences, Vol. 107, Issue 12 https://doi.org/10.1073/pnas.0914109107	journal	March 2010
Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain Li, Qufei; Wanderling, Sherry; Paduch, Marcin Nature Structural & Molecular Biology, Vol. 21, Issue 3 https://doi.org/10.1038/nsmb.2768	journal	February 2014
Structural basis of lipid-driven conformational transitions in the KvAP voltage-sensing domain Li, Qufei; Wanderling, Sherry; Sompornpisut, Pornthep Nature Structural & Molecular Biology, Vol. 21, Issue 2 https://doi.org/10.1038/nsmb.2747	journal	January 2014
Voltage-gated sodium channel (NaV) protein dissection creates a set of functional pore-only proteins Shaya, D.; Kreir, M.; Robbins, R. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 30 https://doi.org/10.1073/pnas.1106811108	journal	July 2011
Structure of a Prokaryotic Sodium Channel Pore Reveals Essential Gating Elements and an Outer Ion Binding Site Common to Eukaryotic Channels Shaya, David; Findeisen, Felix; Abderemane-Ali, Fayal Journal of Molecular Biology, Vol. 426, Issue 2 https://doi.org/10.1016/j.jmb.2013.10.010	journal	January 2014
Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing McCusker, Emily C.; Bagnéris, Claire; Naylor, Claire E. Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2077	journal	January 2012
Simplified Bacterial “Pore” Channel Provides Insight into the Assembly, Stability, and Structure of Sodium Channels McCusker, Emily C.; D'Avanzo, Nazzareno; Nichols, Colin G. Journal of Biological Chemistry, Vol. 286, Issue 18 https://doi.org/10.1074/jbc.C111.228122	journal	May 2011
Bacterial Voltage-Gated Sodium Channels (BacNaVs) from the Soil, Sea, and Salt Lakes Enlighten Molecular Mechanisms of Electrical Signaling and Pharmacology in the Brain and Heart Payandeh, Jian; Minor, Daniel L. Journal of Molecular Biology, Vol. 427, Issue 1 https://doi.org/10.1016/j.jmb.2014.08.010	journal	January 2015
The voltage-gated sodium channel pore exhibits conformational flexibility during slow inactivation Chatterjee, Soumili; Vyas, Rajan; Chalamalasetti, Sreevatsa V. Journal of General Physiology, Vol. 150, Issue 9 https://doi.org/10.1085/jgp.201812118	journal	August 2018
Characterization of the Prokaryotic Sodium Channel NavSp Pore with a Microfluidic Bilayer Platform Saha, Shimul Chandra; Henderson, Alexander J.; Powl, Andrew M. PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0131286	journal	July 2015
Role of the C-terminal domain in the structure and function of tetrameric sodium channels Bagnéris, Claire; DeCaen, Paul G.; Hall, Benjamin A. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3465	journal	September 2013
Unfolding of a Temperature-Sensitive Domain Controls Voltage-Gated Channel Activation Arrigoni, Cristina; Rohaim, Ahmed; Shaya, David Cell, Vol. 164, Issue 5 https://doi.org/10.1016/j.cell.2016.02.001	journal	February 2016
Molecular basis of ion permeability in a voltage‐gated sodium channel Naylor, Claire E.; Bagnéris, Claire; DeCaen, Paul G. The EMBO Journal, Vol. 35, Issue 8 https://doi.org/10.15252/embj.201593285	journal	February 2016
Prokaryotic NavMs channel as a structural and functional model for eukaryotic sodium channel antagonism Bagneris, C.; DeCaen, P. G.; Naylor, C. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 23 https://doi.org/10.1073/pnas.1406855111	journal	May 2014
Potassium Channel Ontogeny Deutsch, Carol Annual Review of Physiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.physiol.64.081501.155934	journal	March 2002
The Birth of a Channel Deutsch, Carol Neuron, Vol. 40, Issue 2 https://doi.org/10.1016/S0896-6273(03)00506-3	journal	October 2003
Biogenesis of the pore architecture of a voltage-gated potassium channel Gajewski, Christine; Dagcan, Alper; Roux, Benoit Proceedings of the National Academy of Sciences, Vol. 108, Issue 8 https://doi.org/10.1073/pnas.1017097108	journal	February 2011
Determinants of pore folding in potassium channel biogenesis Delaney, Erin; Khanna, Pooja; Tu, LiWei Proceedings of the National Academy of Sciences, Vol. 111, Issue 12 https://doi.org/10.1073/pnas.1324274111	journal	March 2014
A Shared Mechanism for the Folding of Voltage-Gated K ⁺ Channels McDonald, Sarah K.; Levitz, Talya S.; Valiyaveetil, Francis I. Biochemistry, Vol. 58, Issue 12 https://doi.org/10.1021/acs.biochem.9b00068	journal	February 2019
Membrane protein folding and oligomerization: the two-stage model Popot, J. L.; Engelman, D. M. Biochemistry, Vol. 29, Issue 17 https://doi.org/10.1021/bi00469a001	journal	May 1990
Refolding of bacteriorhodopsin in lipid bilayers Popot, Jean-Luc; Gerchman, Sue-Ellen; Engelman, Donald M. Journal of Molecular Biology, Vol. 198, Issue 4 https://doi.org/10.1016/0022-2836(87)90208-7	journal	December 1987
The Structure of α-Helical Coiled Coils Lupas, Andrei N.; Gruber, Markus Fibrous Proteins: Coiled-Coils, Collagen and Elastomers, p. 37-38 https://doi.org/10.1016/S0065-3233(05)70003-6	book	January 2005
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Rice Cellulose SynthaseA8 Plant-Conserved Region Is a Coiled-Coil at the Catalytic Core Entrance Rushton, Phillip S.; Olek, Anna T.; Makowski, Lee Plant Physiology, Vol. 173, Issue 1 https://doi.org/10.1104/pp.16.00739	journal	November 2016
Structure of the Shroom-Rho Kinase Complex Reveals a Binding Interface with Monomeric Shroom That Regulates Cell Morphology and Stimulates Kinase Activity Zalewski, Jenna K.; Mo, Joshua H.; Heber, Simone Journal of Biological Chemistry, Vol. 291, Issue 49 https://doi.org/10.1074/jbc.M116.738559	journal	December 2016
High-Light versus Low-Light: Effects on Paired Photosystem II Supercomplex Structural Rearrangement in Pea Plants Grinzato, Alessandro; Albanese, Pascal; Marotta, Roberto International Journal of Molecular Sciences, Vol. 21, Issue 22 https://doi.org/10.3390/ijms21228643	journal	November 2020
The crystal structure of a voltage-gated sodium channel Payandeh, Jian; Scheuer, Todd; Zheng, Ning Nature, Vol. 475, Issue 7356 https://doi.org/10.1038/nature10238	journal	July 2011
Packing of apolar side chains enables accurate design of highly stable membrane proteins Mravic, Marco; Thomaston, Jessica L.; Tucker, Maxwell Science, Vol. 363, Issue 6434 https://doi.org/10.1126/science.aav7541	journal	March 2019
The spontaneous insertion of proteins into and across membranes: The helical hairpin hypothesis Engelman, D. M.; Steitz, T. A. Cell, Vol. 23, Issue 2 https://doi.org/10.1016/0092-8674(81)90136-7	journal	February 1981
Hydrogen bonding in globular proteins Baker, E. N.; Hubbard, R. E. Progress in Biophysics and Molecular Biology, Vol. 44, Issue 2 https://doi.org/10.1016/0079-6107(84)90007-5	journal	January 1984
Crystal structure of full-length KcsA in its closed conformation Uysal, S.; Vasquez, V.; Tereshko, V. Proceedings of the National Academy of Sciences, Vol. 106, Issue 16 https://doi.org/10.1073/pnas.0810663106	journal	April 2009
Phage Display Selections for Affinity Reagents to Membrane Proteins in Nanodiscs Dominik, Pawel K.; Kossiakoff, Anthony A. Methods in Enzymology https://doi.org/10.1016/bs.mie.2014.12.032	book	January 2015
Fluorescence-Detection Size-Exclusion Chromatography for Precrystallization Screening of Integral Membrane Proteins Kawate, Toshimitsu; Gouaux, Eric Structure, Vol. 14, Issue 4 https://doi.org/10.1016/j.str.2006.01.013	journal	April 2006
K2P2.1 (TREK-1)–activator complexes reveal a cryptic selectivity filter binding site Lolicato, Marco; Arrigoni, Cristina; Mori, Takahiro Nature, Vol. 547, Issue 7663 https://doi.org/10.1038/nature22988	journal	July 2017
Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin Zakeri, B.; Fierer, J. O.; Celik, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 12 https://doi.org/10.1073/pnas.1115485109	journal	February 2012
Styrene maleic-acid lipid particles (SMALPs) into detergent or amphipols: An exchange protocol for membrane protein characterisation Hesketh, Sophie J.; Klebl, David P.; Higgins, Anna J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1862, Issue 5 https://doi.org/10.1016/j.bbamem.2020.183192	journal	May 2020
Mechanisms of Integral Membrane Protein Insertion and Folding Cymer, Florian; von Heijne, Gunnar; White, Stephen H. Journal of Molecular Biology, Vol. 427, Issue 5 https://doi.org/10.1016/j.jmb.2014.09.014	journal	March 2015
Membranes Do Not Tell Proteins How To Fold Popot, Jean-Luc; Engelman, Donald M. Biochemistry, Vol. 55, Issue 1 https://doi.org/10.1021/acs.biochem.5b01134	journal	December 2015
Ribosome Profiling of Mouse Embryonic Stem Cells Reveals the Complexity and Dynamics of Mammalian Proteomes Ingolia, Nicholas T.; Lareau, Liana F.; Weissman, Jonathan S. Cell, Vol. 147, Issue 4 https://doi.org/10.1016/j.cell.2011.10.002	journal	November 2011
Pulse-chase studies of the synthesis and intracellular transport of apolipoprotein B-100 in Hep G2 cells. Boström, K.; Wettesten, M.; Borén, J. Journal of Biological Chemistry, Vol. 261, Issue 29 https://doi.org/10.1016/S0021-9258(18)67090-5	journal	October 1986
Crystal structure of a voltage-gated sodium channel in two potentially inactivated states Payandeh, Jian; Gamal El-Din, Tamer M.; Scheuer, Todd Nature, Vol. 486, Issue 7401 https://doi.org/10.1038/nature11077	journal	May 2012
Structural basis for inhibition of a voltage-gated Ca2+ channel by Ca2+ antagonist drugs Tang, Lin; Gamal El-Din, Tamer M.; Swanson, Teresa M. Nature, Vol. 537, Issue 7618 https://doi.org/10.1038/nature19102	journal	August 2016
Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel Zhang, Xu; Ren, Wenlin; DeCaen, Paul Nature, Vol. 486, Issue 7401 https://doi.org/10.1038/nature11054	journal	May 2012
Protein structural motifs in prediction and design Mackenzie, Craig O.; Grigoryan, Gevorg Current Opinion in Structural Biology, Vol. 44 https://doi.org/10.1016/j.sbi.2017.03.012	journal	June 2017
From ancestral peptides to designed proteins Alva, Vikram; Lupas, Andrei N. Current Opinion in Structural Biology, Vol. 48 https://doi.org/10.1016/j.sbi.2017.11.006	journal	February 2018
Conformational Chaperones for Structural Studies of Membrane Proteins Using Antibody Phage Display with Nanodiscs Dominik, Pawel K.; Borowska, Marta T.; Dalmas, Olivier Structure, Vol. 24, Issue 2 https://doi.org/10.1016/j.str.2015.11.014	journal	February 2016
Directed Self-Assembly of Monodisperse Phospholipid Bilayer Nanodiscs with Controlled Size Denisov, I. G.; Grinkova, Y. V.; Lazarides, A. A. Journal of the American Chemical Society, Vol. 126, Issue 11 https://doi.org/10.1021/ja0393574	journal	March 2004
T Cell Receptor-Like Recognition of Tumor In Vivo by Synthetic Antibody Fragment Miller, Keith R.; Koide, Akiko; Leung, Brenda PLoS ONE, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pone.0043746	journal	August 2012
A YidC-like Protein in the Archaeal Plasma Membrane Borowska, Marta T.; Dominik, Pawel K.; Anghel, S. Andrei Structure, Vol. 23, Issue 9 https://doi.org/10.1016/j.str.2015.06.025	journal	September 2015
Locking the Elbow: Improved Antibody Fab Fragments as Chaperones for Structure Determination Bailey, Lucas J.; Sheehy, Kimberly M.; Dominik, Pawel K. Journal of Molecular Biology, Vol. 430, Issue 3 https://doi.org/10.1016/j.jmb.2017.12.012	journal	February 2018
Reconstitution of Membrane Proteins in Phospholipid Bilayer Nanodiscs Ritchie, T. K.; Grinkova, Y. V.; Bayburt, T. H. Methods in Enzymology https://doi.org/10.1016/S0076-6879(09)64011-8	book	January 2009
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
Crystallizing membrane proteins using lipidic bicelles Ujwal, Rachna; Bowie, James U. Methods, Vol. 55, Issue 4 https://doi.org/10.1016/j.ymeth.2011.09.020	journal	December 2011
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
An introduction to data reduction: space-group determination, scaling and intensity statistics Evans, Philip R. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S090744491003982X	journal	March 2011
A short history of SHELX Sheldrick, George M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122 https://doi.org/10.1107/S0108767307043930	journal	December 2007
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
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
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
How good are my data and what is the resolution? Evans, Philip R.; Murshudov, Garib N. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000061	journal	June 2013
Engineering Synthetic Antibody Inhibitors Specific for LD2 or LD4 Motifs of Paxillin Nocula-Lugowska, Malgorzata; Lugowski, Mateusz; Salgia, Ravi Journal of Molecular Biology, Vol. 427, Issue 15 https://doi.org/10.1016/j.jmb.2015.06.004	journal	July 2015
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
Automatic protein structure solution from weak X-ray data Skubák, Pavol; Pannu, Navraj S. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3777	journal	November 2013
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination Brünger, A. T.; Adams, P. D.; Clore, G. M. Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5 https://doi.org/10.1107/S0907444998003254	journal	September 1998
Version 1.2 of the Crystallography and NMR system Brunger, Axel T. Nature Protocols, Vol. 2, Issue 11 https://doi.org/10.1038/nprot.2007.406	journal	October 2007
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
Automated Builder and Database of Protein/Membrane Complexes for Molecular Dynamics Simulations Jo, Sunhwan; Kim, Taehoon; Im, Wonpil PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000880	journal	September 2007
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00255	journal	July 2015
Lipid14: The Amber Lipid Force Field Dickson, Callum J.; Madej, Benjamin D.; Skjevik, Åge A. Journal of Chemical Theory and Computation, Vol. 10, Issue 2 https://doi.org/10.1021/ct4010307	journal	January 2014
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan Journal of Chemical Theory and Computation, Vol. 9, Issue 9 https://doi.org/10.1021/ct400314y	journal	August 2013
Molecular dynamics simulations of water and biomolecules with a Monte Carlo constant pressure algorithm Åqvist, Johan; Wennerström, Petra; Nervall, Martin Chemical Physics Letters, Vol. 384, Issue 4-6 https://doi.org/10.1016/j.cplett.2003.12.039	journal	January 2004
Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models Miyamoto, Shuichi; Kollman, Peter A. Journal of Computational Chemistry, Vol. 13, Issue 8 https://doi.org/10.1002/jcc.540130805	journal	October 1992
Taking the Monte‐Carlo gamble: How not to buckle under the pressure! Gomez, Yessica K.; Natale, Andrew M.; Lincoff, James Journal of Computational Chemistry, Vol. 43, Issue 6 https://doi.org/10.1002/jcc.26798	journal	December 2021
PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data Roe, Daniel R.; Cheatham, Thomas E. Journal of Chemical Theory and Computation, Vol. 9, Issue 7 https://doi.org/10.1021/ct400341p	journal	June 2013

Similar Records

Quaternary structure independent folding of voltage-gated ion channel pore domain subunits

Journal Article · 2022 · Nat. Struct. Mol. Biol. · OSTI ID:1878400

Arrigoni, Cristina; Lolicato, Marco; Shaya, David; +11 more

Quaternary structure independent folding of voltage-gated ion channel pore domain subunits

Journal Article · 2022 · Nature Structural & Molecular Biology · OSTI ID:1878400

Arrigoni, Cristina; Lolicato, Marco; Shaya, David; +11 more

STRUCTURAL BASIS OF THE ALPHA 1-BETA SUBUNIT INTERACTION OF VOLTAGE-GATED CA2+ CHANNELS

Journal Article · 2004 · Nature · OSTI ID:1878400

CHEN, Y; LI, M; ZHANG, Y; +7 more

Title: Quaternary structure independent folding of voltage-gated ion channel pore domain subunits

Citation Formats

References (82)

Similar Records

Related Subjects