Unique roles of iron and zinc binding to the yeast Fe–S cluster scaffold assembly protein “Isu1”

Lewis, Brianne E.; Mason, Zachary; Rodrigues, Andria V.; Nuth, Manunya; Dizin, Eric; Cowan, J. A.; Stemmler, Timothy L.

doi:10.1039/C9MT00172G

Title: Unique roles of iron and zinc binding to the yeast Fe–S cluster scaffold assembly protein “Isu1”

Journal Article · 13 November 2019 · Metallomics

DOI: https://doi.org/10.1039/C9MT00172G · OSTI ID:1562561

Lewis, Brianne E. ^[1]; Mason, Zachary ^[1]; Rodrigues, Andria V. ^[1]; Nuth, Manunya ^[2]; Dizin, Eric ^[2]; Cowan, J. A. ^[2];

^[1]

Department of Pharmaceutical Science, Wayne State University, Detroit, USA
Department of Chemistry, The Ohio State University, Columbus, USA

Model for Zn association to the active site of yeast Fe–S cluster assembly scaffold protein Isu1.

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Sponsoring Organization:: USDOE

OSTI ID:: 1562561

Journal Information:: Metallomics, Journal Name: Metallomics Journal Issue: 11 Vol. 11; ISSN METAIR; ISSN 1756-5901

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (67)

Protein Structure and Function Prediction Using I‐TASSER Yang, Jianyi; Zhang, Yang Current Protocols in Bioinformatics, Vol. 52, Issue 1 https://doi.org/10.1002/0471250953.bi0508s52	journal	December 2015
The Scaffold Protein IscU Retains a Structured Conformation in the FeS Cluster Assembly Complex Yan, Robert; Kelly, Geoff; Pastore, Annalisa ChemBioChem, Vol. 15, Issue 11 https://doi.org/10.1002/cbic.201402211	journal	July 2014
The role of zinc in the stability of the marginally stable IscU scaffold protein: The Stability Determinants of IscU Iannuzzi, Clara; Adrover, Miquel; Puglisi, Rita Protein Science, Vol. 23, Issue 9 https://doi.org/10.1002/pro.2501	journal	July 2014
Clustal Omega for making accurate alignments of many protein sequences: Clustal Omega for Many Protein Sequences Sievers, Fabian; Higgins, Desmond G. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3290	journal	October 2017
Structural characterization of an iron-sulfur cluster assembly protein IscU in a zinc-bound form Liu, Jinyu; Oganesyan, Natalia; Shin, Dong-Hae Proteins: Structure, Function, and Bioinformatics, Vol. 59, Issue 4 https://doi.org/10.1002/prot.20421	journal	April 2005
Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase Kuzmič, Petr Analytical Biochemistry, Vol. 237, Issue 2 https://doi.org/10.1006/abio.1996.0238	journal	June 1996
Mapping iron binding sites on human frataxin: implications for cluster assembly on the ISU Fe–S cluster scaffold protein Huang, Jia; Dizin, Eric; Cowan, J. A. JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 5 https://doi.org/10.1007/s00775-008-0369-4	journal	April 2008
Iron loading site on the Fe–S cluster assembly scaffold protein is distinct from the active site Rodrigues, Andria V.; Kandegedara, Ashoka; Rotondo, John A. BioMetals, Vol. 28, Issue 3 https://doi.org/10.1007/s10534-015-9846-8	journal	March 2015
Zinc Distribution and Expression Pattern of ZnT3 in Mouse Brain Shen, Hui; Wang, Fudi; Zhang, Yuanxun Biological Trace Element Research, Vol. 119, Issue 2 https://doi.org/10.1007/s12011-007-0056-2	journal	June 2007
Mitochondrial functional interactions between frataxin and Isu1p, the iron-sulfur cluster scaffold protein, in Saccharomyces cerevisiae Ramazzotti, Anna; Vanmansart, Vincent; Foury, Françoise FEBS Letters, Vol. 557, Issue 1-3 https://doi.org/10.1016/S0014-5793(03)01498-4	journal	December 2003
Synthesis, delivery and regulation of eukaryotic heme and Fe–S cluster cofactors Barupala, Dulmini P.; Dzul, Stephen P.; Riggs-Gelasco, Pamela Jo Archives of Biochemistry and Biophysics, Vol. 592 https://doi.org/10.1016/j.abb.2016.01.010	journal	February 2016
Special issue on iron–sulfur proteins: Structure, function, biogenesis and diseases Lill, Roland; Broderick, Joan B.; Dean, Dennis R. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 6 https://doi.org/10.1016/j.bbamcr.2015.03.001	journal	June 2015
Zinc(II) binding on human wild-type ISCU and Met140 variants modulates NFS1 desulfurase activity Fox, Nicholas G.; Martelli, Alain; Nabhan, Joseph F. Biochimie, Vol. 152 https://doi.org/10.1016/j.biochi.2018.07.012	journal	September 2018
Metamorphic protein IscU alternates conformations in the course of its role as the scaffold protein for iron-sulfur cluster biosynthesis and delivery Markley, John L.; Kim, Jin Hae; Dai, Ziqi FEBS Letters, Vol. 587, Issue 8 https://doi.org/10.1016/j.febslet.2013.01.003	journal	January 2013
Iron Binding and Oxidation Kinetics in Frataxin CyaY of Escherichia coli Bou-Abdallah, Fadi; Adinolfi, Salvatore; Pastore, Annalisa Journal of Molecular Biology, Vol. 341, Issue 2 https://doi.org/10.1016/j.jmb.2004.05.072	journal	August 2004
Solution NMR Structure of the Iron–Sulfur Cluster Assembly Protein U (IscU) with Zinc Bound at the Active Site Ramelot, Theresa A.; Cort, John R.; Goldsmith-Fischman, Sharon Journal of Molecular Biology, Vol. 344, Issue 2 https://doi.org/10.1016/j.jmb.2004.08.038	journal	November 2004
The Asymmetric Trimeric Architecture of [2Fe–2S] IscU: Implications for Its Scaffolding during Iron–Sulfur Cluster Biosynthesis Shimomura, Yoshimitsu; Wada, Kei; Fukuyama, Keiichi Journal of Molecular Biology, Vol. 383, Issue 1 https://doi.org/10.1016/j.jmb.2008.08.015	journal	October 2008
Recovery of mrs3Δmrs4Δ Saccharomyces cerevisiae Cells under Iron-Sufficient Conditions and the Role of Fe ₅₈₀ Moore, Michael J.; Wofford, Joshua D.; Dancis, Andrew Biochemistry, Vol. 57, Issue 5 https://doi.org/10.1021/acs.biochem.7b01034	journal	January 2018
ISCU(M108I) and ISCU(D39V) Differ from Wild-Type ISCU in Their Failure To Form Cysteine Desulfurase Complexes Containing Both Frataxin and Ferredoxin Cai, Kai; Frederick, Ronnie O.; Tonelli, Marco Biochemistry, Vol. 57, Issue 9 https://doi.org/10.1021/acs.biochem.7b01234	journal	February 2018
Comparison of the Response of Bacterial IscU and SufU to Zn ²⁺ and Select Transition-Metal Ions Roy, Poorna; Bauman, Mariia A.; Almutairi, Hayfa Habes ACS Chemical Biology, Vol. 13, Issue 3 https://doi.org/10.1021/acschembio.7b00442	journal	December 2017
Iron−Sulfur Cluster Biosynthesis: Toward an Understanding of Cellular Machinery and Molecular Mechanism ^† Mansy, Sheref S.; Cowan, J. A. Accounts of Chemical Research, Vol. 37, Issue 9 https://doi.org/10.1021/ar0301781	journal	September 2004
Analysis of Sulfur Biochemistry of Sulfur Bacteria Using X-ray Absorption Spectroscopy ^† Pickering, Ingrid J.; George, Graham N.; Yu, Eileen Y. Biochemistry, Vol. 40, Issue 27 https://doi.org/10.1021/bi0105532	journal	July 2001
Yeast Frataxin Solution Structure, Iron Binding, and Ferrochelatase Interaction ^† ^, ^‡ He, Yanan; Alam, Steven L.; Proteasa, Simona V. Biochemistry, Vol. 43, Issue 51 https://doi.org/10.1021/bi0488193	journal	December 2004
Monomeric Yeast Frataxin Is an Iron-Binding Protein ^† Cook, Jeremy D.; Bencze, Krisztina Z.; Jankovic, Ana D. Biochemistry, Vol. 45, Issue 25 https://doi.org/10.1021/bi060424r	journal	June 2006
A Nonheme High-Spin Ferrous Pool in Mitochondria Isolated from Fermenting Saccharomyces cerevisiae Holmes-Hampton, Gregory P.; Miao, Ren; Garber Morales, Jessica Biochemistry, Vol. 49, Issue 19 https://doi.org/10.1021/bi1001823	journal	May 2010
Molecular Details of the Yeast Frataxin−Isu1 Interaction during Mitochondrial Fe−S Cluster Assembly Cook, Jeremy D.; Kondapalli, Kalyan C.; Rawat, Swati Biochemistry, Vol. 49, Issue 40 https://doi.org/10.1021/bi1008613	journal	October 2010
Human Frataxin Is an Allosteric Switch That Activates the Fe−S Cluster Biosynthetic Complex Tsai, Chi-Lin; Barondeau, David P. Biochemistry, Vol. 49, Issue 43 https://doi.org/10.1021/bi1013062	journal	November 2010
Three-Dimensional Structure and Determinants of Stability of the Iron–Sulfur Cluster Scaffold Protein IscU from Escherichia coli Kim, Jin Hae; Tonelli, Marco; Kim, Taewook Biochemistry, Vol. 51, Issue 28 https://doi.org/10.1021/bi300579p	journal	July 2012
Human Frataxin Activates Fe–S Cluster Biosynthesis by Facilitating Sulfur Transfer Chemistry Bridwell-Rabb, Jennifer; Fox, Nicholas G.; Tsai, Chi-Lin Biochemistry, Vol. 53, Issue 30 https://doi.org/10.1021/bi500532e	journal	July 2014
The Human Iron–Sulfur Assembly Complex Catalyzes the Synthesis of [2Fe-2S] Clusters on ISCU2 That Can Be Transferred to Acceptor Molecules Fox, Nicholas G.; Chakrabarti, Mrinmoy; McCormick, Sean P. Biochemistry, Vol. 54, Issue 25 https://doi.org/10.1021/bi5014485	journal	June 2015
Detection of Labile Low-Molecular-Mass Transition Metal Complexes in Mitochondria McCormick, Sean P.; Moore, Michael J.; Lindahl, Paul A. Biochemistry, Vol. 54, Issue 22 https://doi.org/10.1021/bi5015437	journal	May 2015
Structure and Dynamics of the Iron−Sulfur Cluster Assembly Scaffold Protein IscU and Its Interaction with the Cochaperone HscB Kim, Jin Hae; Füzéry, Anna K.; Tonelli, Marco Biochemistry, Vol. 48, Issue 26 https://doi.org/10.1021/bi9002277	journal	July 2009
X-ray Absorption Pre-Edge Studies of High-spin Iron(II) Complexes Randall, Clayton R.; Shu, Lijin; Chiou, Yu-Min Inorganic Chemistry, Vol. 34, Issue 5 https://doi.org/10.1021/ic00109a007	journal	March 1995
A Mutant Human IscU Protein Contains a Stable [2Fe−2S]²⁺ Center of Possible Functional Significance Foster, Matthew W.; Mansy, Sheref S.; Hwang, Jungwon Journal of the American Chemical Society, Vol. 122, Issue 28 https://doi.org/10.1021/ja000800+	journal	June 2000
Iron−Sulfur Cluster Biosynthesis: Characterization of Iron Nucleation Sites for Assembly of the [2Fe−2S] ²⁺ Cluster Core in IscU Proteins Nuth, Manunya; Yoon, Taejin; Cowan, J. A. Journal of the American Chemical Society, Vol. 124, Issue 30 https://doi.org/10.1021/ja0264596	journal	July 2002
Order of Stability of Metal Complexes Irving, H.; Williams, R. J. P. Nature, Vol. 162, Issue 4123 https://doi.org/10.1038/162746a0	journal	November 1948
A new metal binding domain involved in cadmium, cobalt and zinc transport Smith, Aaron T.; Barupala, Dulmini; Stemmler, Timothy L. Nature Chemical Biology, Vol. 11, Issue 9 https://doi.org/10.1038/nchembio.1863	journal	July 2015
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS Adinolfi, Salvatore; Iannuzzi, Clara; Prischi, Filippo Nature Structural & Molecular Biology, Vol. 16, Issue 4 https://doi.org/10.1038/nsmb.1579	journal	March 2009
Structure and functional dynamics of the mitochondrial Fe/S cluster synthesis complex Boniecki, Michal T.; Freibert, Sven A.; Mühlenhoff, Ulrich Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01497-1	journal	November 2017
Structure of the human frataxin-bound iron-sulfur cluster assembly complex provides insight into its activation mechanism Fox, Nicholas G.; Yu, Xiaodi; Feng, Xidong Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09989-y	journal	May 2019
Physiologically relevant reconstitution of iron-sulfur cluster biosynthesis uncovers persulfide-processing functions of ferredoxin-2 and frataxin Gervason, Sylvain; Larkem, Djabir; Mansour, Amir Ben Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11470-9	journal	August 2019
The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria Adam, Alexander C.; Bornhövd, Carsten; Prokisch, Holger The EMBO Journal, Vol. 25, Issue 1 https://doi.org/10.1038/sj.emboj.7600905	journal	December 2005
Essential role of Isd11 in mitochondrial iron–sulfur cluster synthesis on Isu scaffold proteins Wiedemann, Nils; Urzica, Eugen; Guiard, Bernard The EMBO Journal, Vol. 25, Issue 1 https://doi.org/10.1038/sj.emboj.7600906	journal	December 2005
Acidic residues of yeast frataxin have an essential role in Fe–S cluster assembly Foury, Françoise; Pastore, Annalisa; Trincal, Mathieu EMBO reports, Vol. 8, Issue 2 https://doi.org/10.1038/sj.embor.7400881	journal	December 2006
An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1 Gerber, Jana; Mühlenhoff, Ulrich; Lill, Roland EMBO reports, Vol. 4, Issue 9 https://doi.org/10.1038/sj.embor.embor918	journal	August 2003
In vitro characterization of a novel Isu homologue from Drosophila melanogaster for de novo FeS-cluster formation Dzul, Stephen P.; Rocha, Agostinho G.; Rawat, Swati Metallomics, Vol. 9, Issue 1 https://doi.org/10.1039/C6MT00163G	journal	January 2017
Iron–sulfur cluster biosynthesis and trafficking – impact on human disease conditions Wachnowsky, C.; Fidai, I.; Cowan, J. A. Metallomics, Vol. 10, Issue 1 https://doi.org/10.1039/C7MT00180K	journal	January 2018
Iron–sulfur cluster biosynthesis Bandyopadhyay, Sibali; Chandramouli, Kala; Johnson, Michael K. Biochemical Society Transactions, Vol. 36, Issue 6 https://doi.org/10.1042/BST0361112	journal	November 2008
Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis Sheftel, A. D.; Stehling, O.; Pierik, A. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 26 https://doi.org/10.1073/pnas.1004250107	journal	June 2010
Cleavage and polyadenylation specificity factor 30: An RNA-binding zinc-finger protein with an unexpected 2Fe–2S cluster Shimberg, Geoffrey D.; Michalek, Jamie L.; Oluyadi, Abdulafeez A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 17 https://doi.org/10.1073/pnas.1517620113	journal	April 2016
Structure of human Fe–S assembly subcomplex reveals unexpected cysteine desulfurase architecture and acyl-ACP–ISD11 interactions Cory, Seth A.; Van Vranken, Jonathan G.; Brignole, Edward J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1702849114	journal	June 2017
Frataxin Directly Stimulates Mitochondrial Cysteine Desulfurase by Exposing Substrate-binding Sites, and a Mutant Fe-S Cluster Scaffold Protein with Frataxin-bypassing Ability Acts Similarly Pandey, Alok; Gordon, Donna M.; Pain, Jayashree Journal of Biological Chemistry, Vol. 288, Issue 52 https://doi.org/10.1074/jbc.M113.525857	journal	November 2013
Structure and Ubiquitin Interactions of the Conserved Zinc Finger Domain of Npl4 Wang, Bin; Alam, Steven L.; Meyer, Hemmo H. Journal of Biological Chemistry, Vol. 278, Issue 22 https://doi.org/10.1074/jbc.M300459200	journal	March 2003
Yeast Frataxin Sequentially Chaperones and Stores Iron by Coupling Protein Assembly with Iron Oxidation Park, Sungjo; Gakh, Oleksandr; O'Neill, Heather A. Journal of Biological Chemistry, Vol. 278, Issue 33 https://doi.org/10.1074/jbc.M303158200	journal	May 2003
Characterization and Structure of a Zn ²⁺ and [2Fe-2S]-containing Copper Chaperone from Archaeoglobus fulgidus Sazinsky, Matthew H.; LeMoine, Benjamin; Orofino, Maria Journal of Biological Chemistry, Vol. 282, Issue 35 https://doi.org/10.1074/jbc.M703311200	journal	July 2007
Binding of Yeast Frataxin to the Scaffold for Fe-S Cluster Biogenesis, Isu Wang, Tao; Craig, Elizabeth A. Journal of Biological Chemistry, Vol. 283, Issue 18 https://doi.org/10.1074/jbc.M800399200	journal	March 2008
Iron–sulfur cluster biogenesis and trafficking in mitochondria Braymer, Joseph J.; Lill, Roland Journal of Biological Chemistry, Vol. 292, Issue 31 https://doi.org/10.1074/jbc.R117.787101	journal	June 2017
Progress and challenges in the theory and interpretation of X-ray spectra Rehr, J. J.; Ankudinov, A. L. Journal of Synchrotron Radiation, Vol. 8, Issue 2 https://doi.org/10.1107/S0909049500016423	journal	March 2001
The Cambridge Structural Database Groom, Colin R.; Bruno, Ian J.; Lightfoot, Matthew P. Acta Crystallographica Section B Structural Science, Crystal Engineering and Materials, Vol. 72, Issue 2, p. 171-179 https://doi.org/10.1107/S2052520616003954	journal	April 2016
Regulation of Mitochondrial Iron Accumulation by Yfh1p, a Putative Homolog of Frataxin Babcock, M. Science, Vol. 276, Issue 5319 https://doi.org/10.1126/science.276.5319.1709	journal	June 1997
Zinc Toxicity and Iron-Sulfur Cluster Biogenesis in Escherichia coli Li, Jianghui; Ren, Xiaojun; Fan, Bingqian Applied and Environmental Microbiology, Vol. 85, Issue 9 https://doi.org/10.1128/AEM.01967-18	journal	March 2019
The Yeast Scaffold Proteins Isu1p and Isu2p Are Required inside Mitochondria for Maturation of Cytosolic Fe/S Proteins Gerber, J.; Neumann, K.; Prohl, C. Molecular and Cellular Biology, Vol. 24, Issue 11 https://doi.org/10.1128/MCB.24.11.4848-4857.2004	journal	May 2004
Turning Saccharomyces cerevisiae into a Frataxin-Independent Organism Yoon, Heeyong; Knight, Simon A. B.; Pandey, Alok PLOS Genetics, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pgen.1005135	journal	May 2015
Mammalian Frataxin: An Essential Function for Cellular Viability through an Interaction with a Preformed ISCU/NFS1/ISD11 Iron-Sulfur Assembly Complex Schmucker, Stéphane; Martelli, Alain; Colin, Florent PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016199	journal	January 2011
New Perspectives on Iron Uptake in Eukaryotes Sherman, Harry G.; Jovanovic, Carolyn; Stolnik, Snow Frontiers in Molecular Biosciences, Vol. 5 https://doi.org/10.3389/fmolb.2018.00097	journal	November 2018
The mitochondrial acyl carrier protein (ACP) coordinates mitochondrial fatty acid synthesis with iron sulfur cluster biogenesis Van Vranken, Jonathan G.; Jeong, Mi-Young; Wei, Peng eLife, Vol. 5 https://doi.org/10.7554/eLife.17828	journal	August 2016

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