Metals in Cells

Editors Valeria Culotta, Johns Hopkins University, Baltimore, MD, USA Robert A. Scott, University of Georgia, Athens, GA, USA The last half–century has seen an explosive growth in our understanding of the role of inorganic elements in biology, focusing first on biochemical function of proteins with tightly bound metals. As a result, many structures and functions of biomolecules with metals have been characterized. In parallel, the understanding of inorganic elements in medicinal chemistry and the development of metal–containing drugs has developed. This research led inevitably to an interest in how Nature incorporates inorganic elements into metalloproteins and how cells “manage” their “inorganic portfolio,” acquiring the right amount of each element in the right location without making mistakes, while avoiding toxicity. More recent research efforts have focused on this understanding of inorganic cell biology. Significant advances have been prompted by a combination of new methods to probe intracellular metal locations and the dynamics of metal movement in cells, high–resolution detection of metal–biomolecule interactions, and the revolution of genomic, proteomic, metabolic, and even “metallomic” approaches to the study of inorganic physiology. Environmental metals and metalloids, including iron, copper, zinc, cobalt, manganese, molybdenum, and selenium, are all accumulated by cells and organisms in the micro– to millimolar range. Yet despite this abundant sea of diverse metals, only the correct metal cofactor is matched with a partner metalloprotein – mistakes in metal ion biology rarely occur. At the same time, free metal ions can be detrimental to cellular components and processes, so systems have evolved to carefully control trace element concentrations and locations (homeostasis). This book covers recent advances made by top researchers in the field of metals in cells [the “metallome”] and includes: regulated metal ion uptake and trafficking, sensing of metals within cells and across tissues, and identification of the vast cellular factors designed to orchestrate assembly of metal cofactor sites while minimizing toxic side reactions of metals. In addition, it features aspects of metals in disease, including the role of metals in neurodegeneration, liver disease, and inflammation, as a way to highlight the detrimental effects of mishandling of metal trafficking and response to “foreign” metals. This book is an important addition to the bioinorganic literature and relates new discoveries in systems biology and toxicology to new results in bioinorganic chemistry. About EIBC Books The Encyclopedia of Inorganic and Bioinorganic Chemistry (EIBC) was created as an online reference in 2012 by merging the Encyclopedia of Inorganic Chemistry and the Handbook of Metalloproteins. The resulting combination proves to be the defining reference work in the field of inorganic and bioinorganic chemistry, and a lot of chemistry libraries around the world have access to the online version. Many readers, however, prefer to have more concise thematic volumes in print, targeted to their specific area of interest. This feedback from EIBC readers has encouraged the Editors to plan a series of EIBC Books [formerly called EIC Books], focusing on topics of current interest. EIBC Books will appear on a regular basis, will be edited by the EIBC Editors and specialist Guest Editors, and will feature articles from leading scholars in their fields. EIBC Books aim to provide both the starting research student and the confirmed research worker with a critical distillation of the leading concepts in inorganic and bioinorganic chemistry, and provide a structured entry into the fields covered.

Contributors xi Series Preface xix Volume Preface xxi PART 1: INTRODUCTION 1 Mechanisms Controlling the Cellular Metal Economy 3 Benjamin A. Gilston and Thomas V. O’Halloran PART 2: PROBING METALS AND CROSS TALK IN THE METALLOME 15 The Metallome 17 Vadim N. Gladyshev and Yan Zhang Cyanobacterial Models that Address Cross–Talk in Metal Homeostasis 39 Carl J. Patterson, Rafael Pernil, Andrew W. Foster and Nigel J. Robinson Sparing and Salvaging Metals in Chloroplasts 51 Crysten E. Blaby–Haas and Sabeeha S. Merchant Fluorescent Probes for Monovalent Copper 65 M. Thomas Morgan, Pritha Bagchi and Christoph J. Fahrni Fluorescent Zinc Sensors 85 Amy E. Palmer, Jose G. Miranda and Kyle P. Carter X–Ray Fluorescence Microscopy 99 James E. Penner–Hahn PART 3: MOVING METALS IN CELLS 111 Iron and Heme Transport and Trafficking 113 Yvette Y. Yien and Barry H. Paw Iron in Plants 131 Jessica B. Weng and Mary Lou Guerinot Transport of Nickel and Cobalt in Prokaryotes 145 Thomas Eitinger Transport Mechanism and Cellular Functions of Bacterial Cu(I)–ATPases 155 Jose M. Arguello, Teresita Padilla–Benavides and Jessica M. Collins Copper Transport in Fungi 163 Simon Labbe, Jude Beaudoin and Raphael Ioannoni Structural Biology of Copper Transport 175 Adrian G. Flores, Christopher R. Pope and Vinzenz M. Unger Zinc Transporters and Trafficking in Yeast 183 Yi–Hsuan Wu and David J. Eide Cadmium Transport in Eukaryotes 195 Nathan Smith, Wenzhong Wei and Jaekwon Lee PART 4: METALS IN REGULATION 207 Metal Specificity of Metallosensors 209 Khadine A. Higgins and David P. Giedroc Metal Homeostasis and Oxidative Stress in Bacillus subtilis 225 Zhen Ma and John D. Helmann Regulation of Manganese and Iron Homeostasis in the Rhizobia and Related α–Proteobacteria 237 Mark R. O’Brian The Iron Starvation Response in Saccharomyces cerevisiae 249 Caroline C. Philpott and Pamela M. Smith Hepcidin Regulation of Iron Homeostasis 265 Clara Camaschella and Laura Silvestri NikR: Mechanism and Function in Nickel Homeostasis 277 Michael D. Jones, Andrew M. Sydor and Deborah B. Zamble Regulation of Copper Homeostasis in Plants 289 Marinus Pilon and Wiebke Tapken Regulation of Zinc Transport 301 Taiho Kambe Selenoproteins—Regulation 311 Lucia A. Seale and Marla J. Berry PART 5: METALS IN CELLULAR DAMAGE AND DISEASE 321 Metals in Bacterial Pathogenicity and Immunity 323 Jennifer S. Cavet Manganese in Neurodegeneration 335 Daiana Silva Avila, Robson Luiz Puntel, Felix Antunes Soares, Joao Batista Teixeira da Rocha and Michael Aschner Iron Sequestration in Immunity 349 Colin Correnti and Roland K. Strong Molecular Basis of Hemochromatosis 361 Paul J. Schmidt Copper in Brain and Neurodegeneration 373 Jeffrey R. Liddell, Ashley I. Bush and Anthony R. White Copper Transporting ATPases in Mammalian Cells 395 Nan Yang and Svetlana Lutsenko Copper in Immune Cells 409 Karrera Y. Djoko, Maud E.S. Achard and Alastair G. McEwan Selenoenzymes and Selenium Trafficking: An Emerging Target for Therapeutics 421 William Self and Sarah Rosario Resistance Pathways for Metalloids and Toxic Metals 429 Zijuan Liu, Christopher Rensing and Barry P. Rosen PART 6: COFACTOR ASSEMBLY 443 Fe–S Cluster Biogenesis in Archaea and Bacteria 445 Harsimranjit K. Chahal, Jeff M. Boyd and F. Wayne Outten Mitochondrial Iron Metabolism and the Synthesis of Iron–Sulfur Clusters 473 Andrew Dancis and Paul A. Lindahl [FeFe]–Hydrogenase Cofactor Assembly 491 Eric M. Shepard, Amanda S. Byer, Eric S. Boyd, Kevin D. Swanson, John W. Peters and Joan B. Broderick [NiFe]–Hydrogenase Cofactor Assembly 507 Basem Soboh and R. Gary Sawers Copper in Mitochondria 517 Katherine E. Vest and Paul A. Cobine Mo Cofactor Biosynthesis and Crosstalk with FeS 529 Florian Bittner and Ralf R. Mendel Nitrogenase Cofactor Assembly 543 Jared A. Wiig, Chi Chung Lee, Markus W. Ribbe and Yilin Hu Index 555