Coordination Chemistry in Protein Cages

TAKAFUMI UENO is Professor in the School and Graduate School of Bioscience and Biotechnology at Tokyo Institute of Technology. His current research interests involve the molecular design of artificial metalloproteins and exploitation of meso-scale materials with the coordination chemistry of protein assemblies. He was awarded the Young Investigator Award of the Japan Society of Coordination Chemistry in 2007 and the Young Scientists' Prize of the Commendation for Science and Technology by the Minister of Education, Culture, Sports, Science and Technology, Japan, in 2008.YOSHIHITO WATANABE is Professor in the Department of Chemistry at Nagoya University. Since 2009, he has been appointed a Vice President of Research and International Affairs. His current research interests include the design of hydrogen peroxide-dependent monooxygenase and construction of metalloenzymes with synthetic complexes at their catalytic centers. He is a recipient of the Chemical Society of Japan Award for Creative Work in 1999, and the Japan Society of Coordination Chemistry in 2011. He sits on two editorial boards and an international advisory board.

• Foreword xiiiPreface xvContributors xviiPART I COORDINATION CHEMISTRY IN NATIVE PROTEIN CAGES1 The Chemistry of Nature’s Iron Biominerals in Ferritin Protein Nanocages 3Elizabeth C. Theil and Rabindra K. Behera1.1 Introduction 31.2 Ferritin Ion Channels and Ion Entry 61.2.1 Maxi- and Mini-Ferritin 61.2.2 Iron Entry 71.3 Ferritin Catalysis 81.3.1 Spectroscopic Characterization of -1,2 Peroxodiferric Intermediate (DFP) 81.3.2 Kinetics of DFP Formation and Decay 121.4 Protein-Based Ferritin Mineral Nucleation and Mineral Growth 131.5 Iron Exit 161.6 Synthetic Uses of Ferritin Protein Nanocages 171.6.1 Nanomaterials Synthesized in Ferritins 181.6.2 Ferritin Protein Cages in Metalloorganic Catalysis and Nanoelectronics 191.6.3 Imaging and Drug Delivery Agents Produced in Ferritins 191.7 Summary and Perspectives 20Acknowledgments 20References 212 Molecular Metal Oxides in Protein Cages/Cavities 25Achim M¨uller and Dieter Rehder2.1 Introduction 252.2 Vanadium: Functional Oligovanadates and Storage of VO2+ in Vanabins 262.3 Molybdenum and Tungsten: Nucleation Process in a Protein Cavity 282.4 Manganese in Photosystem II 332.5 Iron: Ferritins, DPS Proteins, Frataxins, and Magnetite 352.6 Some General Remarks: Oxides and Sulfides 38References 38PART II DESIGN OF METALLOPROTEIN CAGES3 De Novo Design of Protein Cages to Accommodate Metal Cofactors 45Flavia Nastri, Rosa Bruni, Ornella Maglio, and Angela Lombardi3.1 Introduction 453.2 De Novo-Designed Protein Cages Housing Mononuclear Metal Cofactors 473.3 De Novo-Designed Protein Cages Housing Dinuclear Metal Cofactors 593.4 De Novo-Designed Protein Cages Housing Heme Cofactor 663.5 Summary and Perspectives 79Acknowledgments 79References 804 Generation of Functionalized Biomolecules Using Hemoprotein Matrices with Small Protein Cavities for Incorporation of Cofactors 87Takashi Hayashi4.1 Introduction 874.2 Hemoprotein Reconstitution with an Artificial Metal Complex 894.3 Modulation of the O2 Affinity of Myoglobin 904.4 Conversion of Myoglobin into Peroxidase 954.4.1 Construction of a Substrate-Binding Site Near the Heme Pocket 954.4.2 Replacement of Native Heme with Iron Porphyrinoid in Myoglobin 994.4.3 Other Systems Used in Enhancement of Peroxidase Activity of Myoglobin 1004.5 Modulation of Peroxidase Activity of HRP 1024.6 Myoglobin Reconstituted with a Schiff Base Metal Complex 1034.7 A Reductase Model Using Reconstituted Myoglobin 1064.7.1 Hydrogenation Catalyzed by Cobalt Myoglobin 1064.7.2 A Model of Hydrogenase Using the Heme Pocket of Cytochrome c 1074.8 Summary and Perspectives 108Acknowledgments 108References 1085 Rational Design of Protein Cages for Alternative Enzymatic Functions 111Nicholas M. Marshall, Kyle D. Miner, Tiffany D. Wilson, and Yi Lu5.1 Introduction 1115.2 Mononuclear Electron Transfer Cupredoxin Proteins 1125.3 CuA Proteins 1165.4 Catalytic Copper Proteins 1185.4.1 Type 2 Red Copper Sites 1185.4.2 Other T2 Copper Sites 1205.4.3 Cu, Zn Superoxide Dismutase 1215.4.4 Multicopper Oxygenases and Oxidases 1225.5 Heme-Based Enzymes 1245.5.1 Mb-Based Peroxidase and P450 Mimics 1245.5.2 Mimicking Oxidases in Mb 1255.5.3 Mimicking NOR Enzymes in Mb 1275.5.4 Engineering Peroxidase Proteins 1285.5.5 Engineering Cytochrome P450s 1295.6 Non-Heme ET Proteins 1315.7 Fe and Mn Superoxide Dismutase 1325.8 Non-Heme Fe Catalysts 1335.9 Zinc Proteins 1345.10 Other Metalloproteins 1355.10.1 Cobalt Proteins 1355.10.2 Manganese Proteins 1365.10.3 Molybdenum Proteins 1375.10.4 Nickel Proteins 1375.10.5 Uranyl Proteins 1385.10.6 Vanadium Proteins 1385.11 Summary and Perspectives 139References 142PART III COORDINATION CHEMISTRY OF PROTEIN ASSEMBLY CAGES6 Metal-Directed and Templated Assembly of Protein Superstructures and Cages 151F. Akif Tezcan6.1 Introduction 1516.2 Metal-Directed Protein Self-Assembly 1526.2.1 Background 1526.2.2 Design Considerations for Metal-Directed Protein Self-Assembly 1536.2.3 Interfacing Non-Natural Chelates with MDPSA 1556.2.4 Crystallographic Applications of Metal-Directed Protein Self-Assembly 1596.3 Metal-Templated Interface Redesign 1626.3.1 Background 1626.3.2 Construction of a Zn-Selective Tetrameric Protein Complex Through MeTIR 1636.3.3 Construction of a Zn-Selective Protein Dimerization Motif Through MeTIR 1666.4 Summary and Perspectives 170Acknowledgments 171References 1717 Catalytic Reactions Promoted in Protein Assembly Cages 175Takafumi Ueno and Satoshi Abe7.1 Introduction 1757.1.1 Incorporation of Metal Compounds 1767.1.2 Insight into Accumulation Process ofMetal Compounds 1777.2 Ferritin as a Platform for Coordination Chemistry 1777.3 Catalytic Reactions in Ferritin 1797.3.1 Olefin Hydrogenation 1797.3.2 Suzuki–Miyaura Coupling Reaction in Protein Cages 1827.3.3 Polymer Synthesis in Protein Cages 1857.4 Coordination Processes in Ferritin 1887.4.1 Accumulation of Metal Ions 1887.4.2 Accumulation of Metal Complexes 1927.5 Coordination Arrangements in Designed Ferritin Cages 1947.6 Summary and Perspectives 197Acknowledgments 198References 1988 Metal-Catalyzed Organic Transformations Inside a Protein Scaffold Using Artificial Metalloenzymes 203V. K. K. Praneeth and Thomas R. Ward8.1 Introduction 2038.2 Enantioselective Reduction Reactions Catalyzed by Artificial Metalloenzymes 2048.2.1 Asymmetric Hydrogenation 2048.2.2 Asymmetric Transfer Hydrogenation of Ketones 2068.2.3 Artificial Transfer Hydrogenation of Cyclic Imines 2088.3 Palladium-Catalyzed Allylic Alkylation 2118.4 Oxidation Reaction Catalyzed by Artificial Metalloenzymes 2128.4.1 Artificial Sulfoxidase 2128.4.2 Asymmetric cis-Dihydroxylation 2158.5 Summary and Perspectives 216References 218PART IV APPLICATIONS IN BIOLOGY9 Selective Labeling and Imaging of Protein Using Metal Complex 223Yasutaka Kurishita and Itaru Hamachi9.1 Introduction 2239.2 Tag–Probe Pair Method Using Metal-Chelation System 2259.2.1 Tetracysteine Motif/Arsenical Compounds Pair 2259.2.2 Oligo-Histidine Tag/Ni(ii)-NTA Pair 2279.2.3 Oligo-Aspartate Tag/Zn(ii)-DpaTyr Pair 2309.2.4 Lanthanide-binding Tag 2359.3 Summary and Perspectives 237References 23710 Molecular Bioengineering of Magnetosomes for Biotechnological Applications 241Atsushi Arakaki, Michiko Nemoto, and Tadashi Matsunaga10.1 Introduction 24110.2 Magnetite Biomineralization Mechanism in Magnetosome 24210.2.1 Diversity of Magnetotactic Bacteria 24210.2.2 Genome and Proteome Analyses of Magnetotactic Bacteria 24410.2.3 Magnetosome Formation Mechanism 24610.2.4 Morphological Control of Magnetite Crystal in Magnetosomes 25010.3 Functional Design of Magnetosomes 25110.3.1 Protein Display on Magnetosome by Gene Fusion Technique 25210.3.2 Magnetosome Surface Modification by In Vitro System 25510.3.3 Protein-mediated Morphological Control of Magnetite Particles 25710.4 Application 25810.4.1 Enzymatic Bioassays 25910.4.2 Cell Separation 26010.4.3 DNA Extraction 26210.4.4 Bioremediation 26410.5 Summary and Perspectives 266Acknowledgments 266References 266PART V APPLICATIONS IN NANOTECHNOLOGY11 Protein Cage Nanoparticles for Hybrid Inorganic–Organic Materials 275Shefah Qazi, Janice Lucon, Masaki Uchida, and Trevor Douglas11.1 Introduction 27511.2 Biomineral Formation in Protein Cage Architectures 27711.2.1 Introduction 27711.2.2 Mineralization 27811.2.3 Model for Synthetic Nucleation-Driven Mineralization 27911.2.4 Mineralization in Dps: A 12-Subunit Protein Cage 27911.2.5 Icosahedral Protein Cages: Viruses 28211.2.6 Nucleation of Inorganic Nanoparticles Within Icosahedral Viruses 28211.3 Polymer Formation Inside Protein Cage Nanoparticles 28311.3.1 Introduction 28311.3.2 Azide–Alkyne Click Chemistry in sHsp and P22 28511.3.3 Atom Transfer Radical Polymerization in P22 28711.3.4 Application as Magnetic Resonance Imaging Contrast Agents 29011.4 Coordination Polymers in Protein Cages 29211.4.1 Introduction 29211.4.2 Metal–Organic Branched Polymer Synthesis by Preforming Complexes 29211.4.3 Coordination Polymer Formation from Ditopic Ligands and Metal Ions 29511.4.4 Altering Protein Dynamics by Coordination: Hsp-Phen-Fe 29611.5 Summary and Perspectives 298Acknowledgments 298References 29812 Nanoparticles Synthesized and Delivered by Protein in the Field of Nanotechnology Applications 305Ichiro Yamashita, Kenji Iwahori, Bin Zheng, and Shinya Kumagai12.1 Nanoparticle Synthesis in a Bio-Template 30512.1.1 NP Synthesis by Cage-Shaped Proteins for Nanoelectronic Devices and Other Applications 30512.1.2 Metal Oxide or Hydro-Oxide NP Synthesis in the Apoferritin Cavity 30712.1.3 Compound Semiconductor NP Synthesis in the Apoferritin Cavity 30812.1.4 NP Synthesis in the Apoferritin with the Metal-Binding Peptides 31112.2 Site-Directed Placement of NPs 31212.2.1 Nanopositioning of Cage-Shaped Proteins 31212.2.2 Nanopositioning of Au NPs by Porter Proteins 31312.3 Fabrication of Nanodevices by the NP and Protein Conjugates 31712.3.1 Fabrication of Floating Nanodot Gate Memory 31812.3.2 Fabrication of Single-Electron Transistor Using Ferritin 321References 32613 Engineered “Cages” for Design of Nanostructured Inorganic Materials 329Patrick B. Dennis, Joseph M. Slocik, and Rajesh R. Naik13.1 Introduction 32913.2 Metal-Binding Peptides 33113.3 Discrete Protein Cages 33213.4 Heat-Shock Proteins 33413.5 Polymeric Protein and Carbohydrate Quasi-Cages 34013.6 Summary and Perspectives 346References 347PART VI COORDINATION CHEMISTRY INSPIRED BY PROTEIN CAGES14 Metal–Organic Caged Assemblies 353Sota Sato and Makoto Fujita14.1 Introduction 35314.2 Construction of Polyhedral Skeletons by Coordination Bonds 35514.2.1 Geometrical Effect on Products 35614.2.2 Structural Extension Based on Rigid, Designable Framework 35814.2.3 Mechanistic Insight into Self-Assembly 36614.3 Development of Functions via Chemical Modification 36614.3.1 Chemistry in the Hollow of Cages 36714.3.2 Chemistry on the Periphery of Cages 36814.4 Metal–Organic Cages for Protein Encapsulation 37014.5 Summary and Perspectives 370References 371Index 375