Interfacial metal coordination in engineered protein and peptide assemblies.

Metal ions are frequently found in natural protein-protein interfaces, where they stabilize quaternary or supramolecular protein structures, mediate transient protein-protein interactions, and serve as catalytic centers. Paralleling these natural roles, coordination chemistry of metal ions is being increasingly utilized in creative ways toward engineering and controlling the assembly of functional supramolecular peptide and protein architectures. Here we provide a brief overview of this emerging branch of metalloprotein/peptide engineering and highlight a few select examples from the recent literature that best capture the diversity and future potential of approaches that are being developed.

[1]  Brian Kuhlman,et al.  Catalysis by a de novo zinc-mediated protein interface: implications for natural enzyme evolution and rational enzyme engineering. , 2012, Biochemistry.

[2]  R. J. Williams,et al.  Order of Stability of Metal Complexes , 1948, Nature.

[3]  Tanja Kortemme,et al.  Computer-aided design of functional protein interactions. , 2009, Nature chemical biology.

[4]  Bryan S. Der,et al.  Metal-mediated affinity and orientation specificity in a computationally designed protein homodimer. , 2012, Journal of the American Chemical Society.

[5]  R. Radford Expanding the Utility of Proteins as Platforms for Coordination Chemistry , 2011 .

[6]  V. Conticello,et al.  Design of a selective metal ion switch for self-assembly of peptide-based fibrils. , 2008, Journal of the American Chemical Society.

[7]  X. Ambroggio,et al.  Evolution of metal selectivity in templated protein interfaces. , 2010, Journal of the American Chemical Society.

[8]  Richard A. Lewis,et al.  Control of protein oligomerization symmetry by metal coordination: C2 and C3 symmetrical assemblies through Cu(II) and Ni(II) coordination. , 2009, Inorganic chemistry.

[9]  L. Makowski,et al.  Three-dimensional structure of a cloning vector. X-ray diffraction studies of filamentous bacteriophage M13 at 7 A resolution. , 1992, Journal of molecular biology.

[10]  Sabina Burazerovic,et al.  Hierarchical self-assembly of one-dimensional streptavidin bundles as a collagen mimetic for the biomineralization of calcite. , 2007, Angewandte Chemie.

[11]  Jennifer E. Padilla,et al.  Designing supramolecular protein assemblies. , 2002, Current opinion in structural biology.

[12]  Kristin N. Parent,et al.  Metal-directed, chemically-tunable assembly of one-, two- and three-dimensional crystalline protein arrays , 2012, Nature chemistry.

[13]  Hidekazu Hiroaki,et al.  Two-Metal Ion, Ni(II) and Cu(II), Binding α-Helical Coiled Coil Peptide , 2004 .

[14]  C. M. Summa,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Retrostructural analysis of metalloproteins: Application to the design of a minimal model for diiron proteins , 2000 .

[15]  F. Tezcan,et al.  Modular and versatile hybrid coordination motifs on alpha-helical protein surfaces. , 2010, Inorganic chemistry.

[16]  L. Serrano,et al.  Strategies for protein synthetic biology , 2010, Nucleic acids research.

[17]  Brian Kuhlman,et al.  Metal templated design of protein interfaces , 2009, Proceedings of the National Academy of Sciences.

[18]  A. Mehta,et al.  Engineering metal ion coordination to regulate amyloid fibril assembly and toxicity , 2007, Proceedings of the National Academy of Sciences.

[19]  D. Tierney,et al.  Nanometer to millimeter scale peptide-porphyrin materials. , 2010, Biomacromolecules.

[20]  Marya Lieberman,et al.  IRON(II) ORGANIZES A SYNTHETIC PEPTIDE INTO THREE-HELIX BUNDLES , 1991 .

[21]  M. Fujita,et al.  Functional molecular flasks: new properties and reactions within discrete, self-assembled hosts. , 2009, Angewandte Chemie.

[22]  Joshua S. Figueroa,et al.  Controlled protein dimerization through hybrid coordination motifs. , 2010, Inorganic chemistry.

[23]  D. Pochan,et al.  Zinc-triggered hydrogelation of a self-assembling β-hairpin peptide. , 2011, Angewandte Chemie.

[24]  Jeanne A. Stuckey,et al.  Hydrolytic catalysis and structural stabilization in a designed metalloprotein , 2011, Nature chemistry.

[25]  R. A. Scott,et al.  Modulating amyloid self-assembly and fibril morphology with Zn(II). , 2006, Journal of the American Chemical Society.

[26]  Aimee L. Boyle,et al.  A basis set of de novo coiled-coil peptide oligomers for rational protein design and synthetic biology. , 2012, ACS synthetic biology.

[27]  J. Brodin,et al.  In vitro and cellular self-assembly of a Zn-binding protein cryptand via templated disulfide bonds. , 2013, Journal of the American Chemical Society.

[28]  T M Handel,et al.  Metal ion-dependent modulation of the dynamics of a designed protein. , 1993, Science.

[29]  F. Tezcan,et al.  Controlling protein-protein interactions through metal coordination: assembly of a 16-helix bundle protein. , 2007, Journal of the American Chemical Society.

[30]  Tillmann Heinisch,et al.  Design strategies for the creation of artificial metalloenzymes. , 2010, Current opinion in chemical biology.

[31]  T. Yeates,et al.  An approach to crystallizing proteins by metal‐mediated synthetic symmetrization , 2011, Protein science : a publication of the Protein Society.

[32]  M. Ghadiri,et al.  Secondary structure nucleation in peptides. Transition metal ion stabilized .alpha.-helices , 1990 .

[33]  F. Tezcan,et al.  Metal-directed protein self-assembly. , 2010, Accounts of chemical research.

[34]  D. Funeriu,et al.  Protein-inorganic array construction: design and synthesis of the building blocks. , 2010, Chemistry.

[35]  G. Erker,et al.  Control of the coordination structure of organometallic palladium complexes in an apo-ferritin cage. , 2008, Journal of the American Chemical Society.

[36]  M. Kennedy,et al.  Metal-binding properties and structural characterization of a self-assembled coiled coil: formation of a polynuclear Cd-thiolate cluster. , 2013, Journal of inorganic biochemistry.

[37]  T. Ueno,et al.  Expanding coordination chemistry from protein to protein assembly. , 2013, Chemical communications.

[38]  Hongbin Li,et al.  Highly ordered protein nanorings designed by accurate control of glutathione S-transferase self-assembly. , 2013, Journal of the American Chemical Society.

[39]  Charles M. Rubert Pérez,et al.  Metal-mediated tandem coassembly of collagen peptides into banded microstructures. , 2011, Journal of the American Chemical Society.

[40]  D. Pochan,et al.  Heavy metal ion hydrogelation of a self-assembling peptideviacysteinyl chelation , 2012 .

[41]  G. Ghirlanda,et al.  De novo design of an artificial bis[4Fe-4S] binding protein. , 2013, Biochemistry.

[42]  N. J. Christensen,et al.  Controlled self-assembly of re-engineered insulin by Fe(II). , 2011, Chemistry.

[43]  F. Tezcan,et al.  Structural characterization of a microperoxidase inside a metal-directed protein cage. , 2010, Angewandte Chemie.

[44]  O. Kharenko,et al.  Cu(I) luminescence from the tetranuclear Cu4S4 cofactor of a synthetic 4-helix bundle. , 2005, Journal of the American Chemical Society.

[45]  Ashley I. Bush,et al.  The metallobiology of Alzheimer's disease , 2003, Trends in Neurosciences.

[46]  J. Horng,et al.  Promoting self-assembly of collagen-related peptides into various higher-order structures by metal-histidine coordination. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[47]  F. Rabanal,et al.  Ferredoxin and ferredoxin-heme maquettes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Solomon,et al.  Preface: biomimetic inorganic chemistry. , 2004, Chemical reviews.

[49]  Borries Demeler,et al.  Controlling self-assembly of a peptide-based material via metal-ion induced registry shift. , 2013, Journal of the American Chemical Society.

[50]  Christopher C. Moser,et al.  Design and engineering of an O(2) transport protein , 2009, Nature.

[51]  K. Hirata,et al.  Polymerization of phenylacetylene by rhodium complexes within a discrete space of apo-ferritin. , 2009, Journal of the American Chemical Society.

[52]  Fangting Yu,et al.  Designing a functional type 2 copper center that has nitrite reductase activity within α-helical coiled coils , 2012, Proceedings of the National Academy of Sciences.

[53]  Richard A. Lewis,et al.  Metal-mediated self-assembly of protein superstructures: influence of secondary interactions on protein oligomerization and aggregation. , 2008, Journal of the American Chemical Society.

[54]  Chad A. Mirkin,et al.  Strategies for the Construction of Supramolecular Compounds through Coordination Chemistry. , 2001, Angewandte Chemie.

[55]  Ehud Gazit,et al.  Plenty of Room for Biology at the Bottom: An Introduction to Bionanotechnology , 2007 .

[56]  P. Harbury,et al.  Automated design of specificity in molecular recognition , 2003, Nature Structural Biology.

[57]  Alessandro Senes,et al.  De novo design and molecular assembly of a transmembrane diporphyrin-binding protein complex. , 2010, Journal of the American Chemical Society.

[58]  Yi Lu,et al.  Design of functional metalloproteins , 2009, Nature.

[59]  M. Zastrow,et al.  Designing functional metalloproteins: from structural to catalytic metal sites. , 2013, Coordination chemistry reviews.

[60]  William V Nicholson,et al.  Microtubule structure at 8 A resolution. , 2002, Structure.

[61]  A. Schepartz,et al.  Altered specificity of DNA-binding proteins with transition metal dimerization domains. , 1993, Science.

[62]  Charles M. Rubert Pérez,et al.  Hierarchical assembly of collagen peptide triple helices into curved disks and metal ion-promoted hollow spheres. , 2013, Journal of the American Chemical Society.

[63]  F. Tezcan,et al.  Re-engineering protein interfaces yields copper-inducible ferritin cage assembly. , 2013, Nature chemical biology.

[64]  U. Sleytr,et al.  S-Layer Proteins , 2000, Journal of bacteriology.

[65]  C. L. Oliveira,et al.  Protein cage nanoparticles as secondary building units for the synthesis of 3-dimensional coordination polymers , 2010 .

[66]  F. Ismail-Beigi,et al.  Supramolecular Protein Engineering , 2010, The Journal of Biological Chemistry.