Organizing protein-DNA hybrids as nanostructures with programmed functionalities.

The structural and functional information encoded in the base sequence of nucleic acids provides a means to organize hybrid protein-DNA nanostructures with pre-designed, programmed functionality. This review discusses the activation of enzyme cascades in supramolecular DNA-protein hybrid structures, the bioelectrocatalytic activation of redox enzymes on DNA scaffolds, and the programmed positioning of enzymes on 1D, 2D and 3D DNA nanostructures. These systems provide starting points towards the design of interconnected enzyme networks. Substantial progress in the tailoring of functional protein-DNA nanostructures has been accomplished in recent years, and advances in this field warrant a comprehensive discussion. The application of these systems for the control of biocatalytic transformations, for amplified biosensing, and for the synthesis of metallic nanostructures are addressed, and future prospects for these systems are highlighted.

[1]  N. Seeman,et al.  A robust DNA mechanical device controlled by hybridization topology , 2002, Nature.

[2]  P. Rothemund.  Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[3]  Itamar Willner,et al.  Increasing the complexity of periodic protein nanostructures by the rolling-circle-amplified synthesis of aptamers. , 2008, Angewandte Chemie.

[4]  Christof M Niemeyer,et al.  DNA‐Directed Assembly of Bienzymic Complexes from In Vivo Biotinylated NAD(P)H:FMN Oxidoreductase and Luciferase , 2002, Chembiochem : a European journal of chemical biology.

[5]  Itamar Willner,et al.  Supramolecular cocaine-aptamer complexes activate biocatalytic cascades. , 2009, Journal of the American Chemical Society.

[6]  G. Mayer.  The chemical biology of aptamers. , 2009, Angewandte Chemie.

[7]  N. Seeman.  From genes to machines: DNA nanomechanical devices. , 2005, Trends in biochemical sciences.

[8]  Harald Schwalbe,et al.  Metal-ion binding and metal-ion induced folding of the adenine-sensing riboswitch aptamer domain , 2007, Nucleic acids research.

[9]  M. Komiyama,et al.  Stepwise and reversible nanopatterning of proteins on a DNA origami scaffold. , 2010, Chemical communications.

[10]  Itamar Willner,et al.  Synthesis of Nanowires Using Dip‐Pen Nanolithography and Biocatalytic Inks , 2006 .

[11]  J. Reif,et al.  DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Itamar Willner,et al.  Nanoengineered electrically contacted enzymes on DNA scaffolds: functional assemblies for the selective analysis of Hg2+ ions. , 2010, Journal of the American Chemical Society.

[13]  Itamar Willner,et al.  DNAzymes for sensing, nanobiotechnology and logic gate applications. , 2008, Chemical Society reviews.

[14]  Shawn M. Douglas,et al.  Self-assembly of DNA into nanoscale three-dimensional shapes , 2009, Nature.

[15]  I. Willner,et al.  Growing Metal Nanoparticles by Enzymes , 2006 .

[16]  C. Niemeyer.  Semisynthetic DNA-protein conjugates for biosensing and nanofabrication. , 2010, Angewandte Chemie.

[17]  Itamar Willner,et al.  Electronic aptamer-based sensors. , 2007, Angewandte Chemie.

[18]  Yingfu Li,et al.  DNA-enhanced peroxidase activity of a DNA-aptamer-hemin complex. , 1998, Chemistry & biology.

[19]  M. Mascini,et al.  Different approaches for the detection of thrombin by an electrochemical aptamer-based assay coupled to magnetic beads. , 2008, Biosensors & bioelectronics.

[20]  J. Kjems,et al.  Self-assembly of a nanoscale DNA box with a controllable lid , 2009, Nature.

[21]  Itamar Willner,et al.  Biocatalytic growth of Au nanoparticles: from mechanistic aspects to biosensors design. , 2005, Nano letters.

[22]  Hao Yan,et al.  Spatially addressable multiprotein nanoarrays templated by aptamer-tagged DNA nanoarchitectures. , 2007, Journal of the American Chemical Society.

[23]  N. Seeman,et al.  Operation of a DNA Robot Arm Inserted into a 2D DNA Crystalline Substrate , 2006, Science.

[24]  A. Tepper.  Electrical contacting of an assembly of pseudoazurin and nitrite reductase using DNA-directed immobilization. , 2010, Journal of the American Chemical Society.

[25]  Hao Yan,et al.  Aptamer-directed self-assembly of protein arrays on a DNA nanostructure. , 2005, Angewandte Chemie.

[26]  G. Pavan,et al.  Optically degradable dendrons for temporary adhesion of proteins to DNA. , 2010, Chemistry.

[27]  C. Niemeyer,et al.  DNA-directed assembly of artificial multienzyme complexes. , 2008, Biochemical and biophysical research communications.

[28]  Hao Yan,et al.  Self-assembled DNA nanostructures for distance-dependent multivalent ligand-protein binding. , 2008, Nature nanotechnology.

[29]  Itamar Willner,et al.  Proteins modified with DNAzymes or aptamers act as biosensors or biosensor labels. , 2007, Biosensors & bioelectronics.

[30]  Itamar Willner,et al.  Enzyme cascades activated on topologically programmed DNA scaffolds. , 2009, Nature nanotechnology.

[31]  Yi Lu,et al.  A colorimetric lead biosensor using DNAzyme-directed assembly of gold nanoparticles. , 2003, Journal of the American Chemical Society.

[32]  I. Willner,et al.  Control of biocatalytic transformations by programmed DNA assemblies. , 2010, Chemistry.

[33]  Shawn M. Douglas,et al.  Folding DNA into Twisted and Curved Nanoscale Shapes , 2009, Science.

[34]  Itamar Willner,et al.  Lighting Up Biochemiluminescence by the Surface Self‐Assembly of DNA–Hemin Complexes , 2004, Chembiochem : a European journal of chemical biology.

[35]  R. Levine,et al.  DNA computing circuits using libraries of DNAzyme subunits. , 2010, Nature nanotechnology.

[36]  C. Niemeyer,et al.  Kinetic analysis of semisynthetic peroxidase enzymes containing a covalent DNA-heme adduct as the cofactor. , 2006, Chemistry.

[37]  E. Torres,et al.  Apoenzyme reconstitution as a chemical tool for structural enzymology and biotechnology. , 2009, Angewandte Chemie.

[38]  Takashi Fujimoto,et al.  MercuryII-mediated formation of thymine-HgII-thymine base pairs in DNA duplexes. , 2006, Journal of the American Chemical Society.

[39]  I. Hamachi,et al.  Construction of Artificial Photosynthetic Reaction Centers on a Protein Surface : Vectorial, Multistep, and Proton-Coupled Electron Transfer for Long-Lived Charge Separation , 2000 .

[40]  Juewen Liu,et al.  Functional nucleic acid sensors. , 2009, Chemical reviews.

[41]  I. Willner,et al.  Control of bioelectrocatalytic transformations on DNA scaffolds. , 2009, Journal of the American Chemical Society.

[42]  I. Willner,et al.  Self-assembly of enzymes on DNA scaffolds: en route to biocatalytic cascades and the synthesis of metallic nanowires. , 2009, Nano letters.

[43]  Friedrich C. Simmel,et al.  Structural DNA Nanotechnology: From Bases to Bricks, From Structure to Function , 2010 .

[44]  S. Katz,et al.  The reversible reaction of Hg (II) and double-stranded polynucleotides. A step-function theory and its significance. , 1963, Biochimica et biophysica acta.

[45]  Eugenii Katz,et al.  Improving enzyme–electrode contacts by redox modification of cofactors , 1995, Nature.

[46]  M. Mascini,et al.  Aptamers as molecular tools for bioanalytical methods. , 2009, Current opinion in molecular therapeutics.

[47]  Milan N Stojanovic,et al.  Fluorescent Sensors Based on Aptamer Self-Assembly. , 2000, Journal of the American Chemical Society.

[48]  A. Klibanov,et al.  Specificity of a DNA-based (DNAzyme) peroxidative biocatalyst , 2007, Biotechnology Letters.

[49]  Z. Ezziane.  DNA computing: applications and challenges , 2006 .

[50]  Itamar Willner,et al.  Fluorescence detection of DNA by the catalytic activation of an aptamer/thrombin complex. , 2005, Journal of the American Chemical Society.

[51]  R. Breaker,et al.  Cooperative binding of effectors by an allosteric ribozyme. , 2001, Nucleic acids research.

[52]  J. Reif,et al.  Construction, analysis, ligation, and self-assembly of DNA triple crossover complexes , 2000 .

[53]  A. Phan,et al.  Human telomeric DNA: G-quadruplex, i-motif and Watson-Crick double helix. , 2002, Nucleic acids research.

[54]  Itamar Willner,et al.  A polycatenated DNA scaffold for the one-step assembly of hierarchical nanostructures , 2008, Proceedings of the National Academy of Sciences.

[55]  Itamar Willner,et al.  Electrochemical, photoelectrochemical, and surface plasmon resonance detection of cocaine using supramolecular aptamer complexes and metallic or semiconductor nanoparticles. , 2009, Analytical chemistry.

[56]  Faisal A. Aldaye,et al.  Assembling Materials with DNA as the Guide , 2008, Science.