Summary
Super-hydrophobicity is a well-known and studied phenomenon in the field of surface sciences. In this review we report a novel approach that exploits micro-fabricated super-hydrophobic surfaces for the oriented and self-organized deposition and suspension of DNA filaments and other macromolecules of biological interest. The self-assembled structures obtained with this approach can be used for the characterization of the biological compounds with several methods such as electron microscopy, X-ray diffraction, Raman and SERS spectroscopies. Besides imaging, the described method has been applied in several fields such as the sensing of few molecules in diluted solutions and innovative templating growth. We will focus in particular on the direct imaging of DNA molecules by Transmission Electron Microscopy with the capability to resolve structural details of the double helix down to a resolution of 1.5 Å. The review starts with a brief historical note on the discovery of the DNA structure and continues with the results obtained by our group along the last 10 years of activity.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Levene P. A. and Jacobs W. A., “Uber die Hefe-Nucleinsaure”, Eur. J. Inorg. Chem., 42 (1909) 2474.
Levene B. Y. P. A. and S L., “Guaninedesoxypentoside from thymus nucleic acid.”, J. Biol. Chem., 81 (1929) 711.
Avery O. T., McLeod C. and Mccarty M. D., “Studies on the chemical nature of the substance inducing transformation of pneumococcal types”, J. Exp. Med., 79 (1944) 137, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2135445&tool=pmcentrez&rendertype=abstract.
Chargaff E., “Chemical specificity of nucleic acids and mechanism of their enzymatic degradation”, Experientia, 6 (1950) 201, http://www.ncbi.nlm.nih.gov/pubmed/8174683.
Wilkins M. H. F., Stokes A. R. and Wilson H. R., “Molecular structure of deoxypentose nucleic acids”, Nature, 171 (1953) 738.
Franklin R. E. and Gosling R. G., “Molecular configuration in sodium thymonucleate”, Nature, 171 (1953) 740.
Franklin R. E. and Gosling R. G., “Evidence for 2-chain helix in crystalline structure of sodium deoxyribonucleate”, Nature, 172 (1953) 156.
Franklin R. E. and Gosling R. G., “The structure of sodium thymonucleate fibres. I. The influence of water content”, Acta Crystallogr., 6 (1953) 673.
Pauling L., Corey R. B. and Branson H. R., “The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain”, Proc. Natl. Acad. Sci. U.S.A., 37 (1951) 205.
Watson J. D. and Crick F. H. C., “Molecular structure of nucleic acids”, Nature, 171 (1953) 737, http://www.nature.com/physics/looking-back/crick/%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/13054692.
Kiskinova M., Marsi M., Di Fabrizio E. and Gentili M., “Synchrotron radiation scanning photoemission microscopy: instrumentation and application in surface science”, Surf. Rev. Lett., 6 (1999) 265.
Collins M. D. and Gordon S. E., “Short-chain phosphoinositide partitioning into plasma membrane models”, Biophys. J., 105 (2013) 2485.
Saenger W., Principles of nucleic acids structure (Springer) 1984.
Taylor R. and Kennard O., “The molecular structures of nucleosides and nucleotides. Part 1. The influence of protonation on the geometries of nucleic acid constituents”, J. Mol. Struct., 78 (1982) 1.
Sette M., D’Addabbo P., Kelly G., Cicconi A., Micheli E., Cacchione S., Poma A., Gargioli C., Giambra V. and Frezza D., “Evidence for a quadruplex structure in the polymorphic hs1.2 enhancer of the immunoglobulin heavy chain 3′ regulatory regions and its conservation in mammals”, Biopolymers., 105 (2016) 768.
Yu X., Li Z., Shen J., Chan M. T. V. and Wu W. K. K., “Role of microRNAs in primary central nervous system lymphomas”, Cell Prolif., 49 (2016) 147, http://dx.doi.org/10.1111/cpr.12243.
Yu A. A., Savas T., Cabrini S., DiFabrizio E., Smith H. I. and Stellacci F., “High resolution printing of DNA feature on poly(methyl methacrylate) substrates using supramolecular nano-stamping”, J. Am. Chem. Soc., 127 (2005) 16774.
Teo P. Y., Cheng W., Hedrick J. L. and Yang Y. Y., “Co-delivery of drugs and plasmid DNA for cancer therapy”, Adv. Drug Deliv. Rev., 98 (2016) 41.
Goodchild J., “Therapeutic oligonucleotides”, Methods Mol. Biol., 764 (2011) 1.
Evers M. M., Toonen L. J. A. and van Roon-Mom W. M. C., “Antisense oligonucleotides in therapy for neurodegenerative disorders”, Adv. Drug Deliv. Rev., 87 (2015) 90, http://www.sciencedirect.com/science/article/pii/S0169409X15000435.
Parashar A., “Aptamers in Therapeutics”, J. Clin. Diagn. Res., 10 (2016) BE01, http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4963637/.
Agarwal A., Rhoades W. R., Hanout M., Soliman M. K., Sarwar S., Sadiq M. A., Sepah Y. J., Do D. V. and Nguyen Q. D., “Management of neovascular age-related macular degeneration: Current state-of-the-art care for optimizing visual outcomes and therapies in development”, Clin. Ophthalmol., 9 (2015) 1001.
Keefe A. D., Pai S. and Ellington A., “Aptamers as therapeutics”, Nat. Rev. Drug Discov., 9 (2010) 537, http://dx.doi.org/10.1038/nrd3141.
Lao Y. H., Phua K. K. L. and Leong K. W., “Aptamer nanomedicine for cancer therapeutics: Barriers and potential for translation”, ACS Nano, 9 (2015) 2235.
Lu H., Busch J., Jung M., Rabenhorst S., Ralla B., Kilic E., Mergemeier S., Budach N., Fendler A. and Jung K., “Diagnostic and prognostic potential of circulating cell-free genomic and mitochondrial DNA fragments in clear cell renal cell carcinoma patients”, Clin. Chim. Acta., 452 (2016) 109.
Connolly I. D., Li Y., Gephart M. H. and Nagpal S., “The ‘Liquid Biopsy’: the Role of Circulating DNA and RNA in Central Nervous System Tumors”, Curr. Neurol. Neurosci. Rep., 16 (2016) 1.
Almassalha L. M., Bauer G. M., Chandler J. E., Gladstein S., Cherkezyan L., Stypula-Cyrus Y., Weinberg S., Zhang D., Thusgaard Ruhoff P., Roy H. K., Subramanian H., Chandel N. S., Szleifer I. and Backman V., “Label-free imaging of the native, living cellular nanoarchitecture using partial-wave spectroscopic microscopy”, Proc. Natl. Acad. Sci. U.S.A., 113 (2016) E6372.
Dempsey G. T., Vaughan J. C., Chen K. H., Bates M. and Zhuang X., “Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging”, Nat. Meth., 8 (2011) 1027.
Turkowyd B., Virant D. and Endesfelder U., “From single molecules to life: microscopy at the nanoscale”, Anal. Bioanal. Chem., 408 (2016) 6885, http://dx.doi.org/10.1007/s00216-016-9781-8.
Wombacher R., Heidbreder M., van de Linde S., Sheetz M. P., Heilemann M., Cornish V. W. and Sauer M., “Live-cell super-resolution imaging with trimethoprim conjugates”, Nat. Meth., 7 (2010) 717.
Flors C., “DNA and chromatin imaging with super-resolution fluorescence microscopy based on single-molecule localization”, Biopolymers, 95 (2011) 290.
Ebeling D. et al., “Imaging of biomaterials in liquids: a comparison between conventional and Q-controlled amplitude modulation (‘tapping mode’) atomic force microscopy”, Nanotechnology, 17 (2006) S221, http://stacks.iop.org/0957-4484/17/i=7/a=S20.
Poma A., Spano L., Pittaluga E., Tucci A., Palladino L. and Limongi T., “Interactions between saporin, a ribosome-inactivating protein, and DNA: a study by atomic force microscopy”, J. Microsc., 217 (2005) 69.
Di Bucchianico S., Venora G., Lucretti S., Limongi T., Palladino L. and Poma A., “Saponaria officinalis karyology and karyotype by means of image analyzer and atomic force microscopy”, Microsc. Res. Tech., 71 (2008) 730.
Lyubchenko Y. L., Shlyakhtenko L. S. and Ando T., “Imaging of nucleic acids with atomic force microscopy”, Methods, 54 (2011) 274.
Lyubchenko Y. L., “DNA structure and dynamics: an atomic force microscopy study”, Cell Biochem. Biophys., 41 (2004) 75.
Billingsley D. J., Bonass W. A., Crampton N., Kirkham J. and Thomson N. H., “Single-molecule studies of DNA transcription using atomic force microscopy”, Phys. Biol., 9 (2012) 21001.
Pyne A., Thompson R., Leung C., Roy D. and Hoogenboom B.W., “Single-molecule reconstruction of oligonucleotide secondary structure by atomic force microscopy”, Small, 10 (2014) 3257.
Uchihashi T., Tanigawa M., Ashino M., Sugawara Y., Yokoyama K., Morita S. and Ishikawa Mitsuru, “Identification of B-Form DNA in an Ultrahigh Vacuum by Noncontact-Mode Atomic Force Microscopy”, Langmuir, 16 (2000) 1349.
Ido S., Kimura K., Oyabu N., Kobayashi K., Tsukada M., Matsushige K. and Yamada H., “Beyond the helix pitch: Direct visualization of native DNA in aqueous solution”, ACS Nano, 7 (2013) 1817.
Tanaka H. and Kawai T., “Partial sequencing of a single DNA molecule with a scanning tunnelling microscope”, Nat. Nanotechnol., 4 (2009) 518, http://dx.doi.org/10.1038/nnano.2009.155.
Shapir E., Cohen H., Calzolari A., Cavazzoni C., Ryndyk D. A., Cuniberti G., Kotlyar A., Di Felice R. and Porath D., “Electronic structure of single DNA molecules resolved by transverse scanning tunnelling spectroscopy”, Nat. Mater., 7 (2008) 68.
Sun H.B. and Yokota H., “MutS-mediated detection of DNA mismatches using atomic force microscopy”, Anal. Chem., 72 (2000) 3138.
Wang H., Yang Y., Schofield M.J., Du C., Fridman Y., Lee S. D., Larson E. D., Drummond J. T., Alani E., Hsieh P. and Erie D. A, “DNA bending and unbending by MutS govern mismatch recognition and specificity”, Proc. Natl. Acad. Sci. U.S.A., 100 (2003) 14822, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=299810&tool=pmcentrez&rendertype=abstract.
Jiang Y. and Marszalek P. E., “Atomic force microscopy captures MutS tetramers initiating DNA mismatch repair”, Embo J., 30 (2011) 2881, http://www.ncbi.nlm.nih.gov/pubmed/21666597%5Cnhttp://emboj.embopress.org/content/embojnl/30/14/2881.full.pdf.
Robin Harris J. and Horne R. W., “Negative staining: A brief assessment of current technical benefits, limitations and future possibilities”, Micron., 25 (1994) 5.
Uyeda Y. and Fujiyoshi N., “The Alumina Supermicrogrid for High Resolution Electron Microscopy”, J. Electron. Microsc., 27 (1978) 75.
Fujiyoshi Y. and Uyeda N., “Direct imaging of a double-strand DNA molecule”, Ultramicroscopy., 7 (1981) 189, http://www.sciencedirect.com/science/article/pii/0304399181900097.
Taylor K. A. and Glaeser R. M., “Electron Diffraction of Frozen, Hydrated Protein Crystals”, Science, 186 (1974) 1036, http://www.sciencemag.org/content/186/4168/1036.abstract.
Brilot A. F., Chen J. Z., Cheng A., Pan J., Harrison S. C., Potter C. S., Carragher B., Henderson R. and Grigorieff N., “Beam-induced motion of vitrified specimen on holey carbon film”, J. Struct. Biol., 177 (2012) 630.
Nogales E., “The development of cryo-EM into a mainstream structural biology technique”, Nat. Meth., 13 (2016) 24, http://dx.doi.org/10.1038/nmeth.3694%5Cn10.1038/nmeth.3694.
Nogales E. and Scheres S. H. W., “Cryo-EM: A Unique Tool for the Visualization of Macromolecular Complexity”, Mol. Cell., 58 (2015) 677.
Mishyna M., Volokh O., Danilova Y., Gerasimova N., Pechnikova E. and Sokolova O. S., “Effects of radiation damage in studies of protein-DNA complexes by cryo-EM”, Micron., 96 (2017) 57, http://linkinghub.elsevier.com/retrieve/pii/S0968432816303626.
Bartesaghi A., Merk A., Banerjee S., Matthies D., Wu X., Milne J. L. S. and Subramaniam S., “2.2 Å resolution cryo-EM structure of β-galactosidase in complex with a cell-permeant inhibitor”, Science, 348 (2015) 1147, http://www.sciencemag.org.ezproxy.lib.monash.edu.au/content/348/6239/1147.abstract.
Banerjee S., Bartesaghi A., Merk A., Rao P., Bulfer S. L., Yan Y., Green N., Mroczkowski B., Neitz R. J., Wipf P., Falconieri V., Deshaies R. J., Milne J. L. S., Huryn D., Arkin M. and Subramaniam S., “2.3 Å resolution cryo-EM structure of human p97 and mechanism of allosteric inhibition”, Science, 351 (2016) 871, http://science.sciencemag.org/content/early/2016/01/27/science.aad7974.abstract%5Cnhttp://www.sciencemag.org/cgi/doi/10.1126/science.aad7974%5Cnhttp://arxiv.org/abs/1011.1669%5Cnhttp://dx.doi.org/10.1088/1751-8113/44/8/085201%5Cnhttp://stacks.iop.org/1751-8121/44.
Henderson R. and Glaeser R. M., “Quantitative analysis of image contrast in electron micrographs of beam-sensitive crystals”, Ultramicroscopy, 16 (1985) 139.
Typke D., Gilpin C. J., Downing K. H. and Glaeser R. M., “Stroboscopic image capture: Reducing the dose per frame by a factor of 30 does not prevent beam-induced specimen movement in paraffin”, Ultramicroscopy, 107 (2007) 106.
Li X., Mooney P., Zheng S., Booth C. R., Braunfeld M. B., Gubbens S., Agard D. A. and Cheng, Y., “Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM”, Nat. Methods, 10 (2013) 584, http://www.nature.com/doifinder/10.1038/nmeth.2472%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/23644547%5Cnhttp://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3684049.
Song F., Chen P., Sun D., Wang M., Dong L., Liang D., Xu R. M., Zhu P. and Li G., “Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units”, Science, 344 (2014) 376, http://www.ncbi.nlm.nih.gov/pubmed/24763583.
Sun M., Luo C., Xu L., Ji H., Ouyang Q., Yu D. and Chen Y., “Artificial lotus leaf by nanocasting”, Langmuir, 21 (2005) 8978.
Barthlott W. and Neinhuis C., “Purity of the sacred lotus, or escape from contamination in biological surfaces”, Planta, 202 (1997) 1.
Wagner T., Neinhuis C. and Barthlott W., “Wettability and Contaminability of Insect Wings as a Function of Their Surface Sculptures”, Acta Zool., 77 (1996) 213, http://doi.wiley.com/10.1111/j.1463-6395.1996.tb01265.x.
Wenzel R. N., “Resistance of solid surfaces to wetting by water”, J. Ind. Eng. Chem. (Washington, D. C.), 28 (1936) 988.
Cassie B. D., Cassie A. B. D. and Baxter S., “Wettability of porous surfaces”, Trans. Faraday Soc., 40 (1944) 546.
Cassie A. B. D. and Baxter S., “Large Contact Angles of Plant and Animal Surfaces”, Nature, 155 (1945) 21, http://adsabs.harvard.edu/abs/1945Natur.155...21C.
De Angelis F., Gentile F., Mecarini F., Das G., Moretti M., Candeloro P., Coluccio M. L., Cojoc G., Accardo A., Liberale C., Zaccaria R. P., Perozziello G., Tirinato L., Toma A., Cuda G., Cingolani R. and Di Fabrizio E., “Breaking the diffusion limit with super-hydrophobic delivery of molecules to plasmonic nanofocusing SERS structures”, Nat. Photon., 5 (2011) 682.
Ciasca G., Papi M., Businaro L., Campi G., Ortolani M., Palmieri V., Cedola A., De Ninno A., Gerardino A., Maulucci G. and De Spirito M., “Recent advances in superhydrophobic surfaces and their relevance to biology and medicine”, Bioinspir. Biomim., 11 (2016) 11001.
Draper M. C., Crick C. R., Orlickaite V., Turek V. A., Parkin I. P. and Edel J. B., “Superhydrophobic surfaces as an on-chip microfluidic toolkit for total droplet control”, Anal. Chem., 85 (2013) 5405.
Quéré D., “Non-sticking drops”, Rep. Prog. Phys., 68 (2005) 2495.
Peng L., Li H., Zhang Y., Su J., Yu P. and Luo Y., “A superhydrophobic 3D porous material for oil spill cleanup”, RSC Adv., 4 (2014) 46470.
Gentile F., Das G., Coluccio M. L., Mecarini F., Accardo A., Tirinato L., Tallerico R., Cojoc G., Liberale C., Candeloro P., Decuzzi P., De Angelis F. and Di Fabrizio E., “Ultra low concentrated molecular detection using super hydrophobic surface based biophotonic devices”, Microelectron. Eng., 87 (2010) 798, http://dx.doi.org/10.1016/j.mee.2009.11.083.
Marini M., Das G., La Rocca R., Gentile F., Limongi T., Santoriello S., Scarpellini A. and Di Fabrizio E., “Raman spectroscopy for detection of stretched DNAs on superhydrophobic surfaces”, Microelectron. Eng., 119 (2014) 151, http://dx.doi.org/10.1016/j.mee.2014.04.008.
Marini M., Falqui A., Moretti M., Limongi T., Allione M., Genovese A., Lopatin S., Tirinato L., Das G., Torre B., Giugni A., Gentile F., Candeloro P. and Di Fabrizio E., “The structure of DNA by direct imaging”, Sci. Adv., 1 (2015) e1500734, http://advances.sciencemag.org/content/1/7/e1500734.abstract.
Gentile F., Coluccio M. L., Accardo A., Asande M., Cojoc G., Mecarini F., Das G., Liberale C., De Angelis F., Candeloro P., Decuzzi P. and Di Fabrizio E., “Nanoporous-micropatterned-superhydrophobic surfaces as harvesting agents for few low molecular weight molecules”, Microelectron. Eng., 88 (2011) 1749, http://dx.doi.org/10.1016/j.mee.2010.12.076.
Gentile F., Coluccio M. L., Rondanina E., Santoriello S., Di Mascolo D., Accardo A., Francardi M., De Angelis F., Candeloro P. and Di Fabrizio E., “Non periodic patterning of super-hydrophobic surfaces for the manipulation of few molecules”, Microelectron. Eng., 111 (2013) 272, http://dx.doi.org/10.1016/j.mee.2013.01.036.
Miele E., Accardo A., Falqui A., Marini M., Giugni A., Leoncini M., De Angelis F., Krahne R. and Di Fabrizio E., “Writing and functionalisation of suspended DNA nanowires on superhydrophobic pillar arrays”, Small, 11 (2015) 134.
Accardo A., Tirinato L., Altamura D., Sibillano T., Giannini C., Riekel C. and Di Fabrizio E., “Superhydrophobic surfaces allow probing of exosome self organization using X-ray scattering”, Nanoscale, 5 (2013) 2295–9, http://www.ncbi.nlm.nih.gov/pubmed/23426504.
Accardo A., Di Fabrizio E., Limongi T., Marinaro G. and Riekel C., “Probing droplets on superhydrophobic surfaces by synchrotron radiation scattering techniques”, J. Synchrotron Radiat., 21 (2014) 643.
Gentile F., Moretti M., Limongi T., Falqui A., Bertoni G., Scarpellini A., Santoriello S., Maragliano L., Proietti Zaccaria R. and Di Fabrizio E., “Direct imaging of DNA fibers: The visage of double helix”, Nano Lett., 12 (2012) 6453.
Gentile F., Coluccio M. L., Limongi T., Perozziello G., Candeloro P. and Di Fabrizio E., “The five Ws (and one H) of super-hydrophobic surfaces in medicine”, Micromachines., 5 (2014) 239.
Gentile F., Battista E., Accardo A., Coluccio M. L., Asande M., Perozziello G., Das G., Liberale C., De Angelis F., Candeloro P., Decuzzi P. and Di Fabrizio E., “Fractal structure can explain the increased hydrophobicity of nanoporous silicon films”, Microelectron. Eng., 88 (2011) 2537, http://dx.doi.org/10.1016/j.mee.2011.01.046.
Gentile F., Coluccio M. L., Accardo A., Marinaro G., Rondanina E., Santoriello S., Marras S., Das G., Tirinato L., Perozziello G., De Angelis F., Dorigoni C., Candeloro P. and Di Fabrizio E., “Tailored Ag nanoparticles/nanoporous superhydrophobic surfaces hybrid devices for the detection of single molecule”, Microelectron. Eng., 97 (2012) 349, http://dx.doi.org/10.1016/j.mee.2012.03.025.
Gentile F., Coluccio M. L., Coppede N., Mecarini F., Das G., Liberale C., Tirinato L., Leoncini M., Perozziello G., Candeloro P., De Angelis F. and Di Fabrizio E., “Superhydrophobic surfaces as smart platforms for the analysis of diluted biological solutions”, ACS Appl. Mater. Interfaces, 4 (2012) 3213.
Sanger F., Coulson A. R., Hong G. F., Hill D. F. and Petersen G. B., “Nucleotide sequence of bacteriophage lambda DNA”, J. Mol. Biol., 162 (1982) 729.
Daniels D. L., Schroeder J. L., Szybalski W., Sanger F., Coulson A. R., Hong G. F., Hill D. F., Petersen G. B. and Blattner F. R., “APPENDIX II Complete Annotated Lambda Sequence”, (1983).
Gentile F., Coluccio M. L., Limongi T., Perozziello G., Candeloro P. and Di Fabrizio E., “The five Ws (and one H) of super-hydrophobic surfaces in medicine”, Micromachines, 5 (2014) 239.
Williams D. B. and Carter C. B., Transmission Electron Microscopy: A Textbook for Materials Science, 2nd edition (Springer-Verlag, New York) 2009, http://www.loc.gov/catdir/enhancements/fy0820/96028435-d.html.
Voet D. and Rich A., “The crystal structures of purines, pyrimidines and their intermolecular complexes”, Prog. Nucleic Acid Res., 10 (1970) 183.
Marini M., Limongi T., Falqui A., Genovese A., Allione M., Moretti M., Lopatin S., Tirinato L., Das G., Torre B., Giugni A., Cesca F., Benfenati F. and Di Fabrizio E., “Imaging and structural studies of DNA-protein complexes and membrane ion channels”, Nanoscale, 9 (2016) 2768.
Marini M., Limongi T., Allione M., Falqui A. and E D. F., “Superhydrophobic Manipulation of DNA”, Adv. Gen. Eng., 3 (2014) 10, http://www.omicsgroup.org/journals/cardiac-specific-knockout-of-p65-mice-resist-to-cardiac-ischemiareperfusion-injury-2169-0111-1000i101.php?aid=42891.
Marini M., Allione M., Torre B., Moretti M., Limongi T., Tirinato L., Giugni A., Das G. and di Fabrizio E., “Raman on suspended DNA: Novel super-hydrophobic approach for structural studies”, Microelectron. Eng., 175 (2017) 38, http://linkinghub.elsevier.com/retrieve/pii/S0167931716305275.
Theophanides T. and Tajmir-Riahi H. A., “Flexibility of DNA and RNA upon Binding to Different Metal Cations. An Investigation of the B to A to Z Conformational Transition by Fourier Transform Infrared Spectroscopy”, J. Biomol. Struct. Dyn., 2 (1985) 995, http://dx.doi.org/10.1080/07391102.1985.10507615.
Parker F. S., “Crystal and solution structures of the B-DNA dodecamer d(CGCAAATTTGCG) probed by Raman spectroscopy: heterogeneity in the crystal structure does not persist in the solution structure”, Biochemistry, 27 (1988) 931, http://www.ncbi.nlm.nih.gov/pubmed/3365372.
Parker F. S., “Applications of infrared, Raman and resonance Raman spectroscopy in biochemistry”, J. Mol. Struct., 128 (1985) 349, http://www.sciencedirect.com/science/article/pii/0022286085850122.
Gentile F., Coluccio M. L., Toma A., Alabastri A., Zaccaria R. P., Das G., De Angelis F., Candeloro P., Liberale C., Perozziello G., Tirinato L., Leoncini M. and Di Fabrizio E., “Plasmonics and Super-Hydrophobicity: A New Class of Nano-Bio-Devices”, Plasmon. Theory Appl., 15 (2013) 501.
Das G., Gentile F., De Angelis F., Coluccio M. L., Liberale C., Proietti Zaccaria R. and Di Fabrizio E., Superhydrophobicity, plasmonics and Raman spectroscopy for few/single molecule detection down to attomolar concentration, Proc. SPIE, 8457 (2012) 84570C, http://proceedings.spiedigitallibrary.org/proceeding.aspx?doi=10.1117/12.936517.
Coluccio M. L., Gentile F., Das G., Nicastri A., Perri A. M., Candeloro P., Perozziello G., Proietti Zaccaria R., Gongora J. S. T., Alrasheed S., Fratalocchi A., Limongi T., Cuda G. and Di Fabrizio E., “Detection of single amino acid mutation in human breast cancer by disordered plasmonic self-similar chain”, Sci. Adv., 1 (2015) e1500487.
Gentile F., Coluccio M. L., Zaccaria R. P., Francardi M., Cojoc G., Perozziello G., Raimondo R., Candeloro P. and Di Fabrizio E., “Selective on site separation and detection of molecules in diluted solutions with super-hydrophobic clusters of plasmonic nanoparticles”, Nanoscale, 6 (2014) 8208, http://pubs.rsc.org/en/content/articlelanding/2014/nr/c4nr00796d%5Cnhttp://pubs.rsc.org/en/content/articlelanding/2014/nr/c4nr00796d#!divAbstract.
De Angelis F., Das G., Candeloro P., Patrini M., Galli M., Bek A., Lazzarino M., Maksymov I., Liberale C., Andreani L. C. and Di Fabrizio E., “Nanoscale chemical mapping using three-dimensional adiabatic compression of surface plasmon polaritons”, Nat. Nanotechnol., 5 (2010) 67, http://dx.doi.org/10.1038/nnano.2009.348.
Tirinato L., Gentile F., Di Mascolo D., Coluccio M. L., Das G., Liberale C., Pullano S. A., Perozziello G., Francardi M., Accardo A., De Angelis F., Candeloro P. and Di Fabrizio E., “SERS analysis on exosomes using super-hydrophobic surfaces”, Microelectron. Eng., 97 (2012) 337, http://dx.doi.org/10.1016/j.mee.2012.03.022.
Hood J. L., San Roman S. and Wickline S. A., “Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis”, Cancer Res., 71 (2011) 3792.
Lee T. H., D’Asti E., Magnus N., Al-Nedawi K., Meehan B. and Rak J., “Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular “debris””, Semin. Immunopathol., 33 (2011) 1.
Dawson T. M. and Dawson V. L., “Molecular pathways of neurodegeneration in Parkinson’s disease”, Science, 302 (2003) 819.
Crews L. and Masliah E., “Molecular mechanisms of neurodegeneration in Alzheimer’s disease”, Human Mol. Genet., 19 (2010) R12.
Kelly J. W., “Amyloid fibril formation and protein misassembly: a structural quest for insights into amyloid and prion diseases”, Structure, 5 (1997) 595, http://www.sciencedirect.com/science/article/pii/S0969212697002153%5Cnhttp://www.ncbi.nlm.nih.gov/pubmed/9195890.
Pepys M. B., Hawkins P. N., Booth D. R., Vigushin D. M., Tennent G. A., Soutar A. K., Totty N., Nguyen O., Blake C. C. F., Terry C. J., Feest T. G., Zalin A. M. and Hsuan J. J., “Human Lysozyme Gene-Mutations Cause Hereditary Systemic Amyloidosis”, Nature, 362 (1993) 553.
Lakshmanan A., Cheong D. W., Accardo A., Di Fabrizio E., Riekel C. and Hauser C. A. E., “Aliphatic peptides show similar self-assembly to amyloid core sequences, challenging the importance of aromatic interactions in amyloidosis”, Proc. Natl. Acad. Sci. U.S.A., 110 (2013) 519, http://www.pnas.org/content/110/2/519.
Accardo A., Gentile F., Mecarini F., De Angelis F., Burghammer M., Di Fabrizio E. and Riekel C., “In situ X-ray scattering studies of protein solution droplets drying on micro-and nanopatterned superhydrophobic PMMA surfaces”, Langmuir, 26 (2010) 15057.
Accardo A., Burghammer M., Di Cola E., Reynolds M., Di Fabrizio E. and Riekel C., “Lysozyme fibrillation induced by convective flow under quasi contact-free conditions”, Soft Matter., 7 (2011) 6792, http://pubs.rsc.org/en/content/articlehtml/2011/sm/c1sm05783a.
Limongi T., Cesca F., Gentile F., Marotta R., Ruffilli R., Barberis A., Dal Maschio M., Petrini E. M., Santoriello S., Benfenati F. and Di Fabrizio E., “Nanostructured superhydrophobic substrates trigger the development of 3D neuronal networks”, Small, 9 (2013) 402.
Cesca F., Limongi T., Accardo A., Rocchi A., Orlando M., Shalabaeva V., Di Fabrizio E. and Benfenati F., “Fabrication of biocompatible free-standing nanopatterned films for primary neuronal cultures”, RSC Adv., 4 (2014) 45696, http://pubs.rsc.org/en/content/articlehtml/2014/ra/c4ra08361j.
Egerton R. F., Li P. and Malac M., “Radiation damage in the TEM and SEM”, Micron, 35 (2004) 399.
Egerton R. F., “Mechanisms of radiation damage in beam-sensitive specimens, for TEM accelerating voltages between 10 and 300 kV”, Microsc. Res. Tech., 75 (2012) 1550.
Eastman A., “The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes”, Pharmacol. Ther., 34 (1987) 155.
Wang D. and Lippard S. J., “Cellular processing of platinum anticancer drugs”, Nat. Rev. Drug Deliv., 4 (2005) 307.
Ono A., Cao S., Togashi H., Tashiro M., Fujimoto T., Machinami T., Oda S., Miyake Y., Okamoto I. and Tanaka Y., “Specific interactions between silver(I) ions and cytosine-cytosine pairs in DNA duplexes”, Chem. Commun. (Cambridge), Issue 39 (2008) 4825.
Singer-Lahat D., Dascal N., Mittelman L., Peleg S. and Lotan I., “Imaging plasma membrane proteins in large membrane patches of Xenopus oocytes”, Pflugers Arch. Eur. J. Physiol., 440 (2000) 627.
Navas P., Nowack D. D. and Morre D. J., “Isolation of purified plasma membranes from cultured cells and hepatomas by two-phase partition and preparative free-flow electrophoresis”, Cancer Res., 49 (1989) 2147.
Sereda V. and Lednev I. K., “Polarized Raman spectroscopy of aligned insulin fibrils”, J. Raman Spectrosc., 45 (2014) 665.
Jahn T. R., Makin O. S., Morris K. L., Marshall K. E., Tian P., Sikorski P. and Serpell L. C., “The common architecture of cross-beta amyloid”, J. Mol. Biol., 395 (2010) 717, http://www.ncbi.nlm.nih.gov/pubmed/19781557.
Van Dyck D. and Chen F.-R., “‘Big Bang’ tomography as a new route to atomic-resolution electron tomography”, Nature, 486 (2012) 243, http://www.ncbi.nlm.nih.gov/pubmed/22699616.
Ophus C., Ciston J., Pierce J., Harvey T. R., Chess J., McMorran B. J., Czarnik C., Rose H. H. and Ercius P., “Efficient linear phase contrast in scanning transmission electron microscopy with matched illumination and detector interferometry”, Nat. Commun., 7 (2016) 10719, http://www.nature.com/ncomms/2016/160229/ncomms10719/full/ncomms10719.html.
Mohri K., Kusuki E., Ohtsuki S., Takahashi N., Endo M., Hidaka K., Sugiyama H., Takahashi Y., Takakura Y. and Nishikawa M., “Self-Assembling DNA Dendrimer for Effective Delivery of Immunostimulatory CpG DNA to Immune Cells”, Biomacromolecules, 16 (2015) 1095.
Marini M., Piantanida L., Musetti R., Bek A., Dong M., Besenbacher F., Lazzarino M. and Firrao G., “A revertible, autonomous, self-assembled DNA-origami nanoactuator”, Nano Lett., 11 (2011) 5449, http://www.ncbi.nlm.nih.gov/pubmed/22047682.
Piantanida L., Naumenko D., Torelli E., Marini M., Bauer D. M., Fruk L., Firrao G. and Lazzarino M., “Plasmon resonance tuning using DNA origami actuation”, Chem. Commun., 51 (2015) 4789.
Torelli E., Marini M., Palmano S., Piantanida L., Polano C., Scarpellini A., Lazzarino M. and Firrao G., “A DNA origami nanorobot controlled by nucleic acid hybridization”, Small, 10 (2014) 2918.
Yan H., Zhang X., Shen Z. and Seeman N. C., “A robust DNA mechanical device controlled by hybridization topology”, Nature, 415 (2002) 62.
Manuscript A. and Malignancies H., “Detection of Circulating Tumor DNA in Early- and Late-Stage Human Malignancies”, Sci. Transl. Med., 6 (2014) 224ra24.
Gray E. S., Rizos H., Reid A. L., Boyd S. C., Pereira M. R., Lo J., Tembe V., Freeman J., Lee J. H. J., Scolyer R. A., Siew K., Lomma C., Cooper A., Khattak M. A., Meniawy T. M. Long, G. V., Carlino M. S., Millward M. and Ziman M., “Circulating tumor DNA to monitor treatment response and detect acquired resistance in patients with metastatic melanoma”, Oncotarget, 6 (2015) 42008, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4747205&tool=pmcentrez&rendertype=abstract.
Aarthy R., Mani S., Velusami S., Sundarsingh S. and Rajkumar T., “Role of Circulating Cell-Free DNA in Cancers”, Mol. Diagnosis Ther., 19 (2015) 339.
Bellassai N. and Spoto G., “Biosensors for liquid biopsy: circulating nucleic acids to diagnose and treat cancer”, Anal. Bioanal. Chem., 408 (2016) 1.
Dinakaran V., Rathinavel A., Pushpanathan M., Sivakumar R., Gunasekaran P. and Rajendhran J., “Elevated levels of circulating DNA in cardiovascular disease patients: metagenomic profiling of microbiome in the circulation”, PLoS One., 9 (2014) e105221.
Bakir M., Engin A., Kuskucu M. A., Bakir S., Gündag O. and Midilli K., “Relationship of Plasma Cell-Free DNA Level With Mortality and Prognosis in Patients With Crimean-Congo Hemorrhagic Fever”, J. Med. Virol., 88 (2016) 1152.
Basak R., Nair N. K. and Mittra I., “Evidence for cell-free nucleic acids as continuously arising endogenous DNA mutagens”, Mutat. Res. Mol. Mech. Mutagen., 793 (2016) 15, http://dx.doi.org/10.1016/j.mrfmmm.2016.10.002.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Marini, M., Limongi, T., Moretti, M. et al. The structure of DNA by direct imaging and related topics. Riv. Nuovo Cim. 40, 241–277 (2017). https://doi.org/10.1393/ncr/i2017-10135-7
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1393/ncr/i2017-10135-7