Spermine induced reversible collapse of deoxyribonucleic acid-bridged nanoparticle-based assemblies
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DNA-linked 2D and 3D nano-assemblies find use in a diverse set of applications, ranging from DNA-origami in drug delivery and medical imaging, to DNA-linked nanoparticle structures for use in plasmonics and (bio)sensing. However, once these structures have been fully assembled, few options are available to modulate structure geometry. Here, we investigated the use of the polycation spermine to induce DNA collapse in small oligonucleotide-linked (54 bp) gold nanoparticle structures by monitoring shifts in the localized surface plasmon resonance (LSPR) peak and by comparing the data with finite-difference time-domain (FDTD) simulations. Our data shows that low concentrations of spermine can be applied to induce large changes in DNA conformation, leading to a significant reduction in interparticle distance (from ~25 to ~3 nm) and enhanced plasmonic coupling. The DNA collapse is near-instantaneous and reversible, and its application at low and high DNA densities is demonstrated with surface plasmon resonance imaging (SPRi), showing the potential of spermine to dynamically modulate distances and geometry in DNA-based nano-assemblies.
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Spermine induced reversible collapse of deoxyribonucleic acid-bridged nanoparticle-based assemblies
)
Abstract
DNA-linked 2D and 3D nano-assemblies find use in a diverse set of applications, ranging from DNA-origami in drug delivery and medical imaging, to DNA-linked nanoparticle structures for use in plasmonics and (bio)sensing. However, once these structures have been fully assembled, few options are available to modulate structure geometry. Here, we investigated the use of the polycation spermine to induce DNA collapse in small oligonucleotide-linked (54 bp) gold nanoparticle structures by monitoring shifts in the localized surface plasmon resonance (LSPR) peak and by comparing the data with finite-difference time-domain (FDTD) simulations. Our data shows that low concentrations of spermine can be applied to induce large changes in DNA conformation, leading to a significant reduction in interparticle distance (from ~25 to ~3 nm) and enhanced plasmonic coupling. The DNA collapse is near-instantaneous and reversible, and its application at low and high DNA densities is demonstrated with surface plasmon resonance imaging (SPRi), showing the potential of spermine to dynamically modulate distances and geometry in DNA-based nano-assemblies.
References(52)
Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Programmable materials and the nature of the DNA bond. Science 2015, 347, 1260901.
Zhan, P. F.; Jiang, Q.; Wang, Z. G.; Li, N.; Yu, H. Y.; Ding, B. Q. DNA nanostructure-based imaging probes and drug carriers. ChemMedChem 2014, 9, 2013-2020.
Tintoré, M.; Eritja, R.; Fábrega, C. DNA nanoarchitectures: Steps towards biological applications. ChemBioChem 2014, 15, 1374-1390.
Jungmann, R.; Avendaño, M. S.; Woehrstein, J. B.; Dai, M. J.; Shih, W. M.; Yin, P. Multiplexed 3D cellular super- resolution imaging with DNA-PAINT and exchange-PAINT. Nat. Methods 2014, 11, 313-318.
Fu, Y. M.; Zeng, D. D.; Chao, J.; Jin, Y. Q.; Zhang, Z.; Liu, H. J.; Li, D.; Ma, H. W.; Huang, Q.; Gothelf, K. V. et al. Single-step rapid assembly of DNA origami nanostructures for addressable nanoscale bioreactors. J. Am. Chem. Soc. 2013, 135, 696-702.
Samanta, A.; Banerjee, S.; Liu, Y. DNA nanotechnology for nanophotonic applications. Nanoscale 2015, 7, 2210-2220.
Tan, S. J.; Campolongo, M. J.; Luo, D.; Cheng, W. L. Building plasmonic nanostructures with DNA. Nat. Nanotechnol. 2011, 6, 268-276.
Petryayeva, E.; Krull, U. J. Localized surface plasmon resonance: Nanostructures, bioassays and biosensing—A review. Anal. Chim. Acta 2011, 706, 8-24.
Thacker, V. V.; Herrmann, L. O.; Sigle, D. O.; Zhang, T.; Liedl, T.; Baumberg, J. J.; Keyser, U. F. DNA origami based assembly of gold nanoparticle dimers for surface-enhanced Raman scattering. Nat. Commun. 2014, 5, 3448.
Chen, Y.; Munechika, K.; Ginger, D. S. Dependence of fluorescence intensity on the spectral overlap between fluorophores and plasmon resonant single silver nanoparticles. Nano Lett. 2007, 7, 690-696.
Hutter, E.; Fendler, J. H. Exploitation of localized surface plasmon resonance. Adv. Mater. 2004, 16, 1685-1706.
Willets, K. A.; Van Duyne, R. P. Localized surface plasmon resonance spectroscopy and sensing. Annu. Rev. Phys. Chem. 2007, 58, 267-297.
Fong, K. E.; Yung, L. Y. L. Localized surface plasmon resonance: Aunique property of plasmonic nanoparticles for nucleic acid detection. Nanoscale 2013, 5, 12043-12071.
Nien, L. W.; Lin, S. C.; Chao, B. K.; Chen, M. J.; Li, J. H.; Hsueh, C. H. Giant electric field enhancement and localized surface plasmon resonance by optimizing contour bowtie nanoantennas. J. Phys. Chem. C 2013, 117, 25004-25011.
Woo, K. C.; Shao, L.; Chen, H. J.; Liang, Y.; Wang, J. F.; Lin, H. Q. Universal scaling and Fano resonance in the plasmon coupling between gold nanorods. ACS Nano 2011, 5, 5976-5986.
Kang, K. A.; Wang, J. T.; Jasinski, J. B.; Achilefu, S. Fluorescence manipulation by gold nanoparticles: From complete quenching to extensive enhancement. J. Nanobiotechnology 2011, 9, 16.
Mandal, S.; Mandal, A.; Johansson, H. E.; Orjalo, A. V; Park, M. H. Depletion of cellular polyamines, spermidine and spermine, causes a total arrest in translation and growth in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 2169-2174.
Feuerstein, B. G.; Pattabiraman, N.; Marton, L. J. Spermine- DNA interactions: Atheoretical study. Proc. Natl. Acad. Sci. U. S. A. 1986, 83, 5948-5952.
Marquet, R.; Houssier, C.; Fredericq, E. An electro-optical study of the mechanisms of DNA condensation induced by spermine. Biochim. Biophys. Acta 1985, 825, 365-374.
Pelta, J.; Livolant, F.; Sikorav, J. L. DNA aggregation induced by polyamines and cobalthexamine. J. Biol. Chem. 1996, 271, 5656-5662.
Burak, Y.; Ariel, G.; Andelman, D. Competition between condensation of monovalent and multivalent ions in DNA aggregation. Curr. Opin. Colloid Interface Sci. 2004, 9, 53-58.
Mertens, J.; Tamayo, J.; Kosaka, P.; Calleja, M. Observation of spermidine-induced attractive forces in self-assembled monolayers of single stranded DNA using a microcantilever sensor. Appl. Phys. Lett. 2011, 98, 153704.
Wilson, R. W.; Bloomfield, V. A. Counterion-induced condensation of deoxyribonucleic acid. A light-scattering study. Biochemistry 1979, 18, 2192-2196.
Lin, Z.; Wang, C.; Feng, X. Z.; Liu, M. Z.; Li, J. W.; Bai, C. L. The observation of the local ordering characteristics of spermidine-condensed DNA: Atomic force microscopy and polarizing microscopy studies. Nucleic Acids Res. 1998, 26, 3228-3234.
Cortini, R.; Caré, B. R.; Victor, J. M.; Barbi, M. Theory and simulations of toroidal and rod-like structures in single- molecule DNA condensation. J. Chem. Phys. 2015, 142, 105102.
Sun, L.; Frykholm, K.; Fornander, L. H.; Svedhem, S.; Westerlund, F.; Åkerman, B. Sensing conformational changes in DNA upon ligand binding using QCM-D. Polyamine condensation and rad51 extension of DNA layers. J. Phys. Chem. B2014, 118, 11895-11904.
Zhang, D. Y.; Seelig, G. Dynamic DNA nanotechnology using strand-displacement reactions. Nat. Chem. 2011, 3, 103-113.
Maye, M. M.; Kumara, M. T.; Nykypanchuk, D.; Sherman, W. B.; Gang, O. Switching binary states of nanoparticle superlattices and dimer clusters by DNA strands. Nat. Nanotechnol. 2010, 5, 116-120.
Chen, J. I. L.; Chen, Y.; Ginger, D. S. Plasmonic nanoparticle dimers for optical sensing of DNA in complex media. J. Am. Chem. Soc. 2010, 132, 9600-9601.
Lermusiaux, L.; Sereda, A.; Portier, B.; Larquet, E.; Bidault, S. Reversible switching of the interparticle distance in DNA- templated gold nanoparticle dimers. ACS Nano 2012, 6, 10992-10998.
Lee, S. E.; Chen, Q.; Bhat, R.; Petkiewicz, S.; Smith, J. M.; Ferry, V. E.; Correia, A. L.; Alivisatos, A. P.; Bissell, M. J. Reversible aptamer-Au plasmon rulers for secreted single molecules. Nano Lett. 2015, 15, 4564-4570.
Chen, J. I. L.; Durkee, H.; Traxler, B.; Ginger, D. S. Optical detection of protein in complex media with plasmonic nanoparticle dimers. Small 2011, 7, 1993-1997.
Akiyama, Y.; Shikagawa, H.; Kanayama, N.; Takarada, T.; Maeda, M. Modulation of interparticle distance in discrete gold nanoparticle dimers and trimers by DNA single-base pairing. Small 2015, 11, 3153-3161.
Lermusiaux, L.; Maillard, V.; Bidault, S. Widefield spectral monitoring of nanometer distance changes in DNA-templated plasmon rulers. ACS Nano 2015, 9, 978-990.
Wang, H. Y.; Reinhard, B. M. Monitoring simultaneous distance and orientation changes in discrete dimers of DNA linked gold nanoparticles. J. Phys. Chem. C 2009, 113, 11215-11222.
Sönnichsen, C.; Reinhard, B. M.; Liphardt, J.; Alivisatos, A. P. A molecular ruler based on plasmon coupling of single gold and silver nanoparticles. Nat. Biotechnol. 2005, 23, 741-745.
Dolinnyi, A. I. Nanometric rulers based on plasmon coupling in pairs of gold nanoparticles. J. Phys. Chem. C 2015, 119, 4990-5001.
Göeken, K. L.; Subramaniam, V.; Gill, R. Enhancing spectral shifts of plasmon-coupled noble metal nanoparticles for sensing applications. Phys. Chem. Chem. Phys. 2015, 17, 422-427.
Chen, H. J.; Kou, X. S.; Yang, Z.; Ni, W. H.; Wang, J. F. Shape- and size-dependent refractive index sensitivity of gold nanoparticles. Langmuir 2008, 24, 5233-5237.
Fang, Y.; Hoh, J. H. Early intermediates in spermidine- induced DNA condensation on the surface of mica. J. Am. Chem. Soc. 1998, 120, 8903-8909.
Rubin, R. L. Spermidine-deoxyribonucleic acid interaction in vitro and in Escherichia coli. J. Bacteriol. 1977, 129, 916-925.
Vijayanathan, V.; Thomas, T.; Thomas, T. J. DNA nanoparticles and development of DNA delivery vehicles for gene therapy. Biochemistry 2002, 41, 14085-14094.
Knight, M. W.; Fan, J.; Capasso, F.; Halas, N. J. Influence of excitation and collection geometry on the dark field spectra of individual plasmonic nanostructures. Opt. Express 2010, 18, 2579-2587.
Jain, P. K.; Huang, W. Y.; El-Sayed, M. A. On the universal scaling behavior of the distance decay of plasmon coupling in metal nanoparticle pairs: A plasmon ruler equation. Nano Lett. 2007, 7, 2080-2088.
Elhadj, S.; Singh, G.; Saraf, R. F. Optical properties of an immobilized DNA monolayer from 255 to 700 nm. Langmuir 2004, 20, 5539-5543.
Hurst, S. J.; Lytton-Jean, A. K. R.; Mirkin, C. A. Maximizing DNA loading on a range of gold nanoparticle sizes. Anal. Chem. 2006, 78, 8313-8318.
Jiang, L. Y.; Yin, T. T.; Dong, Z. G.; Liao, M. Y.; Tan, S. J.; Goh, X. M.; Allioux, D.; Hu, H. L.; Li, X. Y.; Yang, J. K. W. et al. Accurate modeling of dark-field scattering spectra of plasmonic nanostructures. ACS Nano 2015, 9, 10039-10046.
Tam, F.; Chen, A. L.; Kundu, J.; Wang, H.; Halas, N. J. Mesoscopic nanoshells: Geometry-dependent plasmon resonances beyond the quasistatic limit. J. Chem. Phys. 2007, 127, 204703.
Brown, K. A.; Park, S.; Hamad-Schifferli, K. Nucleotide- surface interactions in DNA-modified Au-nanoparticle conjugates: Sequence effects on reactivity and hybridization. J. Phys. Chem. C 2008, 112, 7517-7521.
Van den Broek, B.; Noom, M. C.; van Mameren, J.; Battle, C.; MacKintosh, F. C.; Wuite, G. J. L. Visualizing the formation and collapse of DNA toroids. Biophys. J. 2010, 98, 1902-1910.
Hulme, E. C.; Trevethick, M. A. Ligand binding assays at equilibrium: Validation and interpretation. Br. J. Pharmacol. 2010, 161, 1219-1237.
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Acknowledgements
This work was funded by the Dutch Technology Foundation STW (No.11818). We would like to thank N. van der Velde for his assistance with the SPRi experiments.
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