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Sequence-dependent hybridizability of DNA-monoconjugated nanoparticles: Kinetic complexity unveiled by a dimerization assay

  • Center for Bioanalytical Chemistry, Department of Chemistry, University of Science and Technology of China, Hefei 230026, China

Cite this:
https://doi.org/10.52396/JUST-2021-0195
  • Received Date: 06 September 2021
  • Rev Recd Date: 23 September 2021
  • Publish Date: 30 November 2021
    Abstract

  • Abstract

    Understanding DNA hybridization kinetics is highly important for nucleic acid detections, genomic biotechniques, and DNA nanotechnology. DNA-conjugated nanomaterials offer versatile functionalities for DNA-programmable nanoassembly with superfine controls toward bioanalytical and nanotechnological applications. Although small molecule end-tagging does not incur much attenuation of DNA’s hybridizability, nanoparticle-conjugation greatly suppresses the hybridization kinetics of DNA strands. The impeded hybridization not only decreases the efficiency in building complicated nanostructures, but also causes difficulty in realizing rapidly responsive sensors and nanomotors. With monovalent DNA-nanoparticle conjugates as an ideal system, this work aims to unveil the kinetic complexity of hybridization-driven dimeric assembly assayed by agarose gel electrophoresis. Our results point out a coexistence of different factors that can affect the hybridization kinetics of DNA-conjugated nanoparticles, including: the rigidity of a DNA spacer proximal to the nanoparticle surface; the base-stacking between the spacer and a hybridized domain; the inherent base-sequence-dependent DNA hybridizability; and the spatially confined movement of the hybridization sequences. The dimeric hybridization assay offers a reliable platform for kinetic evaluation of DNA-conjugated nanoparticles to enable structurally complicated and rapidly functioning analytical devices and bio-labelling nanoprobes.

    Abstract

    Understanding DNA hybridization kinetics is highly important for nucleic acid detections, genomic biotechniques, and DNA nanotechnology. DNA-conjugated nanomaterials offer versatile functionalities for DNA-programmable nanoassembly with superfine controls toward bioanalytical and nanotechnological applications. Although small molecule end-tagging does not incur much attenuation of DNA’s hybridizability, nanoparticle-conjugation greatly suppresses the hybridization kinetics of DNA strands. The impeded hybridization not only decreases the efficiency in building complicated nanostructures, but also causes difficulty in realizing rapidly responsive sensors and nanomotors. With monovalent DNA-nanoparticle conjugates as an ideal system, this work aims to unveil the kinetic complexity of hybridization-driven dimeric assembly assayed by agarose gel electrophoresis. Our results point out a coexistence of different factors that can affect the hybridization kinetics of DNA-conjugated nanoparticles, including: the rigidity of a DNA spacer proximal to the nanoparticle surface; the base-stacking between the spacer and a hybridized domain; the inherent base-sequence-dependent DNA hybridizability; and the spatially confined movement of the hybridization sequences. The dimeric hybridization assay offers a reliable platform for kinetic evaluation of DNA-conjugated nanoparticles to enable structurally complicated and rapidly functioning analytical devices and bio-labelling nanoprobes.
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    • References(59)
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    Park S, Brown K A, Hamad-Schifferli K.Changes in oligonucleotide conformation on nanoparticle surfaces by modification with mercaptohexanol. Nano Lett., 2004, 4(10): 1925-1929.
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    Liu B W, Wu P, Huang Z C, et al. Bromide as arobust backfiller on gold for precise control of DNA conformation and high stability of spherical nucleic acids. J. Am. Chem. Soc., 2018, 140(13): 4499-4502.
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    Maye M M, Nykypanchuk D, van der Lelie D, et al.A simple method for kinetic control of DNA-induced nanoparticle assembly. J. Am. Chem. Soc., 2006, 128(43): 14020-14021.
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    Prigodich A E, Lee O S, Daniel W L, et al.Tailoring DNA structure to increase target hybridization kinetics on surfaces. J. Am. Chem. Soc., 2010, 132(31): 10638-10641.
    [36]
    Li Y L, Han X G, Deng Z X. Grafting SWNTs with highly hybridizable DNA sequences: Potential building blocks for DNA-programmed material assembly. Angew. Chem. Int. Ed., 2007, 46(39): 7481-7484.
    [37]
    Maune H T, Han S P, Barish R D, et al.Self-assembly of carbon nanotubes into two-dimensional geometries using DNA origami templates. Nat. Nanotech., 2010, 5(1): 61-66.
    [38]
    Sun W, Shen J, Zhao Z, et al. Precise pitch-scaling of carbon nanotube arrays within three-dimensional DNA nanotrenches. Science, 2020, 368(6493): 874-877.
    [39]
    Zhang J X, Fang J X, Duan W, et al. Predicting DNA hybridization kinetics from sequence. Nat. Chem., 2018, 10(11): 91-98.
    [40]
    Esashika K, Saiki T.DNA Hybridization assay using gold nanoparticles and electrophoresis separation provides 1 pM sensitivity. Bioconjug. Chem., 2018, 29(1): 182-189.
    [41]
    Marimuthu K,Chakrabarti R. Sequence-dependent theory of oligonucleotide hybridization kinetics.J. Chem. Phys., 2014, 140(17): 175104.
    [42]
    Sorgenfrei S, Chiu C Y, Gonzalez Jr R L, et al. Label-free field-effect-based single-molecule detection of DNA hybridization kinetics. Nat. Nanotechnol., 2011, 6(2): 126-132.
    [43]
    Yin Y D, Zhao X S. Kinetics and dynamics of DNA hybridization. Acc. Chem. Res., 2011, 44(1): 1172-1181.
    [44]
    Lee C Y, Nguyen P C, Grainger D W, et al. Structure and DNA hybridization properties of mixed nucleic acid/maleimide-ethylene glycol monolayers.Anal. Chem., 2007, 79(12): 4390-4400.
    [45]
    Erickson D, Li D Q, Krull U J. Modeling of DNA hybridization kinetics for spatially resolved biochips. Anal.Biochem., 2003, 317(2):186-200.
    [46]
    Okahata Y, Kawase M, Niikura K, et al. Kinetic measurements of DNA hybridization on an oligonucleotide-immobilized 27-MHz quartz crystal microbalance. Anal. Chem., 1998, 70(7): 1288-1296.
    [47]
    Schwille P, Oehlenschläger F, Walter N G. Quantitative hybridization kinetics of DNA probes to RNA in solution followed by diffusional fluorescence correlation analysis.Biochemistry, 1996, 35(31): 10182-10193.
    [48]
    Mazumder A, Majlessi M, Becker M M. A high throughput method to investigate oligodeoxyribonucleotide hybridization kinetics and thermodynamics.Nucleic Acids Res., 1998, 26(8): 1996-2000.
    [49]
    Yao G B, Li J, Li Q, et al. Programming nanoparticle valence bonds with single-stranded DNA encoders. Nat. Mater., 2020, 19(7): 781-788.
    [50]
    Zanchet D, Micheel C M, Parak W J, et al.Electrophoretic isolation of discrete Au nanocrystal/DNA conjugates. Nano Lett., 2001, 1(1): 32-35.
    [51]
    Claridge S A, Liang H W, Basu S R, et al.Isolation of discrete nanoparticle-DNA conjugates for plasmonic applications. Nano Lett., 2008, 8(4): 1202-1206.
    [52]
    Kushon S A, Jordan J P, Seifert J L, et al.Effect of secondary structure on the thermodynamics and kinetics of PNA hybridization to DNA hairpins.J. Am. Chem. Soc., 2001, 123(44): 10805-10813.
    [53]
    Riccelli P V, Merante F, Leung K T, et al. Hybridization of single-stranded DNA targets to immobilized complementary DNA probes: comparison of hairpin versus linear capture probes. Nucleic Acids Res., 2001, 29(4): 996-1004.
    [54]
    Gao Y, Wolf L K, Georgiadis R M. Secondary structure effects on DNA hybridization kinetics:A solution versus surface comparison.Nucleic Acids Res., 2006, 34(11): 3370-3377.
    [55]
    Alivisatos A P, Johnsson K P, Peng X G, et al.Organization of 'nanocrystal molecules' using DNA. Nature, 1996, 382: 609-611.
    [56]
    Yuan B F, Zhuang X Y, Hao Y H, et al. Kinetics of base stacking-aided DNA hybridization.Chem. Commun., 2008, (48): 6600-6602.
    [57]
    Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 2003, 31(13): 3406-3415.
    [58]
    Markegard C B, Gallivan C P, Cheng D D, et al. Effects of concentration and temperature on DNA hybridization by two closely related sequences via large-scale coarse-grained simulations. J. Phys. Chem. B, 2016, 120(32): 7795-7806.
    [59]
    Markegard C B, Fu I W, Reddy K A, et al. Coarse-grained simulation study of sequence effects on DNA hybridization in a concentrated environment. J. Phys. Chem. B, 2015, 119(5): 1823-1834.
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    [1]
    Jones M R, Seeman N C, Mirkin C A. Programmable materials and the nature of the DNA bond. Science, 2015, 347(6224): 1260901.
    [2]
    Zhang F, Nangreave J, Liu Y, et al. Structural DNA nanotechnology: state of the art and future perspective.J. Am. Chem. Soc., 2014, 136(32): 11198-11211.
    [3]
    Seeman N C. Structural DNA Nanotechnology. Cambridge:Cambridge University Press, 2016.
    [4]
    Lin Q Y, Mason J A, Li Z Y, et al. Building superlattices from individual nanoparticles via template-confined DNA-mediated assembly. Science,2018, 359(6376): 669-672.
    [5]
    Young K L, Ross M B,Blaber M G, et al. Using DNA to design plasmonic metamaterials with tunable optical properties. Adv.Mater.,2014, 26(4): 653-659.
    [6]
    Fan J A, Wu C, Bao K, et al. Self-assembled plasmonic nanoparticle clusters.Science, 2010, 328(5982): 1135-1138.
    [7]
    Lu C H, Willner B, Willner I. DNA nanotechnology: From sensing and DNA machines to drug-delivery systems. ACS Nano, 2013, 7(10): 8320-8332.
    [8]
    Keyser U F.Enhancing nanopore sensing with DNA nanotechnology. Nat. Nanotech., 2016, 11(2): 106-108.
    [9]
    Pilo-Pais M, Acuna G P,Tinnefeld P, et al. Sculpting light by arranging optical components with DNA nanostructures. MRS Bull., 2017, 42: 936-942.
    [10]
    Zhou C, Duan X Y, Liu N. DNA-nanotechnology-enabled chiral plasmonics: From static to dynamic. Acc. Chem. Res., 2017, 50(12): 2906-2914.
    [11]
    Han X G, Zhou Z H, Yang F, et al. Catch and release: DNA tweezers that can capture, hold and release an object under control. J. Am. Chem. Soc., 2008, 130: 14414-14415.
    [12]
    Zhang C, Macfarlane R J, Young K L, et al. A general approach to DNA-programmable atom equivalents.Nat. Mater., 2013, 12(8): 741-746.
    [13]
    Zhang Y, Lu F, Yager K G, et al. A general strategy for the DNA-mediated self-assembly of functional nanoparticles into heterogeneous systems.Nat. Nanotechnol., 2013, 8(11): 865-872.
    [14]
    Chen G L, Wang S, Song L, et al. Pt supraparticles with controllable DNA valences for programmed nanoassembly. Chem. Commun., 2017, 53(70): 9773-9776.
    [15]
    Zheng Y Q, Li Y L, Deng Z X. Silver nanoparticle-DNA bionanoconjugates bearing a discrete number of DNA ligands.Chem. Commun., 2012, 48(49): 6160-6162.
    [16]
    Li Y L, Zheng Y Q, Gong M, et al. Pt nanoparticles decorated with a discrete number of DNA molecules for programmable assembly of Au-Pt bimetallic superstructures.Chem. Commun., 2012, 48(31): 3727-3729.
    [17]
    Wang H Q, Li Y L, Gong M, et al. Core solution:A strategy towards gold core/non-gold shell nanoparticles bearing strict DNA-valences for programmable nanoassembly. Chem. Sci., 2014, 5(3): 1015-1020.
    [18]
    Wang H Q, Deng Z X. Gel electrophoresis as a nanoseparation tool serving DNA nanotechnology. Chin. Chem. Lett., 2015, 26(12): 1435-1438.
    [19]
    Tikhomirov G, Hoogland S, Lee P E, et al. DNA-based programming of quantum dot valency, self-assembly and luminescence.Nat. Nanotechnol., 2011, 6(8): 485-490.
    [20]
    Pal S, Sharma J, Yan H, et al. Stable silver nanoparticle-DNA conjugates for directed self-assembly of core-satellite silver-gold nanoclusters. Chem. Commun., 2009(40): 6059-6061.
    [21]
    Zhang X, Servos M R, Liu J. Fast pH-assisted functionalization of silver nanoparticles with monothiolated DNA.Chem. Commun., 2012, 48(81): 10114-10116.
    [22]
    Deng Z, Pal S, Samanta A, et al. DNA functionalization of colloidal II-VI semiconductor nanowires for multiplex nanoheterostructures. Chem. Sci., 2013, 4(5): 2234-2240.
    [23]
    Li L, Wu P, Hwang K, et al. An exceptionally simple strategy for DNA-functionalized up-conversion nanoparticles as biocompatible agents for nanoassembly, DNA delivery, and imaging.J. Am. Chem. Soc., 2013, 135(7): 2411-2414.
    [24]
    Song L, Deng Z X. Valency control and functional synergy in DNA-bonded nanomolecules.ChemNanoMat, 2017, 3(10): 698-712.
    [25]
    Hao Y, Li Y J, Song L, et al. Flash synthesis of spherical nucleic acids with record DNA density. J. Am. Chem. Soc., 2021, 143(8): 3065-3069.
    [26]
    Liao Y H, Lin C H, Cheng C Y, et al. Monovalent and oriented labeling of gold nanoprobes for the high-resolution tracking of a single-membrane molecule. ACSNano, 2019, 13(10): 10918-10928.
    [27]
    Howarth M, Liu W H, Puthenveetil S, et al. Monovalent, reduced-size quantum dots for imaging receptors on living cells. Nat.Methods, 2008, 5(5): 397-399.
    [28]
    Takashimaa A, Oishi M. Kinetic study of DNA hybridization on DNA-modified gold nanoparticles with engineered nano-interfaces. RSC Adv., 2015, 5(93): 76014-76018.
    [29]
    Leunissen M E, Dreyfus R, Sha R, et al. Quantitative study of the association thermodynamics and kinetics of DNA-coated particles for different functionalization schemes.J. Am. Chem. Soc., 2010, 132(6): 1903-1913.
    [30]
    Chen C, Wang W, Ge J, et al. Kinetics and thermodynamics of DNA hybridization on gold nanoparticles.Nucleic Acids Res., 2009, 37(11): 3756-3765.
    [31]
    Elghanian R, Storhoff J J, Mucic R C, et al.Selective colorimetric detection of polynucleotides based on the distance-dependent optical properties of gold nanoparticles.Science, 1997, 277(5329): 1078-1081.
    [32]
    Park S, Brown K A, Hamad-Schifferli K.Changes in oligonucleotide conformation on nanoparticle surfaces by modification with mercaptohexanol. Nano Lett., 2004, 4(10): 1925-1929.
    [33]
    Liu B W, Wu P, Huang Z C, et al. Bromide as arobust backfiller on gold for precise control of DNA conformation and high stability of spherical nucleic acids. J. Am. Chem. Soc., 2018, 140(13): 4499-4502.
    [34]
    Maye M M, Nykypanchuk D, van der Lelie D, et al.A simple method for kinetic control of DNA-induced nanoparticle assembly. J. Am. Chem. Soc., 2006, 128(43): 14020-14021.
    [35]
    Prigodich A E, Lee O S, Daniel W L, et al.Tailoring DNA structure to increase target hybridization kinetics on surfaces. J. Am. Chem. Soc., 2010, 132(31): 10638-10641.
    [36]
    Li Y L, Han X G, Deng Z X. Grafting SWNTs with highly hybridizable DNA sequences: Potential building blocks for DNA-programmed material assembly. Angew. Chem. Int. Ed., 2007, 46(39): 7481-7484.
    [37]
    Maune H T, Han S P, Barish R D, et al.Self-assembly of carbon nanotubes into two-dimensional geometries using DNA origami templates. Nat. Nanotech., 2010, 5(1): 61-66.
    [38]
    Sun W, Shen J, Zhao Z, et al. Precise pitch-scaling of carbon nanotube arrays within three-dimensional DNA nanotrenches. Science, 2020, 368(6493): 874-877.
    [39]
    Zhang J X, Fang J X, Duan W, et al. Predicting DNA hybridization kinetics from sequence. Nat. Chem., 2018, 10(11): 91-98.
    [40]
    Esashika K, Saiki T.DNA Hybridization assay using gold nanoparticles and electrophoresis separation provides 1 pM sensitivity. Bioconjug. Chem., 2018, 29(1): 182-189.
    [41]
    Marimuthu K,Chakrabarti R. Sequence-dependent theory of oligonucleotide hybridization kinetics.J. Chem. Phys., 2014, 140(17): 175104.
    [42]
    Sorgenfrei S, Chiu C Y, Gonzalez Jr R L, et al. Label-free field-effect-based single-molecule detection of DNA hybridization kinetics. Nat. Nanotechnol., 2011, 6(2): 126-132.
    [43]
    Yin Y D, Zhao X S. Kinetics and dynamics of DNA hybridization. Acc. Chem. Res., 2011, 44(1): 1172-1181.
    [44]
    Lee C Y, Nguyen P C, Grainger D W, et al. Structure and DNA hybridization properties of mixed nucleic acid/maleimide-ethylene glycol monolayers.Anal. Chem., 2007, 79(12): 4390-4400.
    [45]
    Erickson D, Li D Q, Krull U J. Modeling of DNA hybridization kinetics for spatially resolved biochips. Anal.Biochem., 2003, 317(2):186-200.
    [46]
    Okahata Y, Kawase M, Niikura K, et al. Kinetic measurements of DNA hybridization on an oligonucleotide-immobilized 27-MHz quartz crystal microbalance. Anal. Chem., 1998, 70(7): 1288-1296.
    [47]
    Schwille P, Oehlenschläger F, Walter N G. Quantitative hybridization kinetics of DNA probes to RNA in solution followed by diffusional fluorescence correlation analysis.Biochemistry, 1996, 35(31): 10182-10193.
    [48]
    Mazumder A, Majlessi M, Becker M M. A high throughput method to investigate oligodeoxyribonucleotide hybridization kinetics and thermodynamics.Nucleic Acids Res., 1998, 26(8): 1996-2000.
    [49]
    Yao G B, Li J, Li Q, et al. Programming nanoparticle valence bonds with single-stranded DNA encoders. Nat. Mater., 2020, 19(7): 781-788.
    [50]
    Zanchet D, Micheel C M, Parak W J, et al.Electrophoretic isolation of discrete Au nanocrystal/DNA conjugates. Nano Lett., 2001, 1(1): 32-35.
    [51]
    Claridge S A, Liang H W, Basu S R, et al.Isolation of discrete nanoparticle-DNA conjugates for plasmonic applications. Nano Lett., 2008, 8(4): 1202-1206.
    [52]
    Kushon S A, Jordan J P, Seifert J L, et al.Effect of secondary structure on the thermodynamics and kinetics of PNA hybridization to DNA hairpins.J. Am. Chem. Soc., 2001, 123(44): 10805-10813.
    [53]
    Riccelli P V, Merante F, Leung K T, et al. Hybridization of single-stranded DNA targets to immobilized complementary DNA probes: comparison of hairpin versus linear capture probes. Nucleic Acids Res., 2001, 29(4): 996-1004.
    [54]
    Gao Y, Wolf L K, Georgiadis R M. Secondary structure effects on DNA hybridization kinetics:A solution versus surface comparison.Nucleic Acids Res., 2006, 34(11): 3370-3377.
    [55]
    Alivisatos A P, Johnsson K P, Peng X G, et al.Organization of 'nanocrystal molecules' using DNA. Nature, 1996, 382: 609-611.
    [56]
    Yuan B F, Zhuang X Y, Hao Y H, et al. Kinetics of base stacking-aided DNA hybridization.Chem. Commun., 2008, (48): 6600-6602.
    [57]
    Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 2003, 31(13): 3406-3415.
    [58]
    Markegard C B, Gallivan C P, Cheng D D, et al. Effects of concentration and temperature on DNA hybridization by two closely related sequences via large-scale coarse-grained simulations. J. Phys. Chem. B, 2016, 120(32): 7795-7806.
    [59]
    Markegard C B, Fu I W, Reddy K A, et al. Coarse-grained simulation study of sequence effects on DNA hybridization in a concentrated environment. J. Phys. Chem. B, 2015, 119(5): 1823-1834.
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