Journal Home > Volume 16 , Issue 3

The self-assembly of DNA provides an attractive approach to understanding structural formation mechanism in living organisms and to assisting applications in materials chemistry. Herein, we investigated the effect of metal ions on chiral self-assembly of DNA through the synthesis of chiral mesostructured silica via self-assembly of metal ions, DNA, and silica source. 31 types of multivalent cationic metal ions were found to induce formation of chiral impeller-like DNA-silica complexes due to the chiral stacking of DNA. The strength of the interaction between the metal ion and phosphate group of DNA was speculated for the chiral stacking of DNA due to close distance of adjacent DNA to assure mutual recognition. Theoretical calculations indicated that chiral packing of DNA depends on the stability of the bridging phosphate-metal ion-phosphate bonds of DNA based on electron delocalization in d-orbital conjugation of metal ions.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

Insight on metal ions inducing chiral self-assembly of DNA in silica mineralization

Show Author's information Arepati Azhati1Lu Han2Zhibei Qu3( )Zhouhong Ren4Xi Liu4( )Liwei Chen4Shunai Che1,2( )
School of Chemistry and Chemical Engineering, Frontiers Science Center for Transformative Molecules, State Key Laboratory of Metal Matrix Composites, Shanghai Key Laboratory for Molecular Engineering of Chiral Drugs, Shanghai Jiao Tong University, Shanghai 200240, China
School of Chemical Science and Engineering, Tongji University, Shanghai 200092, China
Department of Medicinal Chemistry, School of Pharmacy, Fudan University, Shanghai 201203, China
School of Chemical Science and Engineering, In-situ Center for Physical Sciences, Frontiers Science Center for Transformative Molecules, Shanghai Jiao Tong University, Shanghai 200240, China

Abstract

The self-assembly of DNA provides an attractive approach to understanding structural formation mechanism in living organisms and to assisting applications in materials chemistry. Herein, we investigated the effect of metal ions on chiral self-assembly of DNA through the synthesis of chiral mesostructured silica via self-assembly of metal ions, DNA, and silica source. 31 types of multivalent cationic metal ions were found to induce formation of chiral impeller-like DNA-silica complexes due to the chiral stacking of DNA. The strength of the interaction between the metal ion and phosphate group of DNA was speculated for the chiral stacking of DNA due to close distance of adjacent DNA to assure mutual recognition. Theoretical calculations indicated that chiral packing of DNA depends on the stability of the bridging phosphate-metal ion-phosphate bonds of DNA based on electron delocalization in d-orbital conjugation of metal ions.

Keywords: silica, chirality, DNA, DNA-metal ions interaction, ultra-small metal-nanoparticle

References(39)

[1]

Lakes, R. Materials with structural hierarchy. Nature 1993, 361, 511–515.

[2]

Reich, Z.; Schramm, O.; Brumfeld, V.; Minsky, A. Chiral discrimination in DNA–peptide interactions involving chiral DNA mesophases:  A geometric analysis. J. Am. Chem. Soc. 1996, 118, 6345–6349.

[3]

Reich, Z.; Wachtel, E. J.; Minsky, A. Liquid-crystalline mesophases of plasmid DNA in bacteria. Science 1994, 264, 1460–1463.

[4]

Strey, H. H.; Podgornik, R.; Rau, D. C.; Parsegian, V. A. DNA–DNA interactions. Curr. Opin. Struct. Biol. 1998, 8, 309–313.

[5]

Bustamante, C.; Samori, B.; Builes, E. Daunomycin inverts the long-range chirality of DNA condensed states. Biochemistry 1991, 30, 5661–5666.

[6]

Minsky, A. The chiral code: From DNA primary structures to quaternary assemblies. Chirality 1998, 10, 405–414.

[7]

Berti, L.; Burley, G. A. Nucleic acid and nucleotide-mediated synthesis of inorganic nanoparticles. Nat. Nanotechnol. 2008, 3, 81–87.

[8]

Tanaka, K.; Yamada, Y.; Shionoya, M. Formation of silver(i)-mediated DNA duplex and triplex through an alternative base pair of pyridine nucleobases. J. Am. Chem. Soc. 2002, 124, 8802–8803.

[9]
Theophanides, T.; Anastassopoulou, J.; Demunno, G. Metal–DNA interactions. In Metal–ligand interactions. Russo, N. ; Salahub, D. R.; Witko, M., Eds.; Springer: Dordrecht, 2003; pp 285–300.
DOI
[10]

Sigel, H.; Griesser, R. Nucleoside 5′-triphosphates: Self-association, acid-base, and metal ion-binding properties in solution. Chem. Soc. Rev. 2005, 34, 875–900.

[11]

Liu, B.; Han, L.; Che, S. A. Formation of enantiomeric impeller-like helical architectures by DNA self-assembly and silica mineralization. Angew. Chem., Int. Ed. 2012, 51, 923–927.

[12]

Cao, Y. Y.; Kao, K. C.; Mou, C. Y.; Han, L.; Che, S. A. Oriented chiral DNA-silica film guided by a natural mica substrate. Angew. Chem. 2016, 128, 2077–2081.

[13]

Cao, Y. Y.; Che, S. A. Optically active chiral DNA-silica hybrid free-standing films. Chem. Mater. 2015, 27, 7844–7851.

[14]

Liu, B.; Han, L.; Duan, Y. Y.; Cao, Y. Y.; Feng, J.; Yao, Y.; Che, S. A. Growth of optically active chiral inorganic films through DNA self-assembly and silica mineralisation. Sci. Rep. 2014, 4, 4866.

[15]

Liu, B.; Han, L.; Che, S. A. Silica mineralisation of DNA chiral packing: Helicity control and formation mechanism of impeller-like DNA-silica helical architectures. J. Mater. Chem. B. 2013, 1, 2843–2850.

[16]

Cao, Y. Y.; Xie, J. J.; Liu, B.; Han, L.; Che, S. A. Synthesis and characterization of multi-helical DNA-silica fibers. Chem. Commun. 2013, 49, 1097–1099.

[17]

Liu, B.; Han, L.; Che, S. A. Formation of enantiomeric impeller-like helical architectures by DNA self-assembly and silica mineralization. Angew. Chem. 2012, 124, 947–951.

[18]

Várnai, P.; Timsit, Y. Differential stability of DNA crossovers in solution mediated by divalent cations. Nucleic Acids Res. 2010, 38, 4163–4172.

[19]

Timsit, Y.; Vilbois, E.; Moras, D. Base-pairing shift in the major groove of (CA)n tracts by B-DNA crystal structures. Nature 1991, 354, 167–170.

[20]

Cherstvy, A. G. DNA cholesteric phases: The role of DNA molecular chirality and DNA–DNA electrostatic interactions. J. Phys. Chem. B 2008, 112, 12585–12595.

[21]

Athanasiadou, D.; Carneiro, K. M. M. DNA nanostructures as templates for biomineralization. Nat. Rev. Chem. 2021, 5, 93–108.

[22]

Zhao, Y.; Dai, X. P.; Wang, F.; Zhang, X. L.; Fan, C. H.; Liu, X. G. Nanofabrication based on DNA nanotechnology. Nano Today 2019, 26, 123–148.

[23]

Winogradoff, D.; Li, P. Y.; Joshi, H.; Quednau, L.; Maffeo, C.; Aksimentiev, A. Chiral systems made from DNA. Adv. Sci. 2021, 8, 2003113.

[24]

Fan, J. C.; Kotov, N. A. Chiral nanoceramics. Adv. Mater. 2020, 32, 1906738.

[25]

Maestre, M. F.; Reich, C. Contribution of light scattering to the circular dichroism of deoxyribonucleic acid films, deoxyribonucleic acid-polylysine complexes, and deoxyribonucleic acid particles in ethanolic buffers. Biochemistry 1980, 19, 5214–5223.

[26]

Livolant, F.; Maestre, M. F. Circular dichroism microscopy of compact forms of DNA and chromatin in vivo and in vitro: Cholesteric liquid-crystalline phases of DNA and single dinoflagellate nuclei. Biochemistry 1988, 27, 3056–3068.

[27]

Jmdan, C. F.; Lerman, L. S.; Jun, J. H. V. Structure and circular dichroism of DNA in concentrated polymer solutions. Nat. New Biol. 1972, 236, 67–70.

[28]

Pittelkow, M.; Brock-Nannestad, T.; Moth-Poulsen, K.; Christensen, J. B. Chiral dendrimer encapsulated Pd and Rh nanoparticles. Chem. Commun. 2008, 2358–2360.

[29]
Kraut-Vass, A. Nist x-ray photoelectron spectroscopy database, version 4.1. NIST X-ray Photoelectron Spectroscopy Database 2000, Version 4. 1.
[30]

Bai, J.; Xu, G. R.; Xing, S. H.; Zeng, J. H.; Jiang, J. X.; Chen, Y. Hydrothermal synthesis and catalytic application of ultrathin rhodium nanosheet nanoassemblies. ACS Appl. Mater. Interfaces 2016, 8, 33635–33641.

[31]

Jin, L. Q.; Zhang, X.; Zhao, W. F.; Chen, S. Q.; Shi, Z. Q.; Wang, J. X.; Xie, Y.; Liang, F.; Zhao, C. S. General method for synthesizing transition-metal phosphide/N-doped carbon nanomaterials for hydrogen evolution. Langmuir 2019, 35, 9161–9168.

[32]

Wang, N.; Lin, R. Y.; Xue, M. Z.; Duan, Y. Y.; Che, S. A. Handedness inversion of chiral mesoporous silica: A diffuse-reflectance circular dichroism study. Chin. Chem. Lett. 2019, 30, 139–142.

[33]

Zanchetta, G.; Giavazzi, F.; Nakata, M.; Buscaglia, M.; Cerbino, R.; Clark, N. A.; Bellini, T. Right-handed double-helix ultrashort DNA yields chiral nematic phases with both right- and left-handed director twist. Proc. Natl. Acad. Sci. USA 2010, 107, 17497–17502.

[34]

Sarkar, S.; Maity, A.; Phukon, A. S.; Ghosh, S.; Chakrabarti, R. Salt induced structural collapse, swelling, and signature of aggregation of two ssDNA strands: Insights from molecular dynamics simulation. J. Phys. Chem. B 2019, 123, 47–56.

[35]

Qiu, X. Y.; Andresen, K.; Kwok, L. W.; Lamb, J. S.; Park, H. Y.; Pollack, L. Inter-DNA attraction mediated by divalent counterions. Phys. Rev. Lett. 2007, 99, 038104.

[36]

Saminathan, M.; Antony, T.; Shirahata, A.; Sigal, L. H.; Thomas, T.; Thomas, T. J. Ionic and structural specificity effects of natural and synthetic polyamines on the aggregation and resolubilization of single-, double-, and triple-stranded DNA. Biochemistry 1999, 38, 3821–3830.

[37]

Duguid, J. G.; Bloomfield, V. A. Aggregation of melted DNA by divalent metal ion-mediated cross-linking. Biophys. J. 1995, 69, 2642–2648.

[38]

Qu, Z. B.; Feng, W. J.; Wang, Y. C.; Romanenko, F.; Kotov, N. A. Diverse nanoassemblies of graphene quantum dots and their mineralogical counterparts. Angew. Chem., Int. Ed. 2020, 59, 8542–8551.

[39]

Qu, Z. B.; Zhou, X. G.; Zhang, M.; Shen, J. L.; Li, Q.; Xu, F.; Kotov, N.; Fan, C. H. Metal-bridged graphene-protein supraparticles for analog and digital nitric oxide sensing. Adv. Mater. 2021, 33, 2007900.

File
12274_2022_4460_MOESM1_ESM.pdf (7 MB)
Publication history
Copyright
Acknowledgements

Publication history

Received: 15 March 2022
Revised: 16 April 2022
Accepted: 20 April 2022
Published: 17 June 2022
Issue date: March 2023

Copyright

© Tsinghua University Press 2022

Acknowledgements

Acknowledgements

This work was supported by the National Key Research and Development Program of China (No. 2021YFA1200300, S. C., 2021YFA1500300, X. L.), the National Natural Science Foundation of China (No. 21931008, S. C., 22072090 X. L, 21991153 L. C.), and the science foundation of the Shanghai Municipal science and Technology Commission (No. 19JC1410300, S. C.).

Return