Backbone-free Duplex-stacked Monomer Nucleic Acids Exhibiting Watson-Crick Selectivity

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2018 Jul 4

PMID 29967169

Citations 15

Authors

Gregory P Smith

Tommaso P Fraccia

Marco Todisco

Giuliano Zanchetta

Chenhui Zhu

Emily Hayden

Tommaso Bellini

Noel A Clark

Affiliations

Soon will be listed here.

Abstract

We demonstrate that nucleic acid (NA) mononucleotide triphosphates (dNTPs and rNTPs), at sufficiently high concentration and low temperature in aqueous solution, can exhibit a phase transition in which chromonic columnar liquid crystal ordering spontaneously appears. Remarkably, this polymer-free state exhibits, in a self-assembly of NA monomers, the key structural elements of biological nucleic acids, including: long-ranged duplex stacking of base pairs, complementarity-dependent partitioning of molecules, and Watson-Crick selectivity, such that, among all solutions of adenosine, cytosine, guanine, and thymine NTPs and their binary mixtures, duplex columnar ordering is most stable in the A-T and C-G combinations.

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References

Vesnaver G, Breslauer K . The contribution of DNA single-stranded order to the thermodynamics of duplex formation. Proc Natl Acad Sci U S A. 1991; 88(9):3569-73. PMC: 51493. DOI: 10.1073/pnas.88.9.3569. View

Gruenwedel D . Salt effects on the denaturation of DNA. IV. A calorimetric study of the helix-coil conversion of the alternating copolymer poly[d(A-T)]. Biochim Biophys Acta. 1975; 395(3):246-57. DOI: 10.1016/0005-2787(75)90195-1. View

Mariani P, Spinozzi F, Federiconi F, Amenitsch H, Spindler L, Drevensek-Olenik I . Small angle X-ray scattering analysis of deoxyguanosine 5'-monophosphate self-assembing in solution: nucleation and growth of G-quadruplexes. J Phys Chem B. 2009; 113(22):7934-44. DOI: 10.1021/jp809734p. View

HOWARD F, Frazier J, Singer M, Miles H . Helix formation between polyribonucleotides and purines, purine nucleosides and nucleotides. II. J Mol Biol. 1966; 16(2):415-39. DOI: 10.1016/s0022-2836(66)80183-3. View

Schweizer M, BROOM A, Tso P, Hollis D . Studies of inter- and intramolecular interaction in mononucleotides by proton magnetic resonance. J Am Chem Soc. 1968; 90(4):1042-55. DOI: 10.1021/ja01006a035. View

Ertem G, Ferris J . Template-directed synthesis using the heterogeneous templates produced by montmorillonite catalysis. A possible bridge between the prebiotic and RNA worlds. J Am Chem Soc. 1997; 119(31):7197-201. DOI: 10.1021/ja970422h. View

Tso P . The hydrophobic-stacking properties of the bases in nucleic acids. Ann N Y Acad Sci. 1969; 153(3):785-804. DOI: 10.1111/j.1749-6632.1969.tb11789.x. View

Fraccia T, Smith G, Zanchetta G, Paraboschi E, Yi Y, Yi Y . Abiotic ligation of DNA oligomers templated by their liquid crystal ordering. Nat Commun. 2015; 6:6424. PMC: 4366493. DOI: 10.1038/ncomms7424. View

Fraccia T, Zanchetta G, Rimoldi V, Clark N, Bellini T . Evidence of liquid crystal-assisted abiotic ligation of nucleic acids. Orig Life Evol Biosph. 2015; 45(1-2):51-68. DOI: 10.1007/s11084-015-9438-1. View

10.

Felsenfeld G, Miles H . The physical and chemical properties of nucleic acids. Annu Rev Biochem. 1967; 36:407-48. DOI: 10.1146/annurev.bi.36.070167.002203. View

11.

Watson J, Crick F . Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature. 1953; 171(4356):737-8. DOI: 10.1038/171737a0. View

12.

Zanchetta G, Nakata M, Buscaglia M, Bellini T, Clark N . Phase separation and liquid crystallization of complementary sequences in mixtures of nanoDNA oligomers. Proc Natl Acad Sci U S A. 2008; 105(4):1111-7. PMC: 2234099. DOI: 10.1073/pnas.0711319105. View

13.

Kilchherr F, Wachauf C, Pelz B, Rief M, Zacharias M, Dietz H . Single-molecule dissection of stacking forces in DNA. Science. 2016; 353(6304). DOI: 10.1126/science.aaf5508. View

14.

Davis J . G-quartets 40 years later: from 5'-GMP to molecular biology and supramolecular chemistry. Angew Chem Int Ed Engl. 2004; 43(6):668-98. DOI: 10.1002/anie.200300589. View

15.

Joyce G . The antiquity of RNA-based evolution. Nature. 2002; 418(6894):214-21. DOI: 10.1038/418214a. View

16.

Becker S, Thoma I, Deutsch A, Gehrke T, Mayer P, Zipse H . A high-yielding, strictly regioselective prebiotic purine nucleoside formation pathway. Science. 2016; 352(6287):833-6. DOI: 10.1126/science.aad2808. View

17.

Riley M, Maling B . Physical and chemical characterization of two- and three-stranded adenine-thymine and adenine-uracil homopolymer complexes. J Mol Biol. 1966; 20(2):359-89. DOI: 10.1016/0022-2836(66)90069-6. View

18.

Spindler L, Drevensek-Olenik I, copic M, Cerar J, Skerjanc J, Mariani P . Dynamic light scattering and 31P NMR study of the self-assembly of deoxyguanosine 5'-monophosphate: the effect of added salt. Eur Phys J E Soft Matter. 2004; 13(1):27-33. DOI: 10.1140/epje/e2004-00037-0. View

19.

Yang C, Kim E, Pak Y . Free energy landscape and transition pathways from Watson-Crick to Hoogsteen base pairing in free duplex DNA. Nucleic Acids Res. 2015; 43(16):7769-78. PMC: 4652778. DOI: 10.1093/nar/gkv796. View

20.

Wilkins M, STOKES A, Wilson H . Molecular structure of deoxypentose nucleic acids. Nature. 1953; 171(4356):738-40. DOI: 10.1038/171738a0. View