Helix Opening in Deoxyribonucleic Acid from a Proton Nuclear Magnetic Resonance Study of Imino and Amino Protons in D(CG)3

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 1984 Nov 12

PMID 6504700

Citations 7

Authors

G V Fazakerley

G A van der Marel

J H VAN Boom

W GUSCHLBAUER

Affiliations

Soon will be listed here.

Abstract

All exchangeable protons in a short DNA helix, d(CG)3 sodium salt, have been studied by proton nuclear magnetic resonance. The cytidine and guanosine amino protons have been assigned for the first time. As a function of temperature the cytidine amino protons and the imino protons behave very similarly, their relaxation is dominated by exchange with solvent above 30 degrees C. The guanosine amino protons, however, show that helix opening can only be described by a multistate model. The most rapid process observed is probably a twist about the helix axis which lengthens or breaks the guanosine amino hydrogen bond and allows rotation of the amino group. The second fastest process is a scissor opening into the major groove which gives rise to solvent exchange with the imino and cytidine amino protons. The slowest process observed is the complete base pair opening in which the guanosine amino protons also exchange with solvent. For the ammonium salt of the oligonucleotide, a specific ammonium ion complex is observed which at low temperature may catalyze exchange of the guanosine amino protons with the protons of the ammonium ion, but retards exchange with solvent. The complex appears to be specific for the sequence d(CpG).

Citing Articles

NMR and CD studies on an oligonucleotide containing N4-methylcytosine.

Fazakerley G, Kraszewski A, Teoule R, GUSCHLBAUER W Nucleic Acids Res. 1987; 15(5):2191-201.

PMID: 3562225 PMC: 340626. DOI: 10.1093/nar/15.5.2191.

Base pairing and mutagenesis: observation of a protonated base pair between 2-aminopurine and cytosine in an oligonucleotide by proton NMR.

Sowers L, Fazakerley G, Eritja R, Kaplan B, Goodman M Proc Natl Acad Sci U S A. 1986; 83(15):5434-8.

PMID: 3461441 PMC: 386301. DOI: 10.1073/pnas.83.15.5434.

Comparison of the conformation of an oligonucleotide containing a central G-T base pair with the non-mismatch sequence by proton NMR.

Quignard E, Fazakerley G, van der Marel G, VAN Boom J, GUSCHLBAUER W Nucleic Acids Res. 1987; 15(8):3397-409.

PMID: 3033602 PMC: 340737. DOI: 10.1093/nar/15.8.3397.

Structures of mismatched base pairs in DNA and their recognition by the Escherichia coli mismatch repair system.

Fazakerley G, Quignard E, Woisard A, GUSCHLBAUER W, van der Marel G, VAN Boom J EMBO J. 1986; 5(13):3697-703.

PMID: 2951250 PMC: 1167413. DOI: 10.1002/j.1460-2075.1986.tb04702.x.

An NMR structural study of deaminated base pairs in DNA.

Carbonnaux C, Fazakerley G, Sowers L Nucleic Acids Res. 1990; 18(14):4075-81.

PMID: 2377453 PMC: 331162. DOI: 10.1093/nar/18.14.4075.

References

Raszka M, Kaplan N . Association by hydrogen bonding of mononucleotides in aqueous solution. Proc Natl Acad Sci U S A. 1972; 69(8):2025-9. PMC: 426860. DOI: 10.1073/pnas.69.8.2025. View

Wong Y, Kearns D, Reid B, Shulman R . Investigation of exchangeable protons and the extent of base pairings in yeast phenylalanine transfer RNA by high resolution nuclear magnetic resonance. J Mol Biol. 1972; 72(3):725-40. DOI: 10.1016/0022-2836(72)90187-8. View

McConnell B, Seawell P . Amino protons of cytosine. Chemical exchange, rotational exchange, and salt-induced proton magnetic resonance chemical shifts of aqueous 2',3'-cyclic cytidine monophosphate. Biochemistry. 1973; 12(22):4426-34. DOI: 10.1021/bi00746a020. View

Raszka M . Mononucleotides in aqueous solution: proton magnetic resonance studies of amino groups. Biochemistry. 1974; 13(22):4616-22. DOI: 10.1021/bi00719a023. View

Hilbers C, Patel D . Proton nuclear magnetic resonance investigations of the nucleation and propagation reactions associated with the helix-coil transition of d-ApTpGpCpApT in H2O solution. Biochemistry. 1975; 14(12):2656-60. DOI: 10.1021/bi00683a015. View

Kan L, Borer P, Tso P . Conformation and interaction of short nucleic acid double-stranded helices. II. Proton magnetic resonance studies on the hydrogen-bonded NH-N protons of ribosyl ApApGpCpUpU helix. Biochemistry. 1975; 14(22):4864-9. DOI: 10.1021/bi00693a013. View

Patel D . d-CpCpGpG and d-GpGpCpC self-complementary duplexes: Nmr studies of the helix-coil transition. Biopolymers. 1977; 16(8):1635-56. DOI: 10.1002/bip.1977.360160804. View

Mandal C, Kallenbach N, Englander S . Base-pair opening and closing reactions in the double helix. A stopped-flow hydrogen exchange study in poly(rA).poly(rU). J Mol Biol. 1979; 135(2):391-411. DOI: 10.1016/0022-2836(79)90443-1. View

Early T, Kearns D, Hillen W, Wells R . A 300- and 600-MHz proton nuclear magnetic resonance investigation of a 12 base pair deoxyribonucleic acid restriction fragment: relaxation behavior of the low-field resonances in water. Biochemistry. 1981; 20(13):3756-64. DOI: 10.1021/bi00516a014. View

10.

Early T, Kearns D, Hillen W, Wells R . A 300-MHz proton nuclear magnetic resonance investigation of deoxyribonucleic acid restriction fragments: dynamic properties. Biochemistry. 1981; 20(13):3764-9. DOI: 10.1021/bi00516a015. View

11.

Pardi A, Morden K, Patel D, Tinoco Jr I . Kinetics for exchange of imino protons in the d(C-G-C-G-A-A-T-T-C-G-C-G) double helix and in two similar helices that contain a G . T base pair, d(C-G-T-G-A-A-T-T-C-G-C-G), and an extra adenine, d(C-G-C-A-G-A-A-T-T-C-G-C-G). Biochemistry. 1982; 21(25):6567-74. DOI: 10.1021/bi00268a038. View

12.

Kopka M, Fratini A, Drew H, DICKERSON R . Ordered water structure around a B-DNA dodecamer. A quantitative study. J Mol Biol. 1983; 163(1):129-46. DOI: 10.1016/0022-2836(83)90033-5. View

13.

Feigon J, Wright J, Denny W, Leupin W, Kearns D . Application of multiple-pulse H-NMR techniques to the study of two synthetic DNA decamers. Cold Spring Harb Symp Quant Biol. 1983; 47 Pt 1:207-17. DOI: 10.1101/sqb.1983.047.01.026. View

14.

Frechet D, Cheng D, Kan L, Tso P . Nuclear Overhauser effect as a tool for the complete assignment of nonexchangeable proton resonances in short deoxyribonucleic acid helices. Biochemistry. 1983; 22(22):5194-200. DOI: 10.1021/bi00291a020. View

15.

Feigon J, Denny W, Leupin W, Kearns D . Proton nuclear magnetic resonance investigation of the conformation and dynamics in the synthetic deoxyribonucleic acid decamers d(ATATCGATAT) and d(ATATGCATAT). Biochemistry. 1983; 22(25):5930-42. DOI: 10.1021/bi00294a037. View

16.

Clore G, Gronenborn A . A nuclear-Overhauser-enhancement study of the solution structure of a double-stranded DNA undecamer comprising a portion of the specific target site for the cyclic-AMP-receptor protein in the gal operon. Sequential resonance assignment. Eur J Biochem. 1984; 141(1):119-29. DOI: 10.1111/j.1432-1033.1984.tb08166.x. View

17.

McConnell B . The amino 1H resonances of oligonucleotide helices: d(CGCG). J Biomol Struct Dyn. 1984; 1(6):1407-21. DOI: 10.1080/07391102.1984.10507528. View