Hydration of the RNA Duplex R(CGCAAAUUUGCG)2 Determined by NMR

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 1996 Oct 1

PMID 8871546

Citations 14

Authors

M R Conte

G L Conn

T Brown

A N Lane

Affiliations

Soon will be listed here.

Abstract

The so-called spine of hydration in the minor groove of AnTn tracts in DNA is thought to stabilise the structure, and kinetically bound water detected in the minor groove of such DNA species by NMR has been attributed to a narrow minor groove [Liepinsh, E., Leupin, W. and Otting, G. (1994) Nucleic Acids Res. 22, 2249-2254]. We report here an NMR study of hydration of an RNA dodecamer which has a wide, shallow minor groove. Complete assignments of exchangeable protons, and a large number of non-exchangeable protons in r(CGCAAAUUUGCG)2 have been obtained. In addition, ribose C2'-OH resonances have been detected, which are probably involved in hydrogen bonds. Hydration at different sites in the dodecamer has been measured using ROESY and NOESY experiments at 11.75 and 14.1 T. Base protons in both the major and minor grooves are in contact with water, with effective correlation times for the interaction of approximately 0.5 ns, indicating weak hydration, in contrast to the hydration of adenine C2H in the homologous DNA sequence. NOEs to H1' in the minor groove are consistent with hydration water present that is not observed in the analogous DNA sequence. Hydration kinetics in nucleic acids may be determined by chemical factors such as hydrogen-bonding more than by simple conformational factors such as groove width.

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References

Poppe L, van Halbeek H . NMR spectroscopy of hydroxyl protons in supercooled carbohydrates. Nat Struct Biol. 1994; 1(4):215-6. DOI: 10.1038/nsb0494-215. View

Prive G, Heinemann U, Chandrasegaran S, Kan L, Kopka M, DICKERSON R . Helix geometry, hydration, and G.A mismatch in a B-DNA decamer. Science. 1987; 238(4826):498-504. DOI: 10.1126/science.3310237. View

Ebel S, Brown T, Lane A . Thermodynamic stability and solution conformation of tandem G.A mismatches in RNA and RNA.DNA hybrid duplexes. Eur J Biochem. 1994; 220(3):703-15. DOI: 10.1111/j.1432-1033.1994.tb18671.x. View

Wang S, Kool E . Origins of the large differences in stability of DNA and RNA helices: C-5 methyl and 2'-hydroxyl effects. Biochemistry. 1995; 34(12):4125-32. DOI: 10.1021/bi00012a031. View

Jenkins T, Lane A, Neidle S, Brown D . NMR and molecular modeling studies of the interaction of berenil and pentamidine with d(CGCAAATTTGCG)2. Eur J Biochem. 1993; 213(3):1175-84. DOI: 10.1111/j.1432-1033.1993.tb17868.x. View

Drew H, DICKERSON R . Structure of a B-DNA dodecamer. III. Geometry of hydration. J Mol Biol. 1981; 151(3):535-56. DOI: 10.1016/0022-2836(81)90009-7. View

Egli M, Portmann S, Usman N . RNA hydration: a detailed look. Biochemistry. 1996; 35(26):8489-94. DOI: 10.1021/bi9607214. View

Chalikian T, Plum G, Sarvazyan A, Breslauer K . Influence of drug binding on DNA hydration: acoustic and densimetric characterizations of netropsin binding to the poly(dAdT).poly(dAdT) and poly(dA).poly(dT) duplexes and the poly(dT).poly(dA).poly(dT) triplex at 25 degrees C. Biochemistry. 1994; 33(29):8629-40. DOI: 10.1021/bi00195a003. View

Liepinsh E, Otting G, Wuthrich K . NMR observation of individual molecules of hydration water bound to DNA duplexes: direct evidence for a spine of hydration water present in aqueous solution. Nucleic Acids Res. 1992; 20(24):6549-53. PMC: 334570. DOI: 10.1093/nar/20.24.6549. View

10.

Piotto M, Saudek V, SKLENAR V . Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR. 1992; 2(6):661-5. DOI: 10.1007/BF02192855. View

11.

Wahl M, Ban C, Sekharudu C, Ramakrishnan B, Sundaralingam M . Structure of the purine-pyrimidine alternating RNA double helix, r(GUAUAUA)d(C), with a 3'-terminal deoxy residue. Acta Crystallogr D Biol Crystallogr. 1996; 52(Pt 4):655-67. DOI: 10.1107/S0907444996000248. View

12.

Otting G, Liepinsh E, Wuthrich K . Protein hydration in aqueous solution. Science. 1991; 254(5034):974-80. DOI: 10.1126/science.1948083. View

13.

Lane A . The determination of the conformational properties of nucleic acids in solution from NMR data. Biochim Biophys Acta. 1990; 1049(2):189-204. DOI: 10.1016/0167-4781(90)90040-9. View

14.

Edwards K, Brown D, Spink N, Skelly J, Neidle S . Molecular structure of the B-DNA dodecamer d(CGCAAATTTGCG)2. An examination of propeller twist and minor-groove water structure at 2.2 A resolution. J Mol Biol. 1992; 226(4):1161-73. DOI: 10.1016/0022-2836(92)91059-x. View

15.

Leroy J, Broseta D, Gueron M . Proton exchange and base-pair kinetics of poly(rA).poly(rU) and poly(rI).poly(rC). J Mol Biol. 1985; 184(1):165-78. DOI: 10.1016/0022-2836(85)90050-6. View

16.

Leonard G, Ebel S, Lough D, Brown T, Hunter W . Crystal and molecular structure of r(CGCGAAUUAGCG): an RNA duplex containing two G(anti).A(anti) base pairs. Structure. 1994; 2(6):483-94. DOI: 10.1016/S0969-2126(00)00049-6. View

17.

Radhakrishnan I, Patel D . Hydration sites in purine.purine.pyrimidine and pyrimidine.purine.pyrimidine DNA triplexes in aqueous solution. Structure. 1994; 2(5):395-405. DOI: 10.1016/s0969-2126(00)00041-1. View

18.

Fawthrop S, Yang J, Fisher J . Structural and dynamic studies of a non-self-complementary dodecamer DNA duplex. Nucleic Acids Res. 1993; 21(21):4860-6. PMC: 311397. DOI: 10.1093/nar/21.21.4860. View

19.

Liepinsh E, Leupin W, Otting G . Hydration of DNA in aqueous solution: NMR evidence for a kinetic destabilization of the minor groove hydration of d-(TTAA)2 versus d-(AATT)2 segments. Nucleic Acids Res. 1994; 22(12):2249-54. PMC: 523681. DOI: 10.1093/nar/22.12.2249. View