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The hydration of nucleic acid duplexes as assessed by a combination of volumetric and structural techniques.

Abstract：

:Using high precision densimetric and ultrasonic measurements, we have determined, at 25 degrees C, the apparent molar volumes PhiV and the apparent molar compressibilities PhiK(S) of four nucleic acid duplexes-namely, the DNA duplex, poly(dIdC)poly(dIdC); the RNA duplex, poly(rA)poly(rU); and the two DNA/RNA hybrid duplexes, poly(rA)poly(dT) and poly(dA)poly(rU). Using available fiber diffraction data on these duplexes, we have calculated the molecular volumes as well as the solvent-accessible surface areas of the constituent charged, polar, and nonpolar atomic groups. We found that the hydration properties of these nucleic acid duplexes do not correlate with the extent and the chemical nature of the solvent-exposed surfaces, thereby suggesting a more specific set of duplex-water interactions beyond general solvation effects. A comparative analysis of our volumetric data on the four duplexes, in conjunction with available structural information, suggests the following features of duplex hydration: (a) The four duplexes exhibit different degrees of hydration, in the order poly(dIdC)poly(dIdC) > poly(dGdC)poly(dGdC) > poly(dAdT)poly(dAdT) approximately poly(dA)poly(dT). (b) Repetitive AT and IC sequences within a duplex are solvated beyond general effects by a spine of hydration in the minor groove, with this sequence-specific water network involving about 8 additional water molecules from the second and, perhaps, even the third hydration layers. (c) Repetitive GC and IC sequences within a duplex are solvated beyond general effects by a "patch of hydration" in the major groove, with this water network involving about 13 additional water molecules from the second and, perhaps, even the third hydration layers. (d) Random sequence, polymeric DNA duplexes, which statistically lack extended regions of repetitive AT, GC, or IC sequences, do not experience such specific enhancements of hydration. Consequently, consistent with our previous observations (T. V. Chalikian, A. P. Sarvazyan, G. E. Plum, and K. J. Breslauer, Biochemistry, 1994, Vol. 33, pp. 2394-2401), duplexes with approximately 50% AT content exhibit the weakest hydration, while an increase or decrease from this AT content causes enhancement of hydration, either due to stronger hydration of the minor groove (an increase in AT content) or due to stronger hydration of the major groove (an increase in GC content). (e) In dilute aqueous solutions, a B-DNA duplex is more hydrated than an A-DNA duplex, a volumetric-based conclusion that is in agreement with previous results obtained on crystals, fibers, and DNA solutions in organic solvent-water mixtures. (f) the A-like, RNA duplex poly(rA)poly(rU) and the structurally similar A-like, hybrid duplex poly(rA)poly(dT), exhibit similar hydration properties, while the structurally distinct A-like, hybrid duplex poly(rA)poly(dT) and non-A-like, hybrid duplex poly(dA)poly(rU) exhibit differential hydration properties, consistent with structural features dictating hydration characteristics. We discuss how volumetric characterizations, in conjunction with structural studies, can be used to describe, define, and resolve the general and sequence/conformation-specific hydration properties of nucleic acid duplexes.

journal_name

Biopolymers

journal_title

Biopolymers

authors

Chalikian TV,Völker J,Srinivasan AR,Olson WK,Breslauer KJ

doi

10.1002/(SICI)1097-0282(19991015)50:5<459::AID-BIP

subject

Has Abstract

pub_date

1999-10-15 00:00:00

pages

459-71

issue

eissn

0006-3525

issn

1097-0282

pii

10.1002/(SICI)1097-0282(19991015)50:5<459::AID-BIP

journal_volume

pub_type

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The hydration of nucleic acid duplexes as assessed by a combination of volumetric and structural techniques.