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PMID: 8599669 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Raman spectroscopy of DNA-metal complexes. II. The thermal denaturation of DNA in the presence of Sr2+, Ba2+, Mg2+, Ca2+, Mn2+, Co2+, Ni2+, and Cd2+.

Biophysical journal ·Vol. 69 ·No. 6 ·1995-12-00 ·Pages 2623-41

Duguid JG, Bloomfield VA, Benevides JM, Thomas GJ

Abstract

Differential scanning calorimetry, laser Raman spectroscopy, optical densitometry, and pH potentiometry have been used to investigate DNA melting profiles in the presence of the chloride salts of Ba2+, Sr2+, Mg2+, Ca2+, Mn2+, Co2+, Ni2+, and Cd2+. Metal-DNA interactions have been observed for the molar ratio [M2+]/[PO2-] = 0.6 in aqueous solutions containing 5% by weight of 160 bp mononucleosomal calf thymus DNA. All of the alkaline earth metals, plus Mn2+, elevate the melting temperature of DNA (Tm > 75.5 degrees C), whereas the transition metals Co2+, Ni2+, and Cd2+ lower Tm. Calorimetric (delta Hcal) and van't Hoff (delta HVH) enthalpies of melting range from 6.2-8.7 kcal/mol bp and 75.6-188.6 kcal/mol cooperative unit, respectively, and entropies from 17.5 to 24.7 cal/K mol bp. The average number of base pairs in a cooperative melting unit (<nmelt>) varied from 11.3 to 28.1. No dichotomy was observed between alkaline earth and transition DNA-metal complexes for any of the thermodynamic parameters other than their effects on Tm. These results complement Raman difference spectra, which reveal decreases in backbone order, base unstacking, distortion of glycosyl torsion angles, and rupture of hydrogen bonds, which occur after thermal denaturation. Raman difference spectroscopy shows that transition metals interact with the N7 atom of guanine in duplex DNA. A broader range of interaction sites with single-stranded DNA includes ionic phosphates, the N1 and N7 atoms of purines, and the N3 atom of pyrimidines. For alkaline earth metals, very little interaction was observed with duplex DNA, whereas spectra of single-stranded complexes are very similar to those of melted DNA without metal. However, difference spectra reveal some metal-specific perturbations at 1092 cm-1 (nPO2-), 1258 cm-1 (dC, dA), and 1668 cm-1 (nC==O, dNH2 dT, dG, dC). Increased spectral intensity could also be observed near 1335 cm-1 (dA, dG) for CaDNA. Optical densitometry, employed to detect DNA aggregation, reveals increased turbidity during the melting transition for all divalent DNA-metal complexes, except SrDNA and BaDNA. Turbidity was not observed for DNA in the absence of metal. A correlation was made between DNA melting, aggregation, and the ratio of Raman intensities I1335/I1374. At room temperature, DNA-metal interactions result in a pH drop of 1.2-2.2 units for alkaline earths and more than 2.5 units for transition metals. Sr2+, Ba2+, and Mg2+ cause protonated sites on the DNA to become thermally labile. These results lead to a model that describes DNA aggregation and denaturation during heating in the presence of divalent metal cations; 1) The cations initially interact with the DNA at phosphate and/or base sites, resulting in proton displacement. 2) A combination of metal-base interactions and heating disrupts the base pairing within the DNA duplex. This allows divalent metals and protons to bind to additional sites on the DNA bases during the aggregation/melting process. 3) Strands whose bases have swung open upon disruption are linked to neighboring strands by metal ion bridges. 4) Near the midpoint of the melting transition, thermal energy breaks up the aggregate. We have no evidence to indicate whether metal ion cross-bridges or direct base-base interactions rupture first. 5) Finally, all cross-links break, resulting in single-stranded DNA complexed with metal ions.

MeSH Terms
Animals Barium/pharmacology Cadmium/pharmacology Calcium/pharmacology Calorimetry, Differential Scanning/methods Cations, Divalent/pharmacology Cattle Cobalt/pharmacology DNA/chemistry,drug effects DNA, Single-Stranded/chemistry,drug effects Hot Temperature Hydrogen-Ion Concentration Kinetics Magnesium/pharmacology Manganese/pharmacology Mathematics Models, Structural Nickel/pharmacology Nucleic Acid Denaturation Potentiometry Spectrum Analysis, Raman/methods Strontium/pharmacology Thermodynamics
Chemicals
Cations, Divalent DNA, Single-Stranded Cadmium Barium Cobalt Manganese Nickel DNA Magnesium Calcium Strontium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Duguid J G
Department of Biochemistry, University of Minnesota, St. Paul 55108, USA.
Bloomfield V A
Benevides J M
Thomas G J
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Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1995-12-00
Pages
2623-41
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1236500
Subset
IM
Grants
NIAID NIH HHS · AI18758 · United States
NIGMS NIH HHS · GM08277 · United States
NIGMS NIH HHS · GM28093 · United States
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