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Vibrational Circular Dichroism Spectroscopy and the Effects of Metal Ions on DNA Structure

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Vibrational Circular Dichroism Spectroscopy and the Effects of Metal Ions on DNA Structure Journal of Molecular Structure 661-662 (2003) 541–560 www.elsevier.com/locate/molstruc Vibrational circular dichroism spectroscopy and the effects of metal ions on DNA structure V. Andrushchenko, D. Tsankov, H. Wieser* Department of Chemistry, University of Calgary, Calgary, AB, Canada T2N 1N4 Received 28 May 2003; accepted 6 August 2003 Dedicated to Professor Bernhard Schrader Abstract The effects of manganese (II), nickel (II), chromium (III), and platinum (II) (cisplatin) on the double helical structure of selected oligonucleotides and DNA as detected by vibrational circular dichroism spectroscopy (VCD) are reviewed. For (dG–dC)20, the VCD spectra displayed unambiguously the transition from the normal right-handed B-form to the left-handed Z-from at the highest concentration of Mn2þ (8.5 [Mn]/[P]). For poly(rU)·poly(rA)·poly(rU), the double-triple- single helix transition induced by nickel (II) was clearly observable at increasing temperatures. For calf thymus DNA, chromium (III) at 0.6 [Cr]/[P] produced a 4-fold increase of the main VCD couplets, which are characterized as c-type spectra. These unusual features are due to condensed particles with dimensions comparable to the wavelength of the probing light and with regular arrangements of DNA double-helices inside the aggregates. c-Type spectra were also observed for DNA with manganese (II) between 55 and 60 8C at 2.4 [Mn]/[P]. Between 2.4 and 10 [Mn]/[P], intense and indistinct VCD features appeared above the DNA melting point indicating aggregation induced by Mn2þ ions at elevated temperature in a relatively wide range of experimental conditions, whereas DNA condensation with Mn2þ ions occurs only in a very narrow range of concentration and temperature. The complexes formed by coordination of cisplatin with d(CCTGGTCC)·d(GGACCAGG) and d(CCTCTGGTCTCC)·d(GGAGACCAGAGG) yielded very detailed VCD spectra, which distinctly confirmed the Gp4pGp5 and Gp6pGp7 lesion sites, respectively. The octamer slowly isomerized to form other adducts, which was not the case for the dodecamer. q 2003 Published by Elsevier B.V. Keywords: Vibrational circular dichroism; Metal ions; Cisplatin; Oligonucleotides; DNA 1. Introduction cesses. They can stabilize and destabilize biological structures. They are found in intimate association Metal ions are present in practically all biological with nucleic acids (NAs) in their natural environ- systems and participate in many biological pro- ment. Together with water molecules in the hydration shell they determine NA conformation [1,2]. Metal ion interaction with NAs plays an * Corresponding author. Tel.: þ1-403-220-4934; fax: þ1-403- important role in different biological processes such 289-7635. E-mail address: [email protected] (H. Wieser). as genetic expression, metallo-enzymatic processes, 0022-2860/$ - see front matter q 2003 Published by Elsevier B.V. doi:10.1016/j.molstruc.2003.08.037 542 V. Andrushchenko et al. / Journal of Molecular Structure 661-662 (2003) 541–560 mutagenesis, carcinogenesis, and DNA packing in can induce a transition from the natural right-handed living cells [3–6]. conformation to the left-handed Z-form [20,27–30]. Among varied other techniques, infrared The left-handed Z-form sequences of DNA are absorption spectroscopy (IR) has been used to believed to play a significant role in a number of probe the effects of metal ions on NA structures important life processes, such as gene regulation and [7–9]. In the present publication, we summarize our DNA replication [31–33]. A protein has been isolated recent applications of vibrational circular dichroism very recently in vitro and from several mammalian spectroscopy (VCD), which we expected to reveal tissues, which specifically recognizes Z-DNA important aspects of metal ion interaction with NAs [34–38]. In our study we used Mn2þ ions to induce that are not evident from IR. VCD is based on the the B–Z transition of (dG–dC)20 [20]. differential absorption of left and right circularly Another important NA conformational change polarized infrared light. It offers several advantages induced by metal ions is double- to triple-strand over conventional electronic circular dichroism transition and formation of triple helical structures (ECD) and conventional IR. The structural details of NAs [17,39,40]. Triple helical NAs are said to in ECD are usually limited by broad and less play a biological role as regulators of eukariotic resolved bands, which arise from electronic tran- gene expression [41]. Homo(purine)·homo(pyrimi- sitions of a small number of chromophores and give dine) sequences are frequently located at the 50-end limited detailed information about molecule struc- of many eukariotic genes and at sites involved in ture. In contrast, VCD intensities arise from normal genetic recombination [41,42]. Formation of triple modes of vibration, which are usually characteristic helices at these sites may be necessary for optimal for smaller molecular groups separated in space and gene expression [43]. A protein capable of binding therefore provide more specific details for the to dT·(dA·dT) triplex was discovered by Kiyama molecular structure. IR, on the other hand, while and Camerini-Otero [44]. This protein has a much having the same advantage of characteristic higher affinity of binding to triplex than vibrational modes, lacks VCDs stereosensitivity. In duplex dA·dT or to single-stranded dA or dT. NA molecules, the VCD signals are due to through- More recently, sequence-specific DNA and RNA space coupling of the normal vibrations of the recognition by specially designed oligonucleotides macromolecule and reflect the helical or ordered focused attention on the possible use of such structure of NAs [10,11]. The high sensitivity of the oligonucleotides as a new class of pharmacologi- VCD signals to changes in the coupled vibrations cally active compounds. These may allow for the leads to a high sensitivity of the spectra to changes in efficient treatment of different diseases with the geometry of the macromolecules. Since the first minimal side effects [45]. Homopyrimidine deox- application of VCD to NAs [12] it has been yoligonucleotides covalently linked to DNA cleav- successfully used to study different aspects of NA ing agents were synthesized, which cut duplex DNA structure [13–19]. in a sequence specific fashion via triplex formation In our laboratory, we have measured the VCD of [46,47]. These studies established the usefulness of several oligonucleotide and DNA complexes with such sequences as probes for chromosome mapping metal ions. These included structural transitions of and as anti-sense DNA for chemotherapeutic NAs between different conformations, namely, B to applications in which gene expression is regulated Z-form, duplex-triplex-single strand, DNA by triplex formation as demonstrated by in vitro condensation and aggregation, and interaction of inhibition of c-myc oncogene expression [48]. In our cis-diamminedichloroplatinum(II) (cis-DDP or study we demonstrated conformational transitions of cisplatin) with DNA. More details on these and other poly(rA)·poly(rU) induced by synergetic action of VCD investigations dealing with NA-metal ion Ni2þ ions and elevated temperatures [21]. The interaction can be found elsewhere [20–26]. poly(rA)·poly(rU) duplex disproportionates into a The natural conformation of DNA is a right- triple helix of poly(rU)·poly(rA)·poly(rU) and a handed B-form helix. However, the addition of single strand of poly(rA) [1]. The extra poly(rU) a number of metal ions to poly- or oligo(dG–dC) strand fits into the major groove of this double helix. V. Andrushchenko et al. / Journal of Molecular Structure 661-662 (2003) 541–560 543 A very important aspect of metal ion effect on platinum coordination, the dihedral angle between DNA is the induction of DNA condensation and the guanine rings ranges between 76 and 878 aggregation. Divalent metal ions, especially at bending the DNA helix toward the major groove at increased temperatures, can induce DNA aggregation the lesion site, flattening and widening the [49–52]. Trivalent and higher valence ions as well as minor groove, and noticeably unwinding the divalent ions acting synergetically with other factors double helix. These distortions of the double can induce DNA condensation into highly condensed helix of d(CCTGGTCC)·d(GGACCAGG) and particles in vitro [6,53]. The condensation process d(CCTCTGGTCTCC)·d(GGAGACCAGAGG) can plays a very important role in DNA packing in living be detected distinctly by VCD [25,26]. Our main cells as well as in the process of gene delivery for gene objective for recording the VCD spectra of these therapy [6]. During condensation a DNA molecule two sequentially similar oligonucleotides was to transforms (or several molecules assemble) into very compare the results with those obtained by NMR dense higher ordered three-dimensional structures, spectroscopy and X-ray crystallography [60–62]. which enables DNA to reduce its volume 104–106 In the present publication we focus explicitly on times [6,54]. In the process of aggregation, DNA also the influence of Pt coordination on the overall forms three-dimensional structures, but in contrast to DNA structure as exemplified by the two analogous condensation these structures are not highly oligonucleotide sequences of different length, ordered and are relatively loose. In our study we one comprising a full helical turn and the other used Cr3þ ions to induce DNA condensation, and including an incomplete one. The results Mn2þ ions at elevated temperatures to induce DNA confirm that the octamer in contrast to the aggregation [22,23]. dodecamer appeared metastable even at 2 8C and Cis-diamminedichloroplatinum(II), otherwise slowly isomerized into other adducts after approxi- known as cisplatin, is a widely used anticancer drug mately 2 h. used for the treatment of metastatic testicular and ovarian tumors, various head and neck tumors, and advanced bladder cancer [55,56]. It cross-links DNA 2. Experimental forming various adducts.
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